protecting and restoring natural ecosystems and imperiled species through science, education, policy, and environmental law
Because life is good.
September 10, 2010
DRECP Independent Science Advisors 1516 Ninth Street Sacramento, CA 95814-5512
SEP 10 2010
SEP 10 2010
RE: Comments on the Independent Science Advisors Report Docket No. 09-RENEW EO01. Dear Science Advisors, The Center for Biological Diversity greatly appreciates the indisputably science-based information but forth in the Draft Recommendations of Independent Science Advisors for The California Desert Renewable Energy Conservation Plan (DRECP) - DRECP-1000-2010-008, August 2010. We look forward to having those recommendations adopted by the DRECP as it moves forward in the process. We have three additional suggestions for the science advisors to consider including in the final version of the Recommendations as follow: 1) Survey data from the current “fast-track” solar projects have documented potentially “new” species. These new species, while not officially described and therefore “recognized” by the scientific community, typically have very restricted ranges. Therefore, in the future and certainly within the lifetime of the plan, once recognized, they may represent an endemic, rare or otherwise “species of special concern”. Recommendations describing mechanisms on how to treat these “newly discovered” species would be very useful and benefit protection of the planning area’s biodiversity (a goal of the plan). 2) In the past, transplantation of rare plants has been tried as a mitigation strategy. Literature on the issue to date indicates significant failures (Fiedler 1991). Despite morphological successes (i.e. plants successfully transplanted and reproducing), Krauss et al. (2002) found that genetically, the transplantation effectively degraded the genetics of one rare plant species. Recommendations on transplantation of rare plants would be useful. 3) In the recent past, avoidance measures have been proposed to conserve rare plants in “halos” or Special-Status Plant Protection Areas – areas within a proposed project site where disturbance would be limited. However literature identifies fragmentation as a significant threat not only of the plant habitat itself (Honnay and Jacquemyn 2007, Matthies et al. 2004, Debinski and Holt 2000, Ellstrand and Elam 1993) but the pollinator habitat, which is crucial for many plants’ reproduction (Kearns et al. 1998). Recommendations on how to effectively conserve rare plants in particular would also be useful. Arizona • California • Nevada • New Mexico • Alaska • Oregon • Montana • Illinois • Minnesota • Vermont • Washington, DC Ileene Anderson, Staff Biologist PMB 447, 8033 Sunset Blvd. • Los Angeles, CA 90046-2401 tel: (323) 654.5943 fax: (323) 650.4620 email: [email protected] www.BiologicalDiversity.org
Guidance on these important issues would be immensely helpful and we appreciate, in advance, the panels’ expert opinion on them.
Ileene Anderson Biologist
cc: Dave Harlow [email protected] Michael Valentine [email protected][email protected] and a hardcopy will be sent to the address below: California Energy Commission Dockets Office, MS-4 Docket No. 09-RENEW EO-01 1516 Ninth Street Sacramento, CA 95814-5512
CBD comments on DRECP ISA Recommendations Page 2 of 3
References included as attachments Debinski, D.M. and R.D. Holt 2000. A survey and overview of habitat fragmentation experiments. Conservation Biology 14(2): 342-355. Ellstrand, N.C. and D.R. Elam 1993. Population genetic consequences of small populations size: Implications for plant conservation. Annual Review of Ecology and Systematics 24: 217-242. Fiedler, P. L. 1991. Final Report – Mitigation-related transplantation, relocation and reintroduction projects involving endangered and threatened, and rare plant species in California. Submitted to Ann Howald, California Department of Fish and Game, Endangered Plant Program, June 14, 1991. Funded by California Endangered Species Tax Check-Off Fund Contract No. FG-8611. Pgs. 144. Honnay, O. and H. Hacquemyn 2007. Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conservation Biology 21(3): 823-831. Kearns, C.A, D. W. Inouye and N. M. Waser. 1998. Endangered Mutualisms: The Conservation of Plant-Pollinator Interactions. Annual Review of Ecology and Systematics 29:83-112. Krauss, S.L., B. Dixon and K.W. Dixon 2002. Rapid genetic decline in a translocated population of the endangered plant Grevillea scapigera. Conservation Biology 16(4): 986-994. Matthies, D., I. Brauer, W. Maibom and T. Tscharntke. 2004. Population size and the risk of local extinction: empirical evidence from rare plants. Oikos 105: 481-488.
CBD comments on DRECP ISA Recommendations Page 3 of 3
A Survey and Overview of Habitat Fragmentation Experiments DIANE M. DEBINSKI* AND ROBERT D. HOLT† *Department of Animal Ecology, 124 Science II, Iowa State University, Ames, IA 50011, U.S.A., email [email protected] †Natural History Museum and Center for Biodiversity Research, Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, U.S.A., email [email protected]
Abstract: Habitat destruction and fragmentation are the root causes of many conservation problems. We conducted a literature survey and canvassed the ecological community to identify experimental studies of terrestrial habitat fragmentation and to determine whether consistent themes were emerging from these studies. Our survey revealed 20 fragmentation experiments worldwide. Most studies focused on effects of fragmentation on species richness or on the abundance(s) of particular species. Other important themes were the effect of fragmentation in interspecific interactions, the role of corridors and landscape connectivity in individual movements and species richness, and the influences of edge effects on ecosystem services. Our comparisons showed a remarkable lack of consistency in results across studies, especially with regard to species richness and abundance relative to fragment size. Experiments with arthropods showed the best fit with theoretical expectations of greater species richness on larger fragments. Highly mobile taxa such as birds and mammals, early-successional plant species, long-lived species, and generalist predators did not respond in the “expected” manner. Reasons for these discrepancies included edge effects, competitive release in the habitat fragments, and the spatial scale of the experiments. One of the more consistently supported hypotheses was that movement and species richness are positively affected by corridors and connectivity, respectively. Transient effects dominated many systems; for example, crowding of individuals on fragments commonly was observed after fragmentation, followed by a relaxation toward lower abundance in subsequent years. The three long-term studies (⭓14 years) revealed strong patterns that would have been missed in short-term investigations. Our results emphasize the wide range of species-specific responses to fragmentation, the need for elucidation of behavioral mechanisms affecting these responses, and the potential for changing responses to fragmentation over time. Sondeo y Revisión de Experimentos de Fragmentación de Hábitat Resumen: La destrucción y la fragmentación del hábitat son las causas fundamentales de muchos problemas de conservación. Realizamos un sondeo de la literatura y examinamos de cerca la comunidad ecológica para identificar estudios experimentales sobre la fragmentación de hábitats terrestres y para determinar si emergen temas homogéneos de estos estudios. Nuestro sondeo revela que existen 20 estudios experimentales de fragmentación en el ámbito mundial. La mayoría de los estudios enfocan en los efectos de la fragmentación sobre la riqueza de especies, o en la(s) abundancia(s) de ciertas especies en particular. Otros temas importantes fueron el efecto de la fragmentación sobre las interacciones interespecíficas, el papel de los corredores y la conectividad del paisaje en los movimientos individuales y la riqueza de especies y la influencia de los efectos de bordes sobre los servicios proporcionados por el ecosistema. Nuestras comparaciones muestran una carencia notable de homogeneidad en los resultados de los estudios, especialmente en lo referente a la riqueza y a la abundancia de especies, y su relación con el tamaño de los fragmentos. Experimentos con artrópodos demostraron que existía un mejor ajuste entre los valores teóricos esperados y los valores reales de aumentos en la riqueza de especies en fragmentos grandes. Los taxones altamente móviles (por ejemplo, aves y mamíferos), las especies de plantas en sucesión temprana, las especies de gran longevidad y los depredadores generalistas no respondieron de la manera “esperada”. Entre las razones que explican estas diver-
Paper submitted February 23, 1998; revised manuscript accepted September 22, 1999.
gencias se incluyen los efectos de bordes, la liberación competitiva en los fragmentos de hábitat y la escala espacial del experimento. Una de las hipótesis más aceptadas establece que el movimiento y la riqueza de especies son afectadas positivamente por los corredores y la conectividad, respectivamente. Algunos efectos pasajeros dominaron muchos sistemas; por ejemplo, el hacinamiento de individuos en fragmentos se observó a menudo después de la fragmentación, seguido de un disminución de la abundancia en los años posteriores. Los tres estudios a largo plazo (⫽14 años) revelaron fuertes patrones que hubieran sido ignorados en investigaciones a corto plazo. Nuestros resultados señalan el amplio rango de respuestas especie-específicas, la necesidad de elucidar mecanismos de comportamiento que afectan las respuestas a la fragmentación y el potencial de respuestas cambiantes a la fragmentación a lo largo del tiempo.
Given the importance of habitat fragmentation in conservation, it is not surprising that there exists a burgeoning literature based on observational studies of fragmented landscapes (e.g., Wilcove et al. 1986; Quinn & Harrison 1987; Gibbs & Faaborg 1990; Blake 1991; McCoy & Mushinsky 1994) and a substantial theoretical literature on the population and community effects of fragmentation (e.g., Fahrig & Paloheimo 1988; Doak et al. 1992; Nee & May 1992; Adler & Nuernberger 1994; Tilman et al. 1994; With & Crist 1995). In contrast, fewer researchers have deliberately created an experimentally fragmented landscape and then assessed the ecological consequences of the fragmentation (Margules 1996). It is easy to see why. Manipulation of entire landscapes tends to be large in scale, laborious, and costly. Yet the difficulty and expense of large-scale spatial experiments makes it particularly important that whatever data they generate be used to address general issues in ecology. In principle, fragmentation experiments could provide a rich testing ground for theories and methodologies dealing with spatiotemporal dynamics (Tilman & Kareiva 1997). Moreover, because of the logistical difficulty of such experiments, synthesis across studies may help provide guidelines and cautionary lessons for the design of future landscape experiments. We present the results from a survey of studies conducted worldwide in experimentally fragmented habitats. By our definition, an experiment involves a deliberate manipulation of the landscape, usually with an eye toward assessing a particular hypothesis. In many descriptive fragmentation studies, researchers cannot control attributes such as patch size, degree of replication, site initiation, and position on the landscape because they are investigating the effects of landscape manipulation (e.g., clearcutting in logging or plowing in agriculture) conducted by others. Thus, we excluded such studies from our review. We concentrated on terrestrial systems because of the major differences in the dynamics of colonization between terrestrial and aquatic systems.
We conducted a literature survey of the major ecological journals (American Naturalist, Biological Conservation, BioScience, Canadian Journal of Zoology, Conservation Biology, Ecography, Ecological Applications, Ecological Modeling, Ecological Monographs, Ecology, Evolutionary Ecology, Forest Science, Heredity, Journal of Animal Ecology, Journal of Biogeography, Journal of Mammalogy, Landscape Ecology, Nature, Oecologia, Oikos, Theoretical Population Biology, and Trends in Ecology and Evolution) since 1984 using the keyword fragmentation. We also canvassed the ecological community using the Internet (CONSBIO listserver) and made informal contact with many colleagues. After compiling a list of candidate studies, we sent out a survey to the authors of the studies which asked questions about experimental design, focal organisms of study, hypotheses being tested, study length, and practical issues such as how the integrity of the experiment was maintained. We summarized the results in the form of a vote count tally of the number of times the hypothesis was supported. We believe that a more formal meta-analysis (e.g., Gurevitch & Hedges 1993) of these experiments is not yet warranted because of the relatively small number of studies and because of the heterogeneity among study designs, spatial and temporal scales, and methodological protocols.
Results Replication and Temporal Span Based on our criteria for fragmentation experiments, we identified 20 experimental studies; 6 were conducted in forests and 14 were conducted in grasslands or old fields. The experimental studies clustered into evaluations of five broad focal issues: species richness, the interplay of connectivity versus isolation, individual species behavior, demography, and genetics. They tested six major hypotheses: (1) species richness increases with area, (2) species abundance or density increases with area, (3) interspe-
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cific interactions are modified by fragmentation, (4) edge effects influence ecosystem services, (5) corridors enhance movement between fragments, and (6) connectivity between fragments increases species richness. For ease in following the discussion of the experiments included in our review (compiled in Table 1), we include within the text a number in brackets corresponding to the experiment number in Table 1. The number of fragmentation experiments and the length of time for which they have been conducted have increased substantially in recent years (Table 1). A decade ago there were just 3 studies extant; at present 14 studies are ongoing. The geographic distribution of the 20 studies was primarily North America and Europe. The spatial scale (Fig. 1) ranged from grassland patches of ⬍1 m2 (Quinn & Robinson 1987 ) to Amazonian rainforest fragments of 1000 ha (Bierregaard et al. 1992 ). Replication (Fig. 1) varied from 1 to 160 per category of patch size. Patch sizes were chosen relative to the questions being addressed and the organism(s) of study. Generally, as the landscape scale increased, there were fewer replicates at larger fragment sizes. There was a threshold of decrease in degree of replication at roughly 0.2 ha; above this size, the number of replicates was usually ⬍10. This weakens the statistical power of conclusions about the effects of large fragment size. The temporal spans for these studies ranged from 1 to 19 years, with a mean of just over 6 years (Table 1). Little experimental data exist on the long-term consequences of habitat fragmentation. Three experiments have been in progress for over a decade, and eight have been in progress for 5–10 years. The remaining projects were run for 3 years or less. These experiments contain taxonomic and habitat biases. Only a few studies explicitly focused on plant population and community dynamics (Table 2). Among animals, there was a heavy emphasis on songbirds and small mammals. A number of studies focused closely on particular species, but few analyzed in detail the effects of fragmentation on pairwise or multispecies interactions (Kareiva 1987  is a notable exception). Several of these projects examined responses across a variety of taxonomic groups simultaneously (Bierregaard et al. 1992 ; Margules 1992 ; Robinson et al. 1992 ; Baur & Erhardt 1995 ; D. Huggard, personal communication ). There also were habitat biases in that most studies were conducted in either forest, grassland, or old fields. This may reflect the economics and mechanics of creating and maintaining experimental patches, such as using mowing in old fields or grassland and relying upon forestry practices or clearcutting in forested biomes.
Predictions that Work Numerous studies reported results that supported theoretical expectations; but many revealed effects con-
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trary to initial theoretical expectations. Here we summarize results relative to the hypotheses tested (Table 2). SPECIES RICHNESS
Following from the theory of island biogeography (MacArthur & Wilson 1967), species richness in habitat fragments is expected to be a function of island size and degree of isolation. Smaller, more isolated fragments are expected to retain fewer species than larger, less isolated habitat tracts (Diamond 1975; Wilson & Willis 1975; Terborg 1976). A major focus of these studies has been the relationship among habitat size, species richness, and individual species’ abundances. Initial theoretical expectations regarding increased species richness with increasing area were supported in only 6 out of 14 examples (not including 3 taxa that exhibited changing patterns over time). In cases in which the hypotheses were upheld, the effects were often striking. For example, even in a 100-ha tropical forest fragment, a beetle community was recognizably different in composition and lower in species richness than those on control sites in continuous forest (Laurance & Bierregaard 1996 ). Collinge (1995 ) found that insect species diversity was lowest in the smallest fragments and highest in the largest fragments. In a comparison of several types of fragmented landscapes, Collinge and Forman (1998 ) found that large-bodied, initially rare species were concentrated in the remaining larger core habitats, as opposed to areas where a central portion of habitat was removed. T. Crist (personal communication ) found a similar decrease in arthropod species richness with increasing fragmentation of an old field and determined that the pattern was driven primarily by the loss of rare species. In an old-field study  in Kansas, larger patches had higher species richness of butterflies, but small mammals and plants tended to show less consistent differences in species richness among patch sizes (Robinson et al. 1992; Holt et al. 1995a, 1995b). Baur and Erhardt (1995 ) found that, after 2 years, isolated grassland fragments were less frequently occupied by various gastropod species than were control patches, leading to lower species richness in the fragments. This set of studies provides a reasonable match with theoretical expectations. Comparable to the effect of area on species richness, one might expect to observe area effects on genetic diversity within species; smaller fragments should have lower effective population sizes, higher rates of genetic drift, and fewer immigrants ( Jaenike 1973). In the experimental studies in our survey, the effect of fragmentation on genetic variation was studied infrequently. Baur and Erhardt (1995 ), however, found reduced fecundity and genetic diversity among herbaceous plant species in isolated patches. Interactions between plants and pollinators also exhibited modifications, with potential
California annual grassland Kansas old field
2. California grassland
South African grassland Canadian subalpine forest Missouri Ozark hardwood forest Colorado short grass prairie Canadian boreal mixed-woods
5. Groenvaly experiment
Bavarian clover patches
Virginia old field
12. German fragmentation study
13. Blandy farm fragmentation study 14. Vole behavior and fragmentation
15. Evensted research station
Ohio old field
11. Miami University fragmentation project
10. Savannah River Site corridor project
9. Boreal mixed-wood dynamics project
8. Colorado grassland
7. Missouri Ozark forest ecosystem project
6. Kamloops project
4. Wog Wog study
3. Kansas fragmentation study
1. Biological dynamics
crop fields and meadows mowed grass mowed grass
mowed grass clearcut
pine plantation clearcut
University of Oslo, Norwegian Forest Research Institute, Agricultural University of Norway
Oregon State University
University of Virginia
University of Georgia, Iowa State University, U.S. Forest Service Miami University
University of British Columbia, University of Alberta, Edmonton
CSIRO Division of Wildife and Ecology University of Pretoria, South Africa British Columbia Ministry of Forests Missouri Department of Conservation, University of Missouri University of Colorado
University of Kansas
National Museum of History, Smithsonian Institution University of California, Davis
0.25 ha (6), 0.875 ha (6), 3.062 ha (6) 0.1 ha (160), 1 ha (27), 10 ha (3)
0.25 ha (6), 0.875 ha (6), 3.062 ha (6)
50 ⫻ 100 m (6), 12 ⫻ 24 m (18), 4 ⫻ 8 m (82)
1 ha (8), 10 ha (8),100 ha (5), 200 ha (1), 1000 ha (3) 2 m2 (32), 8 m2 (8), 32 m2 (2)
Fragment sizes (replication)
Ims et al. 1993
Bowers & Dooley 1993 Wolff et al. 1997
Schmiegelow & Hannon 1993; Schmiegelow et al. 1997 Haddad 1997; Danielson and Hubbard (2000) Crist & Golden, personal communication Kruess & Tscharntke 1994
Kurzejaski et al. 1993
Jaarsveld, personal communication Vyse 1997; Klenner & Huggard 1997
Bierregaard et al. 1992; Bierregaard & Stouffer 1997 Quinn & Robinson 1987; Robinson et al. 1995 Holt et al. 1995a, 1995b; Robinson et al. 1992 Margules 1992; Margules 1996
Reference or contact
A summary of fragmentation experiments with contact persons, references, biomes, dates of initiation and conclusion, patch sizes and replication, and other pertinent data.
Experiment no. and project name or biome
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Aars et al. 1995
Baur & Erhardt 1995
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160 m2 (4), 40 m2 (16)
4.5 ⫻ 4.5 m (24), 1.5 ⫻ 1.5 m (24), 0.5 ⫻ 0.5 m (48)
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0.0225 ha (12), 0.675 ha (4) 1990–1995 (5 years) University of Oslo Norwegian grassland 20. Root vole sex ratio
University of Basel, Switzerland European calcareous grassland 19. Swiss Jura mountains
1993–present (6 years)
annual Miami University
mowed grass mowed grass
17. Predator-prey interactions and fragmentation 18. Ohio old-field project
Institute of Arable Crops Research Cornell University 16. Long Ashton
British croplands New York goldenrod monoculture Ohio old field
mowed grass mowed grass
1995–present (4 years) 1982–1985 (3 years)
Barrett et al. 1995 no
Kareiva 1987 no
9 ⫻ 9 m (36), 27 ⫻ 27 m (5) 20 m2 (3), 6 m2 (30)
Community focus Preexisting matrix Fragment sizes (replication) Time span Institutional affiliation Matrix habitat Patch habitat Experiment no. and project name or biome
(continued) Table 1.
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Reference or contact
ramifications for genetic diversity. For example, butterflies visited flowers less frequently in isolated patches, thus leading to reduced fecundity and possibly lower plant genetic diversity. DENSITY AND ABUNDANCE OF SPECIES
The negative effects of fragmentation on species richness arise in part because of lower-level effects on population abundance and so should be evident even in those species that do not become extinct. The simplest a priori expectation is that, for habitat specialists restricted to the fragments and unable to use the matrix habitat, fragmentation reduces density. The mechanism for this reduced density could be increased demographic stochasticity or the disruption of metapopulation dynamics. The alternative hypothesis, however, is that species move from the matrix habitat to the remaining habitat patches after a disturbance, such that “crowding” ensues in the patches (Whitcomb et al. 1981; Fahrig & Paloheimo 1988; Fahrig 1991). Our summary refers to density and abundance because some authors presented their results as density, whereas others presented results as abundance or trapping success per unit time. Species abundance decreased with fragmentation in 6 out of 13 examples. For instance, Margules and Milkovits (1994 ) found that the abundance of amphipods (family Talltridae) decreased markedly in remnant forest patches relative to controls and that this effect was more dramatic on smaller remnants than on larger ones. In the Kansas project , the cotton rat (Sigmodon hispidus) and the white-footed mouse (Peromyscus leucopus) were differentially more abundant in larger patches (Foster & Gaines 1991; Robinson et al. 1992; Schweiger et al. 1999). H. Norowi (personal communication ) similarly found that weevil and parasitoid densities were consistently greater in contiguous habitat patches than in fragmented patches of equivalent area. The density of tree seedlings declined significantly from continuous forest to forest fragments in the Amazonian Biological Dynamics Project  (Benitez-Malvido 1998). These results demonstrate the effect of fragmentation on key life-history stages in trees. In the Kansas study , which involves old-field succession, colonization by woody plant species is proceeding more rapidly in larger patches (Holt et al. 1995b; Yao et al. 1999). Thus, changes at the level of individual species can often be discerned, even when coarser, whole-community effects of fragmentation are not apparent (Robinson et al. 1992). INTERSPECIFIC INTERACTIONS AND ECOLOGICAL PROCESSES
Spatial dynamics can have profound effects on individual behavior (e.g., Hanski et al. 1995; Redpath 1995) and interspecific interactions such as predation (Aizen & Feinsinger 1994; Tilman & Kareiva 1997), so it is sensi-
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Survey of Habitat Fragmentation Experiments
Figure 1. Frequency distribution of fragmentation studies relative to plot size.
ble to expect that the effects of habitat fragmentation may be mediated or exacerbated through shifts in such interactions. Kareiva (1987 ) demonstrated this effect by performing experiments on a predator-prey interaction between an aphid and a coccinellid predator in monocultures of Solidago. The fragmented treatment had more frequent aphid outbreaks, apparently because fragmentation disrupted the ability of the predator to aggregate rapidly at localized clusters of the aphid in early phases of an outbreak. H. Norowi (personal communication ) found that the rate of weevil parasitism varied with parasitoid species and the spatial scale of analysis. W. Powell (personal communication ) similarly found that carabid beetle assemblages in experimentally fragmented agroecosystems revealed significant spatial and temporal effects arising from altered predator-prey interactions within grassland patches. EDGE EFFECTS
Another rule derived from the theory of island biogeography is that reserves should minimize the edge-to-area ratio to maximize the effective core area of the reserve. Increasing the amount of edge can make a reserve more vulnerable to invasion by exotic species and subject it to more extreme abiotic influences such as wind and tem-
perature (Saunders et al. 1991). Physical changes associated with creating an edge can have profound effects on ecological processes. For instance, R. Bierregaard (personal communication ) documented that edge effects penetrate 300 m or more into a tropical forest remnant, and Didham (1997 ) showed that isolated patches have leaf-litter insect fauna substantially different than that of continuous forest. In principle, the altered abiotic conditions associated with fragmentation can also influence ecosystem services such as nutrient cycling (Saunders et al. 1991). Three projects have addressed ecosystem consequences of fragmentation with varying results. Two forest projects found effects on nutrient cycling (Bierregaard et al. 1992 ; Klenner & Huggard 1997 ), whereas the Kansas oldfield study  did not (Robinson et al. 1992). In the Biological Dynamics Project  and other forest studies, the contrast in abiotic conditions between fragments (e.g., tall forest) and the surrounding matrix (e.g., pasture) is dramatic. In other systems, there are less dramatic differences between the matrix and fragments, so one might expect ecosystem effects to be less noticeable. Because fragmentation inevitably leads to the juxtaposition of qualitatively different habitats, flows of materials and individuals between them can indirectly exert profound influences on within-fragment communities
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(Polis et al. 1997). In the Kansas study , for instance, generalist arthropod predators such as web-building spiders are more abundant in the fragments, particularly along edges, where they can profit from the aerial “drift” of insects from the surrounding productive, mown interstitial turf (T. Jackson et al., unpublished data). Smaller forest fragments similarly had greater community invasibility for successional tree species in the Biological Dynamics Project  (Benitez-Malvido 1998). Laurence et al. (1998) found that recruitment rates were markedly higher near forest edges and highest within 100 m of forest edges. CORRIDORS AND MOVEMENT/CONNECTIVITY
Fragmentation creates barriers to dispersal (e.g., Mader 1984), and behavioral responses to fragmentation may underlie many observed effects at higher organizational levels such as populations and communities. Even narrow breaks (50–100 m) in continuous forest habitat produce substantial barriers to the movement of many species of birds and some insects. Of the five fragmentation experiments that directly tested the effects of corridors, all but one found that corridors enhanced movement for some of the species examined (Collinge 1995 ; Haddad 1997 ; Schmiegelow et al. 1997 ; Wolff et al. 1997 ). Collinge (1995 ) found that corridors slightly decreased the rate of species loss and that this effect was greatest in medium-sized fragments. In another experiment (Haddad 1999; Haddad & Baum 1999 ), three open-habitat butterfly species ( Juononia coenia, Phoebis sennae, and Euptoieta claudia) reached higher densities in patches connected by corridors than in isolated patches. But the abundance of a fourth, generalist species, Papilio troilus, was insensitive to forest corridors. Related to corridors is the effect of landscape pattern on movement, as expressed for instance in rates of colonization and dispersal. H. Norowi (personal communication ) found that the presence of a hedgerow on one side of an experimental patch affected the pattern of colonization of newly created habitat patches by one species of weevil (Gymnetron pascuorum). Kruess and Tscharntke (1994 ) found substantial distance effects on colonization by parasitoids in a clover field but only minor effects on colonization by herbivores. This led to release from parasitism on the isolated patches, analogous to the effects of fragmentation in the predator-prey interaction studied by Kareiva (1987 ). Parasitoid species that failed to establish tended to be those with low and variable populations. These patterns have persisted over several years (T. Tscharntke, personal communication). There is a growing literature on small mammals focusing on the effects of experimental fragmentation on dispersal and home-range size. Diffendorfer et al. (1995a,b ) showed that fragmentation reduced the movement rates and altered spatial patterning of distances moved in several small-mammal species. Wolff et al. (1997 )
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found that fragmentation reduced vole (Microtus canicaudus) movements considerably. Ims et al. (1993 ) found decreased home-range size and more home range overlap in small mammals on smaller patches. Harper et al. (1993 ) found that the shape of habitat patches affected the number of voles that dispersed when population densities were low but not when densities were high. Furthermore, the shape of the habitat patches affected the space-use behavior of resident voles. Bowers et al. (1995 ) examined the space-use behavior of voles (Microtus pennsylvanicus) and found that adult females at edges tended to have larger home ranges, body sizes, residence times, and reproductive rates than individuals in the interior of a patch. Bowers et al. (1995 ) suggest that this edge effect could account for the inverse patch-size effects on abundance for small mammals noted in several studies (e.g., Foster & Gaines 1991 ). Finally, Ims et al. (1993 ) studied the effects of fragmentation on aggressive and docile strains of voles (Microtus oeconomus) and found that different sex and age groups are likely to exhibit different spatial responses to fragmentation. Predictions that Do Not Work SPECIES RICHNESS
In a number of experiments, species richness either increased with or was unaffected by fragmentation. In most cases, these effects could be attributed to an increase in early-successional species, transient species, or edge effects (community “spillover” from surrounding habitats; Holt 1997). For instance, Schmiegelow et al. (1997 ) examined passerine data gathered before fragmentation and during the 2 years thereafter. Despite effects on turnover rates, they found no significant change in species richness as a result of harvesting, except in the 1-ha connected fragment treatment, where the number of species actually increased 2 years after isolation. This increase reflected transient species rather than species breeding in the patches, suggesting that buffer strips were being used as corridors. In the Biological Dynamics Project , frog diversity increased after fragmentation because of unpredicted immigration by generalist species that flourished in the matrix of pasture surrounding the forest fragments (Laurance & Bierregaard 1996). The Wog Wog Study  in southeast Australia (Margules 1996; Davies & Margules 1998; Margules et al. 1998) revealed that different taxa had highly disparate responses to fragmentation, including a lack of response. Plant communities in several experiments have exhibited species-richness patterns contrary to the expectations of island biogeography models. Quinn and Robinson (1987 ) found increased flowering-plant and insect species richness with increasing habitat subdivision. They hypothesized that these patterns might reflect the effect of fragmentation on competition
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A vote-count summary of fragmentation-experiment results, separated by hypothesis tested.* Hypothesis supported
Species richness increases with area 1. Biological dynamics
beetles frogs primates plants
no no yes no
yes no, years 1–7; yes, years 7– present yes, years 0–5; no, years 5– present no yes
2. California grassland
3. Kansas fragmentation study
4. Wog Wog study
8. Colorado grassland
9. Boreal mixed-wood dynamics project
11. Miami University fragmentation project 19. Swiss Jura mountains Species abundance or density increases with area 1. Biological dynamics
yes no no no, treatments and controls yes, isolated fragments no
14. Vole behavior and fragmentation 15. Evensted research station 16. Long Ashton
small mammals small mammals weevils and parasitoids insects small mammals
no no yes
yes (less parasitism on far patches)
Interspecific interactions are modified by fragmentation 12. German fragmentation study
Bierregaard et al. 1992; Stouffer & Bierregaard 1995 Laurance & Bierregaard 1996 Laurance & Bierregaard 1996 Bierregaard et al. 1992 Quinn & Robinson 1987; Robinson et al. 1995 Quinn & Robinson 1987; Robinson et al. 1995 Holt et al. 1995a, 1995b; Robinson et al. 1992 Robinson et al. 1992; Holt et al. 1995a, 1995b Holt et al. 1995a Margules 1992
no, treatments and controls yes, isolated fragments yes
13. Blandy farm fragmentation study
17. Predator-prey interactions and fragmentation 18. Ohio old-field project
Reference or contact
Holt et al. 1995b; Yao et al. 1999 Foster & Gaines 1991; Schweiger et al. 1999 Margules & Milkovits 1994 Margules & Milkovits 1994 Collinge & Forman 1998 Schmiegelow et al. 1997 Schmiegelow et al. 1997 Bowers & Matter 1997; Dooley & Bowers 1998 Wolff et al. 1997 Ims et al. 1993 W. Powell, personal communication Kareiva 1987 Barrett et al. 1995; Collins & Barrett 1997 Kruess & Tscharntke 1994 continued
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Project name 16. Long Ashton 17. Predator-prey interactions and fragmentation Edge effects influence ecosystem services 1. Biological dynamics 6. Kamloops project 3. Kansas fragmentation study Corridors enhance movement between fragments 8. Colorado grassland 9. Boreal mixed-wood dynamics project
10. Savannah river site corridor project 14. Vole behavior and fragmentation Connectivity between fragments increases species richness 8. Colorado grassland 9. Boreal mixed-wood dynamics project
Reference or contact
W. Powell, personal communication Kareiva 1987
nutrient cycling nutrient cycling nutrient pools
yes yes no
Bierregaard et al. 1992 Klenner & Huggard 1997 Robinson et al. 1992
yes no for Neotropical migrants yes for transient species yes for some; no for others no yes
Collinge 1995 Schmiegelow et al. 1997
yes no for Neotropical migrants yes for transient species
Collinge 1995 Schmiegelow et al. 1997
butterflies small mammals small mammals insects birds
Haddad 1997 Danielson & Hubbard 2000 Wolff et al. 1997
Schmiegelow et al. 1997
* Where multiple taxa were examined in a single study, there are multiple entries for the same experimental site.
among plants. In small patches, for instance, short-statured plant species could persist in edges and priority effects could permit local dominance not possible in a single large patch. Robinson et al. (1995 ) also examined invasibility by a native California poppy (Eschscholzia californica) in these same plots and found the speciesrich plots more invasible. Contributing factors included a positive effect of small-mammal disturbance and a negative effect of Bromus diadrus coverage. Invasion by species from the surrounding matrix could lead to a temporary increase in species richness within patches, at least if extinction rates are slow. If smaller fragments experience higher disturbance rates, this could shift competitive regimes such that in some situations species richness is enhanced. During the first 8 years of the Kansas  old-field experiment, patch size had little effect on successional replacement of major plant functional groups. Rather, the main influence of patch size was on the spatial autocorrelation of herbaceous community structure and on local persistence of some rare or clonal plant species (Robinson et al. 1992; Holt et al. 1995a, 1995b; Heisler 1998). In contrast, patch size had substantial effects on the colonization and growth rate of woody species (Yao et al. 1999). DENSITY AND ABUNDANCE OF SPECIES
In several fragmentation experiments, population densities increased on the smaller fragments, perhaps be-
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cause of the crowding effects of fragmentation. This was especially prevalent in small-mammal studies but was also observed in birds and insects. Barrett et al. (1995 ) found vole densities to be greater in a more fragmented landscape. In a review of patch-size effects on small-mammal communities, Bowers and Matter (1997 ) noted that inverse relations between density and patch size are frequently observed, particularly at the smaller patch sizes used in experimental landscape studies. In some cases, the unexpected effect of fragmentation on density seems to reflect the ability of a focal species to utilize both the matrix habitat and the fragment. For instance, Foster and Gaines (1991 ) observed a high density of deer mice on small fragments and substantial numbers in the intervening matrix. They interpreted this pattern as simply a reflection of habitat generalization, but more recent work (Schweiger et al. 1999) suggests that a combination of habitat generalization and competitive release on small patches may explain this density relationship. There appears to be a complex relationship between patch fragmentation and social structure that may underlie some of the inverse-density relationships. For instance, Collins and Barrett (1997 ) found that fragmented patches of grassland support greater densities of female voles than unfragmented sites. Aars et al. (1995 ) found differences in sex ratios among some litters of root voles and speculated that resource conditions (as affected by fragmentation) could lead to such biases.
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Dooley and Bowers (1998 ) found weak fragmentsize effects on the density and recruitment of Microtus pennsylvanicus in a grassland fragmentation experiment. They postulate that higher recruitment rates on fragmented patches result from diminished social costs and enhanced food resources on fragments. Andreassen et al. (1998 ) also found complex behavioral responses of voles to habitat fragmentation. Wolff et al. (1997 ) found that habitat loss did not decrease adult survival, reproductive rate, juvenile recruitment, or population size in the gray-tailed vole (Microtus canicaudus); surviving voles simply moved into remaining fragments. An influx of unrelated females into habitat fragments, however, resulted in decreased juvenile recruitment in those fragments. Crowding effects have also been observed after fragmentation in bird and insect communities. Schmiegelow et al. (1997 ) noted that this crowding effect disappeared for birds after the second year of their study. Margules and Milkovits (1994 ) found that two millipede species experienced population explosions after treatment in both the remnants and the intervening cleared area, but they returned to pretreatment levels after 7 years. Collinge and Forman (1998 ) found crowding effects on fragments in an insect community but did not collect data long enough to test for a temporal effect. CORRIDORS AND MOVEMENT/CONNECTIVITY
A few studies showed movement patterns contrary to what are generally expected to be the effects of habitat fragmentation, patch shape, and corridors. Barrett et al. (1995 ) showed that patch shape does not markedly affect dispersal or demographic variables of the meadow vole (Microtus pennsylvanicus). Andreassen et al. (1998 ) found that the rate of interfragment movements of small mammals actually increases with habitat fragmentation. Even more surprisingly, Danielson and Hubbard (2000 ) found that the presence of corridors reduces the probability that old-field mice (Peromyscus polionotus) will leave a patch in a forest fragment. In this same landscape Haddad (1997 ) found one butterfly species that does not respond to corridors. Schmiegelow et al. (1997 ) showed that Neotropical migrants declined in all fragmented areas, regardless of connectivity. As one might imagine, the use of corridors and the effect of fragmentation on movement patterns seems to be highly species-specific. These results suggest a need for further study of the potentially complex interactions between fragmentation and individual behavior. Logistical Problems and Considerations We concentrated on the fruits of experimentation in the study of habitat fragmentation. But our survey did reveal
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recurrent problems with such experiments, which future workers attempting to conduct fragmentation experiments need to be aware of and consider in designing their experiments. These considerations are important in that they define the likely scope of the applicability of results from fragmentation experiments. Common problems in orchestrating fragmentation experiments mentioned to us by a number of investigators in our survey included the costs and difficulty of adequate replication of large patches, the struggle to maintain patches, and the problems of identification of specimens in many species-rich taxa. Patches carved out of preexisting vegetation are likely to be heterogeneous in many respects; careful thought must be given to overlaying fragmentation treatments on preexisting heterogenous landscapes, especially with a low degree of replication. In cases in which patch sizes are large, costs and other problems with establishing the largest patches often result in low replication. In any system operating within a fixed area, there is a necessary trade-off among interpatch distance, patch size, and replication. Because of such constraints, out of the full domain of potential landscape configurations, experiments are likely to focus on only a modest swath of parameter space (Holt & Bowers 1999). Maintenance of the experimental area also can be expensive, time-consuming, and uncertain. Collaboration between government agencies and/or private landowners and researchers is often key to establishing and maintaining a landscape for experimental purposes. In highly productive habitat such as tropical rainforest, the rate of secondary succession can be so high that it is difficult to keep patches “isolated” (e.g., Bierregaard et al. 1992). If the surrounding sea of vegetation is not completely inhospitable, this could skew results in experiments testing for the effects of isolation. In small experimental fragments, the effects of sampling can be problematic, especially if multiple investigators are collecting data on several taxonomic groups. For example, to sample small patches without trampling the vegetation, G. Robinson (personal communication ) had to build portable scaffolds over the patches. Finally, taxonomic problems were noted by many investigators working on plants and insects (Holt et al. 1995a ; S. Collinge, personal communication ; C. Margules, personal communication ). This mundane problem is important if species-rich groups tend to have stronger responses to fragmentation.
Discussion There was a considerable lack of consistency in results across taxa and across experiments. The two most frequently tested hypotheses, that species richness increases with fragment area and that species abundance
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or density increase with fragment area, showed entirely mixed results. Some of these discrepancies may be explained by differential relaxation times (Brown 1971) and rates of responses to fragmentation by different taxa. Most of the studies that fit initial theoretical expectations about the effects of fragmentation upon species richness involved arthropod assemblages. The species in these assemblages were typically small in body size (relative to the fragment sizes) and short in generation length (relative to the length of the fragmentation experiments). These assemblages might be expected to show responses over time scales commensurate with the time frame of typical field experiments. One of the more consistently supported hypotheses was that corridors supported connectivity between fragments. In four out of five cases, the presence of corridors enhanced movement for at least some of the species examined, and in two out of two examples the presence of corridors increased species richness in fragments. Taxonomic groups that did not respond in the expected manner displayed a range of responses to fragmentation. Some examples include highly mobile taxa whose population-level responses may integrate over spatial domains much larger than that of a single fragment. At short time scales, behavioral responses by mobile organisms can generate idiosyncratic patterns. Crowding of individuals was commonly observed after fragmentation, followed by a relaxation in subsequent years. Other groups that responded differently than expected include long-lived species unlikely to show dramatic population responses in shortterm experiments and taxa with generalized habitat requirements. Predicting fragmentation effects depends on a basic knowledge of the range of habitats that different taxa can utilize and on the factors limiting and regulating population abundance in unfragmented landscapes. The plethora of contradictory results for small mammals in fragmentation experiments seems to be caused by several factors, including habitat generalization, disparate responses among species to edges and corridors, and social interactions that may be modified by landscape changes. Many of the “contrary” results we report may reflect the relatively short time span of the experiments. A number of studies used patches that lasted only one season or an annual cycle to examine changes in the behavior or demography of particular species. The advantage of this approach is that it permits a clearer evaluation of potential mechanisms underlying landscape effects. A disadvantage is that such experiments cannot evaluate the multiplicity of indirect feedbacks that occur in anthropogenically disturbed landscapes. Long-term experiments are vital because they reveal processes that are obscured at shorter time scales. The three long-term studies [1, 3, 4] each revealed strong phenomena that would have been missed in short-term investigations. Some key findings of experimental habitat fragmentation studies might be difficult to achieve in purely obser-
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vational studies, reflecting in part the value of good experimental controls and properly randomized designs. We do not imply that experimental fragmentation projects are more rigorous than observational studies. Experimental fragmentation studies often suffer from the intellectual costs of focusing on small spatial and temporal scales and the use of species that may not serve as good models for the effects of fragmentation on species of conservation concern. Although observational studies pay a price by lacking “controls,” they nonetheless provide more realism with respect to landscape scale and species of concern. The value of having real controls, however, should not be underestimated; controls proved vital in interpreting results in many of these experiments (e.g., Robinson et al. 1995 ; Collins & Barrett 1997 ; Davies & Margules 1998 ; Laurance et al. 1998 ; Danielson & Hubbard 2000 ). Future fragmentation studies should focus on understanding the mechanisms behind observed communityand population-level patterns. For example, a critical issue is how fragmentation affects dispersal and movement. Similarly, a better understanding of species interactions, such as plant-pollinator interactions or competition in fragmented landscapes, is essential. Analysis of the matrix habitat may be crucial for understanding the dynamics of remnant fragments. The most important determinant of which species are retained in isolated patches appears to be the interaction of patches with the surrounding habitat matrix (Bierregaard & Stouffer 1997 ; Tocher et al. 1997 ). There is a growing recognition that connection among habitats that differ in productivity and structure is often a crucial determinant of community dynamics (Holt 1996; Polis et al. 1997), and fragmentation experiments provide a natural forum for analyzing such dynamics. Finally, more analysis of how fragmentation influences genetic variation for both neutral alleles and traits related to fitness would be particularly valuable. Choosing an appropriate landscape scale for the taxonomic group(s) of interest can have major implications for the findings of fragmentation studies. Communities are composed of species that experience the world on a vast range of spatial scales (Kareiva 1990; Holt 1993). In all the studies we reviewed, there were some mobile and/or large-bodied organisms for which the patches were small pieces of a fine-grained environment much smaller than a home range. Usually, however, some species will be present that experience the patches in a coarse-grained manner. An important challenge is to map out an intellectual protocol for applying these finescale experimental studies to scales that are more directly pertinent to conservation problems. The studies described in our review provide a first step in understanding the effects of fragmentation. Our results, however, emphasize the wide range of speciesspecific responses and the potential for changing results
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over time. Fragmentation effects cascade through the community, modifying interspecific interactions, providing predator or competitive release, altering social relationships and movements of individuals, exacerbating edge effects, modifying nutrient flows, and potentially even affecting the genetic composition of local populations. Perhaps it is not surprising then that fragmentation shows inconsistent effects across the experimental studies of fragmentation to date.
Acknowledgments We thank all those investigators who provided insights into their experiences with fragmentation studies. This manuscript benefited from the comments of G. Belovsky and two anonymous reviewers. The research was supported by grant 93-08065 from the Long-Term Research in Environmental Biology program of the National Science Foundation. This is journal paper J-17802 of the Iowa Agriculture and Home Economics Experiment Station, Ames, Iowa (project 3377). Note added in proof: Since this paper was written, we have become aware of an additional experimental study of fragmentation involving microinvertebrate species assemblages on moss patches on boulders. Gonzalez et al. showed strong effects of fragmentation on species diversity and population size (A. Gonzalez, J. H. Lawton, F. S. Gilbert, T. M. Blackburn, and I. Evans-Freke. 1998. Metapopulation dynamics, abundance, and distribution in a microecosystem. Science 281:2045–2047.). Literature Cited Aars, J., H. P. Andreassen, and R. A. Ims. 1995. Root voles: litter sex ratio variation in fragmented habitat. Journal of Animal Ecology 64: 459–472. Adler, F. R., and B. Nuernberger. 1994. Persistence in patchy irregular landscapes. Theoretical Population Biology 45:41–75. Aizen, M. A., and P. Feinsinger. 1994. Forest fragmentation, pollination and plant reproduction in a Chaco dry forest, Argentina. Ecology 75:330–351. Andreassen, H. P., K. Hertzberg, and R. A. Ims. 1998. Space-use response to habitat fragmentation and connectivity in the root vole Microtus oeconomus. Ecology 79:1223–1235. Barrett, G., J. D. Peles, and S. J. Harper. 1995. Reflections on the use of experimental landscapes in mammalian ecology. Pages 157–174 in W. Lidicker, editor. Landscape approaches in mammalian ecology and conservation. University of Minnesota Press, Minneapolis. Baur, B., and A. Erhardt. 1995. Habitat fragmentation and habitat alterations: principal threats to most animal and plant species. GAIA 4: 221–226. Benitez-Malvido, J. 1998. Impact of forest fragmentation on seedling abundance in a tropical rain forest. Conservation Biology 12:380–389. Bierregaard, R. O., Jr., and T. E. Lovejoy. 1989. Effects of forest fragmentation on Amazonian understory bird communities. Acta Amazonica 19:215–241. Bierregaard, R. O., Jr., and P. C. Stouffer. 1997. Understory birds and dynamic habitat mosaics in Amazonian rainforests. Pages 138–156
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Annu.Rev. Ecol. Syst.1993. 24:217-42 Copyright ? 1993 byAnnualReviewsInc. All rightsreserved
POPULATION GENETIC CONSEQUENCES OF SMALL POPULATION SIZE: Implications forPlantConservation NormanC. Ellstrandand Diane R. Elam
Department of Botanyand PlantSciencesand Programin Genetics,University of California, Riverside,California 92521-0124
Abstract thepotential Although geneticrisksassociatedwithrareorendangered plants and smallpopulationshave been discussedpreviously, thepracticalrole of populationgeneticsin plantconservation remainsunclear.Usingtheoryand theavailabledata, we examinetheeffectsof geneticdrift,inbreeding, and inrareplantsandsmallpopulations. geneflowon geneticdiversity andfitness We identify thosecircumstances thatarelikelyto puttheseplantspeciesand at geneticrisk.Warning populations signsthatpopulations maybe vulnerable includechangesin factorssuchas populationsize, degreeof isolation,and fitness.Whenpossible,we suggestpotential management strategies.
INTRODUCTION Becauseofthekeyroletheyplayinearth'secosystems, plantsshouldhave thehighest inconservation efforts. In termsofnumbers, priority plantspecies dominatelistsof rareand endangered species.For example,214 planttaxa compriseover 75% of all taxa listedby theCaliforniaDepartment of Fish and Game as rare,threatened, or endangered. Because of thelargenumber of endangered plantspeciesworldwide(estimated at approximately 60,000; methodfortheirconservation mustbe in situprotection and 88), theprimary 217 0066-4162/93/1120-0217$05.00
management. Successoftheseefforts willdependonidentifying andthwarting generalrisksto theprotected populations. Forovera decade,muchattention has focusedon thepotential geneticrisks associatedwithsmallpopulation size,particularly frominbreeding andgenetic drift(e.g. 1, 32, 95), butalso fromgeneflow(25, 106). Nevertheless, the practicalrole of populationgeneticsin plantconservation remainsunclear. The theoreticalrisks are oftenstraightforward extensionsof population geneticstheory; butrelevant datahavebeenslowtoappearandaresometimes conflicting. Furthermore, therelativeimportance of geneticsin conservation efforts has been called intoquestionby some scientistswho suggestthat ecologicalfactorsmaybe moreimportant (e.g. 61). Our reviewaddressesthefollowingquestion:"Underwhatcircumstances does populationgeneticsplay an important role in plant conservation biology?"We operateunderthe assumptionthat fragmentation, habitat and environmental destruction, stressessuchas pollutionlimitor reducethe size ofplantpopulations. Therefore, we examinethetheoretical consequences of isolationand gene flowthatput smallpopulationsat risk,comparethe predictions withthe availabledata fromsmallplantpopulationsand from endangered plantspecies,and discussthepresentlimitations of boththeory anddata.In each section,thosegeneralconditions inwhichplantspecieswill be at geneticriskas wellas thepotential management strategies forprotection aredescribed.Ourreviewfocusesspecifically on endangered plantspeciesin situ.Space prevents us fromreviewing othertopicsthatfallwithin thegeneral scope of "plantconservation genetics,"such as germplasm collectionand management and the transfer of engineeredgenes fromcrops intonatural populations. Withthelargenumberof speciesat riskand thelimitedamountof time andresourcesavailable,biologically based,easilyappliedgeneralrulesmust be developedandemployed.Therefore, thetimehas comeforevaluatingthe generalprinciples uponwhichmanagement willbe based. Below, strategies we identify whenandwhether rolein population geneticsplaysan important thesecurity of endangered plantspecies.At times,populationgeneticswill be an important thisreview consideration; often,it will notbe. Therefore, shoukdsune as a framework foractionforbothplantconservation managers and biologists.
GENETIC DRIFT AND INBREEDING IN SMALL, ENDANGERED PLANT POPULATIONS Two geneticconsequencesofsmallpopulation size areincreasedgeneticdrift and inbreeding. Geneticdriftis therandomchangein allele frequency that occursbecausegametestransmitted fromonegeneration tothenextcarryonly
PLANT CONSERVATION GENETICS
In largepopulations, a sampleoftheallelespresent intheparental generation. chancechangesinallelefrequency duetodrift aregenerally small.In contrast, mayundergo in smallpopulations (e.g. < 100individuals), allelefrequencies largeand unpredictable fluctuations due to drift(9, 31). Inbreeding is themating ofrelatedindividuals (31, 35). In plantsinbreeding biparental commonly occursin twoways:(i) through selfingand (ii) through maybe prevented inbreeding. Selfing,themostextremeformof inbreeding, in plantsby self-incompatibility will or by dioecy(9). Biparentalinbreeding mostlikelyoccurwhenpopulationsare smallor whentheyexhibitspatial willoftendevelopwhengenedispersalvia pollen geneticstructure. Structure and seed are spatiallyrestricted (e.g. 108). Geneticdriftand inbreeding may influencesmall plantpopulationsby of geneticdiversity changingpatterns and fitness.These effectsand their implications forconservation are discussedin detailbelow.
on GeneticDiversity Effects Geneticdrift ofgeneticvariation in twoways:(i) the changesthedistribution decreaseof variation withinpopulations and eventual (loss of heterozygosity amongpopulations. fixation ofalleles),and(ii) theincreaseofdifferentiation becomemore Everyfinite population experiences geneticdrift, buttheeffects as population that (120) predicted pronounced size decreases(31, 38). Wright drift willsubstantially altertheorganization ofgeneticvariation ofpopulations when 114Neis muchgreaterthanthe mutation rate (,u) and the selection coefficient (s) whereNe is theeffective populationsize. in an idealpopulation Effective population size is thenumber ofindividuals thatwould have the same geneticresponseto randomprocessesas a real because most populationof size N (23, 120). This conceptis important populationgenetictheorydeals withideal populations.To best applythe populationsizes in predictions of populationgenetics,estimates of effective natureare necessary.The effective populationsize is oftendepressedbelow the census size by factorssuch as deviationsfromone-to-onesex ratios, in in progeny andfluctuations variation overlapping generations, production, populationsize (37, 63, 100). Whileeffective populationsizes in natureare oftendifficult to measure,theratioNe/Nis oftenexpectedto fallbetween 0.25 and 1.0 (Nunney& Campbell,in preparation). Populationswith continuallysmall effectivepopulationsizes will be of variationby genetic especiallysusceptibleto theloss and reorganization occasionalfluctuations tosmall drift. thatundergoes However,anypopulation populationsize may also sufferfromloss of variationby chance. Such or founder/colonization events. includepopulationbottlenecks fluctuations allelicvariation is likelytodecreasewithmarkeddropsinpopulation Although as longas population oftenremainsrelatively size, heterozygosity unchanged
size reboundsrapidly(9, 35, 38). The populationgeneticconsequencesof bottlenecks and founder eventsarereviewedby Barrett & Kohn(9). Inbreeding increaseshomozygosity within populations. Smallerpopulations generallyshouldlose heterozygosity fasterthanlargerpopulationsbecause therateoflossis approximately equalto 112Ne eachgeneration. Inpopulations withcontinuous thefrequency inbreeding, of heterozygotes shouldapproach zero (38, 120). of variation Patterns observedin endangered plantsareexpectedto reflect theoretical ifdrift areimportant influences on their predictions andinbreeding geneticstructure. Severalapproacheshave been takento evaluategenetic in rareor endemicplants.Hamrick& Godt (46) asked whether diversity allozymevariationin 449 plant species varied with geographicalrange (endemic,narrow,regional,or widespread).Theyfound,bothat thespecies level andwithinpopulations, less genetic thatendemicscontainsignificantly of loci diversitythanwidespreadspecies as measuredby the proportion heterozygous perindividual, proportion of polymorphic loci, and allelesper polymorphic locus. They suggestedthatwidespreadspecies may have a of large,continuous history populations, whereasendemicsmightconsistof susceptibleto smallerand moreecologicallylimitedpopulations historically loss of variationby driftor bottlenecks. Interestingly, endemicspecieshad thesamelevelsofgeneticdifferentiation as do widespread amongpopulations species.
Karron(54, 57) comparedgeneticvariationin 11 setsof geographically restricted species speciesandwidespread congeners.He foundthatrestricted butnotalways,containless geneticvariation thantheirwidespread generally, of polymorphic loci and numberof congenersas measuredby percentage allelesperpolymorphic locus. The above studiesdid not directlyevaluate any associationbetween populationsize and geneticvariationbecause bothendemicand restricted ormaybe locallyabundant. species(sensu54) mayoccurinsmallpopulations in levels of genetic Yet, populationsize per se may explaindifferences variationbetweenwidespreadand rare congeners.Crawfordet al (22), fourspeciesof Robinsonia,foundthatthetotalgeneticdiversity comparing was highestin thetwomostcommonspeciesthathad thelargestpopulation sizes. The rareR. thurifera, characterized by populationsof fewerthan10 detectedin the othertwo individuals,containedonly20% of thediversity species.Sytsma& Schaal (105) foundthatone widespreadand one endemic species in the Lisianthiusskinnericomplexwere geneticallydepauperate comparedto threeotherendemicscharacterized by largerpopulationsizes and moreoutcrossed breedingsystems. The above studiescomparedrarespecieswithwidespreadspecies. Howindetermining then hasbeenimportant ever,ifgeneticdrift geneticstructure,
PLANTCONSERVATIONGENETICS 221 thanlarger smallerpopulations withina speciesshouldcontainless variation of interpopulation should also show higher levels populations,and they differentiation. We have compileddata for10 speciesthatcomparedlevels sizes and distribution of geneticvariationamongpopulationsof different withinrareor endemicplantspecies size andgeneticvariation In thesespecies,associationsbetweenpopulation thattheeffectsof geneticdriftvarywith are consistent withthehypothesis populationsize. In Table 1, the measuresof geneticvariationmostoften polymorphism (P) associatedwithpopulationsize werepercentage positively In was gene diversity (He) and numberof allelesperlocus (A). a fewcases, covaried, associatedwithpopulation size. Whenpopulation size andvariation in accord withthe high, variationtendedto be relatively among-population secondprediction In thethreestudieswheregenetic of thedrifthypothesis. factorsmaybe more size werenotrelated,historical variation andpopulation patterns of diversity populationsize in determining important thancurrent (19, 79); thatis, populationsin thesestudiesmay not be in evolutionary equilibrium. detectable The studiesin Table 1 involvedlevels of electrophoretically to small variationmayresponddifferently variation.However,quantitative populationsize thando othertypesof variation(63). We are awareof only threerelevantstudies.Ouborget al (82) investigated thecorrelation between in tworarespecies,Salviapratensis variation populationsize andphenotypic and Scabiosa columbaria.They foundthatsmall populations(N ? 90) containedless phenotypic variation thanlargepopulations (N - 200). While theycould not separategeneticand nongeneticsourcesof variation,their in plantspecies. Table 1 Summary of studiesassociatingpopulationsize andgeneticvariation Species Acacia anomala (Chittering populations) Eucalyptuscaesia Eucalyptuscrucis Eucalyptusparvifolia Eucalyptuspendens Eucalyptuspulverulenta Halocarpusbidwillii Salvia pratensis Scabiosa columbaria Washingtonia filifera
= percentpolymorphic loci, A = numberof alleles per locus, H, = gene diversity. 'We considerG,, > 0.1 to represent highamongpopulationvariation.
analysissuggestedthatat leastpartof theobservedphenotypic variationis genetically based. Thesedatasuggestthatmorphological characters respond to populationsize variationin a similarmannerto allozymeloci (111), thehypothesis supporting thatgeneticdrift has beenimportant in determining levelsof variation in thesepopulations. In contrast, R. Podolsky(personalcommunication) foundpopulationsize (range30 - > 1000) was notcorrelated withbroad-sense geneticvariance(Vg) forsix continuoustraitsin Clarkia dudleyena.In fact,largerpopulations tendedto have less variationthansmallpopulations.Similarly,Widen & Andersson (119) foundthata smallpopulation (averageN = 130) ofSenecio integrifolius containedsignificant additivegeneticvariation formorecharactersthana large (averageN = 1260) population.Differencesin spatial structure mayhave influenced theretention of geneticvariationin thiscase. The smallpopulationconsistedof a seriesof small,isolatedpatcheswhile thelargepopulationhad a morecontinuous distribution. Retention ofgeneticvariation can also be affected byseed,bulb,andtuber banksthatbuffer populations againstdramatic changesingeneticcomposition in Stephanomeria (7, 33). Long-term geneticstability exiguassp. coronaria to geneticvariationin (39) and Linanthus parryae(29) has been attributed the seed bank. Geneticdifferences betweenyoung and old seed bank have beendocumented in Carex bigelowii(113) and Luzula subpopulations and its parviflora(12). Similarly,rootstocks of Delphiniumgypsophilum hybridsmay maintaingeneticdiversityin the population(69). To our knowledge,studiesof maintenance ofgeneticvariation by seed banksin rare speciesarelacking,although somerareorendemicspecieshavethepotential to formlong-livedseed banks(e.g. 10, 15, 44). Thus, theimpactof seed bankson conservation geneticsremainsunknown. Because theeffectsof geneticdriftand in populations of limitedsize, we inbreeding maybe especiallypronounced whetherrestricted of rareand investigated populationsize is characteristic We obtainedpermission touse theCalifornia endangered plantsinCalifornia. of Fish and Game's RAREFIND (17) computerdatabase, a Department of information on thedistribution and ecologyof sensitiveplant compilation taxa in California.Specificoccurrencesare listedfor 743 taxa. For the a single constitutes purposesofoursurvey,we assumedthateachoccurrence we recordedthemostrecentspecific population.For each occurrence report, information thenumberof individuals regarding presenton thesite.Census of 559 taxa fora totalof 2993 data wereavailablefor1 to 35 occurrences data points. We foundit necessaryto make certainassumptionswhen populationsizes reportedwere vague. For example,estimatesgiven as 100 wereassumedto containclose to 100 individuals.The "approximately
IMPLICATIONS FOR CONSERVATION
PLANT CONSERVATION GENETICS
~ ~ ~
data are shownin Figure1. Eighteenpercentof theoccurrences contained tenor fewerindividuals, and53% contained100 or fewerindividuals.These datasuggestthatsensitive planttaxamayregularly occurinsmallpopulations. These dataare aptto be biasedtowardsmallpopulationsizes ifbiologists are morelikelyto reportcensusnumbers forsmallpopulations becausethey areeasierto countthanlargepopulations. Forexample,vernalpool annuals, whichare liableto occurin verylargenumbers, are rarelycensused.Some occurrences werereported to contain"many"or "thousands" of individuals. This sortof information couldnotbe used in oursurvey.Nevertheless, even if actualfrequencies of smallpopulationsare halfwhatwe have estimated of sensitivetaxa (e.g. thosewith100 usingRAREFIND, smallpopulations or fewerindividuals)arecommonenoughthatthey,andgeneticfactorssuch as driftand inbreeding thatinfluence them,wouldwarrant specificstudyand attention by managers. A drift-induced geneticchangeofconcernis theerosionofgeneticvariation. Loss of geneticvariationmaydecreasethepotentialfora speciesto persist in theface of abioticand bioticenvironmental change(95, 100) as well as altertheabilityof a populationto cope withshort-term challengessuch as pathogensand herbivores (52). Estimating levels of geneticvariationin populationsof concernshould provehelpfulformanagers.The frequency of monitoring efforts will often be determined and the bypracticalconsiderations, suchas staffing, funding, numberof speciesof concern,butmonitoring shouldbe attempted approximatelyonce per generation, if possible.Withsuch monitoring, erosionof geneticvariationcould be rapidlyrecognizedand stepstakento ameliorate losses.Forexample,introduction ofmigrants maysloworhaltloss ofgenetic variationby drift(however,see below). Monitoring geneticvariationcould also provide information of variationamong regardingthe distribution Whena highproportion ofgeneticvariation is distributed populations. among, ratherthanwithin,populations, it is advisableto preservemorepopulations to ensureretention of allelicand genotypic diversity (e.g. 47). Whenmonitoring of geneticvariation is feasible,it willlikelyinvolvethe use of allozymesor PCR-basedmolecularmarkers.While such discrete markershave a numberof advantagessuch as relativelylow cost and nondestructive is correlated sampling,it is notclearhow welltheirdiversity withothertypesof diversity(e.g. 47). For example,consistentpositive associationsbetweenmorphometric and allozymevariationhave not been if found(45 and references therein).Such discrepancies maybe important different to smallpopulationsize (63). typesof variation responddifferently Because geneticdata pertaining to the level and distribution of genetic variationwillnotalwaysbe availableto managers, aboutthe generalizations natureof geneticvariationin smallpopulationswouldbe usefulin making
PLANT CONSERVATION GENETICS
decisions.Thoughcensuspopulationsize is notnecessarilya management levels of geneticvariationwithinpopulations,it of current good predictor of whatis liable to happento geneticvariation shouldbe a good indicator over time (i.e. how variationis expectedto change as the population betweeneffec(112). The relationship equilibrium) approachesevolutionary thantherelationship variation maybe stronger tivepopulation size andcurrent betweencensussize and variation.If thatis thecase, thensimplemethods populationsizes shouldhelp managersto estimating effective of accurately these levelsof geneticvariation.However,evenwithout predictequilibrium shouldbe minimalwhenpopulations bydrift data,erosionofgeneticvariation for considerations maytakepriority are large.Therefore, othermanagement largepopulations. The history of a speciesmayalso providesomeinsightintocontemporary changesin population of geneticvariation.Whenknown,historical patterns shouldbe considered may (47). Populations size anddistribution bymanagers in population fluctuations be genetically depauperateif recentor recurrent and abundanceare have occurred.Changesin distribution size (bottlenecks) has changedor is liableto change. warningsignsthatgeneticcomposition ofseed,bulb,andtuber thepresenceandgeneticstructure Data concerning of banks,thoughrarelyavailable,arealso valuablein assessingvulnerability to geneticerosion.Thesereservesofgeneticvariation maybuffer populations populationsagainsttheloss of variationand helppreservethepotentialfor adaptivechanges(e.g. 44).
On Fitness Effects influence fitness inbreeding depression, through Geneticdriftandinbreeding The precisemechanism by theloss of fitnesswithincreasing homozygosity. andfecundity whichincreased is relatedtodecreasesinviability homozygosity is controversial (18, 60). The level of inbreeding depressionmayvarywiththematingsystem.In ofdeleterious recessivealleles thefrequency inbreeding populations, typically maydeclineas theybecomehomozygousand are purgedby selection(8). witha longhistory ofinbreeding shouldbe less vulnerable Thus,populations to inbreeding outbreeding populations(18). Howdepressionthantypically and betweenselfing rate inbreeding depression ever,inplants,therelationship fromstrong inbreeding is notprecise,andsometypically selfingspeciessuffer between work also that the relationship Theoretical suggests depression(9). as depressionand matingsystemmaynotbe as straightforward inbreeding expected(50). of population The extentof inbreeding depressionmayalso be a function inlargepopulations withlittlespatialgeneticstructure size. Inbredindividuals or in populationsthathave recentlybecome small are liable to exhibit
inbreeding depressionas homozygosity increases.Chronically smallpopulationsmayexhibitlowerlevelsofinbreeding ifdeleterious depression recessive alleles have been purgedby selectionovertime.On theotherhand,small populationsmay suffergreaterinbreeding depressionthando largerones becauseofthereducedeffectiveness of selectionrelativeto geneticdrift (49); in smallpopulations, deleterious recessives,ratherthanbeingeliminated by selection,couldbecomefixedby chance. Inbreeding depression has seldombeenexaminedinsensitive plantspecies. Karron(56) comparedgeographically restricted and widespreadAstragalus speciesand foundno evidenceof inbreeding depressionin percentseed set and percentembryoabortion.He did, however,detecthigh levels of inbreedingdepressionfor seedlingbiomass in progenyof the restricted species,Astragaluslinifolius. Thisresultis unexpected sincefrequent selfing in thatspeciesis expectedto havepurgedthegenomeofdeleterious recessive alleles (57). We areawareoftwostudiesrelevant to theassociationbetweeninbreeding depressionandpopulationsize in sensitiveplantspecies.Menges(74) found thatgermination increasedwithpopulationsize in Silene regia. percentage Largepopulations (N > 150) exhibited higherand less variablegermination percentages thansmallpopulations, ofregionorisolation.Small independent populationsmay produce seeds of lower fitnessbecause of inbreeding depressionin recentlyreducedpopulationsor inbreeding depressionfrom increasedselfingdue to higherfrequenciesof intraplant pollinations.In contrast,the intensity of inbreeding depressionmeasuredin Scabiosa columbariadid notvarywithpopulationsize (110). Anotherarea of relevantresearchinvolves the associationbetween heterozygosity per se and fitness.Because somerarespeciesare largelyor forthemarker loci examined(e.g. 20, 66, 99, 115), it is fullymonomorphic of interest to ascertainwhether heterozygosity per se is relatedto fecundity and viability.To our knowledge,theonlyrelevantdata forplantsare for commonspecies. Increasedheterozygosity was associatedwithincreasing andincreasedvegetative andreproductive age, earliersexualmaturity, output in Liatriscylindracea(94). In addition,heterozygosity and growthrateare insometemperate correlated treespecies(64 andreferences positively therein; evidencealso comes fromthe observationthatsome 77). Circumstantial than predominantly inbreeding plantsmaintain higherlevelsofheterozygosity some studieshave suggested expected(35 and references therein).Further, abletocontendwithfluctuating thathighlyheterozygous arebetter organisms environments (52 andreferences therein). On theotherhand,Pinus resinosa,a widespreadspecies,has verylow levelsofallozymeheterozygosity andis remarkably uniform morphologically butexhibitconsid(34). Two speciesof Typhaalso lack allozymevariation
PLANTCONSERVATIONGENETICS 227 erableecologicalamplitude (71). Theseresultssuggestthatheterozygosity is notrequisiteforecologicalsuccess(64). IMPLICATIONSFOR CONSERVATION It appears difficultto predict when
inbreeding depressionwill be an important factordecreasingthe fecundity and viabilityof sensitivespecies.Selfingratesare notnecessarily predictive of theexpectedlevel of inbreeding depressionbecause even specieswitha long historyof inbreedingmay sufferfrominbreedingdepression(9). it appearsthatpopulationsize is also not necessarilya useful Currently, predictor of inbreeding depression, althoughmoredataare neededto clarify In addition, thisrelationship. theextent ofinbreeding depression changeswith theenvironment studiedandmaybe moreseverein competitive or otherwise challenging environments (e.g. 49, 110). If heterozygosity perse providesa significant fitness advantage, thenpopulation fitness mightbe estimated using levelsofheterozygosity fordiscretebiochemical markers. Unfortunately, this approachmaybe riskybecauseheterozygosity andinbreeding depressionare notnecessarily associatedin a predictable way (49). Because it is difficult to predictlevelsof inbreeding depressionbased on matingsystem,populationsize, and heterozygosity, monitoring fitness in sensitivespeciesmaybe themostreliableapproachmanagers components can take currently. Significant decreasesin fruitor seed set, forexample, suggestthatintervention may be appropriate, althoughit will probablybe unclearwhetherthe reductionsare caused by geneticfactors.Ecological factorssuch as changesin pollinatorfaunaor behaviormay be equally in determining important fitnessin theshortterm(61, 101). Changesin pollinatorbehaviorin small or rareplantpopulationsmay decreasefitnessif the frequency of intraplant (self) pollinationincreases, whichmayincreaseinbreeding depression(e.g. 74, butsee 109), or if the overall visitationrate decreases. Significantly lower levels of pollinator visitationwere observedin restricted Astragaluslinifoliuscomparedwith widespread A. lonchocarpus (55). Lowervisitation rateswereassociatedwith lowerseed setsin Dianthusdeltoidesin fragmented sitescomparedto intact sites(53). Thesedatasuggestthatan awarenessofchangesinthecomposition and/orbehaviorof the pollinatorfaunamay help managersdetectfitness decreasesin sensitiveplantspecies. from Additionally, self-incompatible plantsinsmallpopulations maysuffer a mate.In a simulation problemsfinding study,Byers& Meagher(16) found that small populations(N < 50) did not maintaina large diversityof alleles. Therefore,the frequencyof available mates self-incompatibility decreased,and thevarianceof numberof availablematesincreased.Thus, lower seed set per individualand increasedvariationin seed set among werepredicted in smallpopulations.In thiscase, introduction individuals of
individualswith different compatibility typesmightoffsetthe observed changes.Although thecompatibility genotype ofindividuals willalmostnever be known,knowingthata sensitivespeciesis self-incompatible, dioecious, or otherwise obligatelyoutcrossing mayhelpmanagersrecognizethiscause of fitnessdecreasein diminishing populations (q.v. 65). Managersmayalso wishto be especiallyconsciousof speciesthathave experienced recentreductions in populationsize relativeto spcie,s thxtha of persistent smallpopulationsize. The latterare apparently a niistory not immediately threatened bytheloweraverageviability thatmaybe associated withsmall populationsize (51 and references therein).Some chronically havea reproductive behaviorthatincreases sparseprairiegrassespresumably theirlikelihoodof persistence despitelow populationsize (86). Species in whichrecentchangesin distribution, abundance,orfitness(e.g. fruitor seed threatened thanthesehistorically set)areobservedmaybe moreimmediately rarespecies.
GENE FLOW IN SMALL, ENDANGERED PLANT POPULATIONS of genesamongpopulations Gene flowin plantsis thesuccessfulmovement of seedsor vegetative by matingor by migration propagules(26, 96). Many discrete.But geographicisolationmay plantpopulationsare geographically not ensurereproductveisolation,eitherwithinor among species (26). Therefore,gene flow may be relevantto the conservation geneticsof a sensitivetaxonin two situations: (i) whenmorethanone populationof the taxonis extant,and(ii) whenopportunities existforhybridization withrelated taxa. Gene flow in plants is idiosyncratic, varyinggreatlyamong species, andseasons.However,geneflowlevelsat isolationdistancesof populations, hundredsto thousandsof metersare frequently highenoughto counteract geneticdriftand moderatelevels of directionalselection(26). Even in predominantly self-fertilizing species, gene flow by pollen may occur at ratesand substantial significant distances(114). Thus,gene flowcannotbe ignoredas a factorin plantconservation genetics.Whatlevelsof gene flow are expectedforsmallplantpopulations? Gene flowrate,thefraction of immigrants pergeneration, m, is expected to increaseas recipient populationsize decreases,otherthingsbeingequal. Two reasonsareoffered forthisexpectation: size decreases, (i) As population therelativefraction ofa fixednumber of immigrant pollengrains,seeds,and sporesincreases(48). (ii) Forzoophilousspecies,optimally foraging pollinatorsspendmoretimewithin thansmallpopulations, largepopulations effecting proportionately moreinterpopulation matingsin thelatter(85).
PLANTCONSERVATIONGENETICS 229 withcropsusinga largesourcepopulationand smallersink Experiments between thisexpectedrelationship populationshave generallycorroborated populationsize and rateof geneflowby pollen(e.g. 11, 14, 21). In a few Forexample,Klingeret al (58) found withexpectations. cases, dataconflict a strongdistancedependenttrend.At shortdistance(1 m), theoretical receivedless gene flowfroma source held;largerpopulations expectations distance(400 m), Butat thegreatest thandid smallerpopulations. population therangeofdistances hasyetsimulated No experiment thetrendwas reversed. However,mostexperiments populations. sizesfoundinnatural andpopulation have shownthatpollengene flowratesgenerallyincreasewithdecreasing ofseeddispersal size. We arenotawareofdatafortherelationships population and sourceor targetpopulationsize. The size of the sourcepopulationrelativeto sink populationmay be gene flowrateintothe sink. Largerpopulations in determining important a strong creating shouldexportmorepollenandseedsthansmallpopulations, fromlargeintosmallpopulations.In an experimental gene flowasymmetry no gene exchangeamongthree study,Ellstrandet al (27) foundessentially each) of wildradisha fewhundredmeters smallpopulations (15 individuals apart,but substantialgene flow into themfromvery large populations ofmeters away.Again,we arenotaware ofindividuals) thousands (thousands In conclusion,small seed dispersalpatterns. of anyrelevantdata regarding populationsare expectedto receivegene flowat a higherratethanlarge and are morelikelyto receivegeneflowfromlargepopulations populations thanfromothersmallones,evenifthelatterare in closerproximity.
GeneFlow Intraspecific biologymay be gene flow in plantconservation The role of intraspecific if more than one conspecificpopulationexists and if those important arecloseenoughforgeneflowtooccur(25). Despite populations conspecific of geneflowand itsprevalencein naturalplantpopulations, theimportance studiesof thegeneticsof sensitiveplantspeciesrarelyaddressgene flowin geneflowrates thespeciesof concern.Mosttacitlyassumethatintraspecific understudyare fullyisolated. are nil and thatthepopulations theaveragelevelsof gene flow Is thisview well founded?We estimated available or otherwisesensitiveplanttaxa (information for32 endangered forNm(24), theaveragenumber formula fromauthors),usingthefollowing of successfulimmigrants pergeneration: Nm Nm =
whereGstis equivalentto a weightedaverageof Wright's(120) Fstover loci (80) and n is thenumberof populations all allelesoverall polymorphic
sampled. This methodis consideredthe most robustof those thatuse populationgeneticstructure data to estimategene flow(97). Althoughthis estimatedependson thesamplingscheme(see 26 fordiscussion),itis useful forjudgingtheorderof magnitude of geneflow.The Nmestimatefromthis methodrepresents recent,rather thancurrent, geneflow(97). For a sample of smallpopulations(N = ca. 10), it reachesnear-equilibrium in about 10 aftera changein geneflowpattern generations (112). Therefore, it tendsto overestimate geneflowforspecieswithrecently isolatedpopulations. Our analysishas certainlimitations.It cannotbe applied to species at all loci studied(e.g. 66, 99). Furthermore, monomorphic some of our estimatescame fromdata on onlyone or two polymorphic loci. Thus, the valuesarecrude.However,we founda widerangeofgeneflowforsensitive planttaxawithNmestimates ranging from0 togreater than15;thedistribution of values is typicalforplantsas a whole(40). The gene flowestimatesare notassociatedwithtaxonomy, habit,breeding system, andpollination system. EstimatesfortenEucalyptusspeciesrangedfrom0.01 to 4.27. Furthermore, thethreelowestgene flowestimatescome froma highlyselfingannual,an annualwithan insect-pollinated mixedmatingsystem,and an outcrossing, tree. wind-pollinated EFFECTS ON GENETIC DIVERSITY AND FITNESS The bestknownevolutionary consequenceofgeneflowis thatitworksto homogenize population structure, ofdrift actingagainsttheeffects anddiversifying selection(e.g. 62, 120). In the case of drift,the rule of thumbis thatone immigrant everysecond or one interpopulation generation matingpergeneration (Nm = 0.5) will be to preventstrongdifferentiation of sufficient (96). Thisresultis independent populationsize, butthetimetoevolutionary equilibrium dependson a variety often of factors,includingpopulationsize (112). Conservation geneticists willhomogenize concludethatone migrant pergeneration populations against theeffects ofdrift we calculated (e.g. 1). Overhalfofthegeneflowestimates forsensitive allelefrequencies planttaxaarelargeenoughtohomogenize (Nm > 0.5; see above), suggesting role in gene flowhas playedan important in thesespecies. organizing geneticdiversity The homogenization of geneticvariationby gene flowis notnecessarily thesameas enhancement oflocalvariation. Ultimate changesinlocaldiversity will dependon the natureof geneticvariationin the gene flow source populationsrelativeto the sink populations.For example,the arrivalof substantial gene flow froma geneticallydepauperatesourcewill actually reducetheamountof variationin a relatively variabletargetpopulation.As notedabove,smallpopulations areexpectedtohavean asymmetric geneflow withlargepopulations. Suchone-waygeneflowwilltendtomake relationship of nearbylargepopulations. thesmallpopulations "satellites" evolutionary
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Conservation have operatedunderthe assumptionthatsince geneticists migration increaseseffective population size,thesamelevelofmigration that maintainsvariationshouldpreventan increasein inbreeding depressionin small populations(1). While this conclusionmay be reasonable,to our knowledgetherelationship betweengeneflowandinbreeding depression has neverbeenaddressedin theoretical detail(M. Slatkin,personalcommunication).The absenceof researchin thisarea maybe due to theuncertainty of thegeneticmechanisms underlying inbreeding depression(18). We predict thattheimpactof geneflowon inbreeding depression mayalso be a function of selectivepressures on thepopulations involved. If selectionfavorsdifferent selecallelesin different locations(disruptive tion),thengeneflowofinappropriate allelescan prevent local adaptation and reducelocal fitness(3, 118). In this case, the importance of gene flow increasesas populationsize decreases.Generally,local adaptationcannot occurwhenm > s wherem is thefraction of immigrants and pergeneration s is the local selectivecoefficient alleles (96). That is, againstimmigrant moderaterates of gene flow (approximately 1-5% per generation)are sufficient to introduce to counterbalance geneticvariation selectionforlocal adaptationof the same magnitude (i.e. 1-5%). Availabledata supportthis studiesoftenshowlocal adaptivedifferenexpectation. Reciprocaltransplant tiationin plantpopulations (reviewedby 68, 116, 117), butgenerallynotat themicrogeographic levelat whichsubstantial geneflowoccurs(e.g. 5, 117) unlessselectionis verystrong(e.g. 4; s > 0.99). Most gene flowestimateswe calculatedfor32 sensitiveplanttaxa (see too smalltoprevent underspatial above)areprobably adaptivedifferentiation selection.However,our largestestimates(two cases, Nm > 10) disruptive representvalues thatare large enoughto oppose a disruptiveselective coefficient of 0.2 in populations of 50 individuals. Adaptivedifferentiation may lead to outbreeding depression,"a fitness reduction betweenpopulations(106). Outbreeding followinghybridization" depressionmaybe commonin plants.Waser(116) reviewed25 studieson thefitnesseffects of outcrossing distancein angiosperms andfoundevidence foroutbreeding innearlythreequarters ofthestudies;theremainder depression showedfitnessincreaseswithincreasinginterparent distance.The fitness decline due to outbreeding depressioncan be substantial.In Ipomopsis from100 metermatingswere32% less fitthanprogeny aggregata,offspring from10 metermatings(118). Furthermore, in Scleranthus annuus,progeny from75 to 100 metermatingssuffered a 19 to 36% decreasein malefertility relativeto thosefrom6 metermatings(104). The frequency of outbreeding will be a function of population depression size if smallerpopulationsreceivegene flow at a higherratethanlarge in smallpopulations ifgeneflow populations.Problemsmaybe exacerbated
leads to highratesof geneflowbypollenfromlargepopulations asymmetry or geneflowcan eitherdrift (3). Interestingly, conditions adaptedto different populations. small in local adaptation prevent Gene flowis usuallyconsideredbenefidepressionand depletion inbreeding preventing biology, cial in conservation But geneflowcan also 1, 52). (e.g. populations small in of geneticvariation itcan certain conditions, under because, populations forsmall be detrimental reduce and differentiation, adaptive local prevent reducelocal variation, gene flow depression.The rolethatintraspecific outbreeding fitnessthrough on the largely depends plans management shouldplayin in situconservation The risk. at of the species history evolutionary recent role it has playedin general the substantially; has changed flow gene when concernoccurs primary shouldbe to maintaingene geneticmanagement goal of plantconservation levels. historic as same the roughly are flowat levelsthat determinehistoricand to going managers conservation How are plant levelsof geneflow historic of Order magnitude flow? levelsof gene current formulawe used same the using data frequency allele from can be estimated generations several takes estimator this Because (24). to estimateNm above estimate a reasonable be should it 112), (97, equilibrium toreachevolutionary current to taxa prior sensitive plant in many flow of gene levels ofthehistoric it seed a bank), with annuals long-term (and most perennials conditions.For The hundred last the over flow years. of gene picture shouldgivean adequate to assignthespeciesat riskintothecategory crudevalueobtainedwillsuffice flow. low gene or high of historically gene whether Once speciesare assignedintosuchcategories,determining will hazard new a to direction a pose in and dramatically flowhas changed high with historically a taxon For sense. common of matter a largelybe gene flow levels (Nm > 0.5), a sharpdrop in gene flow due to habitat maylead to problemsthatcan be solved or loss of pollinators fragmentation geneflowlevelscouldbe approximated Former flow augmentation. by gene or spores,or by cross-pollination of seeds transport by by transplantation, genomespergeneration few successful of a The transfer amongpopulations. flow at the historical gene to maintain sufficient be will per population once flow gene augmentation most perennials, For magnitude. of order species because Furthermore, suffice. would probably decades two every for withhistoriesof highgene flow have generallyhad littleopportunity be will material the of immigration source the geographic differentiation, mononot highly is material introduced the as as long irrelevant largely morphicor arrivingfroma distancegreatenoughto cause outbreeding will be necessaryforpopulations depression.No gene flow enhancement highgene flowwheregene flowlevels have notchanged withhistorically IMPLICATIONS FOR CONSERVATION
PLANT CONSERVATION GENETICS
or increased;if gene flowis augmented, it wouldgenerallyhave no effect butwould be a wasteof effort. Fora taxonwithhistorically low geneflowlevels(Nm< 0.5), unchanged geneflowlevelsorincreasedisolationofthepopulations willhavelittleeffect on itspopulationgenetics.But ifdisturbance actsto increasegene flowfor sucha taxon,thengeneflowmaybe deleterious becauseofthepossibility of outbreeding depression. The impactofoutbreeding depression varieswithm, the fractionof immigrants introduced by gene flow. As populationsize decreasesrelativeto a constant number ofimmigrants, theriskofoutbreeding depressionincreases.Gene flowat thelevel of 1% or less will be of little concern;gene flowat ratesof 10% or moremayhave a substantial impact on fitness.In suchcases, management mustincludereducinggeneflow.The specificsolutionwilldependon whygeneflowlevelshave increased. Increasedgene flow is most likelyto arise in threesituations:(i) if disturbance reducesthesize ofa population of seedssired so thatthefraction by immigrant pollenincreasesor thefraction of immigrant seed increases, (ii) if a commonsubspeciesor race (particularly a weedyone) dramatically witha raresubspecies or sympatric expandsitsrangeandbecomesparapatric or race, or (iii) if misguidedconservationmanagementeffortsinclude transplantation to enhancegeneflowor populationsize. In the firstcase, reducinggene flowmay be difficult. Managementof or flowering hosts pollinators timesarepotential solutions.Plantingalternate in intercepting forthepollinators aroundthepopulation mayproveeffective immigrant pollen. Such "guard rows" or "barrierrows" are generally in preventing effective pollenfromentering cropbreedingblocksand seed the firstcase will probablybe productionfields (see 36). Fortunately, rare. relatively In the second case, reducinggene flow requiresa straightforward, if sometimes of thecommonrelativeof the costly,solution-localeradication taxonat risk.Eradication maybe desirablealso becausetherelativemaybe tothetaxonatriskorothersensitive weedyenoughtoposea competitive threat speciesin theregion. The thirdcase is mostlikelyandpotentially mosttroublesome. Transplantationis oftencitedas a management solutionto bringpopulationsup to in 30). minimum viablesize or to enhancelocal geneticdiversity (references If thetransplanted materialcomes froma populationthathas differentiated fromthe local population,the expressionof outbreeding depressionupon matingwill be immediateand has thepotentialto be severe.Outbreeding as a problemin animalconservation is well-known depression genetics(106) in "canbe severeenoughtoincrease and, thecase ofreintroduced populations, chances of extinctiongreatlyfor a few generations"(95). Outbreeding has alreadycaused the depressioncreatedby conservationmanagement
large (Capra ibexibex,107). Additionally, ofan animalpopulation extinction (30). Ifevidencesuggests projectsoftenhaveotherdrawbacks transplantation andifthenumber willoccuraftertransplantation, depression thatoutbreeding populationsize, the immediate exceeds 10% of the current of transplants thepossiblelong-term wouldfaroutweigh accruedtothepopulation problems If no data populationsize and/orgeneticdiversity. benefitsfromincreasing is desirable,no morethana fewtransplants areavailable,andtransplantation (no morethan1% of theextantpopulation)wouldbothminimizetheimpact and sufficeto enhancegeneticdiversity. depression of possibleoutbreeding and problemsof geneflowshouldbe addressedin anyplant The benefits geneflow ofmostintraspecific plan.Identification management conservation In most cases, shouldbe straightforward. problemsor theiramelioration of gene flowas a potentialhazardby plant and consideration recognition will preventfutureproblemssuch as costly, conservation decision-makers projects. transplantation problematic andpotentially unnecessary,
GeneFlow Interspecific (repeated and introgression gene flowoccursby hybridization Interspecific of a hybridto one or bothparentaltypes-42). "Hybridization backcrossing andspeciation"(90). ofplantevolution andimportant component is a frequent Perhapsmorethan70% of plantspeciesare descendedfromhybrids(42). arecommon hybridization andintergeneric naturalinterspecific Furthermore, in plants;well-studied examplesnumberover 1000 (42, 102), and putative (59). examplesnumberin thetensof thousands biologymaybe The roleof interspecific geneflowon plantconservation ofpartially speciesanda population ofa sensitive whena population important to occur mating or fullycompatible relativesareclose enoughforsubstantial in and of hybridization its prevalence natural (25). Despitetheimportance geneticsrarelyaddress on plant populations,reviews plantconservation flow see 89). (but gene interspecific gene flow in endangered Is thisneglectfromthe factthatinterspecific in conservation an role genetics? plant is so rare as to play insignificant species To answerthisquestion,we used theRAREFIND (17) databaseand others forinterspecific sensitive toidentify California's planttaxawithhighpotential withmorecommontaxa or are gene flow-thosethatare eitherhybridizing withcongeners. sympatric we found22 sensitivetaxa of taxonomicambiguity, Removingsituations with more (ca. 3%) involvedin probableor documentedhybridization commonrelatives(listavailablefromauthors).This listmaybe a significant data on rarespecies of theirnumbers.Biologistssubmitting underestimate biologistsmightavoid Also, conservation mightoverlookhybridization. because theyrecognizethatsensitivespecies inmentioning hybridization
PLANT CONSERVATION GENETICS
volved in naturalhybridization may fail to receiveprotection understrict interpretation of the"HybridPolicy"of theUS EndangeredSpecies Act of 1973 (81). As oflate1992,RAREFINDprovided dataon 743 (outof 1600+) sensitive planttaxa;142werelocallysympatric withcongeners. Therefore, interspecific matingis likelyforover 19% of California'ssensitiveflorain thedatabase, andhybrid swarmsareknownforabout3%. We also surveyed the93 protected plantspecies of the BritishIsles (103) and found9 (10%) thatnaturally hybridizewithmorecommonspecies. In Californiaand the BritishIsles for interspecific opportunities gene flow are commonenoughto warrant consideration as a factorin plantconservation management. (Forinformation on theconservation statusof hybrids, see 81, 89.) Interspecific matingbetween a sensitivespeciesand a commonone will have one of two consequences relevantto conservationbiology. If hybridprogenyand progenyfrom advancedhybridization are vigorousand fertile,thenthe speciesis at risk fromgeneticassimilation. Ifhybrid aresterileorhavereducedvigor, progeny thenthespeciesis at riskfromoutbreeding depression. Extinctionfromgeneticassimilationoccursin the absence of selection againsthybrids. The problemhasbeenknowninplantsfordecades.Ratcliffe of a rare (87) observed"speciesmaybe disappearing through introgression plantwitha morecommonrelativeto producehybridswarmsin whichthe of therarespeciesarefinallyswamped."Geneticassimilation characters has also beenrecognizedas a conservation problemformanyvertebrate species (e.g. 6, 76). Small populations are at greaterriskthanlargeones fromgeneticassimilation.As population size oftheendangered speciesdecreasesrelativeto that of the sympatriccongener,the effectsof geneticassimilationbecome Thesituation also holdstrueforparapatric increasingly important. populations becauseof geneflowasymmetry discussedabove. Outbreeding depressionis theotherconservation problemassociatedwith interspecific mating.Dependingon thespeciesinvolved,hybridization can drasticallyreduce a plant's maternalfitness.Decreased fitnesscan be manifest Forexample, earlyas reducedseed set.The costcan be substantial. crosseswithinspecies of Gilia subsectionArachnionresultin few or no abortedseeds, but crossesamongspeciestypicallyresultin seed abortion rates of 50% or more (41, 43). The dramaticfitnessconsequencesof of unusuallylow outbreeding depressionmayaccountforoccasionalreports seed set whenan endangered witha commonrelative speciesis sympatric (17). can also be manifest of sterileor weak Decreasedfitness bytheproduction EFFECTS ON GENETIC DIVERSITY AND FITNESS
hybrid progeny.Forexample,over75% ofthenaturally occurring hybrids of theBritishIsles are fullyor mostlysterile(102). Even ifhybridprogenyare notsterile,if theparentsare well-differentiated ecologically,theiroffspring mightbe able to growand reproduceonlyin rare,intermediate microsites (2). As in thecase of intraspecific outbreeding depression,the frequency of outbreeding depressionfrominterspecific matingis expectedto increaseas thesize of thepopulationin questiondecreases.Almostone out of fiveof Califomnia's sensitiveflorahave one or morepopulationssympatric witha congener.Manypopulations at riskhave sizes smallerthan100 individuals (17) so thatpollenflowfroma sympatric relativecould have a substantial impacton plantfecundity. IMPLICATIONS FOR CONSERVATION Problemsfrominterspecific gene flow will probablyoccurin onlya fraction of thecases wherea sensitivespecies is sympatric witha congener.Interspecific geneflowmaybe obviousby the presenceof hybrids of intermediate morphology. If morphological traitsare unreliable, hybridization maybe confirmed by biochemicalgeneticmethods (70, 91). Ifno hybrids arepresent, itshouldstillbe relatively easyto identify highrisksituations. First,speciesat riskmustbe sympatric to witha congenerforintermating occur.Whilecongenerscouldbe nativespecies,theycould also be weeds, to many crops,orotherdomesticated plants(25). Forexample,a majorthreat sunflower withtheweedy endangered (Helianthus)speciesis hybridization annualsunflower, H. annuus,whichhas dramatically expandedits range followinghumandisturbance withdomesticated (92). Also, hybridization in theextinction of at leastsix wildspecies(e.g. specieshas beenimplicated 98). In California,the rare Juglanshindsiiis at risk of extinctionby withcultivated hybridization walnut,J. regia(73). mustoccur.Intermating ratesof 10% or Second, substantial intermating moreare probablysufficient to be detrimental. Pollentransfer ratescan be crudelyestimated basedon knowledge ofthedistancebetweenthecongeners, theirbreeding theirphenologies, andtheirpollinators. Distancealone systems, to keep the populationsisolated.Generally,50 m is mightbe sufficient sufficient to isolate a populationif it is highlyselfing(i.e. withtypical ratesof < 10%) (28). Butpopulations rates withhighoutcrossing outcrossing (i.e. self-incompatible ordioeciousspecies)require500 mormore(28). Other typesof prezygoticreproductive isolationare much more effective.For example,plantsthatflowerin different seasonsare highlyisolated,as are thosethatdo notsharepollinators (67). Even if pollentransfer occurs,intermating mightnotoccurif thespecies are cross-incompatible is apparently substantial and (67). If pollentransfer
PLANT CONSERVATION GENETICS
cross-compatibility is unknown, simplecross-pollination experiments should determine whether pollentubesare arrested in thepistil(cross-incompatibility), fertilization occurs but a substantialfractionof seeds are aborted (outbreeding depression), or hybrids areproduced(geneticassimilation). Third,boththe relativeand absolutesize of thepopulationat riskwill determine theimpactofinterspecific willoccur geneflow.Highrisksituations whenthecongeneris numerically superior to thevulnerable population.The difference may be functionally magnifiedif the congenerpopulationis reproductively morevigorousthanthevulnerable population intermsofpollen productionor pollen export(25). Also, when the vulnerablepopulation becomessmall enoughfordemographic stochasticity to become important 50 or less; 75), chanceeventsmayplaya rolein therelative (approximately frequency of interspecific mating. If the evidencesuggestsa high risk of interspecific gene flow, then management stepsmustbe swiftand surebecause of the speed at which can occurand becauseof thesubstantial fitnesslosses geneticassimilation accruedfromoutbreeding depression.Eradicationof thegene flowsource and/ortransplantation are the only solutionsfor the problem(89). For in the example,Rieseberget al (91) used isozymesto confirm hybridization world's only populationof Cercocarpustraskiae.They suggestedthata sympatric individualof C. betuloidesbe removedand that"cuttings representing thefive'pure'C. traskiaetreesbe transplanted tootherareas...where theriskofhybridization is minimal."In certaincases,itmayalso be necessary to eliminateall hybridor introgressed individuals.Thatdecisionshouldbe based on theecologicaland geneticconsequencesof thataction.In thecase of C. traskiaeabove, removalof all hybridswould removea substantial portionof theglobalpopulation of thespeciesanda substantial portionof its geneticvariation(89).
SUMMARY We have identified circumstances thatput rareplantspecies and small at geneticrisk.Although notall rareplantsare at geneticrisk,it populations will occur commonlyenoughto be of concernto conservation managers. Changesin factorssuchas populationsize, degreeof isolation,and fitness arewarningsignsthatpopulations maybe vulnerable. Managersmaybe able to use pre-existing data to determine whether such changeshave occurred, butadditional ordescriptive to make evidencemaybe necessary experimental a determination. Whensuchdata suggestthatpopulations are likelyto be at and simple.We see our risk,mitigation measuresmaybe straightforward workas a firstattempt to bringpopulationgeneticprinciplesintoa context forapplication by plantconservation managers.
ELLSTRAND & ELAM
This paperenjoyedcontributions fromP. Arriola,R. Bittman,J. Clegg, B. Epperson,J. Gehring,S. Junak,J. Karron,A. Montalvo,S. C. Morey,M. Neel, R. Podolsky,M. Price,R. Sherry,D. Steeck,and N. Waser.We are grateful to R. Bittmanand N. Vierraforpermission to use the California Department of Fish and Game's RAREFIND database.We also thankPatti Fagan fortypingthispaper.Portionsof thisworkweresupported by NSF BSR-92-02258to NCE.
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MITIGATION-RELATED TRANSPLANTATION, RELOCATION AND REINTRODUCTION PROJECTS INVOLVING ENDANGERED AND THREATENED, AND RARE PLANT SPECIES IN CALIFORNIA
Submitted by: Peggy L. Fiedler Depaa tment of Biology San Francisco State University San Francisco, California 94132
Submitted to: Ainn Howald California Depm'maent of Fish & Game Endangered Plant Program 1416 Ninth Street, P.O. Box 94409 Sacramento, Califomia 95814-2090
Funded by: California Endangered Species Tax Check-Off Fund Contract No. FG-8611
FINAL REPORT: MITIGATION-RELATED TRANSPLANTATION, RELOCATION, AND REINTRODUCTION PROJECTS INVOLVING ENDANGERED, THREATENED, AND RARE PLANT SPECIES IN CALIFORNIA
To investigate the' efficacy and overall success of transplantation, relocation, and reintroduction of California State-listed endangered, threatened, and rare species, a questionnaire was mailed to 377 individuals, state and federal agencies, and public and private institutions that potentially have been involved in transplantation, relocation, and reintroduction projects. One hundred sixty-eight questionnaires (168) were returned. Of these, twenty-four (24) individuals and/or agencies indicate that they have been directly involved in mitigation-related projects for California plants; one hundred fourteen (114) individuals and/or agencies have not. At minimum, this represents a 45% return rate for the questionnaire. Files of California Department of Fish and Game's Endangered Plant Program were also reviewed to complete the survey. An additional 13 projects involving eight (8) State-listed species were identified as of these types. Information obtained from the Endangered Pl_t Program files supplemented 13 responses to the questionnaire. This report summarizes the results of the questionnaire for each species identified by the respondents and information obtained from the Endangered Plant Program's files. A total of fortysix (46) projects were reviewed, involving fifty-three (53) transplantation, relocation and reintroduction attempts with forty (40) special status species. Of the plant species examined in this review, 25 (63%) axe listed by the State as endangered, 3 (8%) are listed as threatened, 6 (15%) are listed as rare, and 6 (15%) are not listed by the State, but have some other form of protection or special status. In addition, the ;40plant species reviewed belong to 21 plant families. Asteraceae represented the highest number of species involved (9; 23%), followed by the Brassicaceae (4; 10%). Eight (8) additional plant families were represented by two taxa, while ten (10) families were represented in this study by one taxon. The genus Erysimum had the greatest number of taxa (3) involved, followed by the genera Brodiaea, Hemizonia, Lupinus, and Oenothera (2 each). Results of the survey indicate that of the 46 projects reviewed, 38 (83%) are mitigation-related, while eight (8) projects (17%) are research-related. Of the 53 manipulation attempts, forty-one (41; 77%) involved translocation (including relocation) of species of concern, nine (9) projects (17%) involved reintroduction, and 2 projects (4%) involved restoration of a population of a Statelisted species. One additional project reviewed is a research-related project that has yet to include a transplantation, relocation or restoration component. Thirty-six (36) projects have been implemented, while ten (10) projects are still in the planning stages. Seventeen projects (27%) are developments for housing, business parks, or recreational facilities initiated by private companies and corporations. Eleven projects (24%) are the result of state service operations, such as those by the California Department of Transportation and Department of Water Resources. The remaining projects are either initiated by county services (9%), private and public energy utilities (11%), or are research related. Of the total 46 projects, only 15 projects (33%) had explicitly defined criteria for success of the mitigation project, while Final mitigation T/fir June 14, 1991
the remaining 31 (67%) either had no criteria for success or the criteria were only vaguely defined. Only 15% (8) of the 53 transplantation, relocation, or reintroduction attempts reviewed should be considered fully successful (13% of the 46 projects). Plant species for which the project was successful included Amsinckia grandiflora, Dudleya cymosa ssp. marcescens, Holocarpha macradenia, Lasthenia burkei, Opuntia basilaris var. treleasei, and Sidalcea pedata. However, of these eight (8) projects, only four (4) are mitigation-related. Therefore, the success rate of the mitigation-related transplantation, relocation, and reintroduction attempts is 8% (9% of the projects). An additional seven (7) transplantation projects (13%) (9 attempts [17%]) are considered partially successful, or of limited success. Twelve (12) projects (26%) are considered here to be unsuccessful, no information was found in the review of files for four (4) projects (9%), and the success of an additional sixteen (16) projects (35%) could not be evaluated because they are on-going or in the planning stages. In a summary review of the successes and failures of transplantation, relocation and reintroduction of sensitive plant species in California, three broad recommendations can be made that are based on crucial aspects of the biology of imperiled plant species. These recommendations are: (1) Individuals should be removed with as little physical disturbance as possible to the individual, and at a phenologically appropriate time of year, as when the individual is dormant or photosynthetically inactive; (2) The receptor site should be of the same habitat quality, particularly with respect to soil type and its physical characteristics. Various other manipulation aspects of the receptor site may include weeding to decrease competition from native and exotic species, watering during times of drought, and fencing and/or other forms of site protection; and (3) Knowledge of the biology of the organism appears to aid greatly in the design of appropriate horticultural techniques for the preparation of cuttings, transplantation, seed germination, etc. This is problematic, however, because the biology of most State-listed species is poorly known. Although some species such as cacti and succulents may be amenable to standard horticultural techniques for propagation, most are not. Therefore, without sufficient knowledge of the biology of impacted species, success of the transplantation, relocation, or reintroduction will not be assured. Finally, it is suggested that because of the lack of or limited success (21; 32% combined) of most of the transplantation, reintroduction, or restoration attempts documented, and the uncertainty of many of the on-going projects, the Endangered Plant Program of the California Department offish and Game's Natural Heritage Division should remain extremely cautious in any mitigation agreement that will allow any of these techniques to serve as mitigation for project impacts.
Final mitigationTMr June 14, 1991
TABLE OF CONTENTS I. EXECUTIVE SUMMARY
II. INTRODUCTION AND PROJECT OBJECTIVES .........................
V. DISCUSSIONOF FINDINGS .................................... V.A. MitigationSuccesses .................................... V.B. MitigationFailures ...................................... V.C. Overviewand Summary ...................................
70 70 74 77
LIST OF TABLES TABLE 1.
SUMMARY OF RECIPIENTS OF THE MITIGATION QUESTIONNAIRE................................
SUMMARY OF RESPONSES TO MITIGATION QUESTIONNAIRE
CALIFORNIA STATE ENDANGERED, THREATENED, AND RARE PLANT SPECIES INVOLVED IN MITIGATION-RELATED OR RESEARCH-RI_.I .ATED TRANSPLANTATION, RELOCATION, OR REINTRODUCTIONPROJECTS ............................
Final mitigation T## June 14, 1991
PLANT SPECIES INVOLVED IN TRANSPLANTATION, RELOCATION, OR REINTRODUCTION PROJECTS, PROJECT PROPONENTS, AND DEGREE OF MITIGATION SUCCESS ..........
The Endangered Plant Program (EPP) of the California Department of Fish and Game (CDFG) requested that mitigation-related
.relocation, and reintroduction
the State's endangered, threatened, and rare plant species be assessed for overall project efficacy and success. Thus the purpose of this research is to document the results of mitigation-related projects of this type involving the State's rare plant species of concern.
serve in the future as a position paper for the EPP's policy on transplantation,
reintroduction of State-listed species as mitigation.
The Depzuia_ent of Fish and Game currendy requires an approved Mitigation Agreement (MA) for the manipulation of State-listed species (cf. Howald and Wickenheiser 1990). An MA is the legal document used by CDFG to approve mitigation projects for State-listed species that are required under the California Environmental
Quality Act, Statutes, and Guidelines (CEQA).
not explicitly defined in CEQA, But is listed as "including": (a) Avoiding the impact altogether by not taking a certain action or parts of an action. (b) Minimizing impacts by limiting the degree or magnitude of the action and its implementation. (c) Rectifying the impact by repairing, rehabilitating,
or restoring the impacted
environment. (d) Reducing Or eliminating the impact over time by preservation and maintenance operations during the life of the action. (e) compensating for the impact by replacing or providing substitute resources or environments
If these five forms of mitigation are interpreted as priority in Order of listing, then the preferred form of mitigation under CEQA (1986) is project avoidance, followed by minimization of impacts, rectification of impacts, etc. It should be noted that compensation is the least preferable form of Final mitigation T#/r June 14, 1991
mitigation under this interpretation.
To begin the assessment, a questionnaire was developed by the author and
reviewed by members of the CDFG's Endangered
Plant Program. Three hundred seventy-seven
(377) individual questionnaires were sent in the summer of 1989, along with, at that time, a current list of State-listed endangered, threatened, and rare plant species (California Depa_ tment of Fish and Game 1989), to a broad spectrum of pubfic resource and land management
consulting farms, nurseries, museums, academic institutions, and private individuals or conservation organizations
(Table 1). The individuals selected for the survey were compiled from
California Native Plant Society and California Department of Fish and Game files, and personal mailing lists. The questionnaire and cover letter are included as Appendix A. The mailing list is included as Appendix B.
Review of Internal Files: Project and species files held by the EPP were reviewed in the winter of •1990, to clarify materials received from the questionnaire and to gather additional information. These files were particularly helpful regarding the MOU and MA conditions of the mitigationrelated projects. Most, but not all of the current (i.e., on-going and/or currently negotiated) mitigation-related
projects were reviewed.
However, several recently initiated and on-going projects that conform to newly instituted EPP mitigation standards are not reviewed in this document because assessment of their success is not possible at this time.
Mitigation Project Assessment:
received and EPP files reviewed were
examined for the following information: (1) whether the project reported was mitigation- or research-related, Final mitigation T/rR June 14, 1991
(2) mitigation project objective(s), (3) responsible party's criteria for mitigation success, (4) transplantation, relocation, or reimroduction methods, (5) design and implementation (6) respondent's
of the mitigated population's monitoring plan,
assessment of mitigation project success, and
(7) date of transplantation,
or relocation project.
Once these data were compiled, the projects were tallied for their assessed success and efficacy. The results of this analysis are summarized in Section IV.
A total of one hundred sixty-eight (168) questionnaires was returned for this survey. All those organizations and individuals who responded to the questionnaire, and their summary responses are listed in Appendix C.
The majority of respondents (114, 68%) have not been involved in any transplantation, relocation, or reintroduction project involving state- (or federally-) listed endangered, threatened, or rare plant species. Twenty-four (24) individuals have been involved, however, and they are reviewed in detail in Section IV.A and IV.B. Table 2 outlines the responses to questionnaire.
A significant number of respondents reported on transplantation, relocation, and reintroduction projects that were not mitigation-related,
but rather, research-related.
are defined as those that required either an MA or formerly, a Memorandum of Understanding 0VlOU). Thus several of the projects described in the returned questionnaires were research activities that did not require a Mitigation Agreement (MA). These projects were included in the analysis, and are described in Section IV.B. However, the listing is not exhaustive for researchFinal mitigationT/r# June 14, 1991
OF THE MITIGATION
QUESTIONNAIRE Organizationor Individual ConsultingFirms Resource Agencies Federal State County City Private NaturePreserves Museums Private Energy Companies PublicUtilities Private Conservation Organizations BotanicGardens Nurseries Universities
...... 1The numberof questionnaires will not sum to a total of 377 because in many cases several individuals wlm!n me sam.,e.office were sent a quesuonn..a_r." e. Therefore, although the questionnaire may have been uupacatea wlmm any one office, the probability of receiving a response was increased. 2The first number in this column represent the total number of different federal agencies queried. These included the U.S. Fish and Wildlife Service, U.S. National Park Service, U.S. Environmental _eOtecfionAgenc_ U.S. Army Corps of Engineers, U.S. Bureau of Land Management, U.S. Soil Conservation rvice, U.S. Air l-ore,e, U.S. Navy, and the U.S. Forest Service. The number m parentheses indicates the total number of federal agency offices contacted. 3The first number in this column represents the total number of different state resource agencies queried. JRThaec_seoinCluded_the Californ'mDepartment o.fFish and G.ame,Department of Fores.ta.%Dep,'Etmeatof Transportation, n _tate l-ore, s t, State Lanas Resources, t_omm_ssmn,t_alifornia Corps, Califomm Department of Parks ecreatmn, Department of Water Department oftzonservafion Food and Agriculture, and the Division of Mines andand Geology. The number in parentheses indicates the total number of state offices contacted. 4The fi_.t number represents the total number of coanty offices queried. These include planning and resource offices m the followmg ten counties: Chico, Placer, San Diego, San Luis Obispo, Sacramento, Santa _areara,&olano, Sonoma, Tuommne, and Yolo. The number in parentheses represents the total number of county omces contactea. 5plaaning and resource agencies were contacted in the cities of Santa Rosa, Modesto, and San Diego. 6The fast number in this column represents the total number of different colleges and universities queried, including American River College; Butte College; California Polytechnic Pomona; California State Universities at Bakersfield, Chico Hayward Humbolt, Sacramento, San Diego, San Franc sco, San Jose, and San Luis Obispo; Mills College; Pacific Union College; Palomar College Stanford University; University of Califomia at Berkeley, Davis, Santa Barbara, and University of San D ego. Final mitigation Th'lr June 14, 1991
Number of "Q._,,_._.aI_,/_2_
Resoonded Ye_ Responded N02
Private Individuals/ Citizen Groups
Resource Agencies State Agency Offices Federal Agency Offices CountyOffices City
10 (44)8 9 (30) I0(15)
11 7 4
9 13 9
Private Nature Preserves
PrivateConservation Organizations 4
7In all cases in this table, the total number of respondents will not total to 168 because multiple individuals were contacted within a single office or agency, and therefore multiple questionnaires were returned from a single office or agency. Sin all cases, fhst number in the column represents the total number of agencies queried, and the number in parentheses represents the total number of offices contacted. Final mifigatlonT/r# June 14. 1991
relocation, and reintroduction
projects, but it is considered nearly so for
projects of these types.
A total of forty-six (46) projects were review, involving 53 transplantation, relocation, or reintroduction
efforts. Forty (40) plant species were reviewed, 34 (85%) are listed by the State,
federal goverment, or the California Native Plant Society as either endangered,
threatened, or rare.
Specifically, 25 (63%) are listed by the State as endangered, 3 (8%) are listed asthreatened, and 6 (15%) are listed as rare, and 6 (15%) are not listed by the State, but have some other form of protection or special status (California Department ofFish and Game 1990, Smith and Berg 1988).
In addition, the 40 plant species reviewed belonged to 21 plant families.
the highest number of species involved (9; 23%) including species in the genera Blennosperma, Cirsiurn, Eriophyllum, Hemizonia, Lasthenia, and Pentachaeta. This was followed by the Brassicaceae (4; 10%), encompassing the genera Arabis, Eryngium, and Erysimum. Eight additional plant families were represented by two taxa, while ten families were represented in this study by one taxon. The genus Erysimum had the greatest number of taxa (3) involved in this study, followed by the genera Brodiaea, Hemizonia, Lupinus, and Oenothera (2 each).
Additional results of the survey indicate that of the 46 projects reviewed, 38 (83%) are mitigationrelated, while eight (17%) are research-related.
Of the 53 manipulation attempts, forty-one (41;
77%) involved translocation (including relocation) of species of concern, nine (9) projects (17%) involved reintroduction,
and 2 projects (4%) involved restoration of a population of a State-listed
species. One additional project reviewed is a research-related transplantation,
relocation or restoration
project that has yet to include a
Of the 46 projects reviewed, 40 projects have been implemented, Final mitigation T/fir June 14, 1991
while 4 projects are in the
planning stages. Of the total 46 projects, only 15 projects (33%) had explicitly defined criteria for success of the mitigation project, while the remaining 31 projects (67%) either had not criteria for success or the criteria were only vaguely defined.
Only 15% (8) of the 53 transplantation,
relocation, or reintroduction
considered fully successful (13% of the 46 projects).
attempts reviewed should be
I define "success" in this survey as either:
(1) the respondent to the questionnaire felt that the project was successful;
or, (2) greater than 75%
of the mitigation propagules established a reproducing population over the life of the project as reported.
"Unsuccessful" projects were determined to be so in this survey because either: (1) the
respondent in the questionnaire reported that the project was unsuccessful; or, (2) less than 25% of the mitigation propagules
established a population, and subsequently
died. "Limited success" was
assigned to those projects for which: (1) the respondent in the questionnaire reported as "limited" or "partially" successful; or, (2) the respondent reported a middle range of mitigation propagule establishment
(>25% but <75%):
Plant species for which the transplantation,
relocation, or reintroduction
project was successful
included Amsinckia grandiflora, Dudley cymosa ssp. marcescens, Holocarpha macradenia, Lasthenia burkei (3 projects), Opuntia basilaris var. treleaseil and Sidalcea pedata. However, of the eight projects involving these species, only four are mitigation-related; rate of the mitigation-related
therefore the success
attempts is 8%. An additional seven (7) transplantation attempts
(13%) are considered partially successful, or of limited success. Twelve (12) of the 53 attempts (23%) are considered here to be unsuccessful, and the success of an additional four projects is unknown (i.e., unreported or no information was found in EPP f'tles). Sixteen projects (35%) could not be evaluated for their success because they are on-going or in the planning stages.
Final mitigation TRkr June 14, 1991
Plant Species Involved
The following is a discussion of the state- (and federally-) listed species that have been the subject of mitigation-related transplantation, relocation and reintroduction projects, as outlined by the respondents of the questionnaire
and a review of the EPP files. Table 3
lists the endangered, threatened and rare plant species involved in transplantation, relocation, and reintroduction projects. Information from the questionnaire and EPP files is summarized
briefly by species. Questionnaires
and personal notes are on file and available
for review of additional information.
iliclfolia (San Diego Thommint):
Federally Candidate Category 1, CNPS List lB. Respondent:
None. Data obtained from EPP files.
Project Name and Descriotion: "Westview Planned Residential Development." The Pardee Company agreed to mitigate for destruction of a population of A. ilicifolia by the construction of a road (Black Mountain Road) and a housing development by creating a 13.6 acre on-site open space preserve for the San Diego thorn-mint. _:
Proiect Obiective._: The goal of the mitigation plan was to create a viable population of A. ilicifolia in an on-site preserve through the importation of seed and soil. _:
The Pardee Company contracted with Environmental and Energy
Services Company (ERC) to salvage al! the Acanthomintha ilicifolia seeds in the population affected by the construction.
10.8 gm. of seed were collected in July 1988.
Topsoil was then salvaged from the Acanthominta ilicifolia population area to collect seed potentially stored in the soil. The soil was transported to the mitigation site.
Final mitigationTMr June 14, 1991
CALIFORNIA STATE ENDANGERED, THREATENED, AND RARE PLANT SPECIES INVOLVED IN MITIGATION-RELATED OR RESEARCH-RELATED TRANSPLANTATION, RELOCATION, OR REINTRODUCTION PROJECTS
9State of California, Department of Fish and Game, Nongame-Hedtage Program, Endangered Plant Project. Designated Endangered, Threatened or Rare Plants. 1990. Final midgationT/r/¢ June 14, 1991
Twenty-five (25) 4 ft2 experimental plots in the preserve were located and prepared by removing existing vegetation. Seeds sown in the test plots were observed in December, 1988, while the remaining seed was sent to the Rancho Santa Ana Botanic Garden (RSA) for germination tests. Seedlings occurred in 12 of the 25 test plots in March 1989. At the time of the preparation of this reportl no additional information is available.
However, the MOU on
file requires a monitoring program to be established in the mitigation plots that must continue for five (5) growing seasons. Criteria for Success: As outlined by the MOU, performance criteria include: (1) erosion control [soil stabilized]; (2) weed invasion [no interference with A. ilicifolia establishment]; (3) herbivory ["minimal" damage to A. ilicifolia seedlings]; (4) vigor [5 cm minimum height per individual plant]; and, (5) reproductive success [to be determined on the basis of offsite monitoring]. Project Success: Project on-going. Date Project Initiated: July 1988.
2) Respondent: None. Data obtained from EPP flies. Proiect Name and Description: "Shea Homes Palos Vista Development."
designed a development of 979 acres within the city of Escondido that involved the construction of 730 homes and some open space. Shea Homes contracted initially (October 1988) with Royce B. Riggins and Associates (RBR), working in conjunction with Mr. Jim Dillane of the Lake Hodges Native Plant Club, to prepare the biological reports and initial mitigation design for the project. In May, 1989, ERC completed the work initiated by RBR. The mitigation site was selected as the San Diego Wild Animal Park. _:
Project Objcefiv¢,_: The goal of the mitigation contract was to assure the preservation of Final mitigation T/rh" June14,1991
two small disjunct populations ofAcanthomintha
ilicifolia thatwere originally located
within the boundaries of the Palos Vista residential development. Pro_iect Methods:
Plants were collected in June and July of 1988 and transplanted to the
mitigation site. The site is a 40 x 30 ft parcel on which a 2 ft layer of subsoil was imported and laid down prior to transplantation. _:
As outlined by the MOU Onfrie,performance criteria are based on
success, as follows: (1) number of plants shall equal or exceed 30% of the
mean density of plants in natural populations at the fn'st end of the growing season; (2) number of plants shall equal or exceed 50% of the mean density of plants in natural populations at the end of the second growing season; (3) number of plants shall equal or exceed 70% of the mean density of plants in natural populations at _e end of the third growing season; (4) number of plants shall equal or exceed 90% of the mean density of plants in natural populations at the end of the fourth growing season; and, (5i number of plants shall equal or exceed 100% of the mean density of plants in naawal populations at the end of the fifth growing season. _:
None. Data obtained from EPP fries.
Project Name and Descriotion: "Reparation for the Sabre Springs Development." the largest known populations ofAcanthomintha
ilicifolia is located on property located
within the City of San Diego Open Space System, previously owned by the Pardee Company.
In the spring of 1989, the population was reduced by one-third due to an
accidental road grading operation.
In order to avoid prosecution by the State for these
damages, Pardee Company was notified of several measures to rectify the damage.
Company has or is complying with all seven conditions of the reparation plan, but with Final mitigation Tk/r June 14, 1991
varying degrees of success. Miti_ation-Rela_ed?: Pro ieet Obiectives: Acanthomintha
Yes. To rectify the accidental damage inflicted on a large population of
The disturbed population was fenced and bermed, signed, weeded, and
the adjacent roadbed hydroseeded.
A second phase of the project will be to manage
suitable Acanthomintha ilicifolia areas near existing populations to encourage their spread. Seed will be broadcast onto suitable clay soils adjacent to extant stands in January, 1992. Criteria for Su¢¢e,s,S: As stated in the reparation plan, the goal of the project is to increase the remaining Acanthomintha ilicifolia population to predisturbance size or greater. Proiect Succes,s: Project on-going. _:
None. Data obtained from EPP files.
Pro!ect Name and Descriotion: urban development projects.
"Indian Hill," "McIntire" ("Las Brisas"), and "Spyglass" The three projects together required translocation
Acanthomintha ilicifolia to open space areas on the development sites. Mitigation projects were contracted to Pacific Southwest Biological Services (PSBS) of San Diego. PSBS was responsible for all relocation activities, including seed collection, and excavation and placement of clay soils associated with Acanthomintha ilicifolia (PSBS, Inc. 1988). _: Project Obiectives:
Yes. None stated. Presumably the project objectives were to establish viable
populations of Acanthomintha ilicifolia from transplanted plant material at four translocation sites (open space areas onsite at the Las Brisas and Indian Hill sites; within a natural, dedicated open space area at the El Camino Condominium
and Tennis Club; a project
adjacent to the Spyglass project; and within the natural area of the Quail Botanical Garden Final mitigation T/r# June 14, 199I
County Park. Pro_iect Methods:
Seeds were collected at Jetton Property (Las Brisas Mobile Home Park)
during the summer of 1986 and sewn by. hand on the relocated clay lens. Soils were excavated and prepared for seeding within a 24-hour period. Seeds were collected as whole plant material, occupying approximately 1/2 yd3 and weighing about 2 pounds. Criteria for Success: None state specifically. Project Success: The project was halted and the MOU terminated due to the difficulty the EPP had in dealing with PSBS. Success of the transplantation was limited as of May 1988. However, at the Las Brisas relocation site in May 1988, an estimate of between 7001000 individuals (I 100 "flowering heads") was reported. At the Quail Gardens relocation site, the population estimate was made during the seedling stage. As of 8 May 1988, "seed heads" numbered 70, while the population survey during the seedling stage resulted in 200300 plants. PSBS reported that associated native plant species were abundant at the Las Brisas site, though more rare at Quail Gardens. 12_,.__:
baked (Sonoma Sunshine):
Not state listed; Federal
Candidate C2; CNPS List lB. 1) Respondent:
Mr. Charlie Patterson, Plant Ecologist.
Private Consultant, E1 Cerrito.
Project Name and Descriptio0: "Montclalr Park." Project involved the construction of a small housing development
Homes in the city of Sonoma (lead agency
for the permit), entitled "Montclair Park." The mitigation included the dedication (as compensation) development,
2.0 acres of undeveloped land, located on the edge of the
within which up to 1.0 acres of actual vemal pool habitat would be created
and seeded with Blennosperma bakeri and associated vernal pool species. _dil_lg_B.tdalg_Final mitigationT/r# June 14, 1991
Objectives for the housing development were the replacement
0.5 acres of wetlands and of the pre-existing
10,000 individuals ofBlennosperma
of 0.3 to bakeri
that were destroyed during the construction of the housing development. Pr_eet Methods: The habitat was graded and shaped, creating approximately
vernal pools in a soil that is underlain by the same clayplan existing under the destroyed pools. Blennosperma bakeri seeds were collected in late May 1989 by collecting the dry flower heads, vacuuming the surface for seeds, duff and dust, and scraping by hoe, 1-2 inches of the top soil of existing pools. Collected seed and duff was air-dried in shallow trays in a cool, dry environment.
Seeds were transferred to the created pools by hand. The
created pools were fenced (wood and wire) and a berm constructed for protection. The project design also included several additional trial vemalpools
within a storm
runoff detention basin to investigate the feasibility of managing detention basins and vernal pools concurrently as a contaminant
Monitoring of the pools includes: (1) habitat integrity and stability; (2) Blennosperma bakeri growth and reproduction; and, (3) overall vernal pool community development. Criteria for Success: Essentially the replacement
of a self-sustaining
Blennosperma bakeri. This includes: (1) at least 75% of the created vernal pool habitat should be documented
as stable, with no measurable erosion or deposition,
and with no
significant channel formation; (2) at least 75% of the pools should have adequate [undefined] water-holding capacity; (3) local drainage patterns should be shown to be adequate [undef'med] to fill the pools (75%) without input from street runoff Or eucalyptus debris; (4) at least 10 colonies ofB. bakeri should be established in the new pools, and be self-sustaining
populations; (5) the total habitat area of at least 0.3 acres should be
dominated by Blennosperma bakeri for at least 2 years without supplement seeding; (6) the Final mitigation TMr June 14, 1991
total population should number at least 10,000 individuals without supplemental
2 years; (7) at least 75% of the total pool habitat should be dominated by typical (native?) vernal pool plants; (8) each pool should contain at least 4 (native?) vernal pool species; and, (9) encroachment by grasses and/or upland weeds should be documented as stable, with no significant advancement into the pools over the last 2 years of the monitoring program. Project Success: Respondent felt that, after one dry year, the results are promising -- i.e., several thousand individuals ofBlennosperma
bakeri are established. However, the pools
need to be regraded and probably deepened. Date Project Initiated: 1989.
None. Data obtained from EPP files.
Pro iect Name and Description: "Santa Rosa Rare Plants Mitigation Plan San Miguel Estates 1." In 1989 Cobblestone Development Corporation proposed the development of San Miguel Rancho Subdivision (RSM) at 2001 Waltzer Road within the city of Santa Rosa, Sonoma County and San Miguel Estates No. 2 (S/VIE)at 2192 Francisco Avenue, also within Santa Rosa. The SME project is an on-going housing construction and the RSM housing project was a 1989 development.
The projects would destroy approximately
2.51 acres of vernal pool habitat. (see IV.A.19(3) for more details.) Mitigation-Related?:
Project Obiectives: According to the Mitigation Agreement between Cobblestone and CDFG, the mitigation should establish self-sustaining approximately
of plants in
2.97 acres of newly created habitat on the mitigation site. Self-sustaining
defined as approximately 13,000 individuals of Lasthenia burkei and 137,000 individuals of Blennosperma bakeri for 2 consecutive years without supplemental seeding. Project Methods: The mitigation plan was devised by R. Osterling, Inc. (1989). The plan proposed to transplant all existing plants and/or seeds to a 20-acre receptor site located Plnal June mitigation 14, 1991 T#/r
1.5 miles west of the San Miguel Estates property, with existing 3.49 acres
of vernal pool resources.
2:5 acres of vernal pool habitat will be
constructed at the receptor site with pool configuration
and depth based on survey of
existing pools. Grading will be done with small equipment under supervision of a qualified botanist (Charlie Patterson, private consultant). Plant material will be "transferred."
Seed will be collected f(om donor pools and the top 1-2 inches of pool
bottom duff will be excavated and spread in the excavated pools at the receptor site. Monitoring will continue through June 1991. Criteria for Success: None explicitly stated. Proiect Success: Unknown. No information f'ound in EPP files. Date Project Initiated:
(Thread-leaved Brodiaea): State endangered; Federal
Candidate C1; CNPS List lB. Respondent:
None. Data obtained from EPP files.
Pro iect Name and Description: "College Area Specific Plan in San Marcos." The Baldwin Company proposed a development
on 530 acres of undeveloped land in the City of San
Marcos, on a ridge behind the college. The onsite population of Brodiaeafilifolia
is part of
the county's most extensive, known population. According to the monitoring plan (WESTEC 1988), the mitigation plan included: (1) all onsite mitigation activities; (2) a 12-acre preserve that is completely fenced (vinylclad chain-link), protected for the life of the project; (3) planting of (presumably) local plants; (4) creation of a stable, relatively weed free Brodiaeafilifolia
low maintenance; (5) onsite salvage of each plant species included in the preserve; (6) transportation and laying of suitable soils (Huerhuero Series); (7) maintenance during the fast several years; and, (8) monitoring by a qualified botanist. Final mitigationT/r?: June14,1991
Proiect Objectives: Two objectives were identified: (I) to set aside a 12-acre preserve for existing native grassland habitat supporting B.filifolia; and, (2) to reintroduce Stipa pulchra (purple needle grass) to disturbed portions of the preserve (ERC Environmental and Energy Services Co. 1990c). _:
During 1988, clay soils and 8167 B.filifolia corms were collected from a
25 ft2 area within the original population and brought to the preserve. Five plots were marked and rabbit exclosures were installed.
The largest corms collected were planted in
planting holes in the test plots and throughout the preserve.
Smaller corms were shipped to
a contract nursery (Tree of Life Nursery, San Juan Capistrano) to be grown for inci'eased size. A portion of these corms (870) were outplanted in the fall of 1990. Seed of Brodiaea filifolia also was collected from the original population and seedlings were grown at the nursery for two seasons. These were planted in the preserve in 1990 (ERC Environmental and Energy Co. 1990c). , Monitoring includes: (I) overall success; (2) role of corm size in relation to survivorship and flowering; (3) field establishment
of nursery corms under controlled
conditions with and without fertilizer treatments; (4) efficacy of relocating B.filifolia populations by soil importation; (5) role of supplemental irrigation in the establishment transplanted corms; and, (6) use of field-collected corms in restoration (ERC Environmental _t.J_L_&qg_:
seed and nursery-generated
and Energy Services Co. 1990c).
Criteria for success includes: (1) 75% survival rate of Brodiaea
filifolia corms in test plots and 80% in the grassland; (2) 80% survival rate of Stipapulchra plugs (seeds were planted similarly and an 80% survival rate was considered for this activity); (3) weeds should not cover the test plots dense enough to interfere with Brodiaea filifolia establishment
and noxious weed species [undef'med] should be eliminated from the
preserye: The same criteria were considered for the S. pulchra plantings; (4) herbivory Final mitigation T#/r June 14, 1991
damage assessed as above-ground and below-ground growth forB.filifolia.
damage to vegetative material is 10% or less of all plantings. Gopher damage to corms cannot exceed 5% in any one plot or 20% overall; and, (5) acceptable herbivory losses for S. pulchra should not exceed 10%. No criteria were established for reproductive success, "offset" production of corms, or soil importation. Project Success: Project is in-progress and will continue until December 1993. To date, preliminary results of the monitoring efforts indicate that the introduction of Brodiaea filifolia corms has been largely successful. 1989 and 1990. Eighty-seven
Corm growth increased significantly between
percent (87%) of the corms have remained viable and 19.9%
have produced "offsets." Also, fertilizer treatments of corms grown in the nursery did not improve vegetative development. improvement
Irrigation showed initial signs of promise in
of corms, particularly with soil importation.
At the time of
the monitoring report, results were not available for assessing the success of the transplanted
Direct seeding was not successful, in either the
irrigated or non-irrigated seed locations.
Why it was not successful is not known, but it
may be possible that the seeds were held in storage too long and lost viability. The 1989 planting of Stipa pulchra plugs was not successful due to the late planting in conjunction with very warm weather and drought. A portion of the plugs was replaced in winter 1990, and an additional experimental plot was installed in 1990 to test the effects of supplemental irrigation on S. pulchra establishment. Significantly more plants survived than those grown from seed (94.8% vs. 61.6%). Efforts to eliminate sweet fennel (Foeniculum vulgare) and cardoon (Cynara cardunculus) have largely been successful, although mustard (Brassica [nigra?]), wild radish (Raphanus sativus), and invasive annual grasses are not controlled. Herbivory on Brodiaeafilifolia
by rabbits does not appear to be a problem,
although there appears to be some disturbance by gophers within as well as outside the Final mitigation T/rh" June 14, 1991
exclosures (ERC Environmental _:
and Energy Services Co. 1990c).
Brodiaea insiznis (Kaweah Brodiaea):
State endangered; Federal Candidate
C1; CNPS List lB. Respondent:
Mr. John Stebbins, Fresno.
Project Name and Description:
"Kaweah Reservoir Dam Expansion" (Tulare County),
initiated by the California Department Of Water Resources.
Project plans are being drafted
at this time. _:
Project Obiec_iv¢_: Project plans are being drafted at this time. Net yet available. _:
Project plans are being drafted at this time. Net yet available.
Criteria for Success:
Project plans are being drafted at this time. Net yet available.
Project Success: Net yet available. Date Project Initiated:
ereene( (Greene's Mariposa Lily): Not state listed; Federal
Candidate C2; CNPS List lB. Respondent: Mr. William Ferlatte, Siskiyou County Dept. Agriculture and Ms. Barbara Williams, U.S. Forest Service, Klamath National Forest. Proiect Name and Description:
None. Calochortus greenei is not a state-listed species,
and both respondents answered briefly. Project involved a road widening/construction project that required two mitigation _g_: Project Objectives: ]_,_q_: Final mitigation T/r/r June 14, 1991
Yes. None stated. None stated, but presumably the bulbs were dug by hand and transported
to the mitigation sites and replanted there. _ed:iaS[gL_/g_:
Pro!eci Success: Approximately 65 plants/bulbs were transplanted on May 23, 1989. As of May 9, 1990 [sic] (June 1989?), approximately transplantation
onto U.S. Bureau of Land Management
in a survivorship rate of approximately _:
10 individuals survived the and private property.
howeHii (Howell's Spineflower):
State threatened; Federal
Candidate C2; CNPS List lB. Respondent: Ms. Frederica Bowcutt, State of California Department of Parks & Recreation,
Proiect Name and Description: None. Project involved the reintroduction of Chorizanthe howellii and Erysimum menziesii to archeological sites at MacKerricher State Park (Mendocino County) after an archeological dig. The site is a coastal dune ecosystem. University of California, Davis, initiated an archeological dig in 1989-90 at sites containing rare species. (see IV.A.13(1) for more details). _d_ga/_lz_d_d_: Project Obiecfives: _:
Yes. None stated. Seed was collected in the summer of 1989 from the plants on site before
the archeological dig was initiated.
Plug plants were grown at the California Conservation
Corps (CCC) Napa nursery and outplanted in February 1990 by the CCC. plants were monitored by an undescribed photo monitoring technique.
Outplanted plants also were
counted and mapped. Initial costs for the project were: (1) salary $800.00; (2) travel $400.00; and, (3) plants $200.00, for a total of $1400.00. _¢,/_dgL_,_: Final mitigation T/r/r June 14, 1991
Project Success: Project on-going. _I_¢,_:
not yet available.
(Compact Cobweb Thistle):
State listed; Federal Candidate C2; CNPS List lB. l_,J,sp..Q.adg_:Mr. Gary Ruggerone, California Department of Transportation, San Luis Obispo. Proiect Name and Description:
California Department of Transportation
projects, "Little Pico Bridge Replacement"
is involved in two
and "Piedras Blancas Shoulder Widening."
former is on-going, and the latter was conducted in 1986. Both projects are along Highway 1 in San Luis Obispo County on ocean bluffs. Cirsium occidentale var. compc_ctum is found along the disturbed highway shoulders. _0.g_:
Yes. However, neither project included CEQA permit conditions
regarding transplantation of Cirsium occidentale van compactum, although California Department
consulted with the USFWS.
Transplantation and reseeding of the disturbed areas with Circium
occidentale var. compactum to maintain populations. Project Methods:
Plants of various ages were removed from the impact area and were
transplanted to immediately adjacent areas in January and February (1987?). Seed was conected in July through October (1986?), scarified, and scattered in January and February (1987?). Both sites are monitored several times per year until it can be detemained whether a reproducing population has been established. Neither site has received long-'term protection, although the areas are considered by Caltrans as "environmental
areas." Costs of the projects have been absorbed in the overhead. No reports other than brief field notes of the transplantation Final mitigation T/fir .lune14,1991
Criteria for Success: Success was defined as survival of transplants and germination of seed for reintroduction to establish a continued presence of Cirsium occidentale vat. compactum in the area. Project Success:
For Piedras Blancas, there was only partial success. Transplanting
total failure, but the respondent reported some success with reseeding.
For Little Pico, the
transplantation was a failure. Seeding has not yet been initiated. Date Project Initia_ecl: 1986.
Croton wlgginsii 0Niggin's Croton):
State rare; Federal Candidate C3C;
CNPS List 2. Resoonden_:
Mr. Gerald Hillier, U.S. Bureau of Land Management,
Proiect Name and Description:
None. Project involved the construction of a new campsite
("Gecko") at the Imperial Sand Dunes, immediately south of Highway 78 (Imperial County). _Jil_:
Project Obiectives: Objectives were to establish seedings of Croton wigginsii in an adjacent Wilderness Study Area (WSA)I Proiect Methods: Seedlings were dug with a shovel of sand, and then placed in a bucket of wet sand. The buckets were transported approximately
1 mile away to a WSA site on the
north side of Highway 78. A slice with a shovel was made in the new substrate, and the seedlings were transplanted in approximately
5 per group. About 12 groups were
established. The seedlings were visited approximately monitor the success of the transplantation.
every three days for two weeks to
During that two-week period, all the seedlings
died. 121_I/_%_LSa_¢,_: FinaI'mitigadonT/r/r June 14, 1991
Not clearly stated. Respondent suggesied that the criterion was
successful establishment Project Success:
considered that the project was successful because it
established whether transplantation of C. wigginsii seedlings would be a viable option. However, as stated above, none of the seedlings survived and therefore, it should not be considered
successful from a biological viewpoint.
Date Project Initiated:
(Santa Ana River Woollystar):
CNPS List lB.
o_¢,_29_.0.dg_: Mr. Craig Martz, Associate Environmental Planner, California Department of Transportation,
and data obtained from EPP f'des.
Project Name and Description: "Santa Aria River Woollystar Relocation Project." California Depa_tu_ent of Transportation (Caltrans) attempted to change State Route 30 in San Bemadlno County. The project included freeway construction along State Route 30, and a second phase of construction between Interstate 10 in Redlands and Fifth Street in the City of San Bemadino. approximately
Grading in the second phase would have resulted in the loss of
1.24 acres of alluvial scrubland, habitat for 1039 individuals of Eriastrum
densifolium ssp. sanctorum. However, the project was modified to affect only 733 individuals, with the remaining 308 individuals preserved in a designated environmental sensitive area avoided during the construction phase. The area is to be protected in perpetuity once construction is completed. _Project Objectives:
?: Yes. None stated specifically, but the overall objective appears to be the
successful establishment of transplanted individuals of Eriastrum densifolium ssp. sanctorum from along State Route 30 in the Santa Ana River Wash to three transplant receptor areas within the right-of-way. Final mitigation T/rh" June 14, 1991
Prqiect Methods: A contractor (Nativescapes) was hired to transplant 733 individuals of E. densifolium ssp. sanctorum from the west side of the Highway 30 project site to three locations on the east side of the highway; during January through March 1988. Plants were removed with a Vermeer TS-20 tree spade mounted on a Bobcat tractor. Plants were then fitted into burlap-lined mesh baskets that conformed to the rootbaUs for transport to the recipient areas. Indiyiduals were planted in rows within each of the three transplant areas. Each row as initially marked with a wooden stake that was labeled with the number of individuals in the row. However, this labeling method was deemed inadequate in the second year of monitoring.
Transplants were then marked individually with aluminum
tags. Monitoring of the transplants is to be conducted for three years following the transplantation. Criteria for Success: None stated explicitly. Project Success: Respondent
felt that the project had not achieved the level of success that
was hoped for, in part because of the current drought conditions.
After the first year of
monitoring, Transplant Area 1 suffered a 39% mortality, Transplant Area 2 suffered a 56% mortality, and Transplant Area 3 suffered a 48% mortality of transplants.
Most of the
mortality in the first year was attributed to transplant shock, although natural mortality and competition may also be responsible in part (Martz 1990). The first year monitoring report suggests that the transplantation
project was "highly successful thus far" because of
relatively high survivability (61%, 44%, and 52% in Areas 1, 2, and 3, respectively), good seedling production
Results of the May 1990 monitoring (Martz 1990) indicate a survival rate of 46.7% in Transplant Area 1, 38.9% in Transplant Area 2, and 40.5% in Transplant Area 3. The overall survival for the three areas was 332 individuals (44.2%). Approximately percent of the surviving individuals
were considered to be in obvious decline. Final mitigation T/#t June14,1991
however, 31 individuals (9.3%)
Seedling recruitment in the three Transplant Areas numbered 783, 80, and 339, respectively. Martz figured that seedling production in the three areas totalled 3.6 seedlings per Transplant Area 1, 3.3 seedlings per Transplant Area 2, and 5.7 seedlings per Transplant Area 3. However he also suggested that native Eriastrum plants already existing in Areas 2 and 3 may have contributed to these totals. Date Proieet Initiated: January 1988.
(Barstow Woolly Sunfower):
Not State listed;
Federal Candidate C2; CNPS List lB. Respondent:
Mr. James Brownell, California Energy Commission,
Project Name and Description:
"Luz SEGS VII." The project invo!ved the construction in
1988 of a solar power plant by the California Energy Commission, at Kramer Junction in San Bernardino County (Mojave Desert). Luz Engineering, the company that was contracted to construct the power plant, attempted to salvage the plant by collecting seed, topsoil, and additional subsoil material, and by depositing these on the receptor site. The original occurrence
of more than 1700 individuals of Eriophyllum mohavense
on less than 2 acres represented the western-most location of the species, which is one of the main reasons for attempts to preserve this site. The site is also unusual because population densities are much higher here than in other regions where Eriophyllum mohavense is found. Also, a soil investigation
was conducted by ERT (1988a; Fort
Collins, Colorado) to determine whether the distribution of Eriophyllum mohavense (and the Mojave spineflower [Chorizanthe spinosa]) is controlled by edaphic factors. The report established that there are distinct differences between the soils on the low knolls that support Eriophyllum mohavense and adjacent areas that do not. The rare plants apparently grow on areas with a near surface layer (Bm hattie horizon) and an underlying "pan" layer (the lower portion of the natric horizon, the Btkn horizon) that are both highly alkaline. Final mitigationTklr June 14, 1991
These layers apparently restrict rooting and establishment by spiny saltbush and other common shrubs of the area, but are not restrictive to Eriophyllum mohavense that roots above the pan (ERT 1988a). ERT also found very high levels of boron in the soil. This information was used in selection of the receptor site of Eriophyllum mohavense: Mitigation-Related?:
Pro iect Objectives: The state objective was to re-establish a population of Eriophyllum mohavense on a nearby artificially constructed hill. The original location of Eriophyllum mohavense was destroyed by the construction of the solar power plant. Project Method_: According
to the biological resources mitigation implementation
(ERT 1988b), the consulting botanist worked with Mr. Mark Bagiey of Bishop, California, to collect surface material (seed, litter, and the top 0.5 inch of topso!l) within a delineated area at the impacted site. This was done to be done with fiat-bottomed shovels and other hand tools. The collected material was to be stored temporarily by spreading it on plastic sheets near the relocation 'site. About 25 percent of the seed source material was to be used to provide supplemental seed to areas of known habitat for Eriophyllum mohavense. Soil was salvaged in three steps after seed collection.
The base material was to be
applied to the existing surface at the relocation site to increase the southerly aspect of the site to an approximately
4 percent slope. Following application of the base material, more
soil was to be placed on the relocation site, spread, and contoured.
In the last stage, the
seed source was to be applied and raked smooth. The site was to be misted with water to moisten the seed material and help bind it to aid in erosion control. Finally, the relocation sitewas fenced by the Luz Engineering
Corporation to prohibit future disturbance (ERT
No specific success criteria were established. Respondent reported
that the general criteria was to find the species on the relocation site. Proiect Success: Final mitigation T## June14,1991
Respondents claims that at the present time, due to the unusually dry
years since this project has occurred, no systematic monitoring has been conducted and no plants have been found. However, they claim that the success is "uncertain" until the desert receives normal rainfall. _:
(San Diego Button Celery):
endangered; Federal Candidate C1; CNPS List lB. _:
Drs. C.H. Black and Paul Zedler, Dept. Biology, San Diego State
University. Pro iect Name and Description:
"Caitrans Del Mar Mesa Vernal Pools" and "U.S. Navy
North Miramar Project Mitigation."
Transportation (Caltrans) had two major projects on Kearny Mesa that eliminated vernal pools. The first project was mitigated by the purchase of 26 acres of prime vernal pool habitat on Del Mar Mesa and a second acquisition of an additional 52 acres at Del Mar • Mesa. This second acquisition was to be used in an experiment to create artificial pools capable of supporting Eryngium aristulatum var. parishii and Pogogyne abramsii (Zedler and Black 1988). Respondents did not explain the Mirimar Project. (see IV.A.29 for additional information). _tl_l:]_: _:
Yes. For both projects, the objective was to create vernal pool habitat for
Eryngium aristulatum var. parishii and Pogogyne abramsii. _:
A set of 40 artificial basins was excavated in December 1986, and 387
were inoculated with material collected from the natural pools on Del Mar Mesa. _:
Respondents did not specifically designate criteria for success.
Proiect Success: Respondents
feel that the projects are "not yet" successful because the
rare species have not attained population densities found in the natural pools. Final mitigat_un Th'h" June14,1991
Date Proiect Initiated:
caDitatum var. angustatum
(Contra Costa Wallflower):
endangered; Federally endangered; CNPS List lB. Respondent: Ms. Joy Albertson, U.S. Fish and Wildlife Service, San Francisco Bay National Wildlife Refuge Complex. Proiect Name and Descrintion: "Vaca Dixon-Contra Costa 230-kV Reconductoring Project: Habitat Protection and Enhancement for Antioch Dunes." Pacific Gas and Elecwic Company (PG&E) reconductored the San Joaquin River crossing of the Vaca DixonContra Costa 230 kV transmission line in the fall of 1988. The project took place specifically on the Sardis Unit of the Antioch Dunes National Wildlife Refuge (ADNWR), east of the town of Antioch. USFWS personnel conducted a Section 7 consultation with PG&E before granting access permit. (see IV.A.25 for more details.) Mitigation Related?: Yes: Project Objectives:
Objectives were: (1) protection of habitat from future damage caused by
construction/repair activities; (2) transplantation of sensitive species from the access corridor to allow vehicle access to the tower;, (3) establishment of new subpopulations
of existing populations; and, (5) determination of whether direct Seeding or of nursery liners is preferable transplantation
Eighteen wallflowers from the PG&E east parcel access corridor were
transplanted either to other locations on the parcel or to the Sardis Pit area. A small circular area was Fast cleared of all vegetation, then an appropriate sized hole was dug. A plant was placed in the hole and d_ was packed fh'mly around it. Nursery grown plants were planted in a similar manner in pre-selected Three hundred seventy-seven Final mitigation Tk/r June 14, 1991
sites on the PG&E and Sardis Pit parcels.
(377) wallflower seedlings were planted in January 2 8
1990. A survey the following March provided a count of 364 surviving seedlings (96.6%) survival.
Plants were monitored during the first spring and summer to determine whether
additional water or weeding was needed so as to assure adequate survival. A final evaluation of survival will be made in the spring of the second year. Cost of the nursery-grown seedlings was estimated at $0.30/seediing; 377 seedlings produced; therefore it cost $113.10. Criteria for Success: The replacement
of the plants that were destroyed by the construction,
specifically 230 E. capitatum var. angustatum seedlings and 160 O. deltoides ssp. howellii seedlings was the criterion. Pr_ect
Success: Respondent felt that the project was partially successful.
of the wall flowers resulted in aa final 6 I. 1% survival rate for 18 of the 22 plants, and 0.0% survival of the additional four (4) individuals.
However, germination was high and
survival of outplanted seedlings was 96.6% in the first year. Date Project Initiated: April 5, 1989, for transplantation ofE. capitatum vat. angustatum individuals;
January 1990 for seedling outplanting.
State endangered; Federal
Candidate C1; CNPS List lB. 1) Respondent: Recreation,
Ms. Frederica Bowcutt, State of California Department
of Parks &
Project Name and Description: None. Project involved the reintroduction of Erysimum menziesii and Chorizanthe howellii to archeological sites at MacKerricher State Park (Mendocino County) after an archeological
dig. University of California, Davis, initiated
an archeological dig in 1989-90 at sites Containing rare species. (see IV.A.6 for more details.) Miti_,ation-Related?: Yes. FinalmitigationT/r# lurte 14, 1991
Project Ob_iectives: None stated. Project Method_: Seed was collected in the summer of 1989 from the plants on site before the archeological dig was initiated.
Plug plants were grown at the California Conservation
Corps (CCC) Napa nursery and outplanted in February 1990 by the CCC. Plants were monitored by an undescribed photo monitoring technique.
Outplanted plants also were
counted and mapped. Initial costs for the project were: (1) salary $800.00; (2) travel $400.00; and, (3) plants $200.00, for a total of $1400.00. Criteria for Success: Project Success:
Date Project Initiated:
2) Respondent: Recreation,
not yet available.
Ms. Frederica Bowcutt, State of California Department
of Parks &
and data obtained from EPP files.
Proiect Name and Description:
"Spanish Bay." Project involved the reintroduction
Erysimum menziesii, Lupinus tidestromii vat. tidestromii, and Gilia tenuiflora ssp. arenaria to the dunes surrounding the Links at Spanish Bay (Monterey County). (see IV.A.15 and IV.A.22 for more details.) b'lifigation-Related?: Yes. Project Objectives:
To increase the numbers of the three rare plant species and either
enhance existing populations or create new stands. Project Methods: Seed was collected from a population at Asilomar and propagated at Spanish Bay Nursery.
Outplanting of seedlings was to occur during the winter rainy
season. The populations were to be fenced and signed, and a boardwalk constructed to route foot traffic past the outplantings.
Regular maintenance is to include weeding of
invasive species. Criteria for Success: Final mitigation T/r/r June14,1991
of 80% for the total outp!anted seedlings in the first
year, and a total of 70% of the plants within each distinct outplanting site. Should survivorship fall below these standards, replanting would be required to occur during the next rainy season. Project Success: Respondent reports that the project appears successful, although no information held in the EPP fries confirmed this. Date Project Initiated: 1987.
3) Respondent: Dr. John Sawyer, Department of Biology, Humbolt State University, Arcata. Pro!cot Name and Description:
None. Project involved a three-year research project to
study the biology ofErysimum
menziesii and mitigation techniques. The research was
supported by a timber company to mitigate the impacts of their harvest operation. Mitigation-Related?:
Stated objectives were to determined a viable population size and ways
of habitat restoration to achieve a viable population size. Pro_iect Methods:
The current research project has not included any transplantation,
• relocation or reintroduction
at this date. However, 30 permanent plots in existing
populations are monitored quarterly, and have been so for the last two and one-half years. Project costs were given at $650,000.00. Criteria for Success:
Criterion was stated somewhat vaguely as when the existing
population exceeds in size that projected by computer modeling. Proiect Success: Project was still in progress at the time of the questionnaire. Date Project Initiated:
1988 is the date given for the beginning of the project, although seed
in April of 1989.
F'mal mitigation T/r/r lune14,1991
teret(fol_t4ra (Santa Cruz Wallflower):
Federal Candidate C1; CNPS List lB. Respondent:
None. Data obtained from'EPP files.
Pro iect Name and Description: "Revegetation of the Olympia Quarry." The revegetation is to be done in compliance with conditions stipulated in a mining permit administered by Santa Cruz County. The Olympia Quarry is operated by Lone Star Industries, Inc., and is located west of Scotts Valley. The quarry site is approximately 200 acres, the majority of which has been mined for coarse sand for construction. The adjacent vegetation is considered biologically significant because it is a xeric environment of sand hills in the midst of more mesic vegetation.
Some of the rare elements
on the quarry site include rare disjuncts or unusual flower color m0rphs. Mitigation-Relat_?:
Pro iect Objectives: The goal of the revegetation is to establish the Santa Cruz wallflower on the mined slopes and benches of the Olympia Quarry. In addition, a revegetation plan will attempt to recreate the native plant associations on the previously mined areas. Project Methods: Larry Seeman and Associates, Inc. (LSA 1989) proposes to collected 50% of all the seed produced by a group of 300 plants growing in the eastern section of the quarry. The planting areas are composed of 15-ft wide benches at 60-ft intervals along a 1.5:1 slope. The seeding regime is to replicate the density of the Erysimum teretifolium in undisturbed
Criteria for Success: Criteria will be developed by quantitatively sampling the vegetation in areas with Erysimum teretifolium. Project Success: Project is not yet implemented. Information not yet available. Date Proiect Inidoted: Revegetation Plan initially submitted by LSA Associates, Inc. in July 1987 (LSA 1987, 1989). The project has not yet begun, however.
Final mitigation T/r/r June 14,1991
State threatened; Federal
Candidate C1; CNPS List lB. Respondent: Ms. Frederica Bowcutt, S_te of California Department of Parks & Recreation, Sacramento, and data obtained from EPP files. Pro iect Name and Descdplion:
"Spanish Bay." Project involved the reintroduction of
Erysimum menziesii, Lupinus tidestromii var. tidestromii, and Gilia tenuiflora ssp. arenaria to the dunes surrounding the Links at Spanish Bay (Monterey County). (see IV.A.12(2) and IV.A.22 for more details.) Mitigation-Related?: Yes. Project Objectives: To increase the numbers of the three rare plant species and either enhance existing populations
or create new stands.
Proieet Methods: Seed was collected from a population at Asilomar and propagated at Spanish Bay Nursery.
Seeds of sand gilia need stratification and scarification with
differing daylength and t_mpemture regimes.
Outplanting of seedlings was scheduled to
occur during the winter rainy season. The populations were to be fenced and signed, and a boardwalk constructed
to route foot traffic past the outplantings.
to include weeding of invasive species. Criteria for Success:
S_-'vivorship of 80% for the total outplanted seedlings in the first
year, and a total of 70% of the plants within each distinct outplanting site. Survivorship was to be compared in outplanting sites with existing populations in an attempt to account for annual fluctuations that may be environmentally below these standards, replanting Pro_iect Success:
Should survivorship fall
would be required to occur during the next rainy season.
Respondent reports that the project appears successful, although no
information in the EPP files confirmed this. Date Project Initiated:
Final mitigation Tbh" June14,1991
(Gaviota Tarplant): State
endangered; Federal Candidate C1; CNPS Lisi lB. Resnondent: Mr. John Storrer, Storrer & Semonsen Environmental Services, Santa Barbara. Proiect Name and Description: California."
"Gaviota Interim Marine Terminal, Santa Barbara County,
Mitigation was required for the construction of a secondary access road to the
marine terminal. Mitigation-Related?:
Project Obi_¢_ves: The stated objective was the establishment of 5,800 ft 2 of Hemizonia increscens villosa habitat. Proieet Methods: The impacted site was surveyed for Hemizonia increscens ssp. villosa and it was determined that approximately
50 individuals lay within the access road
alignment. There are considerably more individuals found adjacent to the area (approximately
Seed was obtained from plants collected from the
tank farm area prior to construction. An additional 2-3 inches of topsoil was retrieved before grading. More topsoil (3 inches) also was removed from the access road alignment during grading. The receptor site is on California Depmtment of Parks and Recreation property east of the Texaco Interim Marine Terminal.
No further site preparation was
attempted prior to broadcasting of seed. The receptor site was fenced with three strands of barbless wire to delineate boundaries, Additional (approximately)
and the project was signed.
50 tarplant seedlings were discovered during an
inspection of the site in March 1989. Adjacent weedy vegetation was clipped within a 6 inch radius of many of the plants to decrease competition. _/[_,2_[9L,_]£_:
Performance criteria included: (1) no evidence of soil erosion; and,
(2) presence of a viable H. increscens ssp. villosa population. The latter was determined by comparing the density of flowering plants during the peak growing period with that of Final mitigationT#/r June 14, 1991
Project Success: An intensive survey was conducted on May 24, 1989, that recorded 136 flowering tarplants, with an additional nine plants that had died or seeded. The Fast year densitites of 1.2, 2.69 and 1.28 individuals
per m2 recorded were favorable in comparison
with the Chevron restoration site. The project is on-going; however, that the first year's results were promising.
the respondent felt
More information is not yet available.
(Santa Susana Tarplant): State rare; Federal
Candidate C2; CNPS List lB. 1) Respondent:
None. Data obtained from EPP files.
Project Name and Description: "Santa Susana Tarplant (HemizoniaminthorniO
Program 2." Las Virgenes Municipal Water District built a new water reservoir adjacent to its existing reservoir in the Twin Lakes area near Chatsworth. Mitigation for this project involved the salvaging of'Hemizonia minthornii plants, and transplanting the salvaged plants and some nursery plants grown from seed on the 250 m2 cut slopes surrounding the new reservoir. Mitigation-Related?: Project Objectives:
Yes. The overall project objective was to establish a new population of Santa
Susana tarplants on the cut slopes surrounding Project Methods: construction.
the new water reservoir.
The project site boundaries were staked prior to the initiation of the
Seeds were collected in the summer of 1988 at a time considered by the
consultants as not phenologically optimum for Success -- i.e., while the plants were in full bloom. Individual plants were located in either rock crevices or on thin soil in open areas. A pick mattock was used to break up the sandstone crevices to remove the top portion of the root, but the root was very deeply embedded in the substrate and could not be removed without breaking. Final mitigation T/rkr JuneI4,1991
Potting mix was brought to the site and mixed with clean sand and soil from the site. Each transplanted plant was trimmed with clippers to compensate for the loss of the root system, and then potted. Each transplant was watered several times before transportation
to Tree of Life Nursery.
Cuttings were taken from the transplants and
retained for their inflorescences and to attempt root cuttings. A total of 55 plants were potted, representing
70% of the mature plants within the impacted area.
Approximately 50% survived the initial transplantation operation; however, cutting survival and seed germination were poor (McClelland Consultants (West), Inc. 1988). None of the initial seed sown germinated (McClelland Consultants (West), Inc. 1988). A second collection of seed made in October 1988 was germinated at Tree of Life Nursery to compensate
for the losses.
As of February 1989, however, only 8 of the 55 transplants have survived.
1990, the site was visited and monitored only 4 times, as the plants appeared to show signs of naturalizing to th'e cut slope. Criteria for Success: Performance
criteria included the following: (1) 15 surviving mature
plants from the transplants by May 1989; •(2)50 seedlings by May 1989; (3) 10 mature plants flowering by October 1989; (4) 30 mature plants by October 1990; (5) 100 seedlings by October 1990; (6) 50 mature plants by October 1991; (7) 70 mature plants with ground coverage of about 25 m2 by October 1992 (McCleliand Consultants (West) 1988). _:
The project success has not been evaluated only because the project
technically is still on-going. However, the survival of 8 of the 55 transplants, only 7 of which are doing well, is rather poor (McClelland Consultants (West) 19908). The project has been rather controversial (see article in the Los Angeles Times, February 3, 1989, p. 3, 14). Date Project Initiated: July 1988 for the initial collection of seed and excavation of plants in the impacted area; January 1989 for the transplantation Final mitigation Tkk June 14, 1991
of salvaged plants.
None. Data obtained from EPP f'ties.
Pro_iect Name and Description:
"Woolsey Canyon Development."
proposed in 1989 to construct an extensive residential community in Woolsey Canyon, western Los Angeles County. The project site is located in a sensitive ecological areas as designated by Los Angeles County. An environmental assessment performed by Michael Brandman & Associates (November 1988) identified that the proposed project would result in the direct loss of approximately 57 individuals of Hemizonia minthornii, in a population of approximately
Miti_,ation-Related?: Yes. • Pro_iectObi¢¢fives: The primary objective of the mitigation plan will be: (1) to establish on the development site, a second population of Hemizonia minthornii, using propagules derived from individuals in the original population that is impacted by the development. The new population should be capable of natural regeneration over the long term; (2) offset of the loss of approximate!y 57 individuals of Hemizonii minthornii with the introduction of approximately
150 individuals as a founder group in a new population; and, (3) advance
the state of knowledge of Hemizonii minthornii by carrying out appropriate research-related activities in conjunction with mitigation activities (Mistretta 1989). Pr_ect Methods: The plants occur within a single population on a sandstone outcrop on the project site. The original development plan was designed to include 90 individuals in a reserve that would be bordered by the development. CDFG, the reserve site was reconfigured
However, after consultation
to be continuous with an adjacent natural area on
the southern boundary of the project, rather than being an island within the development (Mistretta 1989). The Rancho Santa Aria Botanic Garden (RSABG) has been retained by the Chateau Group to advise on the horticultural and research-related Final mifiga_on T/r/r June 14, 1991
aspects of the program.
Data to be
gathered are: (1) number of individuals on site; (2) soil analyses; (3) population statistics; (4) reproductive capacity; (5) genetic composition; and, (6) floristic composition of the community. The proposed revegetation program indicates that prior to the commencement construction,
the preserve site will be fenced and left undisturbed.
Susana tarplants will have the infructescences
removed by hand at the appropriate
Additional seed collection will be done if deemed necessary.
Collected seed will be cleaned
and dried prior to storage. Half the collected seed will be sown in the preserve after the transplantation of salvaged individuals (see below). The remaining half will be propagated at RSABG for seedling transplantation. In addition, the mature plants in the impacted area will be salvaged by digging with a shovel and pick mattock to a depth of 1 ft. Plants will be placed in planters for temporary off-site storage. Plants will be trimmed and watered 3 times during the f'trst week and weekly thereafter until transplanted. Transplant receptor sites within the preserve will be selected by a botanist/horticulturalist.
Plants will be planted without mulch or fertilizers, and watered
weekly for 4 weeks. The project site will be checked monthly by the botanist/horticulturalist'for
an undetermined period.
(Santa Cruz Tarplant):
State endangered; Federal
Candidate C1; CNPS List lB. 1) Respondent:
None. Data obtalned from EPP files.
Project Name and Description:
"Hilltop Commons Development."
The Nylen Company,
Inc., developed an apartment complex in Pinole, Contra Costa County. Dr. Nell Havlik, then of the East Bay Regional Park District, agreed to perform a salvage of the mature Final mitigationT## June 14, 1991
individuals ofHolocarpha macradenia from the project site and transplant them to a nearby park within the East Bay Regional Park District. Mitigation-Related?:
None specifically stated, but the project was designed to salvage the
mature plants of Holocarpha macradenia from a housing development site in Pinole, and subsequently establish a new population of H. macradenia at Wildcat Canyon Regional Park. Project Methods: Pallets of soil, 4 ft2 by 1 ft deep, containing Holocarpha macradenia plants were dug and seed was collected from these plants. Seed from the salvage was taken by Dr. Havlik and spread as an enlargement of several existing populations in Wildcat Canyon Park (Havlik's Stand Nos. 2, 11, 12, 13, 14, 15; [CNDDB Occ. Nos. 2, 29, 31 for the first three locations]).
Seed also was spread at a site in Sather Canyon on the
east side of San Pablo Rese_oir. Criteria for Success: Project Success:
Havlik monitored 21 populations,
7 of which were new populations,
reported an increase of 30% of the individuals from 1985 to 198610. Date Project Initiated:
State endangered; Federal
Candidate C2; CNPS List 1Bn. 1) Respondent:
Mr. Charlie Patterson, Plant Ecologist, private consultant, E1 Cerrito, and
10See letter to Ms. Susan Cochrane, [formerly] Endangered Plant Coordinator, from Dr. N. Havlik, [formerly of the] East Bay Regional Park District, dated March 9, 1987. nMr. Ken Milam, Sonoma County Planning Director, returned a questionnaire for Lasthenia burkei, but the information provided was so vague as to be useless for this analysis. Therefore, the questionnaire is not included. Final mitigation T /r/r June 14, 1991
data obtained from EPP files. Project Name and Description: "Airport Boulevard Business Park." A business park was constructed in 1984, located just northeast of the Sonoma County Airport. MilSg_ion-Related?: Pro!ect Objectives: replacement
Yes. The stated objective for the mitigation for the business park was the
of 0.3 acres of wetlands and pre-existing 5000 individuals ofLasthenia
with, at minimum, Project Methods:
10,000 individuals. Seed was collected in 1984. Small pools were created by hand, clearing
vegetation and topsoil in low swales within an 100 ft easement. during the winter of 1985-1986.
These pools were seeded
However, much of the easement was disturbed by the
installation of a large storm drain before the seeding trials could beassessed. new larger pools were created later by a bulldozer-mounted
blade during the fall of 1986,
and seeded that year. Criteria for Success: Essdndally the replacement of a self-sustaining colony of Lasthenia burkei was the criterion for success. Project Success: Respondent
felt that the project was successful.
The mitigated seeded
population increased from no Lasthenia burkei to >6000 individuals in three years. However, due to additional complications, the pools were "re-worked" (i.e., enlarged, recontoured and re-seeded).
The current year's results show in excess of 10,000
Mr. Charlie Patterson, Plant Ecologist, private consultant, E1 Cerrito, and
data obtained from EPP files. Pro_iect Name and Description:
"Sonoma County Airport".
This project involved the
contruction of a new, paved apron at the Sonoma County Airport in 1986. Mitigation-Related?: Yes. Final mitigation Th'/r June 14, 1991
Project Ob_iectives: Objectives stated by the respondent for the airport expansion project was the replacement of the colony of Lasthenia burkei lost during construction. Pro_iectMethods: Eleven small artificial pools were created by shovel and hoe in a broad, nearly level portion of the infield between the north end of Runway 14 and Taxiway Y. Pools were made by selecting a low spot and then scraping 1 to 6 inches of the surface. The scraped soil was piled into small berms around the downslope edges of the pools. Pools were seeded the day of construction. Seed was sown both as seed collected in 1985 and from other existing populations 0.5 miles away, and by spreading the scraped topsoil from nearby colonies.
then left alone for most of the winter and spring. Pools were monitored, which involved checking them for water collection and holding capacity, Lasthenia burkei germination, phenology,
(_'iteria for S_ccess: Essentially the replacement of a self-sustaining colony of Lasthenia burkei was the criterion for success. Proiect Success:
Respondent felt that the project was successful.
Seeded areas of existing
ditches now support several thousand individuals of Lasthenia burkei, and another several thousand are growing in the constructed pools.
Carl Wilcox, California Department
data obtained from EPP files.None. Pro!ect Name allglDescription:
of Fish and Game, YountviUe, and
Data obtained from EPP files.
"Santa Rosa Rare Plants Mitigation Plan San Miguel
Estates 1." In 1989 Cobblestone Development
Corporation proposed the development
San Miguel Rancho Subdivision (RSM) at 2001 Waltzer Road within the city of Santa Rosa, Sonoma County and San Miguel Estates No. 2 (SME) at 2192 Francisco Avenue, also within Santa Rosa. The SME project is an on-going housing construction and the RSM housing project was a 1989 development. Final mitigation T/r/r June 14, 1991
The projects would destroy approximately
2.51 acres of vernai pool habitat. (see IV.A.2(2) for more details.) Mitigation-Related?: Yes. Proieet Obieetives: According to the Mitigation Agreement between Cobblestone and i
CDFG, the mitigation should establish self-sustaining populations of plants in approximately 2.97 acres of newly created habitat on the mitigation site. Serf-sustaining is def'med as approximately 13,000 individuals of Lasthenia burkei and 137,000 individuals of Blennosperma bakeri for 2 consecutive years without supplemental seeding. Project Methods: The mitigation plan was devised by R. Osterling, Inc. (1989). The plan proposed to transplant all existing plants and/or seeds to a 20-acre receptor site located approximately 1.5 miles west of the San Miguel Estates property, with existing 3.49 acres of vernal pool resources.
2.5 acres of vernal pool habitat will be
constructed at the receptor site with pool configuration and depth based on survey of existing pools. Grading will be done with small equipment under supervision of a qualified botanist (Charli_ Patterson, private consultant). Plant material will be "transferred."
Seed will be collected from donor pools and the top 1-2 inches of pool
bottom duff will be excavated and spread in the excavated pools at the receptor site. Monitoring
will continue through June 1991.
Criteria for Success: None explicitly stated. Project Success: Respondent indicated that although it was too early to tell because the projects are only in their first year, "[e]arly indications are that they will be the most successful relocations yet achieved in the Santa Rosa Area." Date Project Initiated: March 1989.
Proieet Name and Description: "County of Sonoma Public Service Area 31 Waste Water Storage Pond." The project involved the creation ofa wastewater storage pond in 1988 on Final mitigation T/r# June 14, 1991
approximately 3.7 acres of northern vernal pool, seasonal marsh and intermittent stream habitat (and 10 acres of non-native grassland). Lasthenia burkei was transplanted to an area known as "The Wildflower Preserve'; on the Sonoma County Airport. The receptor site is already protected as part of the Sonoma County Airport mitigation. Miti_,ation-Related?: Yes. proiect Ob_iectives:The project objective was to create 4.4 acres of seasonal wetland habitat and to provide a transplantation site for Lasthenia burkei. pro lect Methods: Seed was collected from plants at the impacted site. Plans in bloom were salvaged, kept in containers until seeded and seed subsequently was collected to be sown at the mitigation site. Topsoil was salvaged from around the plants to spread at the new sites. The number of individuals are to be counted for each of five years. Criteria for Success: Criteria have not been established. Pro_iect Success:
"Although the criteria have not been established, we.feel that, for at least
the fh:st year of monitoring, the transplantation was somewhat successful .... long term viability of the population
is still questionable."
were observed at the mitigation site, while only 150 plants were found at the impacted site. Date Pro iect Initiated:
(Mason's Lilaeopsis): State rare; Federal Candidate C2;
CNPS List lB. 1) Respondent:
Mr. Niall McCarten, Depru'tment of Integrative Biology, University of
California, Berkeley, and Department (questionnaire
of Water Resources (DWR), Sacramento
Project Name and Description: "California Deprutment of Water Resources (DWR) Barker Slough Bank Revetment." Final mitigation T#lr June 14, 1991
The project was initiated in 1989 by DWR for levee bank 4 3
protection on private property. Individuals ofLilaeopsis masonii were transplanted from the east side of the slough to the west side. Mitigation-Related?: Yes. Project Obiectives: Project objectives were the removal ofLUaeopsis mason(i from the proposed rip-rap site and the transplantation
of individuals to suitable habitat.
Proiect Methods: Populations ofLUaeopsis masonii were removed with a shovel, placed in shallow water in plastic containers and then placed in a boat and transported to the potential habitat (receptor site). After placing the transplant into the new site, the surrounding substrate was pressed along the edges to homogenize
Eighteen (18) 50 x 50 cm permanent plots were established, and marked with numbered, color-coded
metal stakes (ECOS, Inc. 1988). Control populations were marked
similarly. All plants were to be counted in each plot five times during the first two years following transplantation,
and three times per year for the following three years.
The receptor site initially was not protected, but due to the biological values of the site, it was purchased by CDFG as a preserve in January 1990. Criteria for Success:
Specific criterion was the survival of 80% or better of the individuals
transplanted over a 5-year monitoring period. Project Success:
Unknown, as the project is on-going. One year of raw data is available
from Mr. David Brown, DWR. DWR respondent claims that it is too early to make a determination
as to whether the project is successful.
Date Project Initiated:
2) Respondent: Recreation,
Ms. Frederica Bowcutt, State of California Depmmaent of Parks &
Proiect Name and Description:
None. Project is being considered; may involve the
transplantation ofLilaeopsis masonii at Brannan Island State Recreational Area near Rio Final mitigation T/fir June 14, 1991
Vista (Contra Costa County). Mitigation-Related?:
Proiect Objectives: Project Methods:
Project still being planned. None stated. Project still being planned.
Criteria for Success:
Project still being planned.
pr_ect Success: Project still being planned. Not applicable. Date Proiect Initiated:
Not yet initiated.
(Milo Baker's Lupine):
State threatened; Federal
Candidate C2; CNPS List lB. Respondent: None. Data obtained from EPP files. Project Name and Description: None. In 1985, California Depmtanent of Transportation (Caltrans) performed road maintenance
along State Highway 162 (Mendocino Pass Road)
near the city of Covelo (Mendocino County). The mitigation project was to offset the impacts of this activity. Mitigation-Related?: Pro!ect Objectives:
Yes. None stated explicitly, but the project was to establish several new
populations to offset the loss of L. milo-bakeri during highway maintenance. Pro_iectMethods: Caltrans collected seed from the CNDDB occurrence #2 forLupinus milobakeri from August through September 1985. Not more than 15% of the population's annual seed crop was collected.
Prior to seeding, the collected seed was rinsed, and the
seed beds prepared by adding topsoil from the parent population.
In October 1985,
Cahrans planted the seed in areas of suitable habitat along Highway 162 between post mile markers (PM) 31.50 and 31.61, and from PM 32.00 to 32.14, as well as planted seed in suitable habitat near the Caltrans equipment yard near Covelo. Criteria for Success: None stated.
Final mitigation T/rk June 14, 1991
Pro iect Success:
In some of the plots, there was considerable competition from annual
grasses. Caltrans annually sprays the highway edges with herbicide, and this added to the growth ofL. milo-bakeri in the seeded arias. 12_IgjlgLI_:
(Tidestrom's Lupine): State
endangered; Federal Candidate 1; CNPS List lB. Respondent: Ms. Frederica Bowcutt, State of California Department of Parks & Recreation, Sacramento, and data obtained from EPP fries. Proiect Name and Descriotion: "Spanish Bay." Project involved the reintroduction of Lupinus tidestromii var. tidestronii, Erysimum menziesii, and Gilia tenuiflora ssp. arenaria to the dunes surrounding the Links at Spanish Bay (Monterey County). (see IV.A.13(2) and IV.A. 15 for additional details) Mitigation-Related?: Yes: project Ob_iectives:To increase the numbers of the three rare plant species and either enhance existing populations or create new stands. Proiect Methods: Seed was collected from a population at Asilomar and propagated at Spanish Bay Nursery. Seeds ofLupinus
tidestromii var. tidestromii need stratification and
scarification with differing daylength and temperature regimes. Outplanting of seedlings was to occur during the winter rainy season. The populations were to be fenced and signed, and a boardwalk constructed to route foot traffic past the outplantings. Regular maintenance was to include weeding of invasive species. Monitoring will continue until 1993. Criteria for Success: Survivorship of 80% for the total outplanted seedlings in the first year, and a total of 70% of the plants within each distinct outplanting site. Should survivorship fall below these standards, replanting would be required to occur during the Final mitigationT#/r June 14, 1991
next rainy season. Project Success: Respondent reports that the project appears successful, although no information
in the EPP files confirmed this.
Di_N Pro!ect Initiated: 1987.
State endangered; Federal Candidate
C1; CNPS List lB. Respondent:
None. Data obtained from EPP files.
project Name and Description: None. The RANPAC Corporation proposed the construction of Vesting Tentative Tract No. 23267 that would impact a population of Mahonia nevinii on the 01d Vail Ranch property. Although 12 plants are found on the property, the mitigation project involved the relocation of a single plant. Mitigation-Related?: Pro_iect Obiectives: Project Methods:
Yes. None' stated explicitly. The impacted plant would undergo crown division and root cuttings.
These would be transplanted in the late fall (no more details were provided). The success of the transplantations would be monitored for three years following transplantation.
was to be collected in the summer of 1989 to be propagated in a nursery and maintained until the success of the transplantation
efforts could be adequately assessed.
Criteria for Success: Success would be based on the number of (trans)plants that grow and reproduce. Project Success: Unknown. Date Pro iect Initiated:
available in EPP files.
endangered; Federal Candidate C3; CNPS List lB. Final mitigation Th'h" June 14. 1991
None. Data obtained from EPP files.
Proiect Name and Description:
None. Mitigation was required for the California
Department of Transportation (Caitrans) construction in 1983 of an 1-15 gap closure and the construction of State Route 52 from 1-805 to Santo Road. _,_t0_l_cdJ_:
The project objective was simply to offset losses of this plant species
caused by construction
of the highway projects.
Pro!ect Methods: For the State Route 52 project, Caltrans collected a total of 55 individual M. linoides ssp. viminea plants within the impacted area, and collected green cuttings of this species for reintroduction
into suitable habitat within the project area. For the two
projects together, Caltrans collected no more than 50% of each year's seed from populations within the impacted area. Prior to broadcasting
of seed, Caitrans reviewed
existing sites to characterize the ecological parameters of the species. Criteria for Success: Project Success:
Norie stated explicitly.
Progress reports were submitted in November
1983, April 1984, June
1985, and May 1986. The 1986 report stated that from June 1985 to December approximately
389 (additional) seedlings died, from the earlier total of 509 plants. This
wastheresultof overcrowding in the nursery.
Two of the original 16 containerized salvaged plants died by Jane 1985. By December 1985, an additional eight plants had died. Findings in the 1986 report were: (1) salvaged M. linoides ssp. viminea plants required parent soil to survive; (2) plants in nursery conditions need to be aggressively pruned; (3) nursery containers must be widely spaced; (4) M. linoides ssp. viminea is easily propagated from seed and cuttings, and, (5) transplantation site in Murphy Canyon. Date Project Initiated: Final mitigafiort T/r/r June 14, 1991
would be at a suitable
_deltoides ssn. howellii
(Antioch Dunes Evening Primrose):
State endangered; Federally endangered; iENPS List lB. Respondent:
Ms. Joy Albertson, U.S. Fish and Wildlife Service, San Francisco Bay
National Wildlife Refuge Complex. Proiect Name and Description:
Costa 230-kV Reconductoring
Habitat Protection and Enhancement for Antioch Dunes." Pacific Gas and Electric Company (PG&E) reconductored
the San Joaquin River crossing of the Vaca Dixon-
Contra Costa 230 kV transmission line in the fall of 1988. The project took place specifically an the Sardis Unit of the Antioch Dunes National Wildlife Refuge (ADNWR), east of the town of Antioch.
USFWS personnel conducted a Section 7 consultation with
PG&E before granting access permit. (see IV.A.12 for more details.) Mitigation Related?: Project Objectives:
Yes. Objedtives were: (1) protection of habitat from future damage caused by
construction/repair activities; (2) transplantation of listed species from access corridor to allow vehicle access to the tower, (3) establishment
Plants from the PG&E east parcel access corridor were transplanted
either to other locations on the parcel or to the Sardis Pit area. A small circular area was first cleared of all vegetation, then an appropriately sized hole was dug. A plant was placed in the hole and soil was firmly packed around it. Nursery grown plants were planted in a similar manner in pre-selected
sites on the PG&E and Sardis Pit Parcels.
Seed germination for Oenothera deltoides ssp. howellii was poor: only 10 seedlings survived to be planted. Final mitigatiunT/r/r June 14, 1991
More seedlings were to be outplanted in December 4 9
1990. Cost of
the nursery-grown seedlings was estimated at $0.30/seedling; 377 seedlings produced; therefore it cost $113.10. Criteria for Success: The replacement of ihe plants that were destroyed by the construction, specifically 160 O. deltoides ssp. howellii seedlings and 230 E. capitatum var. angustatum seedlings was Me criterion. Pro ieet Success:
Respondent felt that the project was partially successful.
Date Project Initiated: April 5, 1989, for transplantation; January 1990 for seedling outplanting.
Federal endangered; 1) Respondent:
basilaris sso. treleasei
Cactus): State endangered;
CNPS List lB.
James Brownell, California Energy Commission,
Project Name and Description:
"Kern River Cogeneration Power Plant Project." Project
involved the construction_of a cogeneration Mitigation-Related?:
power plant along the Kern River in 1983-85.
Project Objectives: Objective of the mitigation project was to keep the cactus located at the edge of the road from being destroyed by truck traffic during construction. Project Methods: Cactus pads were collected and allowed to callus. Approximately two weeks later, the pads were taken to the transplantation site. The receptor site is within the California Living Museum (CALM) property, a non-profit, privately-run educational program.
CALM is located east of Bakersfield within the native range of Opuntia basilaris
var. treleasei. The recepior site had been weeded to remove non-native annual grasses, and soil had been loosened to allow the callus end of the pads to be placed in the soil. One hundred fifteen (115) cactus pads were positioned in nine (9) clumped in two (2) nearby areas. The receptor site was visited each year for three (3) years, and grasses were cleared at each Final mitigafiort Th'/r June 14, 1991
Success was achieved if the cactus flourished at the site.
Pro!cot Success: established
The project was considered successful, because the new plants were
wherever pads were planted.
Date Pr_ect Initiated: October 1983.
Rick York, California Energy Commission,
Sacramento, and data obtained
from EPP files. Project Name and Description:
"Sycamore Cogeneration Project."
Project involved the
mitigation of operation activities of the Sycamore Cogeneration Company.
A population of
Opuntia basilaris vat. treleasei became vulnerable to loss from eros!on on a slope that was cut prior to construction of the project. Mitigation-Related?:
Company, as part of the conditions of
certification by the California Energy Commission, agreed to protect Opuntia basilaris vat. treleasei in the main power plant area, pipeline right-of-ways, transmission line right-ofways, access roads and the fuel oil storage area. If the Bakersfidd
cactus was disturbed,
Sycamore agreed to transplant the affected stands to another area within the project vicinity in a manner similar to that described for the Kern River Cogeneration Project. Pro ieet Methods: No details are provided in the Mitigation Agreement (MA). Information in EPP files indicates that Sycamore Cogeneration morfitoring stipulation in the MA. Criteria for Success: Project Success: D_
No information was received.
Proiect Initiated: 1989.
Final mitigationT/r/r June 14, 1991
Company objected to the five-year
Orcuttla viscida (Sacramento Orcutt Grass):
State endangered; Federal
Candidate C1; CNPS List lB. Respondent:
Mr. Barry Hecht, Balance Hydrologics,
Pro!ect Name and DescrintiQrl: "Sunrise/Douglas Wetland Protection and Creation Program", Sacramento County. Project involved mitigation for two housing developments along Sunrise Boulevard, Sacramento relocation/transplantation _gJ3_/l:F_¢,l_:
County. Techniques for mitigation
The objective for both projects was to re-establish species in vernal
pools and freshwater seasonal wetlands within a 350-acre wetland preserve. Prqiect Methods:
Methods are "pending."
Criteria for $_¢cess:
Respondent reports two specific criteria:
1) Survival for 5 years in
90% of the pools and wetlands to which individuals of Orcuttia viscida are transplanted; and, 2) noticeable vigor ahd expansion of the range of Orcuttia viscida in 50% of the pools/wetlands into which individuals are transplanted. Pro iect Success:
Decision of success is "pending."
Project is "on-going;" presumably construction has not yet begun.
IV, A.28. Pentachaeta
Ivonii (Lyon's Pentachaeta):
Candidate C1; CNPS List lB. Respondent:
Mr. Carl B. Wishner, Envicom Corporation,
Pro_iect Name and Description:
"Lake Sherwood Golf Course."
The mitigation that was
prepared by Envicom Corporation involved a salvage and restoration plan for Pentachaeta lyonii at the Lake Sherwood Golf Course site in Ventura County. The planning unit (Planning Unit No. 1) consisted of a 163-acre golf course, driving range, clubhouse, 146 single-family Final mitigation T/rk June 14, 1991
lots, and 4 estate lots, ranging from 0.3 to 12.7 acres. 5 _)
pro_iectObjectives: Project objectives included: (1) maintenance of at least one site occurrence of Pentachaeta lyonii in perpetuity; (2) maintenance of at least one occurrence in an undisturbed state until the majority has flowered and seeded; (3) harvest of mature seed to establish a "germ plasm" collection at the Rancho Santa Ana Botanic Garden (RSABG), and to establish a living collection; (4) removal of top soil at impacted site for seed collection; (5) development phytosociologieal
of a five-year monitoring program; and, (6) conduction of a
study to determine habitat parameters.
Pro!ect Methods: Seed of Pentachaeta lyonii was collected by hand and by using a portable hand vacuum, yielding 7.75 grams. It was held cryogenically
by the RSABG.
site grading, a target soil removal from areas of high plant density (70 flats of soil) was •" 2 3 of soft conducted, followed by overall surface scraping and stockpll!ng of about yd ". Salvaged soil was redistributed of 0.1 acre ex situ just prior to the first major fall storm (November 1988)..A small amount of seed and three (3) flats of salvaged soil were distributed onto the preserved P. lyonii location. Prior to the extirpation of the Pentachaeta lyonii site, a grid system of 1 m squares was established using string and nails. Presence and ranked order estimates of density for each square meter were recorded. The identity or' all species present within the areal extent of P. lyonii was recorded. A random sample of 60 quadrats was investigated for species presence.
These data were subjected to an ordination analysis, along with similar data from
other sites of occurrence.
The ex situ site was similarly gridded in the spring of 1989. All
species were recorded, and each quadrat checked for Pentachaeta lyonii. _:
Respondent indicated that the plan did not specifically designate
criteria for success. Proiect S0ccess: Success in the stated context was not achieved• The respondent suggested that the plan for salvage was inadequate. Finalmitigation T/r/r June 14, 1991
Pogoevne abramsff (San Diego Mesa Mint): State endangered; Federally
CNPS List lB. Drs. C.H. Black and Paul Zedier, Dept. Biology, San Diego State
University. pr_ect Name and Description: "Caltrans Del Mar Mesa Vernal Pools" and "U.S. Navy North Miramar Project Mitigation." Transportation
California Department of
(Caltrans) bad two major projects on Kearny Mesa that eliminated vernal
pools. The first project was mitigated by the purchase of 26 acres of prime vernal pool habitat on Del Mar Mesa and a second acquisition of an additional 52 acres at Del Mar Mesa. This second acquisition was to be used in an experiment to create artificial pools capable of supporting Pogogyne abramsii and Eryngium aristulatum var. parishii (Zedler and Black 1988). Resporldents did not explain the Mirimar Project. (see IV.A.11 for additional information). Mitigation-Related?:
project Objectives: For both projects, the objective was to create vernal pool habitat for Eryngium aristulatum var. parishii and Pogogyne abramsii. Pro ieet Methods: A set of 40 artificial basins was excavated in December
1986, and 387
were inoculated with material collected from the natural poois on Del Mar Mesa. Criteria for Success: Respondents did not specifically designate criteria for success. project Success:
feel that the projects are "not yet" successful because the
rare species have not attained population densities found in the natural pools. Date Project Initiated:
Final mitigation T/r/r June 14, 1991
State endangered; Federal
Candidate C1; CNPS List lB. Respondent: John Stebbins, California State University, Fresno. Project Name and Description: "Round Mountain Flood Control Project," initiated by the Fresno County Metro Flood District. Project plans are being drafted at this time.
Yes. Pro_iect Obiecfives:
Project plans are being drafted at this time. Net yet available.
Project plans are being drafted at this time. Net yet available.
Project plans are being drafted at this time. Net yet available.
Project Success: Net yet available. _:
Presumablythe project has not yet begun.
(Feather River Stonecrop):
Not State listed;
Federal Candidate C1; CNPS List lB. Respondent:
Sharon Villa, California Department
Pro!ect Name and Descriotion:
"Feather River Canyon Storm Damage Repair." The
project involved the repair of the February 1986 storm damage to State Route 70 in Plumas County. Work included widening at three (3) spot locations where the highway was reduced to a single lane. Initially, the existing rock slopes were cut back approximately
feet to restore two traffic lanes. The roadway was later realigned away from the East Branch North Fork Feather River. Mitigation-Related?:
Yes (for a federal candidate).
Prg!ect Obiectives: The overall goal of the mitigation project was to reduce the severity of project impacts on Sedum albomarginatum.
Specific project objectives were : (1) avoid
unnecessary or inadvertent damage to the population by restricting habitat disturbance to those areas that are located within the slope lines; (2) salvage individual S. albomarginatum
Final mitigation Tkrk June 14, 1991
plants from project impact areas prior to construction,
and reintroduce these plants on
suitable slopes within the immediate area following construction;
(3) collect information on
the distribution, density, and microhabitat i_references of S. albomarginatum within the project area to guide reintroduction
efforts; and, (4) monitor the survival of re-established
plants for a period of five years to evaluate the effectiveness of transplantation as a mitigation measure of Sedum albomarginatum. Pro_iect Methods: An unspecified number of plants (up to 500 individuals) were salvaged from the impacted site, placed in a burlap bag and transferred to labeled flats. These were maintained in a lath house at the Butte College horticultural facility. The salvaged plants were renamed to the area of origin and transplanted after the new highway slopes had been constructed.
Two plantings were performed, one in Fall 1986 and the other in Spring
1987. Each plant was permanently
marked with a numbered aluminum tag wired to a steel
spike driven into the ground. Criteria for Success: _:
Nofie were developed.
One hundred Fifty eight (158) plants were outplanted in Fall 1986 and an
additional 158 were outplanted the following spring. Only 14 (8.8% survival rate) survived the fall transplant, and only three (3) individuals (1.9% survival rate) Survived the spring transplant. Date Proiect Initi_od:
Sidalcea pedata (Bird-Footed Checkerbloom):
State endangered; Federally
CNPS List lB. None. Data obtained from EPP files.
Proieci Name and Descdotion: "Sidalceapedata Transplantation Project." The project involved the construction of a store (Big Bear K-Mart) in the city of Big Bear Lake (San Bernadino county). Final mitigation T_# June 14, 1991
The mitigation involved the transplantation of eleven (11) whole 5
Project Methods: Terms of the Mitigation'Agreement Corporation stipulated that all four Sidalceapedata translocated to a protected site approximately
(MA) between CDFG and K-Mart
plants on the impacted site were to be
0.25 miles away, owned by The Nature
Conservancy. However, by the time the MA was signed, several individuals orS. pedata Were destroyed by equipment operations from an industrial contractor's yard adjacent to the K-Mart proposed site. The remaining twelve plants (10 mature and two seedlings) were transplanted by means of a Vermeer hydraulic spade during November
Site preparation included the removal of several tons of asphalt debris and light discing to reduce the compaction of the recipient area. The 0.9 acre parcel was fenced with a split rail around its entire perimeter. _:
None stated in the materials available for review.
Pro_iect Success: As of 16 May 1990, 10 of the 12 transplants survived to reproduce and one seedling transplant survived, despite two years of drought. This represents a 90% survival rate for the mature plants. T. Krantz, the contractor from Nativescapes responsible for the transplantation
effort, suggests that the project was at least initially
successful. Date Project Initiated:
and Rare Plant Species Involved Relocation
(Large-Flowered Fiddleneck): State endangered;
Federally endangered, CNPS List lB. Respondent: Mr. Kevin Shea, East Bay Regional Parks District (EBRPD), Oakland, and
Final mitigation T#/r June 14, 1991
data obtained from EPP files. Project Name and DCscripti0rl: "Amsinclda Grandiflora Experimental Reintroduction." EPP contracted with Dr. Bruce Pavlik of Mills College, Oakland, to re-establish
grandiflora at Black Diamond Mines Regional Reserve, a park within the East Bay Regional Park District (Pavlik 1990). The project included: (1) reintroduction of Amsinckia grandiflora to its historic location near Antioch, California CStewartviile"), (2) monitoring the new population; and, (3) experimentally
testing the effects of burning,
clipping, and herbicide on survivorship and seed production ofAmsinckia grandiflora. These results would be used to establish additional satellite populations of Amsinckia grandiflora. Mifiuafion-Related?: No. Pro ieet Ob_iectives: Establishment of at least four new Amsinckia populations within its historic range in order to reduce the probability of extinction. Proiect Methods:
A 14 x'17 m plot was fenced with barbed wire to exclude livestock.
Within the area, 20, 2 x 2 m plots of 4 treatments were selected by a stratified random design. Five plots served as controls, five plots were burned after sowing, five plots were hand-clipped,
and five plots were sprayed with a dilute solution of a grass-specific
known as "Fusilade®", produced by the ICI Corporation).
Amsinckia grandiflora nutiets (3460 total), 1800 from a naturally occurring population (Site 300 source) and 1660 grown at the University of California at Davis were sown on October 19 and 20. Each plot was planted with 160 niatlets by pressing each into a shallow depression in the mineral soil. The nuflets were covered with approximately
cc of loose native soil to a depth of 1 cm. No supplements of water or nutrients were applied during the experiment. Amsinckia grandiflora plots were monitored for the following parameters: (1) germination, (2) stress factors, (3) mortality, (4) phenology, (5) reproductive Final mifigatinn T/r/r June 14, 1991
(6) pin-thrum ratio, and (7) nuflet output per plant and per plot. Criteria for Success: Not explicitly stated, but the success of the reintroduction effort was based on the result that the maximum nutiet output in the experimental plots exceeded the predicted nuflet output (based on laboratory studies). Proiect Success: Pavlik reported the project a success in its first year, based upon i.he production of approximately 35,000 seeds from 1140 individuals, representing a ten-fold increase over the number (3460) of individuals used in the experiment. Date Prolect Initiated: October, 1989
Not state or federally
listed, but meets CEQA criteria (§15380?) at the time of transplantation; CNPS List 4. Respondent:
Mr. Gary Schoolcraft,
U.S. Bureau of Land Management,
Prqiect Name and Description: None. U.S. BLM initiated a transplantation project, moving a portion of a population consisting of approximately
the time (1983), was considered the only known population in California. Transplantation was attempted as an •experiment because it was believed that gold mining would return to the area, and the population was located at the edge of the previous mining activity. Mitigation-Related?: No. Proiec_ Objectives: Project was initiated to determine whether transplantation of Antennaria flagellaris could be used in the future as mitigation. Project Methods: Plants were removed in groups from a large (>10,000+ individuals) by shovel. These were then transplanted
immediately in fiats to the relocation sites. Groups
and soils were kept in tact, as much as possible. Some plants were watered with a vitamin B1 mixture, while others were not supplemented.
No difference was observed in growth
• between these two groups. Each summer following the transplantation, Final mitigationT/r# June 14, 1991
the total number of plants (both live
and dead) were counted. No transplanting report was prepared, but internal memoranda describing the transplantation of the transplantation
and the concluding activities were prepared.
was 1 work day per transplant.
Criteria for Success: Establishment and reproduction of the plants on site, to sufficient numbers to guarantee existence of the population. Project Success: populations,
Of the >400 plants transplanted into 4 different
only one newly established
population exists. This consists of only 17 plants
after 6 years. All other died. Schoolcraft suggested that because the plant is a short-lived perennial that reproduces vegetatively primarily by stolons, the receptor site may have had an inappropriate soil texture to allow adequate vegetative reproduction. Date Proiect Initiated:
Federally endangered; Respondent:
CNPS List lB.
Pardee Bardwell, U.S. Bureau of Land Management
(U.S. BLM) and
Michael Baad, California State University, Sacramento. Project Name and Description:
Distribution of Rare Plants on Public Lands
Within the Red Mountain Study Area and A Study of the Population Dynamics and Reproductive Biology of McDonald's Rock-Cress [sic] (Arabis macdonaldiana)."
project was contracted by Dr. Baad with the U.S. BLM to determine the: (1) geographic distribution of rare plants on Red Mountain public lands; and, (2) population dynamics and reproductive biology of MacDonald's rockcress (Baad 1987). Mitigation-Related?:
Pro!ect Obiectives: The overall project objective of the contract was to determine why Arabis macdonaldiana is not morewidely distributed within the rocky habitats of Red Mountain. The project was initiated in part in response to the 1984 Recovery Plan for Final mitlgation T/rhJune 14, 1991
• MacDonald's rock cress. _:_ro!ectMethods: As part of this contract, in November 1985, Dr. Baad planted 30 1 m2 plots with 100 Arabis macdonaldiana seeds each, over a wide range of habitats on Red Mountain. conditions.
Several plots also received seedlings germinated from seed under greenhouse These were monitored during 1986.
Criteria for Success:
Pro_iect Success: The report notes that there was extremely poor germination
Arabis macdonaMiana over the wide range of habitats into which they were outplanted. Dr. Baad concluded that this species has a relatively low rate of germination even in its preferred habitat. Also, the transplants did not do well, surviving in only 3 of the original plots. All but 5 of the original 25 transplants that remained were completely grazed and/or tom out of the ground by herbivores. Date Proieet Initiated: Spring 1984.
].V,B,41 Arctostaphylos endangered;
CNPS List lB.
Respondent: Ms. Terri Thomas, U.S. National Park Service, Golden Gate National Recreation Area, San Francisco. Proiect Name and Description: "Raven's Manzanita Recovery Plan." The "relocation" project was initiated as part of the Raven's manzanita recovery plan. Mitigation-Related?:
Project Obiectives: To expand the number of individuals in the population, so that the single remaining individual could remain undisturbed. Proiect Methods: Horticultural
Approximately 60 cuttings were taken and propagated by the Saratoga
Foundation and the University of California Botanic Garden.
Later, 60 plants
were outplanted in the Presidio in sites identified as similar to the original serpentine site of Final mitigation TMr June 14, 1991
the parent plant. Plants were watered periodically throughout the first season. An unreported number of seeds were collected, soaked in concentrated sulfuric acid for three hours, and then washed. They were then stratified in moist peat for three months at room temperature and then for three months in the refrigerator. Criteria for Success: The criterion for success for the cuttings was simply survival. For the seeds, the criterion for success has not yet been determined, because they arc still experimenting with collection times, germination techniques, etc. However, no mechanism for protection of the transplants has been initiated. Project Success: Of the approximately 160 c)uttingstaken and grown at various local botanical gardens, 60 plants were eventually outplanted. It is not clear from the respondent whether any of these remaining 60 have died, but it appears that they have not. Date Project Initiated: January 1987.
State rare; Federal Candidate C2; CNPS
List lB. Respondent:
Mr. Dave Imper, North Coast Chapter, California Native Plant Society,
Eureka. Pr_ect Name and Description: "Bensoniella Transplant Project." Project was initiated in 1979 by the Six Rivers National Forest because downcutting of stream channels appeared to threaten populations ofBensoniella oregana. Approximately 50 rosettes were removed from the Smokehouse Creek parcel and transplanted to Groves Prairie, east of Willow Creek, in similar habitat. Mitigation-Related?:
Proiect ONeetive_: No specific objectives, although generally the Forest Service wanted to prevent the demise of the streamside populations of Bensoniella oregana. Project Methods: Whole plants (rosettes) were removed from the Smokehouse Final mitigation T/r/r June 14, 1991
Parcel (an outholding held by Six Rivers National Forest specifically for Bensoniella oregana), and transplanted to Groves Prairie, east of Willow Creek in a similar habitat of white fir (Abies concolor)/incense cedar (Calocedrus decurrens). Transplants were monitored
Not clearly defined, other than short-term survival. Respondent
noted that a "rather inadequate" measure of vigor was included in the original monitoring plan. Pro_ieet Success:
Success was not clearly defined, but some rosettes survived. During the
first year, a large increase (>100%) in the number of rosettes and inflorescenees was observed.
However, there has been an apparent failure for these transplants to reproduce
sexually. Respondent indicated that so little of the biology of this species is known that it is not clear whether Bensoniella oregana reproduces sexually anywhere or whether sexually reproduction is intermittent. Also, respondent indicates that the transplant population has declined significantly within the last year. Date Project Initiated:
Dalmatus (Fen'is' Bird's Beak):
endangered; CNPS List lB. _d,_Lq.0.d.¢_: Dr Larry Heckert, Jepson Herbarium, University of California, Berkeley. Pro_iect Name and Description: Mitigation-Related?:
Project Obiectives: None stated. Presumably the objective of Dr. Heckert was to establish a self-sustaining population of Cordylanthus palrnatus at the Mendota Wildlife Refuge. Pro ieet Methods:
An unspecified number of individuals was collected from somewhere
outside the wildlife refuge and transplanted to the refuge. The population lasted for over 10 years, but eventually died out. At some time during this project, a naturally-occurring FinalmitigationT/fir June 14, 1991
population was discovered Criteria for Success: _:
within the Mendota Wildlife Refuge.
Project was successful about a decade, but not for the long term.
Date Project Initilated: late 1970's.
cvmosa sso. raarceseens
(Santa Monica Mountains Dudleya):
State rare; Federal Candidate C2; CNPS List lB. _:
Ms. D.A. Hoover, Woodland Hills, Caiifomia.
Pro_iectName and Description: "Soltice Canyon Native Plant Project." Volunteers from the California Native Plant Society (CNPS) proposed to eradicate invasive exotic species and replace them at SolticeCanyon Park with species native to the Santa Monica Mountains. This project included the reintroduction of Hemizonia minthornii and Dudleya cymosa ssp. marcescens. Mitigation-Related?: Project O_ectives:
(see IV.B.8 for more details).
No.' Objectives as stated were to expand the protected sites for the relatively
rare native species and to learn practical methods for safe propagation without threatening native populations. Project M_thods: Individuals ofD. cymosa vat. marcescens were collected (salvaged) from along a mad in Red Rock canyon that was to be graded for In'e-break maintenance. Approximately
7-8 individuals were lifted from the hard-packed roadside soil and
transplanted to soil-filled pockets on a rocky berm on Humbolt Terrace at Soltice Canyon Park. Each plant was watered by hand for several months. The respondent suggested that the rocky setting protects the plants from gophers and also provides excellent drainage. Plants were monitored by CNPS members through periodic inspections.
included weeding of competing exotics (e.g., castor bean, tree tobacco, mustard, various thistles, etc.) and handwatering of additional native species. Total cost of the project was Final mitigation TMr June 14, 1991
$130.00 (gas @ $10.00 and paid assistance at $120.00). Criteria for Success: None stated for Dudleya cymosa var. marcescens. Prqiect S_ccess: transplantation
For Dudleya cymosa var. marcescens, the respondent felt that the
was successful because the transplanted
However, the respondent also noted that many more individuals ofD. cymosa var. marcescens were lost due to road-scraping. population
through future off-site seed collection,
Date Project Initiated:
The CNPS liopes to expand this reintroduced
1987; project on-going.
(Santa Susana Tarp/ant):
State rare; Federal
Candidate C2; CNPS List lB. Respondent:
Ms. D.A. Hoover, Woodland Hills, California.
Pro_iect Name and De_'ription: "Soltice Canyon Native Plant Project." Volunteers from the California Native Plant Society (CNPS) proposed to eradicate invasive exotic species and replace them at Soltice Canyon Park with species native to the Santa Monica Mountains. This project included the reintroduction of Hemizonia minthornii and Dudleya cymosa ssp. marcescens. Mitigation-Related?: Project Objectives:
(see IV.B.7 for more details).
No. Objectives as stated were to expand the protected sites for the relatively
rare native species and to learn practical methods for safe propagation without threatening native populations. Project MgIhods: Seed was collected from two off-site populations in the Santa Moniea Mountains (Calabasas Peak and Castro Peak), and stored for several weeks. These failed to germinate, but a second collection was made, and seeds were sown the same day of collection. These seeds germinated and subsequently were transplanted to a screen-covered seed bed in Soltice Canyon Park. The populations were subject to gopher predation and FinalmitigationT/rh" ]'une 14, 1991
ovcrwatering, however. Plants were monitored by CNPS members through periodic inspections. Visits included weeding of competing exotics (e_g., castor bean, tree tobacco, mustard, various thistles, etc.) and handwatering of additional native species. Total cost of the project was $130.00 (gas @ $10.00 and paid assistance at $120.00). I_L_._:
None stated forHemizonia minthornii.
Proiect Success: Respondent reported that virtually 100% of the seeds germinated, but the very young transplants died from drought. Approximately 10 individuals survived to flower. The Castro Peak seedlings will be transplanted to various locations in the park to test their ability to survive in each (different?) site. _tg_L]]_]_:
1987; project on-going.
wolfii (Wolfs Evening Primrose):
Not California State listed;
Federal Candidate C2; CNPS List lB. Respondent:
Mr. Dave Imper, North Coast Chapter, California Native Plant Society,
Eureka. Proiect Name and Description: None. Project involved the population expansion within the type locality of Oenothera wolfii at Luffenholtz Beach. In December, 1988, 3 individuals of Oenothera wolfii were transplanted from Luffenholtz parking area to adjacent habitat, along with two greenhouse _gg_Lq/l:_¢._:
seedlings and considerable
amounts of seed.
Project Obiecfivcs: The stated objective was to reduce the impacts of repaving, trampling, and vehicular use to populations of Oenotfiera wolfii at Luffcnholtz Beach. Project Methods: Seeds were collected and grown in rcspondcnt's greenhouse. Approximately 80 seedling rosettes ranging from 1 - 4 inches in diametcr were outplantcd on Dcccmber 26, 1989, in four small areas cast of Scenic Drive, south of the residence
Final mitigationT/r/r June 14, 1991
In addition, a small amount of seed was planted directly.
CViteriafor Success: None staied. Proieet Success:. Late summer mortality was high. Only 55 seedlings from 7000+ seeds currently survive. Five of the 7 onsite transplants survived, and one of the two greenhouse seedlings. However, the respondent suggests that both seeding and transplantation are potentially viable methods for mitigating impacts on this species, and for expanding small populations.
Of the 46 projects reviewed in this analysis, 17 (37%) were conducted by private businesses involved in housing construction, outdoor recreational facilities, and business offices (Table 4). However, state services such as the California Department of Transportation, California Department of Water Resources, California Department of Parks and Recreation, and the services of two counties (Sonoma and Fresno) together were involved in a total of 15 projects (33%). Finally, an additional 5 projects (11%) were conducted by energy companies (both private and public utilities) (Table 4). The remaining projects were research-related or mitigation-related projects conducted by various agencies of the federal government for a variety of reasons,
OF FINDINGS Successes
Seven transplantation attempts were considered successful in this analysis. These attempts involved the plant species Amsinckia grandiflora, Dudleya cymosa ssp. marcescens, Holocarpha macradenia, Lasthenia burkei, Opuntia basilaris var. treleasei, and Sidalcea peclata. Of these species, the first two were not involved in mitigation-related transplantation efforts. However, the Amsinckia project appears to have been so successful because of the great detail and care taken in Finalmitigation T/rfr June 14, 1991
PLANT SPECIES INVOLVED IN TRANSPLANTATION, RELOCATION, OR REINTRODUCTION PROJECTS, PROJECT PROPONENTS, AND DEGREE OF MITIGATION SUCCESS.
_1)pardee Company 2) Shea Homes 3) Pardee Company
_Westview Planned Residential Development Palos VistaDevelopment Reparation for Sabre Springs Development Indian"Hill,Las Brisas, & Spyglass Amsinckia grand_ora Expenmeraal Reintroduction None Geographic Distributionof Rare Plants onPubfic Lands Within theRed Mountain Study Area .... Raven's Manzanita Recovery Plan
PROJECT On-going On-going On-going
4) Unknown N/A: Research-Related
U.S. BLM N/A: Research-Related
N/A: Research-Related Bensoniella Transplant Project l) Christopherson Homes Montclair Park 2) Cobblestone San Miguel Estates DevelopmentCorporation Baldwin Company College Area Specific Plan in San Marcos Dept. Water Resources Kaweah Reservoir Dam Expansion Siskiyou County None . UC Davis None Calif. Dept. Transportation LittlePico BridgeReplacement& Piedms Blancas Shoulder widening N/A: Research-Related None U.S. BLM None N/A: Research-Related None
Limited succe,as Limited success On-going
Calif. Dept. _rransportationSanta Ann WoollystarReIccadonProject
Calif. Energy Commission LUZ SEGS VII Calif. DepCTransponation Caltruns Del Mar Mesa VernalPools
Not successful Partial success
Pacific Gas & Electric Co. Vaea Dixon-Contra Costa 230-kV Reconductoring Project.... 1)UC Davis None 2)Unknown Spanish Bay 3) Unnamed timber company None A Lone Star Industries, Inc. Revegetadon of Olympia¢_mrry Unknown Spanish Bay.
Brodiaeafilifolia Brodiaea insignis Calochortus greenei Chorizanthehowellii Cirsiumoccldentale Var.
,On-go;rag . i'_omtormataon On-going Plating stage No informaUon
1) N/A: Research-Related None 2) Las Vir_enes Municipal Santa SusanaTarplant Mitigation Water District Program Twin Lakes Tank No. z 3) Chateau Builders Woolsey Canyon Development Nylen Company HilltopCommons Development l) Unknown Airport Blvd, Business Park 2) Sonoma Co. Airport Sonoma Co. AirportExpansion 3) Cobblestone _an Miguel Estates Development Corporation 4) Sonoma County Countyof SonomaPublic Service Area 31 Waste Water Storage Pond 1) Dept. Water Resottrces Baker Slough Bank Revetment 2) DepLParks & Recreation None Unknown Spanish Bay
Pacific Gas & Electric Co, Va_aDixon-Contra Costa 230-kV Reconductoring Project.,.. N/A: Research-Related None 1)Calif. Energy Kern RiverCogeneration Power Commission Plant Project 2) Sycamore Cogenemtion Sycamore CogenerationProject _ompany Unknown Sunrise,rOouglasWetland & Creation Progrdm_ Unknown Lake Sherwood Golf Course Calif. Dept. Tmn_ortation Caltrans Del Mar Mesa Vernal Pools Fresno Co. Metro_-'lood Round Mountain Flood Control Control District Project ^ _ Calif. Dept. Transportation Feather River t_anyon:_tormDamage Re:el3air" K-Mart Corporation Sidalceapedata TransplantationProject
Not successful Successful Unknown Ongoing Not successful Partialsuccess Planning stage Not successful Successful
all phases of the research, and that is was peformed by a conscientious and skilled researcher, Dr. Bruce Pavlik. In this instance, the biology of the species was investigated in full, and various relevant (receptor) site treatments were included a_ an experimental component of the research. It appears crucial that the soil and habitat requirements before successful establishment
of the species be understood completely
can be assured.
As for the success of the nonmitigation-related transplantation ofDudleya cymosa ssp. marcescens and the mitigation-related Opuntia basilaris var. treleasei, these species are succulents which in general, have relatively easy horticultural requirements.
Succulents by their biology are rather
hardy and tolerant of drought and other forms of disturbance.
Therefore, in the case of the
Bakersfield cactus, using industry standards for cutting and callus formation may have insured its successful transplantation for the Kern River Cogeneration Power Plant Project. However, the receptor site was also carefully prepared to receive the cactus pads, and this again, appears to be important in assuring success of the transplantation.
The reasons for the success of the thwo Lasthenia burkei vernal pool projects (Sonoma County Airport Business Park, and the Sonoma County Airport Expansion are not clear. The issue of vernal pool creation, mitigation, and enhancement
biologists in the State, and there are many differing opinions about vernal pool mitigation "success" (see Ferren and Gevirtz 1990, for example).
In a survey such as this, we must accept
the accessment of success by the parties responsible for the mitigation, if the established criteria are met and it meets the criteria imposed by this review. In all three cases with Lasthenia burkei, populations
were established with a greater number of individuals than there present originally
(i.e., no individuals). However, because these projects have been on-going for less than 10 years, the long-term viability of the populations is not yet known.
Finalmitigation T## June 14, 1991
What is also interesting about the vernal pool projects in Sonoma County is that they also involved Blennosperma bakeri. Although these projects are technically on-going and were not evaluated as either successful or unsuccessful in this analysis, the early reported results indicate that this species will also successfully establish at created vernal pools. However, one respondent (N. Harrison, San Rosa Jr. College) sugges!ed that despite the purported success of vernal pool creation in Sonoma County, this is an "unsuitable" method for mitigation. Preservation is the only viable mitigation method for vernal pool [plants]. She also reported that Sonoma State University [personnel] has tried for 12 years to vegetate an artificial vernal pool by seeding and transplantation from local sources, but without success. It is not clear from this review why there is such a clear discrepancy in the evaluation of mitigation success for Sonoma County's vernal pool plant species. It is likely that philosophic and ethic differences, rather than biology, drive this debate.
The successful mitigation efforts of the last two species, Holocarpha macradenia and Sidalcea pedata, are not known. For the Santa Cruz tarplant, the salvage of individual plants was accomplished
with care, but preparation of the receptor site was not performed.
It is possible that
H. macradenia is a rather weedy species capable of taking advantage of small site disturbances to establish successfully.
As for the bird-footed checkerbloom,
the individuals were carefully
removed from the construction site, the receptor site was prepared to receive the transplanted individuals,
and the receptor site fenced for protection from disturbance.
The assessment of
success may be premature for this species because the project is only in the second year of monitoring, but the first year survival rate is significant (90%).
Over one quarter (12 out of the 26 projects; 26%) of the transplantation, relocation, and reintroduction projects in this survey are considered failures. They will not be reviewed individually;
however, several are notable, and will serve to illustrate the various reasons for a
Final mitlgafion T#/r June 14. 1991
project's lack of success. The Las Virgenes Municipal Water District's project involving the construction of a water and the consequent destruction of a population of Hemizonia minthornii is a controversial
mitigation failure that received media attention (Los Angeles Times 1989). Several
obvious reasons why this project failed are: (1) seed was collected from plants before it was fully mature (seasoned) and thus subsequent seed germination was poor;, (2) plants were collected during the middle of the growing season when they may have been most vulnerable to disturbance; and, (3) because of the nature of the (rock) substrate, individuals were difficult to collect for transplantation.
Although an attempt was made to extract individuals carefully, in many cases it
appears that the roots had to be broken as individuals were tom from their rock substrate; consequently,
few individual s survived.
The difficulties the California Depa_u,ent of Transportation had with the transplantation of Monardella
linoides ssp. viminea again illustrates the problems of native substrate and soils. One
of the f'mdings made in the 1986 monitoring report was that this species required its parent material to survive in cultivation. This was discovered after a significant number of individuals had died. For Antennariaflagellaris, transplantation
the respondent suggested that the reason this species did not thrive in its
site was because the soils had an inappropriate soil texture to allow for
stoloniferous growth. Arabis macdonaldiana is a serpentine endemic, and many such species are difficult to grow in cultivation. germination
Dr. Baad's work demonstrated that this species has poor
rates even on its native substrate, and did not fare well in any experimental
manipulations in the field. Finally, despite serious efforts to control for the unusual edaphic factors that control the distribution of Eriophyllum mohavense (and Chorizanthe spinosa), tmnsplantadon
of seeds of the Barstow woolly sunflower and its soil by the California Energy
Commission did not succeed. Again, the respondent suggests that the current drought is responsible
for the transplantation
Final midgatinn T/r/r June 14, 1991
Another feature of the mitigation-related
failures is illustrated, again by the
California Department of Transportation, in its efforts to transplant Sedum albomarginatum.
species is a succulent, and unlike the other succulents in this survey, did not survive its transplantation.
It is believed that the transplanted
individuals did not survive in large part due to
the present drought (Martz, personal communication).
The efforts of the U.S. Bureau of Land Management the transplantation
(BLM) illustrate the problems associated with
at different life stages. In this instance attempted to transplant seedlings of
Croton wigginsii. The seedlings were reported as being transplanted with considerable care into an appropriate habitat, but all seedlings died. Because seedlings are a well known to be vulnerable life history stage, manipulations
involving seedlings are not likely to succeed.
For other species, such as Pentachaeta lyonii, the reasons for failure are not clear. Despite considerable efforts on the part of the consultants to insure mitigation success, including cooperation
with the Rancho Santa Ana Botanic Garden for horticultural expertise and sound field
methods, the respondent reported that success of the project objectives was not achieved.
reason offered was that the salvage plan was "inadequate."
In summary of the successes and failures of transplantation,
relocation and reintroduction
sensitive plant species in California, three broad recommendations
can be made that are based on
several aspects of the biology of imperiled plant species. These recommendations
(1) Individuals should be removed with as little disturbance as possible to the individual, and at a phenologically photosynthetically
appropriate time of year when the individual is dormant or
(2) The receptor site should be of the same habitat quality, particularly with respect to soil Final mitigationT_/r June 14, 1991
type and its physical characteristics.
Various other aspects of the receptor site might
include weeding to decrease competition from native and exotic species, watering during times of drought, and fencing and/or other forms of site protection; and
(3) Knowledge of the biology of the organism appears to aid greatly in the design of appropriate horticultural
techniques for the preparation of cuttings, transplantation,
germination, etc. This is problematic, however, because the biology of most State-listed species is poorly known. Although some species such as cacti and succulents may be amenable to standard horticultural
techniques for propagation,
most are not. Therefore,
without sufficient knowledge of the biology of impacted species, success of the transplantation,
will not be assured.
Mitigation of impacts to endangered, threatened, and rare plant species is an issue of considerable debate. On the one hand, the Canadian Botanical Association (Fahselt 1988), the American Society of Plant Taxonomists (ASPT 1989), and the Rare Plant Scientific Committee of the California Native Plant Society (CNPS 1990) do not favor mitigation and in point of fact, oppose transplantation
as a means of plant preservation except in those instances for which there are no
other means of protection. An otherwise doomed population ofPenstemon barreniae was transplanted
under just such circumstances
(Guerrant 1990). Mitigation guidelines propagated by
the CNPS (1990) recommend impact avoidance as outlined in the California Environmental
Act (CEQA §15370) as the favored mitigation technique.
On the other hand, however, transplantation,
relocation, and reintroduction
threatened, or rare species are routinely performed as mitigation for "unavoidable" according to both state and federal environmental Final mitigation T/r/r June 14, 1991
This is currently accomplished
Califomia for listed plant species through Mitigation Agreements. However, it is remarkable that such potentially harmful activities to State- and (federally-) listed species has, until very recently, been so poorly monitored by all parties (but see new guidelines by Howald and Wickenheiser 1990).
What is equally remarkable is the lack of performance criteria (i.e., criteria for success) of the completed mitigation-related projects reviewed here. Only 15 of the 46 projects (33%) have explicitly defined criteria for success, and until quite recently, there was no consistency in these criteria.
Without such "industry" standards, success of translocation,
projects cannot be made objectively.
When criteria are explicitly defined, for
example the College Area Specific Plan in San Marcos for Brodiaeafilifoli a, mitigation successes can be assessed appropriately.
Such policy statements about transplantation, relocation, or reintroduction as mitigation as those promulgated
by the Canadian Botanical Society and the American Society of Plant Taxonomists,
combine an ethical viewpoint with a scientific evaluation of plant (and animal) transplantation efforts. For animals, Griffith et al. (1989) reported that success rates for the translocation of birds in the United States, Australia, Canada, and New Zealand range widely, from 10% to greater than 90%. The results depended upon the type of animal involved and the conditions of release.
concluded that without high quality habitat at the receptor site, translocations had a low chance of success, regardless of how many animals were released or the condition of the individuals. quality receptor habitat may be even more critical for plant transplantations
than for animals,
because of the physical immobility of plants.
For plants, Hall (1986) recently reviewed transplantation environmental
for sensitive plants as mitigation for
impacts in California, and concluded that transplantation
Final mitigation T/rh' June 14, 1991
has not been a "panacea"
for botanical resource conservation. transplantation techniques.
Hall also suggested that the lack of sufficient post-
and monitoring has contributed to the unreliability of these mitigation
however, is a labor-intensive
and as such, may not be
particularly over the long term. In addition, monitoring of rare plant
species can take many forms (see for example, Palmer 1987), and standards for monitoring should be established before mitigation successes can be compared.
This is an enormous task.
The effective of many kinds mitigation-related projects is coming into question elsewhere, and it is a critical resource conservation
issue for the regulatory community and the public alike. For
example, the Florida Depatiauent of Environmental
Regulation recently issued a report that
summarized the success of wetland mitigation required for the issuance of dredge and fill permits under the state Henderson Wetlands Act of 1984 (FDER 1991). The success rate of mitigation was 27% (with some wetland types proving much less successfully mitigated than others). The report also finds that with the institution of simple remedial measures, mitigation success could have been increased to 40% overall. Interestingly, the report documented only 6% (4 out of 63) were found to be in full compliance with the mitigation requirements of the permit.
Some analogies may be relevant here. First, in both instances, success rates for mitigation projects is equal to or less than 25%. This statistic should be unacceptable strongly indicates that theprogram
is not working effectively.
to the regulating agency, and
Second, some plants (as some
wetland habitats) may be more easily manipulated (i.e.,, mitigated) than others. This is clearly reflected in the kinds of plants (e.g., succulents and cacti) that were determined to be successfully mitigated in this review. Third, it is likely that with simple remedial measures (as discussed for the Florida wetlands), e.g., hand-watering, weeding of competing exotics, fencing, etc., mitigation success rates for the transplantation
of State-listed species could be greatly enhanced.
although not part of this study, it should be investigated Final mitigationT#/r June 14, 1991
whether the permittees a?e in full
compliance with the Mitigation Agreements.
There are some success stories, however. Stephanomeria malheurensis (Parenti and Guerrant 1990) and Styrax texana (Cox 1990) are two endangered plants that have been successfully reintroduced back into their native habitats in Oregon and Texas, respectively. such as these two, success of relocation, reintroduction, Herculean means. Thus until we understand
In many instances,
is achieved through
thoroughly the techniques of translocation,
it may be unwise to routinely agree to these forms of
mitigation for endangered,
threatened, or rare botanical resources.
In conclusion, it is recommended that because of the low success rate of the completed mitigationrelated projects involving translocation,
and the reasonably
number of projects that are on-going and for which no conclusive information is currently available, the Endangered
Plant Program should limit their Mitigation Agreements
to those projects
for which such techniques are the only known means of preservation of a population of an endangered, threatened, or rare species, or for impact avoidance is not possible, and for which there is no demonstrated
Final mitigation T/r# June 14, 1991
I gratefully acknowledge all those individuals and organizations who responded to my lengthy questionnaire. In addition, I wish to thank Ann Howald of the Endangered Plant Program for providing me with this opportunity, and for her considerable patience.
Final mitigation TMr June 14, 1991
American Society 0f Plant Taxonomists. 1989. Resolution adopted by the American Society of Plant Taxonomists at their annual meeting, August 7, 1989. Baad, M. 1987. Geographic distribution of rare plants on public lands within the Red Mountain study area and a study of the population dynamics and reproductive biology of MacDonald's rock-cress, Arabis macdonaldiana Eastwood. Consultant's report for the U.S. Bureau of Land Management, Ukiah District Office. California Department of Fish and Game. 1989. Designated endangered, threatened, or rare plants. Nongame-Heritage Division, Endangered Plant Project, January 1989. California Department offish
and Game. 1990. Designated endangered, threatened, or rare
plants. Natural Heritage Program, Endangered Plant Project, March 1990. California Native Plant Society, Rare Plant Scientific Advisory Committee. 1991. Mitigation guidelines regarding impacts to rare, threatened and endangered plants. Unpublished. 17 p. Cox, P. 1990. Reintroduction of the Texas snowbell, (Styrax texana). Endangered Species UPDATE 8(1): 64-65. ECOS, Inc. 1988. Experimental design for a transplant study of Mason's Lilaeopsis. Consultant's report prepared for the U.S. Bureau of Reclamation and the California Department of Water Resources, Central District. ERC Environmental and Energy Services Co. 1990a. Status report, proposed maintenance/Monitoring plan, and performance criteria for the Palos Vista Thorn-mint mitigation program. Consultant's document, prepared February 1990, revised September 1990. ERC Environmental
and Energy Services Co. 1990b. San Diego Thorn-mint
ilicifolia) biological reparation plan for the Pardee Company Sabre Springs Development, prepared June 1990, revised October 1990. FinalmitigationT/r# June 14, 1991
ERC Environmental and Energy Services Co. 1990c. Second annual report: Brodiaeafilifolia mitigation program, San Marcos, California, prepaxed December 1990. ERT, Inc. !988a. Luz SEGS VII sensitive plant salvage soil survey technical report. Consultant's report prepared for Luz Engineering
Los Angeles, California, May 1988.
ERT, Inc. 1988b. Biological resource mitigation implementation Generating Systems, Kramer Junction, California. California Energy Commission,
Fahselt, D. 1988. The dangers of transplantation
plan for the Luz Solar Electric
Consultant's report submitted to the
1988. as a conservation technique.
Journal 8(4): 238-244. [The journal article included the policy statement transplantation as a method of preservation
by the Canadian Botanical Association, adopted June 1987.]
Ferren, W.R., Jr. and E.H. Gevirtz. 1990. Restoration and creation of vernal pools: cookbook recipes or complex science?
Pp. 147-178, in, D.H. Ikeda, R.A. Schlising (eds.), Vernal
Pool Plants. Their Habitat and Biology. Studies from the Herbarium, California State University, Chico, No. 8; June 1990. Florida Department of Environmental mitigation.
1991. Report on the effectiveness
Report submitted to Lawton Chiles, Governor; Gwen Margolis, President of
the Senate; and T.K. Wetherell, Speaker of the House of Representatives. Griffith, B., J.M. Scott, J.W. Carpenter, and C. Reed. 1989. Translocation
March 5, 1991.
as a species
conservation tool: status and strategy. Science 245: 477-480. Hall, L.A. 1986. Transplantation
of sensitive plants as mitigation for environmental
413-420 In, T.S. Elias and J. Nelson (eds) Conservation and Management of Rare and Endangered Plants. Proceedings
of a California Conference on the Conservation and
Management of Rare and Endangered
Plants. California Native Plant Society, Berkeley.
Howald, A.M. and L.P. Wickenheiser. 1990. Mitigation plan annotated outline for endangered plants of California. Endangered Final mitigation Th'/r June 14, 1991
Unpublished 8 0
of Fish and Game, Natural Heritage Division, document, August 1990. 33p.
Inc. 1987. Olympia Quarry revegetation plan. Consultant's report submitted to
Lone Star Industries, July 1987. LSA Associates, Inc. 1989. Draft plan to collect seed of Ben Lomand wallflower (Erysimum teretifolium)
for the revegetation of the Olympia Quarry. Consultant's report submitted to
the California Depruia_ent of Fish and Game, September, 1989. Los Angeles Times. 1989. Tough little plants don't survive term in nursery.
Article by staff
writer Bob Pool, February 3, 1989, p. 3, 14. Martz, C. 1990. Annual monitoring report for Santa Ana WooUystar Relocation California Department
McClelland Consultants (West), Inc. 1988. Santa Susana tarplant (Hemizonia minthornii) mitigation program Twin Lakes Tank No. 2. Initial progress report. Consultant's report submitted to Las Virgenes Municipal Water District and the California Depa_:ia_ent of Fish and Game, December 1988. McClelland Consultants (West), _[nc.1990. Santa Susana tarplant (Hemizonia minthornii) mitigation program Twin Lakes Tank No. 2. Third annual progress report. Consultant's report submitted to Las Virgenes Municipal Water District and the California Depa_ttuent of Fish and Game, December
Mistretta, O. 1989. Amended mitigation and research plan forHemizonia minthornff - Woolsey Canyon Development.
Consultant's report [Rancho Santa Ana Botanic Garden], March
1989. [Ralph] Osterling Consultants, Inc. 1989. Santa Rosa rare plants mitigation plan. San Miguel Estates 1. Consultant's report. Palmer, M.E. 1987. A critical look at rare plant monitoring in the United States. Biological Conservation 39: 113-127. Pavlik, B.M. 1990. Reintroduction ofAmsinckia prepared for the Endangered Final mitlgation T#/r June 14, 1991
grandiflora to Stewartville.
Plani Program, California Department of Fish and Game, 8 "1
Contract No. FG-7434. PSBS, Inc. 1988. Monitoring report. Acanthomintha ilicifolia. Consultant's report, prepared 17 May1988. Smith, J.P., Jr. and K. Berg. 1988. California Native Plant Society's Inventory of Rare and Endangered Vascular Plants of California. Publication
Calif0mia Native Plant Society Special
No. 1, 4th edition, Sacramento.
WESTEC Services, Inc. 1988. Biological mitigation plan for the College Area Specific Plan, San Marcos, San Diego County, California.
Consultant's report, prepared April 29, 1988.
Zedler, P.H. and C. Black. 1988. Species preservation in artificially constructed habitats: preliminary evaluation based on a case study of vernal pools at Del Mar Mesa, San Diego County. Pp. 367-373, In, J.A. Kusler, S. Daly, and G. Brooks (eds.) Urban Wetlands. Proceedings
Final mitigation TF/r Jun_ 14, 1991
of the National Wetland Symposium,
June 26-29, 1988, Oakland, California.
1600 Holloway Avenue San Francisco, California 94132
San Francisco State University
Department of Biology
18 April 1990 Ms. Ann Howaid, Program Ecologist Endangered Plant Program California Depru'tment offish & Game Non-Game Heritage Division 1416 Ninth St. P.O. Box 944209 Sacramento, CA 95814-2090 Dear Ms. Howaid: As part of the California Department of Fish and Game's Endangered PlantProgram review of mitigation for state-listed rare, threatened and endangered plant species, I am conducting a survey of mitigation, transplantation, replantation and reintroduction projects that have been implemented or planned in California. The purpose of this survey is to assess the success of mitigation-related transplantation, relocation and reina'c!duction projects of state-listed plant species. The enclosed form details fifteen 'questions. Please answer each to the best of your knowledge. Should you need more room for your answers, please feel free to attach an additional sheet. Copies of any reports for projects of an unusual or special nature; or illustrative for any particular point, would be greatly appreciated. If you are unable to complete this questionnaire, please contact me at your earliest convenience (415-338-6270). If you would prefer, this questionnaire can be completed by phone if you call me at a time convenient for both parties. Thank you for your time. Your efforts are of considerable importance for a project that has significant ramifications for the future of the rare plant species of California. Yours most sincerely,
Peggy L. Fiedler Assistant Professor Lcdfgq
The City's University
Louise Accurso U.S. Fish & Wildlife Service Box 524 Newark, CA 94516 Lowell Ahart 9771 Ahart Road Oroville, CA 95966 Douglas G. Alexander Depm relent of Biological Sciences California State University Chico, CA 95929 Bob Allen 7 Palm Court Larkspur, CA 94939 David Amine 1314 Curtis Street Berkeley, CA 94702 Jerry Anders GW Consulting Engineers 7447 Antelope Road, Suite 202 ' Citrus Heights, CA 95621 Dick Anderson CEC 1416 Ninth Street Sacramento, CA 95814 John Anderson Yolo County Resource Conservation District Box 231 Winters, CA 95694 John Anderson Tuolumne County Planning Dept. 2 South Green Street Sonora, CA 95370 Joseph Aparicio Biology Department American River College Sacramento, CA 95811
Wayne Armstrong Department of Biology Palomar College San Marcos, CA 92069 Richard Arnold 50 Cleveland Rd., #3 Pleasant Hill, CA 94523 Leland K. Ashford, Jr. Department of Fish & Game 48 West Indianapolis Ave. Clovis, CA 93612 Bill Asserson California Department of Fish & Game 1200 Carter Avenue Bakersfield, CA 93308 Walt Auburn California Conservation Corp 1530 Capitol Avenue Sacramento, CA 95814 Mike Baad Department of Biological Sciences California State University Sacramento, CA 95819 Mark Bagiey P.O. Box 1431 Bishop, CA 93514 Geoffrey Bain U.S. Bureau of Land Management P.O. Box 1112 Arcata, CA 95501 S usan Bainbridge California Depat huent of Fish and Game 1416 Ninth Street, Room 1225 Sacramento, CA 95814 Kate Baird CalTrans 1248 Johnson Avenue San Diego, CA 92103
Richard Baker NPS/Western Regional Office 450 Golden Gate Avenue San Francisco, CA 94102 Doug Barbe 1220 "N" Street, Room 324 Sacramento, CA 95814 Linda Barker 1312 Fairlane Road Yreka, CA 96097 Katie Barrows P.O. Box 478 La Quinta, CA 92253 W. Jim Barry Depat'tment of Parks & Recreation P.O. Box 2390 Sacramento, CA 95811 Jim A. Bartel U.S. Fish & Wildlife Service 2800 Cottage Way, Room E-1823 Sacramento, CA 95825 Ellen Bander 4824 Point Alto La Mesa, CA 92041 Barbara Beard Thomas Reid Associates P.O. Box 872 Palo Alto, CA 94302 Mitchel Beauchamp Pacific Southwest Biological Services, Inc. P.O. Box 985 National City, CA 92050 Tom Beck 19777 Greenley Rd. Sonora, CA 95370 Eric Behn U.S. Army Corps of Engineers 211 Main Street San Francisco, CA 94105
Germaine Belanger CalTrans P.O. Box 911 Marysville, CA 95901
Barbara Benge U.S. Army Corps of Engineers 650 Capitol Mall Sacramento, CA 95814 R.W. Benseler Dept. Biological Sciences Hayward State University Hayward, CA 94542 Kristin Berry P.O. Box 3119 Truckee, CA 95734 Albin Bills Department of Biology Butte College Oroville, CA 95965 Charles Black Department of Biology California State University SanDiego, CA 92102 Martha Black California Depm tment of Parks & Recreation 1600 U.S. Hwy. 101 Garberville, CA95440 Tom Blankinship California Depm tment of Fish & Game 407 W. Pine Street Bishop, CA 93514 Dave Bockman 531 Sumner Street, Apt. D. Santa Cruz, CA 95060 MaryBoland California Department offish & Game 1234 E. Shaw Fresno, CA 93710
Bob Bonderud Pacific Gas and Electric Company 123 Mission Street, #2159 San Francisco, CA 94105 Jack Booth 3551 Eastside Calpella Rd. Ukiah, CA 95482 Steve Botfi Yosemite National Park P.O. Box 577 Yosemite Natl. Park, CA 95389 Frederica Bowcutt P.O. Box 2390 Sacramento, CA 95811 Jacqueline Bowland McClelland Environmental 2140 Eastman Ave. Venmra, CA 93003
David Bradford Envirosphere Co. 10933 Wagner Street Culver City, CA 90230 Dave Bmmlet 1691 Mesa Dr., Apt. A-2 Santa Ana, CA 92707 Dr. Robert Branson National Park Service 57 Ciello Vista Drive Monteray, CA 93940 Rick Breitenbach Bureau of Reclamation 2800 Cottage Way, Room W-2103 Sacramento, CA 95825 Dave Brennan 900 West Grande Porterville, CA 93257 Katya Bridwell URS Corporation 501 J Street Sacramento, CA 95814
Jim Brownell California Energy Commission 1516 Ninth Street Sacramento, CA 95814 AUen Buckman Department of Fish and Game P.O. Box 47 Yountville, CA 94599 Rick Burgess 721 Aster #124 Oxnard, CA 93030 Don Burke Planning Associates 662 Azalea Avenue Redding, CA 96002 Geoff Burleigh 602 North Brand San Femando, CA 91340 Brad Burkhart ERCE 5510 Morehouse Drive San Diego, CA 92121 Robert Burness Sacramento County Planning Depm'tment 827 Seventh Street, Room 230 Sacramento, CA 95814 Tom Burnham 745 West "J" Street Los Banos, CA 936335 Brenda Bumer 14565 Harvard Ct. Los Altos, CA 94022 Joe Callizo 1730 Stockton St. St. Helena, CA 94574 Rosemary Carey EA Engineering Science & Technology 41A Lafayette Circle Lafayette, CA 94549
Clif Carstens Omni-Means, Ltd. 2240 Douglas Boulevard, Suite 260 Roseville, CA 95661 Susan Marie Carter Southern Cal Edison, Research & Development 1190 Durfee Road South El Monte, CA 91733 • Chuck Casena CalTrans 50 Higuera Street, P.O. Box 8114 San Luis Obispo, CA 93403 John Cassady Pacific Gas and Electric Company 123 Mission Street, #2159 San Francisco, CA 94105 Steve Chainey Jones& Stokes Associates, Inc. 1725 23rd Street, Suite 100 Sacramento, CA 95816 Frank Chan Pacific Gas and Electric Company 123 Mission Street, #2159 San Francisco, CA 94105 Norden H. Cheatham Natural Reserves System 300 Lakeside Drive, 6th Floor Oakland, CA 94612-3560 Marvin Chesebro 1545 Wilshire Blvd., #711 Los Angeles, CA 90017 Geoff Chinn Solano County/Environmental 601 Texas Street Fairfield, CA 94533 Curtis Clark Dept. Biology Califomia Polytechnic Pomona, CA 91768
Dick Clark U.S. Army Corps of Engineers 650 Capitol Mall Sacramento, CA 95814 Ronilee Clark 1901 Spinaker Dr. Ventura, CA 93001 William Clark CWESA 1758 N. Academy Sanger, CA 93657 Duffy Clemons 9502 Fairbanks Ave. San Diego, CA 92123 Philip Scott Clemons ESD 7136 Cardinal Road Fair Oaks, CA 95628 Glen Clifton 910 Sanitarium Rd. Deer Park, CA 94576 Bob Coats Phillip Williams & Associates Pier 35, The Embarcadero San Francisco, CA 94133 Steven Cohan Rancho Santa Ana Botanical Garden 1500 North College Avenue Claremento, CA 91711 Dana Cole Jackson State Forest 802 N. Main Street Ft. Bragg, CA Mike Concannon CH2M Hill 2200 Powell Street Emeryville, CA 94608 Lincoln Constance Dept. Integrative Biology University of California Berkeley, CA 94720 Appendix B
Cynthia Copeland Dept. Environmental Mngmt., Solano Co. 601 Texas Street Fairfield, CA 94533 Toni Corelli 678 Perth Court Milpitas, CA 95035 Dave Comman Pacific Gas and Electric 123 Mission Street, #2159 San Francisco, CA 94105 Robin Cox The Nature Conservancy 785 Market Street, 3rd Floor San Francisco, CA 94103 Robin Crabill 345 Jersey St. San Francisco, CA 94114 James V. Crew California Department of Fish & Game 841 E. Scranton Porterville, CA 93257 Katherine Culligan 150 Woodland Way Piedmont, CA 94611 Katherine Cuneo Cuneo Environmental Planning 7 Poco Paso San Rafael, CA 94903 Michael Curto California Deparrnent of Parks & Recreation 8669 Verlane Drive San Diego, CA 92119 Paul Cylinder Jones & Stokes Associates, inc. 1725 23rd Street, Suite 100 Sacramento, CA 95816 Virginia Dains 3371 Ayres Holmes Road Auburn, CA 95603
Charlice Danielson 10 Kerr Ave. Kensington, CA 94707 Karen Danielson NPS - Channel Island NP 1901 Spinnaker Drive Ventura, CA 93001 William DaviUa Biosystems Analysis Inc. 303 Potrero Street, #29-203 Santa Cruz, CA 95060 Sidney W. Davis Davis 2, Consulting Earth Scientists P.O. Box 724 Georgetown, CA 95634 Bruce Dawson 555 Leslie Street Ukiah, CA 95482 Sally deBecker Pacific Gas and Electric Company 3400 Crow Canyon Road San Ramon, CA 94583 Mary DeDecker P.O. Box 506 Independence, CA 93526 Lauramay T. Dempster Jepson Herbarium University of California Berkeley, CA 94720 David Diaz U.S. Forest Service 630 Sansome Street San Francisco, CA 94111 Jim Dice 6066 Portobelo Ct. San Diego, CA 92124 Janet Diehl Trust for Public Land 82 2nd Street San Francisco, CA 94110 Appendix B
Kenneth M. DiVinorio Pacific Gas and Electric Company 3400 Crow Canyon Road SanRamon , CA 94583 Linda Dondanville UNOCAL Geothermal Corp. 2099 Range Avenue, Box 6854 Santa Rosa, CA 95406 Ms. Dondanville Greg Donovan P.O. Box 1152 Santa Ynez, CA 93460 Monica Dreibelbis CalTrans District 7 2520 3rd Street, #3 Santa Monica, CA 90405 Nancy Dubbs U.S. EPA 215 Fremont Street San Francisco, CA 94105 Anthony T. Dunn 6210 Callee Empinada San Diego, CA 92124 Wendie Duron 1063 Pierce Drive, #104 Clovis, CA 93612 John Edell CalTrans District #9 500 South Main Street Bishop, CA 93514 David Edelson Natural Resources Defense Council 25 Kearney Street San Francisco, CA 94108 Robert Edminster DFG-Los Banos Complex 18110 W. Henry Miller Avenue Los Banos, CA 93635
Steve Edwards Tilden Botanic Garden Berkeley, CA 94708 Jean Elder U.S. Army Corps of Engineers 650 Capitol Mall Sacramento, CA 95814 Tom Elias Rancho Santa Ana Botanic Garden 1500 North College Avenue Claremont, CA 91711 Bruce Eliason California Department of Fish & Game 245 W. Broadway, Suite 350 Long Beach, CA 90802 Bruce Elliot Deparmaent of Fish and Game 2201 Garden Road Monterey, CA 93940 Mary Jo Elpers U.S. Fish & Wildlife Service 5825 Creekside Avenue #2 Orange, CA 92669 Larry L. Eng Department offish and Game 2896 Candido Drive Sacramento, CA 95833 Michael Evans Tree of Life Nursery 33201 Ortega Highway P.O. Box 736 San Juan Capistrano, CA 92693 Phillis Faber California Native Plant Society 212 Del Casa Mill Valley, CA 94941 Reynaud Farve U.S. Bureau of Land Management 63 Natoma S_eet Folsom, CA 95630
Stan Farwig 1230 Almar St. Concord, CA 94518 Bill Ferlatte Rt. 1, Box 263D Montague, CA 96064 Jean Ferreira Cnlifomia Dept. Parks & Recreation 2211 Garden Road Monterey, CA 93940 Wayne Ferren Dept. Biological Sciences/Herbarium University of California Santa Barbara Santa Barbara, CA 93106 Wayne Fields Hydrozoology P.O. Box 682 Newcastle, CA 95658 Jeff Finn Department of Fish and Game 13515 Schooner Hill Road Grass Valley, CA 95945 Daniel Fira Santa Barbara County Planning 123 East Anapamu Street Santa Barbara, CA 93101 Ann Fisher Cornflower Farms P.O. Box 896 Sacramento, CA 95827 Steve Fiarmery Sacramento County Parks 4040 Bradshaw Road Sacramento, CA 95827 Doug Flesher Butte College 4841 Round Valley Road Paradise, CA 95969
Cal Fong U.S. Army Corps of Engineers 211 Main Street San Francisco, CA 94106 Holly Forbes Botanical Garden University of California Berkeley, CA 94720 Bruce Forman Sacramento Science Center/Jr. Museum 3615 Auburn Blvd. Sacramento, CA 95821 Steve Forman WESCO 14 Galli Drive, Suite A Novato, CA 94949 Eric Fomo Balance Hydrologics, Inc. 1760 Solano Ave, #209 Berkeley, CA 94707 Mike Foster P.O. Box 1336 Quincy, CA 95971 Leslie Friedman The Nature Conservancy 785 Market Street, 3rd Floor San Francisco, CA 94104 Marilynn Friley USFWS, Division of Ecological Services 2800 Cottage Way, Room E- 1803 Sacramento, CA, 95825 Joel Galbraith City of Santa Rosa P.O. Box 1678 Santa Rosa, CA 95402 Roman Gankin 1525 Regent St., Apt. 5 Redwood City, CA 94061 Carl Geldin-Mayer 1649 Church Rd. McKinleyville, CA 95521 Appendix B
Jim Gibson Consultant 8291 Caribbean Way Sacramento, CA 95826
Dan Gifford Depatialient of Fish and Game 1701 Nimbus Road Rancho Cordova, CA 95670 Valerie Giz'mski California Department of Parks & Recreation 3033 Cleveland Avenue, Suite 110 Santa Rosa, CA 95401 Bernard H. Goldner Santa Clara Valley Water DisMct 5750 Alamaden Expressway San Jose, CA 95118 Cay Goude U.S. Fish and Wildlife Service 2800 Cottage Way, Room E-1823 Sacramento, CA 95825 Steve Granholm LSA 157 Park Place Pt. Richmond, CA 94801 John Gray Dames & Moore 175 Cremona Drive Goleta, CA 93117 Jim Griffin Hasting Natural History Reservation Star Route, Box 80 Carrnel Valley, CA 93924 Tom and Mary Ann Griggs The Nature Conservancy 7100 Desmond Road Gait, CA 95632 Alan Grundman Jasper Ridge Biological Preserve Stanford University Stanford, CA 94305-5020
Hector Guerro Tulare County Planning County Civic Center Visalia, CA 93291 Jack and Betty Guggolz California Native Plant Society 1123 Palomino Road Cloverdale, CA 95425 Laren Hall Dept. Recreation San Diego State University San Diego, CA 92181 J.R. Hailer Dept. Biological Sciences University of California Santa Barbara, CA 93106 William Halvorson Channel Island National Park 1901 Spinnaker Drive Ventura, CA 93001 Michael Hamilton UC James San Jacinto Mtms. ReServe P.O. Box 1775 Idyllwidl, CA 92349 Linnea Hanson 875 Mitchell Ave. Oroville, CA 95965 Rick Hanson URS Corporation 501 J Street Sacramento, CA 95814 Nancy Harrison 1150 Wild Rose Dr. Santa Rosa, CA 95401 Sandy Harrison California Department of Parks & Recreation 730 S. Beckman, Box 1450 Lodi, CA 95241-1450
NellHavlik Solano County Farmlands & Open Space Foundation 1000 Webster Street Fairfield, CA 94533 Barry Hecht Balance Hydrologics, Inc. 1760 Solano Avenue, Suite 209 Berkeley, 94707 Larry Heckard Jepson Herbarium University of California Berkeley, CA 94720 Kristi Hein Pacific Gas and Electric Company 123 Mission Street, #2159 San Francisco, CA 94105 Larry Hendrickson California Native Plant Society P.O. Box 155 Julian, CA 92036 Mary Ann Henry 329 Purdew Ridgecrest, CA 93555 Tom Hesseldenz P.O. Box 409 McCloud, CA 96057 Diana Hickson WESCO 14 Galli Drive, Suite A Novato, CA 94949 Brian Hoffman EIP Associates 1311 I Street, Suite 200 Sacramento, CA 95814 B. Demar Hooper Holliman, Hackard & Taylor 1545 River Park Drive, Suite 550 Sacramento, CA 95815 Doris A. Hoover 4773 Abargo St. Woodland Hills, CA 91364
Natalie Hopkins 906 Elizabeth St., Drawer E Alviso, CA 95002 Barbara Hopper Box. 783 Kenwood, CA 95452 Alice Howard 6415 Regent Street Oakland, CA 94618 Terry Huffman Huffman & Associates, Inc. 69 Aztec Street San Francisco, CA 94110 Thomas Huffman City of San Diego Planning Department 202 "C" Street, MS 5A San Diego, CA 92101 Dave Imper 4612 Lentell Rd. Eureka, CA 95501 Gerda Isenberg Yerba Buena Nursery 19500 Skyline Blvd. Woodside, CA 94062 Dave Isle USFS Stonyford Station HC-1, Box 12 Stoneyford, CA 95979 Diana Jacobs State Lands Commission 1807 13th Street Sacramento, CA 95814 Lawrence Janeway P.O. Box 411 Chico, CA 95927 Tom Jimerson 507 "F" Street Eureka, CA 95501
Bennett Johnston Trust for Public Land 116 New Montgomery Street, 4th Floor San Francisco, CA 94105 Jim Jokerst Jones & Stokes Associates, Inc. 1725 23rd Street, Suite 100 Sacramento, CA 95816 H. Lee Jones Michael Brandman & Associates 4918 No. Harbor Drive, Suite 205-A San Diego, CA 92106 Robert Jones Earthcraft Planning Services 1540 Talrnage Road Ukiah, CA 95482 Eric H. Jonsson 5148 Elnire Place San Diego, CA 92117 Michael Josselyn Dept. Biology San Francisco State University San Francisco, CA 94132 Paul Jorgensen P.O. Box 645 Point Arena, CA 95468 Steve Junak Santa Barbara Botanic Garden 1212 Mission Canyon Rd. Santa Barbara, CA 93105 Holly Keeler City of Sacramento Planning 1231 1 Street Sacramento, CA 95814 Charles Keene California Department of Water Resources 120 S. Spring Street Los Angeles, CA 90012
David B. Kelley Consulting Plant Ecologist 216 F Street, No. 51 Sacramento, CA 95616 Joanne Kerbavaz 1004 Cypress Ln. Davis, CA 95616 Harlan Kessel 376 Bellevue Ave. Oakland, CA 94610 Laurie Kiguchi 304 Park Way Santa Cruz, CA 95060 Holman E. King Dept. Fish & Game 4728 Jimbo Court Denair, CA 95316 Karen Kirtland 1 Park Plaza, Suite 500 Irvine, CA 92714 Doug Kleinsmith U.S. Bureau of Reclamation 2800 Cottage Way, Room W-2103 Sacramento, CA 95825 Walter Knight 1513 Royal Oak Dr. Petaluma, CA 94952 Monti Knutsen USFWS, Endangered Species Office 2800 Cottage Way, Room E- 1823 Sacramento, CA 95825 Robin S. Kohn Holliman, Hackard & Taylor 1545 River Park Drive, Suite 55 Sacramento, CA 95815 Maribeth Kotn_an USDA Forest Service 3348 Alpine Blvd. Alpine, CA 92201
Karla Kramer USFWS, Endangered Species Office 2800 Cottage Way, Room E- 1823 Sacramento, CA 95825 Tim Krantz Big Bear Valley Preserves P.O.Box6154 Big Bear Lake, CA 92315 Tom Kubik Placer County Planning Division 11414 B Avenue Auburn, CA 95603 Laura Kuh Ott Water Engineers Inc. 2334 Washington Ave. Redding, CA 96001 loyce Lacy Depaa'unent of Water Resources 2440 Main Street Red Bluff, CA 96080 Kris Lal Department of Fish and Game, Region 5 330 Golden Shore, Suite 50 Long Beach, CA 90802 • Larry LaPre Tierra Madre Consultants 4178 Chesmut St. Riverside, CA 92501 June Latting 320 Maravilla Drive Riverside, CA 92507 Robert Leidy U.S. Environmental Protection Agency 215 Fremont Street San Francisco, CA 94105 Barbara M. Leimer Leimer Biological Consulting 5944 Taft Avenue Oakland, CA 94618
Veda Lewis California Departa_ent of Transportation P.O. Box 7310 San Francisco, CA 94120 R.John Little Envirosphere Company 555 Capitol Mall, Suite 625 Sacramento, CA 95814 Priscilla Locke Woodward-Clyde Consultants 100 Spear Street, Suite 425 San Francisco, CA 94105 Maggie Loy San Diego Department of Public Works 5555 Overland Ave., Bldg. 2/156 San Diego, CA 92123 Kathleen Lyons Habitat Restoration Group 6001 Buffer Lane, #1 Scotts Valley, CA 95066 Richard A. Macedo Departmento of Fish & Game 6515 Estates Court Kelseyville, CA 95451 Joe Madeiros Great Valley Museum of Natural History 1100 Stoddard Avenue Modesto, CA 95350 Tony Magennis Lefkas/West Placer County Citizens Committee P.O. Box 1075 Rocklin, CA 95677 Jack Major Dept. of Botany University of California Davis, CA 95616 Michael Marangio Harvey & Stanley Associates 6001 Butler Lane, Suite I Scotts VaUey, CA 95066
Laurie Marcus State Coastal Conservancy 1330 Broadway, Suite #1100 Oakland, CA 94612 Craig Martz CalTrans 950 Howe Avenue Sacramento, CA 95825 Mark Matthias Jones & Stokes Associates, Inc. 1725 23rd Street, Suite 100 Sacramento, CA 95816 John D. Mayer Department of Planning, Modesto 1100 H Street Modesto, CA 95355 Joe McBride Depa_ ttt_ent of Forestry & Resource Management University of California Berkeley, CA 94720 Steve McCabe U.C. Santa Cruz Arboretum 205 Morningside Dr. Ben Lomand, CA 95005 NiaU McCarten Department of Integrative Biology University of California Berkeley, CA 94720 Elizabeth McClintoek 1335 Union St. San Francisco, CA 94109 Michael McElligott Vandenberg Air Force Base 4016 Altair Place Lompoc, CA 93436 Malcolm McLeod 2122 Loomis St. San Luis Obispo, CA 93401
Dale McNeal Department of Biology University of the Pacific Stockton, CA David Mayfield San Diego Parks & Recreation 5201 Ruffin Road, Suite P San Diego, CA 92123 Jerry Meral Planning & Conservation 909 12th Street Sacramento, CA 95814
Tim Messick Jones & Stokes Associates, Inc. 1725 23rd Street, Suite 100 Sacramento, CA 95816 Ken Milam Sonoma County Planning Director 575 Administration Drive, Room 105A Santa Rosa, CA 95403 Connie Millar U.S. Forest Service Pacific Southwest Forest & Range Experiment Box 245 Berkeley, CA 94701
Diane Mitchell J & M Land Restoration 3826 Bryn Mawr Drive Bakersfield, CA 9330 Maynard Moe Dept. Biology California State University Bakersfield, CA 93111-1099 Sharon Moreland U.S. Army Corps of Engineers 211 Main Street, Atm: Regulatory Branch San Francisco, CA 94105 Sia Morhardt EA Engineering Science & Technology 41A Lafayette Circle Lafayette, CA 94549
Gilbert Muth Biology Department Pacific Union College Angwin, CA 94508 Mona Myatt Southern California Edison P.O. Box 800, Rm. 427 GC1 Rosemead, CA 91770 Rodney Myatt Dept. Biology San Jose State University San Jose, CA 95192 Jim Nelson State Energy Resources Conservation & Development 1516 Ninth Street, MS 40, 4th Floor Sacramento, CA 95814 Gall Newton Division of Mines & Geology 650-B Bercut Drive Sacramento, CA 95819 Larry Norris USDA, Soil Conservation Servicb 4700 Northgate Blvd._ Suite 015 Sacramento, CA 95814 Patti Novak Los Angeles Department of Water & Power 873 N. Main Bishop, CA 93514 Tom Oberbauer 3739 Oleander St. San Diego, CA 92106 Steven Orr Nature Landscapes 12545 Quito Rd. Saratoga, CA 95070 Rexford Palmer Palmer Honeysett Consulting Route 2 Box 660 • Dixon, CA 95620
V.T. Parker Department of Biology San Francisco State University San Francisco, CA 94132 David Parsons Sequoia & Kings Canyon National Parks Three Rivers, CA 93271 Cam Patterson RECON 1276 Moreno Blvd. San Diego, CA 92110 Charlie Patterson Consultant 7573 Terrace Drive E1 Cerrito, CA 94530 Bruce Pavlik Biology Department Mills College Oakland, CA 94613 Doug Peterson Sacramento County Environmental 827 Seventh Street, Room 220 Sacramento, CA 95814
Taylor Peterson Thomas Reid Associates P.O. Box 872 Palo Alto, CA 94302 Ralph Philbrick Santa Barbara Botanic Garden 1212 Mission Canyon Rd. Santa Barbara, CA 93105 Bob Powell 1306 Toyon Place Davis, CA 956616 Genevieve Prlain Oakland Museum Natural Science I000 Oak Street Oakland, CA 94607
Denyse Racine California Depat a.ent of Fish & Game 3346 Herman Avenue San Diego, CA 92104 Stephen P. Rae Department of Fish & Game 1130 Cayetano Court Napa, CA 94559 John Ranlett Sugnet & Associates 8265 Kingsley Court RoseviUe, CA 95661 Debbie Raphael USFS Angeles National Forest Saugas 30800 Bouquet Canyon Road Saugas, CA 91350 Ron Rempel Department of Fish & Game 4449 East Stetson Clovis, CA 93612 Royce Riggins RBR & Associates 233 "A" Street, Suite 804 San Diego, CA 92101 Larry Riggs GENREC 3828 Everett Ave Oakland, CA 94602 Fred Riley 2933 Eastern Avenue Sacramento, CA 95821 EllenRognas San Luis Obispo Planning Department Government Center Room 370 San Luis Obispo, CA 93408 Alan Romspert Desert Studies 605 N. Pomona Avenue FuUerton, CA 92632
Peter Rowlands P.O. Box 427 Death Valley, CA 92328 Peter Rubtzoff 1678 25th Avenue San Francisco, CA 94122 Gary Ruggerone CalTrans 1449 Hollister Lane Los Osos, CA 93402 Bill Ruskin P.O. Drawer F-2 Felton, CA 95018 Jake Ruygt 3549 Willis Dr. Napa, CA 94558 Bill Sacks P.O. Box 4215 San Luis Obispo, CA 93403 Theodore St. John Mycorrhizal Services 28285 Bundy Canyon Road Menfee, CA 92355 Andy Sanders 422 Campus View Riverside, CA 92507 Randy Sater Teichert Aggregates P.O. Box 15002 Sacramento, CA 15002 John Sawyer 2731 Greenbriar Land Arcata, CA 95521 Carla Scheidlinger P.O. Box 1176 Mammoth Lakes, CA 93546 Suzanne Schettler Hastings Natural History Reservation Star Route, Box 80 Carmel Valley, CA. 93924 Appendix B
Robert Schlising Department of Biology California State University Chico, CA 95929 Rob Schonholtz Larry Seeman Associates, Inc. 157 Park Place Pt. Richmond, CA 94801 Gary Schoolcraft U.S. Bureau of Land Management 2545 Riverside Drive Susanville, CA 96130 Roger E. Scoonover Department of Fish & Game 753 Pendegast Circle Woodland, CA 95695 Peter Schuyler The Nature Conservancy 525 Lorraine Avenue Santa Barbara, CA 93110 Melvin Schwartz 661 Riverlake Way Sacramento, CA 95831 Michael E. Scott U.S. Navy Public Works Dept. (code 183E) San Diego, CA 92145 Clif Sellers City of Chico Planning Office P.O. Box 3420 Chico, CA 95927 Merrily Severance U.S. Navy, Engineering 1220 Pacific Highway San Diego, CA 92132
Field Activity, SW, Code 243
Kevin Shea East Bay Regional Park District 11500 Skyline Blvd. Oakland, CA 94619
Jim U.S. 630 San
Shevock Forest Service, Region 5 Sansome Street Francisco, CA 94111
Marie A. Simovich Biology Depamnent University of San Diego San Diego, CA 92110 Joanne Sorenson Jones & Stokes Associates, Inc. 1725 23rd Street, Suite 100 Sacramento, CA 95816 James P. Smith, Jr. 193 13th St. Arcata, CA 95521 JoAnne Smith J.A. Biological Services 739 Hawthorne Avenue El Cajon, CA 92020 Susan Smith 1730 A Jones St. San Francisco, CA 94109 Susan Sommers 879 Roble #2 Menlo Park, CA 94025 Linda Spahr 3615 Brook Street Lafayette, CA 94549 Connie Spenger , 1318 East Glenwood Fullerton, CA 92631 Fred T. Sproul Pacific Southwest Biological 14353 Mussey Grade Road Ramona, CA 92065
Jack Spruill California Deparmaent ofFish & Game 8621 Doremore Dr. Huntington Beach, CA 92646
John Stebbins 357 Adler Clovis, CA 93612 Bobbie Steele CalTrans P.O. Box 85406 San Diego, CA 92138 Dale Steele 1976 E. Charter Way Stockton, CA 95206 Kingsley Stern Department of Biology California State University Chico, CA 95929 Joan Stewart 4996 Mt. Almagosa Dr. San Diego, CA 92111 Jon Mark Stewart The Living Desert 47900 Portola Ave. Palm Desert, CA 92260 Douglas Stone Biosystems Analysis, Incorporated 303 Potrero St., #29-203 Santa Cruz, CA 95060 Mark Stopher CalTrans 5340 Pirnlico Avenue Sacramento, CA 95841 Larry Stromberg Consulting Plant Ecologist 1048 Santa Fe Avenue Albany, CA 94706 Paul Sugnet Sugnet & Associates 8265 Kingsley Court Roseville. CA 95661 John Sully California Depaa'ta.ent of Transportation 120 S. Spring Street Los Angeles, CA 90012 Appendix B
Karen Swirsky Michael Brandman Associates 4918 North Harbor Drive, Suite 205-A SanDiego,CA 92106 Barbara Talley CalTrans, Office of Environmental 650 Howe Avenue, Suite 400 Sacramento, CA 95825
Karen Tatanish Sonoma State Botanical Garden 11529 Bodega Hwy. Sebastopol, CA 95472 Dean Taylor Biosystems Analysis, Inc. 303 Potrero, Suite 29-203 Santa Cruz, CA 95060 Sherry Teresa California Dept. offish and Game 5841 Primrose Ave. Temple City, CA 91780 Greg Tholen Sacramento County Planning Department 827 7th Street, Room 230 Sacramento, CA 95814 Terri Thomas Golden Gate National Recreation Area Ft. Mason, Bldg. 201 San Francisco, CA 94123 Timothy Thomas National Park Service 22900 Ventura Blvd., Suite 140 Woodland Hills, CA 91364 John Thompson U.S. Air Force 11654 Buckeye Circle Penn Valley, CA 95946 Laura Thompson U.S. Forest Service Tulelake Ranger Station, P.O. Box 369 Tulelake, CA 96134
Rocky Thompson Curcurt Riders Productions 9619 Old Redwood Hwy. Windsor, CA 95492 Robert Thome Rancho Santa Aria Botanic Garden 1500 North College Claremont, CA 91711 Charlie Turner 1050 San Pablo Avenue Albany, CA 94706 Zoe Tyler U.S. Forest Service 100 Forni Rd. Placerville, CA 95667 Wayne Tyson Land Restoration Associates 2456 Broadway San Diego, CA 92101 Julie Vanderweir Mooney Lettieri & Associates 9903 Business Park Avenue San Diego, CA 92131 Ricardo Villasefior EIP 319 llth. Street San Francisco, CA 94103 Larry Vinzant U.S. Army Corps of Engineers, Atm: Regulatory 650 Capitol Mall Sacramento, CA 95814
Marco Waaland Golden Bear Biostudies 2727 Canterbury Drive Santa Rosa, CA. 95405 Connie Wade Wade Associates 735 Sunrise Avenue, Suite 145 Roseville, CA 95678
Gary Wallace 900 Exposition Blvd. Los Angeles, CA 90007 SallyWaiters CalTrans Environmental P.O. Box 1976 Stockton, CA 95201 Ruth Wattling The Living Desert P.O. Box 1775 Palm Desert, CA 92261 Nancy Weintraub Western Area Power Administration 1825 Bell Street, Suite 105 Sacramento, CA 95821 Stuart Weiss Center for Conservation Biology Department of Biological Studies, Stanford University Stanford, CA 94305 Mary Wells 684 Benicia Dr., Apt. 15 Santa Rosa, CA 95405 Barbara Wendt City of Sacramento Planning Department 1231 I Street, Suite 300 Sacramento, CA 95814 Phil Wendt California Dept. Water Resources 1416 Ninth Street P.O. Box 942836 Sacramento, CA 94236-0001 Frank Wemette Department of Fish & Game 4001 North Wilson Way Stockton, CA 95205 Grant Werschkull EIP Associates 1311 I Street, Suite 200 Sacramento, CA 95814
Dale Whitmore Department of Fish & Game 1263 Nadene Drive Marysville, CA 95901 Howie Wier Michael Brandman Associates, Inc. 4918 North Harbor Drive, Suite 205-A San Diego, CA 92106 Carl Wilcox Department of Fish & Game P.O. Box 47 Yountville, CA 94599 Ron Wilkinson 116 McKee St. Ventura, CA 93001 Barbara Williams Klamath National Forest 1312 Fairlane Road Yreka, CA 96097 John Willoughby U.S. Bureau of Land Management 2800 Cottage Way Sacramento, CA 95825 Jim Wilson 5616 Schatz Lane Rocldin, CA 95677 Tamara Wilton • U.S. Forest Service Star Route Box 300 Bridgeville, CA 95526 Steve Windowski LTBMU P.O. Box 8465 South Lake Tahoe, CA 95731 Ted Winfield ENTRIX, Inc. 2125 Oak Grove Rd., Suite 300 Walnut Creek, CA 94598
Carl Wishner ENVICOM Corporation 4674 Park Granada, #202 Calabasas, CA 91302 Charles G. Wolfe Kleinfelder 2121 North California Blvd., Suite 570 Walnut Creek, CA 94596 Roy Woodward Department of Parks & Recreation, OHMVR 1416 Ninth Street Sacramento, CA 95814 Patty Worthing Naval Facilities, Western Division, Atm: Code 1835PW P.O. Box 727 San Bruno, CA 94066 Jack Wright USDA Soil Conservation Service 65 Quinta Court, Suite C Sacramento, CA 95823 Walt Wright 326 Redwood Ave. Brea, CA 92621 Robert Wunner Redwood Community Action Agency 1567 Central Agency McKinleyville, CA 95521 Nancy Wymer Wymer & Associates P.O. Box 2018 Citrus Heights, CA 95661 Dr. Vernal Yadon 165 Forest Avenue Pacific Grove, CA 93950 Ann Yoder CNPS Bristlecone Pine Chapter P.O. Box 330 Lone Pine, CA 93545
Mike Yoder-Williarns Williams Enterprises 1914 North 34th Street, Suite 411 Seatde, Washington 98103 Leslie Zander Harding - Lawson & Associates 7655 Redwood Blvd., P.O. Box 578 Novato, CA 94948 Jack Zaninovich Rt. 2, Box 708 Delano, CA93215 Paul Zedler Depat'unent of Biology San Diego State University San Diego, CA 92182 John Zenter Zenmer & Zentner 925 Ygnacio Valley Road, #250 Walnut Creek, CA 94596
PERSONS RESPONDING TO QUESTIONNAIRE AND SUMMARY RESPONSES
C. Persons Responses
Person and/or Lowell Ahart Oroville, CA
Bob Allen Larkspur, CA
David Amme Berkeley, CA
Joseph Aparicio Biology Department American River College Sacramento, CA
Wayne Armstrong Department of Biology Palomar College SanMarcos, CA
Mike Baad Department of Biological Sciences California State University Sacramento, CA
Balance Hydrologics Berkeley, CA [Contact:BarryHecht]
1Never involved refers to the non-involvement of the person, agency or specific branch thereof, in a mitigation-related transplantation, relocation, or reintroduction of a state-listed endangered, threatened or rare species. The party may have been involved in the transplantation of a state- or federally-listed rare, endangered or threatened species, but the project was not related to mitigation. 2Mr. Amme reported that he had developed a restoration plan for the Alameda manzanita (Arctostaphylos pallida) for the East Bay Regional Park District, but it was never implemented. Appendix C
Ellen Bauder Dept. Biological Sciences San DiegoStateUniversity
R.W. Benseler Dept. Biological Sciences California State University Hayward, CA
Albin Bills Department of Biology Butte College Oroville, CA
Charles Black DepartmentofBiology CalifomiaStateUniversity San Diego, CA
7Mr. Ruggerone sent information on the transplantation work on federal candidate species Circium occidentale var. compactum in two projects, Little Pico Bridge replacement and the Piedras Blancas shoulder widening. 8Neither of these species is state-listed, but Eriophyllum mohavense criteria. Opuntia basilaris ssp.treleasei is a "candidate" for state listing. Appendix C
Califomia Native Plant Society Dorothy King Young Chapter Gualala, CA
California State Food and Agriculture Sacramento, CA [Contact:DougBarbe]
Joe Callizo St.Helena,CA
City of Chico Planning Office Chico, CA [Contact:CliffSellers]
Curcurt Riders Productions Windsor, CA [Contact:RockyThompson]
Katherine Culligan Piedmont, CA
Michael Curto Califomia Deparment of Parks & Recreation SanDiego,CA
CWESA Sanger, CA [Contact:CurtUptain]
Dames & Moore Goleta, CA [Contact: JohnGray]
Mary DeDecker Independence, CA
LauraMay Dempster Jepson Herbarium University of California Berkeley, CA
'. Never Involved
9Mr. Thompson sent information lanuginosum ssp. thermale.
on a research
t0Mr. Curto is no longer with CDPR, and sent personal work with rare plant species.
Fullerton, CA [Contact: Alan Romspert]
Wendie Duron Clovis, CA
EA Engineering Science & Technology Lafayette, CA [Contacts: Sia Morhardt & R. Douglas Stone]
East Bay Regional Park District Oakland, CA [Contact:KevinShea]
EIP Associates Sacramento, CA [Contact:BrianHoffman]
Envicom Corporation Calabasas, CA [Contact:CarlWishner]
Envirosphere Co. Culver City, CA [Contact:DavidBradford]
Phyllis Faber MillValley, CA
Roman Gankin Redwood City,CA
GENREC Oakland, CA [Contact:LarryRiggs]
Betty & Jack Guggolz Cloverdale, CA
GW Consulting Engineers Citrus Heights, CA [Contact:JerryAnders]
Nancy Harrison Dept. Life Sciences Santa Rosa Junior College SantaRosa,CA
11Mr. Shea sent non-mitigation related information on Amsinkia grandiflora conducted in the EBRPD. Appendix C
Larry Heckert Jepson Herbarium Universityof Califomia Berkeley, CA
Cordylanthus palmatus Castilleja uliginosa
MaryAnnHenry Ridgecrest, CA
DorisA.Hoover Woodland Hills, CA
Barbara Hopper Kenwood, CA
Hydrozoology Newcastle, CA [Contact:WayneFields]
J & M Land Restoration Bakersfield, CA [Contact:DianeMitchell]
Dave Keil Depatia.ent of Biological Sciences California Polytechnic Institute ' SanLuisObispo,CA
David B. Kelley Sacramento, CA
12Ms. Henry sent comments potentially threatened.
13Never involved in a transplantation, reintroduction but sent information on non-mitigation-related restoration minthornii and Dudleya cymosa ssp. marcescens Appendix C
or relocation project, project for Hemizonia
Kleinfelder Walnut Creek, CA [Contact:CharlesG. Wolfe]
• L & M Land Restoration Bakersfield, CA [Contact: DianeMitchell]
Leimer Biological Consulting Oakland, CA [Contact: Barbara Leitner]
The Living Desert Palm Desert, CA [Contact:JonMarkStewart]
Los Angeles Department of Water & Power Bishop, CA [Contact: PattiNovak]
Joe McBride Department of Forestry & Resource Management University of California,Berkeley
Niall McCarten Depa_a_ent of Integrative Biology University of California, Berkeley,
Elizabeth McClintock SanFrancisco, CA
Malcolm McLeod Dept. Biological Sciences California Polytechnic Institute SanLuisObispo,CA
Dale McNeal Dept. of Biology University of the Pacific Stockton, CA
Jack Major Dept. of Botany Universityof California,Davis
Jerry Meral Pianning& Conservation Sacramento, CA
Rhonda & Carl Meyers McKinleyville, CA Appendix C
Maynard Moe Dept. Biology California State University Bakersfield, CA
Gilbert Muth Biology Department Pacific Union College Angwin, CA
Mycorrhizal Services Menifee, CA [Contact:TheodoreSt. John]
Pacific Gas and Electric Company Department of Efigineering Research San Ramon, CA [Contact:SallydeBecker]
Pacific Gas and Electric Company San Francisco, CA [Contact: Frank Chan; Ken DiVittorio]
Pacific Southwest Biological Services, Inc. National City, CA [Contact:MitchelBeauchamp]
V.T. Parker Department of Biology SanFranciscoStateUniversity
CharliePatterson E1 Cerrito, CA
Lasthenia burkei, Blennosperma bakeri
Phiilip Williams & Associates San Francisco, CA [Contact: BobCoats]
PlacerCounty Community Development Dept. Auburn, CA [Contact:ThomasKubik]
Planning Associates Redding, CA [Contact: DonBurke]
tenuis. Appendix C
Stern at Chico State regarding
Bob Powell Davis, CA
Rancho Santa Aria Botanical Garden Claremento, CA [Contact:OrlandoMistretta]
Thomas Reid Associates Palo Alto, CA [Contact:TaylorPeter_on]
Peter Rubtzoff SanFrancisco, CA
Jake Ruygt Napa,CA
City of Sacramento Planning Dept. Sacramento, CA [Contact:HollyKeeler]
Sacramento County Dept. of Parks and Recreation Sacramento, CA [Contact:SteveFlannery]
Sacramento County Environmental Impact Section [Contact:DougPeterson]
15Provided nursery stock of Pentachaeta lyonii to Envicom Corporation, Acanthomintha ilicifolia to ERCE, Cercocarpus traskiae to the Catalina Island • Conservancy, and Eriastrum densifolium ssp. sanctorum to the U.S. Bureau of Land Management. 16Firm was not involved in any transplantation, reintroduction or relocation projects for State-listed species, but did devise a p!an for Castilleja neglecta that was never implemented due to project postponement. 17Ms. Keeler recommended contacting regarding the Laguna Creek Project. Appendix C
Sacramento County Planning Department [Contact:RobertBurness]
City of San Diego [Contact: Keith A. Greer]
Monardella linoides ssp. viminea; Eryngium at:istulatum var. parishii18
San Diego Depar anent of Public Works San Diego, CA [Contact: MaggieLoy]
Santa Barbara County Santa Barbara, CA [Contact: John Storrer]
Hemizonia increscens ssp. villosa
Cityof SantaRosa [Contact:DenisePeters]
Responded; seeSonoma CountyPlanningDept.
John Sawyer Biology Department HumboltStateUniversity Arcata, CA
Erysimummenziesii Lilium occidentale
Marie Simovich Biology Department Universityof SanDiego
James P. Smith, Jr. Dept. Biological Sciences Humbolt StateUniversity Arcata, CA
The Nature Conservancy San Francisco, CA [Contact: Robin Cox & Lesfie Friedman]
The Nature Conservancy Santa Barbara, CA PeterSchuyler
Tierra Madre Consultants Riverside, CA [Contact:LarryLaPre]
is no longer
with The Nature
20Tierra Madre Consultants is planning projects that involve the mitigation-related manipulation of Brodiaea filifolia and Eriastrum densifolium ssp. sanctorum. Appendix C
Tree of Life Nursery San Juan Capistrano,CA [Contact: Mike Evans]
Trust For Public Land San Francisco, CA [Contact:BennettJohnston]
Tulare County Planning Visalia, CA [Contact:HectorGuerro]
Tuolumne County Planning Dept. Sonora, CA [Contact:JohnAnderson]
U.S. Army Corps of Engineers Sacramento, CA [Contact:LarryVinzant]
U.S. Bureau of Land Management Arcata,CA [Contact: Carol Tyson & Steve Hawks]
U.S. Bureau of Land Management Folsom, CA [Contact:D.K.Swickard]
U.S. Department of Energy Sacramento, CA [Contact: No name forwarded on questionnaire]
U.S. Bureau of Land Management Riverside, CA [Contact: Gerald Hiliier & Connie Rutherford]
U.S. Bureau of Land Management S usanville, CA [Contact:Gary Schoolcraft]
2tMr. Evans forwarded a list of rare, endangered and threatened plants handled by Tree of Life Nursery. State-listed species include: Acanthomintha ilicifolia, Arctostaphylos imbricata, Brodiaea filifolia, Ceanothus heastiorum, Ceanothus maritimus, Eriastrum densifolium ssp. sanctorum, Eriogonum crocatum, Fremontodendron mexicanum, Hemizonia minthornii, Mahonia nevinii, Malacothamnus clementinus, and Monardella linoides ssp. viminea. Appendix C
U.S. Bureau of Land Management Ukiah,CA [Contact:PardeeBardwell]
Arabis macdonaldiana Contractedwith M. Baad
U.S. Fish and Wildlife Service San Francisco Bay Wildlife Refuge Complex Newark, CA [Contact: Joy Albertson]
U.S. Forest Service Alpine, CA [Contact: Maribeth Kottman]
U.S. Forest Service Klamath National Forest Yreka, CA [Contact:BarbaraWilliams]
U.S. Forest Service Lake Tahoe Basin Mgmt. Unit S. Lake Tahoe, CA [Contact:HelenSoderberg]
U.S. Forest Service Modoc National Forest Tulelake, CA [Contact:LauraThompson]
U.S. Forest Service Pacific Southwest Forest & Range Experiment Berkeley, CA [Contact:ConnieMillar]
U.S. Forest Service Six Rivers National Forest Eureka,CA [Contact: Dave Imper]
Bensoniella oregana,Oenothera wolfii
U.S. National Park Service Channel Island NP Ventura, CA [Contact: Karen Danielson & William Halvorsen]
22Never involved in a mitigation-related transplantation, reintroduction or relocation project, but mentioned that the USFS had reintroduced Rorippa subumbellata three historic locations. No additional information was received. Appendix C
U.S. National Park Service Golden Gate National Recreation Area San Francisco, CA [Contact: Terri Thomas]
Arctostaphylos hookeri var. ravenii
U.S. National Park Service Yosemite National Park Yosemite, CA [Contact:SusanBuis]
U.S. National Park Service Monterey, CA [Contact:RobertBranson]
U.S. Navy Public Works Dept. San Diego, CA [Contact:MikeE. Scott]
U.S. Soil Conservation Service Sacramento, CA [Contact:JackWright]
University of California Botanical Garden Berkeley, CA [Contact:HollyForbes]
University of California Hastings Natural History Reservation Cannel Valley, CA [Contact:SusanSchettler]
University of California James San Jacinto Mtms. Reserve Idyllwild, CA [Contact:MichaelHamilton]
University of California Natural Reserves System Oakland, CA [Contact:NordenH. Cheatham]
WESCO Novato, CA [Contact:DianeHickson]
Western Area Power Administration
Z3Mr. Scott recommended Appendix C
contacting Zenmer and Zentner regarding Miramar. 15
Sacramento, CA [Contact:NancyWeina-aub]
Williams Enterprises, Inc. Seattle, WA [Contact:MikeWilliams]
Vernal Yadon PacificGrove,CA
Yolo County Resource Conservation Winters, CA [Contact:JohnAnderson]
PaulZedler Department of Biology SanDiegoStateUniversity
Susceptibility of Common and Rare Plant Species to the Genetic Consequences of Habitat Fragmentation OLIVIER HONNAY∗ AND HANS JACQUEMYN† ∗
University of Leuven, Biology Department, Laboratory of Plant Ecology, Kasteelpark Arenberg 31, B-3001 Heverlee, Belgium, email [email protected] †University of Leuven, Division of Forest, Nature and Landscape Research, Celestijnenlaan 200E, B-3001 Heverlee, Belgium
Abstract: Small plant populations are more prone to extinction due to the loss of genetic variation through random genetic drift, increased selfing, and mating among related individuals. To date, most researchers dealing with genetic erosion in fragmented plant populations have focused on threatened or rare species. We raise the question whether common plant species are as susceptible to habitat fragmentation as rare species. We conducted a formal meta-analysis of habitat fragmentation studies that reported both population size and population genetic diversity. We estimated the overall weighted mean and variance of the correlation coefficients among four different measures of genetic diversity and plant population size. We then tested whether rarity, mating system, and plant longevity are potential moderators of the relationship between population size and genetic diversity. Mean gene diversity, percent polymorphic loci, and allelic richness across studies were positively and highly significantly correlated with population size, whereas no significant relationship was found between population size and the inbreeding coefficient. Genetic diversity of self-compatible species was less affected by decreasing population size than that of obligate outcrossing and self-compatible but mainly outcrossing species. Longevity did not affect the population genetic response to fragmentation. Our most important finding, however, was that common species were as, or more, susceptible to the population genetic consequences of habitat fragmentation than rare species, even when historically or naturally rare species were excluded from the analysis. These results are dramatic in that many more plant species than previously assumed may be vulnerable to genetic erosion and loss of genetic diversity as a result of ongoing fragmentation processes. This implies that many fragmented habitats have become unable to support plant populations that are large enough to maintain a mutation-drift balance and that occupied habitat fragments have become too isolated to allow sufficient gene flow to enable replenishment of lost alleles.
Keywords: genetic diversity, habitat fragmentation, inbreeding, mating system, population size Susceptibilidad de Especies de Plantas Comunes y Raras a las Consecuencias Gen´eticas de la Fragmentaci´ on del H´abitat
Resumen: Las poblaciones peque˜nas de plantas son m´as propensas a la extinci´on debido a la p´erdida de variaci´ on gen´etica por medio de la deriva g´enica aleatoria, el incremento de autogamia y la reproducci´ on entre individuos emparentados. A la fecha, la mayor´ıa de los investigadores que trabajan con erosi´ on gen´etica en poblaciones fragmentadas de plantas se han enfocado en las especies amenazadas o raras. Cuestionamos si las especies de plantas comunes son tan susceptibles a la fragmentaci´ on del h´ abitat como las especies raras. Realizamos un meta an´ alisis formal de estudios de fragmentaci´ on que reportaron tanto tama˜ no poblacional como diversidad gen´etica. Estimamos la media general ponderada y la varianza de los coeficientes de correlaci´ on entre cuatro medidas de diversidad gen´etica y de tama˜ no poblacional de las plantas. Posteriormente probamos si la rareza, el sistema reproductivo y la longevidad de la planta son moderadores potenciales de la relaci´ on entre el tama˜ no poblacional y la diversidad gen´etica. La diversidad gen´etica promedio, el porcentaje de loci polim´ orficos y la riqueza al´elica en los estudios tuvieron una correlaci´ on positiva y altamente significativa
Paper submitted March 8, 2006; revised manuscript accepted October 3, 2006.
823 Conservation Biology Volume 21, No. 3, 823–831 C 2007 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2006.00646.x
Habitat Fragmentation and Common Species
Honnay & Jacquemyn
con el tama˜ no poblacional, mientras que no encontramos relaci´ on significativa entre el tama˜ no poblacional y el coeficiente de endogamia. La diversidad gen´etica de especies auto compatibles fue menos afectada por la reducci´ on en el tama˜ no poblacional que la de especies exog´ amicas obligadas y especies auto compatibles, pero principalmente exog´ amicas. La longevidad no afect´ o la respuesta gen´etica de la poblaci´ on a la fragmentaci´ on. Sin embargo, nuestro hallazgo m´ as importante fue que las especies comunes fueron tan, o m´ as, susceptibles a las consecuencias gen´eticas de la fragmentaci´ on del h´ abitat que las especies raras, aun cuando las especies hist´ orica o naturalmente raras fueron excluidas del an´ alisis. Estos resultados son dram´ aticos porque muchas especies m´ as pueden ser vulnerables a la erosi´ on gen´etica y a la p´erdida de diversidad gen´etica como consecuencia de los procesos de fragmentaci´ on que lo se asum´ıa previamente. Esto implica que muchos h´ abitats fragmentados han perdido la capacidad para soportar poblaciones de plantas lo suficientemente grandes para mantener un equilibrio mutaci´ on-deriva y que los fragmentos de h´ abitat ocupados est´ an tan aislados que el flujo g´enico es insuficiente para permitir la reposici´ on de alelos perdidos.
Palabras Clave: diversidad gen´etica, endogamia, fragmentaci´on de h´abitat, sistema reproductivo, tama˜no poblacional
Introduction Next to decreasing habitat quality and the introduction of exotic species, habitat fragmentation is one of the main drivers behind the present biodiversity crisis (Young & Clarke 2000). Habitat fragmentation includes three components (Andren 1994): (1) pure loss of habitat, (2) reduced fragment size, and (3) increased spatial isolation of remnant fragments. Small habitat fragments contain small populations, which are more vulnerable to extinction due to environmental and demographic stochasticity (Shaffer 1981; Lande 1988). In addition, small populations may be more prone to extinction due to the loss of genetic variation (Frankham 1996). A decreasing population size may result in erosion of genetic variation through the loss of alleles by random genetic drift. In addition, increased selfing (in plants) and mating among closely related individuals in small populations may result in inbreeding and a reduction of the number of heterozygotes (Schaal & Leverich 1996; Young et al. 1996). Over the short term decreasing heterozygosity and the expression of deleterious alleles may result in reduced fitness (Keller & Waller 2002; Reed & Frankham 2003). In the long term lower levels of genetic variation may limit a species’ ability to respond to changing environmental conditions through adaptation and selection (Booy et al. 2000). To date, most studies dealing with genetic erosion in fragmented plant populations have focused on threatened or rare species (e.g., Raijman et al. 1994; Cruzan 2001; Gonzales & Hamrick 2005). The few available studies that explicitly looked for a relationship between habitat fragmentation and genetic erosion in common species, however, have demonstrated that commonness does not protect a species from loss of genetic variation (e.g., Lienert et al. 2002; Hooftman et al. 2004; Galeuchet et al. 2005). These findings are unexpected because common species are by definition characterized by higher fragment occupancy and/or higher local abundance than rare species (Gaston et al. 2000). These spatial population character-
Conservation Biology Volume 21, No. 3, June 2007
istics can be expected to mitigate the loss of genetic diversity in common species, for example, by allowing genetic rescue (i.e., the replenishment of lost alleles through gene flow between habitat fragments) (Richards 2000; Tallmon et al. 2004). On the other hand, rare species include both species that are historically or naturally rare (e.g., Wolf et al. 2000a) and those that are rare due to recent population declines. The effects of habitat fragmentation are expected to be more severe in recently fragmented populations (Huenneke 1991; Gitzendanner & Soltis 2000). If the loss of genetic diversity in common species appears to be a universal phenomenon, then this may have major consequences for plant community composition and species richness of fragmented habitats. In turn, changing community composition and decreasing species richness may negatively affect ecosystem functioning (Loreau et al. 2001; Leps 2005). Along with rarity, mating system and longevity may also affect the genetic response of plants to habitat fragmentation. Plants display a wide variety of mating systems that differ in their influence on population genetic structure (Barrett & Kohn 1991; Richards 1997). Nevertheless, it is currently not known whether the effects of habitat fragmentation on the degree of inbreeding and genetic drift systematically differ for species with different mating systems and, more specifically, between self-compatible and self-incompatible species (Galeuchet et al. 2005). Longevity (and especially prolonged clonal growth) may also mitigate the loss of genetic diversity because it extends the time between generations and therefore moderates the loss of alleles through genetic drift (Young et al. 1996; Honnay & Bossuyt 2005). Some authors have compared overall genetic diversity between rare and common (congeneric) species (Hamrick & Godt 1996; Gitzendanner & Soltis 2000) although summary of the available habitat fragmentation studies and comparison of the relationship between genetic diversity and population size between common and rare plant species has not been conducted. Thus, we
Honnay & Jacquemyn
conducted a formal meta-analysis of habitat fragmentation studies that report the relationship between population size and genetic diversity. Meta-analysis focuses on the size and direction of effects across studies, examining the consistency of effects and the relationship between study features (i.e., moderator variables) and observed effects. We estimated the overall mean and the variance of the correlation coefficients among different measures of genetic diversity and plant population size and tested for rarity, mating system, and longevity as potential moderators of the relation between population size and genetic diversity. Specifically, we addressed whether small, fragmented plant populations are genetically impoverished compared with larger populations; whether rare species are more vulnerable to habitat-fragmentation-mediated loss of genetic diversity than common species; and how moderator variables mating system and longevity affect the relationship between population size and genetic diversity.
Methods Study Selection and Coding In January 2006 we used the keywords habitat fragmentation AND genetic∗ in a search of Thomson’s on line Web of Science. From this query all papers dealing with plant species and applying codominant markers (allozyme or microsatellite markers) to quantify genetic diversity were selected. Amplified fragment length polymorphism (AFLP) and random amplified polymorphic DNA (RAPD) studies were omitted because we were mainly interested in the effects of habitat fragmentation on the inbreeding coefficient (i.e., on the divergence of observed from expected heterozygosity), which is impossible to infer from dominant DNA markers (Mueller & Wolfenbarger 1999). We supplemented the selected papers with studies we found in the papers’ cited literature. We examined the full-text version of all selected studies. Studies that did not report population sizes, the number of samples used for genetic analysis, and genetic diversity measures at the level of the individual population were excluded. Studies dealing with fewer than five populations were also omitted. In two studies we used population density as a surrogate of population size (Neel & Ellstrand 2001, 2003) In each study we recorded the following measures of genetic diversity for all surveyed populations: inbreeding coefficient (F IS ), expected heterozygosity or gene diversity (H e ), percentage of polymorphic loci (P), and the number of alleles per locus (A). Not all studies reported all diversity measures, and in some cases it was possible to calculate the inbreeding coefficient from the reported expected and observed heterozygosity. We recorded the Pearson correlation coefficient (r) between each of the
Habitat Fragmentation and Common Species
four measures of genetic diversity and population size (number of individuals). In most cases we had to calculate r ourselves. Because the Pearson correlation coefficient quantifies linear fits only, we log transformed population sizes in some cases. This log transformation was not applied more frequently for species defined as common than for species defined as rare. In some studies population sizes were reported as categories. For these cases we calculated the Spearman rank correlation coefficient instead of the Pearson correlation coefficient. The correlation coefficients r between population size and the four genetic diversity measures were used as the effect sizes (ES) of the meta-analysis. Plant species that were explicitly mentioned by authors as “widespread,” “common,” or “quite common” were coded as common. Other species, referred to as “threatened,” “endangered,” “relatively rare,” or “rare” were coded as rare. A species could be common in one study and rare in another (e.g., Van Rossum et al. 1997 vs. Van Rossum et al. 2003) or both common and rare in one study. In the latter case the same species was studied in two different regions where it differed in abundance and patch occupancy (e.g., Mandak et al. 2005). We believe that relying on the expert knowledge of the authors on the status of a certain species in a certain region is far more accurate in this context than defining rarity and commonness based on reported population sizes and patch occupancies. Moreover, patch occupancies of the species were rarely reported, and we found no indication that the range in size of the studied populations was different for common versus rare species. This makes a quantitative approach of rarity and commonness extremely difficult. We also coded whether a rare study species was subjected to recent fragmentation events (e.g., Luijten et al. 2000) or whether it was naturally or historically rare (e.g., Wolf et al. 2000a). Almost all studies provided information on the mating system of the study species. This information was always reported as “obligate outcrossing,” “self-compatible but mainly outcrossing,” or “self-compatible” and was coded accordingly. None of the surveyed species was reported as being a complete selfer. Finally, we recorded whether a species was perennial or annual, and if it was perennial, whether it was reported as being clonal. Statistical Analyses The weight of each study was calculated according to Reed and Frankham (2003) as follows: [(K – 2)N]1/2 , where K is the number of populations in the study and N is the mean number of individuals per population sampled for genetic analysis. The applied weight is, strictly speaking, not equal to the inverse variance of the Spearman rank correlation (K – 3), which is commonly used in meta-analysis (Lipsey & Wilson 2001), but allowed accounting of the number of individuals sampled.
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Habitat Fragmentation and Common Species
We explored the possibility of a publication bias by examining funnel plots and weighted histograms. Funnel plots were constructed by plotting the ES of each study against study weight. We also calculated the significance of the Spearman rank correlation coefficient between ES and study weight (Light & Pillemer 1984). When authors do not submit studies or editors reject submissions with small treatment effects or nonsignificant results, the literature becomes biased (Thornton & Lee 2000). A publication bias against nonsignificant results implies that only large effects are reported by small sample size studies because only large effects reach statistical significance in small samples. This may result in a positive correlation between ES and study weight. We performed the meta-analysis according to Lipsey and Wilson’s (2001) methods and with SPSS (SPSS, Chicago, Illinois) macros written by these authors. We did not, however, apply the Fisher transformation to the correlation coefficients, because it may lead to overestimation of the ES (Hunter & Schmidt 1990). We preferred to use a more conservative, but more realistic, mixed model with maximum likelihood estimation above a fixed model for calculation of the mean ES (Lipsey & Wilson 2001). Heterogeneity of the ES across studies was examined with the Q statistic (Hedges & Olkin 1985). We tested the role of the moderator variables (commonness, mating system, and longevity) in explaining heterogeneity across studies by performing a one-way analysis of variance (ANOVA) analog mixed model and by examining the resulting Q statistic between groups (Lipsey & Wilson 2001). To test for potential confounding interactions between the moderator variables we measured their pairwise degree of association with a chi-square test. All calculations were performed with SPSS (version 12.0).
Results The final database contained 57 records, including 52 different plant species covered in 53 publications (Table 1). Twenty-one records applied to common species and 36 to rare species. Nine of these 36 rare species could be defined as historically rare. For two species, no information regarding the mating system could be retrieved. Allozymes were used in all but three studies, and the median number of polymorphic loci was 7 (range 2–21). There was no Spearman rank correlation between any of the four ES and the number of polymorphic loci (p > 0.1). There was no evidence of a publication bias. All four funnel plots were symmetrical around the mean weighted ES (results not shown), and none of the rank correlations between study weight and F IS (0.15), H e (–0.08), A (−0.13), and P (–0.26) were significant (p > 0.05). The mean weighted ES (±SE) for H e (0.23 ± 0.04), P (0.35 ± 0.05), and A (0.36 ± 0.04) were positive and highly sig-
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Honnay & Jacquemyn
nificant (p < 0.001), whereas no significant ES was found for F IS (–0.04 ± 0.05). There were no significant pairwise associations between the three moderator variables (p > 0.1). Mean weighted ES for F IS , P, and A were not significantly lower for common than for rare species (Table 2). There was, on the contrary, a trend for a stronger correlation between H e and population size for common than for rare species (Table 2, Fig. 1). The difference in strength of the ES for F IS , P, and A between common and rare species remained insignificant when the nine historically rare species were omitted from the analysis (results not shown). Mating system did not affect the strength of the correlation between population size and F IS . Self-compatible species, however, showed a lower ES for P, H e , and A than obligate outcrossers and self-compatible but mainly outcrossing species (Table 3, Fig. 1). Self-compatible species exhibited no significant ES at all (Table 3). Because only two species were reported to be annuals, we did not conduct a statistical comparison between annuals and perennials. Ten species were considered clonal, but they were not significantly less affected by declining population size than nonclonal species (results not shown).
Discussion Based on the results obtained for 52 plant species, small populations consistently contained significantly less genetic variation (measured by H e , A, and P) than large populations. Population size had a lower effect on H e than on P and A, suggesting that alleles lost through habitat fragmentation and population size reduction were mainly those initially present at low densities (Nei et al. 1975; Sun 1996). Our results support the conclusions of Young et al. (1996) and suggest that loss of alleles through population bottlenecks and random genetic drift play an important role in the genetic impoverishment of plant populations. Overall, the homozygosity excess, as measured by F IS , was not affected by population size. Heterozygosity can be lost as a direct result of decreasing gene diversity and, more importantly, through increased inbreeding arising from increased self-pollination or mating between related individuals (Barrett & Kohn 1991; Young et al. 1996). Several not mutually exclusive explanations are possible for the absence of an overall relationship between F IS and population size. The F IS in small populations may be biased downward because homozygotes for rare alleles are absent (Kirby 1975; Young et al. 1999), whereas F IS in large populations may be frequently biased upward because of population substructuring (the Wahlund effect) (e.g., Lowe et al. 2004). Moreover, Lesica and Allendorf (1992) suggest that selection against homozygotes occurs during early stages of growth in plant populations.
Honnay & Jacquemyn
Habitat Fragmentation and Common Species
Table 1. Studies used for the meta-analysis on the relation between genetic diversity and population size.
Study Coates 1988 Young et al. 1993 Dixon & May 1990 Cozzolino et al. 2003 Shapcott 1994 Weidema et al. 1996 Kahmen & Poschlod 2000 Luijten et al. 2000 Mandak et al. 2005 Mandak et al. 2005 Matolweni et al. 2000 Matolweni et al. 2000 Hutrez-Bousses 1996 ˚ Alexandersson & Agren 2000 Wolf et al. 2000a, 2000b Godt et al. 2005 Colas et al. 1997 Lopez-Pujol 2005 Paschke et al. 2002 Neel & Ellstrand 2001 Neel & Ellstrand 2003 Prober & Brown 1994 Berge et al. 1998 Weidema et al. 2000 Raijmann et al. 1994 Vandepitte et al., unpublished Gustafsson 2000 L¨ onn & Prentice 2002 Oostermeijer & De Knegt 2004 Chang et al. 2004 Galeuchet et al. 2005 Berge et al. 1998 Lammi et al. 1999 Chang et al. 2005 Prober et al. 1998 Van Rossum et al. 2002 Van Rossum et al. 2004 Van Rossum et al. 2004 Young et al. 1999 Van Treuren et al. 1991 Van Treuren et al. 1991 Cruzan 2001 Giles & Goudet 1997 Van Rossum et al. 2003 Van Rossum & Prentice 2004 Van Rossum et al. 1997 Dolan 1994 Bacles et al. 2004 Sun 1996 Lopez-Pujol 2003 Vergeer et al. 2003 Buza et al. 2000 Tomimatsu & Ohara 2003 Gonzales & Hamrick 2006 Leimu & Mutikainen 2005 Culley & Grub 2003 McClenaghan & Beauchamp 1986
status: 1, rare; 0, common; n, population size; SC, self-compatible; SC/MO, self-compatible but mainly outcrossing; OO, obligate outcrossing; 1, clonal; 0, not clonal. b Naturally or historically rare.
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Table 2. Difference in effect size (ES) between common and rare species (Q statistic).
Genetic diversity measurea
F IS He common rare P A
48 51 19 32 42 39
Q between groupsb 0.02 3.58∗
Mean weighted ES by groupb
a Key: F , inbreeding coefficient; H , expected heterozygosity; P, IS e percent polymorphic loci; A, number of alleles per locus; n, number of records. b∗ 0.05 ≤ p < 0.1; ∗∗ 0.001 ≤ p < 0.01, ∗∗∗ p < 0.001.
Because in most plant species only a small proportion of the offspring survives into the adult stage, selection against homozygotes may occur without affecting recruitment. Especially under harsh environmental conditions with high selection pressures against homozygotes, heterozygosity may be lost very slowly. For example, in grassland species, highly heterozygous individuals have better survival chances during the gradual process of spontaneous afforestation and subsequent habitat fragmentation (Kahmen & Poschlod 2000). Therefore, the smallest and most fragmented populations do not contain a random sample from previously larger populations; rather they exhibit a significant heterozygosity excess (Raijman et
Figure 1. Effect size (correlation between genetic diversity and population size) for 52 plant species considered in 53 publications for the moderator variables with a significant Q statistic. Bars are standard errors (H e , expected heterozygosity; A, number of alleles per locus; P, percent polymorphic loci; sc, self-compatible; sc/mo, self-compatible but mainly outcrossing; oo, obligate outcrossing).
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al. 1994; Kahmen & Poschlod 2000). In any case further research regarding the uncertain relation between homozygote excess and plant population size remains necessary, especially because a homozygote excess affects short-term fitness (Reed & Frankham 2003). Our most important finding was that population genetic diversity (H e , A, and P) was also eroded in species that were considered common. Even when historically or naturally fragmented populations of rare species were omitted from the analysis, no difference between rare and common species in population genetic response to habitat fragmentation was found. These results are dramatic in that many more plant species than previously assumed may be vulnerable to genetic erosion and loss of genetic diversity as a result of ongoing fragmentation processes. It seems that many fragmented habitats have become unable to support plant populations that are large enough to maintain a mutation-drift balance and that habitat fragments have become too isolated to allow sufficient gene flow to enable replenishment of lost alleles. Although genetic impoverishment may not result in a short-term loss of fitness in all species, given the absence of a general relationship between population size and F IS (Young et al. 1999; Matolweni et al. 2000), the fragmentation-mediated loss of alleles will at least affect the evolutionary adaptation potential of even common species (Ellstrand & Elam 1993). In the global context of rapid climate change, the latter is alarming because many plant species lack the colonization ability to track the shifting climate northward (Honnay et al. 2002). Our results also indicated that obligate or mainly outcrossing species are more vulnerable to the loss of genetic variation through habitat fragmentation than selfcompatible species. This may be an indication that the role of gene flow is very important in conserving genetic diversity in outbreeding species. Obligate outcrossing or mainly outcrossing species can maintain high population genetic diversity through frequent exchange of genes with other populations and even a very few migrants per generation are sufficient to counter genetic differentiation (Wright 1931). Indeed, these species are generally characterized by low between-population genetic differentiation (Hamrick & Godt 1996). With increasing habitat destruction and decreasing local population size and patch occupancy, the exchange of alleles becomes less likely, and the smallest populations may loose genetic diversity without the possibility of replenishing the alleles lost through drift. Almost all surveyed plant species rely on insects for pollination, and changing pollinator behavior may play an important role in this process (Wilcock & Neiland 2002). Small plant populations may become too inconspicuous or too isolated to attract pollinating insects (Kwak et al. 1998; Steffan-Dewenter & Tscharntke 1999). Increasing fragmentation may therefore directly translate into reduced pollinator activity, reduced gene flow, and loss of genetic diversity. Mainly selfing species
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Table 3. Difference in effect size (ES) between different mating systems (Q statistic).
Genetic diversity measurea
Q between groupsb
F IS He self-compatible self-compatible, mainly outcrossing obligate outcrossing P self-compatible self-compatible, mainly outcrossing obligate outcrossing A self-compatible self-compatible, mainly outcrossing obligate outcrossing
46 49 16 15 18 40 11 14 15 41 12 13 16
Mean weighted ES by groupb
0.05 0.33∗∗∗ 0.30∗∗∗
0.07 0.07 0.06
0.16 0.36∗∗∗ 0.46∗∗∗
0.09 0.07 0.07
0.12 0.48∗∗∗ 0.44∗∗∗
0.07 0.07 0.06
F IS , inbreeding coefficient; H e , expected heterozygosity; P, percent polymorphic loci; A, number of alleles per locus; n, number of records. < p ≤ 0.05; ∗∗ 0.001 ≤ p < 0.01, ∗∗∗ p < 0.001.
on the other hand, naturally contain most of their genetic diversity within populations, and their level of population genetic diversity will be less affected by reduced gene flow. Our inability to find an effect of clonality on population genetic response to habitat fragmentation is likely partly due to the unequal sample sizes between clonal and nonclonal plants. Our results point to a serious bias of plant fragmentation studies toward perennial, nonclonal species. Inclusion of annuals and strongly clonal species in future studies will allow a more accurate assessment of the impact of degree of longevity on the population genetic response to habitat fragmentation. Some authors suggest that different taxa cannot be treated as independent samples because of their phylogenetic relatedness and that in the absence of a phylogeny only congeneric comparisons can be made (Felsenstein 1985; Gitzendanner & Soltis 2000). We are not aware, however, of any method that includes phylogenetically independent contrasts in a meta-analytical approach, and we found the required habitat fragmentation data for only five congeneric species pairs. Moreover, possible nonindependence of our data increased the probability of a Type I error, making it unlikely that applying a correction for phylogenetic relatedness will reveal significant differences between the response of common and rare species to habitat fragmentation (Gitzendanner & Soltis 2000). We found a highly significant effect of population size on population genetic diversity, with the exception of the inbreeding coefficient. The population size effect was much more pronounced in self-compatible but mainly outcrossing species and in obligate outcrossing species. Most important, our results revealed that the effect of population size on genetic diversity is as pronounced in common as in rare species. This means that in our fragmented landscapes, even common species may have reached a critical threshold in population size and patch
occupancy; thus, measures mitigating habitat fragmentation are strongly needed.
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Annu. Rev. Ecol. Syst. 1998. 29:83-112 Copyright? 1998 by AnnuailReviews. All rights reserved
ENDANGEREDMUTUALISMS: The Conservationof Plant-Pollinator Interactions Carol A. Kearns,)4 David W Inouye,2'4 and Nickolas M. Waser3'4 1EPOBiology, EnvironmentalResidentialAcademic Program,C.B.176, Universityof Colorado,Boulder,Colorado 80309; 2Departmentof Biology, Universityof Maryland, College Park,Maryland20742; 3Departmentof Biology, Universityof California, RiversideCalifornia92521; 4Rocky MountainBiological Laboratory,P.O. Box 519, CrestedButte Colorado81224; e-mail: [email protected] KEY WORDS: agriculture,ecosystem services, fragmentation,habitatalteration,species invasions
ABSTRACT The pollination of flowering plants by animals representsa critical ecosystem service of great value to humanity,both monetaryand otherwise. However,the need for active conservation of pollination interactionsis only now being appreciated. Pollination systems are under increasing threatfrom anthropogenic sources,includingfragmentationof habitat,changesin landuse, modernagriculturalpractices,use of chemicals such as pesticides and herbicides,and invasions of non-nativeplants and animals. Honeybees, which themselves are non-native pollinatorson most continents,and which may harmnativebees and other pollinators,are nonetheless critically importantfor crop pollination. Recent declines in honeybeenumbersin the United States andEuropebringhome the importance of healthy pollination systems, and the need to furtherdevelop native bees and other animals as crop pollinators. The "pollinationcrisis" that is evident in declines of honeybees and native bees, and in damage to webs of plant-pollinator interaction,may be amelioratednot only by cultivationof a diversity of crop pollinators,but also by changes in habitatuse and agriculturalpractices,species reintroductionsand removals, and other means. In addition,ecologists must redouble efforts to study basic aspects of plant-pollinatorinteractionsif optimal
83 0066-4162/98/1 120-0083$08.00
KEARNS, INOUYE & WASER managementdecisions are to be made for conservationof these interactionsin naturaland agriculturalecosystems.
INTRODUCTION To persist on planetEarth,humansdepend on "life-supportservices"provided by biological, geological, and chemical processes in healthy ecosystems. Services such as the cycling of nutrients and regulation of climate are widely recognized. Othersuch services are less well known, among them biological processes arising from interactionsamong species, including enhancementof otherspecies' populationsby beneficial biotic agents. The pollinationof floweringplantsis a primeexample: Withoutpollinationby animals,most flowering plants would not reproducesexually, and humans would lose food and other plant products(22). One measureof the immense value of ecosystem services is monetaryvalue. A recent estimate places a conservative overall mean value per annum of 33 trillionAmericandollarson all ecosystem services (40); the componentdue to pollination services is $112 billion. Independentestimates placed the annual value of pollinationfor crop systems at $20 billion (102) to $40 billion in the United States alone (159); for global agriculture,the estimated value is $200 billion (172). Of pollinatorsotherthan honeybees, the value to US crop yields may be as high as $6.7 billion per year (141). The economic importanceof pollination, and its esthetic and ethical values, makes it clear that the conservation of pollination systems is an important priority. In this paper, we describe the ecological and evolutionary nature of plant-pollinatorinteractionsand review evidence that they are increasingly threatenedby human activities. We then discuss potential management solutions to amelioratethe "pollinationcrisis" and highlight areas that call for furtherresearch.
THE NATURE OF PLANT-POLLINATOR
INTERACTIONS Modernangiospermscomprisean estimated250,000 species (81), and most of these-by some estimates over 90% (22, p. 274)-are pollinated by animals, especially insects. Bees alone comprise an estimated 25,000-30,000 species worldwide, all obligate flower visitors (22,206,215,237). The ranks of flies, butterfliesandmoths,beetles, andotherobligate or facultativeinsect flowervisitorssurelyareseveraltimes as large,to which must be addedspecies of birdsin severalfamilies (35), bats, and small mammals. The numberof flower-visiting species worldwidemay total nearly 300,000 (141).
Relatively few plant-pollinatorinteractionsare absolutely obligate. Most are more generalized on the part of both plants and animals, and they also vary throughtime and space (61, 62, 78,79, 181, 232). For example, the shrub Lavandulalatifolia in southernSpainis visited by 54 insect taxafrom 3 orders, with insects varying substantiallyin their quality as pollinators (75-77). If added into that is the numberof plant species each pollinatorvisits, the "connectance"of plant and pollinatorspecies in a food web can be high. Jordano (93) reportedan averageconnectanceC of about 0.3 for fragmentsof 36 pollination webs, where C is the realized fraction of the product of n pollinator species and m plant species in the web. C should decline with size of a web, but perhapsnot as stronglyas previouslythought(130, 162). Recognizing most pollinationinteractionsas being far from obligate fundamentally changes the perceptionof their conservation. We must abandonthe perspectivethatto lose one plant species is to lose one or more animal species via linked extinction, and vice versa. If the fundamentalecological natureof pollination "interactionwebs" is that they are relatively richly connected and shift in time and space, dependingin part on the landscapecontext (20), then the job of conservationbiologists is made more subtle and complex. One majorroot of generalizedinteractionsis opportunismon the partof both plants and pollinators. To understandthis, consider what might be called the fundamentalevolutionarynatureof pollination. Plants and animalpollinators aremutualists,each benefitingfrom the other'spresence (13; see also 19, 222). But the mutualismis neithersymmetricalnor cooperative. Indeed,pollination derivesevolutionarilyfromrelationshipsthatwere fully antagonistic(44, 167). The goals of plants and animalpollinatorsremain distinct-in most cases reproductionon the one handand food gatheringon the other-and this leads to conflict of interestratherthancooperation(83, 233, 239, 240). One place to see this conflict is in the behaviorof animals such as bees that "rob"flowers for nectar(87). The conflictof interestdictatesthatnaturalselection will act in divergentways on plantsandpollinators.Pollinatorsareagentsof selection andgene flow from the perspectiveof plants (30) and are involved in evolutionaryevents ranging from plant speciation to molding floral phenotype. But floral phenotypes are not simply those thatare optimalfor the animals(84). Conversely,plantsselect for featuresof the animalphenotype(200), but the result is not optimalfor the plants. The most basic evolutionaryoutcomethatis common acrossbothplants and pollinatorsis efficiency of each in exploiting what for each is a valuableor criticalresource. One common manifestationis opportunismand flexibility on the partof pollinatorstowardplants,and vice versa. To devise the best possible strategies for management, conservation, or restorationof pollination systems, it is essential to have several elements in place. We need excellent knowledge of the natural history of plants and
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pollinators. And we need an appreciationfor interactionwebs and a "Darwinian perspective"on how naturalselection is likely to have shapedbehavior, morphology,and otheraspects of the phenotypeof plants and pollinators.
THE POLLINATIONCRISIS Endangered Pollinators and Plants Disruptionof pollinationsystems, and declines of certaintypes of pollinators, have been reportedon every continent except Antarctica. Although large regions of each continenthave not been evaluated,we can assume thatdisruption is widespreadbecause the causes are widespreadphenomenaassociated with humanactivities. The overall pictureis of a majorpollinationcrisis (22). The causes include habitatfragmentationand otherchanges in land use, agriculture and grazing, pesticide and herbicide use, and the introductionof non-native species.
Biological Effects of Fragmentation Many threatsto pollinationsystems stem from fragmentationof once-continuous habitat. Fragmentationcreates small populations from larger ones, with attendantproblemsthat include increasedgenetic drift, inbreedingdepression, and (for very small populations)increasedrisk of extinctionfrom demographic stochasticity (7, 58, 191). Furthermore,fragmentationincreases spatial isolation and the amount of edge between undisturbedand disturbedhabitat,both of which can harmpollination(133). If the isolation of fragmentedpopulationsbecomes greaterthanthe foraging range of pollinators,if the local pollinatorpopulationbecomes small enough, or if wide-ranging pollinators avoid small populations, the outcome may be reducedpollinationservices. Limitationof pollen receipt occurs in many plant species. Burd (23) found evidence for pollen limitationfor 62% of 258 species surveyed. The degree of limitation typically varies among years, within a season, amongsites withina season, andamongplantsfloweringsynchronously within a site (54 and referencestherein). Population size contributesto pollen limitation. For example, both male function (pollen removal) and female function (fruit set) are functions of population size for three Swedish orchid species (67; see also 110; see 195 for pollinator visitation rates). Some studies of endangeredplants have specifically implicated a lack of effective pollinators. Pavlik et al (152) found that seed set of Oenotheradeltoides ssp. howellii was 26% and 37% of maximum in 2 years and suggested scarcity of hawkmothsas a cause; a related species growing in an unfragmentedhabitathad seed set that was 65% of maximum. Spatial isolation of plants or populationscan also play a role. For example,
isolated plants of Cynoglossumofficinale receive fewer approachesby bumblebees than patches of these plants (108). Percy & Cronk (155) studied an endemic of the island of St. Helena with a total populationof 132 adult trees. Pollinationis accomplishedby small syrphidflies, and pollen deliverydeclines beyond 50 m; thus, isolated trees are effectively left withoutpollination. Pollen limitationdoes not alwaysimplya dang,erousconservationsituation. It is often the naturalconditiondue, amongotherthings, to stochasticityin flower visitation (24). Johnson & Bond (92) found widespreadpollen limitation in wildflowers in the mountainsnear Cape Town, South Africa. They attributed this patternto a general scarcity of pollinatorsand, in some cases, to lack of floralrewards. Populationsize can affect aspects of pollinationotherthanpollen limitation. For example, the composition of the pollinatorfauna often differs in flower patches of differentsize (195,202). In some cases, such a faunal change may result in higher per-flowervisitationrates in small populations(202). Pollination services are also likely to be affected by density of a plant population, which will sometimes, but not always, covary with population size (1 14). Thomson (219) and Schmitt (192) reporteddeclines in pollination services at low density for several species in the Asteraceae. Seed set in the desertannualplantLesquerellafendleridependson the numberof conspecifics flowering within 1 m, but not fartheraway, and behavior of small insect pollinatorsappearsto be the cause (175). Density-relateddeclines in the quality of each pollinatorvisit (the proportionof conspecific versus foreign pollen delivered) can be more importantthan paralleldeclines in the quantityof visits (112, 113, 116). Interactionsof population size, density, and spatial isolation are likely to have even more complex effects on pollination,and these interactionsrequire furtherstudy. For example, outcrossingrate is unrelatedto populationsize of an endangeredSalvia species, but high plant density (in combinationwith low frequencies of male steriles) promotes outcrossing in hermaphrodites(227). Groom(73) reportedthatpollen limitationdependson both populationsize and isolation in a species of Clarkia. Of particularconcern is an Allee effecta threshold density, population size, or combination thereof-below which pollinatorsno longer visit flowers. In a species of Banksia, populationsbelow a thresholdsize producefew or no seeds, presumablyin partbecause of pollen limitation(121; see also 156; for a theoreticalapproachsee 86). Small plant populationsresultingfrom fragmentationtend to sufferfrom increased genetic drift and inbreedingdepression(58,228). This may be due to increasedgeitonogamy,as pollinatorsmay visit a higher proportionof flowers on individualplants, resulting in more self-fertilization(108). Inbreedingdepressionmay explain why small populationsof Ipomopsisaggregata are more
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susceptibleto environmentalstressandhavereducedgerminationsuccess (80). In general, knowledge of the mating systems of plants often is importantfor conservation.Self-incompatibilitymay furthercompoundthe dangersof small populationsize by reducingthe availabilityof suitablemates (27, 49, 122).
Studies of Pollination in Fragments Recent studies illustratesome of the range of fragmentation-relatedeffects on pollination systems. Most of these effects are clearly deleterious. Aizen & Feinsinger (2, 3), who studied habitat fragmentationin dry thorn forest in Argentina,found fragmentation-relateddeclines in pollination, fruit set, and seed set for most of the 16 plant species examined. For at least two species, frequencyand taxon richness of nativeflower-visitorsdeclined with decreasing fragmentsize, but visitation by introducedAfricanized honey bees tended to compensatefor loss of visits by nativesin small fragments. Honeybees can be successful in disturbedand fragmentedhabitats(2, 3, 90, 183), and fragmentation may hastenthe spreadof Africanizedbees (2, 3) and the demise of native pollinators(179, 180). Spears(203) found thatpollen dispersalto neighboringplantsis significantly reduced in island populations relative to mainland populations of the same species. Pollinatorlimitation on islands separatedby fewer than 10 km from the mainlandmay foreshadowthe fate of many increasinglyisolated mainland plant species. For example, seed set in Dianthus deltoides declined in habitat islandseven though nectaravailabilitywas equivalentto that in an undisturbed "mainland"(90). A few studieshave addressedfragmentationandpollinationin tropicalareas. Powell & Powell (164) used fragrancebaits to determinethat male euglossine bees, which arepollinatorsof manyneotropicalorchids,would not cross cleared areasas small as l00 m betweenforesthabitats.Allozyme heterozygosity,polymorphism,andeffective numberof alleles decline in small and isolatedpopulations of the tropicaltreePithecellobiumelegans (74). In seeming contradiction to this apparentgenetic erosion in fragments,pollen dispersal by hawkmoths appearsto be substantialfor this species andseems easily capableof connecting isolated trees and those in fragmentsto the rest of the population(32). The generation of new edges as forests are fragmentedwill change both abiotic and biotic components of the environment.Murcia (138, 139) divided biotic effects into (a) direct effects that involve changes in the abundanceand distributionof species and (b) indirect effects that involve changes in species interactions,including pollination. She detectedno consistent changes in pollination levels at a forest edge in Columbia, which suggests that the primary influence of fragmentationis throughthe creationof smaller populationsand the isolation they experience.
The response of insects to fragmentationis poorly understood(50). Bowers (17) studiedbumblebee colonization,extinction,andreproductionin subalpine meadows of differentsizes. The numberand diversityof queens that colonize meadowsat the beginningof the summerarepositivefunctionsof meadowarea, althoughby mid- to late summerthe flower composition of meadows govern species compositionand the subsequentreproductionof colonies. Not all studies have detected negative effects. Stouffer& Bierregaard(209) sampled understoryhummingbirdsin Amazonian forest before and for nine years afterfragmentation.Two species presentbefore isolation did not change in abundance,but one became nearlytwice as common, and five were captured only afterfragmentation.In contrastto insectivorousbirds, the hummingbirds appearedto be plastic in habitatpreferences. Olesen & Jain (144) described how fragmentationcan harm not only pollination, but also interactionsthat plants have with seed dispersers and other mutualists. Loss of these interactionscould lead to an extinction vortex with potentially catastrophicconsequences for biodiversity. An improved understandingof such effects is critical for conservation(169).
Effectsof AgriculturalPractices on WildPollinators Humansdependon animalpollinationdirectlyor indirectlyfor aboutone third of the food they eat (147, 172). Pollinationis requiredfor seed production(e.g. alfalfa, clover), to increase seed quality (e.g. sunflower)and number(e.g. caraway), for fruitproductionand quality (e.g. orchardfruits, melons, tomatoes), to createhybridseed (e.g. hybridsunflower),andto increaseuniformityin crop ripening(e.g. oilseed rape) (39). Severalfeatuiresassociatedwith modernagriculturemake farmspoor habitat for wild bees andotherpollinators.Cropmonoculturessacrificefloraldiversity, andconsequentlydiversityof pollinatinginsects, over large areas(6, 147, 246). For example, cultivated orchardssurroundedby other orchardshave significantly fewer bees than orchardssurroundedby uncultivatedland (193), and the numberof bumblebeeson crops increases with proximity to naturalhabitats (246). Chemical fertilizers, pesticides, and herbicides harm pollinators. In addition, marginalland is increasingly cultivated(52, 101, 103, 147, 225 and referencestherein),resultingin (a) loss of wild vegetationto supportpollinators, (b) fewer areas where bees can nest, (c) fewer larval host plants for butterflies,and (d) less-variedmicrohabitatsfor egg laying and larvaldevelopment (52,246). For example, since 1938, Britainhas lost 30% of its hedgerow habitats,which provide floral resources and nesting sites for wild bees at the marginsof cultivatedfields (146). Eliminationof manynativepollinatorsis an unappreciatedpricethathas been paid for increasedfood productionover the last 50 years (172, 224, 225). These
pollinatorsare lost to adjacentnaturalecosystems and to crop pollination as well. Although honeybees have long been consideredthe most importantcrop pollinators(references in 10, 147), wild pollinators are also important(165) and can be managedto provide "free"services (10, 39, 165). Shortagesof bees to pollinatecrops have now been predictedin both Europe and the United States (146, 224). At least 264 crop species from 60 families are grown in the EuropeanUnion, 84% of which are believed to be dependent on insect pollination(244). The best evidence for declines in bee populations comes from Europe (38, 143, 147, 172,246), although similar losses have occurredelsewhere. Damage is not restrictedto agriculturalsituations in industrializedcountries.Vinsonet al (229) documenteddisruptionin pollinationsystems following the clearingof tropicaldry forest in Costa Rica to provideland for grazing and agriculture.Where livestock are raised, native grasses are commonly replaced with introducedforage grass, which burnsmore readily and hotly than native grasses. Fires from privatelands spread to adjacentforest reserves, threatening native plants and the insects and bats that pollinate most of them. The direct effect of fire is not the only problem. Some specific relationshipsexist between anthophoridbees such as Centris and oil plants of the family Malphigiaceae. Several species of Centris depend on finding dead wood with holes formed by wood-boring insects, a resource that disappearswhen forests are cleared. Many oil-producingplants burn, and those that survive produce less oil. Bees in the dry forests appearto be decreasing in both numbersand diversity, and trees that historicallyprovidedbee resources, and depended on bees for outcrossing,are disappearing.
Grazing Grazingthreatenspollinatorsthroughremoval of food resources, destruction of undergroundnests and potentialnesting sites, and othermore subtle mechanisms (70, 96, 211). Sugden (211) studied sheep grazing practices in Californiaand the effects on pollinatorsof an endemic vetch (Astragalus monoensis) and found evidence of nest destruction,pollinatorfood removal by sheep, and direct tramplingof bees. Bees at riskincludedAnthidium,Anthophora,Bombus, Callanthidium, Colletes, Hoplitis, and Osmia. Anotherexample of removal of food resources by grazing is the loss of willow shrubs(Salix spp.) due to cattle along riparian areas. These willows are importantbrowse for livestock (186) and provide nectarandpollen for spring-emergingbumblebeequeens and otherpollinators; their loss may harm the pollinators and, in turn, other species of plants that flower laterin the summer.
Pesticides Pesticides pose a majorthreatto pollinators(9). Ironically,the greatestuse of pesticides is on cropplantswherepollinatorsaremost often limited. Pollinators also are harmedby pesticide applicationin grasslands(18, 154,215), forests, (101), urbanareas(103), andeven touristresorts(47). An increasingawareness of environmentalrisks has helpedreducepollinatorpoisonings in industrialized nations (103), but pesticide-induceddeclines in bee abundanceare still being reportedfrom developing countries(43). Bee poisoning from insecticides firstbecame a problemin the United States in the 1870s (91), but advances in agriculturaltechnology and elaborationof new chemicals exacerbatedthe problemafterWorldWar11(5, 91). Poisoning of honeybees (on which most attentionhas been focused) can result in direct mortality,abnormalcommunicationdances, inability to fly, and displacement of queens (91). Foraginghoneybeescan contaminatethe hive with pesticides or otherpollutants. Pesticides, arsenic, cadmium,PCBs, fluorides,heavy metals, andradionucleotides(afterthe 1986 Chernobylaccident)have all been reported in contaminatedhoney or pollen (103). In the 1970s, Kevan(98-100) cautionedaboutthe disruptiveeffects of pesticides on nativepollinators,andhis predictionshavebeen borneout. The best exampleis a long-termstudyconductedin EasternCanada(99, 101, 103, 104, 106, 161). From 1969 until 1978, sprucebudwormwas controlledby aerialspraying of Fenitrothion,an organophosphatethat is highly toxic to bees. Commercial blueberryproductionin the region largelydependedon pollinationby as many as 70 species of nativeinsects. Blueberrycrops failed in 1970 and subsequent years (102). Populationsof bumblebeesandandrenidandhalictidbees declined in blueberryfields near sprayedforests (99), and reproductionof native plants was depressed (218,221). Native bees showed steady signs of recovery after Fenitrothionwas replacedwith a less harmfulinsecticide (101). In the westernUnited States, broad-spectruminsecticides areused to control grasshopperson rangelands(215). Sprayingoccurs during the flowering of a numberof threatenedor endangeredendemicplants(18) andcoincides with the foraging period of most native bees (154). Sprayingis prohibitedin a 3-mile radiusaroundpointswherelistedplantsareknownto occur,butthe 3-mile figure is arbitrarybecauselittle is knownaboutflightdistancesof the pollinators(154). Some of these listed species appearto have pollinator-limitedseed production (63), and their persistancewill be relatedto successful pollination (194, 215).
Herbicides Herbicide use affects pollinatorsby reducing the availabilityof nectarplants (47, 100). In some circumstances,herbicides appearto have a greatereffect
than insecticides on wild bee populations (11,47). Herbicide spraying and mechanical weed control in alfalfa fields can reduce nectar sources for wild bees. The magnitudeof the effect for each species is related to the length of its seasonal flight period. Many bees have a flight period that extends beyond the availabilityof alfalfaflowers. Some of these bee populationsshow massive declines due to the lack of suitablenestingsites andalternativefood plants (11).
Honeybee Declines More than 9000 years ago, humansrealized they could harvesthoney from the stores of some bees (69). Humans have taken honeybees with them as they settled new regions of the world (21). Honeybees have been domesticated and naturalizedin temperateareas of Australia, North America, and South America for centuries (before 1641 in North America) (196), whereas extensive naturalizationin tropical regions is much more recent (183). Although Apis mellifera is native to western Asia, it is not widely naturalizedin other partsof Asia, where five otherspecies of Apis naturallyoccur (37,183). Today, bee productsare still valuable, but the value of crop pollination is far greater(22; references in 10). Honeybees, which are generalists and will pollinate many crops, areeasily managedand transported(147). Some suggest the annualvalue of honeybee pollinatedcrops in the United States alone is as high as $10 billion (235; see also 201, 224). Recently, honeybees have been declining. More than 20% of the cultivated honeybee colonies in the United States have been lost since 1990 (85,235), along with most feral honeybees(235). The numberof commerciallymanaged colonies has declined from a peak of 5.9 million in the 1940s to 4.3 million in 1985 and 2.7 million in 1995 (85). Declines are severe in some regions. For example, in 1994, Californiaalmondgrowershad to importhoneybees from as far away as Florida(235). The Europeancommunitysupportsan estimated7.5 million managedhoneybee colonies (244,245), and these are believed to have been declining since 1985 (245). Two parasiticmites, VarroajacobsoniandAcarapsiswoodi, havebeen particularlydamagingto honeybees. Varroaspreadfrom its originalhost, the Asiatic honeybee (Apis cerana), when A. mellifera was introducedto Asia (57). The mites had spread from Asia to Europe by 1950, to North Africa by 1970, to South America by 1971, and to North America by 1987 (136). A bee infected by Varroaloses protein to the parasite, resulting in lowered life expectancy. Also, bacteriapenetrateholes in the exoskeleton formed by the mites (174). Existence of A. woodi, the trachealmite, was first documentedin England in 1921; subsequentlyit spreadto continentalEurope,Asia, Africa, South America, andNorthAmerica(42,57). Entirebee colonies become infected,resulting in decreased brood production,decreased honey production,and high winter
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mortality(48). Beekeepers can attemptto control both mites with chemicals, but Varroamites are beginning to exhibit resistance (236). Treatmentcan be costly, and chemical residues may appearin honey. New control techniques are being developed, but the difficulty of mite control is causing a decline in beekeeping, particularlyamong hobbyists(103, 235). Africanizedhoneybees also are implicatedin honeybee decline in the Americas. The term Africanizedhas been used to describe hybridsbetween honeybees of Europeandescent andAfricansubspeciesA. melliferascutellata (173). Taylor (214) suggested that the term neotropicalAfrican bees be used for the feral colonies in South and CentralAmerica thatstill retainthe Africanphenotype distinguishableby morphology,behavior,and genetics, and that the term Africanizedbees be used to refer to bees found primarilyin apiariesthat show clear evidence of hybridization.The failure to make these distinctionshas led to differingpredictionsaboutthe spreadof the bees (214). Africanqueens were released accidently in Brazil in 1956 (136) and rapidlydominatedcolonies of Europeandescent. The bees became established in the United States in 1990 (22). The predominatelyAfrican phenotype may be restrictedto the warmer climate of the southernUnited States, but the variablehybridAfricanizedphenotypes may be able to survive farthernorth(214). NeotropicalAfrican bees display severalfeaturesthatmakethemundesirablefor apiculture.They swarm when colonies are relativelysmall and have little honey, and they leave an area when environmentalconditions become unfavorable(64). Furthermore,their reputationfor aggressive behavioris responsible for negative public attitudes and a decline in beekeeping (22,34,201).
Non-Native Pollinators The introductionof non-nativepollinatorshas the potentialto harmnativepollination systems. For example, fig wasps were introducedto California in 1899, at which point non-nativetrees that had been grown there for decades began to produce fruits (51). Because of the introductionof their wasp pollinators,some fig species are now weedy pests in partsof the continentalUnited States, Hawaii, and New Zealand (68,132). The introductionof bumblebees into areassometimes have negativeresults. Non-nativeBombusterrestriswere broughtto Japan to pollinate greenhouse tomatoes but soon escaped and became naturalized (I Washitani, personal communication). Because of their aggressive nature,queens are able to take over the hives of nativebumblebees by killing the queen, and ecologists fear serious declines in nativebumblebee species. Queens of the native JapaneseBombus diversus are importantpollinatorsof at least one endangeredplant,Primula sieboldii (234), and cannotbe replacedby B. terrestris. B. terrestrishas also invadedpartsof Israelin recent decades, expropriatingnectarresourcesto the apparentdetrimentof nativebees
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(46a). Xylocopa carpenterbees arepollinatorsof some plants but are also well known as nectar robbers (87). Little is known about the impact of this bee on native species of flowers or pollinatorsin Hawaii, where it was introduced (82). By far the most significant introductionof non-native pollinatorsinvolves honeybees, whose movement by humansto all areas of the globe can be considereda major,uncontrolledecological experiment.Honeybees in some cases might benefit wildflowers by excluding native pollinators from crops (245), but they are often poor pollinatorsof crops and native flowers comparedwith nativeinsects (10, 115, 147,148,165,172,184, 224, 239). Furthermore,honeybee colonies requireprodigiousamountsof pollen and nectar,and workerbees fly long distancesandrecruitto richfloralresources(21, 183). Thus, honeybees may compete with native pollinatorsfor resources,leading to reduced species diversityof pollinators. Honeybees also are likely to affect the reproductionof native plants, perhapseven facilitatingthe spread of weedy non-nativeplants (4, 8, 82, 128, 188; see also 26). Whetheror not honeybees aid in the spreadof introducedplants, the presence of these plants may disruptnaturalpollination systems because native pollinators sometimes prefer them at the expense of nativeplants (230). Competitionwith honeybees has been implicatedin the decline of buprestid beetles in westernAustralia(109). Thesejewel beetles areimportantpollinators in arid mallee scrub vegetation. Sugden & Pyke (212) demonstratedcompetition by introducinghoneybees into an alpine area of Australiaand examining the nesting and reproductivesuccess of a generalistnative bee. Honeybees remove as much as half of all the availablenectarfrom flowers of the Australian bottlebrush,Callistemonrugulosus,and New Holland honeyeatersrespondby visiting individual flowers less frequently and expanding their feeding territories (149, 150). Honeybees visit many other Australianplants and on some species remove over 90% of the availableresources(151). Roubik et al (176178, 182, 183, 185) studiedcompetitionbetweenAfricanhoneybees andnative pollinatorsin South and CentralAmerica. In French Guiana, African honey bees are common visitors to Mimosa pudica (183). Patches dominated by honeybees had the lowest levels of seed and fruit production,whereashighest levels occurredin patches visited by native Melipona bees. Honeybees have been increasingin moderatelydisturbed,mixed forest-savannahabitats(from 20% of visitors in 1977 to 99% of visitors in 1994), which suggests that they are displacing native insects. Honeybees were introducedonto Santa CruzIsland, off the coast of California,in the 1880s and can now be found foraging on more than one third of the island's plant species (223, 238). Removal of honeybee colonies from the eastern half of the island over the past few years suggests an inverse relationshipbetween honeybee abundanceand native bee
abundance. Experimentsin old field in New York state show that the native megachilidbee Osmiapumila suffersreducedbroodcell productionand pupal mass, andincreasedbroodparasitismin the presenceof honeybees (K. Goodall, unpublished). The hypothesis of competitionis not supportedby all studies. Sugden et al (213) reviewed 24 studies conducted on four continentsand three islands; 16 detected competition under some conditions whereas 8 produced ambiguous results. Although Africanized honeybees reachedthe neotropics two decades ago and the foraging behavior of native bees changes when honeybees are present,there is no strongevidence of declines in native bee populations(25). Perhapsthis is unsurprising:Where honeybees monopolize a rich resource, native species may shift to other flowers and there may be no effect on their populationsize (150, 183, 190). Also, effects of competition are difficult to detect, if they occur, againstthe backgroundof naturalvariationin pollination systems (25, 183). The idea thathoneybees automaticallycompete with natives is probablynaive (183), and more studies, including ones of longer duration, are needed.
POTENTIALMANAGEMENTSOLUTIONS Conservation of Habitats and Pollinators Conservationbiology is undergoinga paradigmshift away from single-species conservationefforts and towardhabitat,ecosystem, and regional efforts. Pollinatorsshould benefitfrom this change, because the pollinatorsof many plant species are not yet identifiedand standto gain protectionfrom blanketconservation efforts. Also, it is difficult to convince the public to devote resources to protectingsmall insect pollinatorswhose aesthetic beauty is not obvious to the unaidedeye. The broadcontext of habitat-or ecosystem-level conservation efforts is especially appropriatefor pollination systems because of the web of interactionsthat links plant species via pollinators(216, 232). Studies of several systems demonstratewhy an ecosystem-basedconservation strategyis valuable. A rare orchid in the western United States, Spiranthes diluvialis, requirespollinators,so managementplans must encompassthe maintenanceof bumblebees, which may be at risk from insecticide spraying on public rangeland(197). The habitatmust also be managedfor appropriate nest sites for bumblebees,and for floral diversityto provide nectar(the orchid produces none) and pollen for the whole flight season of bumblebees (199). Petit & Pors (158) calculatedthe carryingcapacity for nectar-feedingbats on the island of Curaqaoby using the daily availabilityof flowers on three species of columnarcacti. They estimatedthe carryingcapacityfor one bat species at 1200, about 300 more than the actual population,and suggested that removal
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of nativevegetationon the island shouldbe strictlyregulatedto preventfurther decline. Cropper& Calder (45) attributedthe lack of seed set of the rare and endangeredAustralianorchid Thelymitraepipactoides to the absence of pollinators and suggested elimination of naturalfire as the root cause. Burning stimulatesflowering in many coastal heathlandspecies, which helps to maintain high pollinatorspecies diversity. Kwak et al (118) pointed out the value of otherplant species in attractingbumblebeesto small populationsof the rare Dutch plantPhyteumanigrum. The dependenceof wild pollinatorpopulationson appropriatehabitatis increasinglyrecognized. A study of marginsof agriculturalfields (119) pointed out that small areas with flowering plants can be very effective at attracting andmaintainingpollinatorpopulations,includingSyrphidaeand otherDiptera. Habitat could be managed to encourage bumblebee and honeybee populations by providing a seasonal succession of suitable forage plants, protecting them from pesticides and herbicides and providing for long-term set-aside of fields (38, 145; see also 242). The last recommendationmakes sense because butterfliesand bumblebees tend to prefer flowers of perennials and because ground-nestingbees avoid recently disturbedareas (38). Such a policy could also benefit insect species that are not crop pollinators,e.g., satyridbutterflies (53). Conservationof bee habitatmay be the best means of reversingdeclines in pollinatorpopulations(172). In manypartsof the world this may mean conservationof human-madehabitats,some of which prove to be good substitutesfor threatened or destroyed natural habitats (47, 107,242). Many bee species have
colonized restoredareas along the Rhine River. Levees can provide prime bee habitat,especially when built of sand and gravel and managed for high floral diversity (107). Day (47) arguedthat as technology becomes more important and farming startsto decline in Europe, hedgerows, pastures, and woodlands should be regenerated.Disturbedurbanareasmay also be favorablefor some bee communities(189), althoughmultiple types of habitatmay be requiredto satisfy both foraging and nesting requirements(241). Some pollinatorsonly need a relativelysmall patch of habitatneartheirhost plants, but others require large areas. In Santa Rosa National Park in Costa Rica, thereare at least 40 species of sphingidmoths, which pollinate at least 50 plant species as adultsand which live for one generationin the parkduringthe beginningof the rainyseason beforemoving to otherpartsof the countryfor the rest of the year (89). For these and other migratorypollinators,conservation effortscan requirelargegeographicalareasand even internationalcooperation. Perhapsthe most extreme examples are migrantssuch as hummingbirds,butterflies,andmoths, which may be importantpollinatorsalong migratoryroutes extendingfor thousandsof kilometers(12,28,71,231).
Maintenance of Populations and Species in the Absence of Pollinators Relatively few examples exist of the absolute loss of pollinators,but this may reflect only our ignorance. Steiner (204) reportedthe loss of a specialized oil-collecting pollinator of a rare South African shrub, although subsequent work (205) led to discovery of a population where the predicted specialist pollinatorwas still present. Sipes & Tepedino(198, p. 164) suggested that one interpretationof the low visitationand fruit set to a rareplantfrom the western United States is that the original pollinator"is no longer consistently found within the plants' distribution."Lord (125) describeda New Zealandliane that has lost its bat pollinator. One effort thatmay, at least in the shortterm,prove fruitfulfor conservation is hand pollination of plants that have lost naturalpollinators. For example, Trifoliumrefiexum,a prairiespecies threatenedby loss of habitat,was brought into cultivationat the Chicago Botanic Garden,where handpollinationyielded thousandsof seeds for additionalrestorationefforts (208). Hand pollination has also been used for two Hawaiianspecies of Brighamia,whose few remaining individualshave apparentlylost their native pollinators (22), and for an endangeredorchidin Illinois (168). Biosphere 2, an experimentin which a small humanpopulationwas sealed in a (mostly) closed environmentfor 2 years, included a diversity of plants. All pollinatorsquickly went extinct so that most plant species "hadno future beyond the lifetime of individualsalreadypresent"(33). One conclusion is that maintenanceof normalplant-pollinatorrelationshipsis difficultand thatpeople in such circumstancesin the futureshould be preparedfor hand-pollinating. Anotherpossible solutionis the intentionalintroductionof exotic pollinators, although there are risks (10,51, 101,105). The first known example was the introductionof bumblebees to pollinate red clover in New Zealand (51, 65). Morerecently,weevils were introducedto pollinateoil palmsin Malaysia( 101), providingservices valued at $3 million per year (72, 187).
Changed Agricultural Practices and Uses of Pesticides and Herbicides In the United States alone, crop productionis reducedby about 8000 species of insects, 2000 species of weeds, 160 types of bacteria,250 types of viruses, and 8000 species of pathogenic fungi (9). Pesticides and herbicides seem an attractivesolutionbecause they can rapidlyreducenumbersof problemorganisms. However,new chemicals must be continuallydeveloped as pests evolve resistance and for otherreasons (9). One alternativeis to move to more laborintensivecontrolmethodsthatare more "friendly"to pollinators.For example,
some USDA studies comparingorganic farms and nearby farms using pesticides showed similarcropyields (9). The organicfarmscontrolledpests in ways that encouragednaturalpredatorsof pests and createdmore favorablehabitats for pollinators. Thereis an increasingemphasison preventingpollinatorloss due to application of crop pesticides. Toxicity levels of pesticides to honeybees are generally known (103), but this has not been useful in determiningthe effects on other bees (142). Toxicity is in partrelated to surface-to-volumeratio (91), so that bumblebees may be more tolerant, and small solitary bees more susceptible, than honeybees. In addition,details of pesticide use (such as timing, method of application, and formulation)can affect toxicity (43,142). Crops can be sprayedbefore or afterfloweringto minimize the chances of harmingpollinators (66). However,leafcutterbees may collect contaminatedleaf tissue for nest constructioneven when crops are not in flower (142). Timing of application within the day can also be critical. Although honeybees are not active at night, some bees, such as Nomia, rest in crop fields at night where they would be susceptibleto night spraying(142). Bees such as Apis andNomia forage as far as 13 km from the nest (142), so sprayingmay affect bees that nest far from fields. Honeybee apiariescan be either moved or closed-up during pesticide application,but nativebees are not as fortunate.Compoundssuch as benzaldehyde, propionicanhydride,andsome aminesmay proveuseful in repellingbees from fields duringpesticide application(142). Bran-baitsinstead of pesticide sprayingcould be used to kill grasshoppersin rangelands,therebypotentially reducingpollinatormortality(153). Few studies have systematically documented declines of bees other than honeybees (but see 99, 103 and references therein). Documentationcan be difficult because baseline data are generally unavailableand often the importance of non-Apisbees is poorly understood(142). However,enough is known about pesticide problems that much can be done to reduce pollinator losses (103). Kevan (103) suggested regulationand certificationfor pesticide users. In manycountries,regulationsarein place butviolationscarryminimalpenalties (103).
Reintroductions of Plants and Pollinators Reintroductionof endangered plants is still relatively uncommon (60). No plantreintroductionto date appearsto have been stimulatedby the need to support pollinatorpopulations,althoughexisting pollinatorsmay have benefited. Maunder's(131) paper on plant reintroductiondoes not mention pollinators, nor does that by Falk et al (60). One potential problem of reintroducinga plant species into an area is that duringits absence some nativepollinatorsmay have vanished. This loss would be most serious if the plant had a single pollinatorspecies, but such species
appearto be in the minority, and it is common for a plant to have multiple, sometimesvery numerous,pollinators(232). Giventhe variabilityamongyears that can be observed in pollinator populations (e.g. 31, 79, 95, 127, 157), multiplepollinatorsmay often be necessary for plant persistence(232). Hawaii providesone example of an introductionthat inadvertentlyfilled the role of a recently extinct pollinator. Cox (41) described the pollination of Freycinetiaarborea, the indigenousieie vine, by Zosteropsjaponica(Japanese White-eye, introducedin 1929). Museum specimens of threenativebirds,two extinctandone endangered,carriedpollen grainsfrom the plant,indicatingthat they were among the original pollinators. Lammerset al (120) reportedthat White-eyes also visit flowers of an endemic lobelioid, Clermontiaarborescen. Not all Hawaiianplants have been so lucky; some have gone extinct whereas othersare very rare.
Removal of Alien Pollinators Animals have been intentionallyintroducedbecause of their role as pollinators (e.g. honeybees, the alfalfa leafcutter bee). Some intentional introductions involve animals that pollinate but were not introducedfor that reason (e.g. Zosterops in Hawaii, possums in New Zealand) and some unintentional introductionsinvolve pollinators(e.g. cabbagebutterflies,fig wasps). In only a few cases have there been calls for the removalof introducedpollinators. The Europeanbumblebees that were introducedto Japanas pollinatorsof greenhouse crops escaped to establishferal populations. An effortto eradicatethem is underway(M Ono, personal communication). B. terrestriswas also introduced in about 1992 to Tasmania,where an attemptto eradicateit has had little success (163).
Domestication of Wild Bees and Other Pollinators Researchon non-Apisbees as crop pollinatorshas a long history(15, 224), but it recently has achieved new significance (220, 243). As early as the 1980s, concernswere raisedaboutthe need for an increaseddiversityof pollinatorsfor agriculturein North America (148, 172). At least 50 native bee species have been cultivatedexperimentallyor commercially(43, 172, 224, 225). Parkeret al (148) also discussed the use of dipteransas possible crop pollinators. A few success stories illustratethe potential for non-Apisbees as pollinators. The leafcutterbee (Megachile rotundata)was introducedfrom Asia into NorthAmerica and is the primarypollinatorof plantsgrownto producealfalfa seed (171, 220). In 1977, Osmia cornifrons was introducedfrom Japan as a pollinatorof apples; it has now been distributedto 23 states and 2 Canadian provinces (148; see also 172, 225). In the tomato industry,bumblebees can replacehumansequippedwith electric vibrators(the flowersrequire"buzzpollination"to release pollen) or sprayerswith syntheticplanthormonesto induce
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fruit production(124,148, 172). The bumblebee business originated in The Netherlandsabout a decade ago and has now spread as far as North America and Japan(124,148, 172).
Legal Protection Nearly25 %of the planet'svascularplantspecies may become extinctwithinthe next 50 years (170), and 22% of the species in the tUnitedStates is currentlyof conservationconcern(59). The situationfor most pollinatorsappearsless bleak because the numbersare smaller, but this may only reflect poorerknowledge of them. Both plants and pollinatorscan be affordedlegal protectionthrough the EndangeredSpecies Act in the United States and internationallyvia listing in the Conventionon InternationalTradein EndangeredSpecies of Wild Fauna andFlora(CITES).In the UnitedStates,only 390 of the 639 species of flowering plants affordedprotectionby the EndangeredSpecies Act had recovery plans as of December 1997 (http://www.fws.gov/hr9endspp/pltldata.html),andonly 16 species of butterflies, 1 species of fly, 1 species of moth, and 2 species of skippers (Lepidoptera)were included in the list as endangeredor threatened (http://www.fws.gov/r9endspp/invdata.html#Insects)as of that date. Three vertebratepollinators,two flying fox species andthe lesser long-nosedbat(Leptonycteriscurasoae), were also listed as of December 1997. The International Union for Conservationof NatureandNaturalResources(IUCN) now lists 165 generaof vertebratepollinators(including 186 species) of conservationconcern (140), which suggests a need for legal protectionfor many more.
Public Education Education efforts have helped bring publicity to bee conservationefforts in Europe, particularlyfor bumblebees. The Watch Trust for Environmental Educationengaged thousandsof volunteers,mostly children,to documentthe abundanceand distributionof Bombus species and to provide informationon preferredplantspecies (117, 146). The success of this surveyinspireda similar programin The Netherlands. In 1995, The Arizona-SonoraDesert Museum launchedthe ForgottenPollinatorsCampaign.The focus was to drawattentionto the impendingpollination crisis. The campaignincludedpublicationof a book (22), media campaigns,a researchprogramconductedby volunteers,developmentof pollinatorgardens at the museum,and othereffortsto increasepublic awarenessof the importance of pollinatorconservation.
PRIORITIESFOR FURTHERRESEARCH In virtually all cases, biologists must provide scientific information for conser-
vation decisions based on less-than-perfectknowledge. The best approachis
to base scientific input on the consensus of experts;this is vastly preferableto no scientific inputat all or to thatof a small minority(55). At the same time, it is importantfor pollinationbiologists to map out a researchprogramfor filling majorgaps in our knowledge, as we attemptto do here.
TheEcology of AnimalPollinators Typical ecosystems at intermediatelatitudes harboras many as several hundred pollinatinginsect species, most belonging to Hymenoptera,Lepidoptera, Diptera, and Coleoptera (79, 111, 134, 157, 210, 247). The vast majority of hymenopteranpollinatorsare solitary bees (237). Comparedwith our understandingof social bees, we still have much to learn about the nesting biology, demography,and trophicecology of most solitary bees and about the composition of local species assemblages (137, 215). Relative abundancesof given species of solitarybees fluctuatespatiallyandtemporally(31, 157), andwe need to understandhow this relates to floral resources(215). We also need to learn more aboutthe degreeof specializationof individualbee species andthe degree to which even specialists may use otherplant species (31, 46). The picturefor other insect orders is furthercomplicatedby the fact that larvae may require food plants that differ from those of adults. We need to learn how to manage landscapesthat will supportthe entire life cycle of such species (22, 14). Our knowledge of larvalecology is best for the Lepidopterabecause of the intense interestof naturalistsin butterflies(56). More effort needs to be expended in learningcomparableinformationaboutdipteranandcoleopteranlife cycles and larvaldiets. The role of flies as pollinatorsin many ecosystems seems to have been underestimateduntil recently (94, 157, 226, 247).
LinksBetween Pollinationand Plant PopulationDynamics The diversity of pollinatorsis matchedby local diversity of plant species and temporaland spatialvariationin species composition. For example, Tepedino & Stanton (217) reportedsubstantialyear-to-yearvariationin relative abundances and phenologies of differentflowers in a shortgrassprairiein Wyoming (see also 88, 166). Thus, a pollinatorforaging for floral rewardexperiences a complex and fluctuatingmarketplace.It is importantto characterizevariation in floralabundancemorecarefullyandto studyhow pollinationcontributesto it. Ecologists have assumedthatpollinationplays an importantrole in plantpopulationdynamics,butthereis virtuallyno empiricalevidence for it. We do know that pollination is often limiting to seed production(23), although resources (207) or both pollination and resources simultaneously (29, 135) can also be limiting. However, we need more experimentalmanipulationsof seed input, seedling establishment,and other stages of the life cycle with measurementof subsequentchanges (if any) in plantpopulationsize andstructure(1, 126, 129).
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In particular,it would be useful to design such studies so they help us to predict how reductionin pollination services will influence the demographyof plant species that are threatenedbecause of fragmentationof other anthropogenic insults.
The Nature of Interaction Webs Pimm (160) distinguishedfour aspects of ecological stability, one of which is resilience-the degree to which an ecosystem resists furtherchange following initial change. Pollination webs are threatenedwith the loss of component species andadditionof non-natives.The substantialconnectanceof pollination webs makes us suspect that such changes will elicit additional ones, perhaps even cascades of extinction. To our knowledge,nobody has modeled resilience (or other aspects of stability) specifically for mutualistic interactionssuch as those of plants and pollinators,much less studied resilience of such systems empirically.
CONCLUDINGTHOUGHTS The naturalhistory knowledge of pollinationgained over the last several centuries shows that animal-mediatedpollinationis essential for the sexual reproduction of most higher plants. Although many plants are iteroparous,with multipleopportunitiesfor sexual reproduction,spreadby clonal propagationor otherasexual means or having a dormantseed stage, these life-history features cannot compensate in the long term for a chronic loss of pollination services (16). A reductionin plantfecundityis of clear concernfor agroecosystemsbut equallyproblematicalfor naturalecosystems. Thereis indeeda strongargument to be made thatpollinationinteractionsare keystones in both human-managed and naturalterrestrialecosystems (102). In spite of centuries of study, our understandingof interactions between plants and animal pollinatorsis far from complete. Appreciatingthis was our motivationfor stressing that continuedresearchis essential to the long-term conservationof pollination systems. At the same time, we agree with others in political and scientific circles who urge ecologists to become more active in educating those around them about issues in conservation biology. The evidence on multiple fronts is sufficiently alarmingto conclude that there is an ongoing and pending ecological crisis in pollination systems. Although there are dangersin soundingthe alarmfor a pollinationcrisis, and hurdlesto be overcome in explainingthe issues to a wider audience,the alternativeshold far greaterrisks. Our understandingof the keystone role that pollinatorscan play in ecosystems aroundthe world, and the risks faced by both pollinatorsand the plants
they visit, has increasedgreatly duringthe past few decades. Research on endangeredplants, includingrehabilitationand reintroductionprograms,is more likely now thanin the past to include considerationof breedingsystems andthe potentialneed for pollinatorsin managementplans(97, 123). The conservation of insects and theirhabitatsis now a topic for discussion in the scientific literature (36). A decade ago, Feinsinger (62) -foundonly two papers that clearly relatedconservationand animal-flowerinteractions;now these topics are written aboutfrequently,as our review shows. Much progresshas been made since Kevan'splea arisingfrom concern aboutthe damageto pollinatorsfrom pesticide and herbicideuse in Canada(100). The most encouragingprogressis that we now recognize much more clearly what problemsexist and what we need to know to solve them. At the same time, many challengeslie ahead. We mustredoubleourresearch effortson basic aspectsof pollinationsystems at a time when it is difficultto obtain financialsupportfor work thatlacks immediatemanagementapplications. The pace of change in ecosystems and growthof threatsto pollination systems promise to increase in the future. We face acceleratedalterationof habitatby a growing human population, linked with acceleratedinvasion of non-native species, andthe prospectof global climatechange,which threatensto decouple plants and pollinators phenologically and ecologically (166). Although the challenges are daunting,they must be met with our most determinedefforts as ecologists and citizens. Visit the Annual Reviews homne page at http:Hwww.AnnualReviews.org
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Rapid Genetic Decline in a Translocated Population of the Endangered Plant Grevillea scapigera Siegfried L. Krauss, Bob Dixon and Kingsley W. Dixon Conservation Biology Vol. 16, No. 4 (Aug., 2002), pp. 986-994
Abstract Grevillea scapigera is one of the world's rarest plant species, currently known from only five plants in the wild. In 1995, 10 plants were selected from the 47 plants known at the time to act as genetically representative founders for translocation into secure sites. Ramets were micropropagated and introduced into one of these secure sites (Corrigin) in 1996, 1997, and 1998. By late 1998, 266 plants had been successfully translocated and were producing large numbers of seeds. With the development of an artificial seedgermination technique and because of an absence of seed germination in situ, seed was collected from these plants and germinated ex situ, and 161 seedlings were returned to the field site in winter 1999. We used the DNA fingerprinting technique of amplified fragment-length polymorphism (AFLP) to (1) assess the genetic fidelity of the clones through the propagation process, (2) contrast genetic variation and average genetic similarities of the F1s to their parents to assess genetic decline, and (3) assign paternity to the reintroduced seeds to assess the reproductive success of each clone. We found that 8 clones, not 10, were present in the translocated population, 54% of all plants were a single clone, and the F1s were on average 22% more inbred and 20% less heterozygous than their parents, largely because 85% of all seeds were the product of only 4 clones. Ultimately, effective population size (Ne) of the founding population was approximately two. Our results highlight the difficulty of maintaining genetic fidelity through a large translocation program. More generally, rapid genetic decline may be a feature of many translocated populations when Ne is small, which may ultimately threaten their long-term survival Strategies to reverse this genetic decline include equalizing founder numbers, adding new genotypes when discovered, optimizing genetic structure and plant density to promote multiple siring and reduce kinship, promoting natural seed germination in situ rather than artificially germinating seeds ex situ, and creating a metapopulation of numerous translocated populations to restore historical distribution patterns and processes.
OIKOS 105: 481 /488, 2004
Population size and the risk of local extinction: empirical evidence from rare plants Diethart Matthies, Ingo Bra¨uer, Wiebke Maibom and Teja Tscharntke
Matthies, D., Bra¨uer, I., Maibom, W. and Tscharntke, T. 2004. Population size and the risk of local extinction: empirical evidence from rare plants. / Oikos 105: 481 /488. Due to habitat fragmentation many plant species today occur mainly in small and isolated populations. Modeling studies predict that small populations will be threatened more strongly by stochastic processes than large populations, but there is little empirical evidence to support this prediction for plants. We studied the relationship between size of local populations (number of flowering plants) and survival over ten years for 359 populations of eight short-lived, threatened plants in northern Germany (Lepidium campestre, Thlaspi perfoliatum , Rhinanthus minor, R . serotinus, Melampyrum arvense, M . nemorosum , Gentianella ciliata and G. germanica ). Overall, 27% of the populations became extinct during the study period. Probability of survival of a local population increased significantly with its size in all but one species (R. minor ). However, estimated population sizes required for 90% probability of survival over 10 years varied widely among species. Survival probability increased with decreasing distance to the nearest conspecific population in R . serotinus, but not in the other species. The mean annual growth rate of surviving populations differed greatly between species, but was only for G. germanica significantly lower than 1, suggesting that there was no general deterministic decline in the number of plants due to deteriorating habitat conditions. We conclude that the extinction of populations was at least partly due to stochastic processes. This is supported by the fact that in all species a considerable proportion of small populations survived and developed into large populations. D. Matthies, Plant Ecology, Dept of Biology, Univ. of Marburg, DE-35032 Marburg, Germany ([email protected]). / I. Bra ¨ uer, W. Maibom and T. Tscharntke, Agroecology, Univ. of Go ¨ ttingen, Waldweg 26, DE-37073 Go ¨ ttingen, Germany. Present address for IB: Dept of Agricultural Economics, Platz der Goettinger Sieben 5, DE-37073 Go ¨ ttingen, Germany.
Habitat fragmentation is one of the main threats to biodiversity. Because of the destruction and fragmentation of habitats many species today occur mainly in small and isolated populations, which for a number of reasons are expected to face a high risk of extinction. In small patches habitat quality may deteriorate (Oostermeijer et al. 1994a) and modelling studies suggest that small populations will be particularly vulnerable to the effects of demographic, environmental and genetic stochasticity (Goodman 1987, Menges 1991a). While demographic stochasticity is only a threat to very small
populations, environmental stochasticity has been identified as the most important factor threatening extinction to fragmented populations (Lande 1993, Wissel and Zaschke 1994, Menges 1998, Holsinger 2000). Predicted genetic consequences of small population size are increased inbreeding, loss of genetic variation due to genetic drift and the accumulation of deleterious mutations (‘‘genetic erosion’’, Ouborg et al. 1991, Young et al. 1996, Dudash and Fenster 2000). In the short term, genetic erosion may result in a decline of individual fitness and in the long term in a loss of evolutionary
flexibility, which may decrease the potential for a population to persist in the face of environmental change (Huenneke 1991, Ellstrand and Elam 1993). Genetic variability in small plant populations is often reduced (van Treuren et al. 1991, Ellstrand and Elam 1993, Fischer and Matthies 1998a) and some studies have also found a reduced performance of offspring and lower plasticity (Menges 1991b, Oostermeijer et al. 1994a, Fischer and Matthies 1998b, Ke´ry et al. 2000). Moreover, in small populations important interactions with mutualists like pollinators and seed dispersers may become disrupted (Kearns et al. 1998). Because plants in small and isolated patches receive fewer visits from pollinators, fecundity may be reduced due to insufficient ˚ gren 1996, Groom pollination (Lamont et al. 1993, A 1998, Steffan-Dewenter and Tscharntke 1999). Pollen quality may also be lower because in small patches pollination will often be between close relatives. In selfincompatible species reproduction may be reduced in small populations due to a lack of incompatibility alleles (Byers 1995) and in heterostylous species because of unequal morph ratios (Ke´ry et al. 2003). The negative effects of fragmentation on reproduction and on the performance of offspring should affect the dynamics and survival of populations of short-lived species relatively quickly, because population persistence depends on frequent recruitment. In contrast, in longlived species the negative consequences of reduced population size and increased isolation may not become visible for a long time, because established plants often have low mortality (Oostermeijer et al. 1994b, Colling et al. 2002). With respect to the conservation of biodiversity the most important question is what combined effect the various negative effects of reduced population size have on the persistence of populations. It has been suggested that populations reduced below a certain threshold number of individuals may enter a so called extinction vortex, i.e. a downward spiral of ever decreasing population size and plant fitness that may drive a population to extinction (Gilpin and Soule´ 1986, Lamont et al. 1993). However, while there is some direct empirical evidence from animal studies for the negative effects of small population size on the survival of local populations (Pimm et al. 1988, Berger 1990, Thomas 1994a, Lima et al. 1996, Krauss et al. 2003), little such evidence exists for plants. Empirical studies require longterm data on the dynamics and survival of populations which are rarely available for plants. Previous studies have therefore used substitutes for population size like site area (Ouborg 1993) or mean cover (Fischer and Sto¨cklin 1997). In an exceptional programme, the distribution and size of the populations of all endangered plant species had been recorded in the mid 1980s in the state of Lower Saxony in northern Germany (Garve 1994). We 482
re-visited 359 populations of eight short-lived endangered plants ten years later, recorded the number of individuals and used the data to analyse the relationship between the size of local plant populations and their probability of survival. We were also interested in the population size required for survival of populations of the various species. In addition, we studied the mean population growth rate of surviving populations to detect a possible general deterministic decline of species and asked whether there was evidence for extinction vortices, i.e. whether small populations were doomed to become extinct.
Material and methods For the study we selected eight short-lived species which are endangered in northern Germany (Garve 1994) and whose populations are concentrated in southern Lower Saxony: Lepidium campestre (L.) R. Br, Thlaspi perfoliatum L. (Brassicaceae), Rhinanthus minor L. , R . serotinus (Scho¨nh.) Oborny, Melampyrum arvense L. , M . nemorosum L. (Scrophulariaceae) and Gentianella ciliata L. Borkh. and G. germanica (Willd.) Bo¨rner (Gentianaceae). The Rhinanthus spp., Melampyrum spp. and T. perfoliatum are annuals, Lepidium campestre is annual or biennial, G. germanica is a biennial and G. ciliata has been classified as both a biennial and a perennial (Kutschera and Lichtenegger 1982 /1992, Ja¨ger and Werner 2002, Oberdorfer et al. 2002). We selected short-lived plants for the study, because in these species population turnover and extinctions should be most pronounced. The studied plants have no clonal growth and are propagated only by seeds. All species had populations in calcareous grasslands, but the main habitats of M. nemorosum are the margins of woodlands (Matthies 1991) and most populations of L. campestre are found at waysides and in old quarries (Bra¨uer, unpubl.). As part of the plant assessment programme of the state of Lower Saxony, data on the exact location of all populations of rare and endangered plants in Lower Saxony had been recorded since 1982, together with an estimate of the size of populations (Garve 1994). The number of individuals (flowering plants) in each population had been recorded in eight classes (1, 2 /5, 6 /25, 26 /50, 51 /100, 101 /1000, 1001 /10 000, 10 001 /100 000 individuals). In 1996, based on the old records, 359 populations of the study species (36 /54 for each species) in southern Lower Saxony were selected for the study. Care was taken to select for each species a balanced sample of populations of different size. Sites that had obviously been destroyed or strongly disturbed were excluded. In summer and autumn 1996, at the time of peak flowering of the study species, all selected sites were visited and an extensive search for the plants was carried out. If OIKOS 105:3 (2004)
individuals of the study species were still present, the number of flowering plants was recorded. For each population the distance to the nearest population was determined from a map. We used logistic regressions to relate the presence and absence of the species at a site to population size in the mid-1980s and the distance to the next population. The mean recording year was 1986, so we will always refer to 1986 in the following. For the analyses, the geometric mean of the upper and lower boundaries of the old size classes was used as an estimate of population size. Backward elimination based on likelihood ratios was used to derive a model that contained only significant predictors. If population size had a significant effect on population survival, the regression was used to calculate the population size necessary for a 90% probability of survival over 10 years. This is an estimate of a minimum viable population size (Menges 2000) and serves as an overall indicator of a species’ sensitivity to fragmentation. We used a 90% rather than a 95% probability of survival because errors strongly increase near the upper limit of survival values. Mean annual growth rates for the surviving populations were calculated as l/(population size in 1996/ pop. size in the mid 1980s)1/n , where n is the number of years between surveys. Differences among species in mean annual growth rate were tested by analysis of variance and deviations of growth rates from 1 (i.e. no change in population size over time) were analysed with t-tests. All analyses were carried out with SPSS for Windows 10.0.
Results Overall, 73% of the study populations that had been present in 1986 still existed in 1996. The proportion of surviving populations varied among the eight species (chi2 /13.7, df /7, p/0.057). While 84% of the popu-
lations of R. minor had survived, only 56% of those of L. campestre still existed (Table 1). Pooled over all species, large populations had a much higher chance of survival than small populations (chi2 / 67.0, df /7, pB/0.001). Most of the populations consisting of less than 6 plants in 1986 did not survive until 1996, whereas 100% of those with more than a 1000 individuals survived (Fig. 1). The relationship between population size and survival in the individual species was analysed by logistic regression. In seven out of the eight studied species the probability of survival of a population significantly increased with its size (Fig. 2, Table 1). Only in R. minor, the species with the smallest decline in the number of populations, no significant relationship between population size and probability of survival was found (p/0.29), but the logistic regression coefficient had the expected sign. However, there was large varia-
Fig. 1. The relationship between the size of a plant population in 1986 and its probability of survival until 1996. Data were pooled over all eight study species. To achieve sufficient samples sizes, data for populations with less than 6 flowering plants were pooled and the one population with more than 10 000 individuals was pooled with those of the next smaller size class. Numbers denote the number of populations in the respective size category.
Table 1. Proportion of populations surviving from 1986 /1996 and logistic regression equations relating survival probability to population size for eight rare plant species in Northern Germany. *, pB/0.05; **, p B/0.01; ***, pB/0.001. The probability of survival is given by elinear predictor/(1/elinear predictor). In the linear predictor, x/log10 (population size) and y/log10 (distance to the nearest population in km). The distance to the nearest population had a significant effect (chi2 /5.8, p B/0.05) only in Rhinanthus serotinus. N90% gives the calculated population size necessary for a 90% probability of survival over 10 years. N90% was calculated as 10[ln(0.9/0.1)a]/b, where a and b are the constant and the slope parameter from the linear predictor, respectively. Species
Proportion surviving (%)
Lepidium campestre Melampyrum nemorosum Gentianella germanica Rhinanthus serotinus
56 79 66 81
Gentianella ciliata Melampyrum arvense Thlaspi perfoliatum Rhinanthus minor
Fig. 3. The proportion of small populations (B/100 individuals in 1986) of eight threatened plants that became extinct, stayed small or developed into large populations ( /100 individuals) from 1986 /1996. L.c., Lepidium campestre; G.c., Gentianella ciliata ; G.g., Gentianella germanica ; M.n., Melampyrum nemorosum ; R.s., Rhinanthus serotinus, T.p., Thlaspi perfoliatum ; M.a., Melampyrum arvense ; R.m., Rhinanthus minor.
tions (l) was not significantly different from 1 (t-test, p/0.05), i.e. their size in 1996 was about the same as in 1986 (Fig. 4). In three species (L. campestre, R. minor and R. serotinus ), mean population size increased significantly (l/1, pB/0.05) and only in G. germanica did the mean size of the surviving populations decrease (l/0.43, pB/0.05) during the study period. Fig. 2. The relationship between size of a population in 1986 and its probability of survival until 1996 for eight endangered plant species in southern Lower Saxony, Germany. Time between surveys had no significant effect (pB/0.05 for all species). Logistic regression curves are shown if significant. Open circles denote single populations, filled circles several populations of the same size class.
tion among species in the number of plants necessary in a population to make its survival likely. The population size necessary for 90% probability of survival over 10 years varied from 71 individuals for L. campestre to 1276 for M. arvense (Table 1). In R. serotinus survival probability of a population not only increased with its size, but also with decreasing distance to the nearest population. In all other species distance had no effect. Not all small populations were doomed to extinction. While many of the small populations with less than 100 individuals became extinct, a considerable proportion survived in all species as small populations and some even developed into large populations ( /100 individuals, Fig. 3). This was true even for the very small populations (B/26 plants). The mean annual growth rate (l) of the surviving populations during the study period differed strongly among the eight species (F7,252 /5.7, p B/0.001). In four of the species (G. ciliata , M. arvense, M. nemorosum and T. perfoliatum ), the mean annual growth rate of popula484
Discussion In seven of the eight studied plant species the probability of survival increased significantly with population size. In R. minor the overall risk of extinction was relatively low and the relationship between survival and popula-
Fig. 4. Mean annual growth rate of surviving populations of eight threatened plants from 1986 to 1996. Vertical bars denote the 95% confidence intervals. Asterisks indicate growth rates significantly different from 1. *, pB/0.05; **, p B/0.01. For explanation of species abbreviations see Fig. 3. OIKOS 105:3 (2004)
tion size was not significant, but the regression coefficient had the expected sign. Thus, our results provide empirical evidence for the suggested important role of small population size for the extinction of local plant populations (Menges 1991a, 1998). Similar observations have been made in studies that have investigated the relationship between population size and survival in animals, e.g. in birds (Pimm et al. 1988, Bellamy et al. 1996), bighorn sheep (Berger 1990), small mammals (Lima et al. 1996) and butterflies (Thomas 1994a, Nieminen 1996, Krauss et al. 2003). Two previous studies on plants, which were, however, not based on actual numbers of plants, but used substitutes like species area (Ouborg 1993) or cover (Fischer and Sto¨cklin 1997) for population size, have also reported negative effects of small population size on survival. In contrast, Husband and Barrett (1996) found no such relationship in Eichhornia paniculata, an aquatic plant of ephemeral pools in north-east Brazil, which they attributed to the frequent catastrophic changes in local environmental conditions that result in the extinction of populations regardless of their demographic characteristics. There are several possible explanations for the observed relationship. First, there could have been a general deterministic decline in population sizes in the study area due to habitat deterioration. For a given decline, small populations are likely to become sooner extinct than large ones (Thomas 1994b). However, only in one species (G. germanica ) a significant decline in mean population size of surviving populations was observed over the study period. Our estimate of the mean growth rate was based on the growth rate of populations that survived. Because populations with low growth rates will go extinct more often than those with a high growth rate, the mean growth rate of all populations was probably somewhat lower. However, even including populations that became extinct, overall more than 40% of all populations had stable population sizes or increased in size. Thus, a general deterministic decline in the number of individuals is unlikely as an explanation for the observed relationship between population size and extinction. Second, although no general decline in population sizes was found, the higher extinction rate of small populations could be due to a deterministic decline of the number of individuals in small populations. Populations that were small in 1986 might have been small because they occurred in habitats where conditions had deteriorated and thus might have been on their way to deterministic extinction. Negative changes in habitat quality cannot be excluded and may well have contributed to the observed local extinctions. However, in all species a considerable proportion of the small populations survived and even developed into large populations, indicating that habitat quality was not always OIKOS 105:3 (2004)
worse in small than in large populations. This suggests that stochastic processes were at least partly responsible for the increased extinction risk of small populations. Environmental stochasticity is the most likely cause, but genetic stochasticity might have contributed, e.g. in the case of Gentianella germanica (Fischer and Matthies 1998a, b). Simulation studies suggest that even moderate fluctuations of environmental quality greatly increase the extinction risk for small populations (Menges 1998). In contrast to earlier studies involving plants, in the present study the precise location and the number of individuals was known for each population. This made it possible to analyse empirically the relationship between the number of individuals in a plant population and its survival probability and to estimate the number of plants necessary for a certain probability of survival (‘‘minimum viable population size’’, MVP, e.g. Menges 2000). These empirical estimates have the advantage that they are based on observations of real extinction events in a large number of populations over a comparatively long period of time, whereas most simulation studies of extinction risks for plants are based on few populations and demographic data from less than five years (Menges 2000). In contrast, simulation models have the advantage that they are far more versatile, can be used to study different scenarios (e.g. effects of managements) and cover different periods of time. The quantitative estimates of MVPs must, however, be viewed with caution, because due to the log-scale for population size small changes in the relationship will result in large changes in the estimated MVP (Fig. 2). Overall, the results show that very small populations of the studied short-lived plants faced a considerable risk of extinction even over a period of only ten years, while the risk for populations with /1000 individuals was very small. Judged by their MVPs (71 /1276 individuals for 90% probability of survival over ten years) there was considerable variation among the studied species in the number of plants necessary to make survival of a population likely. These differences are not easily explained by life-history traits of the plants. Traits that are known to affect the risk of extinction include longevity and the size and persistence of the seed bank (Pimm et al. 1988, Sto¨cklin and Fischer 1999). The studied species are all short-lived and most have transient seed banks (Melampyrum : Matthies 1991, Rhinanthus : Ter Borg 1985, G. ciliata , Thompson et al. 1997) or seed banks that are short-term persistent but depleted quickly (L. campestre, Roberts and Boddrell 1983). Of the two species with a more persistent seed bank (Baskin and Baskin 1979, Fischer and Matthies 1998c), G. germanica had a much larger MVP than had T. perfoliatum. Moreover, closely related pairs of species with the same life-history like Melampyrum arvense and M. nemorosum and Rhinanthus serotinus and R. minor, 485
differed strongly. This suggests that differences in maximum population growth rates (Fagan et al. 2001), about which little is known for plants, or individual combinations of traits may be responsible for the differences in the number of plants necessary to make population survival likely. Based on simulation models the number of plants necessary to ensure a risk of extinction of less than 5% over 100 years has recently been estimated as 170 plants for the long-lived forest perennial Panax quinquefolium (Nantel et al. 1996) and as 25 genets for the clonal perennial woodland herb Asarum canadense (Damman and Cain 1998). The risk of extinction increases with the length of the time period considered and the required survival probability and these estimates of MVPs are therefore not directly comparable to the values obtained in the current study. However, although we considered a much shorter period of time and allowed a higher risk, most of our estimates of MVPs were much higher than the quoted numbers, suggesting that the studied species are far more sensitive to small population size than Panax and Asarum . These differences are consistent with the expectation that short-lived plants are more sensitive to environmental stochasticity than long-lived plants (Pimm et al. 1988, Quintana-Ascencio and Menges 1996), at least in the absence of a persistent seed bank. The persistence of populations could in principle reflect re-colonisations rather than real persistence. If re-colonisations were frequent one would expect populations that were close to another population to have a lower probability of extinction. However, only in R. serotinus was survival related to the distance to the nearest conspecific population. Moreover, none of the studied species has special adaptations to the long range dispersal of seeds and for most of them it is known that dispersal is very limited, e.g. for Melampyrum spp. (Matthies 1991), L. campestre (Thiede and Augspurger 1996), G. germanica (During et al. 1985, Fischer and Matthies 1998a, b) and Rhinanthus spp. (Ter Borg 1985). Moreover, very few new populations have been found in Lower Saxony despite the long-time assessment programme and, even in those cases, it cannot be excluded that they had only been overlooked earlier (E. Garve, pers. comm.). Thus, the studied plants belong to the many species for which in the current fragmented landscape metapopulations do not occur at a steady state because there is less colonisation than extinction (Hanski et al. 1996). In conclusion, our results provide empirical evidence for the predicted negative relationship between size and probability of extinction of local plant populations and stress the importance of stochastic factors for extinction. However, the results also suggest that the number of individuals required to make population survival likely may vary strongly even among closely related species 486
(Franklin 1980). Small populations of rare species have sometimes been considered to have negligible conservation value (Lesica and Allendorf 1992, Lamont et al. 1993), because it has been suggested that below a certain threshold size local populations will enter an extinction vortex, i.e. a spiral of ever decreasing population size (Gilpin and Soule´ 1986, Lamont et al. 1993). However, there may be some hope even for quite small plant populations, as exemplified by the fact that in all studied species some very small populations survived and developed into large populations, suggesting that extinction is not inevitable. Acknowledgements / We thank the ‘‘Niedersa¨chsisches ¨ kologie’’ and in particular Eckard Garve, for Landesamt fu¨r O access to the data of the plant assessment programme. Henrik Berg, Roland Brandl and Eric S. Menges provided valuable comments on the manuscript.
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