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Ecological Genetics and the Restoration of Plant Communities

Ecological Genetics and the Restoration of Plant Communities

panies restore drill pads. restoration projects of Ecological Genetics and all sizes are becoming common (Kline & Howell 1987). Hard rock and strip mines often require intense recla- mation (Schaller & Sutton 1978). Logged forests, aban- the Restoration of doned agricultural lands, and overgrazed rangelands all require large scale restoration efforts (Millar & Libby 1989; Jackson 1992; Roundy et al. 1995). Communities: In the past, reclamation of degraded land has usually been accomplished with a few species that were often Mix or Match? exotic to the disturbed area. But there is growing awareness that restoring function and bio- logical diversity often requires the use of . 1 Peter Lesica Many animals, especially insects, require specific native Fred W. Allendorf1 for food (Futuyma 1983). In addition, native plants often provide the specific vegetation structure re- quired for nesting or feeding (Bock et al. 1986; McAdoo Abstract et al. 1986; Wilson & Belcher 1989). Furthermore, exotics may compete with native plants (Bock et al. 1986; Lesica We present a conceptual framework for choosing na- & DeLuca 1996) and alter the frequency or intensity of tive plant material to be used in restoration projects ecosystem processes such as fire (Cox et al. 1990). For on the basis of ecological genetics. We evaluate both these reasons the use of native plants in ecological res- the likelihood of rapid establishment of plants and toration is becoming increasingly important. the probability of long-term persistence of restored or Much of the literature on ecological restoration per- later successional communities. In addition, we con- tains to the choice of species to be used (Chambers et al. sider the possible harmful effects of restoration projects 1984). It is becoming increasingly apparent, however, on nearby and their native resident popu- that intraspecific genetic differentiation in relation to lations. Two attributes of the site to be restored play site is also important (Belnap 1995). Many res- an important role in determining which genetic source toration sites, such as mine spoils, pose novel and se- will be most appropriate: (1) degree of vere challenges to vegetation, and only specific and (2) size of the disturbance. Local plants or plants may be able to survive (McNeilly & Bradshaw 1968). from environments that “match” the to be re- On the other hand, plants introduced from distant source stored are best suited to restore sites where degree of populations may not be adapted to the local climatic, disturbance has been low. Hybrids or “mixtures” of edaphic, or biotic environment (Millar & Libby 1989; genotypes from different sources may provide the Knapp & Rice 1994; Linhart 1995). best strategy for restoring highly disturbed sites to One goal of restoration is creation of self-supporting which local plants are not adapted. Cultivars that have communities that will provide ecosystem functions and been modified by intentional or inadvertent selection processes, as well as prevent and provide habi- have serious drawbacks. Nevertheless, cultivars may tat for diverse native species (Bradshaw 1987). Rapid be appropriate when the goal is rapid recovery of establishment of plants with a high survival rate is im- small sites that are highly disturbed. portant to prevent erosion and invasion by exotics. In addition, the long-term persistence of restored or later Introduction successional communities is also important. Restoration of populations has received a good here has been an increase in efforts to restore habi- deal of attention recently (Bowles & Whelan 1994; Falk Ttats degraded by human activities throughout the et al. 1996), but our concern is with restoration and rec- world (Berger 1990; Anderson 1995; Hobbs & Norton lamation of native vegetation rather than reintroduc- 1996). Restoration projects vary greatly in size and de- tion of rare species. gree of disturbance to be ameliorated. Managers of na- Relatively little attention has been given to the effects tional parks and forests attempt to restore vegetation of of restoration projects on nearby ecosystems and their trails, roads, and campgrounds (Majerus 1997). Oil com- native resident populations. Potential threats to local communities and populations from restoration efforts 1Division of Biological Sciences, University of Montana, Mis- result from the introduction of genes and the loss of lo- soula, MT 59812, U.S.A. cally adapted genotypes. Species are likely to require the genetic variation found throughout their range in © 1999 Society for Ecological Restoration order to adapt to future environmental changes. Over

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Ecological Genetics of Restoration the long term, local genotypes may be crucial to the per- ronments in western North America, but there is little sistence of populations or the species as a whole evidence for genetic differentiation among populations (Frankel & Soulé 1981). from most of these (Wu & Jain 1978; Rice & Opinions differ on the correct strategy for choosing Mack 1991). The African grass Pennisetum setaceum has plant materials for restoration (Belnap 1995). Many res- adapted to widely different habitats on the island of torationists use cultivars selected for high performance Hawaii without detectable genetic differentiation (Will- in restoration situations (Wright 1975; Pater 1995; Shaw iams et al. 1995). & Monsen 1995), while others champion the use of local sources (Knapp & Rice 1994; Linhart 1995). A third strategy uses mixtures of populations or hybrid geno- Artificial Propagation types (Millar & Libby 1989; Munda & Smith 1995). We Strong inadvertent directional selection may occur dur- cannot recommend a single correct strategy for any spe- ing cultivation (Knapp & Rice 1994). Production of na- cific situation. Rather, we present a conceptual frame- tive plants for restoration involves collection of wild work for assessing the value of different strategies seed, and genetic variation can be lost through inade- across a wide array of situations. We approach this quate sampling (Brown & Briggs 1991). Assuming that problem by first reviewing the underlying genetic prin- there is genetic variation within cultivated populations, ciples and then placing these principles in the context of some plants will be more vigorous under cultivation restoration ecology. Finally, we evaluate various strate- than others. These plants will produce more seed and gies for choosing restoration plant materials in light of be over-represented in standard nursery seed collec- ecological genetics theory. tions (Knapp & Rice 1994). It is impossible to predict what these inadvertent selection forces will be (Temple- Genetic Principles ton 1991). Intentional selection also often occurs during the Local propagation of native plants for restoration (Voigt et al. 1987; Alderson & Sharp 1994). Several strategies are Numerous studies have demonstrated that plants evolve employed to select for desirable characters such as for- local ecotypes closely adapted to their immediate envi- age and seed production, seed germinability, and toler- ronment (Turesson 1922; Clausen & Hiesey 1958; Brad- ance of salt, heat, and drought. These strategies vary shaw 1972; Turkington & Harper 1979; Linhart & Grant from weak uniparental selection in a single generation 1996; but see Rapson & Wilson 1988). For example, Pen- to strong recurrent selection (Wright 1975; Vogel & Ped- stemon eatonii (firecracker penstemon) seed shows ap- ersen 1993). parently adaptive ecotypic differentiation for germination Selection will increase the frequency of alleles re- requirements. Seed from high-elevation populations re- sponsible for the desired trait but may also result in the quired long chilling periods, while those from low ele- deterioration of other aspects of performance (Hartl & vations needed only short chill times for germination Clark 1989). For example, selection for rapid growth of- (Meyer et al. 1995). High-elevation ecotypes may be able ten will also result in shorter life span. The two primary to establish an initial population in low-elevation sites, mechanisms of genetic correlation are pleiotropy (one but could be curtailed by failure to gene having many phenotypic effects) and linkage dise- recruit a second generation due to inadequate chilling quilibrium (selection for one gene will also affect other periods. Atriplex canescens (fourwing saltbush) popula- closely linked genes on the same chromosome). Strong tions vary for cold hardiness. Warm desert populations directional selection will also reduce the genetically ef- may not survive in cold desert environments following fective and result in increased genetic a severe winter (Meyer & Monsen 1992). There is also a drift and more rapid loss of genetic variation. great deal of intraspecific variation for disease resis- tance in plants (Futuyma 1983; Burdon 1987; Aug- spurger 1988). Pacific slope plantings of interior strains of Pseudotsuga menziesii (Douglas fir) have failed due to diseases of little consequence to resident populations Genetic drift refers to changes in allele frequency from (Silen 1978). generation to generation caused by sampling error. While many widespread species demonstrate adap- That is, the genes transmitted to progeny are an imper- tive genetic variation over their range, others maintain fect sample of the allele frequency in the parents. The a wide ecological amplitude, apparently by means of smaller a population, the greater will be the genetic one or a few highly adaptable, phenotypically drift. Genetic drift causes a loss in genetic variation genotypes (Bradshaw 1965). The Eurasian grasses Bro- (heterozygosity and allelic diversity) within popula- mus tectorum and B. rubens occur in many different envi- tions (Nunney & Elam 1994).

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Genetic drift is potentially of special concern in resto- There is also a danger that introduced populations ration because of the so-called “founder effect.” The will alter local ecological relationships by transferring founding of a new population by a small number of in- adaptive genes to resident populations (Rissler & Mel- dividuals will cause abrupt changes in allele frequency lon 1996). Crop-weed systems are appropriate for mod- and loss of genetic variation (Barrett & Kohn 1991; Ell- eling the genetic effects of introductions on native pop- strand & Elam 1993). Such severe population size “bot- ulations. Transfer of genes from crops into adjacent, tlenecks” associated with the establishment of a new conspecific, or congeneric weed populations regularly population are a special case of genetic drift. occurs (Small 1984; Santoni & Berville 1992). Substantial (1–89% hybrid progeny) has been reported at distances of up to or greater than 1000 meters in a single Gene Flow generation (Kirkpatrick & Wilson 1988; Langevin et al. Gene flow in plants—the immigration of nonlocal 1990; Klinger et al. 1992; Arias & Riesberg 1994). In genes, gametes, or individuals into resident popula- many cases, gene exchange from crops to weed popula- tions—is determined partly by breeding, pollination, tions has led to the evolution of more competitive weeds and dispersal systems (Levin & Kerster 1974). Higher (Panetsos & Baker 1967; Baker 1972; Barrett 1983). levels of gene flow occur in insect-pollinated, wind-pol- linated, and obligate outcrossing species (Ellstrand & Hybridization Hoffman 1990) but substantial gene flow (up to 33% hy- brids in one generation) can occur even in species that High levels of genetic variation resulting from inter- are primarily autogamous (Wilson & Manhart 1993). and intraspecific hybridizations may facilitate adapta- Gene flow can reduce the fitness of local genotypes tion to novel or stressful environments in plants (Ander- (Slatkin 1985). Neutral, or near-neutral, alleles can be son & Stebbins 1954; Mulligan & Moore 1961; McArthur lost from a population by the swamping effect of mass et al. 1988; but see Whitham 1989; Jain 1994. For exam- immigration and genetic drift. Swamping becomes ple, hybrids between the irises, Iris brevicaulis and I. fulva, more likely as the number of immigrants increases rela- occur in habitats unique relative to the parental species tive to the number of residents. But genes that confer a (Cruzan & Arnold 1993). Natural hybrids between the strong and persistent adaptive advantage are not usu- sages, Salvia apiana and S. melifera, are rare but are lo- ally lost from a resident population, even in the face of cally common in novel, but disturbed habitats such as high levels of gene flow (McNeilly 1968; McNeilly & abandoned orchards (Anderson & Anderson 1954). Hy- Bradshaw 1968; Bradshaw 1972; Nagy 1997). brids between two subspecies of Artemisia tridentata Adaptive genes or multiple gene complexes of resi- (big sagebrush) have higher fitness than either parental dent populations could be lost to swamping if their se- in a novel habitat formed following the last gla- lective advantage is temporally variable. Drift and high ciation (Wang et al. 1997). levels of gene flow can act to replace adaptive geno- Populations of multiple ecotypes are likely to show types during periods when selection is “relaxed.” Many increased long-term stability compared to single-line local may not be apparent during “usual” populations (Marshall & Brown 1973) because natural years but may become extremely important when un- selection may vary over short distances or periods of usual extreme conditions occur (e.g., drought, floods, or time. Different ecotypes of Trifolium hirtum (rose clover) extreme temperatures). For example, many genes that germinate better under different conditions. Thus, colo- confer disease resistance have a large selective advan- nies started from mixtures of two ecotypes are more tage when the target disease is present, but these same likely to persist than monomorphic colonies (Martins & alleles are often at a selective disadvantage when the Jain 1979). Stebbins and Daly (1961) studied a hybrid disease is absent (Burdon 1987). The frequency of the swarm between the sunflowers Helianthus annuus and resistance gene will cycle in response to the H. bolanderi in an environmentally heterogeneous site in of the pathogen. Loss of a resistance allele from the California. They found that annuus-like hybrids were population could occur if a large immigration of nonre- more abundant in one part of the population, while sistant genes occurs during that part of the cycle when bolanderi-like hybrids were more common in the other resistance genes are infrequent and not favored by se- part. It is unlikely that either species alone could have lection. Cold-hardiness can be swamped out by a fast- occupied this site as completely as the hybrid popula- growing, cold-vulnerable genotype introduced in large tion. Hybrid populations will not always out-perform numbers during a period of benign weather. For exam- single ecotypes on stressful sites, and more research is ple, coastal Douglas fir grows faster than inland ecotypes; needed to determine the generality of the hybrid supe- but coastal ecotypes may survive for many years only riority phenomenon in the context of restoration. to be killed by occasional extreme cold temperatures In contrast, hybridization between genetically dis- when planted in interior sites (Silen 1978). similar individuals may also result in a decline of prog-

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Ecological Genetics of Restoration eny fitness (i.e., outbreeding depression; Lynch 1991). On the other hand, severely disturbed sites, such as Two mechanisms can account for outbreeding depres- mine tailings or roadsides where the topsoil has been sion (Templeton 1986; Waser 1993). Under the “genetic” removed, will pose a novel and often stressful ecologi- or “intrinsic” mechanism, the parental individuals have cal challenge to introduced plants. High levels of ge- different intra-genomic coadaptations that are dis- netic variation may be needed for long term persistence rupted in the hybrid progeny. Sterile triploid progeny in severely disturbed sites (Munda & Smith 1995). produced by matings between diploid and tetraploid parents is an extreme example of this. The “ecological” Size of Disturbance or “extrinsic” mechanism of outbreeding depression re- sults from of the parents and the pro- The size of the disturbance dictates how much material duction of progeny less suited to either parental envi- will be introduced and is important in determining how ronment (see Local Adaptation section above). severely resident populations will be affected. The area There is evidence for outbreeding depression in to be restored may be small compared to the surround- plants (Sobrevilla 1988; Barrett & Kohn 1991; Waser ing native vegetation. Examples include roadcuts, small 1993); but most examples of outbreeding depression mines, and oil and gas drill pads. In these situations more likely result from the ecological rather than the there is little chance that local adaptive genotypes will genetic mechanism (Waser 1993; Wang et al. 1997; but be swamped out by introduced genes when the latter see Whitham 1989). Ecological outbreeding depression are at a great numerical disadvantage. But introduced can result in the failure of hybrids in parental (i.e., na- genes that are adaptive could spread into resident pop- tive) habitat, thus helping to prevent swamping of in- ulations. digenous genotypes following restoration introductions Larger disturbances, such as strip mines, overgrazed (see Gene Flow section above). But ecological outbreed- rangeland, or intensively harvested forests, present a ing depression should not be relevant for disturbed res- different situation because the quantity of introduced toration sites because they are different from parental genetic material is relatively large compared to that of habitats. Genetic outbreeding depression could result in resident populations immediately surrounding the site. a hybrid zone dominated by individuals with lower fit- Resident alleles will be at a numerical disadvantage ad- ness than the indigenous population (Whitham 1989). jacent to the site, and those not presently under strong selection may be lost to drift.

Restoration Ecological Genetics Restoration Strategies The genetic constitution of an introduced population is A primary goal of restoration is the rapid establishment likely to have an important effect on the short- and of long-term viable populations that will restore ecosys- long-term persistence of the restored and adjacent na- tem functions and processes, prevent erosion, and pro- tive populations. Genotypes may be derived from vari- tect biological diversity. Restoration should also pre- ous sources, including local populations, distant popu- serve the ecological and genetic balances present in lations, or cultivars. Two attributes of the site play an adjacent native communities. Degree and size of the important role in determining which genetic source will disturbance are critical factors. Three general strategies be most appropriate: (1) degree of disturbance and (2) are employed to choose genetic makeup for restoration size of the disturbance. Both are continuous variables, plant material: use (1) genotypes derived from local but for the sake of discussion we treat them as discrete. populations, (2) genotypes selected for high perfor- mance in restoration situations, and (3) hybrid geno- types or genotype mixtures with maximum amounts of Degree of Disturbance genetic diversity. We will evaluate each of these alter- Degree of disturbance is the most important environ- natives in light of the size and degree of the distur- mental variable determining the short- and long-term bances being mitigated. persistence of populations introduced for restoration. Disturbances can vary from slight degradation to Local Genotypes nearly complete devastation (Hobbs & Norton 1996). Local genotypes should be well adapted when severity Local genotypes are best suited to restore sites where has been low and the abiotic environment is not very the degree of disturbance has been low (Fig. 1). Al- different than before the disturbance. Such sites might though close correspondence between environment include overgrazed range where structure remains and genotype argues for the use of local genotypes in intact or logged-over forests where post-harvest treat- restoration (Linhart 1995; Knapp & Rice 1996), of ments have not been severe. seriously disturbed sites bear little resemblance to those

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ulations from environmental incompatibility less likely. Mixture or hybrid populations should also be reason- ably well adapted to extreme local conditions if one of the source populations is local. Thus, they should pro- vide both short- and long-term adaptiveness and may be appropriate when the degree of disturbance is high. Using hybrid mixtures or genotypes will likely intro- duce novel genes into the adjacent resident population through cross-pollination, although the degree of ge- netic introgression will depend on the breeding system. Neutral or near-neutral introduced genes will have lit- tle chance of spreading widely in the resident popula- tion if the size of the restoration is small. On the other hand, large introductions of cultivars could alter the resident neutral gene pool. Furthermore, adaptive Figure 1. General relationship to degree and size of distur- genes could be introduced into the resident population bance of three possible sources of plants to be used for restora- regardless of the size of the restoration, although we be- tion projects. lieve that this danger is less than for cultivars that have been selected for short-term fitness. Using autogamous with which natives evolved. Traits found in dissimilar species or genotypes will lower but not eliminate the populations may be needed for adaptation to highly risk of genetic transfer. For these reasons hybrid mix- novel or stressful conditions. Local genotypes are also tures or genotypes will be most appropriate for restor- desirable when the size of the disturbance is large be- ing smaller disturbances (Fig. 1). cause they will have no adverse effect on the integrity of local gene pools (Knapp & Rice 1994; Linhart 1995). Selected Genotypes Collecting seed from all possible ecological settings within a population will maximize genetic variation Cultivars (selected genotypes) have many serious draw- without sacrificing local adaptiveness (Knapp & Rice backs for restoration. Nonetheless, they often perform 1994). A single local population may encompass a great well in stressful conditions to which local genotypes are deal of adaptive genetic variation correlated with topo- not adapted and may be appropriate when the goal is graphic, edaphic, and biotic differences (McGraw 1985; rapid recovery of small sites that are highly disturbed Farris 1987). For example, a species may occur in shal- (Fig. 1). Cultivars of native species possessing the abil- low, stony soils of ridge tops as well as deeper soils of ity to rapidly colonize highly disturbed sites are often lower slopes. Part of a population may occur in full sun, used in reclamation (Voigt et al. 1987; McArthur 1988; while the other part may be found in the partial shade Pater 1995). These ecotypes are chosen or bred for traits of forest margins. Using local genotypes from all possi- such as transplant survival, seed production, seedling ble ecological niches will help ensure the success of this , vegetative vigor, drought tolerance, metal strategy. Millar & Libby (1989), Kitzmiller (1990), Brown tolerance, and competitive ability (Kitchen 1995; Pater & Briggs (1991), Guerrant (1992), and Knapp & Rice 1995). Restoration cultivars often provide the best im- (1994) provide guidelines for sampling maximum ge- mediate results, establishing quickly and providing ad- netic diversity. equate forage or ground cover. In addition, many se- lected cultivars are readily available from government agencies and private producers. Hybrids or a Mixture of Genotypes Unfortunately, cultivars may be poorly adapted for Hybrids between populations, or mixtures of genotypes long-term persistence. The distribution of species is of- from different populations, may provide the best strat- ten controlled by extreme climatic events such as egy for highly disturbed sites to which local genotypes drought, floods, or periods of hot or cold temperatures. are not adapted (Guerrant 1996) (Fig. 1). Mixtures of Cultivars are likely to succumb to stochastic environ- genotypes from ecologically distinct populations or hy- mental extremes when used outside the range of their brids of these genotypes will possess high levels of ge- progenitor population. Furthermore, introduced culti- netic variation. Introduced populations with enhanced vars may lack resistance to local pests and pathogens. variation are more likely to rapidly evolve genotypes But gene flow from surrounding indigenous genotypes adapted to the novel ecological challenges of severely may eventually increase the adaptiveness of introduced disturbed sites. Using genotypes from a large portion of populations, especially if they are small compared to the species’ range makes complete failure of hybrid pop- the native matrix.

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Introduced cultivars could transfer adaptive genes to communities. They may also fail to provide long-term resident populations, possibly resulting in a shift in viability if not derived from local sources. competitive interactions in the . This danger Many other considerations besides genetics must be is especially great when the introduced cultivars have taken into account when choosing plant material for been selected for fecundity, vegetative vigor, or other restoration. Cost and availability can be critical factors. traits that promote aggressiveness in the field. Use of Planning ahead is important, and increased demand self-pollinating species or genotypes will lower the risk should eventually result in adequate supplies of at least of genetic transfer; but moderate levels of gene flow some locally derived material. Some sites may be so se- may occur even in primarily selfing plants. vere that only cultivars selected for stress tolerance will be able to establish vegetation cover within a reason- able time frame. While it is essential to quickly establish Conclusions vegetation that will provide cover and prevent erosion, The short- and long-term success of a vegetation resto- it is equally important to protect the genetic structure ration project may depend on choosing the appropriate and ecological interactions present in the native mosaic genetic source. The size and degree of disturbance of of locally adapted populations. the area being restored are important variables in deter- mining the source for introduced plant material (Fig. 1). Few situations will be unambiguous, and rigid rules are Acknowledgments not practical. Nevertheless, we propose the following We thank C. Loggers for steering us into this interesting general guidelines: topic; S. Winslow, C. Zabinski, and two anonymous re- (1) Avoid strongly selected cultivars. viewers for commenting on the manuscript; and P. Spru- (2) Initiate new populations with as many genotypes ell for preparing the figure. and as much genetic variation as possible (collect seed from many habitats), especially when distur- LITERATURE CITED bances have been severe. Alderson, J., and W. C. Sharp. 1994. Grass varieties in the United (3) Use local genotypes when feasible, especially for States. U.S. Department of – Ser- large sites. vice (USDA-SCS) Agriculture Handbook no. 170. U.S. Gov- (4) Use phenotypically plastic species with wide ecolog- ernment Printing Office, Washington, D.C. ical amplitudes when feasible. Anderson, E., and B. R. Anderson. 1954. Introgression of Salvia apiana and Salvia melifera. Annals of the Missouri Botanical (5) Use selfing species or those with low dispersal capa- Garden 4:329–338. bilities to minimize the genetic contamination of Anderson, E., and G. L. Stebbins. 1954. Hybridization as an evolu- resident populations. tionary stimulus. Evolution 8:378–388. Anderson, P. 1995. Ecological restoration and creation: a review. We believe that understanding the trade-offs in- Biological Journal of the Linnean Society 56:187–211. volved is essential in choosing an appropriate strategy. Arias, D. M., and L. H. Riesberg. 1994. Gene flow between culti- As restoration projects become larger, it becomes more vated and wild sunflowers. Theoretical and Applied Genet- important to use local sources for plant material to ics 89:655–660. Augspurger, C. K. 1988. Impact of pathogens on natural plant lessen the chance of contaminating the resident gene populations. Pages 413–433 in A. J. Davy, M. J. Hutchings, pool. As the degree of disturbance becomes greater, the and A. R. Watkinson, editors. Plant population ecology. importance of high levels of genetic variation will in- Blackwell Scientific, Oxford, United Kingdom. crease. Locally derived material may provide adequate Baker, H. G. 1972. Migration of weeds. Pages 327–347 in D. H. variation if it is collected from ecologically varied habi- Valentine, editor. Taxonomy, phytogeography and evolu- tion. Academic Press, London. tats. Using species with inherently great ecological am- Barrett, S. C. H. 1983. Crop in weeds. Economic Botany plitude resulting from phenotypic plasticity may also 37:255–282. prove to be a viable strategy. In severely disturbed sites, Barrett, S. C. H., and J. R. Kohn. 1991. Genetic and evolutionary however, using hybrid mixtures or genotypes may be consequences of in plants: implications desirable to help assure that populations can adapt to for conservation. Pages 3–30 in D. A. Falk and K. E. Hols- inger, editors. Genetics and conservation of rare plants. Ox- the novel or stressful environment. If introduced geno- ford University Press, New York. types are to be used, species with breeding systems that Belnap, J. 1995. 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