Ioz Annual Report 2000
Annual Report of the Institute of Zoology
Science for Conservation 2000 The research of The Zoological Society of London the institute of zoology aims to maintain and strengthen its position as a leading centre for research which benefits the conservation of animal species 31 30 28 24 22 18 14 10 6 4 2 1 Publications Representation Staff Education andtraining Scientific publicationsandmeetings Conservation biologyandmanagement Origins andmaintenanceofbiodiversity Population biology Evolutionary ecology Funding andCollaborations Director’s introduction Foreword byPaulHarvey Contents and breedingofthreatenedspecies. conservation educationandthehusbandry Park insupportoftheirprogrammes London ZooandWhipsnadeWild Animal and welfareintheanimalcollectionsat maintains thehigheststandardsofhealth Through itsVeterinary ScienceGroup, organizations andcountries. advanced biologicaltechniquestoother training andbythetransferof through aprogrammeofteachingand application ofthisknowledge science underpinningconservationandthe Disseminates informationaboutthe restored habitats. and inreintroductionstonaturalor the wild,incaptivebreedingprogrammes to theconservationofanimalspeciesin application ofsoundscientificprinciples Puts thisworkintopracticethroughthe veterinary science. genetics, reproductivebiologyand and evolutionaryecology, conservation fields ofanimalbehaviour, population priority forspeciesconservationinthe Carries outresearchofthehighest To thisendtheInstitute: For the Institute of Zoology, the year report spans not only scientific 2000 saw fundamental changes with research of the highest quality, but far reaching consequences. The also the Society's scientific Institute has long aspired to become publications from journals to books, a National Centre for Conservation postgraduate training, veterinary Biology and now, with our new and work, and practical conservation. synergistic association with the Each of those facets of the Institute's University of Cambridge, we are scientific activities is set to flourish foreword working together in this role. with the new administrative structures and academic input The appointment of Dr Georgina available to its staff. Mace OBE as the Institute's new Director strengthens further our Paul Harvey FRS academic leadership of this field. Secretary, The Zoological Society Georgina has worked closely and of London successfully with eminent theoretical, laboratory and field biologists from across the world to make conservation biology an applied science. The result is that ever more accurate predictions about population changes in the light of environmental pressures can be made to inform international and national decision-making processes. Academic distinction has been interwoven with other activities in the career of the Institute's new Director. Georgina has led ZSL Discussion Meetings and Symposia, and edited several books as well as the Society's successful new journal ‘Animal Conservation’. She was also instrumental in forging and formalizing the new association with the University of Cambridge.
It is my pleasure as Secretary of The Zoological Society of London to present this report of a selection of the Institute of Zoology's scientific activities over the past year. The
foreword 1 director’s introduction
2 director’s introduction It was a great privilege for me to be pursuing various routes to strengthen The year included some important appointed as Director of Science. My the linkages with Cambridge: we scientific publications, international thanks go to Dr Bill Holt who was a expect this to be a closer academic prizes, new grants and other most capable Acting Director during partnership than was the case successes. Despite this having been the difficult period following previously with the University a somewhat uncertain year with Professor Morris Gosling’s departure of London. changes in academic partner and in 1999. director, the IoZ staff have continued All staff participated in various to deliver excellent scientific results Our scientific mission to undertake stages of strategic planning to define in an increasingly competitive field. research in conservation biology has our five-year plan for HEFCE. This This report bears testament to that been greatly strengthened this year exercise was particularly helpful for work which will, I am sure, continue through a new funding partnership highlighting our comparative to flourish under our new with the University of Cambridge. strengths and weaknesses, and the arrangements. The Institute’s core research work is way in which our work relates to that supported by an annual grant of of our parent organizations – The about £1.7 million from the Higher Zoological Society of London (ZSL) Georgina Mace Education Funding Council for and the University of Cambridge. We Director of Science England (HEFCE). Since 1988 we reviewed all current projects have received this grant through the according to three criteria: scientific University of London. However, excellence, mission-relevance and following an audit by HEFCE in potential for external funding. Ideally 1998, it became clear that to our work should score highly on all of strengthen our standing as a these but we aim to support some conservation biology research important, but difficult to fund, institute we needed to identify a new projects where they are of great funding partner. Much time over the strategic value. Our research should year was spent investigating and develop at the interface between evaluating alternative new significant practical conservation arrangements. Our preferred choice programmes (by ZSL among others) was for a strategic partnership with and the excellent academic work of the University of Cambridge, which our partners in Cambridge, to support would provide a first class research the conservation of animal species. environment as well as linkages to We value our position as a the network of conservation NGOs in conservation biology research the Cambridge area. A new strategic institute with a wide network of plan for the Institute was drawn up collaborators incorporating academic, with colleagues in the Zoology governmental and non-governmental Department in Cambridge, and was organizations, and hope to develop accepted by HEFCE as a basis for further our role in forging linkages future funding. The new and providing solutions to pressing arrangements came into effect at the conservation problems. end of the year. As I write this we are
director’s introduction 3 FUNDING ORGANIZATIONS
A H Schultz-Stiftung (Switzerland) Alistair Voller Overseas Travel Fund Association for the Study of Animal Behaviour Association of British Wild Animal Keepers Bat Conservation International BBC Natural History Unit BBSRC Cook (UK) Ltd Dalgety/PIC Department of the Environment, Transport and the Regions funding and collaborations English Nature European Union FFI G & A Claraz-Schenkung (Switzerland) GlaxoWellcome Goethe-Stiftung (Switzerland) HEFCE Intervet IUCN Joint Nature Conservation Committee Lincoln Park Zoo MAFF Merial Animal Health National Geographic Society NATO NERC North American Freshwater Fishes TAG Novartis Stiftung (Switzerland) People’s Trust for Endangered Species Primate Conservation Inc. (USA) Royal Geographical Society Royal Society for the Protection of Birds Schweizerische Akademie der Naturwissenschaften (Switzerland) Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Switzerland) Smithsonian National Zoological Park Fund The British Andrology Society The British Council The Leverhulme Trust The Natural History Museum The Royal Society The Wellcome Trust Times Cheetah Appeal Universities Federation of Animal Welfare UPB Porcofram Wildlife Conservation Society WWF-UK XY Inc., Fort Collins (USA)
4 funding and collaborations Institute of Zoology Income 2000
(£2,386,229)
Core grant Research Grants and Contracts (£383,093) Research grants and contracts
Other income Goverment Bodies
Research Councils
European Union
Other organizations
COLLABORATORS
Universities Other Anglia Polytechnic Animal Gene Storage and Resource Centre of Australia Berne (Switzerland) BBSRC Silsoe Research Institute Brigham Young (USA) Bombay Natural History Society (India) Bristol Centre for Ecology & Hydrology (NERC) California (USA) Centre for Environment, Fisheries and Aquaculture Science Cambridge Chinese Academy of Science, Beijing Cardiff CSIRO Australian Animal Health Laboratory Columbia (USA) Department of Agriculture and Rural Development for Northern Ireland Duke (USA) Desert Research Foundation of Namibia Dundee Direction Générale de Forêts (Tunisia) East Anglia Dulwich Hospital Edinburgh Durrell Wildlife Conservation Trust Georgia (USA) English Nature Hong Kong (China) Estación Experimental de Zonas Aridas, Consejo Superior de Investigaciones Imperial College, London Científicas (Spain) Ishinomaki (Japan) Fisheries Research Services (Aberdeen and Pitlochry) King’s College, London Foundation for Nature Research (Norway) Lausanne (Switzerland) GlaxoWellcome Leeds Hungarian Academy of Sciences Lisbon (Portugal) Institut für Zoo- und Wildtierforschung, Berlin Liverpool Institute of Animal Health Louisiana (USA) Instituto Nazionale per la Fauna Selvatica, Bologna Luton IUCN Species Survival Commission Mahajanga (Madagascar) King Khalid Wildlife Research Centre (Saudi Arabia) Michigan State (USA) KORA (Switzerland) Montpellier (France) MAFF Veterinary Laboratories Agency Murcia (Spain) Marwell Zoological Park National University of Ireland (Cork) Moredun Research Institute New England (Australia) National Museums of Scotland Oxford National Wildlife Health Center, Wisconsin Pierre et Marie Curie (Paris) Pig Improvement Company Princeton (USA) Poultry Diagnostic and Research Centre of the Venkateshwara Hatcheries Ltd (India) Queen Mary & Westfield College, London Queensland Department of the Environment and Heritage (Australia) Queensland (Australia) Royal Society for the Protection of Birds Regensburg (Germany) Tanzania National Parks Royal Veterinary College, London Tanzanian Wildlife Research Institute San Juan (Puerto Rico) The Natural History Museum Sheffield The Wildfowl & Wetlands Trust Surrey Roehampton Universities Federation for Animal Welfare Sussex Wildlife Conservation Society University College, London ZooDent International Vermont (USA) Wageningen (The Netherlands) Washington (USA) West of England York Zurich (Switzerland)
funding and collaborations 5 Causes and consequences of genetic structure in the greater horseshoe bat Rhinolophus ferrumequinum Bats represent nearly one quarter of all mammal species world-wide and contribute most to Britain’s mammalian biodiversity. The majority evolutionary ecology of species are highly social, forming colonies in caves, mines, trees or buildings. Over the past few decades many of the suitable roosts and foraging sites on which bats so critically depend have been lost, contributing to a decline of European populations. Yet ecologists have afforded surprisingly little attention to these highly elusive animals. Breeding behaviour in particular, which can have important consequences for the maintenance of genetic variation and is therefore of interest to conservation biologists, is poorly understood in most species. In collaboration with Drs Gareth Jones and Roger Ransome at Bristol University, we used microsatellites to study breeding in the endangered greater horseshoe bat Rhinolophus ferrumequinum which underwent a dramatic tenfold decrease in Britain during the last century. Female greater horseshoe bats form summer breeding colonies, returning annually to the same roost. Single offspring are born in early summer. During autumn females visit and mate with territorial males in caves, some of which guard their territories for many years. Shortly after copulation a plug forms in the reproductive tract of the female, probably preventing further matings. Sperm are then stored throughout Studies on the breeding system and social structure of the endangered greater horseshoe bat Rhinolophus ferrumequinum led to a PhD award.
hibernation until fertilization occurs new species invades because this would interactions. We have used a model in spring. allow us to establish better system of aphids and their parasitoids To determine paternity, we management plans for the conservation (page 8) that, because of the one-to-one compared the paternally derived of whole communities. These relationship of host to adult parasitoid, genotypes of five cohorts of offspring predictions are difficult because not offers a unique opportunity to fully born at a colony in Gloucestershire, only do direct effects on resident quantify all species interactions within south-east England, with those of adult species occur but also a whole sweep of the web. males sampled throughout the indirect effects may result. One such The potential for apparent surrounding area. We found that indirect effect is ‘apparent competition’ competition to occur is analysed by breeding in this species is polygynous; which occurs when two prey species overlap diagrams (below) which show while some males sire few offspring share a predator. If a new prey species the extent to which parasitoids are born at the roost, others are repeatedly invades the community, the predator shared and how symmetrical the successful over successive years. population is able to persist at a higher interactions are. We found the Females breed with males from both population density. The higher density strongest potential for apparent within and outside their natal colony, of predators will cause competition via the highest thereby promoting gene flow among greater consumer consumer level of populations. Interestingly, a few pressures and can 9 secondary successful males are revisited by the lead to the 10 8 parasitoids. same females in separate years, leading extinction of Although to full-siblings within the roost. all prey 11 4 quantified By combining data on highly species webs are successful males with observations of except the valuable for territory tenure we have been able to one that 14 1 predicting identify several important male resists the most territories which can now be highest important safeguarded from future disturbance. predator 15 21 species Our ongoing work will hopefully shed pressure. interactions, more light on this interesting breeding Therefore they do not 16 18 system, as additional individuals are apparent 17 provide direct sampled. competition can be evidence for such responsible for additional interactions or how they ROSSITER S J, JONES G, RANSOME R D & BARRATT E M (2000). Parentage, reproductive success and breeding species exclusions and ultimately the affect species distribution and these behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum). Proceedings of the Royal Society of organization of a community. need to be tested in controlled field London Series B 267: 545-551. One way to evaluate the potential of experiments. This can conveniently be ROSSITER S J, JONES G, RANSOME R D & BARRATT E M (2000). Genetic variation and population structure in apparent competition is the sampling carried out on model assemblages of the endangered greater horseshoe bat Rhinolophus ferrumequinum. Molecular Ecology 9: 1131-1135. of fully quantified food webs. Food insects but would be impossible for webs depict trophic relationships and most vertebrate systems of major energy flows between interacting conservation concern. The Quantified interaction webs species. They are abstractions and, as accumulation of similarly resolved It would be useful if we could predict such, often pool data into classes or webs from various communities can what happens to communities when groups, blurring species boundaries and tell us whether some properties of food a species extinction occurs or when a therefore important species webs are general. If generalities across
evolutionary ecology 7 had not previously been tested, nor had it been possible to evaluate the relative contributions to threat status from the biological traits of species compared to the impacts from human activities. Our study included over 300 species of mammals belonging to the orders Carnivora and Primates where we had independent information on the severity and nature of threats they face, as well as on their life history, distribution and ecology. Using methods that control for phylogenetic relationships, we showed that species at a high trophic level, with low population density, slow life history and, in particular, a small geographical range size are all more likely to have a high extinction risk, even when the insect model food webs exist, this associations between these variables are Parasitoids are insects that could lead to significant insights on controlled for. Altogether these traits feed and develop mainly on important species interactions for the other insects. Aphids explain c. 50% of the variation in maintain large communities composition and complexity of any extinction risk between species. We of parasitoids that occupy natural community. different trophic levels within show how much of the remaining a web: ‘primary parasitoids’ variation is directly attributable to the attack the aphid host and MÜLLER C B, ADRIAANSE I C T, BELSHAW R & GODFRAY H C J (1999). The structure of an aphid- intensity of human-induced processes ‘secondary parasitoids’ attack parasitoid community. Journal of Animal Ecology 68: the primary or secondary 346-370. that can threaten species, whatever parasitoid. their basic biology. For example, several of the Madagascan lemurs are, Innately vulnerable to extinction? according to our model, biologically New compilations of information on robust against extinction but they have the severity of threat faced by the a high threat rate because their habitat world’s mammals have made it possible is disappearing. In contrast, other for us to undertake a systematic study species, such as baboons, that appear on the relationship between basic biologically vulnerable are apparently biological traits of species and their quite secure because they have vulnerability to extinction. From significant populations in relatively general observations it has been undisturbed habitats. suggested that relatively large-bodied, PURVIS A, GITTLEMAN J L, COWLISHAW G & MACE G M slow-reproducing species and those at (2000). Predicting extinction risk in declining species. Proceedings of the Royal Society of London Series B 267: the top of food chains would be more 1947-1952. vulnerable to extinction. However, this
8 evolutionary ecology Distance moved from playback experiments and hunger state
Dummy playbacks Hyaena playbacks Fat Lion playbacks
Medium Hunger state
Thin 100 200 300 400 500 600 700 800 900 1000
Distance moved from speaker (m)
Living with the enemy: cheetahs, through a loudspeaker to examine the moving than at low densities. lions and hyaenas in the Serengeti risk perceived by cheetahs from these Furthermore, both lions and hyaenas Predator avoidance has been carnivores. The results show that are found near high densities of documented for a number of species cheetahs actively moved away from gazelle, the main prey of cheetahs on and could potentially play a key role in both lion and hyaena calls. Cheetahs the Serengeti plains, whereas cheetahs structuring species communities. This is were also much less likely to hunt after are more frequently found near low the case even when the actual mortality lion and hyaena calls than when no densities of gazelle, while avoiding owing to predation is low, as mortality sound was played through the areas with no gazelles. By avoiding may be low because predator avoidance loudspeaker. This reduction in hunting competitors, cheetahs might move is effective. Where competition is activity resulted in a lower kill rate away from areas with high prey intense, then competitor avoidance suggesting that the perceived presence densities to areas of lower prey may also be important. This year we of other carnivores by cheetahs caused densities, where they can survive documented avoidance behaviour them to suffer reduced food intake because of their higher hunting success within a large carnivore community for rates. Also, while cheetahs moved just on small groups or isolated the first time. Cheetahs in the as far after lion calls as after hyaena individuals. The mobility of cheetahs Serengeti, Tanzania, lose kills and their calls, they spent significantly more time and their ability to avoid direct cubs to two species of large carnivores: looking at the loudspeaker and were competition in an ever changing lions and spotted hyaenas. Cheetahs less likely to make a kill after lion calls, landscape of competitors and prey may can do little to defend themselves suggesting that cheetahs perceived lions be the key to their coexistence with because they have small jaws and are of to be a greater threat than hyaenas. lions and hyaenas. a much lighter build than these other Does avoidance have implications DURANT S M (2000). Predator avoidance, breeding carnivores. Cheetahs might therefore for the distribution of cheetahs within experience and reproductive success in endangered cheetahs (Acinonyx jubatus). Animal Behaviour 60: 121-130. be expected to employ avoidance the Serengeti ecosystem? A previous DURANT S M (2000). Living with the enemy: pedator behaviours, particularly when they are study has shown that whenever avoidance of hyaenas and lions by cheetahs in the Serengeti. Behavioral Ecology 11: 624-632. likely to be hunting and hence more cheetahs are found near high densities likely to attract attention. Lion and of lions or hyaenas they are less likely hyaena calls were played to cheetahs to be hunting and more likely to be
Distance moved from lion and hyaena playbacks
1600 hyaenas 1600 lions 1400 1400 old cheetahs 1200 1200 old cheetahs
1000 1000
800 800 young cheetahs 600 600 Distance from speaker (m)
400 young cheetahs 400 200 200 0.0 0.5 1.0 1.5 0.0 0.5 1.0 1.5
Number of surviving cubs/year Number of surviving cubs/year
evolutionary ecology 9 Investigating a recent mass mortality of Caspian seals Phoca caspica The Caspian seal Phoca caspica is unique to the Caspian Sea and is listed as Vulnerable by the IUCN (World Conservation Union). Between April and August 2000 a mass die-off population biology occurred affecting many thousands of individuals. The die-off, first reported in Kazakhstan in the northernmost part of the Caspian Sea, spread southwards to Azerbaijan and Turkmenistan. Our scientists formed part of an international team of researchers (predominantly from the UK and The Netherlands) investigating the cause of the mortality. The investigation was funded in Azerbaijan by the World Bank Ecotoxicology Project via the Japanese Consultant Trust Fund, and in Kazakhstan by the Offshore Kazakhstan International Operating Company. Initial postmortem examinations of dead seals from Kazakhstan and Azerbaijan did not produce any consistent findings, although many seals were emaciated. However, microscopic examination of tissue samples from these seals revealed a consistent pattern of lesions that was highly suggestive of distemper, a disease of terrestrial and aquatic mammals caused by specific viruses of the genus Morbillivirus. Tissue sections were subsequently examined using an immunohistochemical technique with a primary monoclonal antibody that is known to cross-react with canine and phocine distemper viruses, and cetacean morbilliviruses. Morbillivirus Bladder epithelial cells from Caspian seals stained with H&E (right) or a monoclonal antibody against distemper virus (left) gave results which are characteristic of distemper virus infection.
antigen was detected in a range of been identified in Caspian seals, inbreeding depression by deliberate lesions and tissues in seals exhibiting including some individuals that died in inbreeding has been explored both distemper-like lesions. These this mortality event. The possibility theoretically and empirically. The multisystemic tissue lesions associated that high-level exposure to such various empirical studies yield with positive morbillivirus-specific potentially immunosuppressive conflicting results, and the broad immunohistochemical tests confirmed pollutants may have played a discrepancy about the effectiveness of the presence of distemper in Caspian secondary role in the mortality event purging inbreeding depression is seals during the mortality event. must be considered. understandable considering the many Morbillivirus nucleic acid was also factors involved. For example, among KENNEDY S, KUIKEN T, JEPSON P D, DEAVILLE R, positively identified in tissues from seal FORSYTH M, BARRETT T, VAN DE BILDT M W G, the factors which may influence OSTERHAUS A D M E, EYBATOV T, DUCK C, carcasses found on the coasts of KYDYRMANOV A, MITROFANOV I & WILSON S (2000). purging are: the genetic basis of Mass die-off of Caspian seals caused by canine distemper Kazakhstan, Azerbaijan and virus. Emerging Infectious Diseases 6 (6): 637-639. inbreeding depression, such as Turkmenistan by carrying out reverse- distributions of selection coefficients transcriptase polymerase chain reaction and dominance coefficients of (RT-PCR) with two pairs of ‘universal’ Purging inbreeding depression mutations; rates of inbreeding and morbillivirus primers. This technique resulting from deleterious genetic drift; the pattern and strength detects morbillivirus RNA and mutations of selection; reproductive capacity; transcribes it to DNA, which is The phenomenon of inbreeding organization of the genome. amplified to allow subsequent reducing fitness, known as inbreeding An important issue in purging purification and sequencing. The depression, has been widely observed inbreeding depression that has not resulting sequences matched those of in most species of plants and animals. been investigated in previous canine distemper virus (CDV) and were Although still in dispute, substantial theoretical studies is the effect of clearly distinct from those of other evidence from studies involving various selection between inbred lines. Because members of the genus Morbillivirus. fitness traits in diverse organisms has genetic variation is progressively The high degree of similarity of the RT- accumulated, supporting the reduced within lines and increased PCR sequences from these regions of hypothesis that most inbreeding between lines, particularly for recessive the Caspian Sea indicated that these depression is a result of many partially genes, between-line selection should seals were infected with the same recessive and deleterious alleles that are become increasingly effective with strain of CDV, thus establishing clear maintained by mutation and selection inbreeding, compared to within-line spatial and temporal links between the balance, and not to a few selection. Successful highly inbred seal mortalities in these widely overdominant loci. lines, with a performance at least as separated regions. Inbreeding increases homozygosity good as the ancestral outbred The origin of CDV infection in and thus exposes the harmful effects of population, in organisms such as mice Caspian seals and its overall effect on the partially recessive and deleterious and maize are usually developed by the seal population remain to be mutations on fitness. This results in inbreeding a large number of lines in determined although it is possible that inbreeding depression which may parallel and applying between-line the CDV virus may have originated endanger the immediate survival of selection so that the poorest lines are from contact with terrestrial carnivores. small populations. At the same time, eliminated and the best are retained. Although tests for algal toxins in seal however, there is a potential for Therefore one possible strategy for tissues were negative, very high levels purging these mutations and the more effectively purging inbreeding of organochlorine contaminants resultant depression in fitness. In recent depression is to apply artificial (particularly DDTs and PCBs) have years the effectiveness of purging between-line selection, in addition to
population biology 11 Effects of rate of inbreeding 1 (population size, N) on the mean viability relative to the initial population. One deleterious mutation was assumed to occur per 0.9 N=100 diploid genome per generation, with N=50 mean homozygous and heterozygous effects of 0.05 and 0.02 (both in N=20 Relative viability exponential distributions), respectively. The lethal mutation N=10 rate is 0.03 and the dominance 0.8 coefficient of lethal alleles is 0.02. 0 0.1 0.2 0.3 0.4
Inbreeding coefficient
within-line selection and natural deleterious mutations have relatively provide the minimum requirements of extinction of lines. large effects on fitness in species with the breeding pair during limited Another issue that has received little reproductive ability high enough to resource availability. Outside critical attention is the interaction between cope with the depressed fitness owing periods of limited resource availability, inbreeding, genetic drift and selection. to inbreeding, it is not justified to these minimum territories may contain Inbreeding facilitates the selective apply a breeding programme aimed at more resources than needed by the elimination of partially recessive purging inbreeding depression by breeding pair alone, and can sustain deleterious mutations, while genetic inbreeding and selection to a philopatric subordinate animals. drift hinders the purging process and population of conservation concern. In collaboration with Professor may drive the deleterious mutations to S Harris, Bristol University, we have WANG J (2000). Effects of population structures and fixation. Usually inbreeding and selection strategies on the purging of inbreeding examined qualitative predictions arising depression due to deleterious mutations. Genetical genetic drift cannot be separated and Research 76: 75-86. from the RDH in relation to resource operate simultaneously at the same WANG J, HILL W G, CHARLESWORTH D & availability using red fox as a model. CHARLESWORTH B (1999). Dynamics of inbreeding strength (measured by inbreeding and depression due to deleterious mutations in small Red foxes have previously been populations: mutation parameters and inbreeding rate. variance effective sizes) in a small Genetical Research 74: 165-178. described as exemplifying a population. However, under certain ‘contractionist’ strategy. The outbreak circumstances, such as partial of sarcoptic mange in an urban red fox inbreeding in a single population or Sarcoptic mange and spatial population provided an opportunity to subdividing the population into lines organization of red foxes test the RDH and the ‘contractionist’ and limiting migration, inbreeding can Theoretical studies have viewed strategy because fox density changed occur at a higher rate than drift, at least territory size as a function of the trade- temporarily. In a highly subdivided off between different costs and benefits population a deleterious mutation is to territory holders. Among group- quickly eliminated from, or fixed in, a living carnivores, two territorial line owing to the high rate of strategies have been described. Based inbreeding and genetic drift within on co-operative behaviour, lines. However, even if the mutation is ‘expansionists’ may occupy territories fixed in a line, it segregates and is greater than the minimum necessary to subject to selection again after support the basic social unit (a migration or crossing among lines. breeding pair) in order that additional The effect of population animals can share the territory. In subdivision, combined with within-line contrast, ‘contractionists’ show little or and between-line selection and line no co-operative behaviour and crossing, on purging deleterious breeding individuals defend territories mutations of variable effects was of the minimum size necessary to investigated. Extensive simulations provide their requirements. Despite the indicated that the breeding scheme absence of co-operation, groups may with equal within- and between-line arise as a result of the rules by which selection and crossing alternatively with territories are configured. The resource full-sib mating is generally the most dispersion hypothesis (RDH) assumes efficient for purging deleterious that the basic social unit occupies mutations. However, unless most territories that are just large enough to
12 population biology dramatically as a result of mange, and sheep (right), saiga antelope and red data from previous intensive ecological deer identified that both density and studies were available. In contrast to winter temperature were important in the predictions of the RDH and the one or more age class. In each species, ‘contractionist’ strategy, foxes surviving high density and cold winters the mange epidemics increased their depressed fecundity. In contrast, territories after neighbouring groups analyses of the time-series for each had died out but the increases were species did not identify significant neither accompanied by the effects of density on population relinquishment of other parts of the fluctuation. The approach of analysing existing territories, nor were they a relationships between vital response to a decline in food rates, density and climatic variables COULSON T, MILNER-GULLAND E J & CLUTTON-BROCK T (2000). The relative roles of density and climatic availability strategy. may detect important processes variation on population dynamics and fecundity rates in three contrasting ungulate species. Proceedings of the influencing population dynamics that Royal Society of London Series B 267: 1771-1779. BAKER P J, FUNK S M, HARRIS S & WHITE P C L (2000). Flexible spatial organization of urban foxes, Vulpes time-series methodologies may vulpes, before and during an outbreak of sarcoptic mange. Animal Behaviour 59: 127-146. overlook. However, an approach to analysing population dynamics data that uses both process-orientated and Population dynamics in ungulates pattern-orientated methodologies The relative influence of density- would be best. dependent and density-independent processes on population dynamics has been debated in ecology for over half a century. Although both processes are now known to be potentially important, it is currently not possible to make many generalizations. Previous research has typically used pattern- orientated approaches to decompose time-series into contributions from density-dependent and density- independent processes. An alternative process-orientated approach is to estimate the relative roles of each process on inter-annual variation in vital rates. We compared pattern- orientated analyses of time-series with process-orientated analyses of a vital rate in three contrasting ungulate species. Analyses of time-series and vital rates gave different results. Analyses of fecundity rates in Soay Ecological basis of extinction risk A high proportion of mammal and bird species is threatened with extinction. In the last decade or so, huge efforts have been made by international conservation agencies to describe the geographic distribution of biodiversity and extinction risk in these origins and maintenance of biodiversity taxa. Now we can be reasonably sure of which species are threatened with extinction and which regions have unusually high concentrations of threatened species. However, while the description of biological diversity and extinction patterns among mammal and bird species is becoming more complete and precise, we have little knowledge of the evolutionary processes and ecological mechanisms that underlie these patterns. Until very recently we could not answer such deceptively simple questions as why some species are threatened while others appear secure, and why some families contain large numbers of species while others have only a few. Understanding the evolutionary processes and ecological mechanisms that underlie extinction is fundamental to conservation biology. Previously, using statistical and phylogenetic approaches, we established that not all bird families are equally vulnerable to extinction. For example, parrots and albatrosses are unusually vulnerable whereas woodpeckers and cuckoos are unusually secure. However, the reasons for these differences are poorly understood. This may be, in part, because different bird taxa are threatened by different mechanisms. Among 1012 threatened bird species, habitat loss, human persecution and taxa to different sources of extinction introduced predators were by far the risk. As predicted, extinction risk from most common threats. Habitat loss was persecution and introduced predators is cited as a source of risk for over 70% of associated with large body size and threatened species, while human long generation time but is not Extinction – risk via habitat loss persecution and/or introduced associated with degree of specialization, predators were cited in 35% of cases. whereas extinction risk incurred Furthermore, twice as many species through habitat loss is associated with 0.08 (54%) were classified as being habitat specialization and small body 0.06
size but not with generation time. 0.04
Thus, our results corroborate the 0.02 prediction that there are multiple
Proportion of species in family at risk 0.00 routes to extinction among birds. One Small Large route is for large-bodied, slow-breeding Body size species to become threatened when an external factor, such as human persecution or introduced predators, disrupts the delicate balance between fecundity and mortality in bird Extinction – risk via persecution/predation populations. In our analysis, this threatened by either habitat loss alone applies to families such as the kiwis, 0.08 or by human persecution/introduced cassowaries, megapodes, penguins and 0.06 predators alone, than being threatened albatrosses. A second route is for 0.04 by both sources together (27%). ecologically specialized species to Theoretically, sources of extinction become threatened by habitat loss. 0.02
risk that perturb the balance between Such families include the trogons, Proportion of species in family at risk 0.00 Small Large fecundity and longevity, such as human scrub-birds and logrunners. A small persecution and introduced predators, number of families are prone to both Body size should be particularly hazardous for sources of extinction risk. These taxa that have slow rates of population include the parrots, rails, pheasants, growth. In contrast, sources of pigeons, cranes and white-eyes. It is extinction risk that reduce niche this last set of families that we availability, such as habitat loss, should previously identified as being represent a particular threat to taxa that significantly over-prone to extinction. are ecologically specialized. We tested Our results demonstrate the these predictions using a phylogenetic importance of considering separately comparative method and a database on the multiple mechanisms that underlie 95 families of birds. Our analyses contemporary patterns of extinction. support the predictions that different OWENS I P F & BENNETT P M (2000). Ecological basis of lineages are threatened by different extinction risk in birds: habitat loss versus human persecution and introduced predators. Proceedings of the mechanisms of extinction, and that National Academy of Sciences USA 97: 12144-12148. different ecological factors predispose
origins and maintenance of biodiversity 15 Translocation
• Human • Encroachment encroachment The relationships of emerging • Introduction Wildlife EID • Ex situ contact • “Spill-over” and infectious diseases in humans, • Ecological “spill-back” domestic animals and wildlife. manipulation Arrows indicate key factors which drive disease emergence.
Reprinted with permission from Daszak, P., Domestic Cunningham, A.A. & Hyatt, A.D. (2000) animal EID Human EID Emerging Infectious Diseases of Wildlife- Threats to Biodiversity and Human Health. Agricultural • Global travel Science. 287: 443-449. Copyright 2000 intensification • Urbanization American Association for the Advancement • Biomedical of Science. manipulation
Technology and industry
Phylogenetic misfortune as being threatened with extinction Emerging infectious diseases of Evolutionary trees are hierarchical in were to actually go extinct, and we wildlife: threats to biodiversity structure. An inevitable consequence of compared this estimate to the amount conservation and human health this is that even if species extinction predicted by the random model. Our Emerging infectious diseases (EIDs) of rates are quite high, if they are more-or- results show that threatened species are humans have been a focus of public less randomly distributed across far from randomly distributed among health interest for the past two decades. species, then whole higher taxa are taxa and among phylogenetic clades. Recently, we have shown how EIDs nearly always likely to persist simply As a consequence of this, the amount can be a significant threat to the because some constituent taxa do. This of evolutionary history that stands to conservation of animal biodiversity. means that surprising amounts of be lost as a result of the current species Increases in the number of reports of evolutionary history (measured as the extinction spasm is much higher than epizootic wildlife EIDs (e.g. marine complete branch length of a expected – for primates we expect mammal morbillivirus disease, phylogeny) can persist even if a large about an extra 10 million years of kangaroo blindness, amphibian proportion of species dies out. In an evolution to be lost per genus ranavirus disease, herpesvirus-associated influential paper, Nee and May (1997) compared to random expectation. Past mass mortalities of pilchards) suggest illustrated the potential significance of estimates of the effects of species that these are a current and serious this effect by simulating the extinctions on overall biodiversity loss global concern. Some of these diseases, consequences of species extinctions in have therefore given results that such as cutaneous chytridiomycosis of hypothetical phylogenies. For example, were too optimistic. amphibians, have been implicated in in one very large hypothetical the declines, and even extinctions, of PURVIS A, AGAPOW P-M, phylogeny they showed that just 5% of GITTLEMAN J L & MACE G M whole populations. This can happen (2000). Non-random extinction A species could capture 81% of the and the loss of evolutionary either through the direct (e.g. infection history. Science 288: evolutionary history represented in the 328-330. causing death) or the indirect, or phylogeny. However, there are various ‘knock-on’, (e.g. infection causing loss reasons to doubt their assumption that of prey species) effects of disease. species extinctions will in fact be B Although many of these disease randomly distributed. Extinct and outbreaks are seemingly ‘natural’ threatened species are more likely to occurrences, we have shown that be clumped in their distribution anthropogenic (human-mediated) on a phylogeny because they ecological changes have driven the C share traits that increase emergence of the majority of recent vulnerability to extinction and wildlife EIDs, including those in because related taxa are often otherwise pristine areas. These changes located within the same broad D include the ‘spill-over’ of pathogens geographical or habitat types where from domestic animals to wildlife, human-induced threats are human encroachment into wildlife concentrated. We were able to test this habitat, deliberate or accidental directly using recently developed translocation of pathogens (with or E complete phylogenies for mammalian without their hosts) into ‘naïve’ areas carnivores and primates. We estimated or populations (a process we have F how much evolutionary history would termed ‘pathogen pollution’), and the be lost if all the species currently listed management of wildlife for agriculture, G 16 origins and maintenance of biodiversity Sika stag (foreground) and red deer stag and red/sika hybrid hind (background) on a deer park in Ireland. Sika deer of both sexes are about half the size of Scottish red deer.
hunting and even for conservation in biological and economic terms on substantial introgression between the reasons. Further analyses demonstrate Britain’s largest remaining land taxa and 62% of sika deer and 33% of that these anthropogenic changes to mammal. red deer had some hybrid ancestry. wildlife ecology directly affect the Sika deer were first brought to the This new analysis suggests that in sika emergence of disease in human beings, British Isles in the 1860s and were bred deer selection is acting to remove which can lead to significant morbidity and distributed to parks throughout introgressed alleles. This may be and mortality (e.g. the emergence of Ireland, England and Scotland. Later, because sika hinds with introgressed Nipah virus disease in SE Asia, West sika deer were either deliberately alleles tend not to breed in their first Nile virus disease in the USA). released or escaped from deer parks, year whereas pure sika almost all Furthermore, it appears that pathogen establishing feral populations in several become pregnant in their first year. pollution could be as important and places around the British Isles. In If this selection is strong enough to far-reaching a threat to biodiversity Scotland, around ten introductions prevent introgressed alleles from conservation as other major forms of were made between the 1860s and accumulating in the long term, it might anthropogenic impacts, such as habitat 1930s and the descendants of escapees mean that red and sika deer loss or chemical pollution. Our work from these introductions now occur phenotypes will be maintained, despite demonstrates a need for increased across 50% of the available deer habitat ongoing hybridization, instead of vigilance and research into the impact in Scotland. Phenotypic hybrids have collapsing into a continuous of anthropogenic change on the been reported in Scotland from the distribution of hybrid forms, as ecology of disease in wildlife, domestic 1950s onwards where the two species observed in County Wicklow, Ireland. animals and human beings. have come into contact. A new project at the Institute also Following genetic studies of supports the view that distinct DASZAK P, CUNNINGHAM A A & HYATT A D (2000). Emerging infectious diseases of wildlife: global threats to hybridization between red and sika phenotypes of red and sika deer can be biodiversity and human health. Science 287: 443-449. deer in Scotland carried out at the maintained despite ongoing DASZAK P, CUNNINGHAM A A & HYATT A D (2000). Conservation conundrum - Response. Science 288: 2320. Institute of Cell, Animal and hybridization. Red and sika deer from Population Biology, The University of an ancient natural hybrid zone in Edinburgh, a further analysis of these eastern Siberia were analysed using the Hybridization between red deer data is under way at the Institute of same genetic techniques. Preliminary Cervus elaphus and introduced Zoology. The data are from an results show that most deer have some Japanese sika deer Cervus nippon intensive survey in Argyll, including hybrid ancestry in the recent past but in Argyll, Scotland c. 700 deer sampled during the that they can all be classified as red or Human introductions of exotic species 1996–1997 annual cull which were sika on the basis of phenotype. frequently have detrimental effects on screened for 25 species diagnostic Finally, recent analysis of new data native ecosystems. Typically this occurs microsatellite markers and one from microsatellite screening shows via competition for resources, mitochondrial marker. This new that the introduced sika deer originated predation on naïve species or through analysis confirms the strong assortative from the area around Nagasaki, hybridization with related native taxa. mating and rarity of F1 hybrids Kyushu, Japan: until now, the origins A current example of hybridization in between red and sika deer which was of these deer had been obscure because the UK is that of red deer Cervus observed previously. The F1 hybrids are of poor records of the introductions. elaphus and introduced Japanese sika generated at a frequency of only GOODMAN S J, BARTON NH, SWANSON G M, deer Cervus nippon. This hybridization 1/500–1/1000 matings, however, these ABERNETHY K & PEMBERTON J M (1999). Introgression through rare hybridisation: a genetic study of a hybrid zone is progressing rapidly and has the hybrids go on to backcross successfully between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics 152: 355-371. potential to have a serious impact both into both parental taxa. This leads to
origins and maintenance of biodiversity 17 variation wereidentified. genetic markersassociatedwiththis after freezingwasinvestigatedand Variation inboarspermatozoafertility
conservation biology and management individual variation insperm have confirmedthatconsistent inter- studies, usingpigasamodelspecies, exists betweenindividuals.Our recent variation inpost-thawsemen quality successfully inafewspecies,extensive cryopreservation hasbeenapplied option butalthoughsemen from threatenedspeciesisanattractive conservation strategies. when usedinconjunctionwithother banking hasavaluableroletoplay species extinction,however, gene preservation alonewouldend naïve tosuggestthatgamete population. Of courseitwouldbe genetic diversityinanendangered males wecouldmaintainmaximum spermatozoa of‘geneticallyvaluable’ programmes. Bycryopreservingthe stored foruseincontrolledbreeding threatened speciesarefrozenand whereby spermandothertissuesfrom problem isgeneticresourcebanking, resulting infertility. abnormal testisdevelopmentand loss ofgeneticdiversityhasledto panther reproductive fitnessistheFlorida example ofinbreedingcausingreduced viable inbredindividuals.Aclassic in smallpopulations,leadingtoless in size.Geneticvariationislostrapidly populations arealsoinevitablylimited distribution, andcaptive-bred small innumberandfragmented Many threatenedwildpopulationsare following cryopreservation basis forboarspermsurvival Our futureinthefreezer:agenetic The conceptofpreservinggenes One possiblesolutiontothis Felis concolorcoryi in which a Schematic outline of the amplified restriction fragment length polymorphism (AFLP) technique
Taq1 Adapter EcoR1 Adapter
‘freezability’ exists and is inherited. significant costs on UK agriculture Three groups of boars were identified through wastage of semen held at on the basis of a consistent response to ambient temperatures and the loss of Sperm DNA semen cryopreservation (poor, average genetic information from important Extraction and good freezers). Semen viability was boars. The identification of genetic and Digestion determined using % motility, computer markers linked to semen freezability EcoR1 Taq1 assisted semen analysis (CASA) of will have a direct impact on methods motility parameters, plasma membrane of semen preservation in the artificial integrity (SYBR-14 +ve by flow insemination (AI) industry and Restriction cytometry) and acrosome integrity promote cryopreservation as a viable Fragments (fluorescein-labelled peanut agglutinin option for porcine AI. Rigorous +ve stained smears). validation of these molecular markers DNA from boars classified as good as a predictive measure of semen LITIGATION OF ADAPTERS and poor freezers was analysed using freezability will provide an opportunity the amplified restriction fragment to improve the quality of cryopreserved length polymorphism (AFLP) semen through selective breeding technique to identify molecular programmes, leading to improved Restriction Fragments with markers linked to genes controlling the efficiency for UK agriculture. Adapters Ligated ability of sperm to freeze successfully. The identification of genetic markers The AFLP technique is based on the linked to ‘freezability’ genes will allow selective PCR amplification of us to promote genome banking as a A PREAMPLIFICATION PCR fragments of genomic DNA and allows viable conservation tool. Future work A us to screen the genome without prior must aim to identify what aspects of knowledge of nucleotide sequence. The sperm function are controlled by the A DNA fragments are visualized on a freezability genes and develop A sequencing gel and assessed rather like protocols to minimize the effects of A T Preselective PCR Product a DNA ‘fingerprint’. Clear differences freezing on these cellular components. T A in the DNA profiles of individual boars The development of successful were observed and these were related to cryopreservation protocols would AAA SELECTIVE PCR the variation in semen freezability, ensure the maintenance of viable AAA confirming that freezability is stored spermatozoa, protecting both inherited. Sixteen candidate molecular genetic and species diversity for AAA markers linked to genes influencing future generations. A T T A semen cryopreservation were identified. AAA THURSTON L M (2000). An investigation into sources of AAA TTT variation and the genetic basis of boar sperm survival Selective Important practical applications of PCR Product following cryopreservation. PhD Thesis, University of TTT AAA this research extend to both London. domesticated and endangered species. THURSTON LM, SIGGINS K, MILEHAM A, WATSON P F & HOLT W V (2000). Identification of amplified restriction PAGE By identifying markers for genes which fragment length polymorphism (AFLP) markers linked to genes controlling boar sperm viability following may influence semen freezability, we cryopreservation. Journal of Reproduction and Fertility Abstract Series 25. have the potential to influence animal production systems. Current methods of sperm preservation impose
conservation biology and management 19 Veterinary monitoring of scimitar- the Tunisian Direction Générale de horned oryx Oryx dammah Forêts, Park officials and vets from the reintroduced to Tunisia Ministry of Agriculture and Veterinary The reintroduction of a mammal into Faculty considered the management part of its former range is not southern Tunisia for reintroduction to and monitoring of disease in wildlife. straightforward. In order to succeed, two National parks, and a further male FLACH E J, D’ALTERIO G-L, ZAHZAH K, MOLCANOVA R, the reason for the disappearance of the was sent to Bou Hedma to introduce a WAKEFIELD S, BAROSSI D, EULENBERGER K, KOPCOK M, OLLIVET F, PETIT T, VAHALA J & FRÖLICH K (2000). species from the area must have been fresh genetic line. Veterinary monitoring of captive-bred scimitar-horned oryx (Oryx dammah) prior to reintroduction in Tunisia. identified and removed or dealt with, Our veterinary involvement with the Proceedings of the 3rd Scientific Meeting of the European Association of Zoo and Wildlife Veterinarians (Paris). 31 and sufficient habitat for the animals’ oryx reintroduction included: (1) co- May - 4 June 2000: 91-97. requirements must be available. Disease ordination of pre-export health checks is another important factor. Animals performed by the veterinarians at the raised in captivity may carry pathogens zoos providing animals, (2) monitoring Parapoxvirus disease and mortality that were natural in their former range the oryx during transportation and the in red squirrels Sciurus vulgaris but may also carry exotic pathogens, 30 day post-import quarantine period, In our studies to explain the effects of contracted from domestic animals or and carrying out treatment and infectious disease on the population other exotics, especially closely related preventative health measures, and (3) size of endangered species we have species. The stress of transportation monitoring health after release and used red squirrel parapoxvirus (RSPPV) may exacerbate infections or lower assisting with movement of oryx and squirrels as a model. The resistance and the mixing of animals between release sites. All 14 oryx were epidemiology of this infection was of from different collections may expose transported to Tunisia without incident interest because there is good evidence some to pathogens to which they are and were quarantined at the Sidi Toui that parapoxvirus disease causes unaccustomed. Finally, on arrival at the National Park. After 1 month, several significant mortality in red squirrels reintroduction site, the animals may animals were immobilized; one male Sciurus vulgaris, a species which is encounter novel pathogens to which for transport to the Bou Hedma Park, undergoing a marked decline on the they have no immunity. one male and two females for transport UK mainland. A serological survey was The scimitar-horned oryx Oryx to start a third group at Oued Dekouk carried out on red squirrel and grey dammah was formerly widespread in reserve, and two females for fitting squirrel Sciurus carolinensis populations the arid grasslands of the Sahel but is radio-collars. At each opportunity the using an enzyme-linked now extinct in the wild in most, if not animals were re-examined and all were immunoabsorbant assay (ELISA). all, North African countries. The in good health. Further monitoring The results showed that 61% of grey captive population has increased has been continued by a zoologist and squirrels, an introduced species, had dramatically over the last 30 years and Park staff. antibody levels consistent with there are many animals available for A follow-up visit was made in exposure to RSPPV, compared with reintroduction. In 1985 ten oryx were November 2000. The majority of the 2.9% of red squirrels. This finding returned to the Bou Hedma National released animals, plus six offspring represents evidence of endemic Park in central Tunisia. This population born since the reintroduction, were infection of low pathogenicity in grey has grown to c. 100 animals but is sighted during visits to the Bou Hedma squirrels and suggests that they are a inbred owing to the relatedness of the and Sidi Toui National Parks. Training reservoir host of the virus. This could founders. In March 1999 two male and workshops on immobilization and explain why outbreaks of parapoxvirus 11 female scimitar-horned oryx were health checks were held for Tunisian disease continue to occur in small, sent from European institutions to National Park staff. At a meeting with isolated populations of red squirrel.
20 conservation biology and management Red squirrel
Grey squirrel 0/15
Number positive/Number tested 0/34 0/1 1/63 0/6 20/48
3/4
0/10 19/21
0/3
10/11 0/8 30/34 6/49
together with most of the collected in the field. The hormones 20/20 native fauna, are were extracted into the ethanol during threatened with extinction the storage period thereby reducing the 0/36 primarily owing to habitat laboratory processing required. alteration and destruction. Zoo, field Furthermore, although faecal samples and laboratory scientists have been contained variable amounts of The survey results suggested a collaborating for a number of years in indigestible fibrous matter and seeds, as relationship between the geographic order to gain more insight into the well as stones, these did not interfere distribution of grey squirrels with biology of one particular species, the with the hormone assays. Our results antibody to RSPPV and locations mongoose lemur Eulemur mongoz, showed that most females conceived where parapoxvirus disease is either classified as Endangered by IUCN. during the first oestrus of the breeding known to, or believed to, have A study of mongoose lemur socio- season and conception was preceded occurred. At sites where parapoxvirus ecology carried out in 1994/95 by a pseudooestrus, which probably did disease, or disease of similar provided basic knowledge of E. mongoz not result in ovulation. Pseudooestrus description, has never been known to in the wild and, in order to improve and oestrus were identified by occur, grey squirrels were seronegative. the immediate success of captive- investigating the oestrogen:progestagen The transmission of infectious agents breeding, a detailed chemical analysis ratio on each day. Pregnancy was from an abundant reservoir host to a of the diet was carried out. Genetic reliably diagnosed c. 47 days after smaller population of another species variablity in wild and captive conception when progestagen and is now a well recognized threat to populations is currently being assessed oestrogen excretion increased above endangered species, a good example and a species management group, breeding season levels. Gestation was being the occurrence of rabies in which includes researchers from zoos further characterized by high African wild dogs Lycaon pictus, which and universities, was formed last year. progestagen concentrations and a was transmitted from a reservoir in As part of this collaborative effort decline in oestrogen excretion domestic dogs. Where such threats are our reproductive biologists have 70–80 days after conception. A sub- shown to be attributable to human studied female reproductive traits in adult daughter in the wild conceived activities, the case for intervention to one of the first attempts to monitor while still a member of her natal group protect the endangered species deserves reproduction in a group of wild and aborted at 70–80 days of consideration. Vaccination of red primates using non-invasive methods. pregnancy, when progestagens declined squirrels against parapoxvirus is now In 1995 sexual behaviour was but oestrogens remained high. under investigation. monitored in two wild family groups Our results will make a significant and faecal samples were collected from contribution to the captive-breeding SAINSBURY A W, NETTLETON P, GILRAY J & GURNELL J (2000). Grey squirrels have high seroprevalence to a adult females and their sub-adult and conservation of E. mongoz and its parapoxvirus associated with deaths in red squirrels. Animal Conservation 3: 229-233. daughters over a 20 week period. relatives, and have furthered our Samples were stored in ethanol and understanding of their reproductive subsequently analysed for progestagen physiology. Monitoring reproduction in the wild and oestrogen content. These data were CURTIS D J, ZARAMODY A, GREEN D I & PICKARD A R mongoose lemur Eulemur mongoz compared with results from samples (2000). Non-invasive monitoring of reproductive status in wild Mongoose lemurs (Eulemur mongoz). Reproduction of Madagascar collected from two captive animals Fertility and Development 12: 21-29. The lemurs of Madagascar make up a in the UK. substantial proportion of the Ethanol storage was a successful mammalian diversity on the island and, method of preservation for samples
conservation biology and management 21 An essential part of ZSL’s work is Abigail Entwistle and Nigel Dunstone, facilitating the communication of and Genetics, demography and viability of information between professional fragmented populations, edited by Andrew zoologists, researchers and the general G Young and Geoffrey M Clarke. public. We achieve this through a Volume 37 of the International Zoo varied programme of meetings, which Yearbook was published and contains 43 is open to the public and members of articles, 32 of which are on the staff, and the publication of scientific conservation of Psittacines. Nigel scientific publications and meetings journals and books. Collar, BirdLife International, gives an The Journal of Zoology, ZSL’s pre- authoritative overview of the 90 species eminent international journal dedicated of parrots which are threatened with to academic zoology, continues to extinction, while others provide attract contributions from top information on breeding, husbandry, researchers. During the year 160 conservation, health and captive original peer-reviewed articles were management of these fascinating and published in 12 monthly parts of beautiful birds. Articles in Section 2, Volumes 250–252, providing The Developing Zoo World, range comprehensive coverage of the latest from the husbandry and breeding of research and developments in zoology. the Kerry spotted slug to hand-rearing ZSL’s quarterly journal, Animal and reintroduction of a Sumatran Conservation, provides an important orang-utan. The Guest Essay by Sally forum for the rapid publication of Walker addresses the continuing rigorous empirical or theoretical studies establishment of regional or national relating to species and population networks of the Conservation Breeding biology. The journal continues to bring Specialist Group. together exciting new research and After five years in preparation, this ideas from evolutionary biology and year also saw the publication by ecology that contribute to the scientific Chicago University Press of Primate basis of conservation biology. Conservation Biology by Guy Cowlishaw The Conservation Biology book (Institute of Zoology) and Robin series, published in association with Dunbar (University of Liverpool). This Cambridge University Press, includes work is both a review and synthesis of internationally significant advances in current theory and practice in primate the science that underpins conservation conservation. Beginning with an biology. Titles are based either on overview of the diversity and biology symposia held at ZSL or on other of primates, the book goes on to topics which meet these aims. Three address extinction processes in primates titles were published during the year: and the key forces that currently drive Behaviour and conservation, edited by them, namely habitat disturbance and L Morris Gosling and William J hunting. The last part of the book Sutherland, Priorities for the conservation focuses on possible conservation of mammalian diversity, edited by solutions to these problems, including
22 scientific publications and meetings JUNE
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
18 19 20 21 22 23 24 25 26 27 28 29 30
protected areas, sustainable tourism, and captive-breeding and reintroductions. NOVEMBER
The first ZSL Symposium of the new millennium Reproduction and Integrated 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Conservation Science, was held on 9th 18 19 20 21 22 23 24 25 26 27 28 29 30 and 10th November. The objectives were to critically evaluate the role of reproductive sciences in conservation and to suggest priorities for the future recognized wildlife photographer application of reproductive research in Art Wolfe, was particularly popular. this field. The meeting was organized The Science and Conservation by Bill Holt and Amanda Pickard seminars held by the Institute of (Institute of Zoology), David Wildt Zoology included talks by invited (Smithsonian Institution, USA) and speakers on subjects relevant to our John Rodger (Marsupial Conservation research, for example, Biology after the Research Center, Australia). There was a human genome, Snake venom proteins: a large international attendance with over new male contraceptive and Life history and 160 delegates from the Americas, extinction risk in bats. Antipodes, Africa, Asia and Europe. The 2000 Sir Stamford Raffles The papers will be collated in an edited Lecture, How the brain generates book to be published in the consciousness, was presented by Professor ZSL/Cambridge University Press series Susan Greenfield, Director of the Royal on conservation biology. Institution of Great Britain. The event At our regular Scientific Meetings, was sponsored by the Singapore three speakers provide an overview of Tourism Board and Singapore Airlines; important research within a particular we are most grateful for their field. The eight Meetings held during continuing support of this event. the year covered diverse subjects, such as Can parks protect Africa’s predators?, The Zoological Record, published jointly The conservation of animal diversity in with BIOSIS, is the oldest continuous river basins and Cycles in animal information service for the life populations. sciences. As a record of all aspects of Tuesday Talks are aimed at a general zoological research, it is considered the audience. Nine talks were held during foremost publication in its field. The the year covering a wide range of continued generous support of various topics, including Gorilla tactics, institutions, principally the British Mudflats, misconceptions and the Library Document Supply Centre at millennium, and From concrete to warblers Boston Spa and the Natural History - the story of the Wetland Centre. The Museum, London, in providing access Living Wild, a collection of stunning to material for indexing is greatly images presented by internationally acknowledged.
scientific publications and meetings 23 Our PhD students continue to be one Groombridge, Stephen Rossiter and of the Institute’s greatest assets. Their Lisa Thurston, were successful in individual and scientific backgrounds, obtaining their doctorates during the sources of funding support and thesis year. The key results from Stephen subjects reflect the range of research Rossiter and Lisa’s research are featured and collaboration typical across the rest elsewhere in the report. of the Institute. Students regularly Stephen Casey received his PhD for present their work through informal research on the evolutionary and education and training discussions, at the Institute’s annual population genetics of seahorses Student Conference and outside the Hippocampus spp., funded by NERC. Institute at research meetings. Seahorses are threatened by loss of Eighteen PhD students were habitat, trade and by trawls, and the registered at the Institute at the end of impact of this exploitation has been 2000. Gina Caplan, a BBSRC CASE difficult to determine; with few variable student, joined us in October to external characters which can be scored, investigate the potential use of the field species identification has been difficult. vole Microtus agretis as a novel A taxonomic revision of Vietnamese environmental biomarker. In a project species was completed and combining the bioengineering skills of phylogenetic analyses of species world- staff at the Silsoe Research Institute wide were carried out. Population with the Institute’s expertise in non- studies of the heavily fished H. comes in invasive hormone monitoring, she will the Philippines showed low levels of develop techniques for the automated genetic differentiation over tens of monitoring of reproductive status in kilometres, indicating high levels of field voles under both laboratory and gene flow and suggesting that marine field conditions. protected areas may be effective at Three NERC-funded students promoting the recovery of adjacent started in 2000. Julie Anderson will sites. study individual dispersal decisions and Jim Groombridge, funded by the emergent metapopulation dynamics of Mauritius Wildlife Foundation and the Angolan black and white colobus Durrell Wildlife Conservation Trust, monkey in East Africa. Sonya Gowtage- carried out molecular genetic studies Sequeira will investigate the on three critically endangered bird importance of jackals and domestic species endemic to Mauritius dogs in the transmission of infectious (Mauritius kestrel Falco punctatus, pink canine disease to endangered carnivores pigeon Nesoenas mayeri, echo parakeet in southern Africa, and Fredi Devas Psittacula echo). His research on the will study mechanisms which mediate Mauritius kestrel showed that recovery the impacts of both predators and of the population from an extreme competitors on foraging success in a bottleneck (a single wild breeding pair social forager, the desert baboon. in 1974 to over 250 wild pairs) Four students, Stephen Casey, Jim occurred despite the erosion of
24 education and training Frank Clarke (below right) received the Thomas Henry Huxley Award for his PhD research on naked mole-rats from Sir Martin Holdgate (left) and Mr Brian Marsh (centre).
previously high genetic diversity. develop these skills, and to learn from Therefore although half of all and support each other. The informal endangered bird species are island nature of the conference is ideal for endemics, some can make remarkable those who are presenting work for the recoveries. This collaborative study will first time. help to promote the conservation The presentations this year were all priority of other critically endangered excellent and the standard was even island species. Jim is now Project higher than last year, reinforcing the Co-ordinator on the Maui Forest Bird fact that this is an opportunity for Recovery Project in Hawaii. all over the UK. Frank is a graduate of students to progressively develop their Stephen Rossiter, funded by a Glasgow University where he was presentation skills. SaffronTownsend, NERC CASE award, investigated the President of the Zoological Society, Lisa Thurston and Octavio Paulo gave breeding system and social structure of Vice-Chair of the Exploration Society particularly well structured and the greater horseshoe bat Rhinolophus and team leader of expeditions to polished presentations on sheep ferrumequinum in the UK. Patterns of North Cyprus and Trinidad. His PhD domestication, boar sperm genetic exchange and differentiation research was on the hormonal, cryopreservation and phylogeography were investigated together with the behavioural and genetic correlates of of the Iberian lizard, respectively. consequences of population structure dominance and breeding status in Projects currently range from studies of on individual fitness and the evolution captive colonies of naked mole-rats. bumble bee foraging ecology in of kin-biased behaviour at colony level. After completing his PhD Frank London, to human-bear interactions in Stephen is now at Queen Mary and worked at the University of Pretoria, South America, MHC polymorphism Westfield College, London. South Africa, and is now at The and fitness in the great tit, leking in Lisa Thurston, a CASE student University of Aberdeen. topi and analysis of giraffe subspecies funded by BBSRC, studied sources of designations. variation in boar spermatozoa fertility Our second Student Conference, open In October the Institute held its following cryopreservation. Her results to Institute staff, external supervisors Annual Research Conference which is provided evidence of a genetic basis for and collaborators, was held on 28 also open to all staff and students and the individual variation in post-thaw September in the ZSL Education provides another forum for exchange of semen quality, and AFLP technology Department. Research Councils stress ideas and discussion. was used to identify molecular markers the importance of transferable skills linked to genes influencing this and training in the career development In addition to supporting PhD variation. Ultimately this work could of students. Our aim is to provide students, the Institute provides valuable lead to the identification of specific students with excellent experience in resources and skills for training and genes which are crucial to aspects of research and help them gain skills to collaboration with many researchers in sperm function. Lisa is now at the make informed choices about their the laboratory and the field. In any one Royal Veterinary College. future careers. One crucial skill is the year we host a large number of visitors, ability to prepare and present including undergraduate and MSc Frank Clarke was presented with information in a way that inspires and students, visiting postdoctoral the Thomas Henry Huxley Award for informs those receiving it, and by researchers and others. This year was original work submitted as a doctoral asking students to give yearly talks no exception, with undergraduate thesis, a highly competetive and within the conference setting we students from Queen Mary and prestigious award with contenders from provide an opportunity for them to Westfield College and the University of
education and training 25 education and training
East London, MSc students from students maintains the international University College London, Berne and mix, with five students from Spain and Montpelier, and postdoctoral others from Egypt and Japan. There are researchers from the Royal Veterinary now 70 course graduates, from 31 College, Paris and the USA. For countries on six continents. We example, Janice Long (MRes Studies, regularly hear news from the graduates Environmental Science, UCL) worked as they develop their careers and we with Georgina Mace for 3 months on continue to advise them as and when ‘Global conservation priorities for necessary. All veterinarians on the mammals and birds — comparing 1999/2000 course passed and Becki diversity and threat among regions’, Lawson (left) won the prize for the best and Conrad Scofield (MRes student. Some graduates have gone on Studies,York University) carried out his to key posts in zoo and wildlife research project with Chris Carbone medicine, for example, Dr Maud Becki Lawson was awarded examining predator—prey size Lafortune who is now a veterinarian at the prize for best student relationships in snakes. In the field, Calgary Zoo. on the MSc Wild Animal Health course. The prize is John Shemkunde, a Tanzanian student The Quality Assurance Agency sponsored by Mazuri with a wildlife management diploma (QAA) carried out an assessment of the Zoo Foods. from Mweka College, was seconded to standard of teaching in January 2000, the cheetah project from Tanzanian and, like the other courses run by the National Parks. As part of his Masters RVC, the MSc WAH was awarded a degree (University of Wales) he will score of 24/24 (100%). The QAA conduct a leafleting campaign to solicit report noted the high level of photographs from visitors to the Parks enthusiasm and satisfaction expressed to help estimate numbers of cheetahs by the veterinarians on the course and and cub survival across the northern that the pass rates were excellent. circuit in Tanzania. If successful, this scheme may be incorporated within Institute staff also teach on the National Parks as part of a carnivore- ‘Sex, genes and evolution’ course at monitoring plan, enabling us to University College London, and on anticipate and prevent problems to reproductive biology at King’s College cheetah populations across Tanzania. London, St George’s Medical School and the RVC. The Master of Science Course in Wild Animal Health (MSc WAH), run The Centre for Ecology and Evolution jointly with the Royal Veterinary (CEE) was set up in 1994 to create a College (RVC), continues to be centre of excellence for research and oversubscribed and a maximum teaching in the fields of ecology and compliment of 15 students started the evolution and is now a partnership 2000/2001 course in October. This between many UCL Departments, the highly successful course is now in its Institute of Zoology and the Natural seventh year and the current group of History Museum. As well as weekly
26 education and training seminars, the CEE sponsors a series of environmental problems; the reason workshops. This year the ZSL Meeting for the sudden disappearance of Rooms were the venue for a workshop rainforest frogs in protected habitats on ‘Adaptive Molecular Evolution’ and in Australia and Central America. a one-day conference entitled ‘Sex and The study demonstrated how a asex from microbes to multicells’, with multidisciplinary approach could solve speakers including John Maynard a complex environmental problem. The Smith (Sussex), Matthew Meselson Team determined that the frog declines
(Harvard), and Bill Rice (Santa Barbara). were the result of mass die-offs and Andrew Cunningham www.gene.ucl.ac.uk/cee/ identified the cause of the deaths as a (below second from right), our Veterinary Pathologist, new genus of chytrid fungus which was one of the For students and more experienced infects the skin. The research strategy international Amphibian Disease Team awarded the scientists alike, explaining the details of has been identified internationally as prestigious CSIRO medal your research to fellow scientists is the way forward in investigating global (pictured above). often a difficult task. However, problems associated with wildlife explaining it to an audience comprising Nobel laureates, Members of Parliament, Fellows of the Royal Society, school teachers, sixth form pupils and the general public is more of a challenge. The research on the social behaviour of ants being conducted by Andrew Bourke, Rob Hammond and Mike Bruford (Cardiff) formed one of the invited exhibits in this year’s New Frontiers in Science exhibition organized by the Royal diseases and related fields of Society. Assisted by Roselle Chapman, conservation. The research has the exhibit was shown for 3 days in highlighted the potential of London and a further 2 days in introduced/new pathogens as a major Edinburgh. The aim is to promote a threat to natural ecosystems, including wider understanding of science and this those previously considered pristine is an excellent opportunity to inform and outside the sphere of human a wider audience about the work of influence. The research also indicated the Institute. that disease threats to global www.royalsoc.ac.uk biodiversity may be as significant as other forms of anthropogenic Andrew Cunningham, our Veterinary environmental threats, such as global Pathologist, was one of the Amphibian warming or chemical pollution. Disease Team, comprising researchers in Australia and the USA, which solved one of the world’s most puzzling
education and training 27 staff
INSTITUTE OF ZOOLOGY STAFF AND STUDENTS
Senior Management Staff DIRECTOR: Georgina M Mace OBE DPhil ACTING DIRECTOR OF SCIENCE/REPRODUCTIVE BIOLOGY: William Holt PhD INSTITUTE ADMINISTRATOR: Christina Herterich LLM ACIS ACTING HEAD OF CONSERVATION GENETICS: William Jordan PhD ECOLOGY: Richard Pettifor DPhil VETERINARY SCIENCE: Anthony Sainsbury BVetMed CertLAS MRCVS
Administrative and Support Staff ASSISTANT INSTITUTE ADMINISTRATOR: Philip Cottingham BTec (CED) MIScT PA to DIRECTOR OF SCIENCE: Joanne Keogh ADMINISTRATIVE ASSISTANT: Katrine Garn MSc SECRETARIES: Anna-Marie Cummins, Catherine Kerr BA CHIEF TECHNICIAN (ANIMALS): Carol Williams BTec HNC THE ZOOLOGICAL SOCIETY OF LONDON ANIMAL TECHNICIANS: Mandy Gordon IIAT; Jake Rozowski SENIOR WORKSHOP TECHNICIAN: Selwyn Mundy Officers SENIOR PHOTOGRAPHIC TECHNICIAN: Terry Dennett MInstPl PRESIDENT: Sir Martin Holdgate CB MA PhD DSc (h.c.) CBiol FIBiol GENERAL LABORATORY ASSISTANT: Breda Farrell SECRETARY: Professor Paul H Harvey BA MA DPhil DSc FRS TREASURER: Harry Wilkinson OBE MA FCA Honorary Research Fellows Claudio Ciofi PhD Directors Sarah Cleaveland VetMB PhD DIRECTOR GENERAL: Michael Dixon BSc ARCS DPhil Peter Daszak PhD DIRECTOR OF SCIENCE: Georgina Mace OBE DPhil Professor George DuBoulay CBE MB BSM FRCP DMRD DIRECTOR, LONDON ZOO: Jo Gipps OBE PhD Julie Garnier DVM DIRECTOR, WHIPSNADE WILD ANIMAL PARK: Heather Hall PhD Stuart Earley MInstD MInstM FInstSMM Peter Kertesz BDS LDS DIRECTOR OF FINANCE: Norman Reed BSc FCA Professor James Kirkwood BVSc PhD MRCVS FIBiol DIRECTOR OF PERSONNEL: Ian Meyrick BA FCIPD Mark O’Connell PhD Amanda Vincent PhD Professor Paul Watson PhD BVetMed DSc MRCVS Stuart Williams PhD Bruce Winney PhD
Postdoctoral Staff and Veterinary Officers • Peter Armbruster PhD • Michelle Bayes PhD Peter Bennett PhD Andrew Bourke PhD • Kate Byrne PhD Christopher Carbone DPhil • Timothy Coulson PhD Guy Cowlishaw PhD Andrew Cunningham BVMS MRCVS Sarah Durant PhD Alireza Fazeli PhD Edmund Flach MA VetMB MSc MRCVS Stephan Funk PhD ✽ Simon Goodman PhD Rob Hammond PhD Louisa Jenkin PhD Paul Jepson BVMS MRCVS Alison Moore PhD ✽ Christine Müller PhD Amanda Pickard PhD ✽ Andrew Routh BVSc, RCVS Marcus Rowcliffe PhD Stuart Semple PhD Taina Strike BVSc MSc MRCVS • Susan Thornton BVetMed MRCVS ✽ Jinliang Wang PhD
28 staff Technicians EDITORS Animal Conservation CHIEF TECHNICIAN: David Cheesman BTec HNC Michael W Bruford PhD SENIOR TECHNICIANS: Dada Gottelli BSc; Daphne Green HNC AIScT; John L Gittleman PhD Tracy Howard BSc Georgina M Mace OBE DPhil • TECHNICIANS: Miranda Kadwell BSc Robert K Wayne PhD Shaheed Karl Macgregor, HTec MSc FIBMS ASSISTANT EDITOR • Elisabeth Thornton BSc Linda DaVolls BA EDITORIAL ASSISTANT RESEARCH ASSISTANTS Patricia Manly Rob Deaville BSc SCIENTIFIC MEETINGS CO-ORDINATOR • Robert Hutchinson BSc Deborah Body MSc (p/t) ✽ Janice Long MRes
SENIOR VETERINARY NURSE Gillian Ahearne VN • departures ✽ arrivals VETERINARY NURSES Gillian Bell VN BSc • Christine Dean VN Joanne Dodds VN ✽ Ilona Furrokh
Postgraduate Research Students Zelealam Ashenafi BSc Jonathan Baillie MES Daisy Balogh MRes Jacob Bro-Jørgensen MSc Gina Caplan MSc Angus Carpenter MSc Stephen Casey BSc Roselle Chapman MSc David Cope BA Juliet Dukes MSc Sonya Gowtage-Sequeira MSc Jim Groombridge BSc Thomas Maddox BSc Susan O’Brien MPhil Susannah Paisley BSc Octavio Paulo BSc Stephen Rossiter BSc Russell Seymour MSc Lisa Thurston BSc Saffron Townsend BSc
Scientific Publications and Meetings
ZSL Scientific Books EDITORS Peter Olney BSc DipEd CBiol FIBiol FLS Fiona A Fisken BSc ASSISTANT EDITOR Helen F Stanley PhD SALES ADMINISTRATOR Mychael Barratt (p/t)
ZSL Journals and Meetings MANAGING EDITOR Journal of Zoology Juliet Clutton-Brock PhD DSc EDITORS Ian Boyd PhD DSc Tim Halliday MA DPhil Philip S Rainbow PhD DSc
staff 29 Animal Conservation G M Mace (Editor) Animal Reproduction Science W V Holt (Member, Editorial Board) Behavioral Ecology A F G Bourke (Editor) Behaviour G Cowlishaw (Member, Editorial Board) British Andrology Society A Moore (Committee Member) British Veterinary Zoological Society E J Flach (Council Member) British Wildlife Rehabilitation Council A W Sainsbury (Member, Steering Committee) Centre for Ecology and Evolution (London) A F G Bourke, G M Mace, J M Rowcliffe representation representation and publications (Members, Steering Committee) Durrell Wildlife Conservation Trust G M Mace (Council Member; Member, Scientific Advisory Committee) European Commission Working Group on Transmissible Agents A A Cunningham (Member) Insectes Sociaux A F G Bourke (Member, Editorial Board) Institute of Biology W V Holt (ZSL representative) IUCN Cat Specialist Group S M Durant (Member) IUCN Declining Amphibian Population Task Force A A Cunningham (Chair, Pathology and Diseases Working Group) IUCN Species Survival Commission G M Mace (Member, Executive Committee) IUCN Species Survival Commission Conservation Breeding Specialist Group A A Cunningham, P M Bennett, E J Flach, G M Mace, A W Sainsbury (Members) IUCN Species Survival Commission Red List Committee G M Mace (Member) IUCN Species Survival Commission Reintroductions Specialist Group G M Mace (Member) IUCN Species Survival Commission Veterinary Specialist Group E J Flach, A W Sainsbury (Member) Marwell Zoological Park, Animal Heath and Welfare Committee A A Cunningham, E J Flach (Member) NERC Science and Technology Board G M Mace (Member) Primate Society of Great Britain G Cowlishaw (Council Member) Reproduction and Fertility W V Holt (Member, Editorial Board) Royal Society for the Protection of Birds G M Mace (Council Member) Society for Conservation Biology G M Mace (Member, Board of Governors) Society for Low Temperature Biology W V Holt (Committee Member) Society for the Study of Fertility A R Pickard (Committee Member) UK Pig Reproduction Research Liaison Group W V Holt (Committee Member) World Association of Wildlife Veterinarians A W Sainsbury (President)
30 representation AKÇAKAYA H R, FERSON S, BURGMAN M A, KEITH BVZS Spring Meeting. 13-14 May 2000: pp. 17-18. Conservation: pp. 172-197. (Eds L M Gosling & W J D A, MACE G M & TODD C R (2000). Making Sutherland). Cambridge University Press, Cambridge. consistent IUCN classifications under uncertainty. CURTIS D J, ZARAMODY A, GREEN D I & PICKARD A R Conservation Biology 14: 1001-1013. (2000). Non-invasive monitoring of reproductive status in FAZELI A, MOORE A & HOLT W V (2000). British wild mongoose lemurs (Eulemur mongoz). Reproduction Andrology Society’s Workshop: sperm interactions ALBON S D, COULSON T N, BROWN D, GUINESS F Fertility and Development 12: 21-29. with epithelia and their products. Human Fertility 3: E, CLUTTON-BROCK T H & PEMBERTON J M (2000). 166-171. Temporal changes in the key factors influencing the CURTIS D J, ZARAMODY A, GREEN D I & PICKARD A population dynamics of red deer. Journal of Animal R (2000). Non-invasive monitoring of reproductive FINCH A M, ANTIPATIS C, PICKARD A R & Ecology 69: 1096-1109. status in wild mongoose lemurs (Eulemur mongoz): an ASHWORTH C J (2000). Timing and prevalence of investigation of faecal steroid excretion patterns. runting in large white X landrace and Chinese meishan ARMBRUSTER P, HUTCHINSON R A & LINVEL T Proceedings of the European Federation of gilts. British Society of Animal Science Symposium on (2000). Equivalent inbreeding depression under Primatology (Zoological Society of London). 28-29 ‘Early Regulation of Mammalian Development’ laboratory and field conditions in a tree-hole-breeding November 2000. (Aberdeen, Scotland). 18-20 September 2000. mosquito. Proceedings of the Royal Society of London Series B 267: 1939-1945. DASZAK P & CUNNINGHAM A A (2000). Extinction FLACH E J, D’ALTERIO G-L, ZAHZAH K, MOLCANOVA R, by infection. Trends in Ecology and Evolution 14: 279. WAKEFIELD S, BAROSSI D, EULENBERGER K, KOPCOK M, BAKER P J, FUNK S M, HARRIS S & WHITE P C L (2000). OLLIVET F, PETIT T, VAHALA J & FRÖLICH K (2000). Flexible spatial organization of urban foxes, Vulpes DASZAK P & CUNNINGHAM A A (2000). More on the Veterinary monitoring of captive-bred scimitar-horned oryx vulpes, before and during an outbreak of sarcoptic ecological impact of fungal infections on wildlife (Oryx dammah) prior to reintroduction in Tunisia. mange. Animal Behaviour 59: 127-146. populations. Parasitology Today 16: 404-405. Proceedings of the 3rd Scientific Meeting of the European Association of Zoo and Wildlife Veterinarians (Paris). 31 BARKAI-RONAYNE A (2000). Retrospective analysis of DASZAK P & CUNNINGHAM A A (2000). A May - 4 June 2000: pp. 91-97. mortality records and population viability analysis of reassessment of ‘Maladaption syndrome’. 49th Annual trumpeter swans (Cygnus buccinator) in southern Wildlife Disease Association Meeting (Jackson Hole, FLACH E J, RILEY J, MUTLOW A G & McCANDLISH I Ontario. MSc Thesis, University of London. Wyoming, USA). 4-8 June 2000. A P (2000). Pentastomiasis in Bosc’s monitor lizards (Varanus exanthematicus) caused by an undescribed BAYES M K, SMITH K L, ALBERTS S C, ALTMANN J DASZAK P, CUNNINGHAM A A & HYATT A D (2000). sambonia species. Journal of Zoo and Wildlife & BRUFORD M W (2000). Testing the reliability of Emerging infectious diseases of wildlife - threats to Medicine 31(1): 91-95. microsatellite typing from faecal DNA in the savannah biodiversity and human health. Science 287: 443-449. baboon. Conservation Genetics 1: 173-176. FLACH E J, TAYLOR P, BROWN K & DODDS J (2000). DASZAK P, CUNNINGHAM A A & HYATT A D (2000). Immobilisation of giraffe with medetomidine and BILLINGTON S (2000). Extraction and semi- Conservation conundrum - Response. Science 288: 2320. ketamine. Proceedings of BVZS Autumn meeting, quantification of environmental Mycobacterium avium Exotic Animal Anaesthesia & Surgery, (ZSL). 20-21 at the Wildfowl and Wetlands Trust, Slimbridge, DASZAK P, CUNNINGHAM A A & HYATT A D (2000). November: pp. 55-57. using polymerase chain reaction. MSc Thesis, Emerging infectious diseases of wildlife: implications University of London. for human health. International Conference on GODFRAY H C J, MÜLLER C B & KRAAJIEVELD A R Emerging Infectious Diseases (ICEID 2000) (Atlanta, (2000). Habitat heterogeneity and the behavioural and CASEY S (2000). Conservation genetics of seahorses Georgia, USA). 16-19 July 2000. population ecology of host parasitoid interactions. In (Hippocampus species). PhD Thesis, University Ecological Effects of Habitat Heterogeneity: pp. 215- of London. DASZAK P, CUNNINGHAM A A & HYATT A D (2000). 236. (Eds M J Hutchings, A E John & A J A Stewart). Amphibian chytridiomycosis, emerging diseases and Blackwell Science, Oxford. CATCHPOLE E A, MORGAN B J T, COULSON T N, pathogen pollution. Getting the Jump! on amphibian FREEMAN S N & ALBON S D (2000). disease. International Conference on Amphibian GOLDSWORTHY C (2000). Study into the association Factors influencing Soay sheep survival. Applied Disease (Cairns, Australia). 26-30 August 2000. between chronic exposure to polychlorinated biphenyls Statistics 49: 453-472. and thymic involution and cystic change in harbour DASZAK P, CUNNINGHAM A A & HYATT A D (2000). porpoises (Phocoena phocoena) from British waters. CLAUSS M, FLACH E J, GHEBREMESKEL K, TACK C Amphibian chytridiomycosis. International Virtual MSc Thesis, University of London. & HATT J-M (2000). Supplementing the diet of Conference in Veterinary Medicine (University of captive giraffe (Giraffa camelopardalis) with linseed Georgia, Athens, USA). 16 October - 16 November GOOSSENS B, CHIKHI L, UTAMI SRI S, DE RUITER J extraction chips. In Zoo Animal Nutrition: pp. 271- 2000. & BRUFORD M W (2000). A multi-samples, multi- 279. (Eds J Nijboer, J-M Hatt, W Kaumanns, A extracts approach for microsatellite analysis of faecal Beijnen & V Ganslosser). Filander-Verlag, Fürth. DASZAK P, CUNNINGHAM A A & HYATT A D (2000). samples in an arboreal ape. Conservation Genetics 1: Viral emergence within the human–wildlife continuum. 175-162. COULSON T, MILNER-GULLAND E J & CLUTTON-BROCK T H Emergence and control of zoonotic ortho- (2000). The relative roles of density and climatic paramyxovirus diseases: an international symposium. GRENFELL B T, FINKENSTÄDT B F, WILSON K, variation on population dynamics and fecundity rates in Fondation Marcel Merieux. COULSON T N & CRAWLEY M J (2000). Nonlinearity three contrasting ungulate species. Proceedings of the and the Moran effect. Nature 406: 847. Royal Society of London Series B 267: 1771-1779. DASZAK P, CUNNINGHAM A A, BERGER L, HYATT A D, GREEN D E, SPEARE R & PORTER D (2000). GROOMBRIDGE J (2000). Conservation genetics of COWLISHAW G & DUNBAR R (2000). Primate Chytridiomycosis - the cause of amphibian population the Mauritius kestrel, pink pigeon and echo parakeet. Conservation Biology. Chicago University Press, Chicago. declines. Mycological Society of America Annual PhD Thesis, University of London. Meeting (Burlington, Vermont USA). 31 July - 3 CRANDALL K A, BININDA-EDMONDS O R P, August 2000. GROOMBRIDGE J J, JONES C G, BRUFORD M W & MACE G M & WAYNE R K (2000). Considering NICHOLS R A (2000). Conservation biology – ‘Ghost’ evolutionary processes in conservation biology. Trends DURANT S M (2000). Predator avoidance, breeding alleles of the Mauritius kestrel. Nature 403: 616. in Ecology and Evolution 15: 290-295. experience and reproductive success in endangered cheetahs, Acinonyx jubatus. Animal Behaviour 60: GURNELL J, GILRAY J, LURZ P, NETTLETON P, CUNNINGHAM A A, DASZAK P & HYATT A D (2000). 121-130. RUSHTON S, SAINSBURY A W (2000). Parapoxvirus Emerging infectious diseases and amphibian disease in red squirrels: is it responsible for the population declines. Proceedings of the BVZS Spring DURANT S M (2000). Living with the enemy: avoidance of demise of the red squirrel in Europe? 2nd Meeting. 13-14 May 2000: pp. 35-37. hyenas and lions by cheetahs in the Serengeti. Behavioral International colloquim of tree squirrels (Oregon, Ecology 11: 624-632. USA). May 2000. CUNNINGHAM A A, DASZAK P & HYATT A D (2000). Emerging infectious diseases of wildlife: implications DURANT S M (2000). Dispersal patterns, social for conservation & public health. Proceedings of the structure and population viability. In Behaviour and
publications 31 HILTON-TAYLOR C, MACE G M, CAPPER D R, MAR K U (2000). Life-table analysis of captive ferrumequinum). Proceedings of the Royal Society of COLLAR N J, STUART S N, BIBBY C J, POLLOCK C, working Asian elephants (Elephas maximus) of London Series B 267: 545-551. THOMSEN J B (2000). Assessment mismatches must Myanmar. MSc Thesis, University of London. be sorted out: they leave species at risk. Nature ROSSITER S J, JONES G, RANSOME R D & BARRATT E M Correspondence 404: 541. MAYER J (2000). Use of the geographic information (2000). Genetic variation and population structure in the system to investigate mercury levels in correlation with endangered greater horseshoe bat Rhinolophus HOLBROOK J D, BIRDSEY G M, YANG Z, BRUFORD post-mortem findings of Aspergillus induced lesions in ferrumequinum. Molecular Ecology 9: 1131-1135. M W & DANPURE C J (2000). Molecular adaption of the common loon (Gavia immer) in the northeastern alanine: glyoxylate aminotransferase targeting in United States of America. MSc Thesis, University SAINSBURY A W, NETTLETON P, GILRAY J & GURNELL J primates. Molecular Biology and Evolution 17(3): of London. (2000). Grey squirrels have a high seroprevalence to a 387-400. parapoxvirus associated with deaths in red squirrels. MILNER-GULLAND E J, COULSON T N & Animal Conservation 3: 229-233. HOLT W V (2000). Basic aspects of frozen storage of CLUTTON-BROCK T H (2000). On harvesting a semen. Animal Reproduction Science 62: 3-22. structured population. Oikos 88: 592-602. SAINSBURY A W, NETTLETON P, GILRAY J & GURNELL J (2000). Parapoxvirus infection: an emerging disease in HOLT W V (2000). Fundamental aspects of sperm NAIQUE S, PORTER R, CUNNINGHAM A A & red squirrels. Proceedings of the British Veterinary cryobiology: the importance of species and individual HUGHES S (2000). Scoliosis in an orang utan. The Zoological Society (Cotswold Wildlife Park, UK). differences. Theriogenology 53: 47-58. British Association of Clinical Anatomists Summer 13-14 May. 2000 Scientific Meeting (St John’s College, HYATT A D & CUNNINGHAM A A (2000). Cambridge). 20-21 July 2000. SAINSBURY A W, NETTLETON P F, GILARY J A, THOMAS K, Ranaviruses; a threat to amphibians? Getting the McINNES C & GURNELL J (2000). Grey squirrels have Jump! on amphibian diseases. International NETTLETON P F, GILRAY J, THOMAS K, MCINNES C, high seroprevalence to a parapoxvirus associated with Conference on Amphibian Disease (Cairns, Australia). SAINSBURY A W & GURNELL J (2000). Studies on a deaths in red squirrels. Association of Veterinary 26-30 August 2000. poxvirus from the European red squirrel (Sciurus Teachers and Research Workers Annual Conference vulgaris). Proceedings of the 5th International (Scarborough). April 2000. HYATT A D, GOULD A, COUPAR B, HENGTSBERGER Congress of the European Society for Veterinary S & CUNNINGHAM A (2000). Ranaviruses; diversity Virology, (Brescia, Italy). 27-30 August. SELISKAR A, FLACH E J, LUNA S P L & EATWOOD R and impact on commercial fisheries and piscine and (2000). Isoflurane anaesthesia in an Indian rhinoceros herpetological wildlife. 6th Australian Conference for O’KEEFE J (2000). Experimental investigation of the (Rhinoceros unicornis). Proceedings of the 7th World Electron Microscopy (ACEM), (Canberra). pp. 99-100. susceptibility and pathogenesis of West Nile Virus in Congress of Veterinary Anaesthesia, (Berne). 20-23 Mallards (Anas platyrhynchos). MSc Thesis, University September 2000. HYATT A D, GOULD A R, ZUPANOVIK Z, of London. CUNNINGHAM A A, HENGTSBERGER S, SEMPLE S & McCOMB K (2000). Perception of WHITTINGTON R J, KATTENBELT J & COUPAR B E H OWENS I P F & BENNETT P M (2000). Ecological basis of female reproductive state from vocal cues in a (2000). Comparative studies of piscine and amphibian extinction risk in birds: habitat loss versus human mammal species. Proceedings of the Royal Society of iridoviruses. Archives of Virology 145: 301-331. persecution and introduced predators. Proceedings of the London Series B 267: 707-712. National Academy of Sciences USA 97: 12144-12148. JEPSON P D, BAKER J R, KUIKEN T, SIMPSON V R, SMITH A T, BOITANI L, BIBBY C, BRACKETT D, KENNEDY S & BENNETT P M (2000). Pulmonary OWENS I P F & BENNETT P M (2000). Quantifying CORSI F, DA FONSECA G A B, GASCON C, DIXON M pathology of harbour porpoises (Phocoena phocoena) biodiversity: a phenotypic perspective. Conservation G, HILTON-TAYLOR C, MACE G, MITTERMEIER R A, stranded in England and Wales between 1990 and Biology 14: 1014-1022. RABINOVICH J, RICHARDSON B J, RYLANDS A, 1996. Veterinary Record 146: 721-728. STEIN B, STUART S, THOMSEN J & WILSON C PAUL R E L, COULSON T N, RAIBAUD A & BREY B T (2000). Databases tailored for biodiversity KELLY M J & DURANT S M (2000). Viability of the (2000). Erythropoietic sex determination in malaria conservation. Science 290: 2073. Serengeti cheetah population. Conservation Biology parasites. Science 287: 128-131. 14: 786-797. STRIKE T & PICKARD A (2000). Non-invasive PETTIFOR R A, CALDOW R W G, ROWCLIFFE J M, hormone analysis for reproductive monitoring in KENNEDY S, KUIKEN T, JEPSON P D, DEAVILLE R, GOSS-CUSTARD J D, BLACK J M, HODDER K H, female southern white rhinoceros (Ceratotherium FORSYTH M, BARRETT T, VAN DE BILT W G, OSTERHAUS A HOUSTON A I, LANG A & WEBB J (2000). Spatially simum simum). 2nd Annual Symposium on Zoo D M E, EYBATOV T, DUCK C, KYDYRMANOV A, explicit, individual based, behavioural models of the Research, Federation of Zoological Gardens of Great MITROFANOV I & WILSON S (2000). Mass die-off of annual cycle of two migratory goose populations. Britain & Ireland (Paignton Zoo, Devon). 6-7 July Caspian seals caused by canine distemper virus. Journal of Applied Ecology 37(S1): 103-135. 2000: pp. 191-197. Emerging Infectious Diseases 6: 637-639. PETTIFOR R A, NORRIS K N & ROWCLIFFE J M THURSTON L M (2000). An investigation into sources of KIFLAWI M, ENQUIST B J & JORDAN M A (2000). (2000). Incorporating behaviour in predictive models variation and the genetic basis of boar spermatozoa Position within the geographic range, relative local for conservation. In Behaviour and Conservation: pp. survival following cryopreservation. PhD Thesis, abundance and developmental instability. Ecography 198-220. (Eds L M Gosling & W J Sutherland). University of London. 23: 539-546. Cambridge University Press, Cambridge. THURSTON L M, SIGGINS K, MILEHAM A, WATSON P F & KILIAN S A R (2000). Assessment of reproduction in PICKARD A R (2000). Reproductive and welfare HOLT W V (2000). Identification of amplified restriction the Amur leopard (Panthera pardus orientalis). MSc monitoring for the management of captive populations. fragment length polymorphism (AFLP) markers linked to Thesis, University of London. Proceedings of the Zoological Society of London genes controlling boar sperm viability following Symposium ‘Reproduction and Integrated Conservation cryopreservation. Journal of Reproduction and Fertility LAFORTUNE M (2000). Clinical and cardiopulmonary Science’ (London). 9-10 November 2000. Abstract Series 25. evaluation of medetomidine, clove oil and propofol in leopard frogs (Rana pipiens). MSc Thesis, University PICKARD A R, ABAIGAR T, GREEN D I, HOLT W V & VAN WYK J W (2000). A retrospective study of the of London. CANO M (2000). Estrogen excretion as a prediction of pattern of iron storage in captive members of the order fertility in an exotic ungulate, the mohor gazelle Artiodactyla. MSc Thesis, University of London. LAWSON B (2000). The geographical distribution, (Gazella dama mhorr). Theriogenology 53: 343. natural history and pathology of parapoxvirus disease WANG J (2000). Effects of population structures and in red squirrels in the UK. MSc Thesis, University PICKARD A, DI MARCO F & PANKHURST S (2000). selection strategies on the purging of inbreeding of London. Monitoring stress in mara: preliminary findings of depression due to deleterious mutations. Genetical faecal cortisol analysis. 2nd Annual Symposium on Research 76: 75-86. MacDONALD D W, MACE G M & RUSHTON S (2000). Zoo Research, Federation of Zoological Gardens of British mammals: is there a radical future? In Great Britain & Ireland, (Paignton Zoo, Devon). 6-7 WANG J & HILL W G (2000). Marker-assisted Priorities for the Conservation of Mammalian Diversity July 2000: pp. 201-202. selection to increase effective population size by - Has the Panda had it’s day?: pp. 177-205. (Eds A reducing Mendelian segregation variance. Genetics Entwistle & N Dunstone). Cambridge University Press, PIZZI R (2000). Investigations of causes of mortality 154: 475-489. Cambridge. in British garden birds by post-mortem examination. MSc Thesis, University of London. WEBER M (2000). Effects of hunting on tropical deer MACE G M (2000). Summary of the results of the populations in South eastern Mexico. MSc Thesis, review of IUCN Red List categories and criteria 1996- PURVIS A, AGAPOW P-M, GITTLEMAN J L & MACE G M University of London. 2000. In 2000 IUCN Red List of Threatened Species: (2000). Nonrandom extinction and the loss of pp. 57-61. (Ed. C Hilton-Taylor). IUCN, Gland, evolutionary history. Science 288: 328-330. WESCHE P (2000). Isolation of Malassezia Switzerland. pachydermatis from the skin of captive White PURVIS A, GITTLEMAN J L, COWLISHAW G & MACE G M Rhinoceros (Cerathotherium simum simum), Black MACE G M & BALMFORD A (2000). Patterns and (2000). Predicting extinction risk in declining species. 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32 publications © 2001 The Institute of Zoology The Zoological Society of London Registered charity no. 208728
Thanks to the following for use of the photographs on p6/7 Gareth Jones, Bristol University, p8 Richard Cooke, p10 Sue Wilson, World Bank, p11 Seamus Kennedy, Dept. of Agriculture for Northern Ireland, p13 Tim Coulson, University of Cambridge, p14/15 Ian Owens, Imperial College, London, p17 Josephine Pemberton, University of Edinburgh, p21 Deborah Curtis, University of Surrey Roehampton, p27 James Gibbs.
Thanks also to Brian Aldrich, Helen Clarke, Guy Cowlishaw, Rob Deaville, Terry Dennett, Sarah Durant, Edmund Flach, Jo Gipps, Rob Hammond, Michael Lyster, Amanda Pickard and Lisa Thurston for photographs.
Edited by Helen F Stanley and Katrine Garn
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