Limitations Of Captive Breeding In Endangered Species Recovery
Limitations of Captive Breeding in EndangeredSpecies RecoveryNOEL F. R. SNYDER,* SCOTT R. DERRICKSON,, STEVEN R. BEISSINGER, JAMES W. WILEY, g THOMAS B. SMITH,IIWILLIAM D. TOONE,**AND BRIAN MILLER,: g*WildlifePreservation Trust International, P.O. Box 426, Portal, AZ 85632, U.S.A.tNational Zoological Park, Conservation and Research Center, Front Royal, VA 22630, U.S.A. :School of Forestry and Environmental Studies, Yale University, 205 Prospect Street, New Haven, CT 06511,U.S.A.§Grambling Cooperative Wildlife Project, Grambling State University, P.O. Box 815, Grambling, LA 71245, U.S.A.[[Department of Biology, San Francisco State University, San Francisco, CA 94132, U.S.A.**San Diego Wild Animal Park, 15500 San Pasqual Valley Road, Escondido, CA 92027, U.S.A., /Fundaci6n Ecologica de Cuixmala, Apartado Postal 161, Melaque, San Patricio, Jalisco, Mexico 48980Abstract: The use o f captive breeding in species recovery has g r o w n enormously in recent years, b u t w i t h o u ta concurrent g r o w t h in appreciation o f its limitations. Problems w i t h (1) establishing self-sufficient captivepopulations, (2) p o o r success in reintroductions, (3) high costs, (4) domestication, (5) p r e e m p t i o n o f other recovery techniques, (6) disease outbreaks, a n d (7) m a i n t a i n i n g administrative continuity have all been significant. The technique has often been invoked p r e m a t u r e l y a n d should not normally be employed before a caref u l field evaluation o f costs a n d benefits o f all conservation alternatives has been accomplished a n d adetermination m a d e that captive breeding is essential f o r species survival. Merely demonstrating that a species" p o p u l a t i o n is declining or has fallen below w h a t m a y be a m i n i m u m viable size does not constituteenough analysis to justify captive breeding as a recovery measure. Captive breeding should be viewed as alast resort in species recovery a n d not a prophylactic or long-term solution because o f the inexorable genetica n d phenotypic changes that occur in captive environments. Captive breeding can p l a y a crucial role in recovery o f s o m e species f o r w h i c h effective alternatives are unavailable in the short term. However, it shouldnot displace habitat a n d ecosystem protection nor should it be invoked in the absence o f comprehensive efforts to m a i n t a i n or restore p o p u l a t i o n s in wild habitats. Zoological institutions with captive breeding prog r a m s should operate under carefully defined conditions o f disease prevention a n d genetic behavioral m a n agement. More important, these institutions should help preserve biodiversity through their capacities f o rp u b l i c education, professional training, research, a n d support o f in situ conservation efforts.Las limitaciones de la cria en cautiverio en la recuperaci6n de especies en peligro de extinci6nE1 uso de la crfa en cautiverio p a r a la recuperaci6n de especies ha crecido e n o r m e m e n t e en a r osrecientes, pero sin u n crecimiento concurrente en el reconocimiento de sus limitaciones. Los p r o b l e m a s con(1) el establecimiento de poblaciones cautivas autosuficientes, (2) el escazo #xito en la reintroducci6n, (3) losaltos costos, (4) la domesticaci6n, (5) la exclusi6n de otras t#cnicas de recuperaci6n, (6) los brotes de enfermedades, y (7) el m e n t e n i m i e n t o de la c o n t i n u i d a d administrativa h a n sido todos signifivativos. Esta tdcnicaha sido f r u c u e n t e m e n t e invocada en f o r m a p r e m a t u r a y no deberfa ser usada n o r m a l m e n t e sin antes Uevara cabo u n a cuidadosa evaluaci6n a c a m p o de los costos y beneficios de todas las alternativas de conservaci6n y de d e t e r m i n a r si la crfa en cautiverio es esencial p a r a ia supervivencia de la especie. Demostrar sim-Resumen:Address correspondence to Noel F. R. Snyder.S§ Current Address: Chamela Research Station, Instituto de Biologia, UNAM, Apartado Postal 21, Melaque, Jalisco 48980 MexicoPaper submitted June 7, 1995; revised manuscript accepted September 19, 1995.338ConservationBiology,Pages338-348Volume10, No. 2, April1996
Snyder et aL.Captive Breeding of Endangered Species339p l e m e n t e que u n a p o b l a c i 6 n de u n a especie esta declinando o ha caido p o r debajo de 1o que serfa del t a m ago viable m i n i m o , no constitutye u n andtlisis suficiente c o m o p a r a justlflcar la crfa en cautiverio c o m o medida de recuperaci6n. Debtdo a los c a m b i o s gen ticos y fenotipicos inexorables que se p r o d u c e n en a m b i e n t e sde cautiverio, la crfa en cautiverio deberfa ser u n a medida a l t i m a instancia en la recuperaci6n y no u n a proflldxis o soluci6n a largo plazo. La cria en cautiverio p u e d e j u g a r u n p a p e l crucial en la recuperaci6n de alg u n a s especies, p a r a las cuales no se encuentran a disposici6n alternativas efectivas en el corto plazo. Sin embargo, esta no debe desplazar a la protecci6n del hdbttat y del ecosistema, aM c o m o tampoco debe serinvocada en ausencia de esfuerzos comprensivos p a r a m a n t e n e r o reestablecer poblaciones en hd bitats naturales. Las instituciones zool6gicas con p r o g r a m a s de cria en cautiverio, deberian operar bajo condicionesc u i d a d o s a m e n t e definidas en cuanto a la p r e v e n c i 6 n de enfermedades y m a n e j o gen tico/etol6gico. A n m a simportante, estas instituciones deben a y u d a r a la preservaci6n de la biodiversidad a trav s de su capacidadp a r a la educaci6n p blica, el entrenamiento profesiona ia investigaci6n, y el apoyo a la conservaci6n in situ.IntroductionIn recent years there has b e e n a tremendous increase inthe use of captive breeding for recovering endangeredspecies. Captive breeding techniques have been improving continuously, as have techniques for reintroducingcaptive-bred animals into the wild. For some species,such as the California Condor ( G y m n o g y p s californ i a n u s ) , the Mauritius Kestrel (Falco p u n c t a t u s ) , t h eblack-footed ferret ( M u s t e l a n i g r i p e s ) , and the GuamRail ( R a U u s o w s t o n O , captive breeding has clearly represented the difference b e t w e e n survival and extinctionin the short term (Snyder & Snyder 1989; Derrickson &Snyder 1992; Jones et al. 1995; Miller et al., in press).Despite the important role that captive breeding hashad in the recovery of some species, w e are concernedthat it is being p r o m o t e d as a recovery technique formany species that may not benefit from it. We note inparticular that the World Conservation Union's (IUCN)Captive Breeding Specialist Group, renamed the Conservation Breeding Specialist Group (CBSG), has recentlygenerated a series of Conservation Assessment and Management Plans (CAMPs) that call for long-term captivebreeding of numerous taxa. For exami01e, the draftCAMP d o c u m e n t for parrots (Seal et al. 1992) recomm e n d e d long-term captive breeding for roughly half ofthe 330 parrot species in the world. For vertebrates ingeneral, Seal et al. (1993) recommended captive management for a staggering 1192 (34%) of the 3550 taxa examined. Furthermore, captive breeding is r e c o m m e n d e d ina remarkable 64% of the 314 approved recovery plansfor U.S. endangered and threatened wildlife (Tear et al.1993). Of special concern are a n u m b e r of "ark" paradigm proposals that envision long-term preservation ofnumerous species through captive breeding, followed,perhaps centuries from now, by reintroductions to thewild (Soul6 et al. 1986; Foose et al. 1992; Tudge 1992).Because the implications of such large-scale relianceon captive breeding are profound and because someproposals currently before Congress would revise theEndangered Species Act to greatly emphasize captivebreeding, w e believe a review of the overall advisabilityof this technique in species recovery is appropriate. Weexamine the role of captive breeding in the recovery ofendangered animal species, focusing on seven oftenoverlooked limitations of the technique. Although w edo not consider plants, w e believe our discussion alsoh is relevance to plant conservation (cf. Ashton 1988;Allen 1994; Hamilton 1994). Captive breeding for recovery purposes (i.e., for ultimate reintroductions to thewild) should not be confused with captive breeding forother purposes, such as exhibit, conservation education,or research. Although these latter captive breeding programs may also have conservation value, they have quitedifferent characteristics and entail different precautions.Our primary conclusion is that captive breeding has alegitimate role to play in the recovery of only a limitedn u m b e r of endangered species and should be employedonly w h e n other viable alternatives are unavailable.When it is employed, it should always be tightly coupledwith recovery objectives for wild populations and shouldnot be p r o p o s e d as a long-term solution.Limitations of Captive It is often assumed that self-sustaining captive populations can be readily established for most endangered andthreatened taxa. However, only a small percentage ofvertebrate or invertebrate taxa have bred in captivity(Conway 1986; Rahbek 1993), and obtaining consistentreproduction and survivorship under captive conditionshas proven difficult with many species (Table 1). Failures to breed well in confinement can be traced to a variety of causes, including the lack of psychological, physiological, or environmental requirements (Millam et al.1988; Merola 1994), inadequate diet (Setchell et al.1987), effects of hand-rearing (Myers et al. 1988), behav-Conservation BiologyVolume 10, No. 2, April 1996
340CaptiveBreedingofEndangeredSpeciesSnyderet al.Table 1. Examplesof endangered species breeding programs that have encounteredsieniflcant problems in achieving self-sustaining captivepopulations.SpeciesWhooping Crane (Grus americana)Kakapo (Strigops habroptilus)Puerto Rican Parrot (Amazona vittata)Hawaiian Crow (Corvus kubaryt3Aye-Aye(Daubentonia madagascariensis)Giant panda (Ailuropoda melanoleuca)Northern white rhino (CeratotheriumProblemslow numbers, high mortality, infertility,incompatibilitylow numbers, poor sut vallow fertility, incompatibility, inbreeding (?)low numbers, low fertility, high mortality,incompatibilitylow offspring survivallow numbers, poor neonate survival,incompatibilitylow numbers, low conception rateReference(s)Lewis (1990)Merton and Empson (1989)Snyder et al. (1987), Brock andWhite (1992)NRC (1992)Sterling (1993)Hu and Wei (1990)Svitalsky et al. (1993)simum cottonOioral incompatibility (Yamamoto et al. 1989), and inbreeding depression (Rails & Ballou 1983; Danielle &Murray 1986). Identifying these factors can be extremely difficult, and for many endangered taxa effectivecaptive management and husbandry regimes are still unk n o w n even after years of experimentation. Because ofpoor reproduction, self-sustaining captive populationsmay never be achieved for some endangered species.For others, large numbers of individuals must be held incaptivity to attain the production needed to sustain reintroduction efforts.ReintroductionIn a recent review of 145 reintroduction programs ofcaptive-bred animals, largely vertebrates, Beck et al.(1994) found only 16 cases (11%) of successfully established wild populations (although with some programsstill in progress, this rate may rise over time). Captivebred stocks also fared relatively poorly in the reintroduction programs reviewed earlier by Griffith et al. (1989).These results suggest major difficulties with establishingwild populations from captive-bred stock.The causes of failure in reintroductions of captivebred animals vary greatly from case to case and rangefrom a failure to correct the factors originally causing extirpation to significant behavioral deficiencies in released animals, especially with respect to foraging, predator avoidance, and social behavior. Such deficiencieshave been documented in a wide variety of captive-bredanimals (e.g., Lyles & May 1987; Kleiman 1989; Miller etal. 1990; Wiley et al. 1992; Fleming & Gross 1993; Snyder et al. 1994). These deficiencies seem especially frequent in species that learn most of their behavioralrepertoires and in animals that lack opportunities to associate with wild individuals in natural settings duringcritical learning periods. Reintroduction attempts withcaptive-bred individuals of species facing appreciablepredation threats in the wild often fail. It is noteworthythat a substantial fraction of the successful reintroduc-Conservation BiologyVolume 10, No. 2, April 1996tions considered by Beck et al. (1994) involved largespecies, such as the Arabian oryx (Oryx leucoryx) andplains bison (Bison bison), that were reintroduced in areas without predators.Logically, behavioral problems seem least likely in reintroductions of species that lack parental care. However,as a caveat to this assertion, releases of captive-raised juvenile sea turtles, to establish n e w breeding colonies orreestablish extirpated colonies, have been conductedfor decades without documented success (National Research Council 1990). In species with extended parentalcare the behavioral deficiencies of captive-bred stockhave sometimes been overcome by conspecific fostering(Snyder et al. 1987; Wiley et al. 1992). Unfortunately,opportunities for conspecific fostering are few or absentfor many endangered species. The alternative of crossfostering young to adults of other species can lead to behavioral problems in species recognition (Harris 1970;Lewis 1990) and is usually best avoided.It is still early for safe generalizations, but we suggestthat in the absence of fostering, the survival of releasedcaptive-reared individuals may often be best with species whose behavior is instinctive, species at the top offood chains or species introduced to predator-free orpredator-deficient environments. Results to date suggestthat for species whose behavioral repertoires are largelylearned, it may be difficult to reestablish wild populations if all individuals are drawn into captivity at anypoint and if releases are limited to captive-bred individuals (Snyder et al. 1994).DomesticationMany of the problems affecting captive preservation andreintroduction of endangered species are results of genetic and phenotypic changes that occur in captivity.Modern, conservation-oriented breeding programs attempt to ameliorate the genetic effects of inbreeding,drift, and adaptation to the captive environment throughthe deliberate and careful control of reproduction, pop-
Snyderet al.ulation size, and population d e m o g r a p h y (Foose & Ballou 1988; Allendorf 1993). This is a difficult task, however, given (1) the practical limitations of controllingreproduction; (2) the dynamic nature of evolutionaryforces in small populations; (3) the types of genetic variation to be maintained; and (4) the uncertain nature ofselection in the captive environment (Lande 1988; Simberloff 1988). We are particularly concerned that theusual strategy to slow d o w n genetic c h a n g e - - e q u a lbreeding of founder family lines--is impractical form a n y species that do not breed readily in captivity, especially those that are reluctant to accept forced pairingsand are resistant to manipulative techniques such as artificial insemination. Even in those critically endangeredspecies for w h i c h genetic m a n a g e m e n t is relatively feasible, it is not always implemented (Miller et al. in press).Captive environments differ greatly from wild environments, and evolutionary processes do not stop becausespecies are in cages (Spurway 1955; Kohane & Parsons1988; Allendorf 1993). Species b e c o m e progressivelym o r e adapted to captivity even w h e n comprehensivegenetic management is practiced. Given a n u m b e r ofgenerations, one can e x p e c t to see populations that differ from wild stocks in significant ways, with most, ifnot all, of these differences having deleterious effects onfitness in the wild (Mason et al. 1967; Fleming & Gross1993). Upon release such captive stocks may be incapable of producing viable wild populations and/or may exert deleterious genetic pressures on remnant wild populations (Fleming 1994; Philippart 1995).Selection for traits such as tameness can often bestrong in captivity regardless of w h e t h e r it is intentionalor not. And w h e n selection is strong, major changes canoccur quickly. For example, in only 20 generations Belyaev (1979) was able to produce almost fully domesticated forms of silver foxes (Vulpes fulva), exhibitingtypical dog-like characteristics such as two breeding periods p e r year, drooping ears, erect tails, and behavioraltraits such as tail-wagging and a tendency to lick handsand faces of humans (all characteristics that are absentfrom wild fox populations).Domestication can be especially rapid in certain fishesand invertebrates (Moyle 1969; Myers & Sabath 1980;Swain & Riddell 1990; Johnsson & Abrahams 1991), possibly due to the high potential fecundity of individualsand short generation times. Many insects, for example,quickly undergo major changes in behavior and morphology under captive conditions. Because of the magnitude of such changes, efforts to reestablish the largec o p p e r butterfly (Lycaena dispar) in the United Kingd o m have focused on use of endangered wild stocksfrom other countries rather than available captive-bredstocks Ohallin 1993).Behavioral traits that are learned or culturally transmitted are especially p r o n e to rapid loss in captivity, and genetic m a n a g e m e n t provides no relief from these losses.CaptiveBreedingofEndangeredSpecies341For m a n y species captive populations may b e c o m e resistant to reestablishment in the wild for behavioral reasons alone, and within very few, sometimes only sin#e,generations. For example, in species in which younglearn long, annual migrations by associating with experienced individuals, the first captive-produced generationmay not migrate properly in the absence of a wild population or even in the presence of a wild population if itdoes not include parental individuals (Akqakaya 1990).Behavioral changes induced by captivity may be themost significant problem w h e n and if w e try to unloadthe "ark" (Lyles & May 1987).H o w reversible is domestication? Feral populations ofdomestic cats (Felis catus) have b e c o m e establishedfrom captivity in many regions and with p h e n o t y p e s reverting to wild appearance relatively quickly. But, feralpopulations of m a n y domesticated forms are unknown,except in predator-free environments. For example,chickens (Gallus gaUus) and canaries (Serius canarius)have failed to establish wild populations anywhere except on predator-free islands (Derrickson & Snyder 1992).The inability of Wild Turkeys (Meleagris gallopavo) toform wild populations after only a few generations incaptivity has b e e n thoroughly examined (Leopold 1944;Knoder 1959). In this species domestication effects areapparent in certain features of the endocrine and nervous systems. Size of the adrenal glands rapidly declinesin captive flocks and seems closely tied to a loss of thephysiological and behavioral traits essential for survivalin the wild (Knoder 1959).We believe the implications of progressive geneticand phenotypic changes are considerably more seriousthan c o m m o n l y recognized. Proposals based on the"ark" paradigm are built on a misconception of constancy or near constancy of captive populations throughtime. For many species long-term captive breeding, despite all efforts to slow changes, may result in domesticated forms with low reestablishment potentials.Because of progressive domestication, w e should abandon any general expectations that w e can "preserve" endangered species in captivity without significant changeover the long term and l
(1) el establecimiento de poblaciones cautivas autosuficientes, (2) el escazo #xito en la reintroducci6n, (3) los altos costos, (4) la domesticaci6n, (5) la exclusi6n de otras t#cnicas de recuperaci6n, (6) los brotes de enfer-
Captive Insurance Section 500 James Robertson Parkway Nashville, Tennessee 37243 615-741-3805 Captive Manager Designation Form for Captive Insurance Companies 4.List all professional societies and associations this officer, principal, or key employee is a member of. 5. Describe the captive insurance
Registration of captive insurance companies. Under this option, a captive insurer insuring any Washington headquartered company would be required to register with the OIC and pay a premium tax. 3. Establish Washington as a captive insurance domicile. This option would involve authorizing the OIC to license and regulate captive insurance companies
Medicinal and aromatic crops 36 2.2.7. Fruits 37 2.2.8. Vegetables 39 2.2.9. Forecast data for the production of basic cereals and oilseeds from the 2020 harvest 44 2.3. Livestock Breeding Production Results 45 2.3.1. Cattle Breeding and Buffalo Breeding 50 2.3.2. Sheep Breeding and Goat Breeding 53 2.3.3. Pig Farming 56. 2.3.4. Horse Breeding 59
atypical, history of a population rescued by captive breeding. The original wild population may have declined for any number of reasons - habitat loss, competition with invasive species, disease, etc. Some or all of the few remaining wild-born individuals may be captured to establish the captive breeding program in the founding phase.
This study suggested that five major phyla, Firmicutes, Bacteroides, Actinobacteria, Proteobacteria and Sacchari-bacteria were observed to be different in captive and wild leopard. In addition, Fusobacteria was the major phylum in captive leopard. Firmicutes, Bacteroides, Actinobacteria and Proteobacteria were the main microbes of the captive
Non-captives. Table 2 also shows other differences between the default procedures by Captive and Non-captive lessors. Non-captives are writing off bad debts at a much higher percentage than Captives (62.5% vs. 3.8%). Non-captives are also instigating legal action at a rate of 15% of default contracts, while Captives report less than 2%.
Tennessee Captive Insurance Law Revised Tennessee Captive Insurance Act Part 1—General Provisions § 56–13–101. Short Title; Purpose § 56–13–102. Definitions § 56–13–103. License Limitations; Requirements to Do Business § 56–13–104. Original Names §
Crickets are prolific breeders which lend themselves to being bred for commercial production. With a little extra effort, you may wish to add extra containers and sell excess . This book covers two breeding methods, one for small scale production (Zega Substrate Breeding System) and another for large scale production (Batch Breeding System). The
