Ecological Genetics and the Translocation of Native Fishes: Emerging Experimental Approaches

ECOLOGICAL GENETICS AND THE TRANSLOCATION OF NATIVE FISHES: EMERGING EXPERIMENTAL APPROACHES

Craig A. Stockwell1 and Paul L. Leberg2

ABSTRACT.—Conservation biologists often use translocations to augment small populations, establish “refuge” populations, or reestablish populations into historic habitat. For reasons that are poorly understood, translocations often fail. Further, translocations have both short- and long-term consequences for the evolutionary ecology of the targeted taxa. Unfortunately, most information on translocations has been derived from descriptive studies. Recent experimental approaches have provided new data to address a variety of topics associated with translocations, including inbreeding, outbreeding, the relationship between heterozygosity and fitness, and rapid evolution in populations established by translocation. We focus on genetic and ecological aspects of translocations but recognize that contributions from other fields will be essential for the long-term success of many translocation programs. Ongoing research regarding host-parasite interactions points out the need for extensive ecological data as well as genetic data to make informed decisions regarding translocations. Hypotheses derived from this field are ripe for rigorous experimental examination.

Key words: rapid evolution, adaptive management, reintroduction, inbreeding, outbreeding, local adaptation, genetic bottleneck.

Translocating animals has become a widely Our objective is to discuss recent research used tool in the conservation of rare and approaches that should prove useful in under- endangered species (Williams et al. 1988, Grif- standing factors affecting success of transloca- fith et al. 1989); this is especially true for tion. Experimental manipulations of popula- desert fishes (Hendrickson and Brooks 1991, tions together with new analytical techniques Minckley 1995). Historically, translocations can provide important insights into how genetic were often conducted in an emergency context and ecological processes affect translocation to save a rare species from extinction (Miller success. We focus on small fishes because they and Pister 1971, Minckley et al. 1991, Minckley can be experimentally manipulated more eas- 1995). However, translocations are now used ily than other vertebrates and because numer- in a more deliberate manner. Typically, they ous fish species have been the subject of past occur in 4 contexts: to mitigate effects of pro- translocations (Hendrickson and Brooks 1991, posed economic development, to augment Fuller et al. 1999). The results of both manipu- established populations, to create refuge pop- lative and management translocation experi- ulations, and to reestablish historic popula- ments involving fish populations will have tions. Following Wolf et al. (1996), we consider management implications for not only this translocations to include the intentional release important group but also many other verte- of either wild caught or captively reared indi- brate taxa. viduals. Traditional translocation research has em- Translocations will probably continue to phasized genetics (Turner 1984, Vrijenhoek et occur in the management of rare species. More al. 1985, Allendorf and Ryman 1987, Quattro than 80% of recovery plans for endangered and Vrijenhoek 1989, Echelle 1991, Leberg and threatened fishes call for some form of 1991, Ellsworth et al. 1994, Leberg et al. 1994, translocation (Williams et al. 1988). However, Hedrick 1995, Stockwell et al. 1996, Leberg translocation programs typically have low suc- and Ellsworth 1999), but these data are best in- cess rates, and factors associated with translo- terpreted in an ecological context. Most trans- cation failure are poorly understood (Hendrick- location research has been descriptive; how- son and Brooks 1991). ever, recent studies have applied experimental

1Department of Zoology, Stevens Hall, North Dakota State University, Fargo, ND 58105. 2Department of Biology, University of Louisiana, Lafayette, LA 70504.

32 2002] EXPERIMENTAL APPROACHES TO TRANSLOCATIONS 33 approaches to address a variety of translocation Genetic variability has been considered an topics, including effects of inbreeding (Leberg important criterion in selecting stock for rein- 1990a), outbreeding (Philipp 1991, Leberg troduction efforts with the Gila topminnow 1993), relationship between heterozygosity (Vrijenhoek et al. 1985, Quattro and Vrijen- and fitness (Quattro and Vrijenhoek 1989, hoek 1989, Quattro et al. 1996). Quattro and Sheffer et al. 1997), and evolution in recently Vrijenhoek (1989) raised fish from 3 popula- established populations (Reznick et al. 1990, tions of the Gila topminnow under common- Stockwell and Mulvey 1998, Stockwell and garden conditions to assess fitness-related Weeks 1999). characters. They found that the stock with the highest heterozygosity (Sharp Spring) had EXPERIMENTAL ASSESSMENTS OF higher survival, higher fecundity, and higher CONSEQUENCES OF GENETIC VARIATION developmental stability as measured by fluctu- ating asymmetry (FA) than did the less het- Populations established by translocation erozygous Monkey Spring population (Quattro often exhibit reduced genetic variability (Allen- and Vrijenhoek 1989). Recently, Sheffer et al. dorf and Ryman 1987, Leberg 1992, Stockwell (1997) repeated this experiment and found no et al. 1996, but see Turner 1984). Leberg difference in stock performance. This discor- (1990a) established experimental populations dance may reflect differences in laboratory of eastern mosquitofish (Gambusia holbrooki) conditions. For instance, 12-week survivorship that differed in levels of genetic variation. was substantially lower in the first study Populations founded by small numbers of in- (45–56%) than in the latter study (93–96%). dividuals had reduced genetic variation and The difference in survivorship suggests that lower population growth rates (Leberg 1990a). the first study included relatively stressful This work supported the basis for suggestions environmental conditions compared to the that a minimum number of individuals be second study. Thus, it is possible that stock used to found new populations (Allendorf and differences may appear only during subopti- Ryman 1987). However, even when numerous mal conditions. This suggests a need for addi- individuals are translocated, bottlenecks may tional ecological work to assess the interaction occur early in population establishment, lead- between environmental conditions and genetic ing to reduced genetic diversity (Stockwell et background on fitness. al. 1996). Such effects occur in an ecological One means to increase genetic variability context; reductions in population size and con- would be to proliferate outcrossing among sequent reductions in genetic diversity may populations, thereby increasing genetic diver- be due to novel ecological conditions. sity and possibly stock performance (Vrijen- Gene flow from parental populations to hoek et al. 1985, Meffe and Vrijenhoek 1988, refuge populations is one solution to minimize Hedrick 1995). Leberg (1993) experimentally loss of genetic variability in refuge populations examined outcrossing effects by crossing pop- (Stockwell et al. 1996). Further, populations ulations of eastern mosquitofish from the same established by translocation should be periodi- river drainage. For a pair of populations sepa- cally surveyed for genetic diversity (Allendorf rated by 10 km, and with similar allele fre- and Ryman 1987, Stockwell et al. 1996). To quencies, there were no positive or detrimen- detect changes in genetic diversity, large num- tal effects on the growth of outcrossed popula- bers of polymorphic loci and alleles should be tions. Population growth rates were lower for used (Leberg 1992, Richards and Leberg 1996); outcrossed groups than for pure stocks when thus, highly polymorphic microsatellite loci may the 2 parental stocks were separated by 100 prove useful as a monitoring tool. For instance, km and had statistically significant differences by using microsatellites, Parker et al. (1999) in allele frequencies. This outbreeding depres- detected genetic structure in the Gila topmin- sion of growth rates may affect population now (Poeciliopsis occidentalis occidentalis) that viability of small or recently established pop- was not observed with either allozymes or ulations (Leberg 1993). Philipp (1991) also mtDNA. Spencer et al. (2000) found levels of conducted experimental work to examine microsatellite variation to be highly correlated the role of outbreeding between subspecies to founder number in experimental popula- of largemouth bass (Micropterus salmoides). tions of Gambusia affinis. This experiment also suggested outbreeding 34 WESTERN NORTH AMERICAN NATURALIST [Volume 62 depression, which was interpreted as a dis- recently established populations had under- ruption of locally adapted gene-complexes gone rapid evolutionary divergence. A recent (Philipp 1991). Future research should con- analysis suggested this case of evolution may sider the relationship between genetic differ- have occurred over a 4-year period (12–16 entiation and outbreeding depression. This generations; Stockwell and Vinyard 2000). information is especially relevant to the design A variety of other studies have documented of translocation programs. rapid evolution for fishes introduced to new Locally adapted gene complexes are of par- localities (Stearns 1983, Reznick et al. 1990, ticular interest because they illustrate the inter- Hendry et al. 1998, Kinnison et al. 1998, Stock- play between local selective regime and genetic well and Mulvey 1998); however, identifying architecture. Local adaptation is likely to in- the selective factor(s) associated with such volve quantitative traits such as behavior, mor- evolution can be difficult. For example, Reznick phology, or life history characters, but our et al. (1990) originally assumed that size-selec- knowledge of how translocations may influ- tive predation was responsible for rapid life ence quantitative traits has received little history evolution in a population of Trinida- attention. Further, such traits are subject to dian guppies introduced to a site with novel natural selection (Lynch 1996) and may evolve predation pressure. However, new data on this in response to novel environmental conditions system suggest that although predation proba- in refuge habitats (see Stockwell and Weeks bly plays a primary role, the specific mecha- 1999). nism remains uncertain (Reznick et al. 1996). The issue of locally adapted gene-com- This demonstrates the difficulty of predicting plexes is also pertinent for remnant popula- how translocated populations may respond to tions of species formerly occurring over large novel ecological conditions, even in well-stud- spatial scales. For instance, genetic surveys of ied systems. the razorback sucker (Xyrauchen texanus) sug- Rapid evolution is of particular concern gest a lack of genetic structure, and yet con- when target populations have been established cern regarding potential outcrossing effects as “genetic replicates” for an endangered species has stalled efforts to reintroduce fish into their (Stockwell and Weeks 1999). For instance, former range (Dowling et al. 1996). This con- concern for the Devil’s Hole pupfish (Cyprin- cern may be valid. Lack of genetic structure odon diabolis) led to establishment of refuge for neutral markers does not necessarily repre- sent a lack of local adaptation at structural or populations to provide stock for reintroduc- regulatory loci (Allendorf 1983). More experi- tion if the native population was extirpated mental research is needed to assess the effects (Williams 1977). Pupfish from one refuge site of outbreeding depression resulting from mix- differed morphologically from Devil’s Hole ing populations with different levels of genetic pupfish (Williams 1977). Unfortunately, extir- differentiation and geographic isolation. Such pation of this refuge population precluded information will aid in the assessment of man- assessment of whether the change was due to agement risks associated with outcrossing. developmental plasticity or rapid evolution. Rapid evolutionary divergence is most likely RAPID EVOLUTION IN when refuge habitats are not well matched to TRANSLOCATED POPULATIONS the ecology of the native habitat. Even under “best case” scenarios, one or more ecological Another evolutionary consequence of trans- factors are likely to differ between the native locations involves rapid phenotypic shifts in site and the refuge site, which could poten- introduced populations. Stockwell and Weeks tially lead to rapid evolution in the refuge site. (1999) reported rapid life history evolution in Ulimately, rapid evolutionary divergence may recently established populations of western result in refuge populations that are mal- mosquitofish (Gambusia affinis). A common- adapted to their original native habitat. One garden experiment confirmed a genetic basis solution may be to provide artificial gene flow for 2 life history traits shown to vary among 4 between native and refuge populations to retard populations derived from the same population evolutionary shifts in the refuge population. in the late 1930s (Stockwell and Weeks 1999, However, such a strategy could render the Stockwell and Vinyard 2000). Thus, these refuge population less viable. Additional data 2002] EXPERIMENTAL APPROACHES TO TRANSLOCATIONS 35 are necessary to assess how managed migration sublethal effects on White Sands pupfish (Col- rates may influence population divergence. lyer 2000). Future work in this system will focus on the genetics of host response to para- TRANSLOCATIONS AND PARASITE sitism. EXPOSURE HISTORY In other systems genetics play a role in the physiological responsiveness of individuals to Translocations may alter important ecologi- parasites. For example, experiments have shown cal relationships for target taxa. For instance, genetic variation for resistance to the parasite translocations can alter the relationship be- Gyrodactylus in topminnows (Poeciliopsis) and tween rare species and parasites in 4 ways. guppies (Poecilia recticulata; Madhavi and First, parasites novel to the introduction site Anderson 1985, Leberg and Vrijenhoek 1994). may be introduced along with the targeted There is only limited knowledge of the genetic taxon (Hoffman and Schubert 1984). Second, basis for differences in parasite susceptibility, translocated populations may encounter para- but candidate loci include the major histocom- sites that did not occur in the native habitat patibility complex (MHC). Hedrick and Parker (Sakanari and Moser 1990). Third, introduced (1998) have found substantial MHC variation populations may escape historic parasites as a among populations of the endangered Gila result of conditions unfavorable to the parasite topminnow. If this variation is associated with in the refuge habitat. Finally, inadequate sam- genotypic differences in response to parasite pling may result in loss of parasites during infection, then genetic surveys of source stocks translocation. Parasites are typically over-dis- might allow managers to design translocation persed; thus, if the founding population is small, programs to restore populations in the face of the entire parasite community is unlikely to be threats from pathogens. established. These examples demonstrate how a broad These problems are especially likely for research perspective is necessary to develop species occupying a diversity of habitat types. successful translocation programs for endan- For example, rainbow trout (Oncorhynchus gered species. We believe that many advances mykiss) populations vary in resistance to the will be made as interdisciplinary approaches myxosporidean Ceratomyxa shasta, presumably are applied. For example, many of the genetic as a result of their history of exposure to this studies we have discussed involve assessment parasite (Bartholomew et al. 1992). Resistance of phenotypic and genetic responses of popu- to this parasite has a genetic basis, and hybrids lations to novel ecological conditions in the between resistant and nonresistant strains show new habitat. intermediate resistance (Ibarra et al. 1992). This has proven important in one situation TRANSLOCATIONS AS MANAGEMENT where introgression has occurred between non- EXPERIMENTS resistant hatchery stock and a resistant native population (Currens et al. 1997). The experimental nonessential clause in Recent work on the White Sands pupfish the Endangered Species Act (section10j) allows (Cyprinodon tularosa) demonstrates how trans- for the experimental establishment of popula- locations may alter historic host-parasite asso- tions. This ruling has been used extensively to ciations. This state-listed threatened species establish populations under politically adverse occupies 4 isolated localities in southern New conditions (Hendrickson and Brooks 1991). Mexico: Malpais Spring, Salt Creek, Mound However, in our opinion the vast majority of Spring, and Lost River. The latter 2 popula- such stockings do not qualify as “experimen- tions were derived by translocation from the tal” in a scientific sense, and we are unaware Salt Creek population in the 1970s (Stockwell of any efforts to conduct replicated experi- et al. 1998). These historic translocations re- mental translocations with rare taxa. This is un- sulted in altered parasite communities for the fortunate because much can be learned when introduced populations (Stockwell and Collyer populations are transferred to new environ- unpublished data). Altered parasite communi- ments (sensu Reznick et al. 1990, 1996, Stock- ties are of most importance if parasitism is well and Weeks 1999). shown to be costly. Recent experimental work One potential approach is to establish popula- has shown that parasitism has both lethal and tions in artificial habitats where experimental 36 WESTERN NORTH AMERICAN NATURALIST [Volume 62 control can be achieved. This would allow research has focused on “model systems,” but managers to create refuge populations for we suggest that similar experimental approaches endangered species while addressing critical be used with target taxa. It is striking that questions relevant to translocation biology. We despite the widespread use of translocations, recognize that complete replication of native very few translocations have been conducted ecological conditions will not be achieved, but in an experimental context (but see Vrijenhoek such an approach allows more experimental 1989). The experimental opportunities associ- control. Further, this approach has an addi- ated with translocated populations are an un- tional benefit of avoiding conflicts with taxa tapped resource. native to refuge sites. In addition to the formal experiments dis- ACKNOWLEDGMENTS cussed above, translocations can be viewed as management experiments (Leberg 1990b). We appreciate discussions with M. Collyer, Translocations provide unique opportunities T. Crowl, P. Fuller, K. Miller, M. Mulvey, R. to further explore ecological requirements of Sheffer, S. Swift, J. Williams, and an anony- targeted taxa. Application of information re- mous reviewer. CAS was supported by sulting from management activities such as Department of Defense Legacy Grant #DAC translocations is the essence of adaptive man- A87-00-H-0014 administered by M.H. Reiser, agement (Holling 1978, Walters 1986). Prior to 49 CES/CEV Environmental Flight, Hollo- the release of individuals, tissue samples should man Air Force Base. CAS would like to dedi- be collected from translocated individuals, as cate this manuscript to the memory of Dr. well as from members of the species already Gary L. Vinyard, teacher, mentor, and good present at the release site. For researchers to friend. fully benefit from experiences, translocation attempts should be carefully documented LITERATURE CITED (Minckley 1995). In many cases monitoring ALLENDORF, F.W. 1983. Isolation, gene flow, and genetic has not been undertaken following the translo- differentiation among populations. Pages 51–65 in C. cation of fish (Hendrickson and Brooks 1991). Schonewald-Cox, S. Chambers, B. MacBryde, and When monitoring is included, techniques and L. Thomas, editors, Genetics and conservation. Ben- definitions of success vary widely (Hendrick- jamin/Cummings, Menlo Park, CA. ALLENDORF, F.W., AND N. RYMAN. 1987. Genetic manage- son and Brooks 1991), and efforts often go ment of hatchery stocks. Pages 141–159 in N. Ryman unrecorded in the peer-reviewed literature and F. Utter, editors, Population genetics and fishery (Minckley 1995). These problems make it dif- management. Washington Sea Grant, Seattle, WA. ficult to assess broad patterns associated with BARTHOLOMEW, J.L., J.S. ROHOVEC, AND J.L. FRYER. 1992. Ceratomyxa shasta infections of salmonid fish. Pro- translocation failure (Hendrickson and Brooks ceedings of the OJI international symposium on 1991, Minckley 1995). Others have pleaded for salmonid disease. Hokkaido University Press, Soporo, better documentation of translocations (Hen- Japan. drickson and Brooks 1991, Minckley 1995), COLLYER, M.L. 2000. The costs of parasitism for White but data on translocations would be more use- Sands pupfish (Cyprinodon tularosa) infected by white grubs (Diplostomatidae). Master’s thesis, ful if archived in a central database; for a simi- North Dakota State University, Fargo. lar database see Fuller et al. (1999). Therefore, CURRENS, K.P., A.R. HEMMINGSEN, R.A. FRENCH, D.A. we recommend the creation of a web-site BUCHANAN, C.B. SCHRECK, AND H.W. LI. 1997. Intro- database for archiving translocation data in a gression and susceptibility to disease in a wild population of rainbow trout. North American Journal of standardized format. Others have assessed fac- Fisheries Management 17:1065–1078. tors associated with translocation success by DOWLING, T.E., W.L. MINCKLEY, AND P.C. MARSH. 1996. analysis of data obtained from resource agen- Mitochondrial DNA diversity within and among cies (Griffith et al. 1989, Wolf et al. 1996). A populations of razorback sucker (Xyrauchen texanus) as determined by restriction endonuclease analysis. centralized database would facilitate such Copeia 1996:542–550. analyses and help to standardize monitoring ECHELLE, A.A. 1991. Conservation genetics and genetic efforts and definitions of translocation success. diversity in freshwater fishes of western North Amer- Translocation is a common tool in the con- ica. Pages 141–153 in W.L. Minckley and J.E. Deacon, servation of rare species, and yet many ques- editors, Battle against extinction, University of Arizona Press, Tucson. tions remain as to the long-term effects of this ELLSWORTH, D.L., R.L. HONEYCUTT, N.J. SILVY, M.H. strategy. Much of the recent experimental SMITH, J.W. BICKHAM, AND W.K. KLIMSTRA. 1994. 2002] EXPERIMENTAL APPROACHES TO TRANSLOCATIONS 37

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