Ecology. 75(3), 1994, pp. 584-606 «;) 1994 by the Ecological Society of America

EVALUATING APPROACHES TO THE CONSERVATION OF RARE AND ENDANGERED PLANTS'

DOUGLAS W. SCHEMSKE, BRIAN C. HUSBAND, MARY H. RUCKELSHAUS, CAROL GOODWILLIE, INGRID M. PARKER, AND JOHN G. BISHOP Department of Botany, University of Washington, Seattle, Washington 98195 USA

Take your time, hurry up, the choice is yours, don't of genetic variation in rare plant species is a key con­ be late sideration in conservation strategies," while Holsinger -Nirvana and Gottlieb ( 1991) note that "populations large enough to mitigate ecological threats to population viability INTRODUCTION will mitigate genetic ones as well" ( 1991 :205) and that Nearly 25% of the estimated 250 000 species of vas­ "active management of the genetic structure of an en­ cular plants in the world may become extinct within dangered plant species will require an enormous in­ the next 50 yr (Raven 1987), and 22% of vascular plant vestment of time, money, and expertise. Only a few of species in the United States are currently of conser­ the most important species will warrant such heroic vation concern (Falk 1992). Plant conservation efforts efforts" ( 1991:206). With limited funds and such con­ received a critical boost with the passage of the En­ trary points of view, the conservation biologist charged dangered Species Act of 1973 (16 U.S.C. §§ 1531- with species recovery faces an unenviable challenge. 1544: USFWS 1988a). The Act established a legal The successful recovery of an endangered species mandate of unprecedented proportions to promote the requires the best scientific information available, yet collection, analysis, and exchange of biological infor­ the present level of understanding and communication mation. It requires that for each endangered or threat­ among research scientists and resource managers is not ened species occurring in the United States, a recovery sufficient to gather and transmit this information. Our plan be developed which "delineates, justifies, and objective in this paper is to integrate the theory of plant schedules the research and management actions nec­ population dynamics and academic research on rare essary to support the recovery of a species" (16 U.S.C. plants with the practical task of setting guidelines for §§ 1531-1544: USFWS 1988a). species recovery. The conservation biologist is faced with the daunting First, we provide a general review of the ecological task of identifying the biological information needed and genetic factors influencing demographic changes to evaluate the causes of endangerment and ensuring at population and metapopulation levels. Second, we the continued survival of the target species in nature, review research on rare plants surveyed in the scientific as well as developing criteria to determine when re­ literature and evaluate its usefulness in conservation. covery is achieved. The writing and implementation Third, we identify the biological information necessary of recovery plans is made more difficult by levels of for developing recovery guidelines and outline a re­ funding that preclude extensive biological research for search approach. This includes assessing the biological every species. This problem is especially acute for plants. "status" of rare species, identifying life history stages Although nearly 50% of the 728 federally listed threat­ most critical to population growth, and identifying the ened or endangered species are plants (USFWS 1992a), biological causes of demographic variation at these they received only 8% of recovery funds spent by the stages. Fourth, we review recovery plans written for U.S. Fish and Wildlife Service in 1990 (Campbelll991). 98 species of plants listed as threatened or endangered Deciding on an appropriate course of action is fur­ by the U.S. Fish and Wildlife Service. Here we present ther complicated by contrasting opinions presented in information on the biological status of federally listed the conservation literature. One important controversy species, discuss research recommendations, and eval­ regards the relative importance of genetic and demo­ uate criteria used to establish recovery targets. Finally, graphic approaches in conservation efforts (Lande we discuss the importance of biological, political, and 1988). Falk (1992:408) suggests that "the distribution economic constraints to recovery efforts, suggest bio­ logical guidelines for the recovery ofendangered plants, and identify research priorities in plant conservation. ' For reprints of this Special Feature, see footnote I, p. 583. We conclude with a discussion of the need for more April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 585

allele no., frequency ·~ "~,,,,. ~,,, .,,~ ~J.. • ~~0.6 heterozygosaty. ··~ ~~· ,,,,,, ...,,,,. ~ ~ -~ ···-.06~ -~~ ~ "l ...,,,,,,. (!! • ~,,,,;.% ~ ,,,%..0. "~_,.~A S :... .,,_..._,-,.., f'I.Y.A· ·~ ~ .,,,. "'ta: "~ vo/ 0 ~ ...,,,,.7'14 ~'- t) § .,,,,,. ;,r.rJ.i· .,,~ :i § ,,,,. Oq ~ 0 ~ :ill',,,,,, .,,,~, od t. PolJe . ,,,,, ' repr uc ave ~lation ····~, ·~ system --....-.... ~ ~ demographic stochasticity .. dbi;tthh, grot wth, . a1 . . ea ra es eco1 og:tc mteracuons: frequency-/density-dependent + independent effects

FIG. I. Schematic of the ecological (solid arrows) and genetic (hatched arrows) processes affecting within-population dynamics in plants. Population size at time t and t + I is represented by a solid box. Note that processes operating at the scales represented here and in Fig. 2 are not independent. For example, within-population dynamics can affect the size of the metapopulation through local extinctions. effective communication between academic research­ ers and conservation managers. Within-population dynamics The growth or decline of a population is determined FACTORS AFFECTING SPECIES ABUNDANCE by its vital rates, i.e., birth, growth, and death (Caswell To assess the status of rare plant species, and to 1989). Fig. 1 illustrates how the ecological and genetic prioritize among conservation approaches, we must characteristics of populations may influence vital rates first understand the factors that affect the numbers of and how the resulting population size in tum impacts individuals within a species. Plants may pose chal­ the genetic and demographic composition of the pop­ lenges to conservation efforts that are quite distinct ulation. Examples of these processes are listed in Table from those of animals. Unique plant characters include I. For example, Doak's study (1992, cited in Table 1) seed dormancy, a diversity of mating systems from self­ exploring the effects of herbivory on the demography fertilization to complete outcrossing, and frequent re­ of dwarffireweed (Epilobium latifolium) is an example liance on animals for the dissemination of pollen and of an ecological factor with frequency-dependent effects seeds. At some spatial scale, most plant species are on population vital rates and growth rate [represented patchily dist1ibuted due to their sedentary habit and in Fig. I by the horizontal arrow from N,(t) to birth, the spatial heterogeneity of the environment (Levin growth, and death rates, and N,(t + !)].Similarly, Ells­ and Kerster 1974, Holland and Jain 1981, Han ski 1985, trand and Antonovics ( 1985, cited in Table I) found Platt and Weiss 1985, Horvitz and Schemske 1986). that populations of sexually derived individuals had Patchy distributions have been further exaggerated by higher survivorship and fecundity than did populations the activities of humans through habitat destruction of asexually derived individuals (represented in Fig. I and fragmentation. Therefore, predicting extinction or, by the hatched arrow from allele number and allele conversely, ensuring the persistence of species, requires frequency to birth, growth, and death rates.) ecological and evolutionary information at more than Ecological interactions between plants and their en­ one spatial scale. In this section we briefly summarize vironment can influence population growth rates via (I) how within-population dynamics are affected by their effects on fecundity, growth, or survivorship of ecological and genetic attributes, and (2) the ways in individuals (Fig. 1, Table 1). These interactions can be which the dynamics of a metapopulation are affected density-dependent or -independent (Harper 1977, An­ by extinction and colonization patterns. tonovics and Levin 1980). Ecological processes such 586 SPECIAL FEATURE Ecology, Vol. 75, No. 3

TABLE I. Selected examples from the literature illustrating the diversity of ecological and genetic factors influencing population vital rates (see Fig. 1). For each study, we report the independent variable measured (factor affecting vital rate), the vital rate affected (b = birth rate and early establishment, g = growth, d = death), and whether its effect on population growth rate (A.) was measured directly ( + = yes, - = no).

Vital rate A. estimated Independent variable affected directly? References Ecological Environmental variability b,g,d + Aberg 1992 b,g,d + Silva et al. 1991 Intraspecific density b,g,d Watkinson and Harper 1978 b,g Keddy 1981 Interspecific competition g + Tilman and Wedin 1991 b,g,d + Gurevitch 1986 Herbivory b,g,d + Rausher and Feeny 1980 b,g,d + Doak 1992 Mutualisms g,d Janos 1980 g,d + Hanzawa et al. I 988 Pathogens b,d Alexander and Burdon 1984 b,d + Alexander and Antonovics I 988 Pollinators (pollen limitation) b Bierzychudek 1981 b Johnston I 991 Dispersal b Augspurger and Kelly I 984 Genetic Heterozygosity b,g,d Schemske 1983 b,g,d Holtsford and Ellstrand 1990 g,d Groves et al. 1990 Allelic diversity b,g,d + Ellstrand and Antonovics 1985 self-incompatibility alleles b Thien et a!. 1983 b DeMauro I 993

as pollination, which require a minimum density of A recent study of population regulation in mosquitofish individuals, may be particularly important in small (Gambusia holbrooki) found no detectable effect of ge­ populations (Allee et al. 1949, Powell and Powell1987). netic composition on population growth rate (Leberg In addition, biotic interactions such as herbivory may 1993, also see Ayala 1965 for Drosophila). In spite of be enhanced along the edges of a population as a result theoretical relationships between genetic diversity and ofhabitat fragmentation (Lovejoy et al. 1983, Thomp­ species persistence, no empirical evidence exists that son 1985). Clearly the ecological factors shown to in­ directly links the genetic composition of plant popu­ fluence vital rates are diverse (Table 1); however, their lations to their growth rate or survival. direct effects on growth and persistence of populations In addition to the deterministic processes described have received comparatively little attention. above, stochastic processes also affect the demographic Population genetic processes can influence vital rates and genetic composition of populations (May 1973, through changes in the number and organization of Brossard and Gilpin 1989) and therefore can impact alleles within and among individuals. As with ecolog­ vital rates (Fig. 1, Table 1). The effects of such sto­ ical factors, processes affecting genetic diversity in pop­ chasticity are most acute in small populations. For ulations can be density (or frequency) -dependent or instance, chance variation in fecundity among indi­ -independent (Nei 1975, Hedrick 1983) (Fig. 1). These viduals in plant populations is common (Crawford processes can result in changes in the number or fre­ 1984, Heywood 1986), and as population size shrinks, quency of alleles in populations and in levels of het­ the birth rate will reflect the collective fecundities of erozygosity. Both variables have been shown to be re­ those individuals that persist. Stochastic loss of alleles lated to vital rates in some plant species (Table 1). In for quantitative and single gene traits occurs at higher theory, reduced heterozygosity can result in decreased rates in small populations (Nei et al. 1975, Houle 1989, population growth due to inbreeding depression Polans and Allard 1989, Barrett and Kohn 1991, (Charlesworth and Charlesworth 1987). Allele richness Mitchell-Olds 1991), which may affect the evolution­ could contribute to population growth through its effect ary potential of a species. on evolutionary potential, or the ability of a species to As a result of an increased importance of stochastic respond to changes in its selective environment (Koehn processes and changes in ecological interactions in de­ and Hilbish 19 8 7; R. Lande, unpublished manuscript). clining populations, the probability of a population's April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 587

Metapopulation Size (t) Metapopulation Size (t + 1)

Population size Ni (t) Population size Ni (I+ I)

Nl Nl

--+-- within population dynamics

within population --+--dynamics

FIG. 2. Schematic of the ecological (solid arrows) and genetic (hatched arrows) processes affecting metapopulation dynamics in plants. The metapopulation at time t and t + I is represented by an array of n suitable habitats, which are either occupied (solid boxes, N '"I' 0) or empty (open boxes, N = 0). Migration between extant populations and colonization of unoccupied habitats are depicted by curved arrows. One colonization and one extinction event among the four habitat patches are depicted. Note that processes operating at the scales represented here and in Fig. I are not independent. For example, metapopulation processes can influence the dynamics of individual populations through the quantity and quality of migrants and colonists. extinction is expected to be negatively correlated with its size (MacArthur and Wilson 1967, Richter-Dyn and Metapopulation dynamics Goel 1972, Leigh 1981, Wright and Hubbell 1983). In many plants, factors influencing the number of Schoener and Spiller (1987) found that small popula­ populations may be as important as within-population tions were more likely to go extinct than large ones in dynamics in determining whether a species persists or several species of Bahamian spiders, and a simulation becomes extinct. The geographic structure of such spe­ developed by Shaffer and Samson (1985) predicted that cies can be described as a metapopulation, or popu­ the probability of extinction increased in smaller pop­ lation of populations (Levins 1970). Metapopulation ulations of grizzly bears. The relationship between pop­ structure has been included in several mathematical ulation size and extinction probability is not as clear models of population dynamics that are relevant for for plant species. Several studies suggest that external plants (Levins 1969, Bailey 1975, Anderson and May factors, such as large-scale environmental variation and 1986, Fahrig 1988, Hastings and Wolin 1989, Hastings dispersal rates, which may be independent of size, can 1991). As depicted in Fig. 2, these models usually in­ be more important determinants of plant population volve an array of discrete, suitable habitats, of which extinction (Quinn and Hastings 1987, Robinson and only a fraction are occupied at one time. In reality, Quinn 1988, Bowles and Apfelbaum 1989, Menges habitat patches differ in size, quality, and spatial dis­ 1990; B. C. Husband and S. C. H. Barrett, unpublished tribution, and the metapopulation constitutes not just data). the number of populations but their size distribution, In summary, population dynamics are a function of spatial arrangement, and genetic heterogeneity. Change genetic and ecological processes. In addition to these in the size of the metapopulation from time t to t + 1 intrinsic characteristics of populations, immigration and depends on extinction and colonization rates (Levins emigration of individuals can influence vital rates. The 1969). potential role of dispersal in regulating the number of The metapopulation affects within-population dy­ individuals in plant taxa reinforces the need to under­ namics and hence population persistence through dis­ stand the interactions among all populations that com­ persal, which includes migration among inhabited prise a species. patches and colonization of unoccupied patches (curved 588 SPECIAL FEATURE Ecology, Vol. 75, No. 3

arrows in Fig. 2). Because dispersal will be a function likely to determine their geographic distributions. While of the number and spatial distribution of populations the perennial/annual dichotomy may be qualitatively producing and receiving propagules, populations may useful in assessing the importance of metapopulation be indirectly influenced by disturbance of other pop­ dynamics, it likely oversimplifies the factors that in­ ulations and habitats nearby. Dispersal can affect pop­ fluence population turnover rates. The importance of ulation survival through demographic as well as genetic within-population vs. metapopulation dynamics is bet­ means. Demographically, colonization and migration ter predicted by the components of population turn­ may either reduce survival as population size drops over, including dispersal rates (Fahrig and Paloheimo due to emigration (Lomnicki 1980) or help buffer pop­ 1988) and the role of environmental variation and ca­ ulations nearing extinction by adding individuals and tastrophes in causing extinction (Menges 1990). The by recolonizing empty patches (Menges 1990). For ex­ contributions of each of these factors are likely to vary ample, Kadmon and Shmida (1990) showed that 90% among species and hence will need individual consid­ of the individuals of the annual grass Stipa capensis in eration in evaluating the status of rare plants. one population arose from immigrant seed. Similarly, colonization and migration can either enhance or di­ EMPIRICAL APPROACHES TO STUDYING minish levels of genetic diversity in populations (Slat­ RARE SPECIES kin 1977, Wade and McCauley 1988, Levin 1989). It is clear that many factors, operating at a range of Much of our understanding of dispersal is based on spatial scales, may determine the abundance or rarity theory, however, and it has not been shown whether of plant species (Figs. 1 and 2). The biological infor­ either demographic or genetic components of dispersal mation most critical for conserving rare species has have a significant impact on plant population survival. been the subject of discussion for the last 20 yr and no Metapopulation dynamic processes have implica­ consensus has been reached (Duffey and Watts 1971, tions not only for survival oflocal populations but also Franklin 1980, Frankel and Soule 1981, Schonewald­ for survival of the species. For a species to spread or Cox et al. 1983, Soule 1987, Falk and Holsinger 1991). persist, plants must colonize unoccupied patches at Most scientists advocate an approach that is either least as frequently as populations become extinct. As ecological or genetic in emphasis. Proponents of a pop­ a result, there will be a threshold density of patches ulation genetic approach have stressed that under­ below which populations cannot persist due to inad­ standing the organization of genetic diversity is key to equate dispersal (Kermack and McKendrick 1927, the long-term survival of species, since genetic varia­ Levins 1970, Lande 1987). Even slight changes in the tion is a requisite for evolutionary adaptation (Berry number, density, or quality of patches can have an 1971, Lande and Barrowclough 1987, Vrijenhoek 1987, enormous effect on rates of colonization and extinc­ Hamrick et al. 1991 ), and may also have short-term tion, and may be sufficient to tip the balance in favor fitness consequences (Huenneke 1991 ). Others assert of regional extinction (Carter and Prince 1981). There­ that autecological research, i.e., characterizing the bi­ fore, metapopulation dynamics may be particularly otic interactions and habitat requirements of a species, important for species where available habitats as well is critical to sound conservation science (Burgman et as extant populations are few (Menges 1986, Primack al. 1988, Simberloff 1988, Brussard 1991). In this sec­ and Miao 1992) and may explain why the geographic tion we determine the extent to which genetic and eco­ distribution of some plants is more restricted than logical approaches are used in studies of rare plants physiological limits allow (Carter and Prince 1981, through a survey of the scientific literature and then 1988). discuss their effectiveness in conservation programs. We examined studies of rare or endemic plants pub­ Overall dynamics lished in nine scientific journals (American Journal of The abundance of plant species will result from Botany, Biological Conservation, Conservation Biolo­ changes in both the number and size of populations gy, Genetics, Ecological Applications, Ecology, Evolu­ (Brown 1984). Identifying the relative importance of tion, Natural Areas Journal, and Oecologia) from 1987 within-population and metapopulation dynamics, to 1992, plus studies cited within these papers and however, is difficult because demographic processes at within a Life Sciences Database at the University of each level are interdependent. Assuming populations Washington. All studies with the exclusive purpose of are discontinuous, the most important parameter may clarifying taxonomic boundaries of rare plants were be population turnover rate, or the rate of colonization excluded from the analysis. For each remaining paper relative to extinction. Carter and Prince (1981) argued we noted the rationale for the project (motivated by that population turnover would be lower in long-lived conservation or not), the research methods used (ge­ perennials than in annuals, and therefore habitat qual­ netic and/or ecological; demographic or not), and ity and within-population dynamics would be more whether implications for conservation were considered April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 589

in the Discussion section. In total we reviewed 78 pa­ Apfelbaum 1989, Menges 1990) discussed factors that pers, representing 66 angiosperm species. Seven papers influence the metapopulation, such as environmental contained information on two different species. Of the variation and disturbance. 30 species for which data were available, 43% were Although genetic and autecological approaches have found in five populations or less. played a major role in research on rare plants, we ques­ All papers included in the literature survey are cited tion the priority given to such information in many in the Appendix, with selected examples annotated to conservation research programs. The factors examined represent a range of research approaches. Of the 78 are often chosen arbitrarily, with little attention given studies examined, 27 (34.6%) took a genetic approach to the biology of the species. Concentrating on such and 47 (60.3%) were predominantly ecological. Four attributes of natural populations initially in a research studies incorporated both genetics and ecology. More­ program would be ineffective and inappropriate unless over, the research approach used depended on whether their relative impact on population vital rates and long­ the study was motivated by conservation (2 x 2 con­ term persistence has been demonstrated. Our survey tingency test, G = 7.6, P < .05, n = 63; studies with suggests that this information is rarely available. Twen­ both ecology and genetics were excluded). Conserva­ ty-two (48%) of the ecological studies examined in­ tion was the primary motivation in only 52% of 67 cluded some demographic measurements relevant to studies scored. Of these studies, 74% were ecological population vital rates (e.g., Meagher et al. 1978, Hutch­ and 23% emphasized genetics. While there are a sub­ ings I 987, Hegazy 1990); however, only three studies stantial number of investigations with a genetic em­ used demographic models to predict the viability of phasis, ecological research predominated when con­ populations (Fiedler 1987, Mehrhoff 1989, Menges servation was a focus of the study. A genetic approach 1990). With the exception of the investigation of in­ was used more frequently in investigations motivated breeding depression (Karron 1989), none of the genetic by issues other than conservation, such as the conse­ studies related their findings to demographic attributes quences of small population size and number, the evo­ of populations. lutionary history of endemism, or the basic biology of Under some circumstances, autecological and ge­ rare plants. netic approaches may be useful during the initial stages In most of the genetic investigations, evolutionary of research and management. Ecological data will be potential was inferred from geographic surveys of bio­ required when, for example, a single environmental chemical (isozymes) and molecular (DNA) polymor­ factor is the clear cause of population decline. Simi­ phisms (e.g., Moran et al. 1988, Rieseberg and Doyle larly, estimates of genetic diversity may be important 1989). These marker genes provide estimates of allele when specific genes have been identified as the major diversity and levels of heterozygosity within popula­ determinant of decline (e.g., lack of incompatibility tions as well as measures of the distribution of existing alleles; Thien et al. 1983, DeMauro 1993) or when variation among populations (Hamrick et al. 1991, establishing ex situ collections or reintroducing indi­ Schaal et al. 1991); however, their relationship to genes viduals to the wild, particularly when variation is val­ more directly related to fitness is often obscure. For ued for its horticultural or agricultural uses (Schaal et this reason, the magnitude of genetic variation for al. 1991). In general, factors such as the magnitude of quantitative characters may be more relevant and has genetic diversity or levels of herbivory on a species been measured by documenting morphological varia­ represent two of many possible causes of rarity in plants. tion or by using more sophisticated quantitative ge­ While such genetic and ecological information may be netic approaches (R. Lande, unpublished manuscript). considered in future recovery programs, they are of Despite its importance, only six studies in our survey limited use in an initial assessment of species status described variation in quantitative characters in rare because they cannot predict population vital rates nor species (e.g., Meagher et al. 1978), and one considered the future viability of populations. the importance of inbreeding depression (Karron 1989). The ecological studies in our survey focused on sev­ STEPS TOWARD RECOVERY eral attributes of target species including: plant asso­ We suggest that the development of recovery efforts ciates (Buchele et al. 1992b), competitive interactions for an endangered plant species requires a "top-down" (e.g., Batty et al. 1984, Menges et al. 1986), habitat approach, with answers to three fundamental ques­ requirements (Vivian 1967), habitat descriptions tions, each representing a different level of biological (Buchele et al. 1989), and reproduction and pollination inquiry. First, what is the biological status of the spe­ ecology (Mehrhoff 1983, Kevan et al. 1991, Buchele et cies? The conservation biologist must assemble the al. 1992a). In most cases, ecological factors operating necessary demographic information to determine if the within populations were the main focus; however, three numbers of individuals and populations of a species ecological studies (Meagher et al. 1978, Bowles and are increasing, decreasing, or stable. Second, what are 590 SPECIAL FEATURE Ecology, Vol. 75, No. 3

sexual reproduction

regression lseedsl--lseedlingsl .. ljuvenilesl--lsubadultsl ~ladultsl growth growth growth growth t:) t:) t:) t:)

rapid growth FIG. 3. Life cycle graph for a hypothetical plant population with five life history stages: seeds, seedlings, juveniles, subadults, and adults. The arrows indicate the probability a,1 that an individual in stage class i at time t contributes or moves to stage class j by time t + I. the life history stages that have the greatest effect on The only approach to evaluating biological status population growth and species persistence? An answer that provides both an assessment of population growth to this question focuses research efforts on those aspects trajectories and identification of the life history stages of the species biology that constitute the greatest threat that most affect population growth involves matrix to survival. Third, what are the biological causes of projection models (Leslie 1945). Because demographic variation in those life history stages that have a major parameters in plants are determined more by the life demographic impact? Only with this information is it history stage or size of an individual than by its age possible to initiate effective recovery efforts. Our dis­ (Harper 1977), the Lefkovitch stage-based model (Lef­ cussion here focuses on how to best evaluate the health kovitch 1965) is most appropriate for studying plant of a rare plant species in an ideal sense. Logistical, population dynamics. Here we provide a brief over­ political, and economic considerations clearly will place view of this approach. Caswell (1989) provides a com­ constraints on development of a research strategy. plete summary of the theory and uses of the matrix population model, and Menges (1986) discusses its ap­ plication to the conservation and monitoring of rare Evaluating the status of rare and plants. endangered species The matrix population model begins with the clas­ For rare and endangered plants we suggest that the sification of individuals in a population into categories most biologically relevant question is: given current that reflect biologically relevant life history stages. The conditions, is population size increasing, decreasing, individuals are permanently marked, and at each year's or stable? To answer this question requires a demo­ annual census they are classified by stage, and their graphic analysis, i.e., the study of population size and reproductive output is recorded. For each census in­ the growth, survival, and reproduction of individuals terval one obtains a life cycle graph (Caswell 1989) within populations. The simplest approach is a census summarizing all possible transitions within and be­ of the number of individuals through time. Although tween stages. Fig. 3 illustrates a life cycle graph for a this may suffice in many situations, it will not provide hypothetical plant population with five life history an accurate projection oflong-term population trends. stages: seeds, seedlings, juveniles, subadults, and adults. For example, a long-lived species with poor recruit­ With the exception of the arrow indicating the number ment may not show a population decline until the old­ of seeds and juveniles produced by adults, all arrows est individuals begin to die. This approach is also likely in the diagram represent the probability that individ­ to overlook cryptic life history stages such as a dormant uals at a given stage will grow (increase in size), survive seed bank that could contribute to population growth (remain in stage of previous year), or regress (decrease rate. Demographic projections based on population av­ in size) over the time period t to t + I (Fig. 3). Nu­ erages for birth and death rates can estimate population merical values for all possible transitions are assembled trajectories, but like the simple census approach, they in a projection matrix A, where each entry au represents cannot identify the causes of population decline. Only the probability that an individual in stage class i at by identifying the life history stages that have the great­ time t contributes or moves to stage class j by time t est impact on population growth can the conservation + I. To estimate population size at timet + I, a vector biologist begin to design efficient recovery efforts. n, representing the number of individuals in each stage April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 591

class at time t is multiplied by the matrix A, growth. Therefore, incorporating variation in demo­ graphic parameters into projection matrices may be n(t + I) = An(t). critical to developing realistic models of population and species viability. The matrix population model provides a quantita­ tive assessment ofbiological status in terms of the rate Identifving critical l(fe history stages and direction of population growth. This can be based Once the status of an endangered species has been on the transient dynamics of a population that has not established, it is crucial to identify the stages in the life reached its stable stage distribution or on the long-term cycle that contribute most to population or metapopu­ dynamics of a population that has reached its stable lation dynamics. This will allow the conservation bi­ stage distribution, in which case the population grows ologist to investigate biological processes that affect or declines at a constant rate A, equal to the dominant those stages and to design recovery measures. Genetic eigenvalue of the matrix A (Caswell 1989). or autecological approaches cannot provide this kind The projection matrix approach has also been ex­ of information. In contrast, a matrix population model tended to assess consequences for growth at the level can be used in a number of ways to identify the stages of the metapopulation (Horvitz and Schemske 1986, that have the greatest effect on population growth (Cas­ Caswell 1989). In a demographic model of the meta­ well 1989). Simulations and sensitivity and elasticity population, transition matrices for each population or analyses can be used to answer the question: How does patch are treated as submatrices within the metapopu­ a change in each demographic parameter affect pop­ lation transitional matrix, and the entries within the ulation growth rate? Simulations are conducted by cal­ matrix incorporate rates of migration as well as sur­ culating the population growth rate that would result vival and reproduction. Perhaps the most compel­ from prescribed changes in a demographic parameter. ling use of demographic models to assess the biological Fiedler (1987) conducted a simulation of projection status of rare and endangered plants occupying more matrices to show that increasing the seed number per than one population is Menges' (1990) research on the capsule to the maximum observed had relatively little population dynamics of Furbish's lousewort (Pedicu­ effect on the population growth rate of three rare Cal­ laris furbishiae). Through the use of stage-based pro­ ochortus spp., but had a large, positive effect on the jection matrices and metapopulation modeling, Menges population growth rate of a common congener. Sen­ (1990) demonstrated that the persistence of Furbish's sitivity is a measure of how population growth rate lousewort could not be assured by protecting individ­ responds to small changes in a demographic parameter ual populations. Instead, effective management of this and is equal to the slope of the relationship between A species requires the protection of a habitat corridor, and a particular demographic parameter. Elasticity is large enough to maintain a sufficient number of patches a measure of proportional sensitivity and is calculated for recolonization. as the product of the sensitivity for a particular de­ The validity of the assumptions made in a matrix mographic parameter and the actual value of that pa­ population model will depend on how the model is rameter in the projection matrix divided by the pop­ applied (Caswell 1989). Where the goal is to project ulation growth rate. Kalisz and McPeek (1992) long-term population trends, as will often be the case examined the population dynamics of the winter an­ for endangered species, the assumption of a constant nual Collinsia verna using a projection matrix ap­ projection matrix is clearly unrealistic. Deterministic proach and by sensitivity analysis determined that a changes in demographic parameters, as might be caused seed bank was critical to the demography of this spe­ by succession (Horvitz and Schemske 1986), coupled cies. In this example, a demographic analysis was in­ with demographic and environmental stochasticity strumental in identifying a stage that is inconspicuous (Menges 1992), will cause the elements of the projec­ and whose importance would otherwise have been un­ tion matrix to vary in time and space (Bierzychudek derestimated. 1982, Fiedler 198 7). The effect of environmental vari­ It is worth clarifying that sensitivity/elasticity anal­ ation on population persistence has been the subject yses indicate the change in population growth that re­ of several theoretical models (Cohen 1979, Tuljapur­ sults from a proportional change in each demographic kar 1982, Lande and Orzack 1988), but has not been transition probability. However, as stated previously, well studied in natural plant populations (Bierzychu­ transition probabilities are likely to vary in natural dek 1982, Aberg 1992). In a computer simulation, populations, and the magnitude of variation will differ however, Menges ( 1992) found that imposing envi­ among life history transitions. As a result, the stage in ronmental stochasticity on projection matrices from the life cycle most limiting to population growth may natural populations caused an increased risk of ex­ be the one with greatest natural variation and not nec­ tinction in populations that otherwise show positive essarily the one identified as showing the greatest elas- 592 SPECIAL FEATURE Ecology, Vol. 75, No. 3

ticity. This incongruence highlights again the need for us with the opportunity to examine biological attri­ realistic demographic models in assessing the status of butes and recovery measures proposed for the same an endangered species. group of species. Each plan contains four major sections: Introduc­ tion, Recovery, Implementation Schedule, and Ap­ Biological causes of variation in pendix (USFWS 1990a). The Introduction includes a demographically sensitive life history stages description of the species, its distribution, habitat/eco­ Once it is known what stages in the life history have system information, life history/ecology, reasons for the greatest impact on population growth, experiments listing, conservation measures, and strategy for recov­ and observations are needed to estimate the relative ery. The Recovery section includes the objective and importance of the genetic or ecological factors that af­ criteria for recovery, an outline for recovery actions, fect these stages. In the absence of obvious external and the literature cited. The Implementation Schedule threats, the most efficient approach is to simultaneous­ gives task priorities and descriptions, identifies the re­ ly investigate the contribution of a number of factors sponsible parties, and provides cost estimates. The Ap­ to variation in a particular demographic parameter. pendix includes lists of reviewers and copies of some For example, Sork (1987) conducted a series of exper­ of their comments. iments to estimate the relative importance of seed and Here we provide an overview of the biological char­ seedling predation and light levels on seedling estab­ acteristics of the 98 species we surveyed, discuss the lishment of the tropical tree Gustavia superba. Bazzaz research recommendations for those species, and eval­ et al. (1982) examined the influence of both genotype uate the recovery targets that would allow a species to and nutrient levels on survivorship in experimental be delisted. For an in-depth review of recovery plans populations of Phlox, and Schemske and Horvitz (1988) focused on the needs of the field manager, see Cook estimated the contribution of pollinators, antguards, and Dixon (1987). and herbivores to variation in fruit production among Biological characteristics.-The recovery plans we plants of the neotropical herb Calathea ovandensis. By surveyed lacked sufficient biological information to as­ identifying the genetic or ecological factors that pose sess the dynamics ofpopulations or ofmetapopulations the greatest threat to a species, such studies can guide for any of the species. Indeed, detailed demographic effective recovery efforts. information was available for only 33% of the species; in contrast, autecological information was reported for 94% of the species. Genetic information was available REVIEW AND EVALUATION OF RECOVERY PLANS for 8% of the species. The following was provided for We have suggested that the most effective course of most of the listed species, and in the absence of more action towards the recovery of an endangered plant extensive demographic information, probably pro­ species requires a demographic assessment of biolog­ vides the best indication of biological status: (1) the ical status, the identification of life history stages that number of populations, (2) the total number of indi­ have the greatest impact on population growth, and viduals, (3) geographic range, (4) ecological require­ the determination of the biological processes affecting ments, and (5) the present causes of endangerment. these stages. Are present recovery measures consistent Most endangered species are found in only one or a with these approaches? What criteria are now used to few populations (Fig. 4). Of the 91 species for which identify research priorities and recovery targets for en­ these data were available, those with a single extant dangered plants? population are most common (17.6%), and over half To answer these questions we reviewed recovery plans of the species are found in five or fewer populations written for the U.S. Fish and Wildlife Service that were (Fig. 4). These results are consistent with the general available in May of 1992 through the Fish and Wildlife conclusions from other databases, which indicate that Reference Service. Our analysis included only those most rare species occur in few populations (Holsinger recovery plans that provided data and recommenda­ and Gottlieb 1991 ). The vast majority of species have tions for individual species (plans prepared for groups a very restricted geographic range and narrow habitat of species or communi ties were excluded), giving a total requirements. The number of states (or territories, e.g., of 98 species. The average date of publication for the Puerto Rico) per species averaged 1.68 ± 1.54 (mean recovery plans we surveyed was 1987 (range: 1980- ± 1 sn; range 1-12), with 66.3% (65 species) found in 1992). Although other databases are available that pro­ a single state, and 23.5% (23 species) found in just two vide biological information on many more species (e.g., states. Of the 85 species for which habitat data were Center for Plant Conservation 1991 ), we chose to focus available, we classified 85.9% (73 species) as having on species with recovery plans because they provided narrow ecological requirements. A striking example of April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 593

garding the demographic importance of one or more life history stages. en Cl.l 40 Demographic research was proposed for 84% of all "[) species, but for only 17% was the use of projection Cl.l a. matrices indicated. In most cases the proposed de­ Cf) 30 mographic research involved only the monitoring of -0 individuals and/or populations, and it was rarely made Q; 20 clear how such data would be used in developing re­ .0 E covery guidelines. There were, however, some species ::J 1 0 where the recommendations for demographic research z were linked to recovery objectives. For example, the research recommendations for Vahl's boxwood (Buxus 20 40 60 80 100 1 20 1 40 vahlii) included a matrix approach to determine the Number of Populations per Species number of populations and individuals necessary to ensure species stability (USFWS 1987a). Likewise, for FIG. 4. Frequency distribution of the number of extant autumn buttercup (Ranunculus acriformis) a demo­ populations for 91 plant species currently listed as threatened or endangered by the U.S. Fish and Wildlife Service. The graphic matrix approach was proposed for evaluating number of species per class is given for classes with 1-5, 6- the status of populations and to target vulnerable life 10, 11-15, ... , 121-125 populations per species. history stages (USFWS 1991 b). Demographic ap­ proaches were also proposed to identify minimum vi­ able population sizes in clay-loving wild buckwheat a species with a restricted geographic range and narrow (Eriogonum pelinophilum) (USFWS 1988b), Canby's habitat requirements is the white-haired goldenrod dropwort (Oxypolis canbyii) (USFWS 199Gb), and the (Solidago albopilosa), which is found in only three ad­ Uinta Basin hookless cactus (Sclerocactus glaucus) joining counties in Kentucky where it occupies partial (USFWS 1990c), and to establish population growth shade behind the dripline of sandstone rockshelters trajectories for the lakeside daisy (Hymenoxys acaulis) (USFWS 1991a). (USFWS 1990d) and for Texas snowbells (Styrax lex­ We identified the primary cause of endangerment for ana) (USFWS 1987b). each species (Fig. 5). The distinction between the his­ Research in population genetics or ecological genet­ torical causes of species decline and the current threats ics was proposed for 26% of the species. In most cases to persistence are not discernible in recovery plans, so it was not clear how this research would aid in recovery. we treated all factors that adversely influence species For example, the recovery plan for Peter's mountain persistence as causes of endangerment. In addition, mallow (Iliamna co rei) called for the collection of data most species experience more than one threat, so our classification does not represent all of the threats to exotics agriculture endangered species. Development constituted the most water (6.1%) (5.1%) control frequent threat (20.4%), followed equally by grazing (8.2%) (10.2%), and collecting (10.2%). Not surprisingly, hu­ natural man activities were the primary cause of endangerment (1.0%) military for all but one species. (1.0%) trampling logging In summary, the rare and endangered plants in our (8.2%) sample of federally listed species with recovery plans (7.1%) have a small number of populations, a restricted geo­ fire control graphic range, narrow habitat requirements, and face (4.1%) a diversity of threats to their persistence. Research recommendations.-For each species we recorded the kinds of research proposed in the recovery plan for that species. The primary research focus was ecology, recommended in 96% of the recovery plans. oil, gas, roads In most cases the proposed ecological research focused mining (4.1 %) on factors limiting to a species distribution (e.g., soils, (8.2%) nutrients, moisture, etc.), pollination biology, and oth­ FIG. 5. Primary causes of endangerment for 98 plant spe­ er kinds of autecological information. Rarely was the cies currently listed as threatened or endangered by the U.S. ecological research motivated by prior information re- Fish and Wildlife Service. 594 SPECIAL FEATURE Ecology, VoL 75, No. 3

on genetic variation and the subsequent development the recovery plan includes a statement of the recovery of a population genetics model to determine the num­ criteria and objective (USFWS 1990a). The recovery ber of populations and effective population sizes re­ criteria are given in quantitative terms, i.e., the number quired for long-term survival (USFWS 1990e). This of individuals or populations, and the recovery objec­ emphasis on the genetics of rarity is a clear case of tive refers to whether and how the species would be overkill, as only four individuals of the mallow are reclassified if the recovery criteria are met. Guidelines known to exist in the wild. Electrophoretic work was for the recovery criteria and objective section require proposed for Michaux's sumac (Rhus michauxii) the author of the recovery plan to estimate the number (USFWS 1992b) with the justification only that "it of geographically distinct, self-sustaining populations might be useful," and that the relative success of in­ that are necessary for a species to be considered for dividual genotypes may be measured using these data. reclassification. This clearly requires information re­ One common theme in the justification for genetic garding the demography of individual populations (are studies was the need to determine the distribution of they self-sustaining?) and theoretical and/or empirical genetic variation within and between populations. The justification of the number of target populations, yet recovery plan for spreading avens (Geum radiatum) we found little evidence that such data had been con­ (USFWS 1992c) proposed to collect such information, sidered in making the recommendations. but there was no indication as to how these data would We chose to focus on the removal of a species from be used in recovery efforts. The recovery plan for Kral's the list of federally endangered species as the recovery water plantain (Sagittaria secundifolia) suggests that objective in our survey. The mean number of target "the amount of genetic variability within populations, populations per species that would meet the objective and the species as a whole, is also important in as­ of delisting was 11.6 ± 12.2 (mean ± I so, range 1- sessing minimum viable population parameters" 80, n = 74 species), and the mean ratio of target pop­ (USFWS 1991c). Similarly, for prairie bush clover ulations to current populations was 1.99 ± 1.89 (mean (Lespedeza leptostachya) it was suggested that genetic ± 1 so, range 0.08-10, n = 70). Thus, the recovery studies be conducted "to determine minimum popu­ objective proposed for delisting a species is met, on lation parameters that must be reached to sustain in­ average, when the number of self-sustaining popula­ dividual populations and the species as a whole" tions is twice the number of current populations. The (USFWS 1988c). If the proposed genetic study of Fas­ correlation between the number of target populations sett's locoweed (Oxytropis campestris) found that cer­ required for deli sting and the number of current pop­ tain populations contained little genetic variation, it ulations was positive and highly significant (r, = 0.73, was suggested that "the long-term sustainability" of P < .0001, n = 70). This indicates that recovery criteria these populations could be affected (USFWS 1991 d). were based, in large part, on the current number of As we have suggested previously, demographic criteria populations and not on the biological status of the are probably far better indicators of the biological sta­ species. tus of rare species than is information on the magnitude It is worth noting that the guidelines for writing a and distribution of genetic variation, whose connection recovery plan do not require the author to justify the to population viability has been theoretically (Lynch recovery criteria. The following quote from the guide­ and Gabriel 1990, Lynch and Lande 1993), but not lines illustrates the approach: "Quantifying recovery empirically, demonstrated. criteria calls for creative thought, and developing the In summary, the areas of research that received the criteria may require educated guesswork. This may be greatest emphasis were ecology, motivated primarily difficult for scientists accustomed to basing their state­ by the search for "limiting factors," and demography, ments on hard data rather than conjecture" (USFWS mostly involving the monitoring of individuals and/ 1990a:I-11). It is clear from our reading of the recovery or populations. The demographic research proposed, plans that the recovery criteria proposed for a species with some notable exceptions, was not designed to pro­ are, in fact, little more than guesswork. To make a vide information on the biological status of species, decision on recovery criteria requires information on nor to identify life history stages critical to population the population dynamics of the species, but research dynamics. Genetic research was proposed for some aimed at collecting these data is rarely proposed. We species, but in virtually all cases there was little indi­ are left with the disheartening conclusion that although cation as to how these data would be used in recovery the recovery criteria may be the most important com­ efforts. We conclude that the research recommenda­ ponent of a recovery plan, they have minimal scientific tions for federally listed plants are, in general, not suf­ credibility. For the recovery criteria to have any value, ficient to identify the biological information required demographic information regarding the biological sta­ to develop sound recovery guidelines. tus of the species is required. This includes information Recovery targets. -For most federally listed species, on the population dynamics of individual populations April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 595

and on the role of extinction and colonization in meta­ stantial progress can be made if moderate funds are population dynamics. made available. At present funding levels, however, the outlook is not favorable. In 1992 the Congress appropriated $41.5 million for the endangered species CONSTRAINTS ON RECOVERY APPROACHES program of the U.S. Fish and Wildlife Service, which In addition to understanding the biology of endan­ was less than the Agriculture Department's Beef Pro­ gered plants, conservation biologists must be fully in­ motion and Research Board spent on the advertising formed of the political and economic factors that can campaign "Real Food for Real People" (Eaton 1992). limit the feasibility and effectiveness of recovery ef­ This amount supports only the drafting of recovery forts. Clark (1989:3) emphasized that a major weakness plans for endangered species and does not include the of recovery programs for endangered species is a failure additional financial burden on federal land manage­ to recognize that "numerous non-biological factors and ment agencies (e.g., U.S. Forest Service, Bureau of Land forces have direct, immediate and paramount signifi­ Management, National Park Service) whose budgets cance to endangered species recovery." must support coordination and actual implementation A major political hurdle facing managers of rare plant of the recovery plans once drafted by the U.S. Fish and recovery is the coordination of conservation efforts Wildlife Service. Obtaining the biological data required throughout a species' range. For example, the Endan­ to design and implement effective recovery for even a gered Species Act of 1973 (16 U.S.C. §§ 1531-1544: fraction of the federally listed plant species appears USFWS 1988a) protects federally listed fish and wild­ unlikely without a substantial increase in financial sup­ life on all lands, public or private, while endangered port. species of plants are protected only on areas under federal jurisdiction. This seriously limits the authority of many plant recovery efforts; our survey of recovery RECOMMENDATIONS plans showed that private lands were very important The combination of escalating threats to species sur­ to the conservation of 50% of federally listed species. vival and severe fiscal and political constraints have In addition, populations of a single endangered species, created a need for conservation biologists and land even if found exclusively on federal lands, could fall managers to develop realistic and efficient guidelines under the management policies of a number of federal for the management of rare and endangered species. agencies (e.g., U.S. Forest Service, Bureau of Land Despite this imperative, our review ofUSFWS recov­ Management, or National Park Service). In these cases, ery plans shows that a conceptual framework for col­ coordination among agencies becomes a real challenge. lecting and interpreting information necessary for ef­ Both assessment of status and design of new popula­ fective management of federally listed plant species is tions could be seriously impeded because of the num­ lacking. Progress is currently impeded by a lack of ber ofland management agencies potentially involved. biological information and inadequate communication The Clinton administration's recent formation of the among the interested parties. On the one hand, recov­ National Biological Survey within the Department of ery plan recommendations have not incorporated the the Interior may improve communication among fed­ conceptual guidelines and quantitative tools developed eral biologists concerned with endangered species man­ largely by ecologists and population biologists. On the agement. other hand, as is exemplified by the debate over the Even a recovery plan based on excellent biological role of genetics and demography in conservation (Lande information will succeed only if the steps recommend­ 1988, Holsinger and Gottlieb 1991, Menges 1992), ac­ ed in the plan are taken. Fish and Wildlife Service ademics have not provided clear guidelines regarding reports from 1983 and 1984 indicated that little atten­ the most valuable and cost effective approaches for tion was being given to plant recovery efforts (Cook managers involved with endangered species recovery. and Dixon 1987, Dixon and Cook 1990). The 1988 The recommendations we provide here for improving amendment to the Endangered Species Act requires a plant conservation efforts include a realistic approach report on all listed species every 2 yr (J. Knight, per­ to field studies on rare plants, the development of new sonal communication). A systematic review of the suc­ theoretical and empirical tools to guide the resource cess of recovery plans is necessary to both encourage manager in formulating recovery action, and the need their implementation and provide feedback for plan­ for increasing the level of communication among all ners and conservation scientists. concerned with recovery of endangered plants. Based on our review of the recovery plans, the mean estimated cost of recovery for each federally listed spe­ A framework for conservation approaches cies is $159 000 (n = 94 species). Although this is most The research question implicit in most recovery plans certainly an underestimate, it does suggest that sub- is "Why is this taxon rare?" (Cook and Dixon 1987). 596 SPECIAL FEATURE Ecology, Vol. 75, No. 3

As Cook and Dixon emphasize, this is the wrong way from qualitative estimates of abundance for those spe­ to motivate a research program in conservation biol­ cies at low risk to full demographic studies of marked ogy. A more appropriate question is "Is this taxon individuals for those species at highest risk (D. Salzer, declining, and if so, why?" We advocate a demographic personal communication). E. S. Menges and D. R. Gor­ framework for rare plant recovery efforts, which con­ don (unpublished manuscript) propose a three-level, sists of three steps: first determine the biological status hierarchical approach to population monitoring de­ of a species, then identify the life history stages critical signed to accommodate species that differ in priority to population growth, and finally determine the un­ and management objectives. derlying biological causes of variation in critical life For those species with more than one extant popu­ history stages. Demographic approaches provide a lation, assessment of the biological status of the meta­ quantitative way to determine if populations are "self­ population is necessary. An emphasis on metapopula­ sustaining," and can therefore be used to explicitly tion dynamics will be particularly important for evaluate the recovery criteria for delisting rare and assessing the status of species with high population endangered species as is mandated by the U.S. Fish turnover, or when colonization is dependent on en­ and Wildlife Service. vironmental disturbance. For example, Florida golden In contrast to other ecological and genetic approach­ aster (Chrysopsisfloridana) (USFWS 1988d) and hairy es, a demographic approach utilizing projection ma­ rattleweed (Baptisia arachnifolia) (USFWS 1984a) are trices can make predictions regarding the dynamics of dependent on fire for establishment, running buffalo the population and of the metapopulation. Our con­ clover (Trifolium stoloniferum) originally exploited clusion is at odds with the suggestion that "knowledge disturbance by bison (USFWS 1989), and Furbish's of the levels and distribution of genetic variation thus lousewort (Pedicularis furbishiae) colonizes disturbed become a prerequisite for the establishment ofeffective riparian habitats (Menges 1990). Ideally, assessing bi­ and efficient conservation practices" (Hamrick et al. ological status for these species requires a matrix model 1991 :75). Rather, we maintain that only after the de­ for each population. However, when resources are lim­ mographic status is known can the underlying ecolog­ ited, simply monitoring the number and size of pop­ ical and genetic causes of decline be identified and ulations within a broad area would provide informa­ considered efficiently. tion concerning changes in the metapopulation and the For many endangered plants, the best approach to relationships between metapopulation and within­ assessing biological status will be to census marked population dynamics. These metapopulation dynam­ individuals representing all life history stages for the ics are more important for species in ephemeral hab­ purpose of generating the data needed to construct a itats than for species that occupy stable habitats, where matrix population model. Pavlik and Barbour (1988) individual populations may reach and maintain an and Hutchings (1991) also recommended complete equilibrium, e.g., relict trillium (Trillium reliquum) censuses for population monitoring. We recognize that (USFWS 1990/) and white-haired goldenrod (Soli­ it will often be necessary and appropriate to utilize dago albopilosa) (USFWS 1991 a). other methods of assessing biological status. Limited For most rare plant taxa, research to identify the resources can restrict the scope of a monitoring pro­ limiting life history stages and the factors affecting them gram, but biological attributes of the species should needs to begin before the status of a species has been also be considered. For example, there clearly will be completely characterized with a matrix model. In these some species whose plant densities are now so low that cases, the field biologist is forced to combine obser­ using projection matrices to investigate population vations, intuition, and experience to judge which life trends would be useless. Such is the case for Peter's history stages should be the focus of research efforts so mountain mallow (Iliamna corei) which has only four the data collected will contribute to species recovery surviving individuals (USFWS 1990e). For species with (Cook and Dixon 1987). As an initial estimate oflim­ very low numbers, a simple count of individuals at iting life history stages, the current stage structure of regular intervals may suffice. the population can be quantified using a life cycle graph Palmer (1987) reviewed rare plant monitoring, and (Fig. 3) as a template. Using this demographic frame­ emphasized the need to develop monitoring efforts that work, managers will be able to quickly identify "se­ are most consistent with project goals, and suggested nescent" populations that are in jeopardy because early demographic and experimental studies for threatened stages in the life cycle are poorly represented or miss­ species. Criteria for determining the intensity of mon­ ing. For example, no seedlings have been observed in itoring efforts should be based on the degree of endan­ Chapman's rhododendron (Rhododendron chapmanii) germent. For example, The Nature Conservancy in (USFWS 1983) or McKittrick pennyroyal (Hedeoma Oregon has adopted a hierarchical scheme for deter­ apiculatum) (USFWS 1985), and seedling survivorship mining the intensity of population monitoring, ranging is extremely low for the Antioch Dunes evening prim- April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 597

rose (Oenothera deltoides howellii) (USFWS 1984b). information to evaluate the contribution of variation The failure of these species to recruit new individuals at isozyme loci to the viability of populations, such an into their populations indicates that initial recovery endeavor is highly unlikely to aid conservation efforts. efforts should focus on early stages in the life history. Conservation biologists continue to evaluate recov­ However, as a cautionary note, experience in animal ery guidelines, and there is now discussion of moving conservation programs suggests that biological intui­ away from the present focus on the conservation of tion alone may not correctly identify the life history individual species and towards the conservation of eco­ stage most critical to population growth (Crouse et al. systems (Eaton 1992, Fiedler et al. 1993). The basic 1987). Full-scale demographic analysis is the best ap­ premise is that a healthy ecosystem will provide ample proach, because it may reveal non-intuitive patterns opportunity for the historical assemblage of species to in plant population dynamics (e.g., Kalisz and McPeek reach their natural densities without costly and un­ 1992). tested management. Proponents of an ecosystem ap­ For most species, demographic information will be proach argue that single-species conservation efforts far more useful in assessing status and in developing are based on an assumption of equilibrium conditions recovery efforts than will genetic information (see also (Fiedler eta!. 1993). However, this assumption is not Lande 1988, Menges 1992). There are, however, some a prerequisite for single-species conservation when circumstances where genetic research may be justified. metapopulation dynamics are considered. Manage­ For example, when establishing new populations it may ment of endangered species will often require a meta­ be desirable to identify the distribution of genetic vari­ population approach that incorporates migration, patch ation within and between populations to aid in iden­ dynamics, and population turnover (see above, Factors tifying the best source material. However, because most aJfecting species abundance: Metapopulation dynam­ endangered species have a limited number of popu­ ics). Because the populations of many rare and endan­ lations (Fig. 4), obtaining seeds from a large sample of gered plant species are imbedded in a degraded, frag­ individuals from the extant populations will likely cap­ mented landscape, it will often be difficult to acquire ture most of the existing genetic variation (Brown and and restore enough habitat to manage only at the eco­ Briggs 1991 ), and eliminate costly and time-consuming system level. Furthermore, the health of an ecosystem genetic studies (see Holsinger and Gottlieb 1991 ). Ge­ is determined by the health of its constituent species; netic information may be useful for establishing con­ an ecosystem approach will still require that the bio­ servation priorities when only a subset of the current logical status of endangered species be assessed. populations can be protected, as is the case for swamp A general demographic framework will dictate the pink (Helonias bullata) (USFWS 199le). In addition, steps necessary for species recovery. The great diversity genetic surveys may be helpful for determining con­ seen in the biological characteristics of federally listed servation priorities among different plant taxa. In some species, and in the primary causes of their endanger­ cases, taxonomic distinctiveness may be an important ment (Fig. 5), suggests that each species will require a criterion for setting priorities (Holsinger 1992), and somewhat different research plan. The appropriateness genetic analyses may play a role in settling questions of a full matrix population analysis, as well as various of taxonomic status. ecological and genetic studies, will be determined by An example of a potential overemphasis on mea­ the biology of individual species and the primary caus­ sures of genetic diversity in conservation programs is es of endangerment. the recent interest in the establishment of Gene Re­ source Management Units (GRMU). GRMU are de­ Theoretical and empirical research needs fined "as any designated forest area that meets mini­ Scientists in the academic community can contribute mum genetic management objectives" (Millar and to plant conservation efforts by developing new theo­ Libby 1991: 160), and in which genetic conservation is retical and empirical tools for use in designing and given the highest priority. This management approach implementing recovery plans. The breadth of expertise was originally conceived for conservation of wide­ demanded of recovery plan architects under the current spread economically important tree species managed system is unrealistic, and this has led to impractical by foresters (Krugman 1984); in such cases where pop­ and inefficient recommendations for research in plant ulations are effectively monocultures, a genetic focus conservation. In addition, research questions designed may be appropriate. However, discussion of extending to contribute to rare plant recovery must reflect the the GRMU concept to natural communities of her­ external constraints on conservation efforts. Without baceous or woody plants (Millar and Libby 1991) would clearer guidance from scientists whose research on rare not be an effective application of genetic approaches. species is motivated by conservation concerns, meeting Given the costs of surveying genetic diversity for each recovery goals will remain a nearly impossible task. species in the community and the lack of demographic Based on our assessment of rare plant recovery efforts 598 SPECIAL FEATURE Ecology, Vol. 75, No.3

and information published in the scientific literature, must involve an understanding of the underlying caus­ we see five main areas of research in need of attention: es of variation in life history stages deemed critical to (1) development of monitoring guidelines for assessing population growth. Because the biological character­ the demographic status of populations, (2) the role of istics and causes of endangerment of rare plants are dispersal and metapopulation dynamics in species per­ diverse, clarifying the roles of genetic and ecological sistence, (3) the relative contributions of genetic and factors in limiting critical stages remains in part an ecological factors to population and species dynamics, empirical question. Research is needed to address (4) the role of environmental and demographic sto­ questions such as: What are the relative roles of pop­ chasticity in species persistence, and (5) development ulation genetic and ecological characteristics in causing of practical guidelines for designing and creating new extinction? How does population size affect the relative populations. contributions of genetic and ecological attributes to Determining the biological status ofendangered plant population processes? Genetic models exploring pop­ populations is the first step in plant conservation ef­ ulation size trajectories or persistence have been de­ forts. Although we have argued that a matrix popu­ veloped (Lynch and Gabriel 1990, Halley and Manasse lation model is the best way to assess status, we also 1993, Lynch and Lande 1993), and several investiga­ recognize that due to limited resources it will often be tions of population viability have emphasized the role necessary to prioritize monitoring efforts. Detailed de­ of ecological factors (Shaffer 1981, 1987, Gilpin and mographic studies that include the construction of pro­ Soule 1986, Lande 1987, Menges 1990). Few existing jection matrices should be conducted on those species population dynamic models integrate the effects of both with highest priority, while population trends for spe­ genetic and ecological factors on vital rates or popu­ cies with lower priority should be determined by less lation persistence (Pease et a!. 1989, Boyce 1992). labor-intensive monitoring procedures. The major un­ Environmental and demographic stochasticity are of answered question is: What is the minimum amount greatest importance in small populations and can of information needed to provide an accurate projec­ therefore contribute to the risk of extinction of endan­ tion of population size? To establish priorities and gered plant species (Cohen 1979, Tuljapurkar 1982, identify the most effective monitoring procedures will Lande and Orzack 1988, Menges 1992). Identifying require long-term demographic data on a number of the contribution of these stochastic forces to popula­ species and the development of simulation models that tion dynamics requires extensive empirical data cou­ test the predictive value of different monitoring tech­ pled with simulation modeling. This is an area where niques. long-term empirical studies are needed to address ques­ As we have emphasized, consideration ofmetapopu­ tions such as: What is the magnitude of environmental lation dynamics may be important at two different steps and demographic stochasticity? Do the demographic in the recovery of endangered species: in assessing bi­ consequences of environmental stochasticity differ ological status and in establishing the number of pop­ among life history stages? What is the frequency and ulations required for species persistence. However, our spatiotemporal pattern of the environmental factors current understanding of the contribution ofmetapop­ that contribute to variation in demographic parame­ ulation dynamics to species persistence is limited. ters? Because accurate answers to these questions re­ Questions that have not been adequately addressed quire many years of data, it is impractical to expect include: What is the minimum number of populations that such studies can be conducted for more than a or density of available patches required for metapopu­ small subset of species. This calls for focused empirical lation stability? How do different life histories, dis­ efforts to characterize the demographic consequences persal rates, and spatial arrangement of populations of stochastic forces in plant species representing a wide affect metapopulation persistence? Under what con­ range of life histories and habitats (E. Guerrant, per­ ditions are dynamics within populations indicative of sonal communication) and for theoretical efforts to dynamics at the metapopulation level? The present identify ways of predicting long-term responses from failure to appreciate the role of metapopulation pro­ short-term data (K. Holsinger, personal communica­ cesses in plant conservation is perhaps best illustrated tion). by the criterion established in recovery plans that the Perhaps the most challenging task associated with populations comprising a species must be "self-sus­ conservation of rare plant species is the design and taining" to qualify for delisting. Such an emphasis ig­ management of new populations. In spite of state and nores those nonequilibrium species like Furbish's federal regulations mandating restoration of existing lousewort (Pedicularis furbishiae) where metapopula­ habitat following environmental destruction, success tion processes play a central role in the overall dynam­ of such projects has been disappointingly low (Brad­ ics of the species. shaw and Chadwick 1980, Woodruff 1989, Holsinger We have suggested that recovery efforts for rare plants and Gottlieb 1991 ). In addition, attempts at introduc- April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 599

ing rare species into new or historically inhabited areas implement recovery plans are unlikely to have the re­ have produced mixed results (Griffith et al. 1989). None sources and experience necessary to carry out such a of these approaches has included a consideration of the program. Practical guidance and instruction in de­ dynamics of the array of newly created populations mographic techniques need to be available to conser­ (i.e., the metapopulation). Guidance from the academ­ vation managers. Organizations such as the Center for ic community could help address important related Plant Conservation will play a critical role in providing questions, such as: What ecological or genetic factors this kind oflink between the academic community and are the best indicators of minimum viable population those who design and implement recovery efforts (D. size and metapopulation size? In species characterized Falk, personal communication). by high population turnover, how can habitat avail­ Communication among land managers at all levels ability be assessed and ensured? What spatial distri­ of government is another challenge to species recovery. bution of populations will maximize the likelihood that Interaction is crucial among the diverse federal and a species will be self-sustaining? local agencies charged with the responsibility of im­ plementing recovery guidelines, especially when they involve the same target species. Agencies and private CoNCLUSIONS organizations involved in plant conservation would Under the current system for managing endangered gain from sharing biological data on rare plants and species, steps toward conservation are not keeping pace details of the successes and failures of recovery mea­ with escalating losses. Between the 1973 enactment of sures. Recent workshops to discuss research approach­ the Endangered Species Act and I 990, only 16 species es among local and regional groups involved in en­ were delis ted. Over this same period, 26 species which dangered plant management are an encouraging start were either listed or under review for listing have gone (E. Guerrant, personal communication; R. Sutter, per­ extinct (M. Rowland, personal communication). Such sonal communication). unacceptable levels of extinction illustrate the need for Plant conservation cannot succeed unless political, more effective conservation efforts. Collection of ap­ economic, and biological factors are incorporated in propriate biological data and better transfer of infor­ management strategies. Complicated land jurisdic­ mation will foster progress toward this goal. tions, limited funding, and increasing rates of species Scientists' contribution to plant conservation will be extinction each present important challenges to the strengthened by better communication with conser­ conservation of endangered plants. Ultimately, how­ vation managers, an interchange that is necessary to ever, rarity is a biological phenomenon. Without in­ focus research on the questions most relevant to re­ corporation of critical biological information into re­ covery efforts. Increased communication will promote search plans, conservation efforts will continue to fall awareness of the recovery process among scientific re­ short of recovery goals. searchers and will facilitate active participation in con­ servation efforts, from the listing of species to devel­ AcKNOWLEDGMENTS opment and evaluation of recovery plans. Researchers We are grateful to Peter Kareiva for advice and encour­ agement, to Martha Groom, Jan Knight, Sarah Reichard, Dan who choose to make a significant contribution to spe­ Salzer, Rob Sutter, and Jane Wentworth for sharing their cies conservation need an understanding of policy reg­ insights on plant conservation, and to Bob Cook, Don Falk, ulating rare plant management, why that policy is for­ Leslie Gottlieb, Edward Guerrant, Kent Holsinger, PeterKa­ mulated, and political/fiscal constraints on its reiva, Jan Knight, and Russ Lande for critical comments on implementation; that is, a "policy orientation" (Clark the manuscript. et al. 1992). Not all research on rare species will or LITERATURE CITED should be focused exclusively on conservation issues, Aberg, P. 1992. A demographic study of two populations but where conservation is the primary motivation for of the seaweed Ascophyllum nodosum. 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APPENDIX Empirical studies on rare or endemic plants used in the ogy of the endangered species Solidago shortii. V. Plant scientific literature review (see Empirical approaches to study­ associates. Bulletin of the Torrey Botanical Club 119:208- ing rare species). Annotated citations indicate some examples 213.(e) of research motivated by conservation that used an ecological Cabin, R. J., J. Ramstetter, and R. E. EngeL 1991. Repro­ (e) or genetic (g) approach, and that considered demography ductive limitation of a locally rare Asclepias. Rhodora 93: of populations (d) or meta populations (m). 1-10. Campbell, J. J. N., M. Evans, M. E. Medley, and N. L. Taylor. Babbel, G. R., and R. K. Selander. 197 4. Genetic variability 1988. Buffalo clovers in Kentucky (Trifolium stoloniferum in edaphically restricted and widespread plant species. Evo­ and T. rejlexum): historical records, presettlement envi­ lution 28:619-630. ronment, rediscovery, endangered status, cultivation and Baskin, J. M., and C. C. Baskin. 1991. An eight year green­ chromosome number. Rhodora 90:399-418. house study of the cedar glade endemic Onosmodium molle Carulli, J. P., and D. E. Furbrothers. 1988. Allozyme vari­ subsp. molle. Natural Areas Journal11: 190-192. ation in three eastern US species of Aeachynomene (Fa­ Baskin, J. M., C. C. Baskin, P. D. Parr, and M. Cunningham. baceae), including the rare A. virginica. Systematic Botany 1991. Seed germination ecology of the rare hemiparasite, 13: 559-566. Tomanthera auriculata (Scrophulariaceae). Castanea 56:51- Clampitt, C. A. 198 7. Reproductive biology of Aster curtus 58. (e, d) (Asteraceae), a Pacific NW endemic. American Journal of Batty, P.M., B. D. Batty, and G. R. Miller. 1984. Population Botany 74:941-946. size and reproduction of Gentiana nivalis L. at Ben Lowes Clay, K., and R. Shaw. 1981. An experimental demonstra­ NNR. Transactions of the Botanical Society of Edinburgh tion of density-dependent reproduction in a natural pop­ 44:269-280. ulation of Diamorpha smallii, a rare annuaL Oecologia 51: Bayer, R. J. 1992. Allozyme variation, genecology and phy­ 1-6. togeography of Antennaria arcuata (Asteraceae), a rare spe­ cies from the Great Basin and Red Desert with small dis­ Cole, W. W., and S.C. H. Barrett. 1989. Genetic variation and patterns of sterility in the rare disjunct, aquatic Eich­ junct populations. American Journal of Botany 79:872- hornia paradoxa (Pontederiaceae). American Journal of 881. Botany (Supplement) 76:145. Betancourt, J. L., W. S. Schuster, J. B. Mitton, and R. S. Anderson. 1991. Fossil and genetic history of a pinyon Crank, Q. C. B. 1980. Extinction and survival in the en­ pine (Pinus edulis) isolate. Ecology 72:1685-1697. demic vascular flora of Ascension Island. Biological Con­ Bowles, M. L., and S. I. Apfelbaum. 1989. Effects of land servation 17:207-220. use and stochastic events on heart-leaved plantain (Plan­ Crawford, D. J., T. F. Stuessy, and M. Silva. 1988. Allozyme tago cordata Lam) in an Illinois stream system. Natural variation in Chenopodium sancta-clarae, an endemic spe­ Areas Journal9:90-107. (e, d, m) cies ofthe Juan Fernandez Islands, Chile. Biochemical Sys­ Buchele, D. E., J. M. Baskin, and C. C. Baskin. 1989. Ecol­ tematics and Ecology 16:279-284. (e) ogy of the endangered species Solidago shortii. I. Geogra­ Davies, P. A. 1960. Pollination and seed production in Shor­ phy, population and physical habitat. Bulletin of the Torrey tia galacifolia. Castanea 25:89-96. (e, d) Botanical Club 116:344-355. (e) DeMauro, M. 1993. Relationship ofbreeding system to rar­ Buchele, D. E., J. M. Baskin, and C. C. Baskin. 1991a. Ecol­ ity in the lakeside daisy (Hymenoxys acaulis var. glabra). ogy of the endangered species Solidago shortii. II. Ecological Conservation Biology 7:542-550. life cycle. Bulletin of the Torrey Botanical Club 118:281- Dring, M. J., and L. C. Frost. 1971. Studies of Ranunculus 287. ophioglossifolius in relation to its conservation at the Badge­ Buchele, D. E., J. M. Baskin, and C. C. Baskin. 1991 b. Ecol­ worth Nature Reserve, Gloucestershire, England. Biological ogy of the endangered species Solidago shortii. III. Seed Conservation 4:48-56. (e, d) germination ecology. Bulletin ofthe Torrey Botanical Club Erickson, R. 0. 1945. The Clematis fremontii var. riehlii 118:288-291. (e, d) population in the Ozarks. Annals ofthe Missouri Botanical Buchele, D. E., J. M. Baskin, and C. C. Baskin. 1992a. Ecol­ Garden 32:413-460. ogy of the endangered species Solidago shortii. IV. Polli­ Fiedler, P. L. 1987. Life history and population dynamics nation ecology. Bulletin of the Torrey Botanical Club 119: of rare and common mariposa lilies (Calachortus Pursh: 137-141. (e, d) Liliaceae). Journal of Ecology 75:977-995. (e, d) Buchele, D. E., J. M. Baskin, and C. C. Baskin. 1992b. Ecol- Fins, L., and W. J. Libby. 1982. Population variation in April 1994 ENDANGERED SPECIES/ECOLOGICAL THEORY 605

Sequoiadendron: seed and seedling studies, vegetative prop­ peri mental ecological genetics in plantago. III. Genetic vari­ agation and isozyme variation. Silvae Genetica 31:101- ation and demography in relation to survival of Plantago 148. cordata, a rare species. Biological Conservation 14:243- Fritz-Sheridan, J. 1988. Reproductive biology of Erythro­ 257. (e, g, d, m) nium grand(florum and candidum (Liliaceae). American Mehrhoff, L. A. 1983. Pollination in the genus Isotria. Journal of Botany 75:1-14. American Journal of Botany 70:1444-1453. (e, d) Gawler. S.C., D. C. Waller, and E. S. Menges. 1987. En­ ---. 1989. Reproductive vigor and environmental fac­ vironmental factors affecting establishment and growth of tors in populations of an endangered North American or­ Pedicularisfurbishiae, a rare endemic of the St. John River chid, Isotria medeoloides (Pursh) Rafinesque. Biological Valley, Maine. Bulletin of the Torrey Botanical Club 114: Conservation 47:281-296. (e, d) 280-292. (e, d) ---. 1989. The dynamics of declining populations of an Gottlieb, L. D. 1973. Genetic differentiation, sympatric spe­ endangered orchid, Isotria medeoloides. Ecology 70:783- ciation and the origin of a diploid species of Stephanomeria. 786. American Journal of Botany 60:545-553. Menges, E. S. 1990. Population viability analysis for an Graber, R. E. 1980. The life history and ecology of Potent ilia endangered plant. Conservation Biology 4:52-62. (e, d, m) robbinsiana. Rhodora 82:131-140. ---. 1991. Seed germination percentage increases with Hegazy, A. K. 1990. Population ecology and implications population size in a fragmented prairie species. Conser­ for conservation of Cleo me droserifolia, a threatened xero­ vation Biology 5:158-164. phyte. Journal of Arid Environments 19:269-282. (e, d) ---. 1992. Habitat preferences and response to distur­ Hegazy, A. K., and N. M. Essa. 1991. On the ecology, insect bance for Dicerandrafrutescens, a Lake Wales Ridge (Flor­ seed-predation, and conservation of a rare and endemic ida) endemic plant. Bulletin of the Torrey Botanical Club plant species: Ebenus armitagae (Leg). Conservation Bi­ 119:308-313. (e, m) ology 5:317-324. (e) Menges. E. S., and S. C. Gawler. 1986. Four year changes Hickey, R. J.. M. A. Vincent, and S. I. Guttman. 1991. in population size of the endemic plant Furbish's lousewort Genetic variation in running buffalo clover (Trifolium sto­ (P. furbishiae): implications for endangerment and man­ lonz(erum. Fabaceae). Conservation Biology 5:309-316. (g) agement. Natural Areas Journal 6:1-6. (e, d) Homoya, M. L., J. R. Aldrich, and E. M. Jacquart. 1989. Menges, E. S., D. M. Waller, and S.C. Gawler. 1986. Seed The rediscovery of the globally endangered clover, Trifoli­ set and seed predation in Pedicularis furbishiae, a rare en­ um stoloniferum, in Indiana. Rhodora 91:207-212. demic of the St. John River, Maine. American Journal of Hutchings. M. J. 1987. The population biology of the early Botany 73:1168-1177. (e, d) spider orchid. Ophrys sphegodes Mill. I. A demographic Moran, G. F., J. C. Bell, and K. C. Eldridge. 1988. The study from 1975 to 1984. Journal of Ecology 75:711-727. genetic structure and conservation of the five populations Karron. J.D. 1989. Breeding systems and levels of inbreed­ of Pinus radiata. Canadian Journal of Forest Research 18: ing depression in geographically restricted and widespread 506-514. species of Astragalus (Fabaceae). American Journal of Bot­ Moran, G. F., and S. D. Hopper. 1983. Genetic diversity any 76:331-340. (g, d) and the insular population structure of the rare granite rock Karron, J. D., V. B. Linhart, C. A. Chaulk, and C. A. Rob­ species Eucalyptus caesia Butz. Australian Journal of Bot­ ertson. 1988. Genetic structure of populations of geo­ any 31:161-172. (g) graphically restricted and widespread species of Astragalus Moran, G. F., 0. Muona, and J. C. Bell. 1989. Acacia man­ (Fabaceae). American Journal of Botany 75:1114-1119. gium: a tropical forest tree of the coastal lowlands with low Kevan. P. G., J.D. Ambrose, and J. R. Kemp. 1991. Pol­ genetic diversity. Evolution 43:231-235. lination in an understorey vine, Smilax rotundifolia, a Morgan, S. 1983. Lindera melissifolium: a rare southeastern threatened plant of the Carolinian forests in Canada. Ca­ shrub. Natural Areas Journal3:62-67. nadian Journal of Botany 69:2555-2559. (e, d) ---. 1983. Lesquerella filiformis: an endemic mustard. Ledig, F. T., and M. T. Conkle. 1983. Gene diversity and Natural Areas Journal 3:59-62. genetic structure in a narrow endemic, Torrey Pine (Pinus Newberry, G. 1991. Factors affecting the survival of the rare torreyana Parry ex Carr.). Evolution 37:79-86. plant, Sagittariafasciculata E.O. Beal (Alismataceae). Cas­ Lesica, P .. R. F. Leary, F. W. Allendorf, and D. E. Bilderback. tanea 56:59-64. 1988. Lack of genic diversity within and among popula­ Nickrent, D. L., and D. Wiens. 1989. Genetic diversity in tions of an endangered plant, Howellia aquatilis. Conser­ the rare California shrub Dedeckera eurekensis (Polygon­ vation Biology 2:275-283. (g) aceae). Systematic Botany 14:245-253. Levin, D. A., K. Ritter, and N. C. Ellstrand. 1979. Protein Poznanska, Z. 1989. Habitat modifications in the germi­ polymorphism in the narrow endemic Oenothera organen­ nation of seeds and survival of seedlings of the thistle Car­ sis.Evolution 33:534-542. tina onopodifolia Besser. Fragmenta Floristica Geobotanica Libby. W. J. 1990. Genetic conservation of Monterey and 34:27-42. (e, d) coast redwood. Fremontia 18: 15-21. (g) ---. 1991. Succession of xerothermal swards and the Macior, L. W. 1978. The pollination ecology and endemic dynamics of populations and problems of active ecological adaptations of Pedicularis furbishiae S. Wats. Bulletin of protection of Car/ina onopodifolia Besser. Ochrona Przyr­ the Torrey Botanical Club 105:268-277. (e) ody 48:55-84. ---. 1980. The population ecology of Furbish's louse­ Poznanska, Z., and L. Spiss. 1985. Preliminary observations wort (Pedicularis furbishiae S. Wats.). Rhodora 82:105- on the flowering and seed production of the thistle Car/ina 111. onopodifolia Besser. Acta Societatis Botanicorum Poloniae McClenaghan, L. R., Jr., and A. C. Beauchamp. 1986. Low 54:41-51. genic differentiation among isolated populations of the Cal­ Primack, R. B. 1980. Phenotypic variation of rare and wide­ ifornia fan palm ( Washingtoniafilifera). Evolution 40:315- spread species of Plantago. Rhodora 82:87-96. 322. Prober, S. M., C. Tompkins, G. F. Moran, and J. C. Bell. Meagher, T. R., J. Antonovics, and R. Primack. 1978. Ex- 1990. The conservation genetics of Eucalyptus califormis 606 SPECIAL FEATURE Ecology, VoL 75, No. 3

L. Johnson et Blaxell and E. carvifolia Cambage, two rare Strong, M. T., and P.M. Sheridan. 1991. Juncus caesariensis species from SE Australia. Australian Journal of Botany 38: Coville (Juncaceae) in Virginia peat bogs. Castanea 56:65- 79-95. 69. Riese berg, L. H., and M. F. Doyle. 1989. Allozyme variation Sutter, R. D. 1984. The status of Helonias bullata L. (Lil­ in Helianthus praecox ssp. hirtus, a rare sunflower from iaceae) in the southern Appalachians. Castanea 49:9-16. southern Texas. Aliso 12:379-386. (g) Van Treuren, R., R. Bijlsma, W. van Dilden, and N. J. Qu­ Rieseberg, L. H., S. Zona, L. Aberbom, and T. D. Martin. borg. 1991. The significance of genetic erosion in the pro­ 1988. Hybridization in the island endemic, Catalina ma­ cess of extinction. I. Genetic differentiation in Salvia pra­ hogany. Conservation Biology 3: 1-7. tensis and Scabiosa columbaria in relation to population Sampson, J. F., S. D. Hopper, and S. H. James. 1988. Ge­ size. Heredity 66:181-187. (g) netic diversity and the conservation of Eucalyptus crucis Vivian, V. E. 196 7. Shortia galacifolia: its life history and Maiden. Australian Journal of Botany 36:447-460. (g) microclimate requirements. Bulletin of the Torrey Botan­ Schwartz, 0. A. 1985. Lack of protein polymorphism in the ical Club 94:369-387. (e, d) endemic relict Chrysosplenium iowense (Saxifragaceae). Ca­ Waller, D. M., D. M. O'Malley, and S. C. Gawler. 1988. nadian Journal of Botany 63:2031-2034. Genetic variation in the extreme endemic Pedicularis fur­ Soltis, P. S., and D. E. Soltis. 1991. Genetic variation in bishiae. Conservation Biology 1:335-340. (g) endemic and widespread plant species: examples from Sax­ Wiens, D., D. L. Nickrent, C. I. Davern, C. L. Calvin, and ifragaceae and Polystichum (Dryopteridae). Aliso 13:215- N.J. Vivrette. 1989. Developmental failure and loss of 223. (g) reproductive capacity in the rare paleoendemic shrub De­ Soltis, P. S., D. E. Soltis, T. L. Tucker, and F. A. Lang. 1992. deckera eurekensis. Nature 338:65-67. Allozyme variability is absent in the narrow endemic Ben­ Worz, A. 1988. Investigations of distribution and phyto­ soniella oregona (Saxifragaceae). Conservation Biology sociological characteristics of Chaerophyllum elegans Gau­ 6:131-134. (g) dia (Apiaceae). Botanica Helvetica 98:87-96.