Natural behavioural biology as a risk factor in carnivore welfare: How analysing species differences could help zoos improve enclosures

In captivity, some species often seem to thrive, while others are often prone to breeding problems, poor health, and repetitive stereotypic behaviour. Within carnivores, for instance, the brown bear, American mink and snow leopard typically adapt well to captivity and show few signs of poor welfare, while the clouded leopard and polar bear are generally hard to breed successfully and/or to prevent from performing abnormal behaviour. Understanding the fundamental source of such differences could enable reproductive success and behavioural normalcy to be improved in zoos and breeding centres, by increasing the appropriateness of the enclosure designs and environmental enrichments offered particular species, and by allowing these to be offered pre-emptively instead of reactively. Here, we demonstrate that a significant proportion of the variation in apparent welfare between captive carnivore species stems from specific aspects of natural behaviour. We tested pre-existing hypotheses that species-typical welfare is predicted by natural hunting behaviour, general activity levels, ranging, or territorial patrolling (all activities that are constrained in captivity), by collating data on median stereotypy levels and infant mortality for multiple captive species, and then regressing these against median values for the relevant aspects of natural behavioural biology (e.g. hunts per day, proportion of flesh in the diet, home-range size, etc.). Our results revealed that instead of relating to foraging (e.g. hunting), as often assumed, carnivore stereotypy levels are significantly predicted by natural ranging behaviour (e.g. home-range size and typical daily travel distances). Furthermore, naturally wide-ranging lifestyles also predicted relatively high captive infant mortality rates. These results suggest that enclosure designs and enrichments focussing on carnivores’ ranging tendencies (e.g. providing more space, multiple den sites, greater day-to-day environmental variability/novelty, and/or more control over exposure to aversive or rewarding stimuli) could be particularly effective means of improving welfare; and also, that targeting such enrichment programmes on wide-ranging species, before problems even emerge, might effectively pre-empt their development. Alternatively, species with relatively small ranges could instead be made the focus of future collections and breeding programmes, zoos phasing out wide-ranging carnivores in favour of those species inherently more suited to current or readily achievable enclosure sizes and enrichment regimes.     

When hunting benefits raptors: a case study of game species and vultures

Management of hunting activity to serve as a tool for sustainable development has become a key issue in conservation biology. However, little evidence is available showing positive impacts of hunting on ecosystem conservation, limiting its capability to be used as a conservation tool. We analysed hunting and its positive influence on the ecology and conservation of the griffon vulture (Gyps fulvus), a scavenger with a relevant function in the ecosystem, in the Cantabrian Mountains, NW Spain. Use of the area by vultures was addressed by looking for cliffs used as roosts or colonies, and consumption of game species by vultures was evaluated through field surveys and questionnaires to hunters. Results revealed a strong spatiotemporal adjustment in the use of the area by vultures and hunting events, especially of red deer and wild boar. Vultures occupied roosting sites very close to the main hunting sectors of these game species and often were seen consuming their carcasses. The spatiotemporal pattern of roost use by vultures strongly overlapped with hunting of red deer. The numbers of both red deer and wild boar hunting episodes within 3.5 km around the roosts were the best predictors of vulture occurrence and number. Our estimates show that hunting could feed around 1,800 vultures/6 months. Hunting can thus influence species at the top of the ecosystem (scavengers) and could aid sustainable management of griffon vulture populations, reconciling hunting and conservation. However, negative and positive impacts should be taken into account simultaneously for an overall evaluation of hunting on ecosystem conservation.     

Managing subsistence hunting in the changing landscape of Neotropical rain forests

Subsistence hunting has been a vital activity for local people across Neotropical rain forests (NRF). While providing a reliable source of protein, subsistence hunting also reflected the strong relationships that connected local people with the species and ecosystems in which they inhabited. However, the social and ecological context in which subsistence hunting can be sustainable has been altered. The relatively small groups that hunted in large and mostly undisturbed forests, using traditional weapons, have been replaced by a growing population using fragmented habitats and modern hunting methods. Thus, subsistence hunting is less likely to be sustainable, threatening the food security of local people and the persistence of species with critical roles in the functioning of NRF. Managing subsistence hunting in this changing context will require a more efficient combination of tools which might include banning the hunting of large and sensitive species, strengthening protected areas, alternatives to reduce the role of wildlife protein on local people's subsistence and, in some cases, voluntary resettlements of local people, from areas that could still be used as refuge for endangered species.     

Legal subsistence hunting trends in the Ugalla ecosystem of western Tanzania

Sustainable legal subsistence hunting has a place in conservation. Nonetheless, the long-term success of such schemes depends on them being well managed. We assessed the effectiveness of legal subsistence hunting in the Ugalla ecosystem of western Tanzania using data from the local legal hunting scheme. The hunting in the ecosystem is conducted within the partially protected areas around Ugalla Game Reserve. The Wildlife Division of Tanzania supervises hunting activities in the area via local conservation authorities. We analysed hunting success (animals shot per quota per licence) across species in the period from 1997 to 2004. Our results revealed that 10,511 and 5,991 animals were licenced and shot, respectively. There were considerable variations in hunting success across wildlife species. With the exception of common duiker (Sylvicapra grimmia), hunting success trends for most of the species were declining. The documented decline in wildlife off-take should be further investigated to ensure the sustainable management of this area.     

Influence of chimpanzee predation on the red colobus population at Ngogo, Kibale National Park, Uganda

Frequent hunting of red colobus monkeys (Procolobus rufomitratus) takes place at all long-term chimpanzee (Pan troglodytes) study sites where both species are present. Red colobus are the most commonly selected prey of chimpanzees even when other monkey species are more abundant. In particular, the chimpanzee community at Ngogo, Kibale National Park, Uganda, preys heavily on red colobus monkeys: the chimpanzee hunting success rate is extremely high, and chimpanzees kill many individuals per successful hunt. Census data had suggested that the red colobus population is declining and that predation by chimpanzees may be contributing to this decline. In this paper, I address the impact of hunting on the red colobus population at Ngogo. To test the hypothesis that chimpanzee hunting is sustainable, I am using demographic data collected on red colobus monkeys over a period of 3 years, as well as fecundity and mortality data from previous studies of this species. I apply matrix models and vortex analyses using a sensitivity analysis approach to project future population development. Results show that current rates of hunting are not sustainable, but that chimpanzees are neither more “noble”, nor more “savage” than humans are, but that they also hunt to ensure maximum benefit without regard for the consequences for the prey population.     

Seasonal abundance, reproduction and hunting of common quail Coturnix coturnix in the Eastern Cape Province, South Africa

This study investigated the potential overlap between breeding and hunting seasons for a population of common quail Coturnix coturnix in the Alexandria District. Seasonal abundance (assessed as the number of birds flushed per unit effort), sex ratios and reproductive condition (based on gonad sizes) of the quail were measured over a period of 16 months, including two hunting seasons. Hunting impacts were assessed in terms of the number of birds killed per unit of hunting effort. Quail exhibited a spring peak in abundance and reproduction, which coincided with the legal hunting season, and bird numbers varied markedly between years. Sex ratio varied, with males dominating early in spring. Hunters killed nearly 60% of the birds flushed, and hunter efficiency was positively correlated with the abundance of quail. These results confirm the dilemma for managers, as quail are currently hunted during the main breeding season and offtakes are high. The development of management strategies is hampered by a lack of understanding of the population biology and ecology, and impacts of hunting. A number of possible hunting strategies are discussed. Since current harvests may not be sustainable, further research is necessary.     

Grasscutter production: an example of rational exploitation of wildlife

Grasscutters or cane rats (Thryonomys spp.) are widely-distributed and valuable animals in West and Central Africa. Research has been carried out over the past 15 years to select and improve stock in order to improve their adaptability to a restricted life in captivity and to develop rearing programmes in rural and peri-urban areas of Africa. The biology of these rodents and the current status of grasscutter production are reviewed. The cultural and nutritional value of grasscutter meat, compared with that of other domestic animals, is underlined. Diverse economical, nutritional and environmental arguments for implementing grasscutter rearing in rural development programmes in Africa are listed and a method to develop grasscutter farming in any given country is suggested.     

Harvesting a red-listed species: determinant factors for willow ptarmigan harvest rates,bag sizes,and hunting efforts in Norway

A main objective of game management on public lands in Norway is to ensure that harvest levels are sustainable while securing hunting access to the public. The willow ptarmigan is a popular but red-listed small game species, and it is challenging for managers to optimize harvest levels based on uncertain population estimates and limited knowledge of the factors influencing hunting impact. We studied how willow ptarmigan hunting effort, catch per unit effort, and harvest rates were influenced by ptarmigan density, topography, vegetation, and infrastructure. Data were collected during 2013–2016 from 162 hunting blocks covering 26,828 km² state-owned land in the counties Nordland and Troms, northern Norway. Hunting effort averaged 1.27 days/km² (SD?=?2.08), and it was the highest in areas close to roads and cabins. We found an opposite effect on the catch per unit effort (CPUE, mean?=?0.77 ptarmigan/day, SD?=?0.48), which was lower close to roads. There was a marked positive effect of density on CPUE, whereas terrain steepness (slope) had a negative effect. On average, harvest removed <?10% of the autumn population in the hunting areas during the study period. This indicates a relatively low and partially compensatory hunting mortality in most years and areas. Although this study shows a low harvest rate, we recommend managers to survey ptarmigan populations, hunting effort, and harvest, especially in easily accessible areas close to infrastructure and in periods of low population density.     

Effects of hunting on guianan forest game birds

To assess the effect of on-going and of previous or near by hunting pressure on game birds in a neotropical rain forest (French Guiana), I compared species abundances between six hunted and disturbed areas, seven non-hunted and pristine areas and eight intermediate areas, undisturbed and not currently hunted, but formerly hunted or close to current hunting areas. I recorded all birds detected within 100 m-wide strip transects, walked at random through every forest type all day long. The frequency of records per 10 h and flock sizes on each transect were averaged over all surveys in each study site (N = 3025 h). Censused groups included terrestrial (tinamous, woodquails, curassow and trumpeter) and arboreal species (guans, macaws, parrots, toucans), but not waterbirds. The abundance of all game birds was higher in non-hunted than in hunted areas, though not always significantly for secretive understorey species (tinamous, guans, wood-quail) or canopy frugivores (parrots, macaws, toucans). The Black Curassow and Gray-winged Trumpeter exhibited the highest and most consistent increases (7–10-fold) and more so between intermediate and non-hunted sites than between hunted and intermediate sites. The mean flock size also increased along the hunting gradient, especially in flocking species (macaws, parrots, trumpeter). Low reproductive rates and/or seasonal movements may explain that hunting pressure could still be felt after hunting has ceased or when it persists only away from a given area. Such a persistent effect would affect some populations in small protected areas.     

Effects of captivity,diet, and relocation on the gut bacterial communities of white‐footed mice

Microbes can have important impacts on their host's survival. Captive breeding programs for endangered species include periods of captivity that can ultimately have an impact on reintroduction success. No study to date has investigated the impacts of captive diet on the gut microbiota during the relocation process of generalist species. This study simulated a captive breeding program with white‐footed mice (Peromyscus leucopus) to describe the variability in gut microbial community structure and composition during captivity and relocation in their natural habitat, and compared it to wild individuals. Mice born in captivity were fed two different diets, a control with dry standardized pellets and a treatment with nonprocessed components that reflect a version of their wild diet that could be provided in captivity. The mice from the two groups were then relocated to their natural habitat. Relocated mice that had the treatment diet had more phylotypes in common with the wild‐host microbiota than mice under the control diet or mice kept in captivity. These results have broad implications for our understanding of microbial community dynamics and the effects of captivity on reintroduced animals, including the potential impact on the survival of endangered species. This study demonstrates that ex situ conservation actions should consider a more holistic perspective of an animal's biology including its microbes.     

Impacts of taxonomic inertia for the conservation of African ungulate diversity: an overview

We review the state of African ungulate taxonomy over the last 120 years, with an emphasis on the introduction of the polytypic species concept and the discipline's general neglect since the middle of the 20th century. We single out negative consequences of ‘orthodox’ taxonomy, highlighting numerous cases of neglect of threatened lineages, unsound translocations that led to lineage introgression, and cases of maladaptation to local conditions including parasitic infections. Additionally, several captive breeding programmes have been hampered by chromosome rearrangements caused by involuntary lineage mixing. We advocate that specimen‐based taxonomy should regain its keystone role in mammal research and conservation biology, with its scientific values augmented with genomic evidence. While integration with molecular biology, ecology and behaviour is needed for a full understanding of ungulate alpha diversity, we stress that morphological diversity has been neglected despite its tremendous practical importance for some groups of ‘utilizers’ such as trophy hunters, wildlife tourists and conservationists. We conclude that there is no evidence that purported ‘taxonomic inflation’ has adverse effects on ungulate conservation: rather, it is taxonomic inertia that has such adverse effects. We stress that sound science, founded on robust taxonomy, should underpin effective sustainable management (hunting, ranching, captive breeding and reintroduction programmes) of this unique African natural resource.     

The impact of tourist hunting on large mammals in Tanzania: an initial assessment

In Tanzania, where tourist hunting is employed as a conservation tool for habitat protection, information on population sizes and hunting offtake was used to assess the impact of tourist hunting on mammal densities. In general, tourist hunting pressure was unrelated to local population sizes, but for most species, animals were removed at a level of less than 10% of the local population size, suggesting that over-exploitation was unlikely. Eland, however, and perhaps small antelope, bushbuck, kudu and reedbuck were hunted at levels which may be unsustainable in the long term. Analyses also identified areas of Tanzania with high levels of tourist hunting pressure, showed that, in certain areas, species with small population sizes such as eland could be declining as a result of tourist hunting, and suggested that current levels of lion and leopard offtake are too high. These findings, although preliminary, allow recommendations to be put forward for changing hunting quotas for certain species in particular areas of Tanzania.     

Reproductive performance of the wild white-lipped peccary (<Emphasis Type="Italic">Tayassu pecari</Emphasis>) female in the Peruvian Amazon

The ability of any species to support high hunting pressures depends on its reproductive efficiency. Based on the gross anatomic examination of 208 adult female reproductive tracts, we characterised the reproductive biology of the wild white-lipped peccary in the northeastern Peruvian Amazon. White-lipped peccary apparently bred year round in the northeastern Peruvian Amazon, and the number of pregnant females was 80 (38.4%). Mean ovulation rate was 2.09 ± 0.47 CLs, and litter size was 1.60 ± 0.49 embryos or foetuses per pregnant female. A phenomenon of embryo migration was observed in the 27.5% of pregnant females. Estimations suggest 0.89 births per year and a yearly reproductive production of 1.42 piglets per pregnant female. Females in the late pregnancy stage showed a higher hunting vulnerability that could be an important restrictive factor for the reproductive efficiency of the wild white-lipped peccary populations in the Peruvian Amazon.     

Review of albacore tuna, <Emphasis Type="Italic">Thunnus alalunga</Emphasis>, biology,fisheries and management

Albacore is one of the most important commercially harvested species in the world’s oceans. Despite a long history of scientific research, there is no global review or synthesis of knowledge about the species across all oceanic regions. We analysed 613 published studies that report on albacore and summarize the current state of knowledge on biology, stock structure, fisheries and management. To describe the trends in albacore fisheries, we examined the catch and effort databases of Regional Fisheries Management Organisations. The stocks of albacore are generally largest in the Pacific Ocean and smallest in the Mediterranean Sea. The biology of Atlantic and Pacific Ocean stocks are well documented, while the Indian Ocean and the Mediterranean Sea stocks are more data deficient. These two latter areas should be considered as priorities for future research and data collection in order to better understand the state of global stocks of albacore tuna. Improved information would also assist with delineating stock boundaries needed for sustainable management of this species.     

Lion density and population structure in the Selous Game Reserve: evaluation of hunting quotas and offtake

In 1992, tourist hunting in the Selous Game Reserve generated 1.28 million dollars for the Tanzanian government, of which 0·96 million dollars were returned to wildlife conservation. Lions ( Panthera leo ) are one of three critical species for tourist hunting, consistently generating 12%–13% of hunting revenue from 1988 to 1992. Because of their ecological and economic importance (and intrinsic value), it is important that lion quotas be set so that offtake is sustainable. The population density of lions in Selous ranges from 0·08 to 0·13 adults km⁻², comparable to unhunted ecosystems. The adult sex ratio (36–41% male) and the ratio of cubs to adults (29% cubs) are similar to those of unhunted populations. The ratio of lions to hyaenas is lower in heavily hunted areas (0·17 lions/hyena) than in unhunted areas (0·43 lions/hyena). Hunting levels between 1989 and 1994 took 2·7–4·3% of adult males annually, which is sustainable. The current quota is 10–16% of the adult male population, which exceeds natural mortality rates for male lions. To remain stable if the quota was filled, the population would have to compensate via increased fecundity, increased juvenile survival, or an altered sex‐ratio. Compensation occurs in Selous by producing (or raising) more male than female cubs (66–81% of juveniles are male). Only 28% of the Selous quota was filled in 1992. The percentage of quota filled (both in Selous and nationwide) has dropped since 1988 as quotas have increased. The current intensity of lion hunting in Selous is sustainable, but the quota cannot be filled sustainably.     

Parks or arks: where to conserve threatened mammals?

Growing deterministic and stochastic threats to many wild populations of large vertebrates have focused attention on the conservation significance of captive breeding and subsequent reintroduction. However, work on both gorillas and black rhinos questions this shift in emphasis. In these species, field-based conservation can be effective if properly supported and, although this is not cheap, per capita costs may still be considerably lower than for ex situ propagation in captivity. Here we attempt to broaden the scope of this debate by contrasting the breeding success and costs of in situ and captive programmes for a range of threatened mammals. Data are scarce, but we find that across nine large-bodied genera, in situ conservation achieves comparable rates of population growth to those seen in established captive breeding programmes. Moreover, comparing budgets of well-protected reserves with zoos' own estimates of maintenance costs and the costs of zoo adoption schemes, we find that per capita costs for effective in situ conservation are consistently lower than those of maintenance in captivity. Captive breeding may be more cost-effective for smaller-bodied taxa, and will often remain desirable for large mammals restricted to one or two vulnerable wild populations. However, our results, coupled with the fact that effective in situ conservation protects intact ecosystems rather than single species, lead us to suggest that zoos might maximize their contribution to large mammal conservation by investing where possible in well-managed field-based initiatives, rather than establishing additional ex situ breeding programmes.     

Integrating Sustainable Hunting in Biodiversity Protection in Central Africa: Hot Spots,Weak Spots,and Strong Spots

Wild animals are a primary source of protein (bushmeat) for people living in or near tropical forests. Ideally, the effect of bushmeat harvests should be monitored closely by making regular estimates of offtake rate and size of stock available for exploitation. However, in practice, this is possible in very few situations because it requires both of these aspects to be readily measurable, and even in the best case, entails very considerable time and effort. As alternative, in this study, we use high-resolution, environmental favorability models for terrestrial mammals (N = 165) in Central Africa to map areas of high species richness (hot spots) and hunting susceptibility. Favorability models distinguish localities with environmental conditions that favor the species'' existence from those with detrimental characteristics for its presence. We develop an index for assessing Potential Hunting Sustainability (PHS) of each species based on their ecological characteristics (population density, habitat breadth, rarity and vulnerability), weighted according to restrictive and permissive assumptions of how species'' characteristics are combined. Species are classified into five main hunting sustainability classes using fuzzy logic. Using the accumulated favorability values of all species, and their PHS values, we finally identify weak spots, defined as high diversity regions of especial hunting vulnerability for wildlife, as well as strong spots, defined as high diversity areas of high hunting sustainability potential. Our study uses relatively simple models that employ easily obtainable data of a species'' ecological characteristics to assess the impacts of hunting in tropical regions. It provides information for management by charting the geography of where species are more or less likely to be at risk of extinction from hunting.     

Variation in Reproductive Success Across Captive Populations: Methodological Differences,Potential Biases and Opportunities

Our understanding of fundamental organismal biology has been disproportionately influenced by studies of a relatively small number of ‘model’ species extensively studied in captivity. Laboratory populations of model species are commonly subject to a number of forms of past and current selection that may affect experimental outcomes. Here, we examine these processes and their outcomes in one of the most widely used vertebrate species in the laboratory – the zebra finch (Taeniopygia guttata). This important model species is used for research across a broad range of fields, partly due to the ease with which it can be bred in captivity. However despite this perceived amenability, we demonstrate extensive variation in the success with which different laboratories and studies bred their subjects, and overall only 64% of all females that were given the opportunity, bred successfully in the laboratory. We identify and review several environmental, husbandry, life‐history and behavioural factors that potentially contribute to this variation. The variation in reproductive success across individuals could lead to biases in experimental outcomes and drive some of the heterogeneity in research outcomes across studies. The zebra finch remains an excellent captive animal system and our aim is to sharpen the insight that future studies of this species can provide, both to our understanding of this species and also with respect to the reproduction of captive animals more widely. We hope to improve systematic reporting methods and that further investigation of the issues we raise will lead both to advances in our fundamental understanding of avian reproduction as well as to improvements in future welfare and experimental efficiency.     

Systematics,conservation and sustainable development

The contribution of systematics to conservation and sustainable use of species is discussed. An adequate inventory of species is required for both areas and recent field work shows that the inventory is far from complete. This supports the first mission of Agenda 2000 which is to discover described and inventory global species diversity. The importance of making these data available in data base format is stressed. Sound systematics is a necessity for conservation legislation where control depends on the ability to identify organisms correctly. The establishment of reserves is also dependent upon data from systematics about centres of diversity and endemism and examples of this are given. Molecular systematics has made new tools available to conservation such as genetic fingerprinting which is useful both to breeding programmes of rare species and for identification for legal proceedings.Systematics is also one of the foundations for programmes of sustainable development especially in the search for new crops, non-timber forest plants from extraction forests and the identification of wild relatives of crop species. Examples of the role of systematics in a fuelwood programme in Zimbabwe, a sustainable development programme in northeast Brazil and in the search for a chemical component with medicinal properties for curing AIDS are given. The more predictive a classification we can develop using modern cladistic and molecular techniques the more useful systematics will be for both conservation and sustainable development. The goal of Agenda 2000 to organize the information derived from the programme in an efficiently retrievable form that best meets the needs of science and society is a laudable target that is crucial for conservation and the sustainable use of the plant resources of the world.