Captive propagation of threatened primates - the example of the
Lion-tailed Macaque Macaca silenus
Werner Kaumanns 1, MewaSingh 2 & Alexander Sliwa 3
1 LTM Research and Conservation, Eschenweg 5, 37130 Gleichen,
Germany
2 Biopsychology Laboratory,
University of Mysore, Mysuru, Karnataka 570006, India
2 Organismal and Evolutionary Biology Unit, Jawaharlal Nehru Centre for Advanced
Scientific Research, Jakkur, Bengaluru, Karnataka
560064, India
3 Zoologischer Garten Köln, Riehler Straße 173, 50735 Köln, Germany
1 silenus@t-online.de, 2 mewasinghltm@gmail.com
(corresponding author), 3 sliwa@koelnerzoo.de
Abstract: Many conservation-oriented breeding
programs are not likely to reach their goal of establishing self-sustaining
populations. Some zoo biologists
propagate to reconsider zoo-based conservation policies and strategies. The Lion-tailed Macaque is a flagship
species for in situ conservation and a high priority species in captive
propagation. This article reviews
the captive management history of the Lion-tailed Macaque, identifies
management patterns that might have negatively influenced the development of
the programs, and proposes to use this analysis to initiate a new management
perspective. In the North American
captive Lion-tailed Macaque population under the Species Survival Plan (SSP),
the strong reduction in population size and group sizes due to space problems
might have contributed to a decrease in population viability. The population over two decades has
declined from almost 300 to less than 100 individuals. In the European population under the
European Endangered Species Program (EEP), population size was not limited and
larger groups were advocated. The
population grew slowly but steadily to a present size of more than 350
individuals over about 23 years. The effective population size has remained low in both SSP and EEP
populations. A
general conceptual framework that focuses on individuals and their phenotypes
for in situ and ex situ conservation recently developed by field
conservationists is briefly introduced. It is used to suggest improvements in the
management of the Lion-tailed Macaque. It is concluded that the size and structure of a breeding population is
to be decided so as to provide conditions and materials for successful
reproduction rather than by the available zoo space only. For this, large groups and populations
with representation of all age-sex classes are advocated. This would result in a further reduction
in the number of species kept in zoos. It is indicated that zoo biology needs to develop new concepts that
include a large spectrum of concepts of biology and knowledge about the
adaptive potential of animal species under altered and fragmented conditions.
Keywords: Behaviour, captive propagation, effective population size, European
Endangered Species Program, individual-based management, Lion-tailed Macaque,
primate conservation, Species Survival Plan.
doi: http://dx.doi.org/10.11609/JoTT.o3625.4825-39 | ZooBank:urn:lsid:zoobank.org:pub:7BB73AF7-0E44-48F3-9234-B8BA35054503
Editor: Karin Schwartz, George Mason University, Fairfax, Virginia. Date
of publication: 26 October 2013 (online & print)
Manuscript details: Ms # o3625 | Received 15 May
2013 | Final received 08 October 2013 | Finally accepted 09 October 2013
Citation: Kaumanns, W., M. Singh & A. Sliwa (2013). Captive propagation of threatened primates - the example of the
Lion-tailed Macaque Macaca silenus . Journal of Threatened
Taxa 5(14): 4825–4839; http://dx.doi.org/10.11609/JoTT.o3625.4825-39
Copyright: © Kaumanns et al. 2013. Creative Commons Attribution 3.0 Unported License. JoTTallows unrestricted use of this article in any medium, reproduction and
distribution by providing adequate credit to the authors and the source of
publication.
Funding: German Primate Centre (DPZ = Deutsches Primatenzentrum ) and of Cologne Zoo (KölnerZoo) supported the work for
the LTM European Breeding
Program.
Competing Interest: Authors declare no competing interests.
Author Contribution: Equal contribution.
Author Details: Werner Kaumanns worked as a scientist and Head of Breeding and Husbandry section
at DPZ for almost two decades then was a curator of primates at Cologne Zoo. He
was the LTM EEP coordinator for the Lion-tailed Macquefrom 1989–2006 and worked with LTM both in situ and ex situ. He is
specifically interested in the effects of altered living conditions on
primates.
MewaSingh has been
working on primates for three decades and has spent considerable time in the
field studying the behaviour and the ecology of
Lion-tailed Macaqes and of several other primate
species.
Alexander Sliwa is a curator of primates and of other mammals at Cologne Zoo. He
is a member of the EAZA Old World Monkey Taxon Advisory Group. He is also
working longterm with felid and hyaenidpopulations, both in situ and ex situ.
Acknowledgements: We
thank Dr. Tom Ness and Dr.Scott Carter for providing SSP Studbook data, for helpful discussions and for
supporting conservation-oriented research on the Lion-tailed Macaque in
southern India. We also thank the
reviewers for their very insightful comments; TiergartenWels, Austria, and Zoo Dresden, Germany, for supporting in situ conservation research in
southern India; Prof. Dr.H.J. Kuhn, founding director at DPZ, for his initiative to work with
Lion-tailed Macaques and to contribute to their conservation.
For figures, images, tables -- click here
Introduction
There is a growing
number of studies that critically analyze the status
of captive populations of wild animals in conservation-oriented breeding
programs. It seems that many
programs are not likely to reach their goal of establishing self-sustaining
populations that can serve as a reserve for their threatened wild counterparts
(Kaumanns et al. 2000; Lees & Wilcken2009; Conway 2011; Lacy 2013). Many
breeding programs for primates are also facing these problems. Due to low breeding success, they do not
grow properly and are at risk of losing genetic and phenotypic diversity, and a
discussion of the possible reasons for the problem has been started (Kaumanns et al. 2000, 2008). The awareness among the international
zoo community of the seriousness of the situation, however, seems to be still
limited. Only a few zoo biologists
propagate to reconsider or redefine the relevant zoo-based conservation
policies and strategies. According
to Conway (2011), a more sharply focussed approach and more support for, and
collaboration with, parks and reserves are needed for “buying time for wild
animals with zoos”. Lacy (2013)
discusses how to achieve “true sustainability” of zoo populations. This would require managing isolated zoo
populations as part of a metapopulation both within a
global species management program and together with small populations in the
wild.
The Lion-tailed Macaque Macaca silenus is a flagship species for the many
endemic and threatened animal and plant species of the Western Ghats, southern
India, and a high priority species in captive propagation. It was one of the first primate species
for which, in 1983, a National (USA) and in 1987 an International Studbook was established (Gledhill
1987) and one of the first for which a Species Survival Plan (SSP) and a
European Endangered Species Programme (EEP) were established in 1980 and 1989,
respectively, in North America and Europe. A recent analysis of the conservation history of the Lion-tailed
Macaque, however, concluded that even after more than three decades of both in
situ and ex situ efforts, the status of both the wild and the global captive
population has not significantly improved (Singh et al. 2009). This seems to be specifically the case
for the global captive population, where the majority of the subpopulations did
not develop satisfactorily despite a promising start.
The aim of this paper is to review the
management history of the captive population of the Lion-tailed Macaque to
identify management patterns that might have negatively influenced its
development. This analysis will be
used to promote the initiation of new management perspectives for the
Lion-tailed Macaque as well as for other primate species.
Materials and Methods
The material used in this analysis has been
obtained from studbooks and reports of the EEP (1989–2012) and the SSP
(1981–2012). In addition,
author WK has a long experience of managing captive populations of Lion-tailed
Macaques and other primate species and worked as the species coordinator for
the Lion-tailed Macaque EEP between 1989 and 2006. Author MS has decades of experience
studying Lion-tailed Macaques in their natural habitats in the Western Ghats. Author AS has been the EEP coordinator
for the Lion-tailed Macaque since 2006 and the International Studbook keeper
since 2013.
Status
Development of the
historical captive population
The global historical population covering a
recording period of more than 100 years includes the present living population
of about 500 individuals worldwide. A total captive population of 1,041 individuals with the first record
going back to 1,899 was documented in the first International Studbook
(Gledhill 1987) for the Lion-tailed Macaque. More recently, Ness (2011)
recorded a total of 878 (426.385.67) individuals (North American Studbook) and Sliwa (2011; European Studbook) reported 1,150 (514.547.89)
individuals. The global
international studbook is not yet fully updated. A tentative estimation of the number of
individuals kept in other regions would add another 500, thus leading to a
total historical population of about 2,500 individuals. An estimated minimum
of 30% of these were wild caught mainly in the first decades of the 20th
century. As of the end of 2005
Lion-tailed Macaques were kept on all continents except Africa and Antartica, with the two largest sub-populations living in
North America and Europe and smaller populations in India, Japan, China, Korea,
Malaysia, Mexico, and Australia (Fitch-Snyder 2006). The development of the two largest
sub-populations, which constitute the main parts of the global population, is
described below.
North America
Figure 1 shows the development of the North
American population for a period of 50 years between 1960 and 2008. After an increase to a peak of 268
individuals in 1988 (Ness 2011), it steadily decreased to a size of 88 (44.44)
individuals kept in 20 institutions in 2011. The most recent census in 2012 reveals a
number of 74 (37.37.0) individuals (Ness, pers. comm. 2013).
According to the 2011 Studbook, from the
346 females recorded, 182 (52.6%) were recorded dams. The lifetime meannumber of births per dam is 4.05, the median is 4 (only for recorded dams, not
all females, and does not include offspring with unknown dams; N=559 births from
138 dams, max =13, min=1).
At present, none of the 54 founder individuals
is alive. The current managed
population of 46 (20.26.0) has a genetic diversity of 96% but with an effective
to actual population size ratio (Ne/N) of only 0.12
which is far below the typical ratio of 0.30. This indicates a very low breeding
potential of this population (Carter & Ness 2012).
It is reported that there were large
differences in reproductive output for the females and even more for the males
(Lindburg et al. 1989; Lindburg& Forney 1992; Lindburg 2001). No systematic information is available
on the effects of birth control on productivity patterns on population
level. Figure 2 shows the
development of the North American population with reference to births, deaths,
exports and imports. Since about
1990, there has been a considerable decrease in population size.
Europe
Figure 3 and Figure 4 show the development of
the European population. The
population slowly but steadily increased to a size of 343 individuals
(145.180.18) in 2011, kept in 43 institutions (Sliwa2011). The
development with reference to births, deaths and imports has been reported by Kaumanns et al. (2006). In the 1960s and 1970s, population
growth was mainly influenced by the import of wild-born Lion-tailed
Macaques. Between 1985 and 1987, a
further 39 individuals were imported from the SSP population. Kaumanns et
al. (2006) and Sliwa (2011) show that the mean annual
birth rate only slightly increased over the decades. Mean annual mortality rate, however,
decreased considerably, whereas the mean annual infant mortality increased over
the years to a level of 35%, where it remained constant. The mean annual birth rate was only
slightly higher than the mean annual mortality rate, thus leading to the slow
population growth. Taking
into account the varying number of adult females over years and a birth interval
of two to three years, the mean number of births per year was low. As has been described earlier (Kaumanns & Rohrhuber 1995; Kaumanns et al. 2001, 2006), the females, starting with the
founder generation in the 1950s and continuing till now, vary considerably in
reproductive output. On an average,
during the period between 1990 and 2002, only about 30% of potentially
reproductive females gave birth to surviving offspring (Kaumannset al. 2008). Since most groups in
the European population were one-male units, it is evident that the mean
contribution of the males to reproduction was much lower than that of the
females. Overall, the data available on the reproductive output of females and
males suggest that the effective population size in the European Lion-tailed
Macaque population is far below the population size (Kaumannset al. 2006).
Analysis of breeding
programs
Since the 1980s, most of the captive
Lion-tailed Macaques were included in the breeding programs. This led to a more systematic and
conservation-oriented management above the level of individual
institutions. It was expected to
increase productivity and to achieve sustainability. The following more detailed analysis of
the captive Lion-tailed Macaque population will, therefore, focus on these 30
years (1980–2010) of its history covering about six generations, and it
will ask whether the two large programs achieved their goals. Table 1 provides an overview of the
programs.
As it is obvious from Fig. 1, the American
population showed a 100% increase in size already in the decade prior to the
establishment of the SSP in 1981, and during the first decade of the program,
the population almost doubled again (Lindburg &
Gledhill 1992). In 1988, there were
268 individuals recorded. This productive
early period of SSP management was followed by a period of continuous
decline. In the last eleven years,
there have only been six surviving infants (Ness 2011). The European population, too, was
growing already in the years before the EEP was started in 1989, and it grew
continuously since then (Fig. 3). The EEP recorded more than 200 births in the last 10 years (Sliwa 2011).
There were several attempts to establish a
breeding program for the Lion-tailed Macaque in India, its country of origin. Indian zoos, however, have failed in
establishing the necessary organizational and infrastructural conditions for a
successful management so far (Krishnakumar & Manimozhi 2000; Singh et al. 2012). The historical population in Indian zoos
between 1940 and 2010 comprised 273 individuals (Malviya2011). About 40% of these were (and
are) wild caught. The actual
captive population of about 65 individuals is widely scattered over many zoos
and seems to be of low viability; breeding is rare. About 50% of the holders keep unisex
groups only. Additionally, small
numbers of Lion-tailed Macaques are kept in Japan, Australia, Singapore, Korea,
Malaysia, Mexico, and China. They
are managed on a national level. Due to their small numbers, however, they do not play a substantial role
as subpopulations but may contain important genetic material.
Problems and
management strategies in the breeding programs
A national breeding
program for the Lion-tailed Macaque was initiated by the American zoos in 1980 because according to Hill (1971), the
species was classified as threatened with extinction in the wild and a captive
population was planned as a reserve. To reach this goal, the status of the zoo population needed improvement,
which was attempted by establishing an Endangered Species Breeding Program (Foose & Conway 1985). A comprehensive volume reports the
efforts made to optimize the management of the population (Heltne1985).
In his first analysis of the status of the
captive population of Lion-tailed Macaques for the time period 1971–1977,Lindburg (1980a) identified the low number of births
as an important reason for the poor status of this endangered species in
zoos. According to him, less than
25% of the potentially reproductive females gave birth to infants, and a
significant percentage of the latter died soon after birth. A high proportion of non-breeding adult
females is a pattern which has characterized the
captive Lion-tailed Macaque populations since then. It has been regularly noted
in reports and publications and was discussed in all international meetings
both for the SSP and the EEP population (SSP: Lindburg1980b; Lindburg et al. 1989, 1992; Melnick 1990; EEP: Kaumanns &Rohrhuber 1995; Kaumanns et
al. 2001). These authors also point
to high infant mortality as the second key pattern of the captive Lion-tailed
Macaque populations. It seems that the highest proportion of deaths in captive
Lion-tailed Macaques is due to mortality in the first weeks of life (Lindburg et al. 1992; Kaumanns& Rohrhuber 1995; Lindburg2001). Breeding problems were
discussed during the international meeting on the Lion-tailed Macaque in San
Diego in 1990 as a critical factor for the survival of the global captive
population. Appropriate social
management was emphasized as a means to reduce breeding problems (Melnick 1990).
In the years after the San Diego meeting,
however, in the two large breeding programs, management strategies developed
with different goals. In the case of the EEP, establishing a large population
was regarded as an important goal per se and a minimal size of about 400
individuals was recommended based on behavioural and social concerns. In the case of the SSP, increasing the
population size was also propagated in the earlier period of the program. Conway (1985) proposed 500 individuals
necessary for a “save” population. Lindburg (2001), however, stated that in the mid 1980s, the
population already exceeded the 200 spaces that zoos in North America were
willing to devote to the species. Although a substantial number of non-reproducing females remained,
unexplained breeding problems in the SSP population lost the focus of
attention. Mainly due to a lack of
spaces and a decreasing number of zoos interested in keeping the species, SSP
suggestions and recommendations mainly focused on a reduction in population
size but at the same time, on the establishment of “hedge breeding” that is,
breeding on a scale sufficient to maintain a viable population as a hedge
against catastrophic disappearance of the remaining wild population (Lindburg et al. 1997; Lindburg2001). Fitch-Snyder (1990)
reports that following this approach, reproduction was concentrated in selected
institutions and the surplus non-breeding individuals were kept at the other
facilities. Stable
social groups of females were retained by moving only males between
institutions. Cross-fostering of infants (which
were not related to the “new” mother) was propagated to promote genetic
diversity thus increasing the number of non-related individuals in the
group. The use of reversible and
non-reversible birth control (both for males and females) and the establishment
of all-male groups at an early age were recommended. The exclusion of herpes B positive
individuals from the breeding population further reduced the effective
population size.
It was assumed that the resulting much smaller
(but genetically well balanced) population, with many females under
birth-control and neutered individuals, remained viable for the purposes of
“hedge breeding” and could be enlarged by “switching on” reproduction again if
needed (steady- state maintenance, see Lindburg et
al. 1997; Lindburg 2001). It seems that the importance of the fact
that a significant proportion of the females (and groups) still might have
breeding problems was underestimated. In any case zero population growth was desired and therefore only few
“new” infants per year were recommended. However, Lindburg (2001) pointed to the
possible negative consequences of steady-state breeding for social and demographic
structures. As a consequence of
“steady-state policy”, group sizes decreased. Lindburg(1992) stated that most institutions had groups with less than seven members
because young males were removed early and kept separately to avoid social
conflicts. According to Ness
(2011), about 75% of the actual institutions keep less than five
individuals. “Steady-state
breeding” indeed led to a strong decrease in population size. From 163 Lion-tailed Macaques in 1980
and 268 individuals in 1988, population size dropped to 88 individuals in 2011,
with most of the latter probably being non-reproductive (Ness 2011). Of the 81 current individuals, 28 are
non-reproductives due to sterilization and six are
excluded from breeding due to old age and medical reasons (Carter & Ness
2012).
In contrast to what happened in the SSP,
limiting population size was not recommended for the EEP. “Breeding problems”
were regarded as a key topic for the EEP management. Birth patterns were monitored regularly
and discussed in the annual reports between 1990 and 2004. The percentage of females that were
breeding (30%) remained low, and infant mortality remained high (Kaumanns et al. 2006, 2008). A small proportion of the females gave
birth to a large proportion of the infants (Kaumannset al. 2001). The annual EEP
recommendations focused on aspects of behavioural and especially social
management, which were expected to reduce breeding problems. As a key
recommendation, the establishment of large groups, by allowing groups to grow
continuously, was propagated. Large groups were expected to provide better
social and socialization conditions. The absolute number of larger groups grew
(Table 2). The number of groups
with a minimum of five members increased from 7 to 26 between 1989 and
2011. However, the percentage of
such groups increased only marginally.
Since large groups and stability in group
composition and social relationships were propagated, removals and transfers of
individuals between groups were done only to prevent inbreeding and/or to
establish new groups. Between 1990 and 2004, a total of 167 Lion-tailed
Macaques were transferred: 119 (81,38) individuals were transferred within the
EEP and 48 came from or went to non-EEP institutions.
The EEP population, with a mean of about 10%
increase in the number of individuals per year between 1990 and 2002 (Kaumanns et al. 2008), grew only little but steadily (Fig.
3).
Metapopulation management
A key outcome of the San Diego meeting in 1990
was a global five-year action plan (Chivers 1990)
that referred to the important topics and goals of Lion-tailed Macaque
conservation. Similar to previous
meetings, the need for more field studies was emphasized. The field studies should generate more
knowledge about the biology and especially the reproductive biology of the
species, which was expected to help solve breeding problems. A better international cooperation
between the larger programs and the Indian zoos was also strongly recommended. In the years after 1991, international
cooperation was mainly realized via further international congresses. Experts both from the wild and from the
zoos met, exchanged information and discussed the problems of the populations. The exchange of ideas and data
concerning captive management, however, did not lead to a unified management
that would have covered all captive and wild populations. As has been described above, SSP and EEP
even developed divergent “management policies”. Both programs, however, supported field
studies by providing funds and supported Indian zoos by providing know how and
training opportunities. The annual
EEP reports since 1995 reflect a growing tendency to consequently discuss
matters of the EEP population in the context of the global captive and wild
population. Especially the EEP
husbandry guidelines (Kaumanns et al. 2006)
explicitly used new results from field studies, particularly with reference to
the social system and to reproduction, to refine or support the recommended
keeping systems. On the other hand,
data from the captive side, e.g., on the hormonal system and reproduction (for
a summary see Lindburg 2001), contributed to basic
biological knowledge of the species and to the development of field
studies. A real metapopulationmanagement, combining in situ and ex situ programs for the global Lion-tailed
Macaque population, however, was not developed.
Discussion
The aim of this paper was to review the
development and the management history of the captive population of the
Lion-tailed Macaque in order to identify management patterns that might have
contributed to its actual poor status in terms of breeding potential. The
overall analysis of the development of the global captive population of
Lion-tailed Macaques revealed problems and negative trends. The living component of the (global)
historical population in 1980 was transferred into two larger breeding programs,
and it comprised about 350-400 individuals. Within about 30 years, it developed
towards a global population of about 500 individuals. Nearly 70% of them are part of the
European population. At least 25%
of the current global population, including the SSP population, are probably
non-reproductive. The integration
of a large proportion of the captive population into international endangered
species breeding programs evidently supported the survival of the species under
human care so far, but did not lead to a possibly sustainable global captive
population sensu Lacy (2013). Among the living populations, only the
EEP population is significantly larger now than when the program started and
showed a decent number of births in the last 10 years. According to Sliwa(2007), a “gene drop analysis” showed that the population retained a gene
diversity of 96% of the founder population. Whereas this population seems to have
the potential for further breeding and sustainability, the other populations
are not likely to survive without input from outside and new management
programs. The European population,
which constitutes the main and still productive part of the global population,
started in the 1950s. The European
population had 56 founder females and 47 founder males. Only 39.3% of these
wild caught females and 31.9% of these wild-caught males reproduced (Krebs
& Kaumanns 2002). Probably more than 100 other potential
founders in the other populations and hundreds of potentially productive
captive-born individuals could not contribute to a global reserve population
because “their” populations did not survive or were “managed” to a
non-productive status.
What are the shortcomings of the breeding
programs for the Lion-tailed Macaque? The analysis of their management history
does not provide simple answers as illustrated below.
The analysis is confronted with differences in
management policies which make it difficult to compare
their results and to identify common reasons for the problems. After a decade of population growth in
the American population, the latter was managed to shrink. In contrast to this, the European
population was managed to grow continuously. The low reproductive potential of the
current American population with its few remaining potentially fertile, though
ageing, individuals, was certainly not intended. It rather developed as a consequence of
processes triggered by an already small and demographically reduced population
with an artificially induced low effective population size. Group sizes in the SSP population became
much smaller than mean group sizes in the wild. It is evident that in these groups the
demographic structure was simple and the generational overlap low. Due to transfers of individuals between
groups, social stability may have temporarily been low. Social relationships may also have been
negatively influenced by hormonal birth control measures. The behaviour, the social competence
and the reproductive potential of individuals growing up and living under these
altered conditions were likely to be changed and negatively influenced. The resulting, possibly
behaviour-induced, variance and decrease in breeding success might have led to
a further and unwanted reduction in effective population size (see Anthony
& Blumstein 2000). Following
Carroll & Watters (2008), it is possible that the strongly modified social
and non-social environment affected the reproductive success of phenotypes and
the fitness of genotypes. The low
productivity in the shrinking SSP population in the last decade also may be
regarded as an expression of demographic and environmental stochasticity. Demographic stochasticityinvolves random fluctuations in vital rates at the individual level (for
example deviations from the mean number of offspring) and arises from the fact
that individuals are discrete entities (Brook 2008). According to Brook, small populations
are specifically vulnerable to stochastic hazards. The removal of a significant number of
Herpes B positive individuals from the SSP population, and a strong decrease in
the number of holding institutions due to “loss of interest” (Lindburg 2001) might be discussed in the role of such
hazards. Overall it seems possible
that the viability of the Lion-tailed Macaque SSP population decreased as a consequence
of a management-induced strong reduction in population size (as a reaction to a
lack of spaces) and of the resulting drastic changes in some of the life
history patterns like group size and in a number of behavioural systems. Possibly, these conditions hindered the
establishment of a sufficiently large effective population size as necessary
for the survival of a population. Anthony & Blumenstein (2000) demonstrated for a number of different
animal species how the behaviour of individuals, especially in small and
altered populations, could reduce effective population size and thus contribute
to their threatened status.
Although it was managed without putting limits
to population size, the European and specifically the EEP population also did
not develop optimally (Singh et al. 2009). The slow but steady increase in population size that occurred was
determined by births and deaths, but was also supported significantly by
imports from other populations and later by the integration of new EEP participants. The increase in population size would
have been significantly lower without input from outside. The increase was realized in spite of a
low effective population size with a contribution of only about 30 to 40% of
the potentially reproductive females to breeding. As a DEMOG (Demographic Modelling
Software) analysis (Bingaman & Ballou 1997)
revealed, this increase will continue but remain slow over the next two decades
(Kaumanns et al. 2006).
Although the EEP population of the Lion-tailed
Macaque has grown to a considerable size in comparison to other captive primate
populations (Kaumanns et al. 2008), its actual status
cannot be regarded as robust and safe against the risks described above. Under the given condition of slow
population growth, seemingly minor events like the loss of a few of the most
productive females or the exclusion of breeding groups due to institutional or
medical reasons can have serious consequences for the productivity of the
population. If effective breeding
size is low and the differences between the females in terms of reproductive
output are large and unpredictable, even a population of several hundred
individuals may not be safe against a serious loss of viability within short
periods of time. A decrease in
viability, however, may remain undetected for some time, especially when many
females are under birth control or when the reproductive output of the
individual female is not monitored continuously.
Comparing the development of the two
populations under the aspects discussed above, it seems likely that the actual status of the EEP population essentially was
supported by a management that kept population size and structure above a
critical minimal threshold (sensu Snyder et
al. 1996). Furthermore, that status
might be specifically supported by the fact that it comprised an increased
number of large groups with possibly more natural socialization conditions.
The development in both EEP and SSP
populations, however, shows that breeding Lion-tailed Macaques in captivity to
establish a self-sustaining reserve population could not be carried out
efficiently. It has not generated a safe captive status so far. It seems that under the captive
conditions realized so far for the production of one offspring Lion-tailed
Macaque, minimally two or three adult females are needed due to several females
not reproducing and long inter-birth intervals in reproducing females. Therefore, a large reserve of adult
females is required for a substantial population growth.
In wild Lion-tailed Macaque populations, there
is a slow turnover (late maturity, long birth interval, low number of infants
per female lifetime; Singh et al. 2006). Such life history patterns are difficult to handle for the manager of a
small captive population. Furthermore, in combination with much unpredictable variation in terms
of reproductive output under captive conditions, these patterns are even more
challenging. As long as the reasons
for individual differences are not known, the problem will remain pending. It is especially at this point where the
breeding programs for the Lion-tailed Macaque do not succeed. This is puzzling, since from the
establishment of the breeding programs, the status of the knowledge about the
biology of the Lion-tailed Macaque has improved continuously. Due to a large number of field studies
(Singh et al. 2009) and also many captive studies (Lindburg2001), the Lion-tailed Macaque is one of the best-studied macaque species by
now. The availability of biological knowledge therefore so far does not seem to
have contributed much to improving the status of the species, both in situ and
ex situ (Singh et al. 2006; Singh et al. 2009).
The problems influencing the development of
both captive populations, and in particular the development of the American
population, point to the need for stonger application
for the principles of adaptive management (Walters & Hilborn1978; Walters 1997). Following
these authors, conservation management with its usually poor data base and
tentative concepts requires a continuous analysis of what has been achieved so
far, thus enabling the manager to correct and improve if necessary.
It appears that a too strict and rigid
management of populations of wild animals in captivity without controlling its
effects, especially when a lack of spaces in zoos favours very small
populations, can increase the risk of inappropriate management decisions. They
may have fatal consequences for long-term survival of the population. Lacy
(2013) proposed that “instead of trusting that all forms of adaptive variation
will be maintained along with the modelled neutral genetic variation, we will
need to monitor morphological, behavioral, and
physiological variation”. He also
warned that a mere retaining of genetic diversity alone does not necessarily
ensure that all the other characteristics of the conserved populations will
also be protected adequately. Lees
& Wilcken (2009) showed that a large proportion
of zoo populations are in poor shape and are not achieving the conditions for
sustainability, a fact that should be critically discussed with reference to
the management practices used.
In conclusion, the analysis of the development
of the global captive population of the Lion-tailed Macaque and its
subpopulations indicates that management strategies as well as some of the
management tools used so far require improvements and change of perspectives. Effective population size in the
remaining living population is still low, and it is still not known why a large
proportion of the females do not reproduce successfully. These problems can be found in the
majority of captive primate populations and possibly in other mammals (Kaumanns et al. 2008). The scale and the nature of the problems speak against Lees & Wilcken’s (2009) assumption that “the scientific basis for
captive population management is sound” and “therefore, if programmes are
failing, it is likely to be either because the science is not being
appropriately translated into management recommendations or because those
recommendations are not being implemented within institutions”. It rather seems likely that the poor
status of many populations indicates serious deficits in the management
programs themselves and that there is a strong need to reassess the basic
scientific approach chosen by the zoo community for the management of captive
populations (see also Lacy 2013).
A new management approach for primates might
put more emphasis on the perspective that captive primate populations could be
regarded as a special case of fragmentation (Kaumannset al. 2008). The resulting
theoretical and practical consequences should become the basis for
conservation-oriented management concepts and husbandry systems. For the Lion-tailed Macaque, this is
specifically indicated since fragmentation and alterations of habitat and
populations are regarded as the main problems for its conservation and hence
its survival in the wild. A new
approach, therefore, should refer to conservation management as recently
propagated for and practised in threatened wild populations. An outline of such an approach is
presented below.
Management of
populations under altered conditions: General conceptual framework
With special reference to the conservation of
wild populations of animals under fragmented and altered living conditions,
recent studies and new approaches in conservation biology led to the
propagation of a conservation management which, besides dealing with
populations and their habitats as a whole, is consequently more focused on the
status and management of individuals and the phenotypes within the populations
in question (Carroll & Fox 2008). Individuals have to survive and reproduce. The phenotype is
the unit of selection. Consequently the phenotype as a whole
needs to be managed. According to Carroll & Watters (2008), “intense management of
phenotypes can enhance effective population size and thereby protect viability
and genetic variation”. The term
‘phenotype’ here refers to the total appearance of an organism resulting from
the interaction of the genotype and the environment and includes its traits on
the level of morphology, development, physiology, phenology, behaviour and
products of behaviour. The stronger
focus on the individual and its living conditions are also propagated by Lomnicki (1980), who suggested to students of population
dynamics not to look at the average individual in a population but to look for
differences between the individuals and try to find out how these differences
affect the individual’s reproduction and survival (see also Kaumanns1994). This focus evidently
requires much knowledge about patterns and mechanisms of behaviour and their
physiological and hormonal correlates on a proximate level. Individual and
phenotype-oriented management emphasizes that adaptation to rapidly changing
and altered living conditions is more likely to occur under conditions of
sufficient ‘phenotypic variability’, that is when a variety of types of
individuals and a variety of traits in which individuals differ provide a
larger spectrum of solutions to the emerging problems (Carroll & Watters
2008).
The management of captive populations of wild
animals with their sometimes extremely altered and fragmented living conditions
and resulting breeding problems, evidently needs even more focus on the
individual and its phenotype as a whole. In contrast to the management programs commonly used for zoo
populations, this requires approaches that do not mainly focus on genetic
variation and its distribution through the population. Instead, the new programs intend
integration of management of genetic variation into a complex management
concept as introduced above. It is
an accepted fact that a population can become endangered by mismanagement at
the level of genetics, for instance, inbreeding. However, it is equally ignored that a population can as well become endangered by inappropriate
management on the level of individual and social behaviour, since these
traits are also subjected to selection and influence survival of individuals
and populations. Therefore, a key
area of management would be the behaviour of individuals, its influence on the
development and viability of the population and its management with special
emphasis on the social behaviour in the case of primates (see Anthony &
Blumenstein 2000; Gosling & Sutherland 2000; Singh & Kaumanns 2005). In many cases like the Lion-tailed Macaque,
the functioning of the reproductive system is a critical aspect (Singh et al.
2006). In principle, behavioural
management aims at creating living conditions such that they facilitate the
expression of a full range of adaptive behaviours in individuals and optimize
life-history patterns of a species as in their more natural habitats (Kaumanns et al. 2008). This approach has to include much more than enrichment programs.
Altered wild habitats, and even more the
limited and altered conditions of captivity, do not allow control and
optimization of all the relevant factors for management purposes. Management programs, therefore, have to
identify and select key traits (sensu Carroll &
Watters 2008). Orientation as to
which key traits and minimal conditions have to be met for the long-term
survival of a captive population, besides others, might be developed with
reference to specific life history patterns like group size, demographic
structure of groups and populations, birth rate, etc. These patterns refer to key aspects in
an organism’s life. They are shaped
by natural selection, reflect patterns of a species’
adaptive potential and ‘act’ as ‘interface’ between individuals and
populations.
Many of
the relevant traits are probably rather conservative and inertial and act as
constraints on social interactions and mobility. Management and husbandry systems should
allow their realization as far as possible: the differences between captive conditions and wild
conditions should be kept as small as possible. Managers should start designing keeping
systems from optimal conditions, and assess how far they can reduce and alter
from there, without violating the limits of adaptive potential. If living conditions do not allow
the expression of basic social and other behavioral traits, it may lead to
stress and possibly negatively influence reproduction. In particular, suboptimal social
conditions may show effects in the short run such as failure of a female to
reproduce or to competently rear infants, or in the long run, such as high
reproductive variance among individuals. A management that provides
recommendations and living conditions that allow a population to realize
specific life history patterns (e.g., group size and composition) also
facilitates its long-term survival. This approach would include the establishment of a certain range of
variance between parameters in individuals, groups and subpopulations and thus
would contribute to the ‘production’ of a variety of individual phenotypes and
individual differences as referred above. According to Lacy (2013), “most species will need more, not less,
adaptability in the future, and populations being managed as reservoirs for
species conservation will often have to be the source of that restored
variation”.
The following section intends to use this
approach and the results of the review of the Lion-tailed Macaque management
history presented above to outline principles and recommendations for the
captive management of the Lion-tailed Macaque that may supplement the existing
management concepts.
The Lion-tailed Macaque
For the management of Lion-tailed Macaques
under captive and other altered conditions, the following traits and life
history patterns are proposed to be key traits (sensuCarroll & Watters 2008): The Lion-tailed Macaques live in groups with a
modal group size of 13–17 individuals in contiguous forests, whereas in
forest fragments the size varies from six to 53 individuals (Singh et al.
2002). Adult male to female ratio
is 1:2.11 and adult to young ratio is 1:0.84. A group may remain stable
over generations and decades. The Lion-tailed Macaque society is
’female-bonded’ and the females form the permanent core of the group. The
females remain in their natal groups whereas adult males migrate among
groups. The immigration of an adult
male into a group might result in agonistic interactions with the resident
male(s), but the adult females appear to prefer the migratory male to the
resident male in all their social interactions, including mating (Kumar et al.
2001). Adult males are highly
intolerant towards each other (Kaumanns & Singh
2012). All-male groups have not
been found (Singh et al. 2011). The
group members are largely dispersed during the day, and social interactions, as
compared with many other macaque species, are more infrequent. The social interactions between adult
females and adult males are scarce, and between adult males (if there is more
than one in the group) almost absent (Singh et al. 2011). A group has a home range of several
square kilometres, and in contiguous forests, the home ranges of several groups
overlap. Frequent intergroup encounters occur in the overlapping areas.
In the natural habitats, births are observed
almost throughout the year. However, there is a peak from January to April
(Sharma et al. 2006). In captivity, births occur almost at the same rate over
all months (Lindburg et al. 1989; Krebs & Kaumanns 2001, 2002). The female age at first birth is
about 80 months in the wild (Kumar 1987) and about 48 months in captivity (Lindburg et al. 1989; Krebs & Kaumanns2001: 65.2 months). The inter-birth
interval in the wild is about 30 months and infant survivorship is about 0.87
(Kumar 1987; Sharma et al. 2006). Adult males tend to follow females showing sexual swellings. These “consort pairs” often stay away
from the rest of the group. Adult
females and juveniles are often observed disrupting a mating pair. In the Lion-tailed Macaque, a
Multiple-Mount-to-Ejaculate (MME) system is found. The males take fewer mounts to ejaculate
when females show swellings, and during the deflated phase, the mounts hardly
ever result in ejaculation (Sharma et al. 2006). Individuals are highly dispersed during
foraging (Kumar 1987; Krishnamani & Kumar 2000;
Kumara et al. 2000).
Free-ranging Lion-tailed Macaques have a
diverse diet, including a large variety of fruits and seeds. Depending on seasonality, fruits are
selected only with a specific level of ripeness. Lion-tailed Macaques also feed on a
variety of invertebrate fauna, and sometimes even on vertebrates including
young birds, lizards, frogs and mammals to the size of the Indian Giant
Squirrel Ratufa indica. Many food items require processing,
which makes foraging time-consuming. It seems that under the ecological conditions under which Lion-tailed
Macaques live, the populations have reached the carrying capacity of their
habitats. The subpopulations
studied so far did not grow. Lion-tailed Macaques show a slow turnover with few infants per females’
lifetime, large birth intervals and low infant mortality. Lion-tailed
Macaques are almost wholly arboreal. They are generally observed at a height between 10 and 30 meters and
move horizontally through contiguous middle and upper canopy levels of the
forest. Travel distance per day
could be as much as three kilometres. In the highly fragmented patches of
rainforests at the Valparai Plateau in the Western
Ghats, the population, monitored over a period of 16 years, increased only in
two groups but remained stable in several other groups (Umapathyet al. 2011). An in-depth analysis
of population dynamics in a forest fragment showed that almost all females bred
continuously over two breeding periods, thus contributing 29 offspring with
nearly 90% survivorship, but the number of adults increased only by four and
the number of subadults remained almost the same
(Krishna et al. 2006). This brings
out several important points regarding the population dynamics in wild
Lion-tailed Macaques: most of these populations have probably already reached the
carrying capacities of their habitats; the growth rate may be near zero but
births occur every year, maintaining fairly constant age-sex ratios; most of
the deaths appear to occur at the late juvenile or subadultstage in both males and females.
In
agreement with Lindburg (1992), a key recommendation
for the captive management of the Lion-tailed Macaque, is therefore that groups comprising of
minimally 10–20 individuals with an age-sex composition close to that in
the wild should be maintained. Such
groups are therefore proposed as the most important and indispensable elements
of a captive population, since they are likely to provide the appropriate
social and especially socialization conditions for the production of adaptive
individuals. It is necessary, however, that these size and demographic
structures are prevalent in a group over as many years and generations as
possible and that the absolute number of such groups is as high as
possible. Furthermore, to initiate,
stimulate, and facilitate social dynamics, especially with reference to male-female
relationships, to the reproductive system and to male exchanges, as many
institutions as possible should keep two groups of Lion-tailed Macaques each in
adjacent enclosures (“multi-group approach”), thus allowing controlled mutual
stimulation and ‘group encounters’ (see experimental group encounters described
by Kaumanns et al. 1998; Zinneret al. 2001). Since male migration
is a frequent and important aspect of Lion-tailed Macaque social organization,
the periodic exchange of breeding males in captive groups is required not only
to avoid inbreeding, but also to stimulate social life.
It is assumed that these complex keeping
systems with their resulting multitude of social processes and problems would
provide the necessary conditions for the realization of species-specific
behaviour patterns and would support the development of different types and
traits of individuals, as is necessary, following Carroll & Watters (2008),
for a population that has to cope with the altered conditions of captivity.
It is evident that the recommended large social
groups require large, variable and flexible enclosures, which not only provide
the appropriate spatial conditions (necessary as medium for social activities
and processes), but also support the development of complex cognitive and
manipulative skills as described for Lion-tailed Macaques (Westergaard1988). To develop the required phenotypic variability at
population level, as many groups and keeping systems of this kind as possible
should be established. Only this
population as a whole is likely to produce individuals with the
behavioural and social competencies as required for the establishment of a
viable population with predictable patterns of reproduction and a high
effective size.
However, it is difficult and time-consuming to
start from a small demographically poor population to reach this status, as has
been observed in the European population. This seems to be a consequence of the
slow ‘turnover’ from one generation to the next, which determines population
dynamics in Lion-tailed Macaques. The life history patterns in the wild result in a ‘slow’ but so far
evidently adaptive ‘turnover’ and a stable population. The life history patterns in the
historical captive populations also resulted in a slow turnover, but evidently
did not lead to a population with a potential to survive. A more close comparison reveals that the
factors that lead to slow growth may differ considerably between wild and
captive populations. It seems that
in the wild, the majority of the adult females reproduce but produce few
infants per lifetime, show large birth intervals and are older at first
birth. Infant mortality is
low. In
captivity, fewer females breed. They produce many infants per lifetime, have lower birth intervals, are
younger at first birth, and experience high infant mortality. This pattern in captivity, as has
been shown above for the SSP and the EEP populations, leads to an unbalanced
population structure. It can
negatively influence genetics, demography, and social structures, with the risk
of a growing difference between population size and effective population size,
and a loss of viability. It hinders
the establishment of the breeding conditions as recommended above, thus
producing a vicious circle.
As a consequence, for the development of a
management program for Lion-tailed Macaques, and possibly other primate
species, the first critical step is to establish procedures that lead to the
breeding conditions described above. In this initial period the population
has to grow as fast and as much as possible. Generation time should be as short and
generational overlap in groups as strong as possible. It is evident that during this
period of improving a population’s productivity, birth control and other
measures to control population size can be counterproductive. Judging from the development of the EEP
population, this initial period can last for more than 20 years.
Slow growth in the captive Lion-tailed Macaque
population is a consequence of the low mean reproductive output per female, but
to a certain degree also a consequence of (necessary) management procedures,
which hinder or delay the growth of groups. The latter include the frequent (more or
less disruptive) exchange of breeding males for genetic reasons (inbreeding
avoidance, etc.), the (too) early removal of juvenile males, and the removal of
females for the establishment of new heterosexual groups. Even if these procedures are necessary
due to the limited captive conditions, they can lead to long-lasting social
imbalances and stress and therefore may result in breeding problems. More appropriate keeping systems
(multi-group approach) would help to reduce these imbalances and may facilitate
achieving social stability. In
agreement with Lindburg (1992), it is also indicated
to support the further growth of larger groups rather than taking clans of
females out to establish new groups. In continuously growing groups, the generational overlap is likely to be
higher, thus providing richer conditions for socialization. It may happen that an accidentally
male-biased reproductive output in a group over years can force the manager to
reduce group size significantly by removing these males before they start
mating with related females. In
these cases, related juvenile and subadult males
should when possible, be removed as cluster rather than individually. This provides a chance to keep
these males together for a few years, thus reducing the surplus males problem. Due to high a- priori incompatibility,
unfamiliar adult males in Lion-tailed Macaques probably cannot be kept in
unisex groups (Singh et al. 2011; Kaumanns &
Singh 2012).
Terminating the initial phase of a breeding
program for Lion-tailed Macaques and starting a second management period is
indicated when the growth rate is constant and when breeding patterns are
predictable (see also Foose et al. 1986). It is only then that population
management can consider keeping population size and structure on a more stable
level. Since under captive
conditions mortality induced by predators, food shortage and other ecological
factors are absent and therefore do not contribute to limiting population
growth, the only means to achieve this would be controlling, and possibly reducing,
the reproductive output of the females, such that the turnover rates allow only
minor population growth. Euthanasia
would be another means but is not permitted and/or accepted in many countries. In principle, birth control in
individual females has to be done such that it does not negatively affect the
social environment, socialization conditions and thus the reproductive system
at population level. To achieve
appropriate variance in reproductive output, the latter needs to be manipulated
accordingly both per individual and between individuals and groups. Groups have to remain demographically
diverse, with a rich enough spectrum of partners, within the group itself and
between groups in “multi group–setups”, as propagated above. Various means to reduce the number of
offspring include: (a) prevent fertilization directly via contraceptives, and
(b) prevent fertilization indirectly via manipulation of social
conditions. Only in groups with
more than 25 individuals could females along matrilinesbe removed to establish new groups. Removal and integration of individual females into new groups is
counterproductive since it disturbs the demographic and social patterns in a
female-bonded social system.
Evidently, many subadultand adult Lion-tailed Macaque males cannot be permanently kept in breeding
groups. In the wild, groups of
Lion-tailed Macaques usually have only one adult male, but additional male(s)
keep making attempts to enter them, since male migration is a common
phenomenon. Males may remain solitary
for some time, and hence, may face higher predation and are a part of the food
chain. Since euthanasia is often
not accepted as a management technique for ethical reasons and/or by
legislation (see euthanasia statement approved by EAZA Council on 26 September
2011), extra group management of males is inevitable. A male may be kept in a separate
enclosure but in visual contact with the group for a possible future
replacement of breeding males. A
castrated male could also be retained in the natal group over some period of
time as personal observations by WK show. Whether several castrated males can be kept in an all-male group has not
been investigated. Castration, however, should be carefully considered since a
castrated male may not be properly integrated into the group, and the
irreversible means to control productivity may turn out to be counterproductive
in the long run.
Since the function of a captive breeding
population is to provide the conditions and ‘materials’ for successful
reproduction in a species that itself depends on the behaviour of individuals
and on the quality of the breeding units as has been discussed, the (target)
size and structure of the captive population has to be defined from this end in
combination with genetic considerations. It would be against the logic of phenotype-oriented management to fix
size and structure first with reference to available spaces in zoos, only
hoping that sustainability emerges. Based on the analysis of the global historical population and the considerations
presented in this paper, it is postulated that a self-sustaining captive
population of Lion-tailed Macaques needs more than a few hundred individuals
and should comprise of several large subpopulations that have to be managed as
a metapopulation on an international level, with a
significant focus on the country of origin, India, and potential
reintroductions. A general outline
of an integrated in situ and ex situ approach for the conservation of Lion-tailed
Macaque was proposed previously (Singh et al. 2009). However, due to lack of institutional
support, an international metapopulation management
plan has not been produced. It is
in this context that the Indian zoos need to develop infrastructure and
expertise to prepare the ground for the conservation of the Lion-tailed Macaque
in the habitat country by contributing to the global captive population and
conservation activities in India, which might include reintroduction. In a recent paper, Singh et al. (2012)
elaborate the necessary conditions for successful management of captive
populations of primates in Indian zoos.
Many captive primate populations do not appear
to be in good shape and have very low chances to develop towards
sustainability. Recently emerging
views on how to deal with this and to redefine the role of zoos strongly
propagate stronger links with the conservation of wild populations. Through zoos supporting wild
populations, Conway (2011) hopes to “buy time for wild animals”. Lacy (2013) propagated achieving true
sustainability of zoo populations by much more elaborated metapopulationmanagement, including the wild population. While these approaches are appreciated, they should not hinder zoo
biologists from reconsidering captive propagation policies and management plans
that have so far lead to the poor status of populations. There is a risk that a large number of
captive populations will be of little future use for conservation (Leus et al. 2011). If the Lion-tailed Macaque can be taken as a model for the problems and
potential solutions, aspects of the captive propagation of primates emerge that
requires significant changes. Much
more focus has to be put on individuals and their behaviour in social units. The required size and demography of the
population have to be established such that the conditions for successful
breeding are realized. This is
expected to result in reduction of the difference between effective population
size and true population size. Anthony & Blumstein (2000) demonstrate that this can be an important
condition for the survival of populations under altered conditions. Manipulation of the size and structure
of captive populations has to strongly refer to these findings. In this regard, the corresponding
know-how needs to be developed.
It is obvious that most captive populations
need to be much larger than propagated so far as derived from genetic models
alone. Furthermore, living
conditions and keeping systems require improvement, especially with reference
to the available space. This
inevitably would lead to a further reduction in the number of species kept in
zoos and a much more focussed approach to their conservation. It seems that zoo biology has to develop
new approaches which include a larger spectrum of concepts of biology and
knowledge about the adaptive potential of animal species, as developed recently
in studies on populations under altered and fragmented conditions.
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