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Home , Population biology, Population size, Restoration ecology, Small population size

areas of particular importance to restoration Restoration Biology: that offer potentially unique opportunities to couple basic research with the practical needs of restoration- ists. The five research areas are: (1) the influence of A Biology numbers of individuals and in the initial population on population colonization, estab- lishment, growth, and evolutionary potential; (2) the Perspective role of local and life history traits in the success of restored ; (3) the influence of Arlee M. Montalvo1,10,11 the spatial arrangement of landscape elements on 2 dynamics and population processes Susan L. Williams such as migration; (4) the effects of , gene Kevin J. Rice3 flow, and selection on population persistence within 4 an often accelerated, successional time frame; and (5) Stephen L. Buchmann the influence of interspecific interactions on popula- Coleen Cory5 tion dynamics and development. We also 6 provide a sample of practical problems faced by prac- Steven N. Handel titioners, each of which encompasses one or more of Gary P. Nabhan7 the research areas discussed, and that may be solved by addressing fundamental research questions. Richard Primack8 9 Robert H. Robichaux Introduction ur understanding of the ecological mechanisms Abstract O underlying successful restoration is not keeping pace with the societal needs for restoration. An A major goal of population biologists involved in res- improved understanding of the processes involved in a toration work is to restore populations to a level that successful restoration can be gained if we learn from will allow them to persist over the long term within a the “field experiment” that underlies every restoration dynamic landscape and include the ability to undergo project. However, because of the expense of restoration adaptive evolutionary change. We discuss five research and its often mandated practice, biologists cannot wait to learn the specific responses of every species within every different restoration site. Instead, we need inno- 1U.S.D.A. Forest Service, Pacific Southwest Research Station, vative research to develop a general template that will 4955 Canyon Crest Drive, Riverside, CA 92507, U.S.A. help us to manage ongoing projects and provide guid- 2Department of Biology, San Diego State University, San Diego, ance for the design of future restoration efforts. As a CA 92182-0057, U.S.A. step toward addressing this problem, this paper sum- 3Department of Agronomy and Range Science and the Center marizes the results of discussions of the Population Bi- for Population Biology, University of California, Davis, CA ology Group during the Restoration Workshop 95616, U.S.A. of the National Science Foundation. 4U.S.D.A. Agricultural Research Service, Carl Hayden Bee Re- The long-term viability and credibility of the practice search Center, 2000 East Allen Rd., Tucson, AZ 65719, U.S.A. 5Nature Conservancy of Hawaii, 1116 Smith St., Suite 201, of restoration depends on an understanding of the basic Honolulu, HI 96817, U.S.A. biological and ecological processes that operate at a site 6Department of Biology, Nelson Lab, Rutgers University, P.O. under restoration. Restoration projects span a contin- Box 1059, Piscataway, NJ 08855-1095, U.S.A. uum, from augmentation of populations of single spe- 7The Arizona-Sonora Desert Museum, Tucson, AZ 85743- cies within relatively intact to the building 8919, U.S.A. of ecosystems from bare ground. This continuum can 8Department of Biology, Boston University, 5 Cummington provide valuable opportunities for comparing the suc- St., Boston, MA 02215, U.S.A. cess of restored populations under different sets of initial 9 Department of Ecology and , University conditions. However, ultimate goals vary widely, as do of Arizona, Tucson, AZ 85721, U.S.A. the criteria used in judging whether a restoration is suc- 10The order of the three primary authors was assigned ran- cessful (Hobbs & Norton 1996; White & Walker 1997). domly. The remaining authors are arranged alphabetically. 11Corresponding author. The discipline of population biology provides one perspective on what might be considered a successful © 1997 Society for Ecological Restoration restoration. Population biology is a marriage of popula-

DECEMBER 1997 Vol. 5 No. 4, pp. 277–290 277

Population Biology and Restoration tion ecology and population . The field of pop- Third, research conducted within restorations is likely ulation ecology examines birth, growth, reproduction, to involve that are not the conventional “mod- and death within populations and seeks to identify the els” for testing ecological and evolutionary theory. The factors that influence the success and distribution of practical necessity of manipulation of a wider array of populations. seeks to understand organisms should help, in the long run, to increase our how the genetic composition of populations changes understanding of the robustness of theoretical predic- over time, and what factors influence the change. The tions, as well as providing a broader appreciation of integration of the theoretical and empirical aspects of . For example, despite the longstanding in- these disciplines promotes our understanding of the terest in the evolutionary biology of colonizing species processes involved in causing evolutionary change, es- (Baker & Stebbins 1965; Parsons 1983; Barrett & Hus- pecially adaptive change (Harper 1977; Solbrig 1980). band 1989; Rejmánek 1996), there has been surprisingly As was so aptly stated by Dobzhansky (1973), “nothing little direct testing of hypotheses about colonizing abili- in biology makes sense except in the light of .” ties in the field or the genetic consequences of coloniza- In essence, the conceptual framework of population bi- tion. By its very nature, restoration is characterized by ology originates from the theory of organic evolution. colonization processes. This conceptual framework forms the basis of a popula- Finally, successful restorations provide case histories tion biologist’s viewpoint that restoration is ultimately of populations that have persisted despite suboptimal successful when populations are restored to a level that edaphic conditions, pressures, lack of mutu- allows them to persist as dynamic parts of a metapopu- alists, and invasion by non-. These case lation over the long term within a changing landscape. histories, and the potential to design restorations as ex- Restored populations must possess attributes necessary periments (Pavlik et al. 1993), provide a challenging op- for reproduction, growth, migration, and adaptive evolu- portunity for the biologist who wishes to understand tionary change. population processes within the realistic context of en- Restoration provides special research opportunities vironmental variation, multispecies interactions, and for population biology. Although there is a wealth of successional change. Because restorations often occur population genetic and demographic theory, there is an on degraded or virtually unpopulated sites, research empirical gap in testing such theory with species cho- conducted in such sites is relevant to understanding the sen for reasons other than their experimental tractabil- factors that influence colonization, growth, and distri- ity (i.e., model systems). Research in restorations pro- bution of populations within a complex ecological vides a way to close this empirical gap. We see four arena. Such empirical data are needed for basic tests of major research opportunities for population biologists population biology theory. Furthermore, understand- who use restorations for research. First, restorations are ing the responses of populations to extreme ecological fundamentally a manipulation of biota in the field conditions typified by many restorations will help iden- within already degraded. Restorations thus tify the boundary conditions important for population provide a sanction for population biologists to conduct growth, persistence, adaptation, and interactions. Restora- field experiments, sometimes over large spatial scales, tion research should afford a rich payoff for understand- that are otherwise unthinkable for fear of resulting ef- ing fundamental evolutionary and ecological theory. fects on natural populations and communities. For exam- During the National Science Foundation (NSF) Work- ple, the demographic and genetic attributes of popula- shop, we grappled with our charge of identifying re- tions can be manipulated to examine how these factors search gaps that could be uniquely addressed in a resto- influence , or , or both. ration context and also include the definitive components Second, restored communities are also often character- of quality restoration research. This is, in part, because ized by very dynamic temporal change resulting from we kept uncovering population biology research that is colonization events and succession. A common restora- needed by practitioners to carry out economically feasi- tion goal is to either accelerate or freeze the process of ble, successful restorations. Other than special opportu- . Some species and populations will nities discussed above, there really is no reason why a be established deliberately by the restoration while oth- population biologist would submit a proposal, for ex- ers might colonize naturally. Thus, restoration projects ample to the NSF, to conduct research within a restora- provide an opportunity for investigating the role of pop- tion. However, this slights the opportunity for a mar- ulation dynamics and evolutionary responses in non- riage between field tests of fundamental population equilibrium conditions and their importance in determin- biology theory and restoration practice. Instead, the op- ing patterns of succession. The success of restoration may portunity should be promoted as a conscionable use of in part be judged by the re-establishment of successional public funds for research with a tangible bonus of im- processes that, in the long term, may be characterized proved restoration practice. We echo the premise of the by species that were not part of the initial biotic mix. Sustainable Biosphere Initiative put forward by the

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Ecological Society of America that as habitats continue stand much about fundamental population processes as they to deteriorate and as funding for research is limited, “... occur in nature. the greater are the applied needs, the more important becomes the basic research. If this point is not made Research Areas clear, narrowly based applications will carry the day” (Lubchenco et al. 1991). Numerous principles important to restoration research In this paper, we discuss five research areas that were and practice stem from the integration of population of paramount importance in our discussions during the genetic and ecological theory. Many principles and workshop. Though not exhaustive, these research areas their links to restoration biology are identical to those in include fundamental questions that have long occupied the field of because populations of the field of population biology. All were considered ap- restored and threatened or have propriate for pursuit in restorations, address practical small sizes, and restorations can involve threatened or problems faced by practitioners, and will provide the endangered species. Critical reviews of a wide range of bonus of useful information for practitioners of restora- population biology principles important to restoration tion. Research areas 1–2 examine the importance of and conservation practice can be consulted for more de- and of the amount and type of genetic tail (Harper 1977; Millar & Libby 1989, 1991; Falk & Hol- variation to population establishment, persistence, and singer 1991; Guerrant 1992; Ellstrand & Elam 1993; evolutionary potential; 3–4 examine variation in suc- Bowles & Whelan 1994; Handel et al. 1994; Frankham cessful establishment, persistence, and migration of 1995; Falk et al. 1996; Young et al. 1996). For example, the populations and how this may be influenced by succes- basic genetic considerations important in species reintro- sion and the organization of landscape elements; and 5 ductions are described in Millar & Libby (1989), Barrett & examines the influence of interspecific interactions on Kohn (1991), Fenster & Dudash (1994), and Guerrant the colonization, establishment, migration, and growth (1996), while the concepts important to measuring the of populations in the context of community develop- vulnerability and success of populations are discussed in ment. The need to obtain specific autecological knowl- Gilpin & Soulé (1986), Pavlik (1994, 1996), and Guerrant edge and strategies for species reintroductions, as dis- (1996). Although the conceptual basis for restoration bi- cussed in several recent volumes (Falk & Holsinger ology is extant, there is still a need to test many of the 1991; Bowles & Whelan 1994; Falk, Millar, and Olwell predictions generated from basic principles (Barrett & 1996), may be lessened by the formation of general tem- Kohn 1991; Fenster & Dudash 1994; Guerrant 1996). plates produced from the suggested research. We then present a sample from our varied experiences 1. The Influence of Numbers of Individuals and Genetic Variation of practical examples of restoration problems where fun- Represented in the Founding Population on Colonization, damental research in population biology is obviously Establishment, Growth, and Evolutionary Potential. needed. Most of the problems are complex and bridge two or more research areas, emphasizing the challenge Evolution of populations requires genetic variation, and that restorations present to population biologists. the larger the genetic variance, the greater the potential Interaction and communication between biologists for adaptive evolutionary change (Falconer 1981; Hartl & and practitioners of restoration are critical elements of Clark 1989). Because restoration usually begins with rela- restoration biology. Practitioners posed several ques- tively small populations, the amount of genetic variation tions at the workshop that require results from popula- represented in the founding population can be critical. In tion level research (Clewell & Rieger 1997), including: (1) small populations, stochastic changes in size can severely How do we establish indigenous materials at resto- reduce the genetic variation within a population, thus in- ration sites? (2) How do we remove or exclude aggres- creasing the opportunity for non-adaptive evolution by sive weeds, pests, and exotic and animals that random genetic drift at the expense of adaptive change threaten to arrest development of restored projects? (3) by (Ellstrand & Elam 1993). Reduction Can we take advantage of mutualistic relationships to ac- in population size and genetic variance is expected to in- celerate restoration results? (4) How do we know if we crease the opportunity for and subsequent in- are introducing organisms with appropriate gene pools breeding depression. Strong fol- into a restoration site? Such questions, together with the lowing inbred mating has been shown for most wild practical examples of restoration problems presented species examined and can even occur in plants that un- here, point to specific gaps in the understanding of pop- dergo habitual selfing (Charlesworth & Charlesworth ulation biology and the need for an integrated concep- 1987; Lande et al. 1994; Montalvo 1994). Similarly, if a tual framework to guide research that links practical founding population has low , e.g., if the needs with basic science. Indeed, if we could answer the plant material used to restore a site is collected from few questions of restoration practitioners, truly we would under- parents or from an inbred stock, this can result in low ef-

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Population Biology and Restoration fective population size, severe inbreeding depression, Restorations also provide special opportunities for and a decrease in the adaptive evolutionary potential of research linking genetic diversity to population growth. the population (Barrett & Kohn 1991). There are few studies that explicitly examine how the How much genetic variation exists within a popula- persistence and growth of populations vary as a func- tion of a given size and growth rate, and how it changes tion of their genetic diversity (Leberg 1993; Young et al. over time, are thus important to the long-term success 1996). Restored populations can be manipulated in of a restoration. The effective population size (Ne) pro- terms of their initial genetic diversity and population vides an index that relates theoretical models to “real size in the field with relative impunity, as pointed out world” populations and can be used to help predict the in the introduction. Population growth rates can then probability of extinction or evolutionary potential of be modeled to facilitate an explicit comparison of populations. Given a measured amount of genetic drift growth rates of populations having, for example, natu- or inbreeding, Ne is the number of individuals within ral versus reduced genetic diversity. This may entail an “ideal” population mating at random that would population vulnerability analysis (PVA sensu Gilpin & produce the observed amount of drift or inbreeding. Soulé 1986) of rates of population growth, stability, or Thus, “real world” deviations from the ideal assump- decline (Pavlik 1994; Guerrant 1996). Once a demo- tions of genetic theory (e.g., random mating, equal sex graphic model of population growth is constructed, ratio, non-overlapping generations, constant popula- sensitivity/elasticity analyses of the model can then be tion size over generations, and no selection) can be en- used to identify the critical life history stages that make capsulated as differences between the effective popula- the most important contribution to population growth tion size and the number of reproductive individuals. (Caswell 1989). The explicit link between genetic diver- Typically, Ne is smaller than the census population size, sity and population growth rate, which is the compre- and it is notoriously difficult to estimate for organisms, hensive measure of (Endler 1986), could be such as plants, in which matings are difficult to observe made. The results of such experiments could answer or which reproduce vegetatively (Nunney & Elam practical questions about whether there is a critical min- 1994). Nonetheless, Ne captures both genetic and demo- imum population size for population establishment and graphic population processes, and is a metric for evalu- persistence and whether certain mixes of genotypes ac- ating the potential importance of different types of evo- celerate initial population growth. Results of sensitivity/ lutionary processes in altering gene frequencies within elasticity analyses have value for establishing guide- populations. For example, in populations with effective lines for the kind of material (e.g., seeds versus cut- sizes Ͻ100, genetic drift may be very important in alter- tings) to use in restorations. ing gene frequencies from one generation to the next. In Currently, restorations represent missed opportuni- contrast, populations with large effective sizes (e.g., ties for explicitly testing the hypothesis that genetic di- Ͼ1000) in theory are little affected by genetic drift, and versity is necessary for population persistence and, if it changes in gene frequencies are more likely the result of is, over what time frame. In part this opportunity is selection or . missed because it is commonly (although surprisingly In practice, there are relatively few estimates of Ne for to us) argued that genetic diversity is not a critical issue plant populations (Nunney & Elam 1994), and plants when restoring a habitat. For example, there is the cost are the foundation for many restoration projects. Addi- of genetic screening. There is a certain reluctance to em- tionally, very little is known about factors that affect Ne brace the issue of genetic diversity when most previous in nature. For example, Heywood (1986) has demon- research training and focus have been on strated that the large differences in reproduction ob- functioning, e.g., provision of trophic support. There is served among plants within natural populations (i.e., also the view that environmental considerations, such reproductive hierarchies) often reduce effective popula- as for subtidal , are of larger im- tion size dramatically. Experimental manipulations of mediate importance for restoration success. This is cer- both plant density and availability have fur- tainly true, but research should lead to improved site ther indicated that potential reductions in effective pop- selection and preparation such that the short-term suc- ulation size are greatest in dense populations within cess of a restoration is less risky to the long-term goals. productive environments (Rice 1990). Because restora- Improvements in short-term success in turn should en- tion projects often manipulate both plant density and able refocusing on longer-term goals for success. site resource availability, they represent excellent oppor- The academic debate among conservation biologists tunities to increase our understanding of how ecological of the relative importance of demographic consider- factors influence Ne. The potential also exists to study the ations of very versus genetic di- interaction of demographics and genetics on effective versity for effective management of population size because the initial demographic and ge- (Lande 1988; Doak 1989; Schemske et al. 1994) has netic structure can be manipulated in a restoration. helped fuel the belief that genetic diversity is of second-

280 Restoration Ecology DECEMBER 1997

Population Biology and Restoration ary importance in restorations. In part this debate exists sess whether single or multiple sources of seeds present because of the paucity of empirical data that link ge- the best strategy for initiating populations in novel en- netic diversity to population persistence, including di- vironments, especially in the case of in which rect tests of the relative importance of small population genetic variance may already be very low within any size, low genetic diversity, and environmental stochas- single source population (Barrett & Kohn 1991; De- ticity. These tests could be performed in restorations Mauro 1994; Guerrant 1996). Identifying the environ- (Pavlik et al. 1993). As pointed out recently (Nunney & mental amplitude and responses to novel or ex- Campbell 1993; Lande 1994), both genetic diversity and treme habitats (Hoffmann & Parsons 1991) can be a useful demography offer important insights on how popula- bridge between the needs of restoration practitioners tions persist, grow, and adapt. and evolutionary biologists. In summary, restorations should offer excellent ex- Physiological variants that are successful under spe- amples for the population biologist of the potential im- cial conditions also can be identified for many species, portance of evolutionary processes in ecosystem resto- and used or tested in newly restored sites. For example, ration and sustainability. variants that tolerate unusual , such as those rich in heavy metals, offer special opportunities for population biologists interested in the role of ecotypic variation in 2. The Role of and Life History Traits in the the restoration of very degraded sites (Bradshaw & Success of Restoration. Chadwick 1980). Evidence from a variety of ecological and genetic data Locally adapted populations often represent a “ge- supports the view that populations can be locally adapted netic memory” shaped by past selective events that, al- (Bradshaw 1984; Linhart & Grant 1996). For example, though infrequent (e.g., 50-year freezes or 100-year many studies have found correlations between environ- droughts), are nonetheless important agents of selec- mental variables and phenotypic variation in both plants tion. Introductions of non-local genotypes that domi- and animals (Conkle 1973; for review see Endler 1986). nate a population initially, but cannot withstand extreme Given that plants of the same genotype can differ phe- selective events over the long term, represent a non-sus- notypically depending on their environment, some of tainable restoration strategy. The of plants the variation detected could be explained by a plastic well-adapted to local environments can be swamped response to the environment rather than by heritable through with a more poorly adapted gene variation. Indeed, many researchers have argued that pool of non-local plants if they outnumber the local phenotypic plasticity itself is a trait subject to selection plants (i.e., if occurs). In large-scale (for reviews see Bradshaw 1965; Schlichting & Levin restoration projects, introduced plant material with of- 1986; Via 1987). Research has verified that local adapta- ten limited genetic variability may be spread over a tion promotes higher fitness under the specific ecologi- spatial scale that approaches that of a landscape. As a cal conditions of a site, including metal concentrations result, the adaptive capacity of a few genotypes of a and herbivore loads (Clausen et al. 1940, 1947, 1948; Si- particular plant species might determine the success of lander 1985; Schmidt & Levin 1985; for reviews see Harper the restoration of an entire watershed. 1977; Bradshaw 1984; Millar & Libby 1989; Huenneke “Genetic pollution” may also occur through - 1991; Linhart & Grant 1996). ization of individuals from different gene pools. Even For restoration, a critical question involves the source when initial hybrids demonstrate increased fitness rela- of genetic material with respect to its adaptedness. The tive to the parental population (i.e., heterosis or “hybrid large amount of genetic variation in many populations vigor”), subsequent generations may suffer reduced fit- offers restoration ecology an opportunity to closely ness (i.e., outbreeding depression; Wallace 1968; Fal- match locally adapted variants with the proper micro- coner 1981) and the buildup of a “.” Out- site conditions. Use of proper genotypic variants is be- breeding depression has been shown to occur in wild coming a more common concern in restoration plan- species of plants at both regional and very local levels ning (Millar & Libby 1991; Fenster & Dudash 1994; (Waser 1993; Guerrant 1996). However, there is insuffi- Handel et al. 1994; Guerrant 1996). In newly restored cient evidence for deciding the likelihood that out- ecosystems, the presence of ecologically relevant ge- breeding depression will occur in the event that non-lo- netic variation within populations of the few dominant cal gene pools are utilized in restoration (Fenster & species planted on a site may strongly affect restoration Dudash 1994). Within a restoration project, the ability to success (Smith & Bradshaw 1979; Bradshaw & McNeilly manipulate the initial genetic “mix” provides at least 1981). Carefully selected restoration sites can be used to the possibility for testing questions about the persistence test predictions about the performance of suspected lo- and intensity of genetic loads within populations that cally adapted genotypes (including life history vari- represent a mixture of local and non-local genotypes. ants) in novel environments. There is also a need to as- The considerable natural variation within and among

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Population Biology and Restoration species in life history traits including life form (annual, netic diversity, genetic structure, and gene flow data is perennial), sexual versus asexual reproductive mode, needed to better understand metapopulation dynamics and generation time has long held the attention of evolu- and long-term population viability (Hastings & Harri- tionary and population biologists. In plants, life history son 1994). attributes tend to correlate with colonization ability, mat- The lack of knowledge concerning the effects of isola- ing system, population structure, and population growth tion is especially notable for evolutionary processes rates (Hamrick & Godt 1989; Hamrick et al. 1992) and such as adaptation and gene flow, processes that have may provide clues to understanding population coloni- long-term effects on the stability and sustainability of zation, establishment, and subsequent persistence and populations targeted for restoration. For example, frag- growth. Given the correlations of such traits with ge- mentation of populations can either increase or reduce netic diversity and gene flow potential, problems asso- gene flow (Young et al. 1996). Because gene flow is such ciated with using non-local germplasm may be greater a powerful evolutionary force (Slatkin 1985), increased for plants possessing particular combinations of life his- gene flow could drastically alter a species’ genetic archi- tory and reproductive traits. Consequently, the potential tecture and disrupt local adaptation, while decreased for their populations to become locally adapted may also gene flow and isolation of populations could allow higher vary. New research could determine the effect of using rates of genetic drift or selection, depending on the pop- non-local germplasm on population fitness in species ulation size (Endler 1977; Slatkin 1973). that represent a range of life history attributes. This Gene flow among fragmented populations and geneti- would allow tests of predictions concerning the sensitiv- cally divergent restored populations has become a ma- ity of particular combinations of life history attributes to jor concern in the restoration of plant populations (Millar genetic pollution. & Libby 1989; Barrett & Kohn 1991; Fenster & Dudash The link between life history attributes and coloniza- 1994; Knapp & Rice 1994) because of the potential for tion ability is also an important research area. Because outbreeding depression and disruption of local adapta- natural colonization events are difficult to witness, res- tion by an increased influx of inappropriate (i.e., mal- torations provide the opportunity to focus on the colo- adapted) genetic material. Surprisingly little is known nization and establishment phase of population growth. about the effects of human-induced fragmentation on Founding populations can be experimentally manipu- patterns of gene flow (Lacy 1987; Lande & Barrowclough lated in large field settings. One example of a potential 1987; Robinson & Quinn 1992), but studies on “natu- research question is the relative importance of asexual rally fragmented” populations of colonizing or weedy and sexual (seed) reproduction in the survival, growth, species strongly suggest that both the severity and the and spread of plant populations. This question can be pattern of fragmentation should have a marked effect studied under a variety of environments and genetic on gene flow (Larson et al. 1984; Ellstrand & Marshall backgrounds in restorations, allowing an understand- 1985; Young et al. 1996). An explicit consideration of the ing about which life history strategies are favored un- interactions between populations on restored sites and der particular environments. landscape-level elements could significantly improve our understanding of the effects of fragmentation on the demographic and evolutionary dynamics of natural pop- 3. The Influence of the Spatial Arrangement of Landscape ulations. Elements on Metapopulation Dynamics and Population Processes such as Migration and Gene Flow. 4. The Effects of Genetic Drift, Gene Flow, and Selection on The specific position of a restoration within the land- Population Persistence within a Defined, often Accelerated, scape may influence the fate of a restoration project Successional Time Frame. (Bell et al. 1997). Even when restoration is successful, the restored site may be spatially isolated from other Currently, there is very little information on the relative similar habitats. As a result, restored landscapes often importance of evolutionary mechanisms of genetic drift, are fragmented. Understanding the metapopulation dy- migration, , and selection over successional namics of restored populations requires information time. Successional changes at a restoration site provide about natural colonization and extinction rates and the an excellent opportunity to examine whether evolution- degree to which the populations are linked by migra- ary changes occur in concert with community dynam- tion (i.e., gene flow via pollen and seed dispersal; ics. The dynamic nature of successional changes, partic- Gilpin 1987; Hastings & Harrison 1994; Fiedler & Laven ularly if accelerated by human manipulation, can be 1996; Primack 1996). The use of demographic data in used to examine non-equilibrium dynamics of genetic transition matrix models to explore metapopulation dy- variation in space. namics has proved valuable in understanding popula- The limited information available on evolutionary tion viability (Menges 1990). However, inclusion of ge- changes during succession suggests that both selection

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Population Biology and Restoration and drift can occur. Along a forest successional gradi- Understanding how changes in species interactions ent, Scheiner & Teeri (1986) examined the potential ge- influence selection over successional time is a difficult netic basis for population differentiation among popu- problem. In a study on successional processes in perma- lations of a perennial grass (Danthonia spicata) in response nent pastures, Aarssen & Turkington (1985a) proposed to changes in light availability. Two conclusions are rel- that species associations become more predictable as evant to our discussion. First, the persistence of D. spi- succession proceeds. In an accompanying paper (Aars- cata along successional light gradients was primarily de- sen & Turkington 1985b), they further suggested that pendent on phenotypic flexibility (i.e., plasticity) rather increased persistence of species associations fosters than narrowly defined genetic adaptation. Second, the competitive coevolution whereby competitive abilities genetic differences that occurred among D. spicata pop- become more balanced by reciprocal selection during ulations were more likely the result of genetic drift succession. Experiments that test such predictions rather than selection. could be attempted at restoration sites. Because change in physical and biological conditions is intrinsic to restoration, it may be rewarding to use 5. The Influence of Interspecific Interactions on Population restoration experiments to examine how genetic drift Establishment, Colonization, Growth, and Community and selection interact in time to create genetic structure Development. (the non-random distribution of genotypes in space). Experiments could also be done to identify the condi- No population exists in an ecological vacuum, and pop- tions that determine whether a variety of narrowly ulation biologists need to study the effects of biological adapted genotypes or fewer, but phenotypically plastic, interactions on the dynamics of populations. Histori- genotypes in the population leads to greater population cally, such research has been restricted to two interact- success. ing populations and a limited suite of interactions. In restorations, the disturbed habitat might provide a Competition, herbivory, , , and mu- novel environment in which strong selection can occur. tualisms all play roles in the development and fate of However, successful adaptation may not be possible if restored sites. Restorations offer an opportunity to ex- this coincides with conditions for rapid genetic drift pand research on community interactions in a signifi- due to the established population having a small effec- cant way because of the great variation in the “ecologi- tive size. Thus, evolutionary processes might operate at cal theater” (Hutchinson 1965) surrounding them, which a more rapid temporal scale during restoration, blur- can be small, simple, and distant; or extensive, complex, ring the distinction between “ecological time” and and next door. Such variation provides a means to test “evolutionary time.” From the practical point of view, if hypotheses about the influence of population size, spe- degraded sites undergoing restoration provide harsh cies diversity, isolation, and the strength of species in- environmental conditions that translate into extreme se- teractions on population growth and community devel- lection regimes, then the establishment of vegetative opment. The composition and position of the surrounding cover can be delayed by the selective elimination of biotic matrix will steer the restoration into certain pop- poorly adapted genotypes (McNeilly 1987). ulation trajectories, influencing, in turn, the functioning Studies of genetic structure under non-equilibrium and fate of the restored sites. The interplay between the conditions would make important contributions to pop- restored and surrounding populations offers much op- ulation genetics. After Sewell Wright (1943) proposed portunity to understand the fate of colonizing or new that evolution through isolation of populations by dis- populations, especially those that appear at the edge of tance results in the non-random distribution of genetic a range. variation in space, population geneticists have used his Because restoration sites are prone to invasions by F statistics (Wright 1951) to infer levels of gene flow non-native species, and because the history of the site is among populations. However, an underlying assump- usually documented, restorations provide opportuni- tion relating F statistics to gene flow is that the distribu- ties to investigate the ecological effects of non-native tion of genetic variation has reached an equilibrium, species on native communities. The ecological effects of i.e., genetic divergence via genetic drift is balanced by non-native species on native communities are very migration. Theoretical models indicate several hundred poorly known, as pointed out in a Special Features is- generations can be required before equilibrium is reached. sue of the Ecological Society of America (“Advances in Until then, gene flow is highly dependent on how ge- Invasion Ecology,” Ecology, Volume 77 (6), 1996). Com- netic variation is distributed within and among sub- petitive exclusion of desirable natives by weedy exotics populations (Varvio et al. 1985). This theory, and also can threaten the success of restorations, especially on the appropriateness of using equilibrium models such highly degraded sites. In some restorations invaded by as Wright’s F statistics to infer gene flow, could be field- non-native species, the ecological interactions are pain- tested in restorations. fully evident (see below—the practical example of inva-

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Population Biology and Restoration sive species in Hawaii), and the economic impetus to tar and pollen might be limiting. The provision of artifi- study them is great. In other cases, ecological interac- cial substrata for nesting in restorations enables manipu- tions are less apparent. For example, expensive eelgrass lation of population densities (Roubik 1989; Buchmann & restorations were reputed to fail in San Diego Bay due Nabhan 1996). Information about the population sizes, to invasion by the non-native mussel Musculista sen- resource requirements, movements, colonization, and housia. In natural unfragmented eelgrass populations, patterns of mutualists will inform us about po- mussel populations declined, while in the fragmented, tential for the evolution of specialist interactions and sparse eelgrass transplanted populations, the mussels whether restored plant populations reproduce compared interfered with eelgrass vegetative propagation (T. Reusch to merely surviving in a proper microsite. & S. Williams, unpublished data). The ecological inter- Using restorations for experiments regarding the in- actions were much more complex than was suggested fluence of species interactions on the success of popula- by a negative correlation between eelgrass and mussel tions can also provide a critically needed bridge between abundances, and could be dissected only by using both population biology and community ecology. Changes in restored and natural habitats. the structure of communities follow underlying changes Mutualistic interactions play a pivotal role in popula- in the births and deaths in the interacting populations. tion establishment, reproduction, migration, and com- Because restorations experimentally manipulate the num- munity development. The importance of mutualists, bers of individuals and species under at least semi-con- ranging from bacteria and mycorrhizae to trolled conditions, they present the opportunity to quan- seed dispersers, in the ecological functioning of commu- tify the underlying demographic changes in interacting nities and whole ecosystems has become an important populations that fundamentally control community struc- part of ecological research (Boucher 1985; Allen 1991), ture. Thus, the study of the regulation of community and restored populations offer opportunities to address structure can move from being observational and infer- key interactions (Handel et al. 1994; Handel 1997). ential to becoming more mechanistic and predictive. Restoration of plant populations is a necessary, but The practical payoff for research on species interac- not sufficient, action to rebuild a functioning habit. For tions in restorations is great. As many restored sites are most plant species, interactions with mutualists such as financially tied to scarce public funds, links among pollinators and seed dispersers are needed for the sus- plants and mutualists must be established early in a res- tainable growth and population increase of species of toration project to avoid the need for additional inter- interest. Unfortunately, for mutualists such as bees and vention, such as adding new individuals or species, in other pollinating animals that may act as keystone com- future years. Presently, there are virtually no commer- munity members of natural and modified environ- cial sources for many native species of pollinators, and, ments, we usually know little or nothing about their rel- thus, the restorationist will be dependent upon knowl- ative species abundances and diversity. For example, edge of these species in the wild. Furthermore, even if a the biology of thousands of species of native bee polli- surrogate pollinator is very effective, the chance that it nators is poorly known, and many bee species them- will disperse pollen in a way similar to that of the natu- selves are threatened and in need of population en- ral pollinator may be small. Seed-dispersing mutualists hancement (Buchmann & Nabhan 1996). Also, there is a must also be attracted to restoration sites to implement greater diversity among pollinators and dispersers in the dual roles of spreading individuals of installed plant their foraging and movement patterns and their effects species and introducing new ones from surrounding ar- on reproductive success and gene flow of plants (Beat- eas. If seed dispersers are abundant around and within tie 1985; Seeley 1985; Roubik 1989; McClanahan & a restoration site, then the potential for population Wolfe 1993; Robinson & Handel 1993; Willson 1993; growth and gene flow is high, as long as the surround- Buchmann & Nabhan 1996). ing area does not provide more favorable habitat (Bron- Understanding the roles of population size, disper- stein 1995). sion, and distribution among habitat types is critical to Many other types of species interactions have impor- understanding the strength of population interactions. tant effects on restoration success. Populations of herbi- Restored populations, engineered at different sizes and vores may move quickly into a small restoration from a in different settings, give ecologists the opportunity to large surrounding community and devastate the newly understand the thresholds of population size that deter- established plant populations. Microbial and other mine maximum efficiency of dispersal and mutualists such as mycorrhizae, nitrogen-fixing bacte- for interacting populations. For example, the limiting ria, saprophytes, and the many cryptic phyla of animals resource for a mutualist can be identified through ex- potentially regulate the growth rate of restored popula- perimentation in restorations where the initial matrix of tions. Soil amendments and inoculations may add to interacting populations and their sizes are controlled. the richness of these species, and restorationists must For bee species, holes for nest initiation rather than nec- consider the level of soil remediation with these mutu-

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Population Biology and Restoration alists for population persistence. Reserved soil for seed effective population sizes of the restored seagrass pop- bank additions has been used for several sites, and these ulations, this example points to the need to understand soils also may be quite useful for microbial sources (Leck how genetic factors interact with environmental factors et al. 1989). From the discussion above, it should be in determining the persistence of restored populations. clear that the ecology of these interactions is too poorly known to guide restoration practices. The use of non-local germplasm. It is the policy of numer- ous government agencies to follow germplasm transfer guidelines designed to maximize genetic diversity, in- Practical Examples breeding avoidance, and the chance that the germplasm The interfaces among the research areas presented used is appropriately adapted to environmental condi- above are obvious and are exactly where some of the tions of the planting site. A combination of population most challenging research exists. For example, what re- genetic theory, studies on local adaptation in plants, finements of evolutionary theory are needed to capture ecological genetic work, and provenance (common gar- the essence of within the complex den) tests (Clausen et al. 1940, 1948; Kitzmiller 1990), to- background of communities and ecosystems changing gether with numerous studies of the genetic structure through time? The restoration problems highlighted in of natural populations of plants (see Hamrick & Godt the practical examples below include elements from 1989; Westfall & Conkle 1992), served to steer the cre- most of the research areas discussed in the previous ation of guidelines. section. Some also include other elements, such as the Unfortunately, germplasm transfer guidelines for interface of autoecological research and population bi- non-tree species are frequently ignored by land manag- ology. Our current understanding of population biol- ers and practitioners for a variety of logistical, financial, ogy is limited, and this becomes clearer when put to the and personal reasons. The genetic background of plant- test of restoration practice. ing stock used is often non-local or unknown, is often low in genetic diversity, and may even include nursery Limited stock selection from donor populations. Lack of ge- or field-raised individuals exposed to unintentional se- netic diversity within restored populations may acceler- lection (Hillyard 1990; A. Montalvo, personal observa- ate their failure to persist, even in the short term. Sea- tion). If population biologists and agencies expect to grass restorations may be one example. Seagrass beds gain the cooperation of practitioners in adhering to have been targeted for restoration in many coastal areas germplasm transfer guidelines, it is critical that we test because they are important to coastal water quality and the fundamental building blocks of the guidelines in the ecological functioning of intertidal and subtidal ma- ways that have direct application to problems faced by rine environments (Williams & Davis 1996). Seagrass practitioners. The information garnered will allow fine- restorations are conducted by removing vegetative ma- tuning of germplasm transfer guidelines so that practi- terial from an adjacent seagrass bed because seed ger- tioners can be better advised about use of guidelines. mination and seedling recruitment are very limited in The fitness consequences of using non-local germ- natural populations. A practical problem is that the ma- plasm are being examined in coastal sage scrub vegeta- terial is typically collected by SCUBA divers who can- tion. This is one of the most endangered plant commu- not effectively cover large areas of underwater habitat. nities in North America, primarily because of extensive Material has been collected from areas as small as 200 m2 urban development in the Mediterranean climatic re- (S. L. Williams personal observation). Because seagrasses gions of California where it occurs. Within this habitat, are highly clonal, the transplantation stock might repre- frequent wildfires, construction, mitigation, and recre- sent few clones and only a fraction of the natural ge- ational activities result in continuous restoration and netic diversity of a population. Furthermore, adjacent efforts. After large-scale wildfires, public source beds can be ones that were established previ- agencies frequently practice control by seeding ously using similar techniques. Williams & Davis (1996) burned slopes adjacent to densely populated residential have shown that the genetic diversity of transplanted areas. In recent years, mixtures of seeds from native and eelgrass beds is lower than that of natural untransplanted naturalized species have been used in these revegetation beds in San Diego County, California. Previously, more efforts. The genetic background of the seeds was non-lo- attention had been paid to determining the type of sea- cal or unknown. Even in habitat restoration work where grass material to establish, the appropriate site charac- such urgency is not a factor, managers often resort to us- teristics, and the functional equivalency of the created ing plant sources of unknown genetic or ecological origin seagrass habitat than to the population-level attributes. (Hillyard 1990; A. Montalvo, personal observation). Despite this knowledge, most seagrass mitigations have Dramatic differences often exist between individuals resulted in a net loss of habitat (Fonseca et al. 1988). indigenous to a restored site and those introduced. This Given the low genetic diversity and potentially small is especially true for widely distributed species that ex-

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Population Biology and Restoration hibit geographic variation in numerous traits. For ex- natal nest, so their ability to colonize new habitats is ample, nursery stock of the shrub Salvia mellifera Greene limited. A study by Leong (1994) on the pollinators within (black sage) was transplanted into a pipeline corridor six-year-old artificially constructed vernal pools located cut through an ecological reserve in southern Califor- 25 km from a natural pool complex provided further nia. The transplants within the restored zone evidence for the limited dispersal and colonization abil- later than the indigeous surrounding population (A. ity of these andrenid bees. Although the artificial pools Montalvo, personal observation). Such asynchronous contained suitable host plants and were supplemented flowering has been found to be detrimental to fitness in by additional potted plants, over two flowering seasons other plants. In one experimental study of a tropical no andrenid bees were observed visiting . Leong shrub in which groups of plants were forced to flower (1994) further examined the potential impacts of this asynchronously with the rest of the population, the lack of andrenid bee pollinators by using potted individ- smaller, earlier-flowering groups suffered decreased seed- uals of the endemic vernal pool annual Blennosperma set and increased seed predation compared to the gen- nanum (Hook.) Blake (Asteraceae) as phytometers (liv- eral population (Augspurger 1981). Restoration sites of- ing meter sticks) of pollinator effectiveness. Compared fer an opportunity to examine whether phenological, to natural vernal pools, the insect visitation rate, number morphological, or physiological differences affect her- of pollinator taxa, and seed set were significantly lower bivory, pollinator visitation, fruit initiation, seed set, in the artificial pools. Plants within the artificial pools and seed predation of plants. also exhibited a greater tendency for pollen limitation of seed set. Taken together, these results suggest that Genetic bottlenecks and unwanted selection in commercially successful restoration or creation of vernal pools depends produced seeds and plants. Even when local germplasm critically on the proximity of natural pools. In general, is used to provide plants for restoration, there is an op- restoration sites can yield novel opportunities for study- portunity for “unconscious selection” when seeds are ing the relative effectiveness of flower visitors as polli- collected for agronomic “increase” or raising of con- nators and the importance of species-specific host–plant tainer plants for outplanting. First, initial seed collec- mutualisms within sites as well as at a landscape level. tions could be from small or depleted natural popula- Even when a minimally disturbed or essentially natu- tions, introducing founder effects. Second, under the ral habitat appears intact, it can be suffering from what unnatural conditions of seed increase and container plant has been called “chemical ” (Nab- production, it is entirely possible that significant shifts han & Buchmann 1997). One such example of chemi- in genotypic frequency may occur in a relatively short cally altered habitats occurs on federally protected bor- time. Evidence from the agronomic literature suggests derlands between the United States and Mexico. Species that significant shifts can occur within a single genera- of night-blooming cacti (Peniocereus spp.) bloom for tion (Stanford et al. 1960). Third, container plant increase only 2–3 nights per year and are pollinated at night by often involves rooting of cuttings from a limited number hawkmoths in the genera Hyles and Manduca. The lar- of parental individuals, accentuating the potential for se- vae of these moths are the tomato hornworms familiar lection of few genotypes that are well adapted to the to gardeners and are heavily sprayed in Mexico. The nursery environment. Factors such as climatic differ- volant adults are essential to the reproduction of plants ences, fertilizer application rates, harvesting techniques, on the U.S. side of the border where pesticide drift and and horticultural practices might shift the genetic consti- overflights endanger the pollination and subsequent re- tution of a collection in ways that may reduce its poten- production/fruit set of these cacti. This type of subtle tial for successful reintroduction into the original site chemical pollution and strategies to correct it are im- (Rice 1995). There is a need for examining the hypotheti- portant to consider when establishing plant/pollinator cal success of agronomically and horticulturally in- populations at restoration sites. creased populations in restoration sites relative to the use of more diverse, untreated control populations. Competition with . The presence of unwanted invasive species makes restoration a formidable task. Absence of mutualists. Pollinator specificity is a phenom- Restoring native plant communities in the Hawaiian Is- enon that can significantly complicate restoration efforts. lands has been an especially difficult problem because For example, within vernal pool communities in the of the density and aggressiveness of alien plant species Central Valley of California, Thorpe and Leong (1995) (Loope & Medeiros 1994). Naturalized alien species ac- have shown that many of the endemic annual species count for nearly half (47%) of all species found within the pools rely on native, solitary, ground- in Hawaii (Wagner et al. 1990). Any restoration project nesting andrenid bees with high specificity of floral in Hawaii must deal with invasive species that are not hosts. In addition, these pollinators are characterized by only alien to the site but probably alien to the island limited flight ability and a tendency to remain near the chain. Many restoration projects have been “passive,”

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Population Biology and Restoration involving weed eradication and fencing of degraded ar- hibiting a range of life histories and interspecific inter- eas to exclude non-native ungulates in order to allow actions. Tests take place in the wild, typically on small natural to occur. Fencing to protect native populations in which both the demographic and ge- seedlings, however, can sometimes simultaneously ex- netic structure can be controlled. The opportunity exists acerbate the weed problem by eliminating grazing ani- to manipulate species interactions to observe the effects mals (Loope & Medeiros 1994). of mutualists, pests, and competitors on population es- Current research examines life history traits of alien tablishment and growth, providing links between pop- woody species in natural areas throughout Hawaii in ulation and community ecology. The results of such re- an attempt to determine what makes these non-native search will contribute to improved restoration practice species so successful (Reichard 1996). Herbaceous spe- and success of restorations over the long term. cies have not been assessed in this study, though they are a particular problem in mesic and dry sites. Under- standing differences in life histories and environmental Acknowledgments requirements of weeds relative to native species is of The authors thank Jan Beyers, Len Nunney, Tim Paysen, particular interest to land managers and ecologists who Taber Allison, and an anonymous reviewer for offering are attempting to restore a site. This research can be valuable suggestions for improving the manuscript; E. used to test and improve theoretical models of plant in- Allen, D. Falk, M. Snowball, and M. Allen for organiz- vasiveness (Rejmánek 1996). ing the workshop; and the National Science Foundation Reintroduction of threatened and endangered plant populations. for funding the workshop. We acknowledge the follow- ing financial support: S. Williams—the Coastal Ocean Reintroduction of plant populations is a recommended Program, National Oceanic & Atmospheric Administra- strategy in approximately one-third of the management tion (#NA36RGO469); A Montalvo—the National Re- plans for species listed as threatened or endangered by search Initiative Competitive Grants Program (#9A-37101- extinction. Reintroduction is often deemed necessary 0385) and the Metropolitan Water District (agreement because natural dispersers are absent, the habitat is #1551); S. Buchmann and G. Nabhan—W. Alton Jones fragmented, and local seed production is too low. Al- Foundation and the Dodge Foundation; and K. Rice— though it has been assumed that reintroduction is a via- NSF Grant DEB9123979. ble management strategy, evaluations have uncovered a surprisingly high number of failures. These failures raise questions concerning what is the appropriate life LITERATURE CITED history stage (e.g., seeds, seedlings, adults) to use in res- toration. Should material be collected from the wild if Aarssen, L. W., and R. Turkington. 1985a. Vegetation dynamics and neighbour associations in pasture-community evolution. possible, or taken from controlled growth conditions in Journal of Ecology 73:585–603. greenhouses, gardens, and nurseries? What is the effect Aarssen, L. W., and R. Turkington. 1985b. Biotic specialization be- of the number of seeds, their genotype, and age on pop- tween neighbouring genotypes in Lolium perenne and Trifo- ulation establishment, and how do these characteristics lium repens from a permanent pasture. 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Pages 254–277 in A. H. D. Brown, forests in Massachusetts and long-leaf pine forests in M. T. Clegg, A. L. Kahler, and B. S. Weir, editors. Plant popu- South Carolina (Primack 1996). lation genetics, breeding, and genetic resources. Sinauer Asso- ciates, Inc., Sunderland, Massachusetts. Barrett, S. C. H., and J. R. Kohn. 1991. Genetic and evolutionary con- Conclusions sequences of small population size in plants: implications for conservation. Pages 3–30 in D. A. Falk and K. E. Holsinger, ed- We have emphasized that restorations provide a unique itors. Genetics and conservation of rare plants. Oxford Univer- opportunity for testing fundamental predictions made sity Press, New York. Beattie, A. J. 1985. The of ant–plant mutual- from the theory of population genetics and ecology, isms. Cambridge University Press, Cambridge, Massachusetts. while aiding the theory and practice of restoration. Res- Bell, S. S., M. S. Fonseca, and L. B. Mooten. 1997. Linking restora- toration research includes a wide array of life forms ex- tion and . Restoration Ecology. 5:318–323.

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