Research in zoos: a growth area in conservation

Despite early menageries being the source of much useful biological information on anatomy and taxonomy, it is only more recently that the potential for research in zoos has been recongnized. Collections of captive animals are unique and irreplaceable resources for conservation; but without research in zoological parks, progress in conservation science would diminish. There is a flow of information from zoo researchers to field scientists that assists in providing new insights into species biology. Reciprocally, data collected in the field enhance efforts in captive breeding. This paper summarizes the new research initiatives undertaken in zoos, e.g., in the fields of reproductive and genetic technologies, and highlights their significance for conservation and management of threatened species. It is evident that zoo research has a vital role in linking in situ and ex situ conservation. This role needs to be expanded and developed to meet the challenge posed by expanding human and declining wildlife populations and ecosystems.     

Sustainability of threatened species displayed in public aquaria,with a case study of Australian sharks and rays

Zoos and public aquaria exhibit numerous threatened species globally, and in the modern context of these institutions as conservation hubs, it is crucial that displays are ecologically sustainable. Elasmobranchs (sharks and rays) are of particular conservation concern and a higher proportion of threatened species are exhibited than any other assessed vertebrate group. Many of these lack sustainable captive populations, so comprehensive assessments of sustainability may be needed to support the management of future harvests and safeguard wild populations. We propose an approach to identify species that require an assessment of sustainability. Species at risk of extinction in the wild were considered to be those assessed as threatened (CR, EN or VU) on the IUCN Red List of Threatened Species, or data deficient species that may be at an elevated risk of extinction due to life history traits and habitat associations. We defined sustainable captive populations as self-maintaining, or from a source population that can sustain harvest levels without risk of population declines below sustainable levels. The captive breeding and wild harvest records of at risk species displayed by Australian aquaria were examined as a case study. Two species, largetooth sawfish Pristis pristis and grey nurse shark Carcharias taurus, were found to have unsustainable captive populations and were identified as high priorities for comprehensive sustainability assessments. This review highlights the need for changes in permitting practices and zoo and aquarium record management systems to improve conservation outcomes for captive elasmobranchs.     

The “Visitor Effect” and captive black-tailed prairie dog behavior

The presence and density of people at a zoo exhibit is associated with behavioral changes in captive animals. However, most of these studies have only investigated behavioral changes in primates. To widen the range of animal groups studied, we examined the effects of visitor observation on captive black-tailed prairie dog (Cynomys ludovicianus) behavior and enclosure distribution. Due to the rich variety of readily-observable, sophisticated behaviors the black-tailed prairie dog is a wonderful model species for the study of behavior. In this study, we were able to quantify the effects of observation on key behaviors.     

Effect of new founders on retention of gene diversity in captive populations: A formalization of the nucleus population concept

A nucleus population is a small captive population genetically supported by periodic importation of wild caught animals. Periodic importation will allow nucleus populations to maintain the same amount of gene diversity as larger captive populations that do not import wild caught animals. The function of nucleus populations as envisioned by the IUCN/SSC Captive Breeding Specialist Group (CBSG) is to make additional captive space available for endangered taxa not currently maintained in captivity. In this article, mathematical models are developed to assess the effectiveness of the nucleus population concept in reducing the population sizes necessary to maintain appreciable amounts of gene diversity in captive populations. It is shown that the Nucleus I population concept, as defined and promoted by the CBSG, requires an importation rate 10–20 times greater than they have indicated. Whereas nucleus populations are not appropriate for maintenance of significant amounts of gene diversity in long-term breeding programs, small populations can be valuable for research, education, and reintroduction projects with short-term goals. Decisions have to be made on which of the many endangered taxa will be maintained and for what purposes, if captive breeding is to be an effective component of species conservation. © 1993 Wiley-Liss, Inc.     

Propagation of endangered birds in US institutions: How much space is there?

Captive breeding is often touted as a way to preserve species disappearing in the wild. Zoos and related institutions have limited space for animals, however, and use of what space exists may be restricted by conflicting demands of entertainment, education, and propagation. Curators of US bird collections sponsored an analysis of space available for long-term captive management. Seventy-three collections responded to a survey, providing data on 3,174 exhibits and holding areas under their control. The most optimistic analysis indicates room for fewer than 141 long-term management programs. To use space resources optimally for conservation, there is a strong need to develop priorities within management groups. New models and strategies for using captive propagation as a short-term tool to bolster wild populations should be created. Immediate attention should be paid to the most effective and efficient ways of improving husbandry and management techniques for birds. © 1995 Wiley-Liss, Inc.     

Visitor Perceptions of Nature Conservation at Helsinki Zoo

These days zoos often claim that their main objective is the promotion of nature conservation and that they strive to educate their visitors about animals and nature conservation. But how do zoo visitors themselves perceive this emphasis on conservation education? In order to determine how Helsinki Zoo visitors perceive nature conservation during their visit, we undertook a qualitative analysis of 75 structured situational interviews and five autoethnographical visits. Our results show that there was only a limited understanding of nature conservation among the zoo visitors. Their perception follows the typical framing of nature conservation in zoos: conservation projects that embrace captive breeding, in-situ conservation collaboration, and the reintroduction of those species. Moreover, in the Helsinki Zoo case these perceptions may have been influenced by the fact that the zoo did not give concrete advice on how the visitors themselves can contribute to conservation, except in terms of donating money. Framing nature conservation in such ways distances it from visitors’ everyday lives.     

Maximizing species conservation in continental Ecuador: a case of systematic conservation planning for biodiverse regions

Ecuador has the largest number of species by area worldwide, but also a low representation of species within its protected areas. Here, we applied systematic conservation planning to identify potential areas for conservation in continental Ecuador, with the aim of increasing the representation of terrestrial species diversity in the protected area network. We selected 809 terrestrial species (amphibians, birds, mammals, and plants), for which distributions were estimated via species distribution models (SDMs), using Maxent. For each species we established conservation goals based on conservation priorities, and estimated new potential protected areas using Marxan conservation planning software. For each selected area, we determined their conservation priority and feasibility of establishment, two important aspects in the decision-making processes. We found that according to our conservation goals, the current protected area network contains large conservation gaps. Potential areas for conservation almost double the surface area of currently protected areas. Most of the newly proposed areas are located in the Coast, a region with large conservation gaps and irreversible changes in land use. The most feasible areas for conservation were found in the Amazon and Andes regions, which encompass more undisturbed habitats, and already harbor most of the current reserves. Our study allows defining a viable strategy for preserving Ecuador''s biodiversity, by combining SDMs, GIS-based decision-support software, and priority and feasibility assessments of the selected areas. This approach is useful for complementing protected area networks in countries with great biodiversity, insufficient biological information, and limited resources for conservation.     

Impact of Plant Cover on Fitness and Behavioural Traits of Captive Red-Eyed Tree Frogs (Agalychnis callidryas)

Despite the importance of ex situ conservation programmes as highlighted in the Amphibian Conservation Action Plan, there are few empirical studies that examine the influence of captive conditions on the fitness of amphibians, even for basic components of enclosure design such as cover provision. Maintaining the fitness of captive amphibian populations is essential to the success of ex situ conservation projects. Here we examined the impact of plant cover on measures of fitness and behaviour in captive red-eyed tree frogs (Agalychnis callidryas). We found significant effects of plant provision on body size, growth rates and cutaneous bacterial communities that together demonstrate a compelling fitness benefit from cover provision. We also demonstrate a strong behavioural preference for planted rather than non-planted areas. We also assessed the impact of plant provision on the abiotic environment in the enclosure as a potential driver of these behavioural and fitness effects. Together this data provides valuable information regarding enclosure design for a non-model amphibian species and has implications for amphibian populations maintained in captivity for conservation breeding programmes and research.     

The Genetic Integrity of the Ex Situ Population of the European Wildcat (Felis silvestris silvestris) Is Seriously Threatened by Introgression from Domestic Cats (Felis silvestris catus)

Studies on the genetic diversity and relatedness of zoo populations are crucial for implementing successful breeding programmes. The European wildcat, Felis s. silvestris, is subject to intensive conservation measures, including captive breeding and reintroduction. We here present the first systematic genetic analysis of the captive population of Felis s. silvestris in comparison with a natural wild population. We used microsatellites and mtDNA sequencing to assess genetic diversity, structure and integrity of the ex situ population. Our results show that the ex situ population of the European wildcat is highly structured and that it has a higher genetic diversity than the studied wild population. Some genetic clusters matched the breeding lines of certain zoos or groups of zoos that often exchanged individuals. Two mitochondrial haplotype groups were detected in the in situ populations, one of which was closely related to the most common haplotype found in domestic cats, suggesting past introgression in the wild. Although native haplotypes were also found in the captive population, the majority (68%) of captive individuals shared a common mtDNA haplotype with the domestic cat (Felis s. catus). Only six captive individuals (7.7%) were assigned as wildcats in the STRUCTURE analysis (at K = 2), two of which had domestic cat mtDNA haplotypes and only two captive individuals were assigned as purebred wildcats by NewHybrids. These results suggest that the high genetic diversity of the captive population has been caused by admixture with domestic cats. Therefore, the captive population cannot be recommended for further breeding and reintroduction.     

Representation of global and national conservation priorities by Colombia's Protected Area Network

Background

How do national-level actions overlap with global priorities for conservation? Answering this question is especially important in countries with high and unique biological diversity like Colombia. Global biodiversity schemes provide conservation guidance at a large scale, while national governments gazette land for protection based on a combination of criteria at regional or local scales. Information on how a protected area network represents global and national conservation priorities is crucial for finding gaps in coverage and for future expansion of the system.

Methodology/Principal Findings

We evaluated the agreement of Colombia''s protected area network with global conservation priorities, and the extent to which the network reflects the country''s biomes, species richness, and common environmental and physical conditions. We used this information to identify priority biomes for conservation. We find the dominant strategy in Colombia has been a proactive one, allocating the highest proportion of protected land on intact, difficult to access and species rich areas like the Amazon. Threatened and unique areas are disproportionately absent from Colombia''s protected lands. We highlight six biomes in Colombia as conservation priorities that should be considered in any future expansion of Colombia''s protected area network. Two of these biomes have less than 3% of their area protected and more than 70% of their area transformed for human use. One has less than 3% protected and high numbers of threatened vertebrates. Three biomes fall in both categories.

Conclusions

Expansion of Colombia''s Protected Area Network should consider the current representativeness of the network. We indicate six priority biomes that can contribute to improving the representation of threatened species and biomes in Colombia.     

Biodiversity,biological uncertainty,and setting conservation priorities

In a world of massive extinctions where not all taxa can be saved, how ought biologists to decide their preservation priorities? When biologists make recommendations regarding conservation, should their analyses be based on scientific criteria, on public or lay criteria, on economic or some other criteria? As a first step in answering this question, we examine the issue of whether biologists ought to try to save the endangered Florida panther, a well known “glamour” taxon. To evaluate the merits of panther preservation, we examine three important arguments of biologists who are skeptical about the desirability of panther preservation. These arguments are (1) that conservation dollars ought to be spent in more efficient ways than panther preservation; (2) that biologists and conservationists ought to work to preserve species before subspecies; and (3) that biologists and conservationists ought to work to save habitats before species or subspecies. We conclude that, although all three arguments are persuasive, none of them provides convincing grounds for foregoing panther preservation in favor of other, more scientifically significant conservation efforts. Our conclusion is based, in part, on the argument that biologists ought to employ ethical, as well as scientific, rationality in setting conservation priorities and that ethical rationality may provide persuasive grounds for preserving taxa that often are not viewed by biologists as of great importance.     

Achieving True Sustainability of Zoo Populations

For the last 30 years, cooperative management of irreplaceable animal populations in zoos and aquariums has focused primarily on the goal of minimizing genetic decay within defined time frames, and large advances have been made in technologies to optimize genetic management of closed populations. However, recent analyses have shown that most zoo programs are not projected to meet their stated goals. This has been described as a lack of achieving “sustainability” of the populations, yet by definition a goal of managed decay is not a plan for sustainability. True sustainability requires management of the resource in manner that does not deplete its value for the future. Achieving such sustainability for many managed populations may require changing from managing isolated populations to managing populations that are part of a broader metapopulation, with carefully considered exchange between populations across a spectrum of ex situ to in situ. Managing zoo populations as components of comprehensive conservation strategies for the species will require research on determinants of various kinds of genetic, physiological, behavioral, and morphological variation and their roles in population viability, development of an array of management techniques and tools, training of population managers in metapopulation management and integrated conservation planning, and projections of impacts of management strategies on the viability of the captive populations and all populations that are interactively managed or affected. Such a shift in goals and methods would result in zoo population management being an ongoing part of species conservation rather than short‐term or isolated from species conservation. Zoo Biol. 32:19‐26, 2013. © 2012 Wiley Periodicals, Inc.     

Molecular genetic analysis of the yellow-breasted capuchin monkey: recommendations for ex situ conservation

The yellow-breasted capuchin monkey, Cebus xanthosternos, is one of the most endangered species of the Brazilian Atlantic Forest. In situ conservation for this species is problematic due to habitat destruction; therefore, captive conservation has been considered as an alternative strategy. A Studbook for C. xanthosternos has been kept for more than 20 years; however, no genetic data has been collected. Our aim was to provide a preliminary assessment of the genetic variability of C. xanthosternos in captivity in Brazil and compare it with data from the wild. Microsatellite and mtDNA sequencing were carried out in 40 samples from five Brazilian institutions registered in the international Studbook and compared with 8 samples collected in a wild population from REBIO-Una/BA. DNA for analysis was extracted from hair, feces and blood. Our results showed that two of the five captive groups assessed had a genetic variability comparable to wild animals. However, the other three groups apparently require urgent management to improve its genetic variability. Considering that inbreeding effects are more pronounced in captivity due to lack of gene flow, our data indicate a need to increase population size by introducing newly rescued individuals into these captive groups. Our results are the first attempt to provide genetic information for captive C. xanthosternos in Brazil.     

Open‐access platform to synthesize knowledge of ape conservation across sites

Despite the large body of literature on ape conservation, much of the data needed for evidence‐based conservation decision‐making is still not readily accessible and standardized, rendering cross‐site comparison difficult. To support knowledge synthesis and to complement the IUCN SSC Ape Populations, Environments and Surveys database, we created the A.P.E.S. Wiki ( https://apeswiki.eva.mpg.de ), an open‐access platform providing site‐level information on ape conservation status and context. The aim of this Wiki is to provide information and data about geographical ape locations, to curate information on individuals and organizations active in ape research and conservation, and to act as a tool to support collaboration between conservation practitioners, scientists, and other stakeholders. To illustrate the process and benefits of knowledge synthesis, we used the momentum of the update of the conservation action plan for western chimpanzees (Pan troglodytes verus) and began with this critically endangered taxon. First, we gathered information on 59 sites in West Africa from scientific publications, reports, and online sources. Information was compiled in a standardized format and can thus be summarized using a web scraping approach. We then asked experts working at those sites to review and complement the information (20 sites have been reviewed to date). We demonstrate the utility of the information available through the Wiki, for example, for studying species distribution. Importantly, as an open‐access platform and based on the well‐known wiki layout, the A.P.E.S. Wiki can contribute to direct and interactive information sharing and promote the efforts invested by the ape research and conservation community. The Section on Great Apes and the Section on Small Apes of the IUCN SSC Primate Specialist Group will guide and support the expansion of the platform to all small and great ape taxa. Similar collaborative efforts can contribute to extending knowledge synthesis to all nonhuman primate species.     

Documenting Biogeographical Patterns of African Timber Species Using Herbarium Records: A Conservation Perspective Based on Native Trees from Angola

In many tropical regions the development of informed conservation strategies is hindered by a dearth of biodiversity information. Biological collections can help to overcome this problem, by providing baseline information to guide research and conservation efforts. This study focuses on the timber trees of Angola, combining herbarium (2670 records) and bibliographic data to identify the main timber species, document biogeographic patterns and identify conservation priorities. The study recognized 18 key species, most of which are threatened or near-threatened globally, or lack formal conservation assessments. Biogeographical analysis reveals three groups of species associated with the enclave of Cabinda and northwest Angola, which occur primarily in Guineo-Congolian rainforests, and evergreen forests and woodlands. The fourth group is widespread across the country, and is mostly associated with dry forests. There is little correspondence between the spatial pattern of species groups and the ecoregions adopted by WWF, suggesting that these may not provide an adequate basis for conservation planning for Angolan timber trees. Eight of the species evaluated should be given high conservation priority since they are of global conservation concern, they have very restricted distributions in Angola, their historical collection localities are largely outside protected areas and they may be under increasing logging pressure. High conservation priority was also attributed to another three species that have a large proportion of their global range concentrated in Angola and that occur in dry forests where deforestation rates are high. Our results suggest that timber tree species in Angola may be under increasing risk, thus calling for efforts to promote their conservation and sustainable exploitation. The study also highlights the importance of studying historic herbarium collections in poorly explored regions of the tropics, though new field surveys remain a priority to update historical information.     

Being Attractive Brings Advantages: The Case of Parrot Species in Captivity

Background

Parrots are one of the most frequently kept and bred bird orders in captivity. This increases poaching and thus the potential importance of captive populations for rescue programmes managed by zoos and related institutions. Both captive breeding and poaching are selective and may be influenced by the attractiveness of particular species to humans. In this paper, we tested the hypothesis that the size of zoo populations is not only determined by conservation needs, but also by the perceived beauty of individual parrot species assessed by human observers.

Methodology/Principal Findings

For the purpose of data collection, we defined four sets of species (40 parrots, 367 parrots, 34 amazons, 17 macaws). Then, we asked 776 human respondents to evaluate parrot pictures of the selected species according to perceived beauty and we analyzed its association with color and morphological characters. Irrespective of the species set, we found a good agreement among the respondents. The preferred species tended to be large, colorful, and long-tailed.

Conclusions/Significance

We repeatedly confirmed significant, positive association between the perceived beauty and the size of worldwide zoo population. Moreover, the range size and body size appeared to be significant predictors of zoo population size. In contrast, the effects of other explanatory variables, including the IUCN (International Union for Conservation of Nature) listing, appeared insignificant. Our results may suggest that zoos preferentially keep beautiful parrots and pay less attention to conservation needs.     

Conservation biology of Malagasy strepsirhines: a phylogenetic approach

The phylogenetic diversity of extant lemurs represents one of the most important but least studied aspects of the conservation biology of primates. The phylogenetic diversity of a species is inversely proportional to the relative number and closeness of its phylogenetic relatives. Phylogenetic diversity can then be used to determine conservation priorities for specific biogeographic regions. Although Malagasy strepsirhines represent the highest phylogenetic diversity among primates at the global level, there are few phylogenetic data on species-specific and regional conservation plans for lemurs in Madagascar. Therefore, in this paper the following questions are addressed for extant lemurs: 1) how does the measure of taxonomic uniqueness used by Mittermeier et al. (1992 Lemurs of Madagascar; Gland, Switzerland: IUCN) equate with an index of phylogenetic diversity, 2) what are the regional conservation priorities based on analyses of phylogenetic diversity in extant lemurs, and 3) what conservation recommendations can be made based on analyses of phylogenetic diversity in lemurs? Taxonomic endemicity standardized weight (TESW) indices of phylogenetic diversity were used to determine the evolutionary component of biodiversity and to prioritize regions for conserving lemur taxa. TESW refers to the standardization of phylogenetic diversity indices for widespread taxa and endemicity of species. The phylogenetic data came from recent genetic studies of Malagasy strepsirhines at the species level. Lemur species were assigned as being either present or absent in six biogeographic regions. TESW indices were combined with data on lemur complementarity and protected areas to assign conservation priorities at the regional level. Although there were no overall differences between taxonomic ranks and phylogenetic rankings, there were significant differences for the top-ranked taxa. The phylogenetic component of lemur diversity is greatest for Daubentonia madagascariensis, Allocebus trichotis, Lepilemur septentrionalis, Indri indri, and Mirza coquereli. Regional conservation priorities are highest for lemurs that range into northeast humid forests and western dry forests. Expansion of existing protected areas in these regions may provide the most rapid method for preserving lemurs. In the long term, new protected areas must be created because there are lemur species that: 1) are not found in existing protected areas, 2) exist only in one or two protected areas, and 3) are still being discovered outside the current network of protected areas. Data on the population dynamics and feeding ecology of phylogenetically important species are needed to ensure that protected areas adequately conserve lemur populations in Madagascar.     

Zoos through the Lens of the IUCN Red List: A Global Metapopulation Approach to Support Conservation Breeding Programs

Given current extinction trends, the number of species requiring conservation breeding programs (CBPs) is likely to increase dramatically. To inform CBP policies for threatened terrestrial vertebrates, we evaluated the number and representation of threatened vertebrate species on the IUCN Red List held in the ISIS zoo network and estimated the complexity of their management as metapopulations. Our results show that 695 of the 3,955 (23%) terrestrial vertebrate species in ISIS zoos are threatened. Only two of the 59 taxonomic orders show a higher proportion of threatened species in ISIS zoos than would be expected if species were selected at random. In addition, for most taxa, the management of a zoo metapopulation of more than 250 individuals will require the coordination of a cluster of 11 to 24 ISIS zoos within a radius of 2,000 km. Thus, in the zoo network, the representation of species that may require CBPs is currently low and the spatial distribution of these zoo populations makes management difficult. Although the zoo community may have the will and the logistical potential to contribute to conservation actions, including CBPs, to do so will require greater collaboration between zoos and other institutions, alongside the development of international agreements that facilitate cross-border movement of zoo animals. To maximize the effectiveness of integrated conservation actions that include CBPs, it is fundamental that the non-zoo conservation community acknowledges and integrates the expertise and facilities of zoos where it can be helpful.     

Conservation planning with insects at three different spatial scales

Deciding which areas to protect, and where to manage and how, are no easy tasks. Many protected areas were established opportunistically under strong political and economic constraints, which may have resulted in inefficient and ineffective conservation. Systematic conservation planning has helped us move from ad-hoc decisions to a quantitative and transparent decision-making process, identifying conservation priorities that achieve explicit objectives in a cost-efficient manner. Here we use Finnish butterflies to illustrate different modeling approaches to address three different types of situations in conservation planning at three different spatial scales. First, we employ species distribution models at the national scale to construct a conservation priority map for 91 species at the resolution of 10×10  km. Species distribution models interpolate sparse occurrence data to infer variation in habitat suitability and to predict species responses to habitat loss, management actions and climate change. Second, at the regional scale we select the optimal management plan to protect a set of habitat specialist species. And third, at the landscape scale, we use a metapopulation approach to manage a network of habitat patches for long-term persistence of a single butterfly species. These different modeling approaches illustrate trade-offs between complexity and tractability and between generality and precision. General correlation-based models are helpful to set priorities for multiple species at large spatial scales. More specific management questions at smaller scales require further data and more complex models. The vast numbers of insect species with diverse ecologies provide a source of information that has remained little used in systematic conservation planning.     

Monitoring for management of conservation and recreation in Australian protected areas

Protected areas are key to conservation of biodiversity, and Australia is one of the world’s megadiverse regions. Monitoring programs provide the information to assess the state of conservation resources, the severity of threats and the success of management responses. Here we compare the management priorities, monitoring priorities and actual monitoring practices of protected area management agencies in Australia, using four sets of data at continental scale and five at a more restricted regional scale. We track changes over a period of several years and focus at successively finer levels of detail. At both continental and regional scales, most management plans emphasise fire, invasive species and visitor management; and most monitoring programmes refer to visitor numbers and impacts as well as species and ecosystems. There is only a weak match, however, between reported management priorities and actual monitoring programmes; and the effectiveness of management responses is rarely monitored. The level of detail in visitor monitor programmes varies considerably: most parks count visitors, but few know what those visitors do. Threats from fire and invasive species receive more attention that those from recreation. At regional scale, the proportion of parks with defined monitoring programmes and priorities increased significantly from 2003/2004 to 2006/2007. Whilst only a proportion of protected areas monitor endangered species populations, for those that do this is the parameter reported in most detail, with many parks reporting single records of single individuals. Some parks also maintain anecdotal records of rare species outside routine monitoring programs.