Download Untitled - Durrell Wildlife Conservation Trust

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. Thanks to Mark O’Connell and Rosemary
Moorhouse-Gann (and Nicolas Zuël of course) for advice on
statistics. Jamie Copsey, thank you for facilitating the whole
process. MK’s participation in the 2014 Durrell Postgraduate Diploma in Endangered Species Recovery course was
supported by a New Noah scholarship from Wildlife Preservation Canada.
References
Armstrong, DP and Reynolds, MH (2012). Modelling
reintroduced populations: the state of the art and future
directions. In Ewen, JG, Armstrong, DP and Parker, KA
(eds). Reintroduction Biology: Integrating Science and
Management. Chichester: John Wiley and Sons, 165–
222.
Bates, D and Maechler, M (2009). lme4: Linear mixed-effects
models using S4 classes. R package version 0.99937531. Available at: http://lme4.r-forge.r-project.org/.
Blake, S, Wikelski, M, Cabrera, F, Guezou, A, Silva, M,
Sadeghayobi, E, Yackulic, CB and Jaramillo, P (2012).
Seed dispersal by Galapagos tortoises. Journal of
Biogeography 39: 1961–1972.
Cain, ML, Milligan, BG and Strand, AE (2000). Long-distance
seed dispersal in plant populations. American Journal of
Botany 87: 1217–1227.
Carlson, JE, Menges, ES and Marks, PL (2003). Seed dispersal
by Gopherus polyphemus at Archbold Biological Station,
Florida. Florida Scientist 66: 147–154.
Cheke, A and Hume, JP (2008). The Lost Land of the Dodo: An
Ecological History of Mauritius, Réunion and Rodrigues.
New Haven: Yale University Press.
Corlett, RT (2013). The shifted baseline: Prehistoric defaunation
in the tropics and its consequences for biodiversity
conservation. Biological Conservation 163: 13–21.
Diemer, JE (1992). Home range and movements of the
tortoise Gopherus polyphemus in northern Florida. Journal
of Herpetology 26: 158–165.
Gibbs, JP, Marquez, C and Sterling, EJ (2008). The role
of endangered species reintroduction in ecosystem
restoration: tortoise–cactus interactions on Española
Island, Galápagos.Restoration Ecology 16: 88–93.
Gibbs, JP, Sterling, EJ and Zabala, FJ (2010). Giant tortoises
as ecological engineers: a long-term quasi-experiment
in the Galápagos Islands. Biotropica 42: 208–214.
Solitaire No. 27
Gibson, CWD and Hamilton, J (1983). Feeding ecology and
seasonal movements of giant tortoises on Aldabra atoll.
Oecologia 56: 84–92.
Gibson, CWD and Hamilton, J (1984). Population processes
in a large herbivorous reptile: the giant tortoise of Aldabra
atoll. Oecologia 61: 230–240.
Griffiths, CJ (2010). Conservation and Restoration of Mauritian
Plant Communities using Taxon Substitutes. PhD thesis.
Bristol: University of Bristol.
Griffiths, CJ, Jones, CG, Hansen, DM, Puttoo, M, Tatayah, RV,
Müller, CB and Harris, S (2010). The use of extant nonindigenous tortoises as a restoration tool to replace extinct
ecosystem engineers. Restoration Ecology 18: 1–7.
Griffiths, CJ, Hansen, DM, Jones, CG, Zuël, N and Harris, S
(2011). Resurrecting extinct interactions with extant
substitutes. Current Biology 21: 762–765.
Griffiths, CJ, Zuël, N, Tatayah, V, Jones, CG, Griffiths, O and
Harris, S (2012). The welfare implications of using exotic
tortoises as ecological replacements. PloS One 7:
e39395.
Griffiths, CJ, Zuel, N, Jones, CG, Ahamud, Z and Harris, S
(2013). Assessing the potential to restore historic grazing
ecosystems with tortoise ecological replacements.
Conservation Biology 27: 690–700.
Guzmán, A and Stevenson, PR (2008). Seed dispersal, habitat
selection and movement patterns in the Amazonian
tortoise, Geochelone denticulata. Amphibia–Reptilia 29:
463–472.
Hansen, DM (2010). On the use of taxon substitutes in rewilding
projects on islands. In: Pérez-Mellado, V and Ramon, C
(eds). Islands and Evolution. Menorca: Institut Menorquí
d’Estudis, 111–146.
Hansen, DM, Donlan, CJ, Griffiths, CJ and Campbell, KJ
(2010). Ecological history and latent conservation
potential: large and giant tortoises as a model for taxon
substitutions. Ecography 33: 272–284.
Hansen, DM, Kaiser, CN and Müller, CB (2008). Seed dispersal
and establishment of endangered plants on oceanic
islands: the Janzen-Connell model, and the use of
ecological analogues. PLoS One 3: e2111.
Hunter, EA, Gibbs, JP, Cayot, LJ, and Tapia, W (2013).
Equivalency of Galápagos giant tortoises used as
ecological replacement species to restore ecosystem
functions. Conservation Biology 27: 701–709.
Janzen, DH and Martin, PS (1982). Neotropical anachronisms:
the fruits the gomphotheres ate. Science 215: 19–27.
Jerozolimski, A, Ribeiro, MBN and Martins, M (2009). Are
tortoises important seed dispersers in Amazonian forests?
Oecologia 161: 517–528.
Kaiser-Bunbury, CN, Traveset, A and Hansen, DM (2010).
Conservation and restoration of plant–animal mutualisms
on oceanic islands. Perspectives in Plant Ecology,
Evolution and Systematics 12: 131–143.
McRae, WA, Landers, JL and Garner, JA (1981). Movement
patterns and home range of the gopher tortoise.
American Midland Naturalist 106: 165–179.
Page, W (1998). Diospyros egrettarum. The IUCN Red List of
Threatened Species. Version 2014.2. www.iucnredlist.org
(downloaded on 17 September 2014).
Parker, KA, Seabrook-Davison, M and Ewen, JG (2010).
Opportunities for nonnative ecological replacements in
ecosystem restoration. Restoration Ecology 18: 269–273.
39
Research report
Rick, CM and Bowman, RI (1961). Galapagos tomatoes and
tortoises. Evolution 15: 407–417.
Russo, SE, Portnoy, S and Augspurger, CK (2006). Incorporating
animal behavior into seed dispersal models: implications
for seed shadows. Ecology 87: 3160–3174.
Schupp, EW (1993). Quantity, quality and the effectiveness of
seed dispersal by animals. In: Fleming, TH and Estrada,
A (eds). Frugivory and Seed Dispersal: Ecological and
Evolutionary Aspects. Netherlands: Springer, 15–29.
Seddon, PJ, Griffiths, CJ, Soorae, PS and Armstrong, DP (2014).
Reversing defaunation: Restoring species in a changing
world. Science 345: 406–412.
Strong, JN and Fragoso, J (2006). Seed dispersal by
Geochelone carbonaria and Geochelone denticulata
in northwestern Brazil. Biotropica 38: 683–686.
Terborgh, J, Nuñez-Iturri, G, Pitman, NC, Valverde, FHC,
Alvarez, P, Swamy, V, Pringle, EG and Paine, CT (2008). Tree
recruitment in an empty forest. Ecology 89: 1757–1768.
Varnham, KJ, Roy, SS, Seymour, A, Mauremootoo, J, Jones,
CG and Harris, S (2002). Eradicating Indian musk shrews
(Suncus murinus, Soricidae) from Mauritian offshore islands.
In: Veitch, CR and Clout, MN (eds). Turning the Tide: The
Eradication of Invasive Species. Gland, Switzerland: IUCN
Invasive Species Specialist Group, 342–349.
Waibel, A, Griffiths, CJ, Zuël, N, Schmid, B, and Albrecht, M
(2013). Does a giant tortoise taxon substitute enhance
seed germination of exotic fleshy-fruited plants? Journal
of Plant Ecology 6: 57-63.
Wunderle Jr, JM (1997). The role of animal seed dispersal
in accelerating native forest regeneration on degraded
tropical lands. 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