© Springer Science+Business Media New York 2014
William V. Holt, Janine L. Brown and Pierre Comizzoli (eds.)Reproductive Sciences in Animal ConservationAdvances in Experimental Medicine and Biology75310.1007/978-1-4939-0820-2_22. “Mayday Mayday Mayday”, the Millennium Ark Is Sinking!
(1)
Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, VA 22630, USA
Abstract
Despite exceptional advances in ensuring the health and well-being of animals in human care, zoos of the twenty-first century are ill-prepared and overwhelmed by the sheer number of species requiring conservation support. Furthermore, small population management paradigms have failed to achieve the demographic and genetic targets required to sustain most endangered species in human care. Predictions made in the 1980s regarding the potential of a “millennium ark”—aided by the use of assisted reproductive technologies (ARTs)—for saving species have proven to be wildly over-optimistic. ARTs continue to be touted as a panacea for saving endangered species and even for resurrecting extinct ones. And yet, while the first successful interspecies embryo transfer in a wildlife species occurred 30 years ago, there still is not a single example of embryo-based technologies being used to consistently manage a conservation-reliant species. The limited contribution of ARTs to species conservation to date principally stems from the lack of knowledge of species biology, as well as inadequate facilities, space, expertise, and funding needed for their successful application. ARTs could and should be an important tool in our conservation toolbox, but we cannot fall into the trap of believing that we can “assist” or clone our way out of the present biodiversity crisis. Reproductive technologists overstate the potential of ARTs for saving endangered species, zoos overestimate their ability to sustain genetically and demographically viable captive populations with existing resources, and conservationists underestimate their need for zoos in the face of failing efforts to sustain species in nature. Unless all parties concerned—reproductive technologists, zoo biologists and conservationists—adopt parallel efforts to sustain wild populations and places, zoos risk becoming living museums exhibiting relic species that no longer exist in nature.
Keywords
ZoosAssisted reproductive technologiesEndangered speciesMillennium arkConservation1 Introduction
Zoos and aquariums have evolved over the past century from primitive menageries to modern zoological parks, with naturalistic exhibits and habitats designed to ensure the health and well-being of animals in human care (Wemmer 1995a; Hoage and Deiss 1996). London Zoo, founded in 1826, was the first zoo established to support scientific study (Wemmer and Thompson 1995), but it was not until the 1960s that stand-alone zoo-based research departments were established (e.g., London Zoo, Smithsonian’s National Zoo, San Diego Zoo) with expanded research portfolios in disciplines we now know as “Zoo Biology”—reproductive biology, genetics, behavior and animal health and husbandry sciences (Benirschke 1984). Today, roughly 20 % of accredited European and American zoos have research departments, but a much smaller number employ full-time Ph.D.-level scientists and conservationists (Reid et al. 2008).
There is no question that modern zoos, working with diverse partners and stakeholders, have become champions for conservation. Zoos have pioneered the concepts of conservation breeding linked to species reintroduction and restoration of species like the golden-lion tamarin (Kleiman et al. 1986), California condor (Toone and Wallace 1994; Walters et al. 2010), black-footed ferret (Lockhart et al. 2005), and Wyoming toad (Dreitz 2006), among others. And the global zoo community currently invests more than $350 million per year in field conservation programs (WAZA 2005; Penning et al. 2009; Gusset and Dick 2010). But the challenge facing zoos in conserving species is daunting. The IUCN estimates that 25 % of mammals, 12 % of birds, 20 % of reptiles, 30 % of amphibians, 20 % of fishes, and 30 % and 68 % of invertebrate and plant species evaluated to date, respectively, are threatened with extinction (IUCN 2012). Faced with this accelerating global loss of species (Collen et al. 2008), zoos are forced to perform triage in determining which species to save, and which will be left to fend for themselves in nature (Conway 2003; Nijhuis 2012).
Despite exceptional advances, zoos of the twenty-first century have yet to achieve their potential as “conservation centers” or “environmental resource centers” focused on holistic conservation that emphasizes both species and the habitats they require for survival (Rabb 1994; Conway 1996, 2003; IUDZG/CBSG 1993). Furthermore, well-intentioned cooperative population management efforts designed to slow the inevitable loss of genetic diversity that occurs in small, closed populations, have largely failed due to insufficient numbers of founders, inadequate space, poor reproductive management, and inadequate knowledge of species biology (Lacy 2013). Numerous analyses have revealed that “most zoo populations are not being managed at adequate population sizes, reproductive rates, genetic diversity levels, and projected long-term viability that would allow them to contribute positively to species conservation.” (CBSG 2011).
2 The Millennium Ark
In a landmark paper, Soulé et al. (1986) predicted that if environmental destruction rates continued unabated, virtually all primates, large carnivores, antelopes, rhinoceros, wild equids, and hundreds of species of birds, reptiles and amphibians would effectively disappear from the wild within 100 years. As a response to this impending biodiversity apocalypse, a group of scientists proposed the creation of “millennium arks” to buy time for the more than 2,000 wildlife species that would likely survive only under human care. The concept called for establishing zoo-maintained populations consisting of at least 20 founders per target species with a goal of sustaining 90 % of the genetic variation of the original founder population for a period of at least 200 years. While the authors recognized the limitations of the ark model, their great faith in unforeseen breakthroughs clearly was evident: “The captive breeding of so many species will saturate the available space and resources, but, hopefully, advances in cryogenics and similar technologies will obviate the need to maintain all of these at one time as living organisms.” These authors went on to predict that, “…based on the recent successes in bovids, equids, and primates, we consider it likely that traditional captive breeding programs for many species in these groups will be obsolete in a few decades (given reliable refrigeration).” It is especially noteworthy that none of the authors of this paper were reproductive biologists.
Now, only 30 years later, some have concluded that the millennium ark is sinking (Lees and Wilcken 2009). Even relaxing the goal of sustaining 90 % genetic variation from 200 to 100 years does not alter the grim facts that: (1) less than 50 % of all of the worlds’ zoo-managed animal populations are breeding to replacement levels; and (2) only 55 % are sustaining more than 90 % gene diversity. Presently, about 75 % of zoo-based programs for birds and 66 % of those for mammals are not achieving specified demographic and genetic targets (de Man 2011). Overall, 30 % of all zoo-maintained populations are declining and 30 % have fewer than 20 founders (Long 2011). Simply stated, zoos are overwhelmed and ill-equipped to manage more than 500 high-priority species programs due to lack of space, specialized facilities, technical expertise, and funding.
We possess an appalling lack of fundamental scientific knowledge of species biology. In a review of the roughly 250 wildlife species referenced in the reproductive sciences literature, 75 % of these species were represented by three or fewer references (Wildt et al. 2003). Additionally, only three species classified by IUCN as endangered (African elephants, Asian elephants, and cheetah) were considered relatively “well-studied”, having more than ten peer-reviewed publications (Wildt et al. 2003). The routine application of research tools like noninvasive endocrine and genetic methods has increased the number of species studied over the past decade, but efforts are heavily skewed towards mammals and birds (Monfort 2003; Schwartz and Monfort 2008), and our knowledge of the reproductive biology of the vast majority of species in the animal kingdom remains rudimentary or non-existent.
3 The Application of ARTs for Conserving Endangered Species
Early breakthroughs in the application of ARTs to endangered species were stunning, including successful interspecies embryo transfers from eland (Dresser et al. 1982) and gaur (Stover and Evans 1984) to domestic cow, and bongo to eland (Dresser et al. 1985)—successes that soon raised great expectations that ARTs would revolutionize the management of endangered species. During these heady times, the concept of “Frozen Zoos”—biorepositories of frozen tissues—was introduced (Benirschke 1984; Clarke 2009), long before the benefits of such collections were fully understood, and before the name “Genome Resource Bank (GRB)” entered our lexicon (Wildt et al. 1997).
ARTs, including artificial insemination (AI), the use of sex-sorted sperm, embryo collection and transfer (ET), in vitro oocyte maturation (IVM) and fertilization (IVF), and cloning have been widely promoted as having tremendous potential for enhancing breeding management and the genetic and demographic sustainability of small populations of rare species (Pukazhenthi and Wildt 2004; Holt and Lloyd 2009). A wide range of ancillary methods and tools have been developed and applied, including hormonal and behavioral assessments for developing fundamental knowledge in diverse species (e.g., ovulatory mechanisms, seasonality, pregnancy, infertility), manipulating (e.g., superovulation, estrous synchronization), augmenting or overcoming blocks to reproduction (e.g., AI, ET, IVF), suppressing fertility (e.g., contraception, aggression control), and establishing biorepositories for capturing extant genomic diversity (e.g., cryoprotectant evaluations and cryopreservation methods).
Despite an early emphasis on embryo technologies in the 1980s, and recent interest in cloning and other genomic approaches for “rescuing” or even resurrecting extinct species (Zimmer 2013), major technical and ecological challenges remain for their application in conservation. This is reflected in the fact that 30 years after the first successful interspecies embryo transfer in a wildlife species, there is not a single example of embryo-based technologies having been used to consistently produce or manage a conservation-reliant species. The simple explanation for this is that reproductive mechanisms are incredibly diverse, and what works in one species likely will not be directly applicable to another species—even among closely related species in the same taxonomic group (Wildt et al. 2009). The problem has been summed up succinctly as follows: “Cow AI technology does not work in a cheetah or a gorilla. But, why should it? Each species is evolutionarily distinct, having developed highly specialized reproductive adaptations. It is the job of reproductive biologists to understand the diverse ways that animals reproduce, because reproduction is the essence of species survival.” (Wildt and Wemmer 1999).
The time has come to stop and take stock in why we have generally underperformed in applying even the most basic ARTs such as AI for routinely producing offspring and managing the genetics and demography of wildlife species. We are in an age when genomes can be wholly reconstructed, and biodiversity genomics will soon be yet another tool to add to the ART toolbox. But what good are new or better tools to a mechanic when he or she has absolutely no idea of how the engine was designed to operate in the first place? The trap for the reproductive technologist—especially those with zero experience or knowledge of wildlife biology—is ignorance in believing that any ART can be successfully applied to any species. While history demonstrates that this is a specious notion, the latest technological applications continue to attract attention disproportionate to their potential for sustainably managing reproduction in endangered species, much less resurrecting extinct species (The Long Now Foundation 2013). Whether it is the successful application of AI or the use of cloning to sustain an endangered living species or resurrect an extinct one, success is dependent upon knowledge of a species’ biology, ecology, social structure, reproductive cycle, seasonality, implantation, placentation, gestation, parturition, maternal behavior, neonatal care, nutrition, disease susceptibilities, and causes of endangerment. Failure to appreciate the need for this fundamental information is an epic miscalculation that dooms the application of ARTs to certain failure, at least in a practical sense.
4 Case Studies
While this chapter is not intended to provide a comprehensive overview of ART applications in endangered species, a few examples follow that demonstrate both the promise of these approaches, as well as the very real challenges to their practical application.
4.1 ARTs in Endangered Fish
One of the oldest applications of ARTs was invented in the mid-nineteenth century when Joseph Remy and Antoine Géhin harvested eggs and milt from trout and then artificially propagated them by the thousands in vitro (Halverson 2010). This is essentially the method that remains in use today for cultivating diverse species such as carp, salmon, trout, catfish, and tilapia, among others. For example, more than five billion hatchery-reared juvenile salmonids are released annually into the Pacific Ocean from North American hatcheries, alone (Flagg and Nash 1999). In addition, hormone-induced spawning at commercial levels has been practiced for decades (Mylonas 2010), and while fish embryo cryopreservation remains challenging (Hagedorn et al. 2002), sperm has been cryopreserved in more than 200 freshwater and 40 marine fish species worldwide, with routine offspring production using frozen-thawed sperm (Chew and Zulkafli 2012). As the numbers of threatened or endangered fish species increases, “conservation aquaculture,” including the use of ARTs, has emerged as a strategy for conserving the genotypes, phenotypes and behaviors of locally-adapted fish populations in support of comprehensive recovery strategies (Anders 1998). However, new research suggests that this approach is not without risks, as the impacts of large-scale mixing of hatchery-produced fish with wild stocks have been shown to reduce overall fitness in species like salmon (Reisenbichler and Rubin 1999) and trout (Araki et al. 2007). Nonetheless, conservation hatcheries, augmented by ARTs, are likely to become increasingly important for recovering critically endangered fish populations—especially those of commercial value—to avoid reductions in population size and the loss of genetic diversity that could increase the risk of extinction (Drauch Schreier et al. 2012).
Zoos and aquariums are increasingly being called upon to help conserve endangered fish species using both ex situ and in situ approaches (Reid et al. 2013). After more than a century of management practice, it now appears that simply producing and releasing large numbers of hatchery-reared fish is not sufficient to sustain and/or recover fish populations. Conservation aquaculture is in its infancy, and its clear that more research is required to understand the impacts of diverse factors such as genetics (inbreeding, outbreeding), broodstock sourcing, maturation and development, growth rate modulation, environmental enrichment, anti-predator conditioning, as well as an improved understanding of anthropogenic impacts on aquatic environments, such as habitat loss/fragmentation, pollution, and climate change (Flagg and Nash 1999, Reid et al. 2013). To maximize their conservation impact, zoos and aquariums will need to make new capital investments in space, infrastructure and scientific expertise, as well as to leverage extant resources to create new and novel partnerships with governments, universities, fish hatcheries, aquaculturists and other technical experts, as required to achieve success.
4.2 ARTs in Endangered Birds
Intravaginal AI has been used in the domestic poultry industry for more than a half-century (Quinn and Burrows 1936), and today nearly 300 million turkeys are produced annually in the United States, alone (USDA Statistical Service 2012). AI has now been used to produce chicks in numerous species of raptors, cranes, waterfowl, psittacines, and passerines (Gee 1995), and this technology has played a key role in successful species recovery programs for the Peregrine falcon (Hoffman 1998), houbara bustard (Saint Jalme et al. 1994), and whooping crane (Ellis et al. 1996). The success of these excellent programs was underpinned by systematic research in diverse disciplines, including behavior, genetics, animal husbandry, veterinary medicine, and chick rearing (Ellis et al. 1996). While AI in wild or rare birds can be incredibly challenging, this approach has tremendous potential for augmenting reproduction in endangered birds for maintaining gene diversity in small populations, and especially when natural breeding is not possible due to behavioral incompatibility, reproductive asynchrony, physiological stress, poor libido, physical abnormalities, among other causes. For all bird species, successful application of AI requires pre-emptive research in semen collection and processing, access to sufficient numbers of birds for basic and applied research, baseline knowledge of species’ biology, and appropriate facilities and expertise (Blanco et al. 2009).
An incredibly successful example of the application of ARTs to the conservation of an endangered bird species can be found with houbara bustards. Since the mid-1980s, scientists in Saudi Arabia (Saint Jalme et al. 1994; Seddon et al. 1995) and the United Arab Emirates (International Fund for Houbara Conservation 2012) have conducted extensive research on houbara bustards in the areas of behavior, genetics, reproductive biology, veterinary medicine, as well as the ecology, status, distribution and wild population trends. Since 1996, the Emirates-led program has released a total of more than 111,000 houbara in North Africa, with 20,310 released in 2013, alone; the long-term goal is to release 50,000 birds per year (International Fund for Houbara Conservation 2012). Success of this magnitude has required massive long-term financial investments in facilities infrastructure, scientific and husbandry expertise and logistical support motivated, in large part, by the desire to restore sustainable wild houbara bustard populations to support a strongly ingrained cultural interest in falconry. While conservation breeding programs of this magnitude are clearly out of reach of the zoological community, there are many valuable lessons to be learned from such programs that could be scaled appropriately to conserve zoo-maintained endangered bird species.
4.3 ARTs in Endangered Ungulates
It is not surprising that initial successes were achieved in the Bovidae, as many of the ARTs were developed and applied in domestic cattle in efforts to refine their reproductive management for economic benefit. The simplest of these techniques, AI, has now been successfully applied to produce live offspring in 14 species of non-domestic bovids and seven cervid species (Morrow et al. 2009). Yet, despite tremendous strides in developing this technology, AI is used to routinely manage the genetics of only a single zoo-maintained endangered ungulate, the Eld’s deer (Rucervus eldi), and only in a very small number of individuals (Monfort et al. 1993).
The case studies of two endangered species—Eld’s deer (critically endangered with fewer than 1,500 animals in the wild) and the scimitar-horned oryx (Oryx dammah, extinct in the wild)—illustrate some of the challenges in applying ARTs to the genetic management of small populations held in zoos. Both species were the subject of comprehensive research programs that successfully characterized ovarian cycles, developed estrous synchronization methods, semen collection and sperm cryopreservation protocols, and were found useful for routine offspring production (~50 % conception rate) following a single insemination with frozen-thawed sperm (Monfort et al. 1993; Morrow et al. 2000). Despite the clear potential for these methods for enhancing the genetics and demographics of ex situ populations, few zoos possessed the facilities or expertise to permit animals to be safely handled twice to permit insertion and removal of intra-vaginal progesterone-releasing devices during the prescribed 12- to 14-day estrous synchronization interval; followed by anesthesia and laparoscopic AI. In the early 1990s the author contacted a veterinarian at another zoo, which held the second largest Eld’s deer population (of six AZA zoos managing this species), to inquire about the possibility of conducting AI to manage the genetics of their inbred Eld’s deer population. The veterinarian conveyed that the risk of injury and/or mortality associated with simply darting (anesthetizing) the deer was too great, making this approach impractical. Thus, despite years of systematic research and proven success, ARTs could not be applied due to the limitations imposed by existing facilities and management schemes typical of most zoos. A decade later, AI is still only used to manage Eld’s deer reproduction at the Smithsonian’s National Zoological Park, which maintains a GRB for Eld’s deer sperm, and has facilities that permit safe handling and manipulation of this species.
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