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Conservation and Animal Behavior
Conservation and Animal Behavior R. Swaisgood, San Diego Zoo’s Institute for Conservation Research, Escondido, CA, USA ã 2010 Elsevier Ltd. All rights reserved.
Introduction Conservation is the end result of a human value system that seeks to maintain the diversity of life forms on earth and ensure the ecological integrity of our natural heritage. People may be motivated to conserve nature by utilitarian values, such as recognition of the important services that a functioning ecosystem provides to humanity, or by a deep and abiding philosophy that other forms of life have intrinsic value as well. The biophilia hypothesis – championed by the founding father of biodiversity and sociobiology, E.O. Wilson – posits that humans are predisposed to an emotional attachment to nature that motivates them toward environmental stewardship. It may be argued that animal behaviorists, who spend long hours observing animals, have a more-than-average dose of biophilia, making their late arrival on the conservation stage surprising. Although the modern academic discipline of conservation biology has its roots in wildlife management that goes back generations, it was not founded until the 1980s. Conservation behavior – as the application of behavioral research to conservation is sometimes called – traces its formal, academic beginnings to the waning moments of the last millennium. As an emerging discipline, conservation behavior is still seeking to define itself and find its niche in both conservation biology and behavioral science. Conservation behaviorists, a small group of individuals by any definition, are attempting to reinvent the way behavioral research is applied to conservation efforts. At the end of just over a decade of concerted effort, much of the heady promise of this nascent field has yet to come to fruition. A series of influential books and papers have, in recent years, addressed the many implications that behavior – particularly behavioral ecology – has for conservation. That the behavior of animals influences conservation is a truism, but the challenge for behavioral scientists has been to move from the implication phase of conservation behavior to more active applications to solve the real-world conservation problems. The discipline has experienced growing pains, but has real potential, some of which is just beginning to be realized. Several subdisciplines within animal behavior have contributed to the emergence of conservation behavior, but to date most proponents have been rooted in behavioral ecology. Many of the topics in behavioral ecological research appear promising for conservation application – including mating strategies, mate choice, dispersal and habitat selection, behavioral responses to habitat fragmentation
and anthropogenic disturbance, and the many behavioral facets of reintroduction programs. The strong theoretical framework afforded by behavioral ecology provides the basis for a hypothetico-deductive approach to conservation science. We are learning that a more integrated approach across the four levels of explanation in animal behavior – causation, development, adaptive utility, and evolutionary history – and across larger ecological scales – population, community, ecosystem, landscape – holds the most promise for the successful application of behavioral research to conservation.
Taking Stock of the Problem: What Are Some of the Challenges Facing Animal Conservation? Today’s natural world faces an onslaught of anthropogenic processes that threaten the functional integrity of ecosystems, leading to escalating rates of species loss seldom seen during the history of the planet. Habitat degradation and outright destruction are the single largest culprits, and the resulting fragmentation of habitat supporting wildlife has multiplicative rather than additive effects on loss of biodiversity. Widespread urbanization and intensive agricultural practices eliminate most of these lost species, whereas other human activities degrade much of the remaining natural areas. Chemical pollutants may affect survival and reproduction, and thus population recruitment rates. Noise pollution may likewise disturb mating and parenting behavior or lead to chronic stress, with its attendant consequences for immunocompetence, fertility, and allocation of energetic resources away from other demands of survival. A single aircraft overflight has been known to cause the immediate loss of most chicks in a white pelican nesting colony. Sadly, even our love for nature in the form of ecotourism may be harming animals. Ever-increasing numbers of nature enthusiasts converging on whales and dolphins may tip the energetic balance, causing chronic sublethal effects. A simple walk on the beach disturbs shorebirds, diverting them away from foraging, mating, or parenting behavior. Multiplied by thousands of beachgoers, the cumulative effects on survival and reproduction can mean population decline. Pets, acting as predators along edges of natural communities, can have reverberating effects on community dynamics deeper in the reserve. Studies have shown that even on-leash dogs can reduce diversity along a surprisingly wide trail margin.
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Humans also often aid transport and colonization of invasive nonnative species. Those species with the right suite of behavioral and life-history characteristics sometimes get a foothold in their new environment and – without the ecological controls in their place of origin – undergo rapid population expansion. Over-run with exotics, the results for native competitors or prey species can be devastating. Take the case of the mountain yellow-legged frog (Rana muscosa) in California (Figure 1). The introduction of brown trout and the larger and more aggressive bullfrog have contributed to the decline of this endangered species. This high-mountain frog has little coevolutionary history with fish predators and its tadpoles are vulnerable to predation by nonnative trout. Populations have recovered rapidly when trout have been experimentally removed. Overlaid on top of these long-known threats to animal populations is the unpredictable impact of anthropogenic climate change, which will exacerbate other impacts. Climate change may precipitate range shifts in many species, but fragmented habitat may prevent migration, calling upon even greater human intervention (such as widespread translocations of animals to help track shifting habitats). Wildlife management is likely to become increasingly intensive in the future, as protected areas become more zoo-like, managed parks. Smaller, isolated populations will call upon the skills and resources of conservation biologists more than ever. Conservation behaviorists will undoubtedly play a larger role. Just monitoring animal populations so that we know what we have will require considerable resources, though greatly aided by emerging technologies. Because behavior affects detectability, behaviorists will need to play an increasing role in survey and monitoring efforts. In managed areas, we will need to obtain a better understanding
Figure 1 One of the estimated 122 surviving adult mountain yellow-legged frogs in Southern California, decimated by invasive species and chytrid fungus. Photo by Ron Swaisgood.
of carrying capacity – the population size that can be sustained in a given patch of habitat. The ecological factor(s) limiting an animal’s carrying capacity may be food, water, shelter, refuges from predators, or breeding sites. Modifying the factors limiting the carrying capacity can be one way to alter a population’s size, for better or worse. Some species have been rescued from the wild and placed in conservation breeding programs in zoos and other facilities. These small populations need to be managed for genetic diversity to avoid the deleterious effects of inbreeding and to preserve as much of the species evolutionary potential as possible. Managers combat both random genetic drift and, more importantly, artificial selection that causes domestication-like effects on captive or even wild populations living under increasingly artificial conditions. The long-term objective of conservation breeding and other small population management programs is to sustain a secure genetic reservoir until conditions in the wild can be improved. When suitable habitat is found or created, populations can be reestablished through reintroduction and translocation programs. Reintroduction of key species can serve to restore ecological integrity of natural areas, especially if the reintroduced species are ecosystem engineers. For example, fossorial rodents such as ground squirrels create burrows used by a variety of wildlife species. Experimental removal of kangaroo rats precipitates invasion of nonnative grasses (Figure 2). Removal of top predators, such as mountain lions, can lead to increased numbers of smaller predators (mesopredator release) that decimate prey species, such as songbirds. Ecological restoration through reintroduction is one of the most promising areas for behavioral research contributions. Animal relocations – whether from captive-bred or wild-caught animals – require intensive behavioral research and management to prepare animals for release
Figure 2 The endangered Stephens’ kangaroo rat of Southern California. A translocation program led by the San Diego Zoo is trying to re-establish this keystone species in suitable habitat. Photo by Ron Swaisgood.
Conservation and Animal Behavior
to a novel environment and, in many cases, monitor and manage their postrelease behavior. Most reintroductions to date have taken a fairly simplistic approach to postrelease management, relying primarily on soft-release practices such as acclimation pens and short-term provision of food and water resources. Behaviorists can redefine the meaning of ‘soft’ in these programs, replacing these practices with more ecologically relevant ones guided by a strong theoretical framework. That said, the application of conservation behavior is not limited to triage and is as diverse as the imagination and creativity of its proponents.
Tackling the Problem: How Can Behavioral Research Contribute to Conservation? Animals on the Move: Space Use, Dispersal, and Habitat Settlement Animal movement patterns figure critically in many aspects of conservation management. Movement patterns determine size and shape requirements for reserves and the degree of connectivity needed for adequate migration between protected areas to sustain genetically viable metapopulations across the landscape. Animals with large home ranges more often range outside the boundaries of protected areas, where they are no longer protected. In fact, wild dog home ranges are so large relative to most reserves that only those groups living well within the core of the reserve are not exposed to the risks outside reserve boundaries. The longest animal movements are seen in dispersal – generally the once-in-a-lifetime movement away from the natal home to settle in new habitat. Reserves need to be designed to accommodate these dispersal distances, which can be many times larger than the typical home range for the species. Dispersal is important for discovering and occupying new habitat and for inbreeding avoidance. Conservation planners need better data on spatial movements, including how far an animal can move, through what types of habitat it moves, and how this is influenced by topography and human-altered landscapes. The last decade has witnessed a revolution in spatial ecology, brought on by emerging technologies such as GPS satellite telemetry and remote infrared-triggered camera and video traps. These technologies have proved especially useful in linking fine-scale movements of individual animals (of interest to behavioral ecologists) with larger landscape-level patterns (of interest to population and landscape ecologists). In the fragmented habitats that many wildlife species occupy, animals must cross gaps to maintain connectivity among animal populations. Forest specialists, in particular, may be reluctant to cross a gap caused by clear cutting or a road. It is rarely physical ability that limits gap
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crossing, but instead the animal’s perception of risk from predators or stress-mediated avoidance of an unfamiliar landscape. Common sense might inform whether an animal can pass through a habitat, but experimentation is required to determine under which motivational circumstances they will actually do so. In this experimental approach, playbacks of conspecific vocalizations have been broadcast to lure individuals into or across particular landscape features, or animals have been experimentally relocated across gaps that vary in size and quality. These bioassays can be used to determine the permeability of different habitat types over varying spatial and temporal scales. Behavioral constraints on dispersal may compromise conservation efforts. A common misconception is that if suitable habitat is present, then dispersers will find and occupy it, but such build-it-and-they-will-come approaches do not always work. Seminal research by Judy Stamps in the 1980s demonstrated that dispersers often prefer to settle near conspecifics, even among less social, territorial species. Such conspecific attraction in habitat settlement may serve to guide dispersers to suitable habitat without long, costly direct sampling of habitat quality. Research has further shown that dispersal is often the most risk-prone life history stage, exposing animals to the risks of predation and starvation in unfamiliar habitat. These risks select for more conservative dispersal strategies and the use of cues correlated with habitat suitability. Using this theoretical framework, conservation behaviorists have used bird song playbacks to recruit black-capped vireos to new areas, model decoys to attract terns to new colonies, white wash (mimicking droppings) to attract vultures, and rhino dung to encourage settlement in translocated black rhinos. This tool is proving particularly powerful in reintroduction and translocation programs, because, in fact, these conservation actions force a dispersal-like event upon animals whether or not they are prepared for dispersal. It is no surprise that most mortalities occur soon after release. Behavioral management of dispersal during this postrelease period could prove critical in determining the success or failure of the program. Consider the example of caribou translocated from open prairies to mountain forests, which suffer higher mortality than those translocated from more similar habitat types. The difference lies in their behavioral response to the environment. In winter, mountain caribou move to the north slopes to forage upon lichens that grow prevalently on the cooler, moister slopes. In winter, prairie caribou forage on open tundra, digging under the snow to expose hidden lichens, and, when translocated, maladaptively move to the more open south slopes in an attempt to use their foraging strategy in the new locale. In another example, red squirrels translocated from Corsican pine forests traversed through Scotch pine in search
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of Corsican pine to settle. Conversely, squirrels captured in Scotch pine forests reject Corsican pine in favor of Scotch pine habitats. Such behavior can be explained by natal habitat preference induction (NHPI). More formally, NHPI occurs when dispersers prefer new habitats that contain stimuli comparable to those in their natal habitat. NHPI may help explain why relocated animals are so often prone to travel so long distances, at their peril – they are searching for someplace like home. Understanding this phenomenon enables the implementation of several new approaches to reintroduction programs, including efforts to match habitat type at capture and release site or to manipulate conspicuous cues in the postrelease habitat to match those from the animal’s place of origin. Foraging Ecology Research on foraging ecology can provide key insights into animal–environment interactions important for conservation. NHPI provides but one example. Long-term studies across seasons may identify key limiting resources that determine the size of the population that can be sustained in an area (carrying capacity); such studies can be crucial for proactive conservation management to ensure those resources remain available, or can suggest ways to enhance these resources to support populations at risk. Conservation behaviorists may also identify key roles that animals under study provide for the ecosystem, such as seed dispersal, population control for smaller predators (by keystone predators), or interspecific competition for resources. Security Areas Security is another critical need for animals. Nesting and denning sites can be limiting resources. For example, endangered red-cockaded woodpeckers must excavate nests in live pine trees, a task that can take more than a year. This limiting resource shapes many aspects of the species’ behavioral ecology, including the phenomenon of cooperative breeding. Because dispersal to new areas is limited by the availability of nesting cavities, young woodpeckers remain with their parents and help raise subsequent offspring, banking on future access to nest sites nearby. Understanding this system led to a novel conservation management action. Because of the high number of reproductively mature birds without access to nesting opportunities, construction of artificial cavities led to a rapid increase in the breeding population and was key to rapid recovery following loss of many cavities in a hurricane. New research is now suggesting that giant pandas may also be limited by access to quality den sites. After centuries of logging, few trees of sufficient girth to contain a panda-sized
cavity remain, and panda females may have few quality dens to select from, limiting their ability to provide proper care for cubs. Too Much of a Good Thing: Mating Strategies, Reproductive Skew, and Effective Population Size Understanding mating patterns has several important consequences for conservation. Of those, reproductive skew may be most important. If some males have mating advantages over other males – either by direct male–male competition or female mate preferences – they will sire disproportionately more offspring. In small populations, this can further exacerbate loss of genetic diversity, and much larger populations will be required to maintain sustainable populations over the long term. A key concept is that of effective population size (Ne), which is the number of breeding animals in an ideal, randomly mating, population that would lose genetic diversity at the same rate as the actual population. The greater the reproductive skew, the smaller the Ne and the greater the concern for the long-term viability of the population. With the loss of genetic variability, species lose some of their evolutionary potential, their ability to adapt to changing environments, and may suffer consequences of inbreeding depression. To maintain long-term population viability, there is a point where small populations require management to ensure that reproduction is distributed more equitably. Experimental manipulation of behavioral mechanisms related to mate choice is one course of action being pursued by conservation behaviorists. For example, Fisher and colleagues were able to control female preferences of threatened pygmy lorises by manipulating the level of odor familiarity with potential mates (Figure 4). These researchers reasoned that females should prefer more familiar-smelling males because males capable of monopolizing an area with their odors are more competitive than males that fail to do so. This demonstrates the importance of understanding the theoretical framework provided by behavioral ecology. If male–male competition is responsible for reproductive skew, then temporary removal of the most successful male can increase Ne, as has been done with threatened Cuban rock iguanas. Relationships Matter: The Role of Social Behavior in Conservation Several social processes have important ramifications for conservation. The Allee effect – the proposal that reproduction is maximized when animals are optimally aggregated – suggests that human-mediated alterations to animal population density may influence population growth and stability. Numerous studies have shown the benefits of sociality, even for relatively solitary species,
Conservation and Animal Behavior
suggesting one consequence of a reduction in animal densities is the breakdown of social processes that confer fitness advantages – ranging from predator avoidance to opportunities for mate selection. Indeed, these social benefits may drive the phenomenon of conspecific attraction, discussed earlier. The (mostly unproven) role for conservation behaviorists is to determine optimal social density. An example from captive breeding programs is instructive: mongoose lemurs housed in pairs near other conspecifics had 500% higher rates of reproduction than isolated pairs. Courtship behavior in flamingos is greatly enhanced by allowing them to view themselves in mirrors, effectively increasing the perceived animal density. For highly social animals, we need to be mindful of the significant time and energy that animals invest in building and maintaining social relationships, and the advantages that these relationships confer. In translocation programs, for example, animals are often captured and relocated to another area, without due consideration given to social relationships. Debra Shier found that black-tailed prairie dogs had 500% higher survival rates if they were released in familiar groups than if they were released randomly with regard capture location. We must also keep in mind that solitary animals are not asocial and that even territorial species invest in relationships with neighboring animals. In reintroduction programs, animals experience many challenges related to being placed in novel environments, and the added costs of renegotiating stable relationships may mean the difference between death and survival. This may explain why the normally solitary black rhinoceros experiences a surge in conspecific aggression following translocation. A team of researchers led by Wayne Linklater addressed this problem and have found, for example, that this aggression can be mitigated by releasing rhinos in larger reserves at lower social densities, which helps them to avoid direct encounters and gradually build social familiarity (Figure 3).
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Figure 3 Dr. Wayne Linklater spreads black rhinoceros dung in research designed to guide postrelease dispersal behavior in a large-scale translocation program in southern Africa. Photo by Ron Swaisgood.
Scared to Extinction: Stress, Disturbance, and Antipredator Behavior Human activities can disturb wild animals, altering their behavior in ways detrimental to their survival and reproduction. Behavioral researchers studying the stress response system are helping to understand human impacts and suggest new ways to mitigate against these impacts. Stress is the animal’s behavioral and physiological response to biological challenge, and, when chronic, can negatively impact health and reproduction. There are numerous measures of stress, many of them problematic if observed in isolation, but immunoassay of concentrations of glucocorticoid hormones is most common. Researchers have documented a number of anthropogenic activities that activate the stress response system: noisy snowmobiles impact wolves and elk, radiocollars may affect wild dogs, noisy
Figure 4 Researchers manipulated mate preferences for a conservation breeding program for threatened pygmy lorises. Photo by Heidi Fisher.
crowds disturb captive giant pandas, and approaching hikers affect bighorn sheep, even if they do not run away. Human activities may also affect behavioral decisions that have energetic consequences. For example, sperm whales spend less time surfacing to replenish oxygen supplies when helicopters fly overhead and foraging grizzly bears consume fewer calories when hikers are nearby.
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More recently, researchers have taken a closer look at human disturbance, using a more predictive approach from the theoretical framework provided by economic models of antipredator behavior. If animals perceive humans and their activities as potential predators, then much of their response can be predicted from our understanding of antipredator behavior. A growing literature indicates that human disturbance, like predation threat, alters animals’ time budgets, with energetic and lostopportunity costs. These indirect sublethal costs can have cumulative effects worse than actual predation. Scott Creel and colleagues found that temporal and spatial proximity to wolves dramatically affected foraging patterns, causing elk to avoid the best forage in open areas in favor of suboptimal forage near cover. The consequences of this decision-making process were substantial, leading to poor body condition, lower reproduction rates, and high calf mortality. The economic principles of antipredator behavior have proved effective at predicting many of the dynamics of animal responses to human disturbance, such as the effects of tourist group size, speed of approach, and distance to cover. Disturbance can also affect mate choice and parental investment in offspring in predictable ways. But Wait, There’s More: Other Applications of Behavioral Research to Conservation Creative conservation behaviorists are exploring many other avenues to apply their craft in the service of conservation efforts. Several researchers have assisted in the many behavioral facets of reintroduction programs, most prominently, in the application of ontogenetic processes to train prey organisms in the antipredator behavior of their species prior to release. Debra Shier and Don Owings, for example, have shown that captive-born black-tailed prairie dogs can be trained to recognize and deal with predators more effectively than their untrained counterparts. When these investigators used wild-caught prairie dogs to demonstrate appropriate antipredator behavior to captive-reared conspecifics, these prairie dogs were more likely to survive when released to the wild than individuals that were trained with predators without such a conspecific demonstrator. Behavioral plasticity is another key concept in conservation behavior. Understanding and predicting behavioral response to a changing world will inform many conservation decisions. For example, behavioral elasticity preadapts invasive species to colonize novel habitats, and lack of elasticity may spell the doom of native species that cannot adapt to the invader. Natural populations comprise a number of different behavioral types – suites of correlated behavioral traits, analogous to temperament or coping styles. Aggressive animals may be predictably more active across many situations than less aggressive animals. While this
aggressiveness may confer advantages in intraspecific competition, such an advantage may be offset by increased susceptibility to predation. In some cases, even immune function is influenced by behavioral type. The sum total of behavioral types for a population is called a ‘behavioral syndrome.’ A reduction in the range of types within a syndrome can cause conservation problems if the members comprising a population can no longer adapt and respond to temporally and spatially variable environmental factors. Conservation breeding programs, in particular, may not produce the full mix of behavioral types for release, especially if the captive environment does not contain the environmental features needed for the development of some behavioral types. Conservation behaviorists need to understand these suites of correlated traits so that they can ensure that release groups, of captive or wild origin, contain those individuals that perform different important roles, such as warning against predators or locating and exploiting novel foods. To do this, we must guard against differential reproduction among different types and provide enriched environments to shape ontogenetic processes for a plurality of personalities. There is also evidence that some populations contain dispersal phenotypes, individuals that are behaviorally and physiologically prepared for the risks and rigors of dispersal – clearly important for any relocation program. Thus, to maximize population persistence, it takes all types. To move forward, conservation behavior needs to continue to become more integrated across disciplines and levels of analysis. Behavioral ecologists bring much to the table, such as the strong theoretical framework that allows hypotheses and predictions to be formulated. Psychologists and applied ethologists bring a rich tradition of applied science focused on proximate mechanisms. Because proximate mechanisms can be manipulated in the service of conservation, whereas adaptive value cannot, more focus on proximate mechanisms will help move this discipline from the implications to the applications phase of research. See also: Anthropogenic Noise: Impacts on Animals; Conservation and Anti-Predator Behavior; Conservation and Behavior: Introduction; Habitat Imprinting; Habitat Selection; Learning and Conservation; Mate Choice in Males and Females; Mating Interference Due to Introduction of Exotic Species; Mating Signals; Ontogenetic Effects of Captive Breeding.
Further Reading Anthony, LL and Blumstein, DT (2000). Integrating behaviour into wildlife conservation: The multiple ways that behaviour can reduce Ne. Biological Conservation 95: 303–315. Be´lisle, M (2005). Measuring landscape connectivity: the challenge of behavioral landscape ecology. Ecology 86: 1988–1995.
Conservation and Animal Behavior Blumstein, DT and Ferna´ndez-Juricic, E (2004). The emergence of conservation behavior. Conservation Biology 18: 1175–1177. Buchholz, R (2007). Behavioural biology: An effective and relevant conservation tool. Trends in Ecology & Evolution 22: 401. Caro, T (2007). Behavior and conservation: A bridge too far? Trends in Ecology & Evolution 22: 394–400. Frid, A and Dill, LM (2002). Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology 6: 11. Gosling, LM and Sutherland, WJ (2000). Behaviour and Conservation. Cambridge: Cambridge University Press. Griffin, AS, Blumstein, DT, and Evans, CS (2000). Training captive-bred or translocated animals to avoid predators. Conservation Biology 14: 1317–1326. Holway, DA and Suarez, AV (1999). Animal behavior: An essential component of invasion biology. Trends in Ecology & Evolution 14: 328–330. Linklater, WL (2004). Wanted for conservation research: behavioral ecologists with broader perspective. BioScience 54: 352–360. McDougall, PT, Re´ale, D, Sol, D, and Reader, SM (2006). Wildlife conservation and animal temperament: Causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Animal Conservation 9: 39–48. Stamps, JA (1988). Conspecific attraction and aggregation in territorial species. American Naturalist 131: 329–347. Stamps, JA and Swaisgood, RR (2007). Someplace like home: Experience, habitat selection and conservation biology. Applied Animal Behaviour Science 102: 392–409.
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Swaisgood, RR (in press). The conservation-welfare nexus in reintroduction programs: A role for sensory ecology. Animal Welfare. Swaisgood, RR (2007). Current status and future directions of applied behavioral research for animal welfare and conservation. Applied Animal Behaviour Science 102: 139–162. Swaisgood, RR and Schulte, BA (in press). Applying knowledge of mammalian social organization, mating systems and communication to management. In: Kleiman, DG, Thompson, KV, Baer, CK, (eds.) Wild Mammals in Captivity, 2nd edn. University of Chicago Press. Ward, MP and Schlossberg, S (2004). Conspecific attraction and the conservation of territorial songbirds. Conservation Biology 18: 519–525.
Relevant Websites http://www.animalbehavior.org/ABSConservation – Animal Behaviour Society Conservation. http://www.iucnredlist.org – IUCN Redlist online. http://www.sandiegozoo.org/conservation/ – San Diego Zoo’s Conservation Research. http://www.zsl.org – Zoological Society of London.
Introduction Conservation is the end result of a human value system that seeks to maintain the diversity of life forms on earth and ensure the ecological integrity of our natural heritage. People may be motivated to conserve nature by utilitarian values, such as recognition of the important services that a functioning ecosystem provides to humanity, or by a deep and abiding philosophy that other forms of life have intrinsic value as well. The biophilia hypothesis – championed by the founding father of biodiversity and sociobiology, E.O. Wilson – posits that humans are predisposed to an emotional attachment to nature that motivates them toward environmental stewardship. It may be argued that animal behaviorists, who spend long hours observing animals, have a more-than-average dose of biophilia, making their late arrival on the conservation stage surprising. Although the modern academic discipline of conservation biology has its roots in wildlife management that goes back generations, it was not founded until the 1980s. Conservation behavior – as the application of behavioral research to conservation is sometimes called – traces its formal, academic beginnings to the waning moments of the last millennium. As an emerging discipline, conservation behavior is still seeking to define itself and find its niche in both conservation biology and behavioral science. Conservation behaviorists, a small group of individuals by any definition, are attempting to reinvent the way behavioral research is applied to conservation efforts. At the end of just over a decade of concerted effort, much of the heady promise of this nascent field has yet to come to fruition. A series of influential books and papers have, in recent years, addressed the many implications that behavior – particularly behavioral ecology – has for conservation. That the behavior of animals influences conservation is a truism, but the challenge for behavioral scientists has been to move from the implication phase of conservation behavior to more active applications to solve the real-world conservation problems. The discipline has experienced growing pains, but has real potential, some of which is just beginning to be realized. Several subdisciplines within animal behavior have contributed to the emergence of conservation behavior, but to date most proponents have been rooted in behavioral ecology. Many of the topics in behavioral ecological research appear promising for conservation application – including mating strategies, mate choice, dispersal and habitat selection, behavioral responses to habitat fragmentation
and anthropogenic disturbance, and the many behavioral facets of reintroduction programs. The strong theoretical framework afforded by behavioral ecology provides the basis for a hypothetico-deductive approach to conservation science. We are learning that a more integrated approach across the four levels of explanation in animal behavior – causation, development, adaptive utility, and evolutionary history – and across larger ecological scales – population, community, ecosystem, landscape – holds the most promise for the successful application of behavioral research to conservation.
Taking Stock of the Problem: What Are Some of the Challenges Facing Animal Conservation? Today’s natural world faces an onslaught of anthropogenic processes that threaten the functional integrity of ecosystems, leading to escalating rates of species loss seldom seen during the history of the planet. Habitat degradation and outright destruction are the single largest culprits, and the resulting fragmentation of habitat supporting wildlife has multiplicative rather than additive effects on loss of biodiversity. Widespread urbanization and intensive agricultural practices eliminate most of these lost species, whereas other human activities degrade much of the remaining natural areas. Chemical pollutants may affect survival and reproduction, and thus population recruitment rates. Noise pollution may likewise disturb mating and parenting behavior or lead to chronic stress, with its attendant consequences for immunocompetence, fertility, and allocation of energetic resources away from other demands of survival. A single aircraft overflight has been known to cause the immediate loss of most chicks in a white pelican nesting colony. Sadly, even our love for nature in the form of ecotourism may be harming animals. Ever-increasing numbers of nature enthusiasts converging on whales and dolphins may tip the energetic balance, causing chronic sublethal effects. A simple walk on the beach disturbs shorebirds, diverting them away from foraging, mating, or parenting behavior. Multiplied by thousands of beachgoers, the cumulative effects on survival and reproduction can mean population decline. Pets, acting as predators along edges of natural communities, can have reverberating effects on community dynamics deeper in the reserve. Studies have shown that even on-leash dogs can reduce diversity along a surprisingly wide trail margin.
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Humans also often aid transport and colonization of invasive nonnative species. Those species with the right suite of behavioral and life-history characteristics sometimes get a foothold in their new environment and – without the ecological controls in their place of origin – undergo rapid population expansion. Over-run with exotics, the results for native competitors or prey species can be devastating. Take the case of the mountain yellow-legged frog (Rana muscosa) in California (Figure 1). The introduction of brown trout and the larger and more aggressive bullfrog have contributed to the decline of this endangered species. This high-mountain frog has little coevolutionary history with fish predators and its tadpoles are vulnerable to predation by nonnative trout. Populations have recovered rapidly when trout have been experimentally removed. Overlaid on top of these long-known threats to animal populations is the unpredictable impact of anthropogenic climate change, which will exacerbate other impacts. Climate change may precipitate range shifts in many species, but fragmented habitat may prevent migration, calling upon even greater human intervention (such as widespread translocations of animals to help track shifting habitats). Wildlife management is likely to become increasingly intensive in the future, as protected areas become more zoo-like, managed parks. Smaller, isolated populations will call upon the skills and resources of conservation biologists more than ever. Conservation behaviorists will undoubtedly play a larger role. Just monitoring animal populations so that we know what we have will require considerable resources, though greatly aided by emerging technologies. Because behavior affects detectability, behaviorists will need to play an increasing role in survey and monitoring efforts. In managed areas, we will need to obtain a better understanding
Figure 1 One of the estimated 122 surviving adult mountain yellow-legged frogs in Southern California, decimated by invasive species and chytrid fungus. Photo by Ron Swaisgood.
of carrying capacity – the population size that can be sustained in a given patch of habitat. The ecological factor(s) limiting an animal’s carrying capacity may be food, water, shelter, refuges from predators, or breeding sites. Modifying the factors limiting the carrying capacity can be one way to alter a population’s size, for better or worse. Some species have been rescued from the wild and placed in conservation breeding programs in zoos and other facilities. These small populations need to be managed for genetic diversity to avoid the deleterious effects of inbreeding and to preserve as much of the species evolutionary potential as possible. Managers combat both random genetic drift and, more importantly, artificial selection that causes domestication-like effects on captive or even wild populations living under increasingly artificial conditions. The long-term objective of conservation breeding and other small population management programs is to sustain a secure genetic reservoir until conditions in the wild can be improved. When suitable habitat is found or created, populations can be reestablished through reintroduction and translocation programs. Reintroduction of key species can serve to restore ecological integrity of natural areas, especially if the reintroduced species are ecosystem engineers. For example, fossorial rodents such as ground squirrels create burrows used by a variety of wildlife species. Experimental removal of kangaroo rats precipitates invasion of nonnative grasses (Figure 2). Removal of top predators, such as mountain lions, can lead to increased numbers of smaller predators (mesopredator release) that decimate prey species, such as songbirds. Ecological restoration through reintroduction is one of the most promising areas for behavioral research contributions. Animal relocations – whether from captive-bred or wild-caught animals – require intensive behavioral research and management to prepare animals for release
Figure 2 The endangered Stephens’ kangaroo rat of Southern California. A translocation program led by the San Diego Zoo is trying to re-establish this keystone species in suitable habitat. Photo by Ron Swaisgood.
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to a novel environment and, in many cases, monitor and manage their postrelease behavior. Most reintroductions to date have taken a fairly simplistic approach to postrelease management, relying primarily on soft-release practices such as acclimation pens and short-term provision of food and water resources. Behaviorists can redefine the meaning of ‘soft’ in these programs, replacing these practices with more ecologically relevant ones guided by a strong theoretical framework. That said, the application of conservation behavior is not limited to triage and is as diverse as the imagination and creativity of its proponents.
Tackling the Problem: How Can Behavioral Research Contribute to Conservation? Animals on the Move: Space Use, Dispersal, and Habitat Settlement Animal movement patterns figure critically in many aspects of conservation management. Movement patterns determine size and shape requirements for reserves and the degree of connectivity needed for adequate migration between protected areas to sustain genetically viable metapopulations across the landscape. Animals with large home ranges more often range outside the boundaries of protected areas, where they are no longer protected. In fact, wild dog home ranges are so large relative to most reserves that only those groups living well within the core of the reserve are not exposed to the risks outside reserve boundaries. The longest animal movements are seen in dispersal – generally the once-in-a-lifetime movement away from the natal home to settle in new habitat. Reserves need to be designed to accommodate these dispersal distances, which can be many times larger than the typical home range for the species. Dispersal is important for discovering and occupying new habitat and for inbreeding avoidance. Conservation planners need better data on spatial movements, including how far an animal can move, through what types of habitat it moves, and how this is influenced by topography and human-altered landscapes. The last decade has witnessed a revolution in spatial ecology, brought on by emerging technologies such as GPS satellite telemetry and remote infrared-triggered camera and video traps. These technologies have proved especially useful in linking fine-scale movements of individual animals (of interest to behavioral ecologists) with larger landscape-level patterns (of interest to population and landscape ecologists). In the fragmented habitats that many wildlife species occupy, animals must cross gaps to maintain connectivity among animal populations. Forest specialists, in particular, may be reluctant to cross a gap caused by clear cutting or a road. It is rarely physical ability that limits gap
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crossing, but instead the animal’s perception of risk from predators or stress-mediated avoidance of an unfamiliar landscape. Common sense might inform whether an animal can pass through a habitat, but experimentation is required to determine under which motivational circumstances they will actually do so. In this experimental approach, playbacks of conspecific vocalizations have been broadcast to lure individuals into or across particular landscape features, or animals have been experimentally relocated across gaps that vary in size and quality. These bioassays can be used to determine the permeability of different habitat types over varying spatial and temporal scales. Behavioral constraints on dispersal may compromise conservation efforts. A common misconception is that if suitable habitat is present, then dispersers will find and occupy it, but such build-it-and-they-will-come approaches do not always work. Seminal research by Judy Stamps in the 1980s demonstrated that dispersers often prefer to settle near conspecifics, even among less social, territorial species. Such conspecific attraction in habitat settlement may serve to guide dispersers to suitable habitat without long, costly direct sampling of habitat quality. Research has further shown that dispersal is often the most risk-prone life history stage, exposing animals to the risks of predation and starvation in unfamiliar habitat. These risks select for more conservative dispersal strategies and the use of cues correlated with habitat suitability. Using this theoretical framework, conservation behaviorists have used bird song playbacks to recruit black-capped vireos to new areas, model decoys to attract terns to new colonies, white wash (mimicking droppings) to attract vultures, and rhino dung to encourage settlement in translocated black rhinos. This tool is proving particularly powerful in reintroduction and translocation programs, because, in fact, these conservation actions force a dispersal-like event upon animals whether or not they are prepared for dispersal. It is no surprise that most mortalities occur soon after release. Behavioral management of dispersal during this postrelease period could prove critical in determining the success or failure of the program. Consider the example of caribou translocated from open prairies to mountain forests, which suffer higher mortality than those translocated from more similar habitat types. The difference lies in their behavioral response to the environment. In winter, mountain caribou move to the north slopes to forage upon lichens that grow prevalently on the cooler, moister slopes. In winter, prairie caribou forage on open tundra, digging under the snow to expose hidden lichens, and, when translocated, maladaptively move to the more open south slopes in an attempt to use their foraging strategy in the new locale. In another example, red squirrels translocated from Corsican pine forests traversed through Scotch pine in search
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of Corsican pine to settle. Conversely, squirrels captured in Scotch pine forests reject Corsican pine in favor of Scotch pine habitats. Such behavior can be explained by natal habitat preference induction (NHPI). More formally, NHPI occurs when dispersers prefer new habitats that contain stimuli comparable to those in their natal habitat. NHPI may help explain why relocated animals are so often prone to travel so long distances, at their peril – they are searching for someplace like home. Understanding this phenomenon enables the implementation of several new approaches to reintroduction programs, including efforts to match habitat type at capture and release site or to manipulate conspicuous cues in the postrelease habitat to match those from the animal’s place of origin. Foraging Ecology Research on foraging ecology can provide key insights into animal–environment interactions important for conservation. NHPI provides but one example. Long-term studies across seasons may identify key limiting resources that determine the size of the population that can be sustained in an area (carrying capacity); such studies can be crucial for proactive conservation management to ensure those resources remain available, or can suggest ways to enhance these resources to support populations at risk. Conservation behaviorists may also identify key roles that animals under study provide for the ecosystem, such as seed dispersal, population control for smaller predators (by keystone predators), or interspecific competition for resources. Security Areas Security is another critical need for animals. Nesting and denning sites can be limiting resources. For example, endangered red-cockaded woodpeckers must excavate nests in live pine trees, a task that can take more than a year. This limiting resource shapes many aspects of the species’ behavioral ecology, including the phenomenon of cooperative breeding. Because dispersal to new areas is limited by the availability of nesting cavities, young woodpeckers remain with their parents and help raise subsequent offspring, banking on future access to nest sites nearby. Understanding this system led to a novel conservation management action. Because of the high number of reproductively mature birds without access to nesting opportunities, construction of artificial cavities led to a rapid increase in the breeding population and was key to rapid recovery following loss of many cavities in a hurricane. New research is now suggesting that giant pandas may also be limited by access to quality den sites. After centuries of logging, few trees of sufficient girth to contain a panda-sized
cavity remain, and panda females may have few quality dens to select from, limiting their ability to provide proper care for cubs. Too Much of a Good Thing: Mating Strategies, Reproductive Skew, and Effective Population Size Understanding mating patterns has several important consequences for conservation. Of those, reproductive skew may be most important. If some males have mating advantages over other males – either by direct male–male competition or female mate preferences – they will sire disproportionately more offspring. In small populations, this can further exacerbate loss of genetic diversity, and much larger populations will be required to maintain sustainable populations over the long term. A key concept is that of effective population size (Ne), which is the number of breeding animals in an ideal, randomly mating, population that would lose genetic diversity at the same rate as the actual population. The greater the reproductive skew, the smaller the Ne and the greater the concern for the long-term viability of the population. With the loss of genetic variability, species lose some of their evolutionary potential, their ability to adapt to changing environments, and may suffer consequences of inbreeding depression. To maintain long-term population viability, there is a point where small populations require management to ensure that reproduction is distributed more equitably. Experimental manipulation of behavioral mechanisms related to mate choice is one course of action being pursued by conservation behaviorists. For example, Fisher and colleagues were able to control female preferences of threatened pygmy lorises by manipulating the level of odor familiarity with potential mates (Figure 4). These researchers reasoned that females should prefer more familiar-smelling males because males capable of monopolizing an area with their odors are more competitive than males that fail to do so. This demonstrates the importance of understanding the theoretical framework provided by behavioral ecology. If male–male competition is responsible for reproductive skew, then temporary removal of the most successful male can increase Ne, as has been done with threatened Cuban rock iguanas. Relationships Matter: The Role of Social Behavior in Conservation Several social processes have important ramifications for conservation. The Allee effect – the proposal that reproduction is maximized when animals are optimally aggregated – suggests that human-mediated alterations to animal population density may influence population growth and stability. Numerous studies have shown the benefits of sociality, even for relatively solitary species,
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suggesting one consequence of a reduction in animal densities is the breakdown of social processes that confer fitness advantages – ranging from predator avoidance to opportunities for mate selection. Indeed, these social benefits may drive the phenomenon of conspecific attraction, discussed earlier. The (mostly unproven) role for conservation behaviorists is to determine optimal social density. An example from captive breeding programs is instructive: mongoose lemurs housed in pairs near other conspecifics had 500% higher rates of reproduction than isolated pairs. Courtship behavior in flamingos is greatly enhanced by allowing them to view themselves in mirrors, effectively increasing the perceived animal density. For highly social animals, we need to be mindful of the significant time and energy that animals invest in building and maintaining social relationships, and the advantages that these relationships confer. In translocation programs, for example, animals are often captured and relocated to another area, without due consideration given to social relationships. Debra Shier found that black-tailed prairie dogs had 500% higher survival rates if they were released in familiar groups than if they were released randomly with regard capture location. We must also keep in mind that solitary animals are not asocial and that even territorial species invest in relationships with neighboring animals. In reintroduction programs, animals experience many challenges related to being placed in novel environments, and the added costs of renegotiating stable relationships may mean the difference between death and survival. This may explain why the normally solitary black rhinoceros experiences a surge in conspecific aggression following translocation. A team of researchers led by Wayne Linklater addressed this problem and have found, for example, that this aggression can be mitigated by releasing rhinos in larger reserves at lower social densities, which helps them to avoid direct encounters and gradually build social familiarity (Figure 3).
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Figure 3 Dr. Wayne Linklater spreads black rhinoceros dung in research designed to guide postrelease dispersal behavior in a large-scale translocation program in southern Africa. Photo by Ron Swaisgood.
Scared to Extinction: Stress, Disturbance, and Antipredator Behavior Human activities can disturb wild animals, altering their behavior in ways detrimental to their survival and reproduction. Behavioral researchers studying the stress response system are helping to understand human impacts and suggest new ways to mitigate against these impacts. Stress is the animal’s behavioral and physiological response to biological challenge, and, when chronic, can negatively impact health and reproduction. There are numerous measures of stress, many of them problematic if observed in isolation, but immunoassay of concentrations of glucocorticoid hormones is most common. Researchers have documented a number of anthropogenic activities that activate the stress response system: noisy snowmobiles impact wolves and elk, radiocollars may affect wild dogs, noisy
Figure 4 Researchers manipulated mate preferences for a conservation breeding program for threatened pygmy lorises. Photo by Heidi Fisher.
crowds disturb captive giant pandas, and approaching hikers affect bighorn sheep, even if they do not run away. Human activities may also affect behavioral decisions that have energetic consequences. For example, sperm whales spend less time surfacing to replenish oxygen supplies when helicopters fly overhead and foraging grizzly bears consume fewer calories when hikers are nearby.
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More recently, researchers have taken a closer look at human disturbance, using a more predictive approach from the theoretical framework provided by economic models of antipredator behavior. If animals perceive humans and their activities as potential predators, then much of their response can be predicted from our understanding of antipredator behavior. A growing literature indicates that human disturbance, like predation threat, alters animals’ time budgets, with energetic and lostopportunity costs. These indirect sublethal costs can have cumulative effects worse than actual predation. Scott Creel and colleagues found that temporal and spatial proximity to wolves dramatically affected foraging patterns, causing elk to avoid the best forage in open areas in favor of suboptimal forage near cover. The consequences of this decision-making process were substantial, leading to poor body condition, lower reproduction rates, and high calf mortality. The economic principles of antipredator behavior have proved effective at predicting many of the dynamics of animal responses to human disturbance, such as the effects of tourist group size, speed of approach, and distance to cover. Disturbance can also affect mate choice and parental investment in offspring in predictable ways. But Wait, There’s More: Other Applications of Behavioral Research to Conservation Creative conservation behaviorists are exploring many other avenues to apply their craft in the service of conservation efforts. Several researchers have assisted in the many behavioral facets of reintroduction programs, most prominently, in the application of ontogenetic processes to train prey organisms in the antipredator behavior of their species prior to release. Debra Shier and Don Owings, for example, have shown that captive-born black-tailed prairie dogs can be trained to recognize and deal with predators more effectively than their untrained counterparts. When these investigators used wild-caught prairie dogs to demonstrate appropriate antipredator behavior to captive-reared conspecifics, these prairie dogs were more likely to survive when released to the wild than individuals that were trained with predators without such a conspecific demonstrator. Behavioral plasticity is another key concept in conservation behavior. Understanding and predicting behavioral response to a changing world will inform many conservation decisions. For example, behavioral elasticity preadapts invasive species to colonize novel habitats, and lack of elasticity may spell the doom of native species that cannot adapt to the invader. Natural populations comprise a number of different behavioral types – suites of correlated behavioral traits, analogous to temperament or coping styles. Aggressive animals may be predictably more active across many situations than less aggressive animals. While this
aggressiveness may confer advantages in intraspecific competition, such an advantage may be offset by increased susceptibility to predation. In some cases, even immune function is influenced by behavioral type. The sum total of behavioral types for a population is called a ‘behavioral syndrome.’ A reduction in the range of types within a syndrome can cause conservation problems if the members comprising a population can no longer adapt and respond to temporally and spatially variable environmental factors. Conservation breeding programs, in particular, may not produce the full mix of behavioral types for release, especially if the captive environment does not contain the environmental features needed for the development of some behavioral types. Conservation behaviorists need to understand these suites of correlated traits so that they can ensure that release groups, of captive or wild origin, contain those individuals that perform different important roles, such as warning against predators or locating and exploiting novel foods. To do this, we must guard against differential reproduction among different types and provide enriched environments to shape ontogenetic processes for a plurality of personalities. There is also evidence that some populations contain dispersal phenotypes, individuals that are behaviorally and physiologically prepared for the risks and rigors of dispersal – clearly important for any relocation program. Thus, to maximize population persistence, it takes all types. To move forward, conservation behavior needs to continue to become more integrated across disciplines and levels of analysis. Behavioral ecologists bring much to the table, such as the strong theoretical framework that allows hypotheses and predictions to be formulated. Psychologists and applied ethologists bring a rich tradition of applied science focused on proximate mechanisms. Because proximate mechanisms can be manipulated in the service of conservation, whereas adaptive value cannot, more focus on proximate mechanisms will help move this discipline from the implications to the applications phase of research. See also: Anthropogenic Noise: Impacts on Animals; Conservation and Anti-Predator Behavior; Conservation and Behavior: Introduction; Habitat Imprinting; Habitat Selection; Learning and Conservation; Mate Choice in Males and Females; Mating Interference Due to Introduction of Exotic Species; Mating Signals; Ontogenetic Effects of Captive Breeding.
Further Reading Anthony, LL and Blumstein, DT (2000). Integrating behaviour into wildlife conservation: The multiple ways that behaviour can reduce Ne. Biological Conservation 95: 303–315. Be´lisle, M (2005). Measuring landscape connectivity: the challenge of behavioral landscape ecology. Ecology 86: 1988–1995.
Conservation and Animal Behavior Blumstein, DT and Ferna´ndez-Juricic, E (2004). The emergence of conservation behavior. Conservation Biology 18: 1175–1177. Buchholz, R (2007). Behavioural biology: An effective and relevant conservation tool. Trends in Ecology & Evolution 22: 401. Caro, T (2007). Behavior and conservation: A bridge too far? Trends in Ecology & Evolution 22: 394–400. Frid, A and Dill, LM (2002). Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology 6: 11. Gosling, LM and Sutherland, WJ (2000). Behaviour and Conservation. Cambridge: Cambridge University Press. Griffin, AS, Blumstein, DT, and Evans, CS (2000). Training captive-bred or translocated animals to avoid predators. Conservation Biology 14: 1317–1326. Holway, DA and Suarez, AV (1999). Animal behavior: An essential component of invasion biology. Trends in Ecology & Evolution 14: 328–330. Linklater, WL (2004). Wanted for conservation research: behavioral ecologists with broader perspective. BioScience 54: 352–360. McDougall, PT, Re´ale, D, Sol, D, and Reader, SM (2006). Wildlife conservation and animal temperament: Causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Animal Conservation 9: 39–48. Stamps, JA (1988). Conspecific attraction and aggregation in territorial species. American Naturalist 131: 329–347. Stamps, JA and Swaisgood, RR (2007). Someplace like home: Experience, habitat selection and conservation biology. Applied Animal Behaviour Science 102: 392–409.
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Swaisgood, RR (in press). The conservation-welfare nexus in reintroduction programs: A role for sensory ecology. Animal Welfare. Swaisgood, RR (2007). Current status and future directions of applied behavioral research for animal welfare and conservation. Applied Animal Behaviour Science 102: 139–162. Swaisgood, RR and Schulte, BA (in press). Applying knowledge of mammalian social organization, mating systems and communication to management. In: Kleiman, DG, Thompson, KV, Baer, CK, (eds.) Wild Mammals in Captivity, 2nd edn. University of Chicago Press. Ward, MP and Schlossberg, S (2004). Conspecific attraction and the conservation of territorial songbirds. Conservation Biology 18: 519–525.
Relevant Websites http://www.animalbehavior.org/ABSConservation – Animal Behaviour Society Conservation. http://www.iucnredlist.org – IUCN Redlist online. http://www.sandiegozoo.org/conservation/ – San Diego Zoo’s Conservation Research. http://www.zsl.org – Zoological Society of London.