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Contents 3 Are we doing the right type of conservation science? 8 Training two captive Sumatran orang-utans for ultrasound scanning 11 As dead as a dodo – when do we declare a species Extinct? 13 Conservation and data management 17 Morbidity of Alaotran gentle lemurs at Durrell Wildlife Park 22 Effects of diet on the health of captive Geoffroy’s marmosets 25 Biodiversity loss in Gerald Durrell’s early works 27 Assessing muscle condition in captive Livingstone’s fruit bats 30 Conservation update on the ploughshare tortoise 33 Seed dispersal by ecological replacement Aldabra giant tortoises Welcome to Solitaire 27. This issue starts with a very thought-provoking essay by Professor Richard Griffiths that highlights some of the problems both field and zoo-based conservationists face not only in doing high quality research, but in communicating it to the rest of the conservation world. These are problems Durrell’s staff and students face regularly, and they are problems for which Solitaire is trying to provide some solutions. Although we are aiming at the highest standards, we are often working with small numbers of individuals, and in situations that cannot be easily, if ever, repeated. Solitaire is an outlet for such studies, making our results available to a wider audience and, hopefully, stimulating more research and encouraging collaboration. This year’s Solitaire demonstrates perfectly what we are trying to do to improve evidence-based conservation and the management of threatened species. Articles range from descriptions of techniques that have the potential to be of benefit to a wide variety of species – for example, habituating our female Sumatran orangutans to ultrasound equipment so that they can be monitored during pregnancy without stress – through updates on vitally important conservation initiatives in the field, to basic research on biology, behaviour and health, providing information that forms the essential underpinning of any conservation action. I hope you enjoy this issue and that it gives you an insight into the huge range of work that Durrell is doing around the world to achieve its mission of saving species from extinction. Very best wishes Solitaire No. 27 Eluned Price Wildlife Park Research Coordinator [email protected] Cover photo: Alaotran gentle lemur (James Morgan) 2 Guest essay Are we doing the right type of conservation science? Richard Griffiths Durrell Institute of Conservation and Ecology, University of Kent Although he had no formal scientific training , Gerald Durrell recognised the importance of a systematic, scientific approach to animal husbandry and conservation very early on in his career. Few other zoos embraced this philosophy at the time, which meant that the Jersey Zoological Park was founded using scientific principles that have continued to underpin the organisation through to the present day. Indeed, many zoos – and many of the broader conservation organisations – have been playing catch-up, as ‘evidence-based decision making’ has become increasingly recognised as an essential component of good management practice. However, the ‘evidence’ that is needed to do effective conservation is often complex, costly, and time-consuming to accumulate. In addition, there are often competing pressures on researchers that dictate the type of research that they do. So what type of data do we need to inform sound conservation and how do we go about collecting, analysing and disseminating the results? Hard and fuzzy data The terms ‘science’, ‘research’ and ‘evidence’ are often used synonymously, but actually mean slightly different things. When we talk about ‘evidence’ we refer to factual information to support conservation needs. This information may take a variety of forms – published papers and reports, quantitative data, qualitative data, or even information residing in the heads of experts that is extracted during a workshop. However, scientists are a sceptical lot that need a lot of convincing. The scientific method is rooted in rigorous hypothesis testing using designs that incorporate observational, experimental or theoretical methods (or preferably a combination of all three). This is fine if you are working in a physics lab where It has been difficult to publish field research on the impacts of predation on the Mallorcan midwife toad because of small sample sizes (Photo: Richard A. Griffiths). Solitaire No. 27 3 Guest essay extraneous variables can be neatly controlled, or even if you fuzzy data that might cause a journal editor to wince, but it still are working on fruitflies where multiple generations can be may be valuable. For some endangered species it is not unusual bred in a couple of months in a converted broom-cupboard. for there to be practically no data at all, and in such cases you For larger scale ecological and conservation questions, aphave to rely on opinions from experts or from local people plying the scientific method is enormously challenging. who are familiar with the species or habitats. Fortunately, a In addition to the problem of scale, you may find you are range of methods are available to obtain such data, and these working on a rare and cryptic species that confounds the reare being increasingly embraced within conservation. The quirements of sample size and research design. We recently Population and Habitat Viability Analysis workshop process investigated how much survey effort would be has been invaluable in extracting information needed to reliably detect a population change from experts and using it to build population in a threatened amphibian species. Our “Within conservation, models of a whole range of threatened statistical models revealed that using traspecies (e.g. Conservation Breeding ditional methods we would actually need scientific rigour needs to Specialist Group 2016). As individual to monitor more sites than were actually experts are not always right (Austen at in existence to reliably detect a decline! be laced with a healthy al. 2016), there are also various tools On another occasion, we were doing fieldavailable for consensus building among work in a remote mountain range on a very dose of pragmatism” experts and consolidating information in rare endemic frog – the Mallorcan midwife a systematic and balanced way (e.g. Pullin toad – that was threatened by introduced predaet al. 2004; MacMillan & Marshall 2006; tors. We stumbled upon a small pond where it was uniquely Sutherland et al. 2011). In China, carrying out standard possible to do a predator removal experiment. We took some surveys of the giant salamander in streams and rivers has counts and measurements, and then duly removed the predaproved to be logistically challenging. However, a survey of tors and monitored the impacts on the ecology, behaviour local communities has revealed extremely useful information and morphology of our rare frog over the coming weeks – a about past and present status and distribution (Pan et al. 2015). simple ‘before’ and ‘after’ field experiment using a single Scientists are starting to appreciate that within conservation, site. The results were quite compelling and showed signifiscientific rigour needs to be laced with a healthy dose of cant predator impact, but we have never been able to publish pragmatism, and that the timescales needed for conservation the results. This is because referees of the paper deemed it action are usually substantially shorter than those needed to do insufficiently replicated. To do it properly we would have the relevant conservation research. Indeed, analytical methods needed to find at least another 10 sites with predators and anare now emerging that combine available quantitative data other 10 without predators to act as controls. Unfortunately, with expert opinions (Kuhnert et al. 2010), and these have such sites were just not available. considerable potential for informing conservation practice. So what do we do when we just cannot get hard data? The simple answer is you have to work with what you have got When do we stop doing research and start doing and make an informed decision. This may include unpublished conservation? So when do we decide that we have accumulated enough evidence to make an informed decision about a conservation intervention? This problem was neatly summarised by McCoy (1994) when considering what we do about amphibian declines: ‘…do ecologists wear their conservationist hats and muster their expertise in defense of life, or do they wear their scientist hats and muster their expertise in defense of “truth”?’. At one end of the spectrum, if conservationists have insufficient evidence to support a management intervention there is a risk they make an expensive mistake. At the other end of the spectrum, if they are too cautious and delay action until all necessary evidence has been assembled, the species may be extinct. Amphibian conservation provides examples of both extremes. In the early days of natterjack toad conservation in the UK, there was concern that ponds were drying up too early and killing all the tadpoles. The solution at the time seemed quite simple – deepen the ponds to make them more permanent. Unfortunately, this made the ponds much more attractive to predators and competitors that were unable to survive in temporary ponds, with the result that the natterjacks were actually worse off. Longer term research revealed that breeding in temporary ponds and occasional loss of natterjack tadpoles to desiccation is actually quite normal and part of Conservation management of the natterjack toad has a wider metapopulation process. These are long-lived toads been altered in light of long-term data on its requirements and only need one or two seasons of reproduction in their (Photo: Bernard Dupont, Creative Commons Attributionlifetime to keep the population ticking over. As a result of Share Alike 2.0 license). Solitaire No. 27 4 Doing conservation science editorial aspirations of enlightened scientific journals, and the assessment criteria of grant panels. However, the crossdiscipline push in conservation has been largely spearheaded from within one discipline – natural sciences. This is perhaps not surprising, as natural scientists are generally a highly collaborative lot that relish engagement with those working in other fields and learning new methodologies. Equally, there are rather a lot of natural scientists being churned out by universities (I count myself as one of the crowd). Perhaps it is also not surprising, then, that the heads of many conservation organisations have received a fairly traditional training in biology. However, I see far fewer researchers from the social sciences and humanities moving into cross-disciplinary conservation research. There are a number of related issues that emerge from this trend. Firstly, what is – and what is not – good cross-disciplinary research depends on the discipline you come from. An ecologist may wax lyrical about how the application of an economic model to an ecological system The golden toad became extinct despite being well-studmay be highly revealing, while an economist may regard ied in the wild. this as both misleading and pedestrian. A social anthropologist may elegantly reveal how cultural practices influence attitudes to conservation using qualitative methodologies, but a biologist may dismiss the findings because they are not based on quantitative data that have been analysed statistically. Academic institutions are still organised around this research the management programme was adjusted disciplinary structures that were formulated in the distant accordingly (Beebee 1993). The extinction of the golden past, and forging effective collaboration between researchers toad of Costa Rica has gone down as one of the classic with different world views and philosophies may be difficult stories of amphibian declines. The toad was once abundant (Evely et al. 2010). in the Monte Verde rainforest and was quite well-studied, but There are certainly good examples of ecologists, declined to extinction within a couple of years (Crump et al. geneticists, veterinarians, spatial modellers, economists, 1992). Conservationists subsequently criticised scientists for planners, lawyers and social anthropologists all doing their letting this happen, and suggested that there was a missed bit in a research project for the greater good. However, these opportunity to set up a safety-net population in captivity collaborations often fail to integrate methodologies at any (Harding 1993). Whether this was a sensible depth or embrace the public or conservation option at the time remains debateable, but practitioners (Evely et al. 2010). Because these two cases illustrate the dilemma “Many fundamental of the predominance of natural that conservationists face when trying scientists within conservation, it to assess the evidence to support conservation problems require also means that cross-disciplinary conservation management. research often leans towards the The sad reality is that we rarely small data that are basic yet research philosophies associated with have the luxury of being able to decide that discipline. Despite the upbeat when to – or when not to – intervene still challenging to collect.” talk coming from funding agencies on the basis of available evidence. The and journals, with research quality decision is often made for us by extraneous circumstances, benchmarks firmly rooted within traditional disciplines it is such as political agendas, availability of funding and difficult to give novel cross-disciplinary research the exposure, timeliness. In such circumstances, all we can do is synthesise support and uptake it needs. If conservation is to truly benefit what is available at the time from all sources of hard and fuzzy from cross-disciplinary research then two challenges must data, and make an informed decision on the basis of that. be surmounted: (1) getting a better balance of researchers involved across the relevant disciplines; and (2) developing Cross-disciplinary research an infrastructure for integrating the contributions from the That conservation requires an approach that straddles differdifferent disciplines more effectively. ent disciplines to solve all its problems has become something of a mantra in recent years. For example, ecologists may be Big data and small data needed to assess populations and habitats, veterinarians to Globalisation, new technologies and scientific advances do health checks, social scientists to examine the role of lohave meant that we can now tackle problems with millions cal communities, lawyers and policy makers to work out of data points that would have been completely intractable a how any plan fits with the political agenda and economists few years ago. The laptop that I am now writing this article to work out the cost-effectiveness. Ideally, some overarchon has more computer power than the truck-sized mainframe ing recommendations should emerge from all this research. computer that analysed my PhD data some years ago. The This discipline-diverse approach is reflected in the mission availability of such technology is therefore driving scienstatements and staff profiles of many organisations, in the tists to address bigger and bigger problems with larger and Solitaire No. 27 5 Guest essay The way forward? Despite the shortcomings in research meeting conservation needs, this is not an issue that has gone ignored by the conservation and research community. Indeed, exploring the science-implementation gap is becoming something of a topical research discipline in itself (e.g. Arlettaz et al. 2010). At the institutional level, some of the issues are being addressed. My own institution – DICE – was founded back in 1989 specifically to bridge the gap between social and natural sciences and between research and implementation. That mission remains as relevant today as it was over a quarter of a century ago, and over this period DICE has equipped over 900 graduates from nearly 100 countries with the cross-disciplinary tools needed to tackle conservation problems. I actually feel quite proud that the majority of our graduates have gone on to forge careers in conservation practice rather than join the treadmill of academia. Indeed, many have gone on to become leaders in their respective fields and pass on their skills and knowledge to a new generation of practitioners. The conservation evidence initiative based at Cambridge University is another project that aims to identify the key questions that are most important to practitioners and develop mechanisms to make research results and other forms of evidence more accessible to practitioners (http://www.conservationevidence.com/). This has resulted in several syntheses of conservation evidence focusing The scientific journal problem on specific problems or taxa. In addition, the open access Unfortunately, publishing conservation research in scientific journal Conservation Evidence has been developed specifijournals has become something of a high-stakes game in recally to publish case studies of conservation interventions by cent years. Within academia, careers, promotions and grant practitioners. These are exactly the sort of funding all depend on not so much case studies that would have difficulwhat you are publishing but where you are publishing it. Getting your “Journals increasingly shun ty in getting published in mainstream journals, and would end up buried in work into a broad, mainstream inaccessible reports or possibly not journal – such as Nature or Scistudies based on single written-up at all. In addition to being ence – will indeed be a cause to completely open access to all, Conserpop open the champagne. As journals species or single ecological vation Evidence is also unusual in that strive towards broad readership, they init levies no page charges. The Centre for Evidence creasingly shun studies based on single species systems” Based Conservation at Bangor University (http://www. or single ecological systems unless they can shed cebc.bangor.ac.uk/) promotes evidence-based conservation light on problems of wider interest. However, most practipractice through the development of systematic evidence tioners are more concerned about how to best manage their reviews, and also produces an open access journal, Environspecies or site rather than the broader scientific relevance of mental Evidence. In Australia, the Centre of Excellence for doing so. So this results in several trends. Firstly, conservaEnvironmental Decisions (CEED: http://ceed.edu.au/) was tion journals publish a lot of papers on broad, generic topics set up in 2011 to carry out research to solve environmental that are of little relevance to conservation because practiproblems and evaluate the outcomes. From the initiative has tioners have not asked the question that is being addressed. emerged an online magazine, Decision Point, which carries Secondly, most conservation research is carried out in the lively articles and viewpoints on a wide variety of environdeveloped world on species and systems that may not be top mental decision-making and the research that informs it. conservation priorities (Milner-Gulland et al. 2009; Griffiths Scientific journals – the vehicles by which knowledge & Dos Santos 2012). Thirdly, scientists are getting quite is disseminated – are also having to adapt to a rapidly clever at dressing up their research in grandiose narratives changing research landscape. Governmental drivers towards that make it sound more widely relevant than it actually is. research transparency and making publically-funded research On top of these issues, is the fact that in true Orwellian fashaccessible to all means that research findings no longer need ion, some animals are more equal than others. For example, to be buried in a journal only available to those paying a Bonnet et al. (2000) neatly showed that if you are working subscription: they can be found online with a few few clicks on ‘more popular’ mammals and birds, you can get away of a mouse. Much cross-disciplinary research falls between with less conceptual/theoretical introductory material in a the stools of traditional journals, and open access journals that research article than if you are working on fishes, amphibpublish on technical merit – rather than prevailing fashions, ians and reptiles. So if you want to publish your desert lizard agendas and perceptions of what is of ‘broad interest’ – are paper in a top journal, try and slip in the species and habitat providing a welcome home for much research that crosses names later on in the paper, after you have framed it in some the divides. grander, more theoretical problem of global importance. more complex data sets. Of course, this is all very worthwhile. If we are ever to fully understand the impacts of climate change, for example, we must continually build and test increasingly sophisticated models that stretch available computer power. However, many fundamental conservation problems require small data that are rather basic yet still very challenging to collect. Species conservation action plans are often hamstrung by the absence of a basic understanding of such things as survival rates, number of offspring and the factors regulating population size. Obtaining such small data on rare – and often cryptic – species may take several years of challenging fieldwork. This may be beyond the timeframe of a conventional research grant, and beyond the patience of a smart young scientist keen to progress quickly through the academic ranks. When the hard-won data are eventually written-up, it is quite likely that the editor of a high-impact journal will regard the work too limited in taxonomic and geographical scope to be of general interest. This creates further disincentives to pursue small data projects and motivates ambitious researchers to engage ever-more enthusiastically with the big data agenda. Is it therefore surprising that conservation practitioners bemoan the fact that scientists are doing work that manifestly fails to address their on-the-ground needs? Solitaire No. 27 6 Doing conservation science Despite the drive towards big data over small data, there is also a move towards increasing employability of graduates and improving the impact of research. A mechanism by which this can be achieved is through partnerships between Universities and research-users, such as conservation agencies and zoos. Most conservation agencies do not have the resources they would like to pursue all of their goals, and student interns can be an extremely cost-effective way of dealing with this. Indeed, it can be a ‘win-win’ situation – the student gains valuable work experience that will enhance the CV while the organisation gains an extra pair of hands in the office or field at little extra cost. Furthermore, students carrying out dissertation projects within conservation organisations can often collect badly needed small data that would otherwise not be considered a priority for a University supervisor. So conservation science seems to be moving in the right direction, but perhaps not at the speed that conservation needs it to. References Arlettaz, R, Schaub, M, Fournier, J, Reichlin, TS, Sierro, A, Watson, JEM and Braunisch, V (2010). From publications to public actions: when conservation biologists bridge the gap between research and implementation. Bioscience 60: 835-842. Austen, GA. Bindemann, M, Griffiths, RA and Roberts, DL (2016). Species identification by experts and non-experts: comparing images from field guides. Scientific Reports 6: 33634. DOI: 10.1038/srep33634. Beebee, TJC (1993). Conservation of the golden toad. British Herpetological Society Bulletin 46: 28. Bonnet, X, Shine, R and Lourdais, O (2000). Taxonomic chauvinism. Trends in Ecology and Evolution 17: 1-3. Conservation Breeding Specialist Group (2016). http://www. cbsg.org/our-approach/workshop-processes/phvaworkshop-process (accessed 16 October 2016). Crump, ML, Hensley, FR and Clark, K (1992). Apparent decline of the golden toad: underground or extinct? Copeia 1992: 413-420. Evely, AC, Fazey, I, Lambin, X, Lambert, E, Allen, S and Pinard, M (2010). Defining and evaluating the impact of cross-disciplinary conservation research. Environmental Conservation 37: 442-450. Griffiths, RA and Dos Santos, M (2012) Trends in conservation biology: Progress or procrastination in a new millennium? Biological Conservation 153: 153-158. Harding, KA (1993) Conservation and the case of the golden toad. British Herpetological Society Bulletin 44: 31-34. Kuhnert, PM, Martin, TG and Griffiths, SP (2010). A guide to eliciting and using expert knowledge in Bayesian ecological models. Ecology Letters 13: 900–914. MacMillan, DC and Marshall, K (2006). The Delphi process – an expert-based approach to ecological modelling in data-poor environments. Animal Conservation 9: 11-19. Milner-Gulland, EJ, Fisher, M, Browne, S, Redford, KH, Spencer, M and Sutherland, WJ (2009) Do we need to develop a more relevant conservation literature? Oryx 44: 1–2. McCoy, E (1994). “Amphibian decline”: a scientific dilemma in more ways than one. Herpetologica 50: 98-103. Pan, Y, Wei, G, Cunningham, AA, Li, S, Chen, S, MilnerGulland, EJ and Turvey ST (2015). Using local ecological knowledge to assess the status of the Chinese giant salamander Andrias davidianus in Guizhou Province, China. Oryx 50: 257-264. Pullin, AS, Knight, TM, Stone, DA and Charman, K (2004). Do conservation managers use scientific evidence to support their decision-making? Biological Conservation 119: 245–252. Sutherland, WJ, Fleishman, E, Mascia, MB, Pretty, J and Rudd, MA (2011). Methods for collaboratively identifying research priorities and emerging issues in science and policy. Methods in Ecology and Evolution 2: 238-247. Professor Richard Griffiths is Professor of Biological Conservation at the Durrell Institute of Conservation and Ecology, University of Kent. He has had a long association with Durrell and in particular with Durrell Conservation Academy. E-mail: [email protected] Keep in touch Durrell Conservation Academy Like our page, share our information and help spread the word so we can achieve our mission – saving species from extinction Durrell Conservation Learning Network Keep in touch with other graduates, access useful information, comment, post & share links by joining this Alumni Group Solitaire No. 27 7 Technical report Operant conditioning two captive Sumatran orang-utans to present for ultrasound scanning Sarah Fowkes and Melissa Frost Durrell Wildlife Conservation Trust Abstract Using operant conditioning through positive reinforcement to train captive apes to participate in veterinary procedures is a low stress alternative to inspection via anaesthesia. Two pregnant female orang-utans at Durrell Wildlife Conservation Trust were trained using positive reinforcement techniques to present for voluntary ultrasound scanning to monitor foetal development. The two females differed in their response to training, but both were successfully monitored during pregnancy and delivered healthy infants. Key words: Pongo abelii, positive reinforcement, pregnancy, sonograph, training Introduction There is a growing trend in zoological, veterinary and laboratory communities to recognise the value of using operant conditioning as an animal care and management tool. The use of operant conditioning to train non-human primates to co-operate with routine scientific, husbandry, and veterinary procedures is recommended by many legislative and professional guidelines (Home Office 1989; International Primatological Society 1989). Training is recommended as it has been shown to reduce fear, anxiety and distress caused by traditional captive management procedures such as anaesthesia (Reinhardt et al. 1995). In positive reinforcement based training, animals are rewarded with something they like for responding to a caregiver’s cue or command (Laule et al. 2003). The positive reinforcement approach to non-human primate captive management is now used in zoological communities to increase primate welfare by successfully supporting the cooperation of captive primates in animal transfers (Bloomsmith et al. 1998) and husbandry procedures, including veterinary interventions, while improving the rapport between keeper and animal (Savastano et al. 2003). Colahan and Breeder (2003) trained captive primate populations at Disney Animal Kingdom to display a wide range of behaviour using positive reinforcement to improve animal care, veterinary inspection and infant care. For example, positive reinforcement was used to train pregnant females for separation from groups for inspection, breast manipulation for lactation assessment and infant pick-up, present and holding behaviours. This paper discusses how two pregnant female orang-utans at Durrell Wildlife Conservation Trust were trained to present voluntarily for ultrasound scanning to monitor foetal development using positive reinforcement techniques without the need for anaesthesia. Solitaire No. 27 Methods Subjects Operant conditioning was used to train two pregnant female Sumatran orang-utans housed at Durrell Wildlife Conservation Trust, Dana (25 years old) and Annette (30 years old) to present their abdomens for ultra sound scanning. Training area Training was conducted in the exit tunnels of the exhibition areas of the orang-utan building as the mesh was large enough to pass an ultrasound probe through and subjects could be easily isolated (see Fig. 1). Figure1. Annette at training station in exit tunnel. 8 Orangutan ultrasound training Positive reinforcement A training plan was first devised to outline the steps necessary to condition the subjects to present for ultrasound scanning. A positive reinforcement technique was then used to complete these steps. Conditioned commands, for example “touch”, were given by the keeper trainer. If this was followed by a conditioned response by the orang-utans, such as allowing the trainer to touch the abdomen, then a reward of a favoured food item was given. Once the conditioned responses became habituated, using the bridge phrase “good girl” was enough to sustain the behaviour and a reward was given only when the behaviour had been completed (see Fig. 2). Once one command had been learnt the next was introduced, resulting in the building of behaviours necessary for ultrasound scanning. All training sessions were recorded in daily reports. Materials A jackpot reward of three grapes was given when a new behaviour was first displayed. A reward of a single grape was then given when the behaviour was repeated. Grapes were used as a reward as they are a favoured food item that is not part of the orang-utans’ daily diet. A peanut was used initially but it was too highly prized a reward, resulting in the orang-utan becoming impatient and in turn frustrated during training sessions. The grapes were originally put in a yoghurt pot in sight of the orang-utan but this caused Dana and Annette to become quickly distracted. Therefore grapes were instead placed in a pouch attached to the trainer’s belt so that they were out of view, and this resulted in much higher levels of concentration. A fake ultrasound machine, constructed from card board boxes (see Fig. 3), was used to desensitise Dana to novel stimuli, while latex gloves and a damp cloth were used to desensitise her to novel textures. Annette did not have the same suspicion of novel stimuli so these items were not necessary for her training. Portable Sonosite Micromax© and Sonosite 180 Plus© scanners (see Fig. 3) were used to conduct the sonographs. Clear Image© medical ultrasound gel was used as a conductive medium between the skin and the ultrasound probes. Dana did not like the sensation of the gel but preferred medical gel to the Sonogel© that is typically used for veterinary scanning. As Dana was adverse to the gel, a trans-vaginal probe was initially used externally to conduct ultrasound scans with both subjects, as it required only a small amount of gel. A larger probe head with a depth of 22 cm was used later, once Dana was desensitised to the gel, as the trans-vaginal probe’s depth of only 10cm was not sufficient to gain clear images of Dana’s developing foetus. Non-invasive scanning enabled us to monitor the pregnancies carefully, and was particularly beneficial in Dana’s case, as she was considered at high risk because of a previous haemorrhage following a stillbirth (Maclachlan et al. in press). CC → CR → BRIDGE → R “touch”→ present stomach→ “good girl”→ grape Figure 2. Positive reinforcement used to train orang-tans to present for ultrasound training. Solitaire No. 27 Figure 3. (Above) Fake ultrasound machine, and (below) Sono 180 plus© portable ultrasound machine. 9 Technical report Table 1. Training steps for each female orang-utan. Step 1: Present stomach 2: Tolerate a fake probe 3: Desensitise to novel textures 4: Hold and bridge Dana Time taken to complete step 1 session If Dana put her stomach close to the mesh and allowed the keeper to touch it with her hand the command ‘touch’ was given, followed by a reward. 1 session If Dana tolerated the fake probe being pressed on her stomach when she presented it the ‘touch’ command was given, followed by a reward. 1 session A latex glove was placed over the fake ultrasound probe with ultrasound gel underneath to desensitise Dana to novel textures. If Dana tolerated the fake probe with the glove on the end of it being pressed on her stomach when she presented it the ‘touch’ command was given, followed by a reward. 4 sessions Dana given touch command to present her stomach and allow the fake probe to be pressed against her stomach. Probe held on her stomach and Dana given a ‘hold’ command. If Dana held her stomach in position for < 45 seconds without grabbing the probe then she was given a reward. The bridge word ‘good girl was used to sustain the hold behaviour until the reward was given Annette Time taken to complete step 3 sessions If Annette put her stomach close to the mesh and allowed the keeper to touch it with her hand the command ‘touch’ given, followed by a reward. Annette had no fear of novel stimuli so this step was skipped. Annette had no fear of novel textures so this step was skipped. 5 sessions 5: Desensitise to novel people 6: Desensitise to novel temps 1 session Dana rewarded for tolerating the presence 1 session of veterinary staff at training sessions 2 sessions 7: Introduce probe 5 sessions 8: Introduce ultrasound gel 5 sessions 9: Larger probe introduced 1 session Fake ultrasound probe covered with a warm damp cloth to mimic the temperature of ultrasound gel and Dana rewarded for presenting and holding her stomach on command and allowing keeper to touch her stomach with the cloth covered probe. This was then repeated with gel behind the cloth. Dana rewarded for presenting and holding 1 session on command for a novel trans vagianl probe Ultrasound gel put on end of probe. Dana 1 session rewarded for presenting and holding her stomach on command and allowing the keeper to touch her stomach with the gel covered probe for a successful ultrasound scan Dana rewarded for presenting and holding her stomach on command and allowing the keeper to touch her stomach with the larger gel covered probe for a successful ultrasound scan. Conclusion Operant conditioning was successfully used to train two pregnant female orang-utans for ultrasound scanning. The time investment devoted to train naïve animals was minimal but was affected by individual differences in the orang-utan’s temperament. Dana took 20 training session to complete a Solitaire No. 27 Annette given touch command to present her stomach and allow the fake probe to be pressed against her stomach. Probe held on her stomach and Annette given a ‘hold’ command. If Annette held her stomach in position for< 45 seconds without grabbing the probe then she was given a jackpot reward. The bridge word ‘good girl was used to sustain the hold behaviour until the reward was given Annette rewarded for tolerating the presence of veterinary staff at training sessions Annette had no fear of novel temperatures so this step was skipped. Annette rewarded for presenting and holding on command for a novel trans vaginal probe Ultrasound gel put on end of probe. Annette rewarded for presenting and holding her stomach on command and allowing the keeper to touch her stomach with the gel covered probe for a successful ultrasound scan Larger probe not necessary for Annette voluntary ultrasound scan, while Annette took only 11 sessions. Similar individual differences have been found at Durrell using a similar approach with tamarins (Brayshaw et al. 2015). Annette has a very trusting nature and enjoyed the interaction with staff members, and so she did not have to be desensitised to novel stimuli and participated in training 10 Orangutan ultrasound training sessions with enthusiasm. In comparison Dana has a history of medical interventions by keepers and veterinary staff, resulting in suspicion of novel stimuli and people. Dana also did not like the sensation of the ultrasound gel. Therefore Dana’s training involved more steps to desensitise her to these stimuli. We believe that the long-term welfare gains of monitoring the orang-utans’ pregnancies and the ability to conduct necessary ultrasound scanning in a low stress manner, outweigh the initial costs in time to train the subjects. The long-term welfare advantages of increased ease of veterinary assessment and treatment and the more subtle benefits of voluntary participation in management procedures and the building of trust between animals and care givers are vast. It should be noted that a key factor in the success of the training was consistency. A primary keeper trainer taught all the behaviours necessary for ultrasound scanning. A training plan was designed with each step outlined prior to interaction with the animals. Furthermore all training session were recorded in daily reports to keep track and to avoid missing or skipping training steps. These precautions were taken to reduce confusion and frustration for the orang-utans and to ensure training sessions were always a positive experience. The training steps could be used and are recommending for ultrasound scanning future pregnant orang-utans and other species. However using a clicker as a bridge instead of the ‘good girl’ vocal cue would be more effective as it would be consistent across keepers. More training for the keepers on how to position and manipulate the scanning probe to gain the best ultrasound images would also be of an advantage. In conclusion, operant conditioning, through positive reinforcement, can be used to train orang-utans to present for ultrasound scanning, increasing the wellbeing by reducing stress induced by veterinary procedures. Potential disadvantages of training are the lack of consistency between trainers and individual differences in subjects. The predominant cost of training is the time investment required to change behavioural repertoires. However the welfare benefits of positive reinforcement far outweigh these costs. References Bloomsmith, MA, Stone, AM and Laule, GE (1998). Positive reinforcement training to enhance the voluntar y movement of group-housed chimpanzees within their enclosures. Zoo Biology 17: 33–341. Brayshaw, SK, Lopez FJ and Wormell, D (2015). Ultrasound training for pregnancy monitoring in tamarins. Solitaire 26: 30–33. Colahan, H., and Breder, C. (2003). Primate training at Disney’s Animal Kingdom. Journal of Applied Animal Welfare Science 6: 235–246. Home Office (1989). Code of Practice for the Housing and Care of Animals Used in Scientific Procedures. London: Her Majesty’s Stationery Office. International Primatological Society (1989). IPS International guidelines for the acquisition, care and breeding of nonhuman primates. Primate Report 25: 3–27. Laule, GE, Bloomsmith, MA and Schapiro, SJ (2003). The use of positive reinforcement training techniques to enhance and care, management, and welfare of primates in the laboratory. Journal of Applied Animal Welfare Science 6: 163–173. Maclachlan, N, Hunt, G, Fowkes, S, Frost, M, Miller, J, PurcellJones, G, Sullivan, P, Barbon, A, Routh A., López FJ and Price EC (in press). Successful treatment of infertility in a female Sumatran orangutan Pongo abelii. Zoo Biology. Reinhardt, V, Liss, C and Stevens, C (1995). Restraint methods of laboratory nonhuman primates: A critical review. Animal Welfare 4: 221–238. Savastano, G, Hanson, A and McCann, C (2003). The development of an operant conditioning training program for New World primates at the Bronx Zoo. Journal of Applied Animal Welfare Science 6: 247–261. Sarah Fowkes formerly worked at Durrell Wildlife Park, specialising in the care of apes and Old World monkeys. She is now at Bristol Zoo. Mel Frost was a veterinary nurse at Durrell Wildlife Park at the time of this study. E-mail: [email protected] As dead as a dodo – when do we declare a species Extinct? Rosalind Kennerley Durrell Wildlife Conservation Trust; IUCN SSC Small Mammal Specialist Group (SMSG) There is no doubt that some species, such as the Dodo, sadly no longer exist. However, in some cases it is not always simple to come to a decision about whether the last individual of a species has truly disappeared or not. This article considers how the IUCN Red List of Threatened Species defines and applies the Extinct category, using a number of interesting examples that have come out of the Small Mammal Spe- Solitaire No. 27 cialist Group (SMSG)’s latest Red List reassessments that demonstrate some of the challenges involved. By December 2016 the SMSG had reassessed over two thousand species and assessed new species for the Red List. This updating of the Red List provides regular checks for species, which are crucial to our understanding of how the world’s wildlife is changing and for setting conservation priorities. 11 Essay The IUCN Standards and Petitions Subcommittee (2016) acknowledges that extinction is very difficult to determine. In the guidance provided by the IUCN, a species should be considered Extinct when there is no reasonable doubt that the last individual has gone. In order to presume extinction there should be evidence from exhaustive surveys in suitable habitat, which should be undertaken at appropriate times (diurnal, seasonal, annual), and throughout its historic range. Additionally, surveys should take place over a time frame appropriate to its life cycles and life form. So, what constitutes sufficient survey effort? In the following example it appeared to be a clear cut case. Most people will not have heard of the Bramble Cay melomys (Melomys rubicola), which became the first mammal likely to have been wiped out by severe storms and rising sea level, events which were probably exacerbated by human-induced climate change. It was the only mammal species endemic to Australia’s Great Barrier Reef and resident on one tiny island with an area of just five hectares. The severe weather and rising sea level caused dramatic habitat loss, making the cay gradually less inhabitable. After sightings became increasingly rare, researchers set out to capture any remaining individuals and start a captive breeding programme. The rescue mission to such a remote location required significant planning, and upon reaching the island five months later the team found no trace of the species despite targeted surveys. Given the small size of the island, the fact that almost no vegetation remained, and the level of surveying, it was a straightforward decision to reclassify the Bramble Cay melomys from Critically Endangered in 2008 (Leary et al. 2008) to Extinct (Woinarski and Burbidge 2016b) in the most recent Red List reassessment. However, questions were raised about this decision in the discussions in Gynther et al. (2016), who proposed that the species or a close relative may still exist in the Fly River delta region on the island of New Guinea. Whilst it is true that New Guinea warrants further comprehensive small mammal inventories, because it is only a hypothesis that this particular species may have originated from there, this is not sufficient reason to prevent the use of the Extinct category according to the IUCN definition. This unfortunate example of the Bramble Cay melomys extinction, which could have been avoidable, provides the specialist group with a timely reminder about the urgency to have a captive breeding strategy in place for species represented by the group and also that the threat of climate change needs to be taken into account within the strategy. The The Bramble Cay melomys, now extinct as a result of rising sea levels (Photo: Queensland Government, Creative Commons Attribution 3.0 Australia (CC BY) licence. Solitaire No. 27 first stage of producing this strategy will be to take stock of the current situation to identify the species which are already in captivity, and the purpose they fulfil within the collections. The second phase will then be to conduct a systematic needs assessment for ex-situ and in-situ captive breeding for SMSG species, using a series of questions and criteria to identify goals, threats and conservation options. The SMSG intends to have these prepared in 2017, with the aim of identifying species at most risk in the wild which are in need of immediate rescue to avoid extinction. There are inevitably a few situations where we have confirmation that the Extinct category was incorrectly assigned. An unusual case arose recently, which involved the Machu Picchu arboreal chinchilla rat (Cuscomys oblativa). Since the beginning of the Red List in 1982, this species has been considered Extinct, with the justification that it was described from just two skulls collected at an Inca burial site (Pacheco et al. 2008). These specimens were estimated to be around 400 years old and of unknown origin (Pacheco et al. 2008). This particular species featured very low down (number 77) on a list of 90 animals with fewer than five total sightings ranked in order of their probability of rediscovery (Fisher and Blomberg 2012). Remarkably, in 2009 C. oblativa was photographed and rediscovered. Finding living examples of taxa that were previously considered to be extinct represents a special case of the “Lazarus effect” and this has only been noted a handful of times among mammals and other vertebrates (Dawson et al. 2006). This term is usually used to describe the reappearance of taxa after a long absence in the fossil record (Fara 2001; Jablonski 1986). Interestingly, concerns had been raised previously that there was doubt over whether or not C. oblativa could still be found there, with Emmons (1999) suggesting that there was no actual evidence that it had become extinct since 1500 and that it was likely to be still extant. Despite these ideas, Pacheco et al. (2008) stated that the species was not detected during various surveys of the region. The current situation is that very little is known about the species and as a result it is now listed as Data Deficient (Roach 2016). Minimising subjectivity in Red List accounts is vital, as there will always be some differences of opinion about how to apply the guidelines. Indeed, this is reflected by the fact that guidelines for interpretation of the standards of evidence supportive of Extinct and Critically Endangered (Possibly Extinct) classifications are currently under development (IUCN Standards and Petitions Subcommittee 2016). Such guidelines would limit inconsistencies. In the example of the lesser stick-nest rat (Leporillus apicalis), there has been a lack of consensus across the years between assessors. It was listed as Extinct in all previous assessments, except in 2008, when it was moved to Critically Endangered by Robinson and Burbidge (2008). It was then declared Extinct again in the most recent reassessment (Woinarski and Burbidge 2016a). The switches between categories result from differences in the interpretation of the guidelines and also a paucity of data. The species is considered to have severely declined, predominantly due to predation by feral cats (Felis catus), though other threats may have contributed to its decline, for example predation by red foxes (Vulpes vulpes) and habitat degradation caused by introduced herbivores, in particular during severe droughts (Woinarski and Burbidge 2016a). The last two specimens of lesser stick nest rat were collected near Mt Crombie, south 12 Defining extinction of the Musgrave Ranges in north-western South Australia in 1933. Since then, there have been a couple of unconfirmed records, such as one from 1970 and occasional reports of fresh vegetation being added to old stick-nests. It seems likely that a species which builds such obvious nests would have been found, if still extant, but it is worth noting that much of this species’ range is in remote portions of central Australia that have not been fully surveyed. In conclusion, there will always be a degree of subjectivity about how and when to declare a species officially Extinct on the Red List. There are likely to be knock-on effects for conservation of declaring a species Extinct. The “Romeo Error” (Collar 1998) was a term coined to describe when funding and protective measures are removed from threatened species in the mistaken belief that they are already extinct. An evidence-based approach to classifying extinctions is required to encourage continued conservation work until there is no reasonable doubt that the last individual of a species has died. On the other hand, if assessments are too evidentiary, then extinction rates based on the Red List risk being underestimates. References Collar, NJ (1998). Extinction by assumption: or, the Romeo Error on Cebu. Oryx 32: 239-244. Emmons, LH (1999). A new genus and species of abrocomid rodent from Peru (Rodentia, Abrocomidae). American Museum Novitates 3279: 14. Dawson, MR, Marivaux, L, Li CK, Beard, KC and Métais, G (2006). Laonastes and the” Lazarus effect” in recent mammals. Science 311:1456-1458. Fara, E (2001). What are Lazarus taxa? Geographical Journal 36: 291-303. Fisher, DO and Blomberg, SP (2012). Inferring extinction of mammals from sighting records, threats, and biological traits. Conservation Biology 26: 57-67. Jablonski, D (1986). Causes and consequences of mass extinctions: a comparative approach. In: Elliott, DK (ed.), Dynamics of Extinction. New York: Wiley-Interscience: 183–229. Gynther, I, Waller, N and Leung, LK-P (2016). Confirmation of the Extinction of the Bramble Cay melomys Melomys rubicola on Bramble Cay, Torres Strait: Results and Conclusions from a Comprehensive Survey in August– September 2014. Unpublished report. Brisbane: Department of Environment and Heritage Protection, Queensland Government. IUCN Standards and Petitions Subcommittee (2016). Guidelines for Using the IUCN Red List Categories and Criteria. Version 12. Prepared by the Standards and Petitions Subcommittee. Available at: http://www. iucnredlist.org/documents/RedListGuidelines.pdf Leary, T, Singadan, R, Menzies, J, Wright, D and Thomson, B (2008). Melomys rubicola. The IUCN Red List of Threatened Species 2008: e.T13132A3412635. Pacheco, V, Zeballos, Z, Vivar E and Dunnum, J (2008). Cuscomys oblativa. The IUCN Red List of Threatened Species 2008: e.T136658A4324252. Roach, N (2016). Cuscomys oblativa. The IUCN Red List of Threatened Species 2016: e.T136658A22182152. Robinson, T and Burbidge, A (2008). Leporillus apicalis. The IUCN Red List of Threatened Species 2008: e.T11633A3298296 Woinarski, J and Burbidge, AA (2016a). Leporillus apicalis. The IUCN Red List of Threatened Species 2016: e.T11633A22457421. Woinarski, J and Burbidge, AA (2016b). Melomys rubicola. The IUCN Red List of Threatened Species 2016: e.T13132A97448475. Ros Kennerley has been involved in a number of threatened bird and mammal programmes around the world. She began her role as Programme Office for the SMSG based at Durrell in April 2015. Prior to this she completed her PhD on the conservation of two endemic mammals in the Dominican Republic, as part of the Durrell-led Darwin Initiative funded Last Survivors Project. E-mail: [email protected] Conservation and data management Finella Blair Durrell Wildlife Conservation Trust A major component of running effective programmes for saving endangered species, in or ex situ, is the monitoring of individuals and populations using evidence-based scientific research to inform actions and evaluate the impact of programmes. This is something Durrell is striving to improve both in our zoo and overseas research programmes. These efforts result in an abundance of data generated in programmes all over the world, on islands in Mauritius Solitaire No. 27 and the Caribbean, grasslands in India, offices in Bath and at the zoo in Jersey. These data start life mostly in notebooks, but also on camera storage cards, spreadsheets and in the heads of the researchers, managers and field workers. Why is data management important? Data are valuable; in conservation organisations they are often the result of long hours in the field in difficult 13 Technical report Figure 1. Illustration of the natural loss of information about datasets (metadata) with time (from Michener et al., 1987). conditions and, in the case of critically endangered species, in situations that cannot be repeated if data are lost. Good data management is often common sense but can be given low priority when there are so many other demands on everyone’s time. Good data management practice, when incorporated with technological solutions such as data entry forms on tablets and phones, can also save time, something anybody who has had to re-enter all their data because they didn’t have a back-up will identify with. What counts as data? Data can be many things, including notebooks full of surveys, spreadsheets of information, photograph collections (digital and analogue), sound recordings and information about data, known as ‘metadata’. A lot of incredibly valuable data is often just stored in people’s heads and only missed when they leave! Without putting too fine a point on it, if you were (unfortunately) hit by a bus tomorrow, would anybody tasked with carrying on your work where you left off know where your data was, how it was captured and what it represents? The ‘Information Entropy’ diagram (Fig. 1) illustrates the potential hazards of not documenting your data properly. Good data management will ensure that valuable and hard-earned data will be preserved for future use to aid the endangered species that we care about so much. It should also ensure that researchers get the credit for the data they collect. Increasingly, scientific journals are beginning to insist that authors provide access to the datasets on which their papers are based, generally by assigning Digital Object Identifiers (DOI). Anybody asking to reuse the data must then ask permission and correctly cite the dataset and its originators in any papers they publish. Managing data in Mauritius I was very fortunate to spend two months in Mauritius in 2016, helping Dr Nik Cole review a large volume of historical reptile survey data, which was stored in MS Excel. Solitaire No. 27 Excel is an excellent tool for many tasks and is often thought of as a “database”. It is intuitive and is the software package of choice for many researchers as it has some analysis functionality. Although it is great for things like pivot tables and charting, it can be very difficult to sort and report on relational data, particularly when data are spread between sheets and different files. Over time, inconsistency of data entry, particularly when more than one person is entering the data, and sheer volume makes querying or reporting the data more and more time consuming. At this point, a relational database such as MS Access is often a much more appropriate tool. Part of building an effective relational database is understanding how the data are collected and recorded, the logistical difficulties of moving it to electronic format (adverse weather, lack of internet connection or electricity), how best to collate and store it and make sure that it can be reported effectively. As a result, I spent part of my time in Mauritius visiting Ile aux Fouquets, Ile aux Aigrettes and Round Island with MWF staff, to take part in and understand as many type of surveys as possible. As part of the reptile project I field tested the use of data collection forms on smartphone and tablets for different types of surveys. The forms are created using MS Excel and Open Data Kit (ODK), free open source software that can be used with a Google app (see Figures 2 and 3). Correctly set up, forms can be context sensitive, data consistency can be improved by selecting answers from drop-down boxes and data is saved immediately and automatically sent to a central internet repository as soon as an internet connection becomes available. The data can then be downloaded and imported into a central database or further analysed in programs such as ‘R’. Directly entering data onto a tablet in the field cuts out the need to transfer data from notebook into an Excel spreadsheet at a later date, a process that can take a long time, opens up opportunities for typographic errors and creates delays in analysis. The time from field to central database can be reduced from days or weeks to hours or even minutes. Field testing is in its early stages in Mauritius. The use of ODK forms instead of notebook and pencil for Capture-Mark-Recapture surveys of Bojer’s skinks has the potential to speed up the data handling process as data are completed and sent while still on the island, rather than waiting for access to a computer and MS Excel back at the office. Feedback from researchers in the field indicates that further modification and testing is required. Ideally ODK forms are used during the survey, replacing notebook and pencil, but in some circumstances, for example in distance sampling where recordings are rapid, the screen refreshing required by ODK forms may slow down data entry, so ODK forms can be used for data entry immediately after the survey is complete. 14 Managing conservation data Back on the mainland, I designed and built a database structure in MS Access to incorporate the reptile survey data collected on both the new forms and the historical data. It’s important to ensure that the structure can accommodate all sorts of reporting requests and one of the skills of a good developer is to try and anticipate these. The reptile database will enable faster reporting of reptile survey data across species, islands and survey methods. MS Access has powerful querying and sorting capabilities and data reported can be exported if necessary, to documents, spreadsheets or ‘R’ for further analysis. Figure 2. ODK Main menu on smartphone. Back in the Bath office we are building several databases, some of which will support the development of the Durrell Index. We now have a publication database of Durrell staff-authored research papers, books and book chapters, academic theses, action plans and grey literature. A species database, for any animal species associated with Durrell, past or present, has been set up and recently a plant section has been added to support work on endemic and invasive plants in Mauritius. Work has just started to further develop an Academy database which will link Academy course attendance with the Alumni Network. A new intern at the Bath office, Rachael Gerrie, is working on the data that Durrell need to collect to assess the impact of Durrell Conservation Academy for the Durrell Index and this will be linked to the Academy database in due course. The data management team in Bath, headed by Lianne Concannon, will be producing some information on guidelines for good data management over the next few months. In the meantime, I have included a few pointers below. Most are common sense and are probably already part of your routine; there are also some really good resources on the internet, the best of which are shown below. Figure 3. Example of ODK data collection form showing drop-down list. Solitaire No. 27 Figure 4. MS Access database design. 15 Technical report If you can identify with any of the following situations, then following some straightforward data management guidelines could help you. Sorting Be careful using sort in Excel. Sorting can go very wrong, for example when there is a blank row somewhere within your data. Writing a report: all the data you need is in different formats or spreadsheets or locations (or a combination of all three)? Online resources Data management: https://www.dataone.org/sites/all/ documents/L01_DataManagement_Handout_FINAL. pdf Field notebooks: the precious field notebook with all its data has been lost or damaged? Laptop or hard drive: a component fails just as an important report is required? Excel spreadsheets: Everything was set up beautifully at the beginning of the surveys but years have passed and the dataset is huge and extracting the information needed for reporting is either difficult or impossible? Backups All data should be backed up, but the more of a disaster it would be if you lost it, the more important it is that you back it up, preferably to two different locations. Field notebooks Notebooks are very vulnerable to loss and damage. If you have field notebooks full of data that haven’t been transcribed to MS Excel yet, then scan or photograph each page. It might take half an hour for each notebook but it is then safe. Use a tablet or smartphone to take a photo of each notebook page at the end of each survey then email it to yourself for a permanent record. Laptops Back up your important files to an external drive or thumb drive or a central facility like Sharepoint or Dropbox if you have it. Make sure that the backups are labelled with the date of backup and are sensibly named. While Dropbox can be extremely frustrating where connection speeds are poor, having important files in Dropbox (preferably not shared to prevent anyone else inadvertently deleting it) at least ensures that you can retrieve previous versions of files. File names It is really easy to end up with multiple copies of files where it is difficult to tell which is most up to date, so incorporate version numbers and dates when making back-up copies. E.g. reptile_database_v1.2_220716 MS Excel files Master files If you are working constantly on a file (e.g. cleaning data) take a copy of the file and label it with the date at the end of each work session. Then if you find that you have made a mistake (e.g. on a sort) you can track back through your copies to see where it happened and you don’t have to go back to the last backup which may be many sessions out of date. Solitaire No. 27 Data sharing: https://www.dataone.org/sites/all/ documents/L02_DataSharing_Handout_FINAL.pdf Best practices for spreadsheets and data files: https://www.dataone.org/sites/all/documents/L04_ DataEntryManipulation_Handout_FINAL.pdf Data quality control: https://www.dataone.org/sites/ all/documents/L05_DataQualityControlAssurance_ Handout_FINAL.pdf Backups and archives: https://www.dataone.org/sites/ all/documents/L06_DataProtectionBackups_Handout_ FINAL.pdf Metadata – documentation of your data: https:// www.dataone.org/sites/all/documents/L07_Metadata_ Handout_FINAL.pdf Reference Michener, W.K., Feller, R.J. and Edwards, D.G. (1987). Development, management, and analysis of a longterm ecological research information base: example for marine macrobenthos. In Boyle, T.P. (ed.), New Approaches to Monitoring Aquatic Ecosystems. Philadelphia: ASTM International, 173–188. Finella Blair has been working parttime for Durrell since October 2015, after completing her Masters in Conservation Biology at DICE, University of Kent. Before that, she spent many years building relational databases and managing data, something she also does part time for a NERC-funded tropical forest programme at the University of Oxford. As Data Management Intern for Durrell, she is working with Lianne Concannon at Durrell’s Conservation Science hub in Bath to facilitate the flow of data from the point of data collection in the field up to the global headline indicators presented on the Durrell Index, Durrell’s organisational monitoring and evaluation framework, and has set up databases to support reporting, data analysis and decision making. E-mail: [email protected] 16 Health of Hapalemur alaotrensis Morbidity of Alaotran gentle lemurs (Hapalemur alaotrensis) at Durrell Wildlife Park (1990–2014) Alberto R. Barbon, Zoavina Randriana and Gale Glendewar Durrell Wildlife Conservation Trust Abstract This study presents a preliminary overview of medical problems encountered in captive Alaotran gentle lemurs at Durrell Wildlife Park over a period of 24 years. Individual medical records for 65 lemurs (36 males and 23 females) were examined. Overall, gastrointestinal and integumentary problems were the most prevalent issues, but age and sex were not good predictors of the occurrence of medical problems. Additional research on the nutrition and behaviour of captive specimens may help to understand and reduce the incidence of some of these pathologies. Key words: diet, disease, medical problems, veterinary care Introduction The Alaotran gentle lemur (AGL) or bandro (Hapalemur alaotrensis) is one of the five bamboo lemur species that exist in Madagascar (Mittermeier et al. 2010). It is a small bodied lemur (1240 ±140 g), characterised by its highly specialised feeding patterns (Mutschler et al. 1998). The AGL is found in the marsh habitat surrounding Lac Alaotra, the largest lake in central Madagascar (Mutschler & Feistner, 1995) (Figure 1). Its limited geographical range, combined with increasing anthropogenic pressure, has led to a population decline of more than 80% over a period of 24 years, and it is currently classified as critically endangered with a declining trend (Andriaholinirina et al. 2014) The remaining wild population is estimated to comprise around 2500 individuals (Ratsimabazafy, pers. comm., 2013). A small population is managed in zoological collections. Ninety-nine individuals (40.44.15) are maintained in 24 institutions worldwide (T. Wright and G. Glendewar, unpublished data). From a founding population of 10 animals, in the period to 2014, Durrell Wildlife Park (DWP) in Jersey had held 65 individuals. The aim of this study was to establish the most common medical problems found in the AGL housed at the DWP over a period of 24 years (1990 to 2014). 1, while the current diet is shown in Table 2. Variations in the diet provided in different enclosure have been established given the differing availability of forage in the outside areas. Results Medical records from 65 AGL (36 males and 23 females) were evaluated. Seven different clinicians were involved in the description of the medical problems. Six individuals were stillborn and only post mortem information was available. Of the remaining 59 individuals, 12 Methods AGL at DWP have been housed in a wide range of enclosures. (Figure 2). At the time of this study three different types of enclosures were being used. The oldest enclosures consisted of an outside planted area (38.5 m2) and an indoor heated area with vertical and diagonal bamboo poles. Another enclosure built in 1998 included a very large outside area of around 800 m2, with planted bamboo and willow trees and a heated shed. The newest enclosure consists of a heated shed and planted outside area with additional vertical bamboo poles. AGL have usually been housed in pairs and families in single species enclosures. Diet has changed over time; a description of the diet in 1995 (Courts 1995) is given in Table Solitaire No. 27 Figure 1. Alaotran gentle lemurs in their natural habitat. 17 Research report Table 1. Diet described in 1995 for captive gentle lemurs (Courts 1995). 0900 1 small (approx. 5 g) piece of: apple, banana, 2 other fruits eg. pear, plum; 2 small pieces of carrot, 2 soaked Old World Monkey pellets (Special Diet Services) 1200 Forage: bamboo stem (preferably with shoots), reeds, grass or willow 1600 Fresh vegetables/salad, eg.: 2 small (2–4 g) pieces of lettuce heart, celery, cucumber, tomato, carrot plus half a hard-boiled egg (no shell) twice per week Supplements 0.5 g Vionate (Ciba-Geigy Animal Health). Diluted condensed milk given to lactating females either died naturally or were euthanased for medical reasons, and 39 were exported to other institutions. Eight individuals were still housed at DWP at the time of the study. In total, 78 individual medical problems were identified (Table 3). Figures 3 to 7 illustrate some of the pathologies observed. Prevalence of medical problems within the eight body systems by sex is presented in Table 4. Approximately half of the AGL population (49.1%) housed at Durrell from 1990 to 2014 had some medical problems, and the prevalence was slightly higher in females (52%) than in males (47.2%), but this difference was not statistically significant (F=0.78; p>0.05). Gastrointestinal and integumentary pathologies showed the highest prevalence, with diarrhoea and wounds being the most common problems across the whole population. Prevalence of medical problems within body systems by age is presented in Table 5. Most of the medical problems were diagnosed in the adult group. The juvenile group showed Figure 2. Current enclosures for AGL at DWP. Table 2. Diet from 2002 to present. Daily extras are no longer offered in the current diet iteration, but they were offered in the past. 0900 Approx. 15 g dry leaf-eater pellet, 2 pieces (approx. 5 g) carrot. Added Vionate supplement. Forage Available through the day. Bamboo (Phylfeed lostachys sp), willow (Salix sp), perennial grass (Miscanthus sinensis), sedges (Carex hachijoensis, Carex pendula) Chicory (Cichorium sp). Bamboo is offered through the year; not all the plants listed are available in every enclosure, which has led to diet variations depending on the enclosure. Afternoon Chicory, ¼ tomato, 3 small pieces celery, 2 feed small pieces cucumber, 2 small pieces carrot. Fruit (including apple, pear, banana, grapes, nectarine, plum, pomegranate, melon, raspberry) only occasionally. Supple1 ml calcium vitamin D supplement (Collo-cal ments D) administered in bread for 6 months to nursing mothers Daily Bread (Monday), ¼ boiled egg (Tuesday), ¼ extras boiled egg (Thursday), small piece cooked sweet potato (Friday), small piece cooked sweet potato (Sunday). Solitaire No. 27 Figure 3. Digit injury exposing distal phalanx. Figure 4. Severe dental disease, showing gingivitis, tartar accumulation, and gingival recession. 18 Health of Hapalemur alaotrensis Figure 5. Axillary glands in gentle lemurs exhibiting normal secretions; these glands are bilateral and present a nodular appearance, not to be mistaken with subcutaneous abscesses. Figure 7. Localised alopecia in the base of the tail, suspected to be caused by prolonged pressure in this area due to specimens resting position next to heaters in indoors areas. Figure 6. Subcutaneous liposarcoma. Table 3. Individual medical problems diagnosed in AGL, classified by system, showing the total number of cases and the percentage of the total number of medical problems identified. Body system (number of cases) Dental (9) Medical problems Dental abscess Gingivitis Maxillary localised swelling Gastrointestinal (18) Integumentary (30) Metabolic (6) Musculoskeletal (5) Reproductive (2) Sensory (2) Urinary (6) Solitaire No. 27 Number of cases 6 1 Percentage of total 7.7 1.3 Constipation Diarrhoea Vomiting Abscess Cyst Liposarcoma Localised alopecia Localised swelling Wound Obesity Lameness Fracture Vertebral spondylosis Miscarriage Leydig interstitial cell tumour Cataract Corneal ulcer 2 1 14 3 2 1 2 4 4 17 6 3 1 1 1 1 1 1 2.5 1.3 18 3.8 2.5 1.3 2.5 5.1 5.1 21.8 7.7 3.8 1.3 1.3 1.3 1.3 1.3 1.3 Renal cysts Renal failure 1 5 1.3 6.4 19 Research report Table 4. Prevalence of medical problems (%) within body systems by sex of captive Alaotran gentle lemurs (Hapalemur alaotrensis) housed at Durrell Wildlife Park, Jersey (1990–2014). Body system Dental Gastrointestinal Integumentary Metabolic Musculoskeletal Reproductive Sensory Urinary Male (n=36) 16.6 19.4 61.1 11.1 8.3 2.8 0 11.1 Female (n=23) 13 47.8 34.8 8.7 8.7 4.3 8.7 8.7 Durrell population (n=59) 15.2 30.5 50.8 10.2 8.5 3.4 3.4 10.2 the highest prevalence of renal pathology. However, age was not statistically a significant predictor of medical problems occurrence in captive AGL (F=0.69, p>0.05). Faecal parasites (see Table 6), specifically Entomoeba sp., were linked to diarrhoea only in one instance; the remaining positive results were incidental findings, not associated with clinical signs. The following bacterial species and genera have been isolated as part of routine or diagnostic faecal screening: Acaligenes xylosalidans, Campylobacter sp., Campylobacter jejuni, Escherichia coli, Enterobacter agglomerans, Klebsiella pneumoniae, Manheimia haemolytica, Pasteurella pneumotropica, Pseudomonas sp, Rahnella aquatilis, Staphylococcus epidermis and Vibrio metschnikovi. None of the isolates were associated with diarrhoea or other clinical signs. Most wounds were the result of conspecific aggression towards males. A detailed breakdown of wound aetiology, if known, is given in Table 7. Discussion Alaotran gentle lemurs are underrepresented in biomedical research literature on prosimians, despite extensive reviews of prosimian medicine (Benirschke et al. 1985; Junge 1999; Junge 2003; Williams 2015). The only published report relates to the death of two animals at DWP of renal failure following the ingestion of Russian vine (Polygonum baldschuanicum) (Robert and Allchurch 1995). Table 6. Faecal parasitology findings in Alaotran gentle lemurs at DWP from 1990 to 2014. Result No parasites observed Entomoeba sp. Hymenolepis sp. Cryptosporidium sp. Giardia sp. Unidentified cestode ova Unidentified nematode larvae Solitaire No. 27 Number of samples 266 8 8 4 8 11 4 Percentage of samples 86% 3% 3% 1% 3% 4% 1% Table 5. Prevalence of medical problems (%) within body system by age (years) of captive Alaotran gentle lemurs (Hapalemur alaotrensis) housed at the Durrell Wildlife Park, Jersey (1990–2014). Body system Dental Gastrointestinal Integumentary Metabolic Musculoskeletal Reproductive Sensory Urinary Infant (0–0.5) 0 0 1.7 0 0 0 0 0 Juvenile (>0.5–2) 1.7 0 6.7 5.1 1.7 0 0 6.7 Adult (>2–16) 11.9 23.7 37.2 5.1 6.7 3.4 3.4 1.7 Geriatric (> 16) 1.7 6.7 5.1 0 0 0 0 1.7 To our knowledge this is the first review of morbidity in captive AGLs; however, our study has significant limitations. Apart from the relatively small sample size for a morbidity study, multiple clinicians were involved in the description of medical problems, introducing a potential bias factor in the diagnosis. Additionally, the diagnosis on multiple occasions was limited to clinical signs rather than a specific pathology. Aetiology was rarely identified and in some cases insufficient evidence was provided to associate the aetiology and the pathology identified. Despite these shortcomings, some trends emerge from this morbidity review that may help to focus future research efforts on this species’ pathology in captivity. Diet is one of the main aetiologies, or at least a contributory factor, to consider for over half of the problems observed, including gastrointestinal, renal and dental pathologies and obesity. Dietary studies in their natural habitat have shown that Alaotran gentle lemurs are highly specialised feeders, relying for most of their diet on only four plant species from the Cyperaceae and Poaceae families, resulting in a low-energy (17.3±1.7 MJ/kg dry matter), low protein (crude protein 131.6 ± 56.7 g/kg dry matter) and moderate fibre diet (crude fibre 221.1±72.5 g/kg dry matter) (Mutschler 1998). This is in strong contrast to diets offered in captivity during certain periods of time in terms of food variety and nutritional composition. Dietary analysis performed in 1996 revealed relatively high levels of protein in some plant parts selected by AGLs during certain times of the year (between 339 and 373 g/kg dry matter) (Fidgett et al, 1996). Differences in dietary requirements between the highly specialised Hapalemur and other lemur species are also reflected in gastrointestinal passage time, but despite a longer passage time in captive gentle lemurs it is suspected that this is shorter in captivity in comparison with wild specimens. (Cabre-Vert and Feistner 1995). The distribution of food intake through the day may play a role in some of the medical problems observed; in the wild this species appears to be cathemeral, feeding in periods throughout the whole day. Providing the food over a shorter period of time during the day (8 hours). instead of over a 24-hour period as in the wild, may contribute to obesity as energy density and intake may change, as shown in humans (Ello-Martin et al. 2005). 20 Health of Hapalemur alaotrensis Table 7. Wound aetiology. Aetiology Conspecific aggression Unknown Capture Enclosure Number of cases Percentage Male/female 10 62.5% 9/1 5 1 1 31% 6% 6% 2/3 0/1 0/1 Given variations in the diet over time and the limited sample size, it is difficult to establish the role of diet in the aetiology of many pathological processes. A cross institutional study with standardised diets would be helpful in increasing our understanding of the role of diet in morbidty and mortality in this species. Cryptosporidium infection has been associated with severe diarrhoea in some lemur species such as sifakas, while lemurs are reportedly asymptomatic carriers of Giardia (Williams 2015). Despite the detection of these parasites in AGLs, no clinical signs were associated with their presence. Despite the relatively high frequency of observation of cestodes in faecal parasitology, other than infection in prosimians as an intermediate aberrant host by Taenia and Equinococcus (Denk et al. 2016), no morbidity was associated with the detection of cestodes in AGLs. Wounds are the most prevalent problem, with males receiving the majority of the injuries, Field studies have revealed that females are more dominant and more aggressive than males, with intersexual conflicts arising mostly during feeding times (Waeber and Hemelrijk 2003). In primates intragroup competition has been linked to food distribution (Isbell 1991), and so evaluating the behaviour of gentle lemurs in captivity under different food presentation regimes may help to reduce aggression and therefore rates of injury. References Andriaholinirina N, Baden A, Blanco M, Chikhi L, Cooke A, Davies N, Dolch R, Donati G, Ganzhorn J, Golden C, Groeneveld LF, Hapke A, Irwin M, Johnson S, Kappeler P, King T, Lewis R, Louis EE, Markolf M, Mass V, Mittermeier RA, Nichols R, Patel E, Rabarivola CJ, Raharivololona B, Rajaobelina S, Rakotoarisoa G, Rakotomanga B, Rakotonanahary J, Rakotondrainibe H, Rakotondratsimba G, Rakotondratsimba M, Rakotonirina L, Ralainasolo FB, Ralison J, Ramahaleo T, Ranaivoarisoa JF, Randrianahaleo SI, Randrianambinina B, Randrianarimanana L, Randrianasolo H, Randriatahina G, Rasamimananana H, Rasolofoharivelo T, Rasoloharijaona S, Ratelolahy F, Ratsimbazafy J, Ratsimbazafy N, Razafindraibe H, Razafindramanana J, Rowe N, Salmona J, Seiler M, Volampeno S, Wright P, Youssouf J, Zaonarivelo J and Zaramody A (2014). Hapalemur alaotrensis. The IUCN Red List of Threatened Species 2014 (downloaded on 2 November 2016). Benirschke K, Miller C, Ippen R and Heldstab A (1985). The pathology of prosimians, especially lemurs. Advances in Veterinary Science and Comparative Medicine 30:167– 208. Cabre-Vert N and Feistner ATC (1995). Comparative gut passage time in captive lemurs. Dodo, Journal of the Jersey Wildlife Preservation Trust 31:76–81. Solitaire No. 27 Courts SE (1995). The Jersey Wildlife Preservation Trust Dietary Manual. Jersey: Jersey Wildlife Preservation Trust. Denk D, Boufana B, Masters NJ and Stidworthy MF (2016). Fatal echinococcosis in three lemurs in the United Kingdom – a case series. Veterinary Parasitology 218:10–14. Ello-Martin JE, Ledikwe JH and Rolls BJ (2005). The influence of food portion size and energy density on energy intake: implications for weight management. American Journal of Clinical Nutrition 82 (suppl): 236–241. Fidgett AL, Feistner ATC and Galbraith H (1996). Dietary intake, food composition and nutrient intake in captive Alaotran gentle lemurs Hapalemur griseus alaotrensis. Dodo, Journal of the Jersey Wildlife Preservation Trust 32:44–62. Isbell, LA (1991). Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behavioral Ecology 2:143–55. Junge, RE (1999). Diseases of prosimians. In Fowler, ME and Miller, RE (eds), Zoo and Wild Animal Medicine, 4th edition. Philadelphia: Saunders, 365–368. Junge RE (2003). Prosimians. In Fowler, ME and Miller, RE (eds), Zoo and Wild Animal Medicine, 5th edition. Philadelphia: Saunders, 334–346. Mittermeier, RA, Louis Jr, EE, Richardson, M, Schwitzer, C, Langrand, O, Rylands, AB, Hawkins, F, Rajaobelina, S, Ratsimbazafy, J, Rasoloarison, RM and Roos, C (2010). Lemurs of Madagascar, 3rd edn. Arlington, VA: Conservation International. Mutschler, T (1998). Folivory in a small-bodied lemur. The nutrition of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). In Rakotosamimanana B, Rasamimanana H, Ganzhorn JU and Goodman SM (eds), New Directions in Lemur Studies. Kluwer Academics/Plenum Publishers, 221–240. Mutschler, T and Feistner, ATC (1995). Conservation status and distribution of the Alaotran gentle lemur Hapalemur griseus alaotrensis. Oryx 29: 267–274. Mutschler, T, Feistner, ATC and Nievergelt CM (1998). Preliminary field data on group size, diet and activity in the Alaotran gentle lemur Hapalemur griseus alaotrensis. Folia Primatologica 69: 325–330. Robert N and Allchurch A (1995). Poisoning of Alaotran gentle lemur (Hapalemur griseus alaotrensis) by Russian vine ( Polygonum baldschuanicum ) at the Jersey Wildlife Preservation Trust. Verhandlungsberichte des Internationalen Symposiums über die Erkrankungen der Zootiere 37: 207–210. Waeber PO and Hemelrijk CK (2003). Female dominance and social structure in Alaotran gentle lemurs. Behaviour 140: 1235–1246. Williams CV (2015). Prosimians. In Fowler, ME and Miller, RE (eds), Zoo and Wild Animal Medicine, 8th edition. Philadelphia: Elsevier-Saunders, 291–301. Alberto Barbon is a veterinary surgeon at Durrell Wildlife Park and has carried out research into the health of a number of key species. Zoavina Randriana is a Malagasy veterinarian and a Durrell Conservation Academy graduate, with a history of working with small animals and wildlife conservation in Madagascar. Gale Glendewar is a senior mammal keeper at Durrell. E-mail: [email protected] 21 Research report Effects of dietary changes on the health of captive Geoffroy’s marmosets Callithrix geoffroyi Dominic Wormell and Eluned Price Durrell Wildlife Conservation Trust Abstract This study used analysis of medical records at Durrell Wildlife Conservation Trust to investigate the impact of dietary changes, namely the addition of acacia gum and an increase in insects, on the health of Geoffroy’s marmosets Callithrix geoffroyi. Rates of death, illness and individual symptoms were calculated per animal per year for two periods: the eight years before the changes, and seven years following the changes. Rates of death, bouts of illnesses and occurrences of specific symptoms per animal-year were all lower, often markedly so, following the changes to the diet. This study emphasises the importance of using information on diets in the wild to manage the nutrition of captive animals. Key words: Callitrichidae, gum, insects, morbidity, mortality, nutrition Introduction It is now clear from the growing number of field studies of callitrichids that their various ecological adaptations are associated with considerable differences in the composition of the diet in the wild (e.g. Ferrari and Lopes Ferrari 1989; Ferrari 1993; Rylands 1996), yet until relatively recently, most institutions holding callitrichids in captivity have provided largely the same diet for all species. Health and breeding problems that have been experienced with captive callitrichids, such as stillbirths and abortions, marmoset “wasting syndrome”, and susceptibility to infection (e.g. Shimwell et al. 1979; Barnard et al. 1988; Crook 1989; Price 1992a; Wormell et al. 1996) may be due at least in part to a diet which is not suitable for the species concerned. An understanding of natural diets is therefore vital for captive management. The most significant feature of the feeding habits of marmosets (genera Callithrix, Mico and Cebuella) is their use of plant exudates (Martins and Setz 2000; Ferrari and Rylands 1994; Ferrari and Digby 1996; Digby and Barreto 1996; Rylands 1989), and they possess adaptations in dentition and gut morphology to enable them to exploit these (e.g. Coimbra-Filho and Mittermeier 1976; Ferrari 1993; Power and Oftedal 1996). Geoffroy’s marmoset Callithrix geoffroyi (Figure 1) is endemic to the Atlantic coastal forests of Brazil and, like other marmosets, its diet in the wild is heavily dependent on plant exudates and insects (Passamani 1998; Passamani and Rylands 2000). An investigation of the nutrition of Geoffroy’s marmosets at Durrell Wildlife Conservation Trust was initiated in 1991 in an attempt to tackle frequent adult health problems and high infant mortality that was not due to incompetent parental behaviour (Price 1992a,b). There was also a worrying loss of young adults one to two years old, and Yersinia pseudotuberculosis was a common cause of death. Up to December 1991, 84% of the animals in the collection Solitaire No. 27 had had some health problems (Price 1992b); severe weight loss, diarrhoea, poor coat condition and lethargy were the commonest symptoms. Broken limbs in some monkeys may have been related to calcium deficiency. The species’ diet was therefore investigated to see if some light could be shed on these problems. The results (Price 1992a) suggested that the diet at the time of the study may have been low in protein, in some vitamins and minerals, and possibly also in energy, particularly perhaps during pregnancy and lactation. Consequently, the diet was modified, with an increase in insects and the daily provision of gum arabic. In this paper we attempt to assess whether or not the health of the Geoffroy’s marmosets at Durrell improved following the introduction of gum to the diet. Figure 1. Geoffroy’s marmoset (Photo: Hans Hillewaert; Creative Commons Attribution-Share Alike 3.0 Unported licence). 22 Marmoset diet and health Methods To obtain information on disease and mortality in Durrell Wildlife Conservation Trust’s Geoffroy’s marmosets, colony records were examined for the period between the arrival of the first marmosets in Jersey on 1 December 1984, until the end of December 1999 (from 2000 onwards very few marmosets remained in the collection). As gum, in the form of gum arabic diluted with water (Herron et al. 2001) was introduced as a daily component of the diet at the end of November 1992, this period was split into two phases: (1) 1 December 1984 - 31 December 1992, and (2) 1 January 1993 - 31 December 1999. The following information was extracted: (1) dates and causes of death (if known) of all noninfant marmosets that had died while at the zoo; (2) details of illnesses that had not resulted in death. For the latter, both separate bouts of illness (which could include several symptoms), and each symptom within an episode of illness, were tabulated. A bout of illness was considered terminated when it was followed by a record of improved health. No account was taken of the duration of bouts. The number of different individuals affected by non-fatal illness was also tabulated. As the main focus of the study was health in relation to diet, injuries caused by fighting were excluded from the analysis. Symptoms were categorised as follows: Weight loss: A record of a drop in weight from a previous known weight. Diarrhoea: Loose faeces, consistency varying from watery to more solid but unformed stools. Poor pelage condition: Matted coat, hair loss. Lethargy: Reluctance to move, sometimes associated with seeking heat and blinking, but able to move approximately normally if necessary. Weakness/lack of mobility: Inability to move properly. Broken bones: Usually presenting as limping or lack of use of a limb and confirmed on x-ray. Abnormal urine: Any abnormality detected using Multistix urine test. Other: Rare symptoms such as vomiting shown only by one or two marmosets on isolated occasions. Analysis As the number of marmosets in the collection varied over the study period, the length of time each marmoset that survived past the age of 30 days was present in the collection was calculated. These values were summed for each phase to give the number of animal-years. Frequencies of illnesses, deaths and symptoms per animal-year in each phase were then calculated and compared. Statistical analyses were not performed as the data were not independent: some marmosets were present for both phases, others for only one. Results Mortality Other than premature births and infants less than 1 month old, for whom accurate causes of death were not available, 21 Geoffroy’s marmosets died during the study period, 17 from the end of 1984 to the end of 1992, and 4 from 1993 to 1999. Of deaths before the end of 1992, seven (46.7%) died of confirmed or suspected pseudotuberculosis, three (20%) of other infections, and one (6.7%) of septicaemic shock following a fight with conspecifics. Cause of death was not firmly established in the other six cases, two of which were infants less than six weeks old. Of the four subsequent deaths, two were due to pseudotuberculosis, and the remaining two were sudden, one occurring during an examination. Rates of death per animal-year were lower following the introduction of gum to the diet (Figure 2). Other illness From 1984 to 1992, of 31 animals held at Jersey who survived to the age of more than 30 days, 22 (71%) were affected by non-fatal illnesses. An additional four animals who had not had any previous record of illness died, resulting in a total of 26 individuals (84%) who at one time or another suffered some degree of ill-health. The severity of symptoms ranged from isolated and mild cases of diarrhoea or vomiting, to fatal infections. A total of 95 instances of symptoms of poor health were recorded. Most common were observations of weight loss Deaths Bouts of illness Weight loss Diarrhoea Poor pelage condition After gum Weakness/lack of mobility Before gum Broken bones Lethargy Abnormal urine Other 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 Figure 2. Occurrence of deaths, non-fatal bouts of illness and individual symptoms within bouts, calculated per marmoset per year, before and after the introduction of gum to the diet. Solitaire No. 27 23 Research report (20%), diarrhoea (17%), poor coat condition (14%) and lethargy or listlessness (14%). There were nine records of injury, but six of these were broken limbs associated with other illness, especially suspected calcium deficiency in one female. From 1993 to 1999, 21 marmosets were held at Jersey, excluding infants which did not survive to more than 30 days. Of these, 9-10 (the exact number is not known as some animals in one group were not individually identifiable) were affected by non-fatal illness. Another died suddenly without having shown any previous signs of illness. Thus, after the introduction of gum, 43-48% of the marmosets in the collection suffered some degree of ill-health, just over half the percentage observed in the period before gum was introduced. In all, 34 instances of separate symptoms were noted. Bouts of illnesses and occurrences of individual symptoms per animal per year are presented in Figure 2. In all cases there was a reduction in the rate of occurrence after the introduction of gum to the diet, and this decrease was often marked. Discussion Finding the root causes of health problems in captive animals, and developing effective means of combatting them, is a complex task. Improved management techniques, such as minimally disruptive husbandry routines and larger cages with more complex furnishings, have in some cases dramatically improved the breeding success of captive callitrichids (e.g. Snowdon et al. 1985). Many of these measures have been adopted at Durrell (e.g. Wormell et al. 1996). However, one of the most important factors is likely to be diet. Problems such as osteomalacia in breeding females, for example, may be a result of calcium deficiency. Marmosets are obligate gummivores, with anatomical and physiological adaptations to feeding on exudates (CoimbraFilho and Mittermeier 1976; Ferrari 1993; Power and Oftedal 1996). Gum is an important source of calcium and energy (Passamani and Rylands 2000) and in the wild, gum forms nearly 70% of the diet of Callithrix geoffroyi (Passamani 1998; Passamani and Rylands 2000). In the past, gum was typically offered to captive marmosets only as a means of environmental enrichment (e.g. McGrew et al. 1986). Providing gum arabic on a daily basis for all Callithrix in Durrell’s collection was one of the first steps taken to combat health problems in this species, and the results of this analysis suggest it has had considerable health benefits. Since we began our investigations of health and diet in marmosets, gum has become a standard component of the diet for captive marmosets in many institutions and similar benefits have been reported (S. Muir, pers. comm.). Of course, management of captive animals should be under constant review, and diet is only one element of a suite of changes that have been made to the husbandry of callitrichids at Durrell to address problems in the health and reproduction of a number of species (e.g. Wormell et al. 1996), but we believe that our experience emphasises the importance of taxonspecific diets to the success of captive breeding programmes for endangered species. References Barnard, D, Knapka, J and Renquist, D (1988). The apparent reversal of a wasting syndrome by nutritional intervention in Saguinus mystax. Laboratory Animal Science 38:282288. Solitaire No. 27 Coimbra-Filho, AF and Mittermeier, RA (1976). Exudateeating and tree-gouging in marmosets. Nature 262: 630. Crook, G (1989). A nutritional reversal of marmoset wasting syndrome. Australian Primatology 4:21. Digby, LJ and Barreto, CE (1996). Activity and ranging patterns in common marmosets ( Callithrix jacchus ). Implications for reproductive strategies. In: Norconk, MA, Rosenberger, AL and Garber, PA (eds). Adaptive Radiations of Neotropical Primates. Plenum Press: New York, 173-185. Ferrari, SF (1993). Ecological differentiation in the Callitrichidae. In: Rylands, AB (ed.). Marmosets and Tamarins. Systematics, Behaviour, and Ecology. Oxford: Oxford University Press, 314-328. Ferrari, SF and Digby, LJ (1996). Wild Callithrix groups: stable extended families? American Journal of Primatology 38:19-27. Ferrari, SF and Lopes Ferrari, MA (1989). A re-evaluation of the social organisation of the Callitrichidae, with reference to the ecological differences between genera. Folia Primatologica 52:132-147. Ferrari, SF and Rylands, AB (1994). Activity budgets and differential visibility in field studies of three marmosets (Callithrix spp.). Folia Primatologica 63:78-83. Herron, S, Price, E and Wormell, D (2001). Feeding gum arabic to New World monkeys: species differences and palatability. Animal Welfare 10: 249-256. Martins, MM and Setz, EZF (2000). Diet of buffy tufted-eared marmosets ( Callithrix aurita ) in a forest fragment in southeastern Brazil. International Journal of Primatology 21: 467-476. McGrew, WC, Brennan, JA and Russell, J. (1986). An artificial “gum-tree” for marmosets (Callithrix j. jacchus). Zoo Biology 5:45-50. Passamani, M (1998). Activity budget of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic forest in southeastern Brazil. American Journal of Primatology 46: 333-340. Passamani, M and Rylands, AB (2000). Feeding behavior of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic forest fragment of south-eastern Brazil. Primates 41: 2738. Power, ML and Oftedal, OT (1996). Differences among captive callitrichids in the digestive responses to dietary gum. American Journal of Primatology 40:131-144. Price, EC (1992a). The nutrition of Geoffroy’s marmoset Callithrix geoffroyi at the Jersey Wildlife Preservation Trust. Dodo, Journal of the Wildlife Preservation Trusts 28:58-69. Price, EC (1992b). The Health and Nutrition of Geoffroy’s Marmoset ( Callithrix geoffroyi ) at the Jersey Wildlife Preservation Trust. Unpublished report. Jersey: Jersey Wildlife Preservation Trust. Rylands, AB (1989). Sympatric Brazilian callitrichids: the black tufted-ear marmoset, Callithrix kuhli, and the goldenheaded lion tamarin, Leontopithecus chrysomelas . Journal of Human Evolution 18: 679-695. Rylands, AB (1996). Habitat and the evolution of social and reproductive behavior in Callitrichidae. American Journal of Primatology 38: 5-18. Shimwell, M, Warrington, BF and Fowler, JSL (1979). Dietary habits relating to ‘wasting marmoset syndrome’ (WMS). Lab Animals 13:139-142. Snowdon, CT, Savage, A and McConnell, PB (1985). A 24 Marmoset diet and health breeding colony of cotton-top tamarins ( Saguinus oedipus). Laboratory Animal Science 35: 477-480. Wormell, D, Brayshaw, M, Price, E and Herron, S (1996). Pied tamarins Saguinus bicolor bicolor at the Jersey Wildlife Preservation Trust: Management, behaviour and reproduction. Dodo, Journal of the Wildlife Preservation Trusts 32: 6-97. Dominic Wormell is Head of the Mammal Department at Durrell Wildlife Conservation Trust, and Eluned Price is Zoo Research Coordinator. Both have conducted a wide range of research into the conservation, behaviour, health and management of marmosets and tamarins. E-mail: [email protected] Biodiversity loss in Gerald Durrell’s early works Gregory Byrnes Between 1947 and 1950, Gerald Durrell made three animal collecting expeditions. A year or so later, he began his professional writing career with accounts of these expeditions which were published in 1953 and 1954. I The Overloaded Ark 1. Page 15 2. Pages 19–21 3. Pages 167–8 4. Page 229 Superficially, Durrell’s first three books belong to the genre of light travel literature. Their style, for the most part informal and humorous, may have disguised the fact that they also have a serious purpose. Attentive reading, in fact, identifies numerous passages which highlight biodiversity loss. Biodiversity, an abbreviation of biological diversity, had not been coined in the period examined here, but Durrell was concerned about loss of biodiversity avant la lettre, as will be shown below. His first three expeditions were to the British Cameroons in 1947–8 and again in 1949, and to British Guiana in 1950. Sources for studying them include diaries and letters, but this essay confines itself to Durrell’s published accounts: The Overloaded Ark (1953), Three Singles to Adventure (1954) and The Bafut Beagles (also 1954). Reading them with an awareness of rhetorical devices such as repetition, sarcasm and contrast, one notices a sustained concern about the destruction of forests for large-scale cultivation and the commercial, industrial and residential structures that follow in its wake. Comparison of Durrell’s personal reminiscences with independently established facts and dates in standard reference works confirms that his observations are reliable. For convenience, some passages in which particular attention is drawn to biodiversity issues are set out in abbreviated form below: Solitaire No. 27 Gerald Durrell (Photo: Durrell Wildlife Conservation Trust). 25 Essay II Three Singles to Adventure 1. Page 4 2. Pages 67– 70 3. Pages 265– 6 III The Bafut Beagles 1. Page 104 One word in particular, “civilisation”, stands out by the way it is used repeatedly and always in a sarcastic tone: “a landscape denuded of its flora and fauna by the beneficial influences of civilization” (I, 1); “This was a bit of civilized Africa, and I shuddered to look at it…” (I, 4); “…with cinemas, snack bars, neon lights, and other doubtful privileges of civilization.” (II, 1); “the blessings of civilization” (II, 2). Another word much repeated and always negative is “plantation”: “apparently endless palm plantations… the endless rows of palm trees about us, serried ranks…” (I, 2 ); “the palm plantations …around Tiko…” (I, 4); and regarding banana plantations, “mile upon mile of nothing but banana trees in a great characterless sheet, arranged in neat rows like a green chessboard. Hideous regimentation, a thousand million banana trees standing in serried ranks…” (I, 4). Small-scale farming around Bafut, however, is shown in a positive light: “Below us lay a mosaic of small fields, green and silver and fawn, broken up by minute palm thickets and an occasional patch of rust red where the earth of a field had been recently hoed.” (III, 1). Galagos were living in the forest around those farms. Then there was “the real forest country”, the “beauty and colour” of which is described in lyrical detail (I, 2, and, for Guiana, compare II, 3: “a feeling of awe”). Durrell, from a lookout, saw a vast forest and contemplated how it “ stretched, almost unbroken, right across Africa, until it merged into the savannah land of the east.” (I,3). He attempted to estimate the number of animals living there but the mental arithmetic made him dizzy; the unstated implication is that every plantation meant so much biodiversity lost. These texts also show concern for indigenous people. This is relevant because, as mentioned by Fa et al. (2011, p. 5), “ [h]uman cultural diversity could also be considered part of biodiversity since human cultures represent ‘solutions’ to the problems of survival in particular environments.” The destruction of indigenous communities in South America is presented in a way that hints at the parallel confinement of wildlife in protected areas: “…the Amerindians have had their country wrested away from them and are forced to live in reserves…” (II, 2). Solitaire No. 27 The effect of plantations on the people of Cameroon is suggested by an understated contrast which speaks for itself: “…a clearing containing a white bungalow, in which lived a European overseer; or a row of horrible corrugated iron sheds, in which lived the banana pickers…” (I, 4). These passages have not always been appreciated: “In fact there is not a glimmer to be found in the book [The Overloaded Ark] – or, for that matter, in its immediate sequels…– of Gerald’s views on…animal conservation in general…Yet before the mid-fifties there is no written evidence at all of any particular interest in animal conservation or in environmental matters as a whole.” (Botting 1999, pp. 206–7). That author dates Durrell’s “first public protest at the role of man in the destruction of nature” to a radio talk on 29 August 1956.( Botting 1999, p. 239). The opinion that “little of this way of thinking [i.e. conservation] could be found in his [Durrell’s] books” is repeated on page 241. That interpretation is contradicted by the quotations above. They show that Durrell expressed his concern about loss of biodiversity in print in 1953 and 1954, based on experiences which date back to 1948. Clearly, it is worthwhile revisiting these early books. Further study of them, and of archival material not included here, could throw more light on the development, chronological and philosophical, of Durrell’s thinking about conservation. Acknowledgements I thank the State Library of New South Wales, the Sydney City Library and the University of New South Wales Library. References Botting, D (1999). Gerald Durrell: The Authorised Biography. London: Collins. Durrell, GM, (1953). The Overloaded Ark. London: Faber. Durrell, GM (1954a). Three Singles to Adventure. London: Rupert Hart-Davis [Pagination referred to here is that of the Ulverscroft Large Print Edition]. Durrell, GM (1954b). The Bafut Beagles. London: Rupert HartDavis. Fa, JE, Funk, SM and O’Connell, D (2011). Zoo Conservation Biology. Cambridge: Cambridge University Press. Gregory Byrnes, MPhil is from Sydney, Australia. He has a background in the humanities and currently teaches English to international students. He enjoys natural history and is a member of the Australian Wildlife Society and a Taronga Zoo Friend. At present he is writing a book about Gerald Durrell’s little-known second expedition around Australia in 1969-1970. Email: [email protected] 26 Measuring muscle in bats Assessing muscle condition in captive Livingstone’s fruit bats Dominic Wormell1, Scot Ramsay2, Will Masefield1, David Houston3 and Eluned Price1 Durrell Wildlife Conservation Trust, Jersey James Hutton Institute, Aberdeen, UK 3 Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, UK 1 2 Abstract It can be difficult to provide captive fruit bats (Pteropodidae) with adequate space for normal flight, and this can be a factor in the development of obesity and related medical conditions. This is often a particular problem in dominant males, who defend feeding territories and are therefore largely sedentary. Lack of muscle use can lead to atrophy, thus exacerbating the problem. A muscle moulding technique previously used in birds was tested in six adult males from a colony of Livingstone’s fruit bats (Pteropus livingstonii) before and after a move to a larger enclosure. The technique enabled us to compare muscle mass between individuals, and within individuals over time, and has great potential in evaluating methods of alleviating health problems associated with captivity. Key words: alginate, captive management, muscle moulding, Pteropodidae, Pteropus livingstonii Introduction Fruit bats (flying foxes) are keystone species in many tropical forests. They play important roles in both pollination and seed dispersal of forest plants (McConkey and Drake 2006; Reiter et al. 2006). Many species are now threatened because of habitat loss and persecution, and captive breeding programmes have been established for a number of such species (Carroll et al. 1995; Masefield 2003). Among these is the Critically Endangered Livingstone’s fruit bat Pteropus livingstonii from the Comoro Islands in the Indian Ocean (Mickleburgh et al. 2008; see Figure 1). In 1992–1995, 17 wild-caught Livingstone’s bats were brought to Durrell Wildlife Conservation Trust’s headquarters in Jersey, and the captive population now numbers over 60. Wild fruit bats typically roost in groups of varying sizes (Smith and Leslie 2006; Kerth 2008), flying at night to feeding sites that may be several kilometres or more away (Richter and Cumming 2006; Tidemann and Nelson 2003). When fruit bats are brought into captivity it is impossible to provide comparable flying conditions to those in the wild, and as a consequence animals may suffer from muscle atrophy and become obese (Courts 1996, 1999). Dominance hierarchies, particularly amongst males, are also established in these colonial animals, and dominant bats tend to defend small feeding territories (Kunz and Lumsden 2003). In the wild, the bats must fly to and from these territories, but in captivity territory-holding males remain relatively sedentary and as a result often becoming overweight, leading to difficulty flying (Wilson 1988; LeBlanc 2009; Courts 1999). It is well known from domestic animals and human health studies that these Solitaire No. 27 changes can have a substantial number of health consequences (Wilmore and Costill 2004; McArdle et al. 2000). Following their arrival, obesity as a result of lack of exercise and year-round good quality food became a problem in the Livingstone’s bats at Durrell. The mean weight of the ten adult wild-caught male bats at capture was 657g; after about 1.5–2 years in captivity, their weight had increased by an average of 16%. Although some of the bats had been moved to an enclosure with an outdoor aviary in 1995 (Courts 1996), the space available was still relatively restricted and flying activity Figure 1. Livingstone’s fruit bat (Photo: James Morgan). 27 Research report Figure 2. Exterior view of the flight tunnel at the time of the study. Figure 3. Interior view of the flight tunnel at the time of the study. was extremely limited. In 2003, as part of the programme to improve the health status of the captive group, animals began moving into a modified horticultural polythene tunnel (Wormell 2012). This provided a massive increase in the space available for flight, providing a straight flight path of 38 m and a total volume of approximately 1200 m3 (Figures 2 and 3). As well as providing excellent opportunities for flying, the enclosure also supplied a large area for climbing. Measuring muscle mass would be a valuable indicator of fitness and a means of assessing the success of such changes in management. The present study tested whether a bodymoulding technique that has been successfully used in birds to predict the mass of the pectoral muscles (e.g. Veasey et al. 2000; Barboutis et al. 2011) could also be applied in fruit bats. Subjects Six captive-born male bats were studied (see Table 1). All were adult (pteropodid bats reach maturity at 12–24 months; Pierson and Rainey 1992; Welbergen 2010). Weights were recorded and muscle mouldings taken when they were moved to the tunnel in August 2003, and again in October 2004. This was done as part of routine health screening of the animals, under anaesthetic. a discrete muscle block (Yalden and Morris 1975), and is covered in dense fur. However, the muscle mass on the wings forms a discrete, lightly furred, and easily moulded mass. We used alginate moulding to record the cross-sectional area of the whole wing muscle mass overlying the humerus bone. The anaesthetised bats were laid on their backs, the wings extended, the membrane dusted with talcum powder, and dental alginate poured over the muscle mass overlying the humerus bone; we also included some of the radius, to give a fixed reference point for later sectioning. After the alginate had set, it was removed from the wing, and the wing membrane lightly wiped with a damp cloth to remove excess talcum. The cavity in the mould was then filled with a liquid plaster of Paris, which was left to set. The plaster “cast” of the muscle mass was then removed from the mould, and sectioned in a band saw at a set distance of 1 cm from a clearly identifiable bony protuberance at the proximal end of the radius. A photocopy image was obtained of each cross-section (both sides) by placing the cast face down on the photocopier plate, together with a scale bar 50 mm long. The paper copy was subsequently scanned using a digital scanner to produce a digital image of the cross sections together with a scale bar. To standardise the area of muscle measured, we identified two places on each cross section where the wing membrane Moulding We moulded muscle shape using dental alginate, CA37, manufactured by Cavex Holland, P.O. Box 852, 2003 RW Haarlem, Netherlands. This technique has been used in birds to record the cross-sectional area of the pectoral muscle region, a measure which has been shown to correlate well with the actual weight of the pectoral muscle mass (Selman and Houston 1996). Alginate, when mixed with water, remains in a cream-like condition for about 90 seconds, before solidifying within a few seconds. Once hardened, it remains rigid enough to retain the shape of the moulded object in great detail. It does not adhere to skin or fur, and can easily be removed from the bat’s wing after treatment. In bats the wing muscle system on the torso is not suitable for moulding because it is more complex than that in birds, does not form Figure 4. Cross-sectional area of cast showing cut-off line drawn between wing membranes. Methods Solitaire No. 27 28 Measuring muscle in bats Table 1. Details of bats studied. Mean muscle area at 2nd moulding (mm2) Durrell ID Name Date of birth M2244 Ghost 6 May 1996 1064 961 303 277 M2277 Iggy 24 August 1996 1233 1046 348 321 M2504 Ruggiero 5 March 1999 1001 1043 269 287 M2618 Lysander 17 May 2000 937 1013 318 342 M2682 Balthazar 7 May 2001 890 918 275 324 M2694 Melchior 26 June 2001 793 943 231 293 Mean 986.3 987.3 290.7 307.2 CV 14.1 5.0 12.9 7.5 meets the arm, and used this as the cut-off point: a horizontal line was drawn between these two points (see Figure 4), and the muscle area above this line was measured using ‘Scion Image’ (Scion Image Beta 4.0.2.; Scion Corporation). As the positioning of this line required some judgement, we repeated each measure and used the mean of the two measures. Results Mean determined muscle areas for all bats are presented in Table 1. We were not able to establish whether the cross sectional muscle area we measured was correlated with actual muscle mass, because this would have involved killing animals: such a relationship, however, has been established for this technique in birds (Selman and Houston 1996). One non-destructive way to indirectly examine the accuracy of the method, however, is to examine “within-bat” variation (between left and right wings) in comparison to “between-bat” variation (variation in mean wing muscle area between different bats). Observed within-bat variation would result from both actual natural variation in muscle size between left and right wings and any inherent inaccuracies or errors in the moulding technique. Between-bat variation, on the other hand, should reflect actual differences in gross muscle mass between individuals plus, again, any inherent inaccuracies or errors in the moulding technique. As one would expect flight muscles to be fairly symmetrical, the actual difference between left and right wing muscles within individuals should be small relative to the differences in muscle mass between individuals. Also, the level of error in the technique should be roughly similar between wings and between bats. Therefore, if observed “between-bat” variation proved to be significantly greater than observed “within-bat” variation, this would indicate that the technique should be reliable enough to detect reasonable changes in body muscle size (at least changes of a magnitude similar to mean differences in muscle size seen between different individuals). From Table 1 it can be seen that in both 2003 and 2004, between-bat variation was significantly greater than within-bat variation (i.e. the variation between left and right wings). In 2003 between-bat variability accounted for 87.3% of total observed variation, Solitaire No. 27 Weight at 2nd moulding (g) Mean muscle area at 1st moulding (mm2) Weight at 1st moulding (g) whilst in 2004 between-bat variability accounted for 70.4% of total observed variation. This indicates that the technique is sufficiently reliable and accurate to be useful for our needs. Discussion Captivity has effects not only on the behaviour of animals, but also on their morphology (O’Regan and Kitchener 2005). The roost and feeding sites of wild bats are usually a significant distance apart: satellite telemetry studies of wild Eidolon helvum and Pteropus poliocephalus suggest that flying foxes tend to forage 15–50 km from their day roosts each night (Richter and Cumming 2006; Tidemann and Nelson 2003). Captive fruit bats, on the other hand, typically spend only a very small proportion of their time flying (e.g. Carroll 1979). Bats brought into captivity are therefore almost certain to lose muscle condition, while gaining fat. In this study, we have demonstrated that muscle mass in fruit bats can be measured by a technique originally developed for use in birds. This method should help in evaluating the extent to which modifications to the housing and management of captive fruit bats are successful in increasing activity, especially flight, and thus health. Acknowledgements We are grateful to all the mammal and veterinary staff at Durrell Wildlife Park for their support. References Barboutis, C, Mylonas, M and Fransson, T (2011). Breast muscle variation before and after crossing large ecological barriers in a small migratory passerine (Sylvia borin, Boddaert 1783). Journal of Biological Research – Thessaloniki 16: 159–165. Carroll, JB (1979). The general behavioural repertoire of the Rodrigues fruit bat Pteropus rodricensis in captivity at the Jersey Wildlife Preservation Trust. Dodo, Journal of the Jersey Wildlife Preservation Trust 16: 51–59. Carroll, JB, Gilmour, L and Courts, S (1995). Rodrigues Fruit Bat Pteropus rodricensis International Studbook. Volume 1. Jersey: Jersey Wildlife Preservation Trust. 29 Research report Courts, SE (1996). An ethogram of captive Livingstone’s fruit bats Pteropus livingstonii in a new enclosure at Jersey Wildlife Preservation Trust. Dodo, Journal of the Wildlife Preservation Trusts 32: 15–37. Courts, SE (1999). Dietary studies of Livingstone’s fruit bat Pteropus livingstonii: feeding behaviour, diet evaluation and modification. Dodo 35: 26–47. Kerth G (2008). Causes and consequences of sociality in bats. BioScience 58: 737–746. Kunz, TH and Lumsden, LF (2003). The ecology of cavity and foliage roosting bats. In: Kunz, TH and Fenton, MB (eds). Bat Ecology. Chicago: University of Chicago Press, 3–89. LeBlanc, D (2009). Environmental enrichment for long-term captive bats. In: Barnard SM (ed.). Bats in Captivity, Volume 3: Diet and Feeding. Washington DC: Logos Press, 281–305. Masefield, W (2003). European Studbook for Livingstone’s fruit Bat (Pteropus livingstonii), 1st edn. Jersey: Durrell Wildlife Conservation Trust. McArdle, WD, Katch, FI and Katch, VL (2000). Essentials of Exercise Physiology, Vol 3. Baltimore: Limmincott, Williams and Wilkins McConkey, KR and Drake, DR (2006). Flying foxes cease to function as seed dispersers long before they become rare. Ecology 87: 271–176. Mickleburgh, S, Hutson, AM and Bergmans, W (2008). Pteropus livingstonii. The IUCN Red List of Threatened Species. Version 2014.1. www.iucnredlist.org (downloaded on 11 July 2014). O’Regan, HJ and Kitchener, AC (2005). The effects of captivity on the morphology of captive, domesticated and feral mammals. Mammal Review 35: 215–230. Pierson, ED and Rainey, WE (1992). The biology of flying foxes of the genus Pteropus: a review. In: Wilson, DE and Graham, GL (eds). Pacific Island Flying Foxes: Proceedings of an International Conservation Conference. US Fish and Wildlife Service Biological Report 90: 1–17. Reiter, J, Curio, E, Tacud, B, Urbina, H and Geronimo, F (2006). Tracking bat-dispersed seeds using fluorescent pigment. Biotropica 38: 64–68. Richter, HV and Cumming, GS (2006). Food availability and annual migration of the straw-coloured fruit bat (Eidolon helvum). Journal of Zoology 268: 35–44. Selman, R and Houston, DC (1996). A method for estimating the muscle condition of small, live passerine birds. Ibis 138: 348–350. Smith, SJ and Leslie, DM Jr (2006). Pteropus livingstonii. Mammalian Species 792, 1–5. Tidemann, CR and Nelson, JE (2003). Long-distance movements of the grey-headed flying fox (Pteropus poliocephalus). Journal of Zoology 263: 141–146. Veasey, JS, Houston, DC and Metcalfe, NB (2000). Flight muscle atrophy and predation risk in breeding birds. Functional Ecology 14: 115–121. Welbergen, JA (2010). Growth, bimaturation, and sexual size dimorphism in wild gray-headed flying foxes (Pteropus poliocephalus). Journal of Mammalogy 91: 38–47. Wilmore, JH and Costill, DL (2004). Physiology of Sports Science, 3rd edn. Champaign: Human Kinetics. Wilson, DE (1988). Maintaining bats for captive studies. In: Kunz, TH (ed.). Ecological and Behavioral Methods for the Study of Bats. London: Smithsonian Institution Press, 247–263. Wormell, D (2012). The recycled roost. Zooquaria 80: 22–24. Yalden, BW and Morris, PA (1975). The Lives of Bats. Newton Abbot: David and Charles. Dominic Wormell is Head of the Mammal Department at Durrell. Scot Ramsay is at the James Hutton Institute in Aberdeen. Eluned Price is Zoo Research Coordinator, and Will Masefield was formerly a senior mammal keeper at Durrell. Professor David Houston is Honorary Senior Research Fellow at the Institute of Biodiversity Animal Health and Comparative Medicine, University of Glasgow. E-mail: [email protected] Conservation update on the ploughshare tortoise Angelo Ramy Mandimbihasina Durrell Wildlife Conservation Trust The ploughshare tortoise, Astrochelys yniphora, locally named “angonoka”, is one of Madagascar’s endemic land tortoises (Figure 1). Its distribution is very limited, in the vicinity of the Baly Bay area, north-western Madagascar. Its habitat consists of bamboo scrub and scrub shrub of a total of 160 km2. Wild populations of A. yniphora are very fragmented and subject to many threats such as bush fires, use of its habitat by zebus belonging to local people, and poaching. Combined with the slow growth Solitaire No. 27 Figure 1. Ploughshare tortoise (Photo: Matt Goetz). 30 Ploughshare tortoise conservation of this species – it takes at least 20 years for an individual to be able to lay eggs – these threats are causing its decline. The population size of wild A. yniphora has been estimated to be less than a thousand since the late 1990s. Because of its low numbers, the ongoing decline and its limited distribution, A. yniphora has been listed as Critically Endangered in the Red List of threatened species (Leuteritz and Pedrono 2008). Historical overview of ploughshare conservation The ploughshare tortoise was described in 1885 by Léon Vaillant, a French zoologist, from a specimen obtained by sailors. Before the mid 1980s, captive breeding was attempted in Ivoloina Zoological Park but reproduction was unsuccessful. In the mid 1980s, Durrell, then known as Jersey Wildlife Preservation Trust (JWPT), was appointed by the IUCN to save the species. A new captive breeding centre was established in 1986 by Durrell in Ampijoroa, not far from its natural range. Nesting and the first hatching success occurred the following year, and has continued since then. Research in the field has continued to study the habitat requirements, distribution and biology of the species. Conservation of the ploughshare tortoise with the local community started in the early 1990s with public awareness campaigns through festivals. As a result, a National Park was created at the end of 1997, and all known habitats of this tortoise have been included in this park. Since the creation of the Park, local people have participated in the conservation of this species by creating and maintaining fire breaks around the Park boundary and around the limit of core zones. A trial release of captive-born ploughshare tortoises took place in 1998 into an abandoned habitat and has shown success. In 2005, this reintroduction continued with a set of 20 tortoises every year. Over 100 tortoises have been reintroduced, and they have produced more than 20 juveniles. Despite the success of reintroducing captive-raised tortoises back into the wild, recent research has highlighted the rapid and worsening decline of the wild ploughshare tortoise population as a result of worsening poaching activities for the international illegal wildlife trade. Since the 1960s, the species has been protected by Malagasy law 60–128 which prohibits all harvesting, eating and trade. That law was updated in the mid 2000s and the species is still in category 1, class 1, which means that it is protected, no harvesting or poaching is allowed, and eating the tortoises is prohibited. All habitats of the ploughshare tortoise have been declared part of the core zone of the National Park, which gives more protection to the species as entry in these zones is forbidden without permits from the Ministry of the Environment and Forest, and are granted only for education, research, or conservation purposes. The species was listed as Endangered (EN) in the 1990s in the IUCN Red List, and uplisted to Critically Endangered (CR) Solitaire No. 27 in 2008. It is listed in Appendix 1 of CITES, which means that exporting ploughshare tortoises or any parts derived from the species from Madagascar is forbidden as is importing it into a member country of CITES. Ongoing conservation activities To reverse the situation of wild ploughshare tortoise populations, Durrell Wildlife Conservation Trust has been investing in many activities, in order to protect the remaining ploughshare tortoise population, of course with help from donors. A key action has been to continue to increase public awareness with supports from local authorities, by means of big celebrations, village meetings, and collaboration with schools. Another important action is lobbying all higher authorities in order to have transparency in actions and to prove to people that we need to protect this species. Technology has improved our fire survey system. Our field team is now receiving fire alerts by e-mail from NASA’s Fire Information for Resource Management System (FIRMS) and Conservation International’s “Firecast” Systems in near real time (NRT). The purpose of this is to improve rapid local actions to fight fires. Since 2010, village patrols, known as para-rangers, have been put in place to undertake daily patrols inside the habitat of the ploughshare tortoise, and ensure a permanent presence in the field (Kiester et al. 2013). Local villagers have been living closely with their forests and they know the park very well, so they know the poachers’ access routes. They also inform the Park Manager by phone if they see a fire or poachers. This system has led to a reduction in the damage caused by fire as it enables a more rapid response; it has also led to the arrest of poachers. Since 2014, village patrols have been improved with the use of GPS and GPS cameras in order to easily locate reported signs of incursion or other threats to the species. In addition, patrol data have been recorded into SMART® in order to show transparency and facilitate decision making. SMART imports all GPS tracks recorded Figure 2. Fire breaks created and maintained by villagers, following the park boundary in Andranomatavy (Photo: Angelo Ramy Mandimbihasina). 31 Conservation report analysis, reporting and facilitate decision-making. Baly Bay National Park began investing in SMART at the end of 2014 and it was successfully in use a year later despite a lack of equipment. As ploughshare habitats are very remote, no electricity generation facilities are in place yet, and it is still a big challenge to charge batteries in the field for the use of GPS. Investing in efficient solar panels and batteries is an option that could help our field team. In addition, the use of smartphones with power banks and/or small solar panels should help. The use of smartphones for in-field mobile data entry can greatly reduce time-consuming and error-prone and we will be trialling “Cybertracker” over the coming months. Figure 3. Photo taken by a camera trap on 08 April 2016 at 09:03 pm inside a ploughshare habitat. during patrols; this can show the patrol effort in terms of time spent and distance walked. Patrollers are supervised by a responsible person from the Durrell team and also by Park Rangers. As Baly Bay is a National Park, there are eight Park Rangers undertaking patrols there, including within ploughshare habitats. Their patrol data are also put into SMART. They undertake supervision of the villagers doing patrols and also ensure that villagers are helping to maintain fire breaks around the habitats and park boundaries. They also mark trees with permanent enamel paint in order to let people know where park boundaries and core zones are. The third type of patrol is done with the military. During the ploughshare’s active period, three groups of armed people from the military along with Park rangers, representatives of the Ministry of Ecology, Environment and Forest, and a team member from Durrell also carry out patrols. Patrol data from these teams are also entered into SMART in order to measure their effort and to better understand the effectiveness of these patrols To enhance security, camera traps have been installed inside the ploughshare habitats since 2012 in order to take pictures of poachers and trespassers. Conservation impact Patrols are one of the ways in which we can reduce poaching activities, but the known trails inside the park and other ploughshare habitats only enable us to access about 7000 ha, which is about 45% of the entire habitat. Creating new trails would mean creating more access into the habitats, which might backfire by giving improved access for poachers, so it is important that we find ways to conduct patrols without following defined trails and increase the reach of the existing patrols. Even with this coverage, poaching signs have been seen and reported by patrollers. The use of SMART to monitor patrols, threats and biodiversity is a new conservation tool to enhance data Solitaire No. 27 Fires have been seen inside Baly Bay National Parks even when firebreaks were made properly following park boundaries and limits of core zones (Figure 2). Fires inside ploughshare habitats have been noticed both by fire alerts and patrollers. During 2016, we have noted an increased number of fires and burnt areas compared to 2015. Information gathered by the village patrols has led to arrests. Some of the people that were arrested were successfully prosecuted, went to jail and were fined for entering the core zone of the National Parks, even if they had not taken any tortoises, which is very encouraging! Camera-traps have shown good results and people have been arrested directly because of the images. Figure 3 shows two poachers captured by a camera trap in one of the ploughshare habitats in April 2016, at night. Conclusion The information and data arising from these actions show that poaching of A. yniphora exists and continues. Poachers may not come in when military personnel are present on site, so a permanent presence and patrols by armed guards may be necessary in order to ensure protection of this species in the wild. However, all conservation actions should be continued and reinforced with awareness-raising activities in order to get good results. Efforts should be put into the use of GPS and adoption of and training in technology so that patrol effort can be evaluated and results can flow more rapidly, ensuring that appropriate responses to fires and incursions by poachers can be taken more quickly. Angelo Ramy Mandimbihasina started working with Durrell in 2000 as a student studying the population genetics of the ploughshare tortoise. He joined us as Baly Bay Project Manager in 2005, and received training in Jersey in 2009. Since 2010 Angelo has focused on coordinating research activities for the ploughshare tortoise, including his own PhD. E-mail: [email protected] 32 Tortoise seed dispersal Reviving lost interactions: seed dispersal by ecological replacement Aldabra giant tortoises on Ile aux Aigrettes, Mauritius Martin Kastner1, Ysabella Montaño1 and Nicolas Zuël2 Durrell Wildlife Conservation Trust Mauritian Wildlife Foundation 1 2 Abstract Giant tortoises are keystone herbivores and seed dispersers on many oceanic islands. Their eradication throughout much of their former range has led to the dispersal limitation of many large-seeded tree species, putting those species at increased risk of extinction. The introduction of ecological replacement tortoises could restore seed dispersal of endangered tree species, which may be crucial to the recovery of their populations. We quantified seed dispersal distances of the critically endangered ebony Diospyros egrettarum by ecological replacement Aldabra giant tortoises (Aldabrachelys gigantea) on Ile aux Aigrettes, Mauritius. Average seed dispersal distance was 85.0 m (range 0–350.3 m). Dispersal by male tortoises was higher than that of females, but the difference was not statistically significant. We recorded a large proportion of long-distance dispersal events, with 40% of recorded dispersals over 100 m, and 6% over 200 m. Our results suggest that dispersal by the ecological replacement tortoises may be depositing most ebony seeds beyond the range of density-dependent mortality effects, potentially encouraging germination and establishment. Long distance dispersal could promote gene flow within the population as well as colonisation of suitable habitat. Our study contributes to the important and ongoing process of documenting the results of ecological replacement experiments. Key words: Diospyros egrettarum, ebony, habitat restoration, islands Introduction Until relatively recently, tortoises were the dominant herbivores and seed dispersers on many oceanic islands (Hansen et al. 2010), but they have been driven to extinction throughout most of their former range. Large and giant tortoises play a number of important ecological roles within the ecosystems they inhabit, including the maintenance of habitat openness and heterogeneity through browsing, grazing and trampling (Gibbs et al. 2010), the promotion of nutrient cycling (Hunter et al. 2013), as well as seed dispersal (Kaiser-Bunbury et al. 2010). Mauritius was historically inhabited by two endemic species of giant tortoise of the genus Cylindraspis, itself unique to the Mascarene Islands. It appears that both species were particularly concentrated in the lowland palm-dominated forests, which were likely to have been kept relatively open by their grazing pressure. The tortoises were eradicated from the mainland of Mauritius by the early 18th century, though some individuals persisted on offshore islands into the 19th century. Their extinction was caused by a combination of intense hunting and predation by introduced pigs and cats (Cheke and Hume 2008). The loss of the Cylindraspis tortoises and other endemic frugivores has led to the dispersal limitation of a suite of tree species in Mauritius (Hansen et al. 2008). On Ile aux Aigrettes, an offshore islet, Griffiths (2010; Griffiths et al. 2011) confirmed the absence of recruitment of Diospyros egrettarum, a critically endangered endemic ebony, prior to the introduction of ecological replacement tortoises. Reintroducing a recently extirpated generalist seed disperser could, in theory, be a relatively straightforward Solitaire No. 27 solution to restore a large number of interactions within an ecosystem (Kaiser-Bunbury et al. 2010). Indeed, Gibbs et al. (2008) documented the positive effect a giant tortoise reintroduction had on the recruitment of an endangered keystone cactus species in the Galápagos. However, high rates of endemicity on oceanic islands mean that in many cases, local extirpation is synonymous with global extinction (Hansen 2010). In that case, practical options for management include letting the ecosystem reach a new equilibrium (Corlett 2013), managing the ecosystem with a human workforce (Griffiths et al. 2013) and introducing an ecological replacement species (Griffiths et al. 2013; Hansen 2010; Kaiser-Bunbury et al. 2010; Parker et al. 2010). Results from experiments using non-native tortoise species or subspecies as ecological replacements on offshore islets in Mauritius (Griffiths et al. 2010, 2011, 2013) and Pinta Island in the Galápagos (Hunter et al. 2013) have shown positive impacts on the restoration of ecosystem function and potential for application elsewhere (Hansen et al. 2010). There is a small but growing literature on the role of tortoises as seed dispersers (Blake et al. 2012; Carlson et al. 2003; Gibbs et al. 2008; Guzmán and Stevenson 2008; Griffiths et al. 2011; Jerozolimski et al. 2009; Strong and Fragoso 2006). Tortoises often live at high population densities, spread relatively evenly over the landscape (Gibson and Hamilton 1984; Strong and Fragoso 2006), eat large quantities of seeds of many species (Blake et al. 2012; Jerozolimski et al. 2009), move over relatively long distances (Blake et al. 2012; Guzmán and Stevenson 2008) and rest both in covered and open areas for thermoregulation (Griffiths 2010; Strong and 33 Research report Fragoso 2006). Their gut passage may be important for the germination success of native species (Griffiths et al. 2011; Rick and Bowman 1961) and can have detrimental impacts on that of non-natives (Carlson et al. 2003; Rick and Bowman 1961; but see Waibel et al. 2013). The Janzen-Connell model predicts that seed and seedling mortality has an inverse relationship with dispersal distance. Therefore, dispersal away from the parent tree may be crucial for seedling establishment (e.g. Hansen et al. 2008). Griffiths et al. (2011) demonstrated that the introduction of ecological replacement tortoises on Ile aux Aigrettes was successful in breaking the longstanding recruitment limitation of D. egrettarum, through the effects of their gut passage as well as dispersal beyond the seed shadow of parent trees. The only estimates of dispersal distance for tortoises published to date (Blake et al. 2012; Guzmán and Stevenson 2008; Jerozolimski et al. 2009; Strong and Fragoso 2006) have been derived through inference as opposed to direct observation. Our study aimed to fill this gap. Our principal aim was to measure the seed dispersal distances of ecological replacement Aldabra giant tortoises on Ile aux Aigrettes. Dispersal distance depends on a variety of factors including gut passage time, which in turn is affected by fruit pulp, and seed shape and size (C.J. Griffiths, pers. comm.). In order to increase the reliability of the results, we focused the study on the dispersal of a single species, the fleshy-fruited ebony D. egrettarum, which is commonly consumed by the tortoises (see Griffiths 2010; Griffiths et al. 2011). Our primary research question was: how far are Aldabra giant tortoises dispersing ebony seeds on Ile aux Aigrettes? Hansen et al. (2008) suggest that “even a tortoise will likely move a greater distance than 25 m within 1–3 weeks.” While we did not specifically measure gut passage time, our observations in the field indicated that it nearly always fell within the range of 10–21 days over the course of our experiment. We therefore predicted that the tortoises would disperse Diospyros egrettarum seeds significantly further than 25 metres. Secondly, in their native habitat, male and female Aldabra giant tortoises have differing spatial distribution patterns (Gibson and Hamilton 1983). We therefore expected ebony seed dispersal distances to be different for male and female Aldabra giant tortoises on Ile aux Aigrettes. contains some of the last remnants of ebony-rich lowland forest in the country (Griffiths et al. 2011; Varnham et al. 2002). As a nature reserve operated by the Mauritian Wildlife Foundation since 1987, it has been the site of intensive conservation and restoration work, including the eradication of black rats – important seed predators – weeding of invasive plants and the reintroduction of native and endemic plant and animal species (Varnham et al. 2002). Ile aux Aigrettes is demarcated by a permanent 12.5 m x 12.5 m survey grid. Diospyros egrettarum Richardson (Ebenaceae) is a critically endangered ebony species endemic to Mauritius (Page 1998; see Figure 1a). It was once a dominant coastal hardwood, but logging has reduced it to fewer than 10 individuals on the mainland. The only viable population is on Ile aux Aigrettes, where it has benefitted from the eradication of rats and weeding of exotic plants (Page 1998), as well as the introduction of Aldabra giant tortoises (Griffiths et al. 2011). Its fruits are large and roughly spherical, each containing 8 ± 2 large seeds (see Figure 1b, c), encased in a sticky pulp and a brittle exocarp (see Griffiths 2010). The species is generally dioecious. Its main historical seed dispersers would have been Cylindraspis tortoises and, possibly, Leiolopisma mauritiana, a giant skink (Griffiths 2010). Aldabra giant tortoises (Aldabrachelys gigantea; see Figure 1d) were first introduced to Ile aux Aigrettes in 2000 as ecological replacements for the extinct Cylindraspis species. They are considered suitable “proxies” given their phylogenetic and ecological similarities to the endemic species (Griffiths et al. 2010). All animals were born and raised in captivity, but they adapted well to the natural setting; they are not fed but are provided water for welfare reasons, as there is no standing water on the island. They were first held in enclosures, and were then released into the wild when it was deemed that they were not harming the native vegetation (Griffiths et al. 2012). There have been as many as 26 non-juvenile tortoises on the island (Griffiths et al. 2012), but at present there are 21 individuals, 10 male and 11 female (including one subadult). All the tortoises on the island are individually identifiable, and some of their life history is known (see Griffiths et al. 2012). The individuals included in the study were all adults, with a sex ratio of 10 females to 9 males. Methods Dispersal distance study Our dispersal distance study was conducted between June and August 2014 (see Table 1). Ripe ebony fruit was collected opportunistically over the island. Only fruits found on the ground – likely candidates for tortoise consumption – were Study site and species Ile aux Aigrettes (57o73’05”E, 20o42’03”S) is a 25 ha coralline islet located 700 m off the southeast coast of Mauritius, reaching a maximum elevation of 12 m above sea level. It Table 1. Numbers and ratios of Aldabra giant tortoises fed on Ile aux Aigrettes, by sex and feeding event, and corresponding faecal deposit recovery rates. Females fed (% total) Males fed (% total) Total tortoises fed Faeces recovered – females (% fed) Faeces recovered – males (% fed) Faeces recovered – total (% fed) June 13–14, 2014 8 (47) 9 (53) 17 8 (100) 8 (89) 16 (94) June 26–27, 2014 9 (50) 9 (50) 18 7 (78) 9 (100) 16 (89) July 10–11, 2014 10 (52.5) 9 (47.5) 19 9 (90) 8 (89) 17 (89.5) 27 (50) 27 (50) 54 24 (89) 25 (92.5) 49 (91) Dates fed Overall Solitaire No. 27 34 Tortoise seed dispersal Figure 1. (a) Diospyros egrettarum, showing signs of dispersal limitation; (b) D. egrettarum fruit; (c) D. egrettarum seeds; (d) Aldabrachelys gigantean; (e) Feeding A. gigantean; (f) faeces containing coloured pellets and D. egrettarum seeds. All photos: M. Kastner 2014. collected. Fruit that appeared overripe, desiccated or damaged was avoided, and gathered fruit was never kept longer than three days. Two tortoises were excluded from the study: one, a large male, because he appeared to be lethargic, and the other, a subadult female, in order to maintain consistency in age class. The remaining tortoises (n=19; 10 female and 9 male) were each fed a total of three times, with two exceptions. One was fed twice and another only once, because those individuals could not be located at the time. In order to feed the tortoises, we located them and presented them with 12–13 ebony fruits, along with a unique combination of coloured, non-toxic plastic pellets (1 tbsp per colour; 1–5 mm in diameter; Albert GmbH and Co. KG, Bünde, Nordrhein-Westfalen), in a shallow metal plate (see Figure 1e). The ebony fruits were fed to the tortoises to Figure 2. Maps of Ile aux Aigrettes showing (a) Aldabra giant tortoise feeding locations and (b) faecal deposits. Note the greater number of deposits than feeding locations. Solitaire No. 27 35 Research report Figure 3. Dispersal distances by Aldabra giant tortoises on Ile aux Aigrettes by (a) sex and (b) feeding event. Results encourage corresponding “natural” gut passage times, and hence representative dispersal distances. The pellets were encrusted in a banana to encourage consumption (Waibel et al. 2013). The tortoises always ate the banana and almost always ate all (and never less than half) of the ebony fruits. The coordinates of each feeding location were recorded using a global positioning system (GPS) device (eTrex 20; Garmin, Schaffhausen). Faecal deposits were located systematically as well as opportunistically. Systematic searches were conducted over the entire area of known tortoise distribution, plus a one gridsquare buffer surrounding that area. Any tortoise faeces found during searches were examined for coloured pellets (see Figure 1f) and broken apart if necessary – it was recorded if at least one identifiable pellet of each colour was found within the faecal matter. For each deposit, we recorded GPS coordinates, pellet colours, faeces appearance (fresh or not fresh), whether or not it contained ebony seeds, and any other noteworthy contents. A deposit was considered unique if it was separated by a minimum of 1m from its nearest neighbour. Dispersal distances A total of 143 faecal deposits were found (µTOTAL = 2.6 deposits/feed; µMale = 2.5, µFemale = 2.8) for 57 feeding events (see Figure 2). Faecal deposits were found for 91% of feeding events (Feed 1: 94%, Feed 2: 89%, Feed 3: 89.5%; see Table 1). On average, tortoises dispersed seeds 85.0±62.1 m away from the site of ingestion. Male dispersals (96.2±62.6m) were longer than those of females (75.1±60.4m; see Figure 3a), but not significantly so (F = 1.883; p = 0.193). Average female dispersal distance was skewed by two exceptionally long dispersal events, of 276.5 and 350.3m (the next-longest female dispersal was of 172.5m). Dispersal distances were higher for the third feeding event (105.6±77.1m; see Figure 3b) than for the first (76.4±53.8m) or the second (71.3±45.1m), but not significantly so (F = 3.052; p = 0.0517). Overall, the vast majority of recorded dispersals (88.11%) were over 25 m (males: 89.55%; females: 86.84%), and the square-root transformed data (n = 143; µ= 8.56; SD = 3.4) Table 2. Dispersal distances by Aldabra giant tortoises on Ile aux Aigrettes in distance classes <25m, 25–100m, 100–200m, and >200m, by sex and feeding event. Dispersal distance <25m 25–100m 100–200m >200m Total Dates fed F M Total F M Total F M Total F M Total F M Total June 13–14, 2014 4 2 6 11 7 18 9 7 16 0 0 0 24 16 40 June 26–27, 2014 2 3 5 21 11 32 3 11 14 0 1 1 26 26 52 July 10–11, 2014 4 2 6 9 11 20 11 7 18 2 5 7 26 25 51 Overall 10 7 17 41 29 70 23 25 48 2 6 8 76 67 143 (% total) (13) (10) (11) (54) (43) (49) (30) (37) (34) (3) (9) (6) Solitaire No. 27 (100) (100) (100) 36 Tortoise seed dispersal Table 3. Generalised linear mixed effects models assessing dispersal distance by tortoise sex (fixed effect), and different combinations of random effects. K: number of parameters, LL: log-likelihood, AIC: Akaike’s Information Criterion, ΔAIC: differences in AIC. Random effects K LL AIC ΔAIC ID + FEED 4 -1987 3981 0 ID + FEED + RAINFALL 5 -1944 3987 6 ID + RAINFALL 4 -1997 4003 22 ID 3 -2143 4291 310 was significantly greater (t = 9.136; p < 2.2 x 10-16) than a simulated normal distribution of equal sample size and variance. Nearly half (46.27%) of the males’ dispersals were over 100m (females: 32.89%), and 8.96% were over 200m (females: 2.63%; see Table 2). Mixed-effects model A generalised linear mixed-effects model for dispersal distance, with SEX as a fixed effect and ID and FEED as random effects, was selected based on its relative AIC as compared to other iterations of the model with different combinations of random effects. AIC dropped substantially when FEED was added as a random effect. RAINFALL did help model fit when added to ID, though not as much as FEED; including it alongside ID and FEED only complicated the model (see Table 3). SEX was not a significant predictor of dispersal distance (p = 0.479), but it did account for 53.43% of the variation with the standard error of the model’s fixed effects. Nearest-neighbour analyses On average, male tortoises were located 45.8±32.9m, and female tortoises 53.9±43.9m, away from the nearest member of their respective sex (see Figure 4a). Males and females were therefore not clustered by sex when we located them for feeding (F = 0.264; p = 0.615). Male tortoises tended to be located further (µMales = 73.6±45.1m), on average, than females (µFemales = 59.2±30.1m), from the nearest water point (see Figure 4b), although the difference was not significant (F = 0.727; p = 0.406). Discussion Coloured plastic pellets have been used with tortoises to measure gut passage times (Blake et al. 2012) and to mark individuals in a germination experiment (Waibel et al. 2013). Our study is novel in using plastic pellets to measure seed dispersal distances in situ. We recovered pellets for 91% of individuals fed (see Table 1). This result suggests that the method is viable for collecting robust dispersal distance datasets from free-ranging tortoises. Their tendency to avoid dense woody vegetation (Gibbs et al. 2008) and to rest in clearings (Strong and Fragoso 2006) may help in achieving high recovery rates. The method is nevertheless work-intensive, and benefited, in our case, from a relatively small and high-density population. Recovery is most efficient when tortoises are visited daily over the expected period of gut passage. Strong and Fragoso (2006) estimated a minimum dispersal distance of 91.2 m for Geochelone carbonaria and G. denticulata in the Brazilian Amazon, by multiplying the mean daily dispersal by the minimum gut passage time they recorded. This method may be problematic, since it assumes linearity in movement over consecutive days. Guzmán and Stevenson (2008) recorded a similar figure (89.6 ± 9.2 m) for G. deniculata in Peru, whereas Jerozolmiski et al. (2009) estimated mean dispersal distances of 174.1 m in the rainy season and 276.7 m in the dry season for the same species. The latter study overlaid the range of gut passage times they recorded in captivity with movement data measured in the field to produce potential “seed shadows”. Blake et al. (2012) used similar methodology on Chelonoides nigra on Santa Cruz Island in the Galápagos to produce an average seed dispersal Figure 4. Distance of each Aldabra giant tortoise fed on Ile aux Aigrettes to the nearest (a) member of the same sex, an indicator of clustering, and (b) water point. Solitaire No. 27 37 Research report distance of 394 m. We recorded a mean of 85.0 m, with a minimum of 0 m and a maximum of 350.3 m. Given the range of species, habitats and methods used to produce the estimates, it is perhaps less remarkable that estimates differ substantially than that they are all within the same order of magnitude. The vast majority of recorded dispersals (over 88%; see Table 2), were longer than 25 m, and mean dispersal distance was significantly higher than 25 m. We can therefore reject the null hypothesis that Aldabra giant tortoise ebony seed dispersal distance on Ile aux Aigrettes is less than or equal to 25 m, and confirm the accuracy of Hansen et al.’s (2008) prediction that tortoise seed dispersal tends to be longer than that distance. This suggests that dispersal by the ecological replacement tortoises is generally far enough to allow ebony seeds to escape most density-dependent mortality factors (Hansen et al. 2008), although some density-dependent effects are certainly manifested within tortoise-dispersed seed clusters (Griffiths 2010). This interpretation is based on the assumption that the Janzen-Connell model applies to this tree species. The 25 m threshold may be conservative, since the diameter of an average D. egrettarum canopy on Ile aux Aigrettes, the seed shadow within which most non-dispersed seeds are confined, is probably smaller than that distance. Our findings support the evidence compiled by Griffiths et al. (2011) demonstrating that dispersal by Aldabra giant tortoises is helping ebony on Ile aux Aigrettes to overcome long-standing recruitment limitation caused by the extinction of their historical dispersal agents. It should be noted that the removal of pulp during gut passage, and deposition within nutrient-rich and moisture-retaining faecal matter, are other potentially important factors contributing to the germination and eventual survival of seedlings (Griffiths 2010). Cain et al. (2000) stress the critical importance of longdistance seed dispersal for plant population dynamics, and the scarcity of studies capturing the tails of seed dispersal curves. Nearly 40% of the dispersal distances we recorded were longer than 100m, and 6% were longer than 200m: such dispersals can be considered as “long distance” (Cain et al. 2000) and “very long distance” (Blake et al. 2012), respectively. Long distance seed dispersals contribute significantly to dynamics and gene flow of tree populations (Cain et al. 2000; Jerozolimski et al. 2009). They may be especially important for dioecious species such as D. egrettarum, which need to compensate for the loss of one sex role relative to their hermaphroditic competitors (Griffiths 2010). Long distance dispersals may also contribute to maintaining species diversity within a forest (Janzen and Martin 1982; Terborgh et al. 2008), and to the restoration of disturbed landscapes (Wunderle 1997). D. egrettarum was logged on some portions of Ile aux Aigrettes (Griffiths et al. 2011) and tortoise-mediated dispersal may help the species to re-establish on suitable habitat. It will only be possible to truly assess the effect of tortoise seed dispersal on such ecosystem processes in the very long term, as ebony trees are particularly slow-growing, and have long generational times. Nevertheless, our results support the body of evidence demonstrating that the introduction of ecological replacement tortoises on Ile aux Aigrettes is reviving important plant-animal interactions on the island (Hansen et al. 2010; Kaiser-Bunbury et al. 2010). There are a number of components to seed dispersal effectiveness beyond dispersal distance, such number of seeds dispersed, effects of gut passage and faecal matter, and deposition site (Schupp 1993). Several authors have suggested Solitaire No. 27 that tortoises are effective seed dispersers, in that, beyond dispersing over relatively long distances, they also consume large quantities of a wide variety of fruit, their digestion is relatively benign and may sometimes help in germination, their populations are often dense but scattered over the landscape, and they occupy a wide range of microhabitats (Jerozolimski et al. 2009; Strong and Fragoso 2006). We observed dispersal by Aldabra giant tortoises of a variety of large-seeded native and non-native species, including Eugenia on a regular basis, as well as Dracaena, Hibiscus, Scaevola, Morinda and Acacia species. Griffiths et al. (2011) have demonstrated the beneficial effects of tortoise gut passage for D. egrettarum. Those benefits may extend to other fleshyfruited species potentially prone to fungal infection, such as Eugenia. Tortoises on Ile aux Aigrettes certainly do deposit seeds over a full gradient of shaded to open microhabitats (pers. obs.). It seems reasonable to hypothesise, therefore, that Aldabra giant tortoises are acting as effective seed dispersers on Ile aux Aigrettes. On the other hand, their impact will logically be restricted to their area of occupancy, and it does appear that their range is restricted on the island (see Figure 2). Their potential habitat may be confined by access to water, locally dense vegetation or barriers of coralline rock; alternatively, they may not be exploiting all available habitats if the population is below its carrying capacity. Sex was not a significant predictor of dispersal distance. However, it does account for a substantial proportion of the variation within the model, and male tortoises did disperse seeds farther, on average, than females. Figure 2 clearly shows differential distribution of tortoises by sex on the island, with females especially concentrated near buildings by the western coast and males more common inland. Although the result was not statistically significant, male tortoises were generally encountered further from water points than females. Fresh water appears to be the major motivating factor for long distance movements by tortoises on Ile aux Aigrettes (Z. Ahamud and N. Zuël, pers. comm.), and it is possible that male tortoises are travelling relatively long distances on a regular basis to drink water, with important implications for seed dispersal. Gibson and Hamilton (1983) noted differential habitat use by sex in Aldabra giant tortoises in their native range. While the species is relatively gregarious, some level of home range fidelity by the tortoises on Ile aux Aigrettes in apparent. Differential home range size (Diemer 1992) and movement patterns (McRae et al. 1981) by sex have been documented for Gopherus polyphemus in Florida. Furthering our understanding of tortoise behaviour, including sex-dependent variations therein, will help us refine seed dispersal models in the future (Russo et al. 2006). Skewing the sex ratio of populations is common practice in animal translocations (Armstrong and Reynolds 2012), especially for the purpose of maximising breeding rates. If the goal of the translocation is the restoration of ecological processes, as is the case in rewilding projects (Seddon et al. 2014), then managers should consider the possibility of sex-related differences in contribution to ecosystem function within a species. It would be useful to expand this study to cover seasonal and annual variations in environmental conditions and ebony fruit availability. It is also difficult to assess the applicability of the method to other locations. The small size of the tortoise population and restricted island area may have been advantageous in achieving a high recovery rate for pellets. 38 Tortoise seed dispersal Difficulties may be encountered, however, in areas with rapid decomposition rates and/or difficult access. Nevertheless, our study is the first to measure precise point-to-point seed dispersal distances for tortoises in a natural setting, and our results contribute to the existing evidence suggesting that the ecological replacement tortoises are acting as effective seed dispersers on the island. They appear to be filling at least part of the ecological niche left vacant by the extinction of the native Cylindraspis tortoises, and contributing to the restoration of critical plant- animal mutualisms. However, the success of this ecological replacement experiment, and others that may be inspired by it, will only be confirmed in the long term, and the perceived benefits should always be weighed against any potential or actual negative impacts. Acknowledgements Many thanks to Christine Griffiths for feedback. Thank you Zairabee Ahamud for teaching us all about the tortoises on Round Island. 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Forest Ecology and Management 99: 223235. Martin Kastner and Ysabella Montaño carried out this study as part of their PG Dip course in Endangered Species Recovery with Durrell Conservation Academy, Mauritius in 2014. Martin participated in the course on a New Noah scholarship from Wildlife Preservation Canada. He is currently based in Guam working as an avian restoration project manager for Colorado State University. Ysabella is completing her MSc in Environmental Biology at Suranaree University of Technology, Thailand. Nicolas Zuël is Fauna Manager at the Mauritian Wildlife Foundation. Email: [email protected] Learn from the conservation experts We are world leaders in saving species from extinction and empowering others to run conservation projects worldwide, operating right at the interface between animals in the wild and those in captivity. Our courses We cover a wide variety of topics and cross-disciplinary skills relevant to successful conservation and wildlife management. From 3–5 day courses to a 6-month Post Graduate Diploma, the Academy provides career-long training services in Jersey, Mauritius, UK and online. Endangered species recovery techniques Technical training in topics such as GIS, education, husbandry, conservation management and leadership Specific information, course outlines and dates can be found online at www.durrell.org To apply, please email [email protected] Solitaire is edited by Eluned Price E-mail: [email protected] Contact us: Durrell Wildlife Conservation Trust, Les Augres Manor, Trinity, Jersey, Channel Islands, JE3 5BP Tel: +44 (0) 1534 860000 Fax: +44 (0) 1534 860001 www.durrell.org