REVIEW 2016-17 INSTITUTE OF ZOOLOGY ZOOLOGY OF INSTITUTE SCIENCE FOR CONSERVATION FOR SCIENCE

ZSL Institute of Zoology Review | 2016-17 Sambar deer (Rusa unicolor), Sariska National Park, India, location of the CONTENTS Interventions in Wildlife Health field course

Welcome 3 The Institute’s global reach 4 Institute news 6 Director’s intro 8

Impacts Making an impact 9 The ‘one health’ approach 10 Saving small populations from extinction 12 Wildlife microbiomes 14 Monitoring species through telemetry 16 Fostering coexistence between people and nature 18 Conservation genetics 20

Highlights Research 23 Research highlights 24 How our science is done 28 Education and training 30 ZSL Library 33 Communicating science 34 ZSL Scientific Awards 36 Funding 37 Governance and staff 38

2 ZSL Science Review 2016-17 zsl.org WELCOME

The President and Director General of the Zoological Society of London present the Institute of Zoology Review 2016-17.

s President of the Zoological Society of London, I am he Institute of Zoology is at the forefront of tackling the pleased to introduce the Institute of Zoology Annual Review. challenges faced by the world’s most seriously threatened One of the key successes of 2016 was the successful wildlife, developing new techniques and a deeper translocationA of hihi to the New Zealand mainland since their Tunderstanding of the issues at hand to help drive conservation disappearance from the area over a century ago. The Institute’s action across the globe. researchers have been working with hihi for over a decade, In 2016 our scientists made a step forward in the fight to eradicate alongside several conservation partners and the New Zealand fungal pathogens, such as chytrid fungus (Batrachochytrium Government, and the successful growth of hihi populations dendrobatidis), a disease that has devastated amphibian populations represents the project’s strong emphasis on planned research globally. A new study indicated that microbiome diversity could be a and theoretical frameworks. critical trait in predicting host resistance to disease, and research will Another area I am extremely proud of is our work to understand continue into whether microbiome diversity can weaken pathogens. and mitigate the effects of infectious pathogens on wildlife Meanwhile, our UK Cetacean Strandings Investigation Programme health. The increased pace of human activity – motorised continues to monitor strandings and put pressure on the UK transport, the encroachment of wildlife habitats and an expanding Government to speed up the destruction of polychlorinated biphenyls population – has exposed both wildlife and humans to infections (PCBs) through a variety of policy-focused reports. PCBs pose a major they have not previously contended with. Our major research in global threat to the future of marine apex predators, such as killer this area includes the discovery of snake fungal disease in Europe; whales, and the issue was widely covered in several broadsheet providing the scientific evidence demonstrating that culling of newspapers – bringing the toxic legacy of PCBs to public attention badgers increases the risk of bovine tuberculosis spillover to more than ever before. livestock; and a 10-year study into the ecology of pathogens We are dedicated to educating the scientists of the future, supporting carried by West African fruit bats. more than 100 PhD and master’s students, and we remain one of the ZSL’s Institute of Zoology remains at the cutting edge of world’s leading institutions for zoological study. We continue to run MSc developing conservation technology to address the long-term courses in Wild Animal Biology and Wild Animal Health, in collaboration issues facing wildlife. Genetic diversity is crucial to the future with the University of London’s Royal Veterinary College, and support survival of species, and the Institute has developed new software capacity building in developing nations through our ‘Interventions in to evaluate genetic diversity based on population size, as well Wildlife Health’ field course. Meanwhile, our Soapbox Science initiative as new methods for estimating individual relationships based provides a platform for women scientists to encourage greater diversity on genetic marker data. in the next generation of research scientists. This review presents six key impact areas in which our research Finally, as we look back at the past 12 months at the Institute, I must is making a difference to conservation and increasing our take this opportunity to announce my own retirement after 13 years at understanding of the natural world. Thank you to those involved, the helm of this incredible Society. ZSL’s Institute of Zoology is vital to whose tireless diligence makes our work possible. the future of our wildlife and it has been an honour to be a part of such an important organisation.

Professor Sir John Beddington CMG, FRS Ralph Armond President, Zoological Society of London Director General, Zoological Society of London

zsl.org ZSL Science Review 2016-17 3 GLOBAL REACH

The Institute’s global reach

A Iceland B United Kingdom The light-bellied brent goose (Branta bernicla Previously found in almost every county of England and Wales, the hrota) has one of the longest migratory journeys common dormouse (Muscardinus avellanarius) has undergone of any goose species, and spends most of May a marked decline over the past century. The Institute’s refuelling in Iceland before breeding in the High Disease Risk Analysis and Health Surveillance team Arctic. Institute researchers, in collaboration carries out essential research on disease management with the University of Exeter and the University for reintroduction, for example, screening dormice of Iceland, are using long-term ringing data to for pathogens that could present a health risk for the understand how differences in migratory route dormice themselves or other wildlife at the release and habitat use during the Icelandic staging site. In 2016, in partnership with the People’s Trust for period can influence individual reproductive Endangered Species and Natural England, 38 dormice success. Understanding how individuals use were released into managed woodland in the Yorkshire foraging resources across their entire annual Dales National Park. range, and how these patterns drive variation in breeding success, has important implications for the management of threatened populations in the wild.

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C Mauritius Only 25 years ago, fewer than 20 echo parakeets (Psittacula eques) remained in the wild after widespread habitat loss and increasing competition with introduced, exotic species. Through the intense work of the Mauritian Wildlife Foundation, the population has now increased to almost 600 wild birds. Institute research is examining the underlying demography of the population and, in particular, its response to environmental conditions, disease and management actions, to ensure a long- term, viable population. To find out more about our current research projects, visit zsl.org/science/research

4 ZSL Science Review 2016-17 zsl.org Institute of Zoology research is truly international. Each dot on the map represents at least one project. Here, we highlight six projects that illustrate the breadth of our work.

D Spain E Namibia The Institute has partnered with the Spanish National Ephemeral rivers are fundamental to Research Council for almost 20 years, investigating biodiversity in arid lands. Although dry and the geographic distributions and impacts of emergent sandy for most of the year, their groundwater viral and fungal diseases of amphibians. Our work has supports riparian woodlands, which act as identified species and amphibian habitats most at risk a linear oasis, providing food and shelter of ranavirus and chytridiomycosis, the diseases that to a wide variety of desert animals, as well as most threaten Europe’s amphibian biodiversity. We natural resources to local people. However, have been developing strategies to mitigate disease these unique ecosystems are under threat. In impacts, including characterising skin microbial Namibia, we have been investigating widespread communities that can help amphibians fend off and decline among the riparian trees of the Swakop River, one of the clear infections, and applying antifungal and antiviral country’s most important rivers (and on which our Tsaobis Baboon interventions that have, in some cases, cleared Project is based). Our results suggest that damming is largely infections from isolated amphibian populations. responsible, but that the management of tributary flows may help Our goal is to ensure the survival of the novel and to alleviate local impacts. highly endemic Spanish amphibian species community in the face of F New Zealand an ever-expanding repertoire of The New Zealand fairy tern (Sternula threatening infectious diseases. nereis) is New Zealand’s rarest bird. Only 39 adult individuals remain and this tiny population is facing a range of threats, including human encroachment on breeding habitat and predation from non-native mammalian species. A recent evaluation of past recovery actions has called for more aggressive strategies that may promote recovery, but that are also risky. This includes translocation to establish breeding colonies in areas protected from predators and away from beachfront development. Institute researchers are working closely with the Department of Conservation in New Zealand to compare alternative recovery strategies, thus allowing an evidence-based choice of management that provides the best chance for population recovery.

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zsl.org ZSL Science Review 2016-17 5 NEWS Institute news Over the past year, Institute research has continued to improve our understanding of the natural world and advance a range of important conservation issues. ▼ Below: (left to right) Laura Bellingan, Elaine King, Sir John Beddington CMG FRS, Graeme Reid and Sue Hartley Hihi highlights ▼ Our conservation efforts with New Zealand hihi (Notiomystis cincta) have continued to reap rewards over the past year. An exceptionally successful breeding season in the reintroduced population on Tiritiri Matangi Island, which ZSL manages via a contract from the New Zealand Department of Conservation, resulted in 40 juvenile birds being translocated to a new site in the Taranaki Region of the North Island – Rotokare Scenic Reserve. This is the first time hihi have been in the region since their local extinction 130 years ago. The efforts of ZSL and the multiple conservation partners we work with in New Zealand have resulted in a growth of hihi populations Making Brexit work for Beddington CMG FRS, Professor Sue Hartley, from one offshore island remnant in the conservation science ▲ Dr Elaine King and Professor Graeme Reid, early 1980s to an extra six reintroduced In September ZSL held the event ‘Making focused on the key role science plays in populations spread across northern Brexit work for ecology and conservation the UK to help society address current New Zealand by 2017. The Institute’s science’, in collaboration with the British and upcoming environmental challenges, John Ewen co-chairs the recovery team Ecological Society, the Campaign for making the point that the UK has a world- for this species and ZSL has recently Science and Engineering, the Royal Society class scientific community capable of co-published the project’s first formal of Biology, and Wildlife and Countryside informing governmental decisions in annual review. Link. Speakers, including Professor Sir John the face of environmental uncertainty.

Mauritius Partnership Meeting ▶ In June, various partners involved in a wide range of conservation programmes in Mauritius met to review progress and plan future work. The meeting covered endangered species recovery, island restoration and the control of non-native predators. Outcomes from the meeting include a plan for a new conservation breeding and release project to boost numbers of Mauritius kestrel (Falco punctatus), which will be supported by staff from ZSL London Zoo; a network of zoos that are helping breed pink pigeons (Nesoenas mayeri) in captivity for ultimate release into the wild; and an ambitious idea to create a predator-free ‘island’ on the mainland of Mauritius, to protect olive white-eyes (Zosterops chloronothos) and other threatened birds and reptiles.

◀ Left: Hihi (Notiomystis cincta) ▶ Right: Round Island petrel (Pterodroma arminjoniana)

6 ZSL Science Review 2016-17 zsl.org Keep up to date with all the latest Institute news and breakthroughs at zsl.org/science/news

◀ Soapbox Science The 2017 season of Soapbox Science, our public outreach platform for promoting women scientists, was our biggest year to date, with 19 events across the globe, including new events in Canada, Germany and Ireland. Soapbox Science, founded in 2011 by Seirian Sumner, University College London, and the Institute’s Nathalie Pettorelli, transforms public spaces into arenas for public learning and scientific debate, giving everyone the opportunity to interact with, and be inspired by, leading women scientists.

◀ Left: Institute researcher Jenny Jaffe at Soapbox Science

◀ Royal College of Veterinary Surgeons Fellowship Congratulations are due to Andrew Cunningham (right, accepting award), who has been elected Fellow of the Royal College of Veterinary Surgeons. This prestigious accolade is awarded in recognition of outstanding contribution to the veterinary profession. Following 28 years of conducting world-class science, Andrew received the Fellowship for his ‘meritorious contributions to knowledge’. In the mid-1990s Andrew led the groundbreaking multidisciplinary team that identified one of the greatest emerging threats to amphibian populations worldwide – the Batrachochytrium dendrobatidis fungus. Andrew’s research includes the identification of vulture declines in South Asia, the discovery of ranavirus disease of amphibians in Europe and the spillover of zoonotic pathogens from bats in West Africa.

▲ From PhD to Parliament and the Royal Society PhD student Dani Rabaiotti was lucky enough to undertake two policy placements during the past year: one in the Parliamentary Office of Science and Technology (POST), funded through the British Ecological Society, and one at the Royal Society, funded by the Natural Environment Research Council. While working in Parliament Dani prepared a research summary, known as a POSTnote, on environmental crime and organised an event for MPs to discuss environmental crime with experts. At the Royal Society, Dani helped the policy team with its work on genetic technologies. These placements offer an excellent opportunity for researchers to learn about how Parliament and wider science policy work.

zsl.org ZSL Science Review 2016-17 7 DIRECTOR’S INTRO

Science offers real hope for wildlife conservation Director of Science Professor Ken Norris recognises the devastating environmental impact of human activity, but argues that conservation is making a difference.

elcome to the Anthropocene. Human impacts on the natural world are now so huge that we have our own epoch. This is the first time in the Earth’s history that a single species Whas defined a geological era. The evidence of our impacts is both overwhelming and terrifying, as revealed in our most recent Living Planet Report. The nature conservation challenges we face as a result are global and daunting. But all hope is not lost. Evidence is emerging that shows conservation action can reduce human impacts. Global analyses have demonstrated that conservation has slowed down the rate of wildlife losses, which would have been more severe had conservationists not intervened. It is often important in human medicine to slow down the progress of a disease sufficiently for a patient to lead a relatively normal life, irrespective of whether a cure is possible. Conservation is no different. Progress is being made.

Saving species from extinction In a few places, human impacts have been The Endangered pink pigeon sufficiently reduced to improve the conservation (Nesoenas mayeri) from status of threatened species. We are involved in Mauritius has been the subject two of these places – Mauritius and New Zealand. of an intensive recovery Here, intensive conservation work is restoring programme for more than some of the most threatened wildlife in the world. 30 years. As result, the species We are quite literally helping bring back species has been restored from around from the very brink of extinction. You can read six birds in one location about our work on threatened species on page to 400 birds split between 12 in this report. Mauritius is remarkable in that it six subpopulations on is one of only a few countries that improved the mainland Mauritius. status of its wildlife in recent years. Conservation In collaboration with the can make a difference – a big difference – and Mauritian Wildlife Foundation, we are beginning to understand the factors that Institute researchers are now define conservation success, so we can improve. undertaking a telemetry study The trajectory is upwards. to understand pink pigeon Earlier this year, we were part of the habitat use and identify Conservation Optimism Summit. This meeting movement corridors between brought people together to understand and subpopulations to inform celebrate the very real difference conservation long-term conservation has made to wildlife and people around the management strategies. world. The challenges we face are daunting, but we know how to succeed. Don’t lose hope!

To learn more about the IoZ’s conservation science, visit zsl.org/science

8 ZSL Science Review 2016-17 zsl.org African wild dog (Lycaon pictus)

Making an impact In the pages that follow, we highlight a selection of Impact Areas where our research is making a difference. From the management of small populations to understanding wildlife microbiomes, monitoring the status of the world’s biodiversity to a ‘one health’ approach to wildlife and human health, our work is continually advancing conservation science.

The ‘one health’ Saving Wildlife Monitoring Coexistence Conservation approach populations microbiomes species through between people genetics 10 from extinction 14 telemetry and nature 20 12 16 18

zsl.org 9 IMPACT AREAS

The ‘one health’ approach Infectious pathogens harboured by wildlife are a threat to both human and animal health – Institute researchers are finding solutions.

ver recent decades, there has species (for example, turning to bats been a growing realisation of the for bushmeat in the absence of larger importance of infectious agents animals that have been depleted due to O(or pathogens) harboured by wildlife, and overhunting), our exposure to new wildlife their effects on both wildlife populations pathogens has increased. and public health (Cunningham et al. 2017). At the same time, motorised transport Although wildlife pathogens have caused and increased human population densities disease in wild animals for millennia, provide new opportunities for human- human activities are increasingly enabling to-human transmission and spread of these to become a conservation threat. novel pathogens. Infected people are This can be through the reduction in size now able to reach towns, cities and hospitals The IoZ carried of wild animal populations to a level where prior to recovery or death, and the volume out a 10-year disease becomes significant to their survival and speed of international travel allows study into pathogens or, more dramatically, when people (usually pathogens to spread even before the first carried by West inadvertently) transport pathogens to new signs of disease are detected. African fruit bats areas, exposing and infecting populations and species that have not naturally evolved Tackling the root of the problem with the infection. As people move wild Clearly, these two issues, of disease threats animals and wild animal products, and to wildlife conservation and to public health, therefore wild animal pathogens, in increasing are interconnected and require a common volumes and at greater speeds around the mitigation approach that tackles the root al. 1998). In the UK, our researchers recently world, disease is occurring – and being of the problem (Cunningham et al. 2017). discovered finch trichomonosis, caused recognised as a growing threat to species Such an approach, often termed ‘one health’, by the protozoan parasite jumping from conservation (Cunningham et al. 2017). ‘ecohealth’ or ‘planetary health’, has been pigeons and doves to finches, and showed It is not just wild animals that are at risk a key focus of Institute research for many this is causing sudden and rapid population from wildlife pathogens. These years, and it is gaining public declines of the greenfinch (Chloris chloris) diseases can cross over into and political attention. (Lawson et al. 2012). other species, including We have a long and livestock and people successful history Minimising the risk of spillover (Cunningham et al. of diagnosing From a public health perspective, our 2017). Indeed, as we where disease is research aims to understand the host- have learned to a conservation pathogen-human system, including combat and control threat, identifying the ecology of the pathogen in nature. diseases natural to the causes and Knowledge of pathogen infection dynamics human beings – as underlying drivers in the natural host(s) can be used to inform well as those such of such diseases, the modification of human behaviours to as measles that we and developing minimise zoonotic spillover risk. Working acquired from our food mitigation methods in collaboratively with social scientists is and companion animals captivity and in the wild. often essential to understanding human around the time of For example, in the 1990s, behaviours and motivations and how to domestication – we are faced the Institute led the international implement solutions (Wood et al. 2012). with the prospect of dealing with new consortium of scientists who discovered the Our work in this field is exemplified by diseases spilling over into people from non-hyphal chytrid fungus Batrachochytrium research to understand the significance wildlife. Such spillover has been ever dendrobatidis as a cause of amphibian of badgers (Meles meles) as hosts of bovine present, but as we encroach further into disease, and showed that this disease is tuberculosis and the factors that increase remaining wildlife habitats, and as we causing multi-species amphibian population the likelihood of spillover to livestock (and interact with many previously ignored declines and extinctions globally (Berger et eventually to people). Institute scientists and

10 ZSL Science Review 2016-17 zsl.org Main image: research on West African fruit bats Inset left: Institute scientists found that culling badgers For further information, contact Andrew improves understanding of public health risks increased the spread of bovine tuberculosis Cunningham: [email protected]

humans to coexist (Wood et al. 2012; Wood et al. 2016). Future work in this area will include research to better understand the impacts of viral infections on the bats and how these infections can persist over time in their host populations. ‘One health’ was the subject of a special issue of the journal Philosophical Transactions of the Royal Society B: Biological Sciences, published in June 2017 and edited by the Institute’s Andrew Cunningham along with Ian Scoones (Institute of Development Studies) and James Wood (University of Cambridge). This special issue, entitled One Health for a changing world: zoonoses, ecosystems and human well-being, brought together a wide range of natural and social scientists to examine how well one health is working for conservation, livestock and public health, where it is failing and to identify priorities for further research. All papers in the special issue are available free online at rstb.royalsociety publishing.org/content/372/1725. collaborators found that the control measure of proactive culling of badgers actually References increases the rate of spread and likelihood of Berger, L, Speare, R, of the National Academy of Wood, JLN, Cunningham, spillover; an important result for informing Daszak, P, Greene, DE, Sciences of the United States AA, Suu-Ire, RD, Jephcott, mitigation measures that will actually work Cunningham, AA, Goggin, of America 111: 9193-9198 FL and Ntiamoa-Baidu, Y (Bielby et al. 2014). CL, Slocombe, R, Ragan, (2016) Ebola, bats and MA, Hyatt, AD, McDonald, Cunningham, AA, Daszak, P evidence-based policy. Public health risks KR, Hines, HB, Lips, KR, and Wood, JLN (2017) EcoHealth 13: 9-11 In collaboration with the University of Marantelli, G and Parkes, H One Health, emerging Cambridge, we have carried out a 10-year (1998) Chytridiomycosis infectious diseases and Wood, JLN, Leach, M, study into the ecology of viral pathogens causes amphibian wildlife: two decades of Waldman, L, MacGregor, H, carried by West African fruit bats, such as mortality associated with progress? Philosophical Fooks, AR, Jones, K, the straw-coloured fruit bat (Eidolon helvum). population declines in Transactions of the Restif, O, Dechmann, D, Fruit bats are often termed ‘keystone the rain forests of Australia Royal Society, Series B. Hayman, DTS, Baker, KS, species’ because of their importance for the and Central America. 372: 20160167 Peel, AJ, Kamins, AO, maintenance of ecosystem structure and Proceedings of the National Fahr, J, Ntiamoa-Baidu, function. Without these bats dispersing seeds Academy of Sciences of the Lawson, B, Robinson, RA, Y, Suu-Ire, R, Breiman, and pollinating forest and orchard trees, our United States of America Colvile, KM, Peck, KM, RF, Epstein, J and diet would be depleted of many fruits, and 95: 9031-9036 Chantrey, J, Pennycott, TW, Cunningham, AA (2012) tropical forests would fail to regenerate in Simpson, VR, Toms, MP and A framework for the their current form. Bielby, J, Donnelly, CA, Cunningham, AA (2012) The study of zoonotic disease By understanding the ecology of Pope, LC, Burke, T and emergence and spread of emergence and its pathogens such as rabies and Ebola viruses Woodroffe, R (2014) Badger finch trichomonosis in the drivers: spillover of bat in their natural bat hosts, and the interactions responses to small-scale British Isles. Philosophical pathogens as a case study. between bats and people that lead to human culling may compromise Transactions of the Royal Philosophical Transactions infection, we hope to find ways of minimising targeted control of bovine Society, Series B. 367: of the Royal Society, Series public health risks – allowing bats and tuberculosis. Proceedings 2852-2863 B. 367: 2881-2892

zsl.org ZSL Science Review 2016-17 11 IMPACT AREAS

Saving small populations from extinction The Institute’s work is safeguarding some of the world’s most vulnerable and threatened small populations.

n the face of unprecedented biodiversity We are working with colleagues in losses, effective strategies for saving small China to provide the scientific information populations from extinction are urgently needed for informed conservation decisions. Irequired. Among conservationists there is This includes improving estimates of the almost universal agreement on the need spatiotemporal requirements of Hainan for evidence-based management decisions gibbon social groups, suggesting that habitat and for science that supports conservation availability may not be the current driver of decision-making. However, management of poor population growth (Bryant et al. 2017). small populations remains primarily based Through field monitoring using acoustic on the application of experience without call playback methods, Bryant et al (2016a) careful evaluation of evidence. discovered an additional small social group For management to be truly evidence- of Hainan gibbons. This amazing discovery the probability that individuals recruit into based the science should seek to provide increased the known number of breeding- establishing populations (Richardson et information that will help in choosing age female Hainan gibbons from five to six al. 2016). Importantly, all reintroduced hihi management actions. In general, science can individuals. Additional breeding individuals populations require substantial support, support management by firstly predicting the are critically important and provide more including supplementary feeding. Our consequences of management actions based options for interventions to manage the most recent work shows that the benefits on available evidence; secondly, reducing extremely high rates of inbreeding and of supplementary food are equally strong uncertainty around choices between reduced genetic diversity also revealed even when hihi are released into mature and alternative actions; and, finally, providing by Bryant et al (2016b). pristine forest (Doerr et al. 2017), a finding specialist tools to help select the best action that continues to improve our understanding for a given set of objectives. Hihi conservation in of their habitat needs and the beneficial Institute researchers aim to inform New Zealand roles supportive management can provide. small population recovery in a variety of The hihi (Notiomystis cincta) is an endemic ways – for example, we have predicted the and threatened passerine of New Zealand. Wolf conservation in Europe consequences of supplementary feeding Institute researchers have been working The science support we provide to (Ewen et al. 2015) and predator control with hihi for well over a decade, providing management decisions is often closer (Maggs et al. 2015), reduced uncertainties a substantial level of science and decision to home. Carbon reduction is of growing around the effectiveness of disease support to their continued recovery. From a environmental importance and Europe is management (Hudson et al. 2016) and low point of a single remaining population addressing this by considering changes helped select the best management on an offshore island, the hihi is now found in how energy is produced. Wind farming option under risk aversion (Canessa et al. spread across this remnant island and in is one attractive alternative, yet the 2016). The evidence support we provide six additional reintroduced populations. infrastructure associated with wind farms is frequently done in a highly collaborative Some of these reintroduced can be damaging to small and way, embedding our science directly populations are on the threatened populations, into management, working alongside mainland of New Zealand including wide-ranging local partners. and are thus exposed carnivores, such as to population wolves (Canis lupus). Hainan gibbon conservation establishment Institute research in China challenges linked has provided a The Hainan gibbon (Nomascus hainanus) to dispersal from decision support is possibly the world’s rarest mammal, protected areas. framework offering with only 25 individuals known in the wild. Our research an optimal trade-off This level of rarity is important not only is showing between energy for the management of a species on the how individual capacity and overlap verge of extinction, but also because we temperament with critical wolf have very limited knowledge of the predicts dispersal reproduction habitat in species’ ecology. distances and can shape Croatia (Passoni et al. 2017).

12 ZSL Science Review 2016-17 zsl.org Main image: Institute researchers and their Chinese colleagues have discovered a new social group of rare Hainan gibbons. Below left: the Institute has successfully reintroduced populations of hihi in New Zealand. Below right: wind-farming infrastructure is damaging wolf populations

For further information, contact John Ewen: [email protected]

References Bryant, JV, Brule, A, Wong, feeding in species MHG, Hong, X, Zhou, Z, Han, conservation. Conservation W, Jeffree, TE and Turvey, ST Biology 29: 341-349 (2016a) Detection of a new Hainan gibbon (Nomascus Hudson, MA, Young, RP, hainanus) group using D’Urban Jackson, J, Orozco- acoustic call playback. Terwengel, P, Martin, L, International Journal of James, A, Sulton, M, Garcia, Primatalogy 37: 534–54 G, Griffiths, RA, Thomas, R, Magin, C, Bruford, MW and Bryant, JV, Gottelli, D, Zeng, Cunningham, AA (2016) X, Hong, X, Chan, BPL, Dynamics and genetics of Fellowes, JR, Zhang, Y, Luo, a disease-driven species J, Durrant, C, Geissmann, T, decline to near extinction: Chatterjee, HJ and Turvey, lessons for conservation. ST (2016b) Assessing current Scientific Reports 6: 30772 genetic status of the Hainan gibbon using historical and Maggs, G, Nicoll, M, Zuël, demographic baselines: N, White, PJC, Winfield, E, implications for conservation Poongavanan, S, Tatayah, management of species of V, Jones, C and Norris, K The Hainan gibbon extreme rarity. Molecular (2015) Rattus management This work shows how science tools can help is possibly the world’s Ecology 25: 3540-3556 is essential for population resolve complicated and often conflicted rarest mammal, with persistence in a Critically conservation objectives. only 25 individuals Bryant, JV, Zeng, X, Hong, X, Endangered passerine: known in the wild Chatterjee, HJ, and Turvey, combining small-scale field Science support for recovering ST (2017) Spatiotemporal experiments and population small populations requirements of the Hainan modelling. Biological Conservationists recognise the absolute gibbon: Does home range Conservation 191: 274-281 need for evidence-based conservation constrain recovery of the action; however, the scientific support that world’s rarest ape? American Passoni, G, Rowcliffe, JM, provides this often fails to truly influence Journal of Primatology Whiteman, A, Huber, D decisions. It is important we understand 79: e22617 and Kusak, J (2017) why this happens, and our work is providing Framework for strategic leading insights on this issue. For example, Canessa, S, Guillera-Arroita, wind farm site prioritisation Taylor et al (2017) investigated how well G, Lahoz-Monfort, JJ, based on modelled wolf science supported management within Southwell, DM, Armstrong, reproduction habitat in reintroduction biology, finding that most DP, Chadès, I, Lacy, RC and Croatia. European Journal research failed to clearly assist the choice Converse, SJ (2016) Adaptive of Wildlife Research 63: 38 among alternative management actions, management for improving which is the ultimate requirement of science species conservation across Richardson, KM, Ewen, support to conservation. Our research the captive-wild spectrum. JG, Brekke, P, Doerr, LR, suggests that changes need to occur in what Biological Conservation Parker, KA and Armstrong, conservation science is done (developing a 199: 123-131 DP (2016) Behaviour during more holistic understanding of population handling predicts male recovery) and in how it responds to Doerr, LR, Richardson, KM, natal dispersal distances management needs (by directly Ewen, JG and Armstrong, in an establishing embedding within decision-making). DP (2017) Effect of reintroduced hihi Conservation science should supplementary feeding on (Notiomystis cincta) target uncertainties that are reproductive success of population. Animal relevant for management, hihi (Stitchbird, Notiomystis Conservation 20: 135-143 explicitly comparing the cincta) at a mature forest expected outcomes of reintroduction site. New Taylor, G, Canessa, S, Clarke, alternative actions, and Zealand Journal of Ecology RH, Ingwersen, D, Armstrong, managing adaptively rather 41: 34-40 DP, Seddon, PJ and Ewen, than by trial and error. In doing JG (2017) Is reintroduction so we stand to reap substantial Ewen, JG, Walker, L, Canessa, biology an effective applied rewards through the successful S and Groombridge, JJ (2015) science? Trends in Ecology recovery of threatened species. Improving supplementary and Evolution 32: 873-880

zsl.org ZSL Science Review 2016-17 13 IMPACT AREAS

Wildlife microbiomes Institute research is advancing our understanding of the complex microbial communities essential to the health of species and ecosystems.

icroscopic organisms are found and what consequences this variation has everywhere on Earth: in soils, for disease resistance. oceans and living in association New research led by the Institute Mwith animal and plant hosts. Complex has revealed that common frogs (Rana microbial communities, known as the temporaria) living in habitats with greater ‘microbiome’, play an essential role in bacterial diversity in turn had more diverse maintaining the health of both individual skin microbiomes. More importantly, frogs species and entire ecosystems. with more diverse microbiomes were less In animals, the microbiome underpins susceptible to the lethal pathogen ranavirus. a myriad of physiological processes In a separate study, we have shown that critical to host health, including midwife toads (Alytes obstetricians) metabolism, digestion, in populations suffering optimal immune system more severe outbreaks function and protection of Bd, characterised from pathogens. by rapid population Understanding the declines, exhibited links between the lower microbiome microbiome and diversity compared animal health to populations can help us to suffering milder Bd tackle a broad infection dynamics. range of global Thus, microbiome conservation diversity appears challenges. Institute to be a critical trait in scientists are conducting predicting host resistance groundbreaking research to disease and disease into the fundamental science of dynamics, and colonisation host-microbiome interactions, how of the host by bacteria living in the these principles can be applied to issues environment may be a crucial process such as global population declines caused determining that diversity. Future research by wildlife disease, and how best to manage will probe the mechanistic basis of these links threatened populations. between microbiome diversity and disease for wildlife disease. Previous work has resistance. For example, we will use both demonstrated that the ability of a single Interaction between shotgun metagenomics and metabolomics probiotic bacterium to inhibit Bd is not microbiome and to understand whether increased consistent across multiple variants of chytrid wildlife pathogens microbiome diversity also results in a greater isolated from separate geographic locations. Infectious diseases are responsible for the diversity of bacterially derived metabolites By adopting a community-level approach decline of amphibian biodiversity around that may directly attenuate the pathogen. to probiotic development, we have the globe. These declines have largely demonstrated that using a combination been caused by fungal pathogens such Bacterial probiotics to of multiple bacterial isolates as a single as Batrachochytrium dendrobatidis (Bd) mitigate wildlife disease ‘consortium probiotic’ yields broader- and Batrachochytrium salamandrivorans, A novel tool for the mitigation of wildlife spectrum inhibition of Bd compared to and the virus ranavirus. The amphibian disease involves the augmentation of the single bacteria. This research highlights the skin microbiome can defend the host host microbiome with bacteria known possibility that bacterial consortia may offer against these pathogens, and so it is vital to inhibit the growth of the pathogen. a more robust tool for the probiotic inhibition that we understand what drives variation The Institute plays a leading role in the of wildlife diseases, such as chytridiomycosis, among individuals in their microbiome, development of probiotic treatments in the wild.

14 ZSL Science Review 2016-17 zsl.org Main image and inset: light-bellied brent geese Left: Institute scientists are studying the European For further information, contact Xavier Harrison: can help us understand the link between the gut common frog to explore how the amphibian [email protected] microbiome and nutritional health skin microbiome protects against disease

Linking gut microbiome to hrota) as a model allow individuals nutrition and physiology system. Migratory to specialise on Bacteria living in animal digestive tracts have brent geese use different food enormous potential to impact host health fat reserves stored sources by providing and physiology by controlling the efficiency of during the spring a pre-adapted energy metabolism from food. There is now staging period in metabolic toolkit growing interest in the idea that differences Iceland to finance digestion of specific among individuals in their gut microbiomes the energetic cost nutrients. Results may underpin the differences we observe in of reproduction in the from this study will have the wild in animal body condition and health, Canadian Arctic. Thus, geese marked implications for our and the extent to which individuals are able able to liberate more energy management of wildlife populations. to specialise on different food resources. from food can store more fat and lay more For example, we may be able to improve The Institute is leading a novel research eggs. This study will probe the mechanistic the health of animals translocated to new programme to understand the links between link between gut microbiome composition areas by administering probiotics that gut microbiome and nutritional health, using and ability to maximise energy metabolism, will optimise their ability to digest local food/ the light-bellied brent goose (Branta bernicla and how differences in microbiome may prey items.

zsl.org ZSL Science Review 2016-17 15 IMPACT AREAS

Monitoring species through telemetry Tracking technologies are revolutionising how we monitor populations, allowing us to record high-resolution data on the behaviour and movements of animals. Institute researchers lead the way in combining telemetry and novel analyses for conservation.

nderstanding the long-term behaviour number of less precise, but cheaper, devices to thrive, but these are also some of the of animals in their natural habitat is such as geolocation or acoustic tags? In hardest places to monitor species. This crucial for effective conservation. The recent years, research at the Institute has challenge is epitomised through our research Udevelopment of smaller, cheaper and more demonstrated how more information can be on species that occupy the marine realm, powerful tracking equipment is enhancing extracted from both high- and low-resolution particularly as the remote nature of some of the scale and variety of species that can be devices using novel machine learning these locations makes them susceptible to monitored across the globe. methods – the automated recognition of unregulated activity, such as illegal fishing. This increasing sophistication of tag design patterns in big data by computers – as an Spatial network analyses that quantify is transforming species conservation from important tool for conservation. how animals link different habitats, in determining simply where and when species A priority for developing these machine combination with electronic monitoring, are present to understanding and predicting learning tools is to better measure the offer a broad set of analytical tools that help how changes in the environment and ecology interaction of wide-ranging animals with us to assess the efficacy of protected areas of species drive patterns of distribution. one another and their local environments in for highly mobile species such as sharks and The volume and richness of data available order to understand the broad and complex seabirds. Developments in these tools, and from animal-borne data devices require drivers of population dynamics. Our recent how they are likely to contribute to improved increasingly versatile and powerful tools to work in this area revealed that patterns of conservation strategies, were recently extract and interpret this vital information; global wind speed and direction obtained assembled in a comprehensive review Institute research continues to play a leading via remote sensing can be used to predict (Jacoby and Freeman 2016). role in advancing both tagging and analytics the behaviour and movement energetics in for improved species conservation. a wide-ranging seabird, the Manx shearwater From tags to targets (Gibb et al. 2017). Alongside their application for conservation Inferring behaviour through Machine learning methods in the marine management, these sophisticated machine learning approaches environment can play a significant role in monitoring tools can have broader use in The Institute currently monitors a host of species conservation. For fish species that assessments of species extinction risk and populations using a broad range of tracking rarely surface and for which it is therefore in feeding into global biodiversity indicators technologies. These include, but are not difficult to obtain frequent satellite positions, (eg estimating changes in population size, limited to, acoustic transmitters on sharks in acoustic transmitters and receivers provide range size or the impact of specific threats). Palmyra (Central Pacific Ocean), the Chagos coarse residency and space-use patterns. Indicator development for the Sampled Archipelago (Central Indian Ocean) and the Recently, we developed a widely applicable Red List Index and Living Planet Index Bahamas; light-based geolocation tags on method for inferring social interactions relies on monitoring data but often lacks seabirds in the UK, Chagos and Mauritius; from acoustic telemetry data, enabling us information for difficult-to-monitor species and our own open-source, low-cost GPS to establish patterns of social leadership in remote locations. Improvements in trackers (Mataki tags) deployed on tigers behaviour in a population of grey reef sharks telemetry to monitor populations could (Panthera t. tigris) in India, pygmy three-toed (Carcharhinus amblyrhynchos) at a remote help fill gaps in our knowledge of biodiversity sloths (Bradypus pygmaeus) in Panama, atoll in the Pacific Ocean (Jacoby et al. trends worldwide. Manx shearwaters (Puffinus puffinus) in the 2016). It is hoped that behavioural inference Our research is at the forefront of UK, and a variety of large carnivores in Africa. at the population level will ensure that communicating global biodiversity trends Typically, researchers and conservationists characteristics, such as a species’ tendency (eg McRae et al. 2016), developing indicators wishing to employ telemetry to monitor to aggregate or move in a specific way, can for policy used to measure progress towards species have faced a trade-off; with limited be built into future vulnerability assessments. international biodiversity targets. These budget, should one favour a small number advances in biodiversity monitoring therefore of sophisticated, often satellite-linked and Applied telemetry contribute not only to single-species expensive electronic tags that give high Remote refuges can provide wilderness areas management, but to the conservation of spatial and temporal resolution, or a larger where we might expect animal populations biodiversity more broadly.

16 ZSL Science Review 2016-17 zsl.org Below: data from remote sensing can help predict the acoustic transmitters to study grey reef sharks in the Pacific For further information, contact behaviour of Manx shearwaters. Below right: a common Ocean. Bottom left: an acoustic receiver used to monitor Robin Freeman: [email protected] guillemot with a Mataki tag. Bottom right: the Institute uses movement patterns and social networks in sharks

Learn more about the Living Planet Index at livingplanet index.org

The References Institute Gibb, R, Shoji, A, Emerging Network-Based monitoring arrays. J R Soc has developed Fayet, AL, et al (2017) Tools in Movement Interface 13: 20160676 a method for inferring Remotely sensed wind Ecology. Trends in Ecology social interactions between speed predicts soaring and Evolution 31: 301–314 McRae, L, Freeman, R and grey reef sharks in behaviour in a wide- Marconi, V (2016) ‘The the Pacific Ocean, ranging pelagic seabird. Jacoby, DMP, Living Planet Index’ in: using acoustic J R Soc Interface doi: Papastamatiou, YP Living Planet Report 2016: telemetry data 10.1098/rsif.2017.0262 and Freeman, R (2016) Risk and resilience in a Inferring animal social new era (ed.Oerlemans N). Jacoby, DMP and networks and leadership: WWF International, Freeman, R (2016) applications for passive Gland, Switzerland

zsl.org ZSL Science Review 2016-17 17 IMPACT AREAS

Fostering coexistence between people and nature Institute research improves our understanding of the relationships between nature and people, and develops and evaluates mechanisms to support coexistence.

uman development, as explicitly Human-wildlife conflict acknowledged in the UN Sustainable The Institute has ongoing research Development Goals, can only be programmes that seek to understand the Hsustainable if it does not destroy the relationship between wildlife and local ecosystems on which people and wildlife communities in order to develop mitigation depend. Yet human populations continue strategies to reduce human-wildlife conflict. to grow and anthropogenic impacts are New research in this area has involved an increasingly affecting every corner of the assessment of the socio-economic correlates globe. The global human population is and management implications of livestock expected to reach nearly 10 billion by 2050, depredation by large carnivores, as well as and rising per capita consumption will place an analysis of local attitudes to livestock unprecedented pressures on the planet’s husbandry practices and approaches to support systems. Maintaining biodiversity reducing livestock loss in the Tarangire- in the face of these pressures is an enormous Simanjiro ecosystem, northern Tanzania. challenge and depends on knowledge of the These results demonstrate the importance complex interdependencies between people of fortified bomas as a long-term solution and nature. to reduce night-time livestock depredations, while adult herders help to prevent losses Assessing natural capital during daytime grazing at pasture. This Evaluating the state of nature in relation research is key to developing effective (Entry Level Stewardship, ELS) – and to human wellbeing underpins our ability strategies to foster coexistence with large sampling a representative selection of crop to sustainably manage natural resources carnivores (Mkonyi et al. 2017a,b). and non-crop habitats, we were able to show while delivering development goals. Recent that pollination services were higher on work at the Institute has focused on the Sustainable agricultural organic farms overall compared to CG or use of satellite remote sensing data in the development ELS. These findings support organic farming assessment of natural capital and The need to feed a growing practices that increase floral resources in ecosystem services. This human population means crop habitats, such as sowing clover or research demonstrates that more food will need reduced herbicide usage, as mechanisms that satellite remote to be produced from to enhance pollination services (Hardman sensing-based the limited amount et al. 2016a,b). Understanding how methodologies can of land available different farming approaches can better be used to provide globally that foster biodiversity will help improve the a wide array of is suitable for sustainability of agricultural development. metrics that can agriculture. inform conservation Finding ways to Fencing policies for in data-deficient increase agricultural people and wildlife areas, such as the production, while In dryland ecosystems, mobility is essential Sahara (Pettorelli maintaining biodiversity, for both wildlife and people to access et al. 2016). It goes on is a mounting challenge. unpredictable and spatially heterogeneous to make an urgent call We investigated the resources. In Africa there have been for scientists in biodiversity impacts of different wildlife- growing calls to increase fencing to and satellite remote sensing to work friendly production schemes on separate wildlife and people as a means together in order to agree on standardised biodiversity and ecosystem service delivery to protect wildlife populations from measures that can be used to hold national on farms in the UK. By comparing organic overhunting, poaching, human-wildlife governments to account on their national farming with two non-organic wildlife- conflict and human encroachment. and international commitments to friendly farming schemes – one prescriptive However, research led by the Institute biodiversity conservation. (Conservation Grade, CG) and one flexible shows the need to exercise caution in

18 ZSL Science Review 2016-17 zsl.org Main image and inset: in Africa, Institute research has For further information, contact investigated the effectiveness of traditional and new Sarah Durant: [email protected] approaches in reducing livestock losses to large carnivores

Fostering coexistence between people and nature

the use of fencing, as fences can prevent References connectivity vital for the mobility of Hardman, CJ, Harrison, Boitani, L, Breitenmoser, C, livestock depredation wildlife and people. This research DPG, Shaw, PJ, Nevard, TD, Broekhuis, F, Christianson, by large carnivores in identified six research areas that are key Hughes, B, Potts, SG and D, Cozzi, G, Davenport, the Tarangire-Simanjiro to informing evaluations on fencing Norris, K (2016a) Supporting TRB, Deutsch, J, Devillers, ecosystem, Tanzania. initiatives: economics, edge permeability, local diversity of habitats P, Dollar, L, Dolrenry, S, Human Ecology 45: 513–523 reserve design, connectivity, ecosystem and species on farmland: a Douglas-Hamilton, I, Dröge, services and communities. Implementing comparison of three wildlife- E, FitzHerbert, E, Foley, C, Mkonyi, FJ, Estes, AB, Msuha, this research agenda to evaluate fencing friendly schemes. Journal of Hazzah, L, Hopcraft, JGC, MJ, Lichtenfeld, LL and interventions will enable better management Applied Ecology 53: 171-180 Ikanda, D, Jacobson, A, Durant, SM (2017b) Socio- and policy decisions (Durant et al. 2015). Joubert, D, Kelly, MJ, Milanzi, economic correlates and Our research underlies a proposed Hardman, CJ, Norris, K, J, Mitchell, N, M’Soka, J, management implications concerted action to investigate the impact Nevard, TD, Hughes, B Msuha, M, Mweetwa, T, of livestock depredation of linear barriers on wildlife movement and Potts, SG (2016b) Nyahongo, J, Rosenblatt, E, by large carnivores in the in Africa, which is under consideration Delivery of floral resources Schuette, P, Sillero-Zubiri, Tarangire ecosystem, at the 2017 Conference of Parties of the and pollination services C, Sinclair, ARE, Stanley northern Tanzania. UN Convention for the Conservation of on farmland under three Price, MR, Zimmermann, International Journal Migratory Species. different wildlife-friendly A and Pettorelli, N (2015) of Biodiversity Science, Future priorities for our work in this schemes. Agriculture, Developing fencing policies Ecosystem Services & area include developing a better Ecosystems & Environment for dryland ecosystems. Management 13: 248-263 understanding of the social and cultural 220: 142-151 Journal of Applied Ecology dimensions of conservation and 52: 544-551 Pettorelli, N, Owen, HJF development interventions. Our ultimate Durant, SM, Becker, MS, and Duncan, C (2016) aim is to contribute to the development Creel, S, Bashir, S, Dickman, Mkonyi, FJ, Estes, AB, Msuha, How do we want satellite of effective mechanisms to foster biodiversity AJ, Beudels-Jamar, RC, MJ, Lichtenfeld, LL and remote sensing to support and human wellbeing, helping to attain Lichtenfeld, L, Hilborn, Durant, SM (2017a) Fortified biodiversity conservation sustainable development goals alongside R, Wall, J, Wittemyer, G, bomas and vigilant herding globally? Methods in Ecology improved nature conservation. Badamjav, L, Blake, S, are perceived to reduce and Evolution 7: 656-665

zsl.org ZSL Science Review 2016-17 19 IMPACT AREAS

Conservation genetics The Institute’s researchers develop methods and tools in conservation genetics, and apply these to inform the conservation of threatened species.

enetic diversity influences the these methods to investigate the historical health and long-term survival of and current effective population size of populations, with decreased genetic Hainan gibbons (Nomascus hainanus) from Gdiversity associated with reduced fitness microsatellite data (Bryant et al. 2016). and adaptability to changing environments. Conservation genetics provides the theory Inferring population structure and methods to estimate historical and Individuals of a species may not constitute current genetic diversity and to predict a genetically homogeneous population. the future distribution of genetic diversity Instead, they are usually clustered into in populations and species. This crucial different populations due to patchy information informs conservation strategy geographic distribution and a limited ability in order to minimise risk of extinction in to disperse. Inferring population structure by threatened species. delineating the number and distribution of populations and by measuring the genetic Estimating effective differentiation among populations helps population size us to understand the current distribution Threatened species usually have small and of genetic diversity. declining population sizes, and genetic Institute research has shown that the diversity is lost due to genetic stochasticity. most appropriate statistic for quantifying The rate of loss of genetic diversity is genetic differentiation is Fst (a measure determined by the effective population of genetic differentiation between size (Ne) of the species, which is affected by populations). However, Fst can underestimate factors including the total population size differentiation when calculated from highly (N), variance in reproduction and sex ratio. polymorphic microsatellite data. We have For wild populations, Ne can be dramatically shown for the first time the circumstances smaller than N, especially for when microsatellites give species with extremely locus-dependent and unbalanced sex ratio underestimates of Fst, and high reproductive such as high mutation dominance. rate and low migration Therefore, it rate. We have since is essential to developed a measure the Ne correlation analysis of a population to detect such for conservation circumstances management. We from genotype data have developed (Wang 2015). methods to estimate We have also used Ne from genetic marker a Bayesian clustering data (most recently Wang method (Structure) to 2016a), and produced user- make individual assignments friendly computer software called Colony, to populations from multi-locus genotype which is available on the Institute website for data, most recently to investigate the use by conservation genetics practitioners. population structures of grey squirrels Thousands of downloads of the Colony (Sciurus carolinensis) (Signorile et al. 2016). software have been recorded over the past A new study showed that Structure is easily 12 months and new Institute research used misused when sampling is unbalanced,

20 ZSL Science Review 2016-17 zsl.org Main image: bumblebee family lineage survival historical and current effective population size For further information, contact Jinliang Wang: is enhanced in high-quality landscapes. Inset left: of Hainan gibbons [email protected] microsatellite data are used to investigate the

zsl.org ZSL Science Review 2016-17 21 Below left: Institute genotyping methods were used to estimate the effective population size of cheetahs IMPACT AREAS using scats detected by trained dogs

and could yield biased results when the Non-invasive genotyping alleviates some of default parameter values of the software these difficulties by obtaining DNA by indirect References were adopted (Wang 2017). Our research sampling of a specimen. This does not require Becker, MS, Durant, SM, Garner, TWJ, Bosch, has provided alternative parameter values, handling (or even the presence of) the animal, Watson, FGR, Parker, J and Fisher, MC which yield more accurate population as DNA can be extracted from small quantities M, Gottelli, D, M’soka, J, (2016) Climate forcing structure inferences in both simulated and of hair, feathers, scales or scats, which can Droge, E, Nyirenda, M, of an emerging real datasets. be genotyped by polymerase chain reaction. Schuette, P, Dunkley, S pathogenic fungus We have applied this technique to a range and Brummer, R (2017) across a montane Relatedness and of species, enabling ecological, evolutionary Using dogs to find multihost community. relationship ascertainment and conservation genetics studies of species cats: detection dogs Philosophical Knowing the genetic relatedness among that could not have been studied otherwise. as a survey method for Transactions of the individuals is essential for investigating However, data quality can be problematic wide-ranging cheetah. Royal Society 371: breeding behaviour, inbreeding and because the quality and quantity of DNA Journal of Zoology 201505454 inbreeding depression, social structure, from non-invasive samples is often low and 302: 184-192 and population demographics and genotyping errors are common. An important Signorile, AL, Lurz, connectivity. Traditionally, relatedness is application of non-invasive genotyping, Brekke, P, Ewen, JG, PWW, Wang, J, Reuman, calculated from pedigrees (eg Brekke et al. estimating population census size by Clucas, G and Santure, DC and Carbone, 2015). However, pedigree data are rarely the genetic capture-recapture model, is AW (2015) Determinants C (2016) Mixture or available in wild populations. particularly vulnerable to genotyping errors. of male floating mosaic? Genetic We have proposed advanced behaviour and floater patterns in UK grey likelihood methods for identifying reproduction in a squirrels support a individuals from multi-locus threatened population human-mediated genotypes obtained from non- of the hihi (Notiomystis ‘long-jump’ invasion invasive samples, accounting for cincta). Evolutionary mechanism. Diversity genotyping errors and missing Applications 8: 796-806 and Distributions data (Wang 2016b). Our methods 22: 566-577 have recently been used to Bryant, JV, Gottelli, estimate the density and effective D, Zeng, X, Hong, X, Wang, J (2015) Does Gst population size of cheetahs using Chan, BPL, Fellowes, underestimate genetic scats detected by trained dogs JR, Zhang, Y, Luo, J, differentiation from (Becker et al. 2017). Durrant, C, Geissmann, marker data? Molecular T and Chatterjee, Ecology 24: 3546-3558 Disease emergence HJ (2016) Assessing Infectious diseases can threaten current genetic status Wang, J (2016a) A populations, species and entire of the Hainan gibbon comparison of single- communities of wildlife, and the using historical sample estimators of consequences of disease can and demographic effective population be exacerbated when genetic baselines: implications sizes from genetic diversity of wildlife populations for conservation marker data. Molecular is low. Wildlife hosts of pathogens management of species Ecology 25: 4692-4711 can respond to the emergence of extreme rarity. of disease through selection, Molecular Ecology 25: Wang, J (2016b) To facilitate studies of wild populations, we and we have used population genetics to 3540-3556 Individual identification developed methods to estimate relationship detect both natural and sexual selection in from genetic marker and relatedness from genetic marker data, diseased populations. Carvell, C, Bourke, AF, data: developments producing a computer program called We have shown how the genetic Dreier, S, Freeman, SN, and accuracy Coancestry. Our studies, among many others, interactions between host and pathogen are Hulmes, S, Jordan, WC, comparisons of have used these methods to assess inbreeding strongly regulated by environmental variation Redhead, JW, Sumner, methods. Molecular and inbreeding depression in diverse species, caused by climate change (Clare et al. 2016), S, Wang, J and Heard, Ecology Resources and were most recently used to investigate and we now need to examine how genes are MS (2017) Bumblebee 16: 163-175 the survival and reproduction of bumblebee expressed under these different conditions. family lineage survival (Bombus spp.) queens (Carvell et al. 2017). Hosts cannot fend off pathogens with a single is enhanced in high- Wang, J (2017) The molecular toolkit, so we will continue to quality landscapes. computer program Conservation genetics by unpick the complexities of host immune Nature 543: 547-549 STRUCTURE for non-invasive genotyping gene expression. assigning individuals Threatened species are often difficult to Clare, FC, Halder, JB, to populations: easy sample for genetics studies. Some animals Daniel, O, Bielby, J, to use but easier to To download Colony, visit zsl.org/ are dangerous, such as large carnivores, or Semenov, MA, Jombart, misuse. Molecular science/software/colony – and for difficult to access, such as marine mammals, T, Loyau, A, Schmeller, Ecology Resources. Coancestry, visit zsl.org/science/ while some others are elusive, such as okapis DS, Cunningham, doi:10.1111/1755- software/coancestry (Okapia johnstoni). AA, Rowcliffe, JM, 0998.12650

22 ZSL Science Review 2016-17 zsl.org Research projects include screening for snake fungal disease to discover the origins of the condition

Research highlights Institute researchers continue to advance our understanding of the natural world. In the following pages we highlight new science and report on a diverse range of subjects – from the impact of climate change on African wild dogs to the identification of a new fungal skin disease in snakes. Also in this section, two of our scientists describe what their work entails, we explain how we communicate our knowledge, and we celebrate our students’ work and the outstanding contribution of our award winners.

Europe’s chemical Seabirds Citizen scientists High New species Badger pollution remotely sense help study temperatures of extinct vaccination wind speed wildlife affect African Late Quaternary against bovine TB wild dogs giant tortoise

zsl.org Annual Report and Accounts 2016 23

ZSL SCIENCE REVIEW RESEARCH

Research highlights Through their published research, Institute staff and students continue to widen our knowledge and understanding of the natural world. Here, we present just a few of the papers that have been making an impact over the past year.

Snake fungal disease found in Europe Snake fungal disease (SFD) is an emerging disease of conservation concern in eastern North America. Ophidiomyces ophiodiicola, the causative agent of SFD, has been isolated from more than 30 species of wild snake from six families in North America. While O. ophiodiicola has been isolated from captive snakes outside North America, the pathogen has not been reported from wild snakes elsewhere. We screened 33 carcasses and 303 moulted skins from wild snakes collected from 2010-2016 in Great Britain and the Czech Republic for the presence of macroscopic skin lesions and O. ophiodiicola. The fungus was detected using real-time polymerase chain reaction in 26 (8.6%) specimens across the period of collection. Follow-up culture and histopathologic analyses confirmed that both O. ophiodiicola and SFD occur in wild European snakes. Although skin lesions were mild in most cases, in some grass Europe’s inadequate chemical learn the science and policy lessons from the snakes (Natrix natrix) they were severe and pollution remediation US approach as a matter of urgency. There is were likely to have contributed to mortality. Polychlorinated biphenyls (PCBs), chemicals also a general lack of compliance – globally Culture characterisations demonstrated once widely used in manufacturing, remain a – for PCBs under the Stockholm Convention, that European isolates grew more slowly major global threat to marine apex predators, with approximately 80% of global PCB than those from the United States, and with killer whales (Orcinus orca) still the most stockpiles on land still awaiting destruction. phylogenetic analyses indicated that isolates PCB-polluted mammalian species globally Aside from the International Council for the from European wild snakes reside in a clade (ICES 2017; Law and Jepson 2017; Stuart- Exploration of the Sea (ICES), reports of the distinct from the North American isolates Smith and Jepson 2017). Europe produced lingering effects of PCBs on marine mammals examined. These genetic and phenotypic between 299,000 and 585,000 tons of PCBs were also widely covered in the broadsheet differences indicate that the European isolates prior to the ban on their production – but newspapers, including an editorial in The Times represent novel strains of O. ophiodiicola. many EU member states are not assessing or on 3 May 2017. Further work is required to understand the decontaminating PCB-contaminated materials, individual and population-level impact of this sites or waste stockpiles sufficiently. In Europe, References pathogen in Europe and which species are only Norway, Sweden and Switzerland have ICES (2017) Working Group on the Biological Effects affected. Comparing how SFD affects wild established procedures for secure disposal or of Contaminants. ices.dk/community/groups/Pages/ snakes on different continents may help us destruction of highly contaminated PCBs in WGBEC.aspx understand the origin of the disease and help joint sealants. The United States is relatively managers identify mitigation strategies. proactive in terms of PCB mitigation nationally Jepson, PD (2017) Thunderer: Killer whales must be and at state level, including numerous US saved from toxic chemicals The Times, 3 May 2017 Reference Environmental Protection Agency Superfund Franklinos, LHV, Lorch, JM, Bohuski, E, Rodriguez- sites. As a direct result, PCB levels in the US Law, RJ and Jepson, PD (2017) Europe’s insufficient Ramos Fernandez, J, Wright, ON, Fitzpatrick, have slowly declined in humans and other pollutant remediation. Science 356: 148 L, Petrovan, S, Durrant, C, Linton, C, Baláž, V, biota, such as fish, for many years and overall Cunningham, AA and Lawson, B (2017) Emerging PCB mitigation is generally considered to be Stuart-Smith, S and Jepson, PD (2017) Persistent threats fungal pathogen Ophidiomyces ophiodiicola in successful. We argue in a number of policy- need persistent counteraction: responding to PCB wild European snakes Scientific Reports 7: 3844 focused reports and papers that Europe should pollution in marine mammals. Marine Policy 84: 69-75

24 ZSL Science Review 2016-17 zsl.org Top right: Institute research showed that remotely a founding partner in the Frog Mortality Project. sensed wind speed and direction could predict soaring Left: killer whales are the most PCB-polluted mammal behaviour in the Manx shearwater. Below: ZSL was

Remotely sensed wind speed predicts seabird soaring behaviour Global wind patterns affect flight strategies in many birds, including pelagic seabirds, many of which use wind-powered soaring to reduce energy costs during at-sea foraging trips and migration. Such long-distance movement patterns are underpinned by local interactions between wind conditions and flight behaviour, but these fine-scale relationships are not well understood. Our research has shown for the first time that Citizen scientists help remotely sensed wind speed and direction reconstruct wildlife can predict soaring behaviour in a migratory disease emergence pelagic seabird, the Manx shearwater (Puffinus Emerging infectious disease can puffinus). High-frequency GPS tracking data pose a considerable threat to wildlife. and statistical behaviour state classification Reconstructions of disease emergence were used to identify two energetic modes in driven by climate change could impact can enable action to mitigate against at-sea flight, corresponding to flap-like and this and other species. This research also further spread or prevent new emergences. soar-like flight. Importantly, the research demonstrates the potential of high-frequency Unfortunately, reconstructions of wildlife found that soaring was significantly more GPS biologgers to provide detailed diseases are rare, often because wildlife likely to occur in crosswinds and tailwinds quantitative insights into fine-scale flight populations are not intensively sampled. faster than eight metres per second. These behaviour in free-living animals. Institute researchers combined citizen science periods of wind-powered soaring may data with genetic information to overcome enable birds to reduce metabolic costs Reference these challenges, and to study how viruses by preferentially soaring over flapping. Our Gibb, R, Shoji, A, Fayet, AL, Perrins, CM, Guilford, causing a fatal disease in amphibians and results suggest a behavioural mechanism by T and Freeman, R (2017) Remotely sensed wind reptiles (ranavirus) had spread in the UK. ZSL which wind conditions may shape foraging speed predicts soaring behaviour in a wide- was a founding partner in the Frog Mortality and migration ecology in pelagic seabirds, ranging pelagic seabird. Interface DOI: 10.1098/ Project (FMP), a citizen science project and thus indicate that shifts in wind patterns rsif.2017.0262 initiated 25 years ago to collate information from the British public about incidents of frog mortality. The pattern of mortality incidents derived from the FMP database was used to model disease emergence and test hypothetical drivers, such as climate change, pathogen spread following introduction, and changes in reporting behaviour. We found evidence that ranavirus was independently introduced to the UK at least twice. Following introduction, most new outbreaks were explained through local dispersal of infected amphibians, but additional incidents, likely explained by translocations of infectious materials by people, were important in bringing about a rapid, nationwide spread. Our study supported the reinforcement of guidelines on limiting the movement of potentially infectious materials, but also highlighted how citizen science could help to reconstruct disease emergence in a timescale enabling information to flow into ZSL management decisions. co-founded the Frog Mortality Reference Project, a citizen Price, SJ, Garner, TWJ, Cunningham, AA, Langton, science programme TES and Nichols, RA (2016) Reconstructing the initiated emergence of a lethal infectious disease of 25 years ago wildlife supports a key role for spread through translocations by humans. Proceedings of the Royal Society Series B 283: 20160952

zsl.org ZSL Science Review 2016-17 25 RESEARCH

High temperatures impact Botswana site coincided with falling wild New species of extinct Late reproductive success in dog recruitment. Our findings suggest a Quaternary giant tortoise African wild dogs direct impact of high ambient temperatures The Caribbean islands have experienced Climate change may be harming the future on African wild dog demography, indicating the world’s highest level of mammal of African wild dogs, also known as African that this species, which is already globally extinction during the Holocene Epoch (the hunting dogs (Lycaon pictus), by impacting Endangered, may be highly vulnerable to past 11,700 years), as a result of pre-modern the survival rates of pups, according to one of climate change. human exploitation, habitat destruction and the first studies on how shifting temperatures This vulnerability would have been missed introduction of invasive species. However, the are affecting tropical species. We explored by trait-based assessments. Seasonal extent to which other vertebrate groups have associations between weather conditions, reproduction, which is less common at low also suffered human-caused extinctions in the reproductive costs and reproductive success, latitudes than at higher latitudes, might Caribbean is much more poorly understood. drawing on long-term wild dog monitoring be a useful indicator of climate change Giant tortoises are absent from current-day data from sites in Botswana, Kenya and vulnerability among tropical species. insular Caribbean ecosystems, but tortoise Zimbabwe. High ambient temperatures Ongoing research will focus on identifying fossils from Late Quaternary deposits indicate were associated with reduced foraging time, conservation actions that might reduce these the former widespread occurrence of these especially during the energetically costly climate impacts on wild dogs, and working animals across the northern Caribbean. pup-rearing period. out where they are most needed. Interestingly, giant tortoises are extremely Across all three sites, packs that reared rare in Quaternary fossil deposits across most pups at high ambient temperatures Reference of Hispaniola, a large island that has been produced fewer offspring than did those Woodroffe, R, Groom, R and McNutt, JW (2017) studied extensively by palaeontologists over rearing pups in cooler weather. At the Hot dogs: High ambient temperatures impact the past century. We recovered and analysed non-seasonal Kenya site such packs also had reproductive success in a tropical carnivore. new giant tortoise material from several longer inter-birth intervals. Rising ambient Journal of Animal Ecology doi.org/10.1111/1365- cave sites in Pedernales Province, southern temperatures at the longest-monitored 2656.12719 Dominican Republic, Hispaniola, representing

26 ZSL Science Review 2016-17 zsl.org Below left: humeri of Chelonoidis marcanoi sp. nov. vaccination had no discernible risks. Left:climate from Pedernales Province, Dominican Republic. change may be diminishing African wild dog Below right: an Institute study showed that badger survival rates

Badger vaccination against bovine TB offers alternative to culling Concerns that vaccinating badgers against bovine tuberculosis (TB) might increase transmission rates of the disease to cattle have been diminished by new research showing no discernible behavioural impacts from this treatment. The study, led by the Institute, offers hope of a practical alternative to the UK Government’s controversial cull policy. The behaviour of 54 GPS-collared badgers was studied across four study sites in Cornwall. Scientists found that of these animals, the 15 that had received the TB vaccine during the course of the project had the same ranging behaviour as unvaccinated badgers. Badger vaccination is less risky, more humane and cheaper than culling. We hope that this research will open the door for greater exploration of badger vaccination as a tool to control TB in cattle.

Reference Woodroffe, R, Donnelly, CA, Ham, C, Jackson, SYB, Moyes, K, Chapman, K, Stratton, NG and Cartwright, SJ (2017) Ranging behaviour of badgers Meles meles vaccinated with Bacillus Calmette Guerin. Journal of Applied Ecology 54: 718-725

Fossils indicate the Badger at least seven former widespread vaccination is individuals, which occurrence of giant less risky, more we describe as tortoises across humane and cheaper a new extinct the northern than culling species, Chelonoidis Caribbean marcanoi. The surprising abundance of giant tortoise remains in both vertical and horizontal caves in Hispaniola’s semi-arid ecoregion may indicate that this species was adapted to open dry habitats. We hypothesise that the Hispaniolan giant tortoise became restricted to a habitat refugium in south- eastern Hispaniola following climate-driven environmental change at the Pleistocene- Holocene boundary, making it more vulnerable to hunting by prehistoric human colonists who arrived in Hispaniola around 6,000 years ago. This research suggests that Hispaniola’s dry forest ecosystem may have been shaped by giant tortoises for much of its evolutionary history.

Reference Turvey, S, Almonte, J, Hansford, J, Scofield, RP, Brocca, JL and Chapman, SD (2017) A new species of extinct Late Quaternary giant tortoise from Hispaniola. Zootaxa 4277: 1-16

zsl.org ZSL Science Review 2016-17 27 SCIENCE

How our science is done Two Institute researchers describe the variety of their working days and explain the rewards of a career in conservation science.

Monika Böhm reflects on the of Threatened factors, such as habitat benefits of collaboration Species. This is a change, and by Human impact is altering natural huge collaboration re-examining sampling environments and pushing species to the of organisations and regimes to adequately brink of extinction. My work looks at the people, which has represent extinction main factors affecting species and what produced assessments risk trends in groups of may predispose them to be at an intrinsically of extinction risk for more megadiverse species, such higher risk. The majority of my time is spent than 80,000 species – a vast as spiders. In many cases, these on groups of species that are little-known in data repository on the status, distribution, activities again rely on collaboration and comparison to birds and mammals, such as ecology, habitat and threats of species. data sharing, for example, to pull together reptiles and invertebrates. Yet this doesn’t Over the past 10 years, we have data sets on species traits. mean I spend all my life in the field, observing contributed more than 9,000 assessments to I see science as sharing knowledge and animals in their changing environments – in the IUCN Red List, again through extensive data widely, fairly and constructively, to fact, I hardly do any fieldwork! collaboration with species experts. This address real-world problems. Sometimes The science I do relies heavily on extensive hard work results in huge data sets, which we’re the donors, other times the recipients collaborations and collating vast data sets we can now use to study the causes of high of large data sets. The best thing, in my to test hypotheses about the causes of extinction risk across a large number of opinion, is that each of these exchanges high extinction risk and population decline. species. Using these data, my research is helps to shape collaborations, builds One of my main collaborations is with the trialling new ways of carrying out species research networks and brings people with International Union for Conservation of assessments, by predicting extinction risk different expertise together – and more than Nature (IUCN), specifically on its Red List from species traits and environmental once, you even make friends for life.

28 ZSL Science Review 2016-17 zsl.org Below right: veteran baboon observer Alecia Carter watching. Left: Monika Böhm collects vast data sets on sets off for a day with the troop.Below: sometimes reptiles such as the chuckwalla (Sauromalus sp.) the field observers are not the only ones doing the

Guy Cowlishaw describes the joys of fieldwork Understanding animal behaviour and among them as if we were a member of ecology is fundamental to conservation. their social group. In my case, this perfectly Without knowing how animals describes our working conditions on the survive and reproduce, and their Tsaobis Baboon Project, a long- ability to adapt to changing term, individual-based study of environments, it is difficult desert baboons (Papio ursinus) to prioritise scarce resources in Namibia. or to design appropriate Field days with the management interventions. baboons are long and The best way of learning tiring, involving 12-hour about animal behaviour dawn-to-dusk follows on and ecology is to spend time foot, travelling large distances with the animals themselves. over hazardous mountain Often this is a significant challenge, terrain, carrying a heavy backpack although exciting new developments in in intense heat. Moreover, during this tracking technology now make it possible for time, observers are continuously collecting Institute scientists to study animals that have data from the baboons (using customised previously been out of reach – ranging from smartphones), and may also be carrying oceanic birds, like the Round Island petrels out field experiments, ranging from (Pterodroma spp.), to marine predators, such novel food presentations (to study the as scalloped hammerhead sharks (Sphyrna transmission of social information) to lewini). In other cases, our study species playbacks of threat vocalisations (to explore are more accessible and can be observed male sexual coercion). directly. Ideally, we work on foot; for instance, Nevertheless, field days with the baboons in our research on threatened island birds, are also very rewarding. All of the baboons are but we also use vehicles, especially when individually recognisable and are well-known observing large carnivores such as cheetahs to us; indeed, we’ve followed most of them (Acinonyx jubatus) and African wild dogs since they were born. Each individual lives in (Lycaon pictus). a complex network of family and friends, and animal societies work, about how social The most privileged field biologists, their daily dramas unfold like a soap opera. animals are likely to cope with accelerating and I count myself among them, work But, crucially, in addition to the pleasure of environmental change, and about what with animals that can be habituated to the sharing their lives with them, the baboons conservation support is needed to ensure presence of observers, allowing us to walk are also teaching us about how complex that social animals survive into the future.

zsl.org ZSL Science Review 2016-17 29 EDUCATION

Education and training Educating the next generation of conservation scientists is central to the Institute’s work. Here, we look at student achievements over the past academic year.

Our PhD students

t has been another busy year for our student body. We have a fantastically dynamic and enthusiastic group that is keen Ito have an impact on how the Institute evolves. As an institution we have been working hard to improve our support structures, focusing on welfare and developing a nurturing working environment for students and staff. Students have been directly involved in this process by being part of our science development focus groups, having representatives in our Athena Scientific Women’s Academic Network (SWAN) panel and management board, co-managing our speed talk sessions and social committee, and volunteering their time and expertise in a number of events, such as UCL Summer School visits, British Science Week, Soapbox Science and Zoo Nights. Being a postgraduate tutor over the past year has been immensely rewarding. My co- postgraduate tutor, Jon Bielby, left the Institute This year we have Pterodroma petrels); in February, but his legacy has had a huge welcomed 12 new PhD Freya Jephcott (Inefficient positive impact on our work environment, and students from the SCENARIO responses to unlikely me personally – he was incredibly generous NERC Doctoral Training outbreaks: a case study of with his time and a great sounding board for all Partnership (DTP), London DTP and a supposed monkey-borne virus the different student policies and programmes Science and Solutions for a Changing Planet outbreak in the Brong-Ahafo region of Ghana); we have been implementing. I am also very DTP, as well as international students based in Andrew Jacobson (Large carnivores under fortunate that Guy Cowlishaw took on this Chile, China and New Zealand. We have joined threat: investigating human impacts on large role upon Jon’s departure, and he has been two new DTPs – Centre for Doctoral Training carnivores in East Africa); Natoya Jourdain just as enthusiastic and involved. Recently, in Quantitative and Modelling Skills in Ecology (New analytical methods for camera trap we have focused on developing mental health and Evolution, and Environmental Research – data); Elizabeth Moorcroft (Paws for thought: awareness in the student body; our Athena and hope these will lead to new collaborations assessing the efficacy of monitoring SWAN application; and the development of the and students in the coming year. techniques for rare and elusive species); student hub, which will open in autumn 2017. We also bid farewell to 13 students who Leandro Patino (Evolution and community We continue to support programmes such successfully completed their PhDs, producing structure of parasites in Galápagos giant as the Student Lunches, where students meet, impressive theses. They are: Kirsten McMillan tortoises); Silke Riesle-Sbarbaro (The share lunch and invite representatives from (Epidemiology of the amphibian pathogen persistence and zoonotic emergence of viral different ZSL departments. These lunches Batrachochytrium dendrobatidis, across infections in fruit bats in Ghana); as well as improve student integration, particularly multiple spatial scales); Clare Duncan Charlotte Clarke and Juliet Wright highlighted with our new student cohorts, and give them (Mangrove forest ecosystem services: right. Time and time again, our students the opportunity to learn about different biodiversity drivers, rehabilitation and produce high-calibre research that makes a non-academic careers in conservation and resilience to climate change); Andrés real difference to conservation. We could not network with a wider group of conservation Valenzuela-Sénchez (Is chytridiomycosis a be prouder! professionals. We also awarded four ‘Daisy threat to the mouth-brooding Darwin’s frog Patricia Brekke, postgraduate tutor Balogh’ grants to Cassandra Raby, Sahil (Rhinoderma darwinii)? A multi-approach Nijhawan, Kirsten McMillan and Sarah Brooke disease risk assessment); Dominic Bennett Learn more about postgraduate to support travel and subsistence costs (An appraisal of the ‘living fossil’ concept); opportunities at zsl.org/science/ associated with their PhDs and not covered Katherine Booth-Jones (Distribution and postgraduate-study by PhD budgets. gene-flow in a hybridising population of

30 ZSL Science Review 2016-17 zsl.org Below: PhD student Juliet Wright in the Dja Reserve, Cameroon. Bottom: Charlotte Clarke on the Isle of Rum. Left and inset: a diseased palmate newt (Lissotriton helveticus) and its habitat

Juliet Wright Projects promoting alternative livelihood activities are implemented to reduce reliance on bushmeat hunting, yet evidence that these projects succeed in changing local behaviours is limited. Through my PhD, I sought to gain a better understanding of the complexities of rural people’s lives in Cameroon, and assess how alternative livelihood projects work in practice. I took an interdisciplinary approach and gleaned insights from across the social sciences with the aim of changing the way we think about livelihood projects in conservation and, ultimately, how we might do them better in the future. I have since been involved in designing an impact evaluation of alternative livelihood projects for USAID and have just started a job with the Wildlife Conservation Society to coordinate its bushmeat research activities in the Congo.

Charlotte Clarke My PhD focused on investigating a novel amphibian-infecting Dermocystid affecting palmate newts on the Isle of Rum in Scotland. Using a multidisciplinary approach, including DNA extraction and sequencing, histological analysis and epidemiological techniques, a pathogen profile was developed to better understand the host-parasite dynamics on the island. The most rewarding part of my PhD was being able to work and collaborate with different people and be exposed to such a vast array of research. I am now living in the Middle East and exploring the possibility of working with the World Wide Fund for Nature in the Gulf or moving towards public health utilising the epidemiology aspects of my work.

zsl.org ZSL Science Review 2016-17 31 Main image: veterinarians at the Interventions in studied by Victoria Wilkinson for her MSc on Wild Animal Health field course. Below left: American wildlife disease surveillance in small, secretive EDUCATION black bears (Ursus americanus), one of the species or Endangered species

Our MSc courses

MSc courses in Wild Animal Biology and Wild Animal Health Over the past 22 years, more than 400 students, from 57 countries and six continents have graduated from our MSc courses in Wild Animal Biology (WAB) and Wild Animal Health (WAH). In 2016, 17 students took the MSc WAB, of which two were awarded distinctions, seven received a merit, and eight passed. Seven students took the MSc WAH, of which one received a distinction, one a merit and four passed. Phoebe Griffith received the award for the MSc WAB student with the highest aggregate marks, and Victoria Wilkinson gained the most marks for the MSc WAH. The best research project prizes were awarded to Rebecca Lewis (MSc WAB) and Victoria Wilkinson (MSc WAH). Recent analysis of graduate career destinations shows that 84% of WAH and 85% of WAB graduates have gained posts in wild animal health or conservation (of 334 graduates surveyed), forming a valuable global network of wild animal health professionals, contactable through Wild Animal Alumni.

Interventions in Wild Animal Health field course In February, ZSL ran the second Interventions in Wild Animal Health field course in the beautiful setting of Sariska National Park, Rajasthan, India, in collaboration with the Wildlife Institute of India and the University of Edinburgh. Twenty-six veterinarians attended and received in-depth, practical tuition in population monitoring, surveillance of wild animal disease, and physical and chemical restraint of free-living wild animals. Of the attendees, 23 veterinarians were from biodiverse developing countries where increased capacity of wildlife health professionals is desperately needed.

MSc course in Conservation Science The MSc course in Conservation Science, run Hollie Booth was awarded the Joseph Hooker in partnership with Imperial College, the Royal prize for the best coursework performance. Botanic Gardens, Kew and Durrell Wildlife Ans Vercammen was awarded the Durrell Conservation Trust, remains popular with prize for the best project, which evaluated students focused on starting or enhancing a novel approach to spatial planning for their careers in conservation research and conservation of reefs in the coral triangle by action. The 2016 cohort included students developing a spatially explicit model of coral from Indonesia, Trinidad, Palestine, the USA condition across the region. and several European countries, as well as the UK. In all, 29 students graduated, with the Access the full Conservation Science award of 15 distinctions and 14 merits. thesis archive at iccs.org.uk/content/ Joss Lyons-White was awarded the TH thesis-archive-msc-consci Huxley prize for the best student overall, and

32 ZSL Science Review 2016-17 zsl.org Top right: the ZSL Library has vast and varied Below: drawing of fish from the collection resources. Below right: Platydactylus gecko, from of Francis Day Animals of India by Samuel Richard Tickell, 1864. LIBRARY

ZSL Library The ZSL Library develops and facilitates access to resources in zoology and conservation science. Our unique collections Visit our online provide an ideal opportunity for lifelong learning. catalogue at library.zsl.org

ZSL Library renamed In honour of HRH The Duke of Edinburgh’s long-standing support for ZSL, the ZSL Library has been renamed the Prince Philip Zoological Library and Archive.

Events and exhibits The Wellcome Collection borrowed five items for the Making Nature exhibition, which was visited by more than 130,000 people. An exhibition in the Aquarium at ZSL London Zoo featured drawings of birds and mammals from the manuscripts of Brian Houghton Hodgson as part of our Britain-Nepal 200 celebrations. The exhibit was seen by an estimated 505,000 visitors. This was followed by a display of drawings of fish from the collection of Francis Day. The collection consists of around 690 art originals bound in four volumes. Visits from external groups included City University, the Natural History

Digitisation The Charles Hayward Foundation kindly donated to the cost of conservation, repair and digitisation of the six volumes of Brian Houghton Hodgson’s manuscript volumes of birds of India and Nepal. Hodgson (1800-1894) is widely recognised for his enormous contribution to the descriptions of the birds and mammals of Nepal. Hodgson wrote more than 140 zoological papers, ranging from descriptions of single species to checklists of the fauna. The mammal volumes Museum, Cleveland Museum of Natural have been repaired and digitised, and can History, King’s College London, The Bartlett be viewed following the link from the online Zoo History Society, the Buckland Foundation, catalogue. Descriptions and illustrations of the Smithsonian and Sparsholt College. Indian animal species by Samuel Richard Tickell have also been digitised and can Artefacts be viewed in the online catalogue. Tickell Our monthly Artefacts blog on the ZSL was related to Hodgson through marriage website showcases unique items in our and both presented their manuscripts to collection. Recent posts include Sir Stamford ZSL in 1875. Beryl Leigh kindly funded the Raffles, Sir Richard Owen’s involvement digitisation of three volumes of the Daily with ZSL and his creation of the word Occurrences. We aim to offer access to this ‘dinosaur’, the extinction of the thylacine, primary research material worldwide, to and Women, art and zoology: Celebrating support conservation and taxonomy across International Women’s Day with women the world and to provide public appreciation Follow us on twitter @ZSLLibrary artists and illustrators. and enjoyment.

zsl.org ZSL Science Review 2016-17 33 EDUCATION

Communicating science Facilitating the communication of science among professional zoologists and researchers, and to the public, is an important part of our work. We achieve this through the publication of scientific journals and a varied programme of events.

Symposia ZSL symposia bring together teams of international experts to discuss important topics in conservation science, providing an opportunity for leaders to exchange ideas and communicate their research. At our symposium ‘The Living Planet Report 2016: Science and threats, pressures conservation events and addressing the ZSL’s popular science and conservation challenges’, leading events are free and open to the public. Each experts examined the meeting highlights the latest developments primary drivers of in conservation and zoological research. wildlife population This year’s programme included lectures on declines, with the aim of ‘Conserving the mountain chicken frog: the exploring how individuals, impact of chytridiomycosis under scrutiny’, communities and ‘The state of the Thames’ and ‘Immigrants governments can make to the rescue! How can immigration help to better choices in order save threatened wildlife populations?’. to preserve biodiversity.

‘CSI of the Sea’ wins BIAZA Gold Education Award In May, ZSL was awarded a BIAZA Gold Education Award in recognition of our ‘CSI of the Sea’ events, which highlight the work of Institute staff involved with the Cetacean Strandings Investigation Programme. At two sell-out events, audiences had the opportunity to observe a cetacean post-mortem taking place in real time and engage directly with our scientific staff. Broadening public understanding of conservation science is a fundamental part of our remit, and using dissections as an engagement tool has both increased public understanding of our work and acted as a proof of concept for other zoos, aquaria and scientific institutions.

34 ZSL Science Review 2016-17 zsl.org Below: Yadvinder Malhi delivers the Stamford Raffles Estuary is home to a thriving population of harbour Lecture. Bottom left: a live post-mortem of a harbour seals (Phoca vitulina). Below left: the North Island porpoise to investigate the effect of pollutants on robin (Petroica longipes) benefits from long-term cetaceans at ‘CSI of the Sea 2017’. Far left: the Thames genetic management

Stamford Raffles Lecture The Stamford Raffles Lecture is the foremost event in ZSL’s Scientific publications programme of scientific events. The 2017 lecture, ‘How animals shape ZSL publishes scientific journals and books that habitats, ecosystems and the global biosphere’, given by Yadvinder feature the latest research in zoology and Malhi, University of conservation science. Oxford, described the ways in To see our Animal Conservation which animals Animal Conservation publishes current programme can influence quantitative research on the of events, from public ecosystem conservation of species and habitats. The lectures to scientific structure, journal includes regular feature papers symposia, visit zsl.org/ biomass, and ‘Letters from the Conservation Front science/whats-on fire regimes Line’, to highlight research questions and even that are important to the conservation climate. Knowing practitioner community. how animals influence ecosystem function can reveal how even low-disturbance ecosystems carry the legacy of past extinctions. Yadvinder explained that in a world Journal of Zoology of increasing human pressure and Our monthly journal includes hypothesis- shifting climates, animals can have driven studies that advance our an important role in maintaining understanding of animals and their resilient ecosystems. systems. Special features include the Watch the lecture online at annual Huxley review paper, a series of zsl.org/science/whats-on/ ‘Hidden Gems’ from the archives, and stamford-raffles-lecture-2017. a journal blog and podcast.

Remote Sensing in Ecology and Conservation Our fully open-access journal provides a new platform for innovative science at the interface between ecology, conservation and remote sensing. Read the latest research at rsecjournal.com.

International Zoo Yearbook An invaluable resource for researchers, animal managers and anyone interested in ex-situ wildlife conservation, the latest volume presents a range of research projects, case studies and reviews on conservation translocations.

For more information on our publications, visit zslpublications. onlinelibrary.wiley.com/hub

zsl.org ZSL Science Review 2016-17 35 Below: (left to right) Claire Spottiswoode, Richard Simon Chen and Tim Birkhead FRS Griffiths, Sarah Cleaveland FRS, Paul Pearce-Kelly, Shan Inset: Alexandra Eyles-Owen and her teacher, Quah, Richard Fortey FRS, Richard Thompson, Sarah Rella LaRoe, Surbiton High School, receiving AWARDS Reece, Ashleigh Griffin, Sir John Beddington CMG FRS, the ZSL Prince Philip Award and Marsh Prize

ZSL Scientific Awards ZSL recognises outstanding achievements in zoological science and conservation through its annual presentation of awards. The following were presented at our most recent awards ceremony in June 2017.

ZSL Frink Award The Society’s highest award, presented to a professional zoologist for substantial and original contributions to science. Awarded to Sarah Cleaveland FRS, University of Glasgow, for outstanding contributions to the understanding of wildlife disease and the dynamics of infections in natural ecosystems.

ZSL Scientific Medal Presented to scientists with up to 15 years’ postdoctoral experience for distinguished work in zoology. Awarded to Ashleigh Griffin, University of Oxford, for advancing our understanding of behavioural and evolutionary ecology; Sarah Reece, University of Edinburgh, for outstanding research on the ecology and evolution of malaria parasites; and Claire Spottiswoode, University of and/or freshwater ecosystems. Awarded to of Cambridge, for his project ‘Attachment Cambridge, for influential contributions to Richard Thompson, University of Plymouth, mechanisms in caterpillars’. behavioural ecology, and our understanding for influential research that informs policy on of parasitic and mutualistic interactions marine pollutants. ZSL Thomas Henry Huxley between species. Award and Marsh Prize Presented for the best zoological doctoral thesis ZSL Silver Medal produced in the UK. Awarded to Shan Quah, Awarded for contributions to the understanding University of Oxford, for her thesis ‘Conservation and appreciation of zoology. Presented to and innovation – the evolution of the metazoan Richard Fortey FRS for major contributions to microRNA landscape and its contribution to science communication. reproduction and development’.

ZSL Stamford Raffles Award ZSL Clarivate Analytics Award Awarded to an individual for distinguished for Communicating Zoology contributions to zoology outside the scope Presented for a book or film of a zoological of their profession. Presented to Malcolm Tait nature that has an outstanding impact on a for writing, editing and publishing activities general audience. Awarded to Tim Birkhead that enhance an appreciation for wildlife. ZSL Prince Philip Award FRS, University of Sheffield, for his book and Marsh Prize The Most Perfect Thing: Inside (and Outside) ZSL Marsh Award for Awarded to an A-Level or Higher student a Bird’s Egg. Conservation Biology for an outstanding biology project. Awarded For contributions of fundamental science to Alexandra Eyles-Owen, Surbiton High ZSL Medal and its application to the conservation School, for her project ‘Dietary turmeric Presented to a member of staff for outstanding of animal species and habitats. Awarded reduces inflammation and improves achievement and service to ZSL. Awarded to to Richard Griffiths, University of Kent, for mood and mobility in horses with fetlock Paul Pearce-Kelly for significant contributions significant contributions to amphibian and joint inflammation’. to invertebrate conservation. reptile conservation. ZSL Charles Darwin Award ZSL would like to thank the Marsh Marsh Award for Marine and and Marsh Prize Christian Trust and Clarivate Analytics Presented for the best zoological project by an Freshwater Conservation for their generous support of our For contributions of fundamental science undergraduate student attending university scientific awards programme and its application to conservation in marine in the UK. Awarded to Simon Chen, University

36 ZSL Science Review 2016-17 zsl.org Below left: Shinto John, Victoria Wilkinson, Becki Below right: the Institute is carrying out imaging Lawson and Katharina Seilern-Moy of the Garden surveys of Greenland’s ocean floor Wildlife Health team FUNDING

Funding The Institute depends on funding from a wide source of Funding organisations Arcus Foundation donors, including the Higher Education Funding Council ASCOBANS Conservation Fund AXA Foundation for England, to carry out its research. Bertarelli Foundation Biotechnology and Biological Sciences Research Council (BBSRC) carbon sinks and nurseries for juvenile fish. Sustainable fishing in the Arctic British Ecological Society Kirsty Kemp and Chris Yesson were Trawl fisheries directly impact the seabed Crown Estate (Marine Stewardship Fund) awarded £250,000 from the IUCN/European by removing target species and damaging Darwin Initiative Commission Biodiversity and Ecosystem vulnerable, habitat-forming organisms. We DEFRA Services in Territories of European are carrying out imaging surveys of the West Environment Agency Overseas (BEST) programme for the project Greenland benthos to document existing Environment Canada ‘Sustainable fishing in the Arctic: Can the seafloor communities from 200-1,000m Esmee Fairbairn Foundation harvest of Greenland’s biggest export be depth. Our surveys will revisit the sites of European Commission compatible with the conservation of benthic historical photographic surveys to provide Higher Education Funding Council for ecosystems?’ Greenland’s west coast is home a unique perspective of changing habitats England (HEFCE) to commercially important cold-water prawn in relation to climate change and fishing Honolulu Zoo and halibut fisheries. However, entrance of pressure. A real strength of this project is the Howard Buffett Foundation the fisheries into the Marine Stewardship breadth of engagement across Greenlandic IUCN Council sustainability scheme revealed a society, from school children to fishermen IUCN/European Commission – Biodiversity lack of knowledge of Greenland’s ocean floor. to policymakers. The project will help to and Ecosystem Services in Territories of European Overseas (BEST) Programme Benthic habitats play vital roles in marine ensure the long-term sustainability of key Laurentian University ecosystems, for example, functioning as Greenlandic fisheries. Marine Institute Maungatautari Ecological Island Trust Medical Research Council National Geographic Society Natural England Natural Resources Wales Natural Environment Research Council (NERC) Oceanario Lisboa Pauline Meredith Charitable Trust Royal Society Royal Society for the Protection of Birds Royal Society of New Zealand (Marsden Fund) Rufford Foundation Science and Technology Facilities Council Southoe Consultancy Ltd St Louis Zoo Sustainable Fisheries Greenland Taronga Conservation Society Australia Thriplow Charitable Trust period (2016-2019) to support GWH’s public Garden Wildlife Health Universities Federation for Animal Welfare Garden Wildlife Health (GWH) is a citizen outreach and information dissemination (UFAW) science project that investigates diseases activities. We aim to inform the public, and University College London affecting amphibians, reptiles, garden conservation NGOs and their members, University of Cambridge birds and hedgehogs in Great Britain, and about disease threats to wildlife conservation University of Edinburgh their conservation significance. Institute and to offer evidence-based practical Wildlife Conservation Society veterinary scientists coordinate the GWH solutions to safeguard wildlife health. Online WWF International project in collaboration with partners at resources include a library of disease fact WWF Namibia the British Trust for Ornithology, Froglife sheets, e-newsletters, social media, and WWF UK and the Royal Society for the Protection of informative signage within the new Wildlife Birds. The Animal and Plant Health Agency Garden at ZSL London Zoo, designed to If you are interested in helping to fund helps fund the disease investigations, and provide visitors with tips on how to enhance ZSL’s vital work, call 0344 225 1826 or the Esmée Fairbairn Foundation awarded a their garden habitats for native wildlife find out more at zsl.org/support-us second grant of £150,000 over a three-year species. gardenwildlifehealth.org

zsl.org ZSL Science Review 2016-17 37 GOVERNANCE AND STAFF

Governance and staff ZSL would like to thank its students, interns, volunteers and collaborators, as well as its staff.

ZSL/University College Sarah Durant, Theme Leader, Postgraduate London Joint Committee People, Wildlife and Ecosystems Research Students University College London Trenton Garner, Theme Leader, Mario Andres Alvarado Rybak Frances Brodsky (Director, Evolution and Molecular Ecology Judith Ament Division of Biosciences); Chair Tim Blackburn, Professor of Paul Barnes Helen Chatterjee (Professor Invasion Biology (UCL/ZSL) Kieran Bates of Biology, UCL Biosciences, John Ewen Katie Beckmann Head of Research and Teaching, Paul Jepson Dominic Bennett UCL Culture) Malcolm Nicoll Katherine Booth-Jones Andrew Pomiankowski (Head of Nathalie Pettorelli Matilda-Jane Brindle Department, Research Strategy Marcus Rowcliffe Stephanie Brittain Director of CoMPLEX) Anthony Sainsbury Adam Britton Geraint Rees (Dean, Faculty of Samuel Turvey Sarah Brooke Life Sciences) Jinliang Wang Ella Browning Rosie Woodroffe Lewis Campbell ZSL Peter Carr Ralph Armond (Director General) Postdoctoral Philip Chapman Geoff Boxshall FRS (ZSL Secretary; Research Staff Charlotte Clarke Natural History Museum) Monika Böhm Sérgio da Silva Henriques Sir Cyril Chantler (Honorary Fellow; Patricia Brekke, Anthony Dancer Daniella Rabaiotti former Chairman UCL Partners) Postgraduate Tutor Clare Duncan Cassandra Raby Ian Owens (Natural History Jessica Bryant Sally Faulkner Jonathan Rio Museum) David Curnick Guilherme Ferreira Charlotte Selvey David Daversa Liam Fitzpatrick Rebecca Short In Attendance Ellie Dyer Deborah Fogell Thomas Smallwood Edward Hall (Head of Finance, Robin Freeman Victoria Franks Donal Smith School of Life and Medical Mona Fuhrmann Helen Gath Fiona Spooner Sciences, UCL) Rosemary Groom Cally Ham Gemma Taylor David Meech (Divisional Manager, Xavier Harrison James Hansford Joseph Taylor Biosciences, UCL) Audrey Ipavec Anne Hilborn Andrés Valenzuela Sánchez Loren Moyse (Faculty Manager, David Jacoby Michael Hudson Rosie Williams Life Sciences, UCL) Kirsty Kemp Freya Jephcott Juliet Wright Cheryl Buffonge (Science Becki Lawson Sarah Johnson Operations Manager, ZSL) Tom Letessier Angharad Jones EZCM Resident Fiona Evans (Human Resources Nicholas Mitchell Samuel Jones in Wildlife Director, ZSL) Alexandra Morel Natoya Jourdain Population Health Ken Norris (Director of Science, Adam Piper Alexander Knight Helle Bernstorf Hydeskov Institute of Zoology, ZSL) Stephen Price Kate Lee Amanda Smith (Finance Director, ZSL) Alexa Varah Stephen Long Project Coordinator Piero Visconti Heidi Ma Becky Shu Chen IoZ Oliver Wearn Gwendolyn Maggs Ken Norris, Director of Science Christopher Yesson Agnese Marino Taussig Interns de Bodonia Matthew Bennion Senior Research Staff Postgraduate Claudia Martina Luna Isabel Nicholson Thomas Andrew Cunningham, Deputy Research Staff Kirsten McMillan Holly Pringle Director; Theme Leader, Stefanie Deinet Thalassa McMurdo Hamilton Wildlife Epidemiology Jenny Jaffe Lisa Mogensen Technical Staff Chris Carbone, Theme Leader, Valentina Marconi Daniel Nicholson Kelly Astley Biodiversity and Macroecology Louise McRae Helen O’Neill Robert Deaville, Cetacean Guy Cowlishaw, Theme Leader, Katharina Seilern-Moy David Orchard Strandings Programme Manager Behavioural and Population Victoria Wilkinson Diana Alexandra Louise Gibson Ecology; Postgraduate Tutor Hannah Wood Penafiel Ricaurte Dada Gottelli, Chief Technician

38 ZSL Science Review 2016-17 zsl.org Below: a red-footed booby (Sula sula) in the British Indian Ocean Territory – the orange mark on the breast indicates it is carrying a GPS tracking device to record where it forages at sea

Patron Her Majesty The Queen His Royal Highness The Prince of Wales (Vice Patron)

ZSL Council Members 2016 President: Sir John Elizabeth Passey Beddington CMG FRS Maggie Redshaw Secretary: Geoff Boxshall FRS Sean Rovai+ Treasurer: Paul Rutteman CBE Martin Rowson Sheila Anderson MBE (Vice President) (Vice President) Ken Sims Brian Bertram Paul Wilson Martin Cooke Victoria Wilson+ Ray Heaton* Robert Wingate* Andrew Kitchener+ Ken Livingstone** * to June 2016 Professor Anna Meredith ** retired March 2016 Ruth Padel* + from June 2016 ZSL Directors Director General: Director of Science: Ralph Armond Ken Norris Conservation Finance Director: Programmes Director: Amanda Smith Jonathan Baillie** Commercial and Human Resources Director: Communications Director: Kevin Hopkins, Senior Technician Lynne Rushton, Health & Safety Fiona Evans Rich Storton Seth Jackson Administrator Zoological Director: Development Director: Inez Januszczak Alexandra Thomas, Wildlife David Field James Wren Shinto John Health Bridge Coordinator Director of Conservation: *from June 2017 William Leung Isla Watton, Soapbox Science Matthew Hatchwell* **to November 2016 Matthew Perkins, Coordinator Senior Technician Chris Sergeant, Animal Technician Scientific Publications Library Tony Fooks, Celia Serrano and Meetings Ann Sylph MCLIP, Librarian Animal Health and Linda DaVolls, Head of Scientific Sarah Broadhurst, Veterinary Laboratories Administrative Staff Publications and Meetings Archivist and Records Manager Agency Cheryl Buffonge, Science Fiona Fisken, Managing Editor, Emma Milnes, Deputy Librarian Simon Goodman, Operations Manager International Zoo Yearbook James Godwin, Library Assistant University of Leeds Denise Bamfo, PA to Director Jennifer Howes, Scientific Kate Jones, and Administrator Events Coordinator Honorary University College London Amrit Dehal, Information Elina Rantanen, Research Fellows James Wood, Systems Administrator Journals Manager Sarah Ball University of Cambridge

Publication acknowledgements Contact us Design and editorial coordination: Think Monika Böhm, Patricia Brekke, Jessica Bryant, IoZ enquiries 020 7449 6610 Head of Scientific Publications Alicia Carter, Charlotte Clarke, Guy Cowlishaw, The Zoological Society of London, and Meetings: Linda DaVolls Dave Daversa, Ben Dean, Sarah Durant, Robin Regent’s Park, London NW1 4RY Publishing officer: Jonathan Kemeys Freeman, Helen Gath, Trent Garner, James zsl.org/science Editorial consultants: Claire Sargent, Godwin, Rosemary Groom, Lucy Hulmes – Registered charity in England and Claire Sweeting Centre for Ecology & Hydrology, Seth Jackson, Wales: no 208728 Art director: George Walker Bernice Kohl, Ivan Kuzmin/ZSL, Mhairi Sub-editors: Rica Dearman, McCready, Russ Miles, Royal College of Marion Thompson Veterinary Surgeons, Martin Sanders, Scottish © ZSL and contributors 2017. All rights Marine Animal Strandings Scheme, reserved. Printed on 100% recycled paper. Shutterstock, John Sibley, Dan Sprawson, We extend thanks to all ZSL staff and other Malcolm Nicoll, Victoria Wilkinson, ZSL Cover: colleagues for the use of images, including: John Sibley.

zsl.org ZSL Science Review 2016-17 39 Animals and their habitats face increasing threats across the world. Through our scienfic research we are helping to build a future where animals are valued and their conservaon assured. ZSL is a registered charity in England and Wales no: 208728

The Zoological Society of London zsl.org

Regent’s Park London NW1 4RY and at:

ZSL Whipsnade Zoo Dunstable Bedfordshire LU6 2LF

For a closer look at ZSL’s work, look out for our other annual publications at zsl.org/about-us/zsl-annual-reports

ZSL Annual Report and ZSL Conservation Review 2016-17 Accounts 2016-17 An in-depth look at our conservation Our annual overview of the year, and research, showing how we are featuring our Zoos, fieldwork, achieving our key targets at home science and financial statements. and abroad.

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