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Estimating minimum area of suitable habitat and viable population size for the northern muriqui (Brachyteles hypoxanthus)

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A population viability analysis (PVA) using the computer package VORTEX was conducted to assess the minimum viable population (MVP) of the Atlantic Forest endemic primate Brachyteles hypoxanthus. The objectives were: (1) to estimate demographic and genetic MVPs that could be used as quasi-extinction thresholds for future modeling, and (2) to estimate the minimum area of suitable habitat (MASH). The model predicted that populations of 40 and 700 individuals were necessary to achieve demographic and genetic stability, espectively. The model was more sensitive to changes in inbreeding depression, sex ratio and reproduction (percentage of breeding females). MASH estimated to contain genetically viable populations reached 11,570 ha. Muriquis have managed to persist despite severe habitat disturbance, but the results suggest that although most of the extant populations are not threatened by extinction, they are too small to be genetically viable in the long-run, and will loose most of their heterozygosity.
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Biodiversity and Conservation (2006) 15:4197–4210
Ó Springer 2006
DOI 10.1007/s10531-005-3575-1
-1
Estimating minimum area of suitable habitat
and viable population size for the northern muriqui
(Brachyteles hypoxanthus)
DANIEL BRITO1,3,* and CARLOS EDUARDO V. GRELLE2
1Programa de Po´s-Graduac¸a˜o em Ecologia, Conservac¸a˜o e Manejo de Vida Selvagem (ECMVS),
Instituto de Cieˆncias Biolo´gicas, Universidade Federal de Minas Gerais, Avenida Antoˆnio Carlos
6627, Belo Horizonte, MG 31270-901, Brasil; 2Laborato´rio de Vertebrados, Departamento de Eco-
logia, Instituto de Biologia, CCS, Universidade Federal do Rio de Janeiro, CP 68020, Ilha do Funda˜o,
Rio de Janeiro, RJ 21941-590, Brasil; 3Present address: Rua Andrade Neves 93/802, Rio de Janeiro,
RJ 20510-230, Brasil; *Author for correspondence (e-mail: brito.dan@gmail.com)
Received 28 May 2004; accepted in revised form 27 September 2005
Key words: Atlantic Forest, Brachyteles, Extinction, Minimum area of suitable habitat (MASH),
Minimum viable population (MVP), Population viability analysis (PVA), Quasi-extinction,
VORTEX
Abstract. A population viability analysis (PVA) using the computer package VORTEX was con-
ducted to assess the minimum viable population (MVP) of the Atlantic Forest endemic primate
Brachyteles hypoxanthus. The objectives were: (1) to estimate demographic and genetic MVPs that
could be used as quasi-extinction thresholds for future modeling, and (2) to estimate the minimum
area of suitable habitat (MASH). The model predicted that populations of 40 and 700 individuals
were necessary to achieve demographic and genetic stability, respectively. The model was more
sensitive to changes in inbreeding depression, sex ratio and reproduction (percentage of breeding
females). MASH estimated to contain genetically viable populations reached 11,570 ha. Muriquis
have managed to persist despite severe habitat disturbance, but the results suggest that although
most of the extant populations are not threatened by extinction, they are too small to be genetically
viable in the long-run, and will loose most of their heterozygosity.
Introduction
Conservationists attach much importance to the knowledge of population size
because small populations are more likely to go extinct than large ones (Pimm
et al. 1988; Caughley and Gunn 1996). Therefore, estimating minimum viable
population (MVP) is a fundamental cornerstone of conservation biology
(Shaffer 1981; Belovsky 1987). Franklin (1980) proposed that effective pop-
ulation size (Ne) should not be less than 50 to ensure short-term survival, and
a Ne of 500 would be sufficient to ensure long-term persistence. Taken
together, MVPs for both short- and long-term survival have resulted in the
so-called 50/500 rule, which has been widely implemented as a management
goal for a large number of threatened species (Lande and Barrowclough
1987). However, recent research suggests that these population sizes are likely
to underestimate MVP size for survival for several reasons, and MVP may be

4198
considerably larger than 500 (Lande 1995; Lynch and Lande 1998; Reed and
Bryant 2000).
Protecting biodiversity requires the protection of sustaining populations of
all species into the foreseeable future, and protecting species requires sufficient
habitat to support MVPs over time (Allen et al. 2001). For instance, under
simple mammal-habitat association models, the total area occupied by 15 or
more mammal species was 30,448 ha, but it decreased to only 7820 ha under
model conditions incorporating minimal critical areas to support MVPs (Allen
et al. 2001). This reflects the fragmented condition of many landscapes, where
most patches are too small to support viable populations. The Atlantic Forest
is one of the most endangered ecosystems of the world (Fonseca 1985; Myers
et al. 2000), and recent studies on the effects of forest fragmentation on
Atlantic Forest mammal communities indicate that only large forest reserves
(>20,000 ha) can sustain structured communities with viable populations
(Chiarello 2000). However, only about 20% of all protected areas remaining in
the Atlantic Forest are equal to or larger than this size (Chiarello 2000). Even
for a small species in this biome, the long-furred woolly mouse opossum
Micoureus paraguayanus (previously M. demerare and M. travassosi, see Voss
and Jansa 2003), it was estimated that a minimum size of 3600 ha is necessary
to maintain viable populations (Brito and Grelle 2004). Due to habitat
requirements, species typically show a patchy distribution even in large areas of
continuous habitat (Lawton and Woodroffe 1991). This means that for many
blocks of forest, only a portion of the forest will offer suitable habitat.
Therefore, it is also important to consider the minimum area of suitable habitat
(MASH) necessary for population persistence.
Two decades ago, fewer than 500 muriquis were reported from just 11 iso-
lated forests (Mittermeier et al. 1987). Over the past years, additional popu-
lations have been reported, nearly doubling both the number of localities and
the total estimated population size (1158 individuals) (Strier and Fonseca 1996/
1997). Traditionally, muriquis have been classified as only one species,
B. arachnoides. However, due to recent morphological and genetic findings, the
taxonomic status of muriquis went under revision and northern and southern
populations have been divided into separate species: B. hypoxanthus and
B. arachnoides (Coimbra-Filho et al. 1993; Rylands et al. 1995; Brito 2004).
B. hypoxanthus is one of the most endangered primates surviving in what
remains of the Atlantic Forest, being classified as critically endangered by
IUCN red list of threatened species (Hilton-Taylor 2000), and is also listed as
one of the world’s top 25 most endangered primates (Konstant et al. 2002).
The objectives of the present study are: (1) to estimate MVPs for the
northern muriqui Brachyteles hypoxanthus; (2) to estimate critical population
sizes that could be used as quasi-extinction thresholds for future population
modeling; and (3) to estimate the minimum area of suitable habitat (MASH)
needed to maintain such populations.

4199
Materials and methods
Natural history of Brachyteles hypoxanthus
The muriquis Brachyteles are the largest Neotropical monkeys, weighting up to
12–15 kg, found in mature evergreen to deciduous lowland Atlantic Forest
(Aguirre 1971; Emmons and Feer 1997). B. hypoxanthus is diurnal and arbo-
real (Aguirre 1971; Emmons and Feer 1997), but may descend to the ground
when in need to cross gaps in the canopy (Dib et al. 1997). It feeds chiefly on
fruit, flower and leaves, being able to rely on bark and bamboo as well (Aguirre
1971; Milton 1984; Strier 1991a; Emmons and Feer 1997). In the wild, males
reach sexual maturity at about 7 years, and females at an average of 9 years
(Rylands et al. 1998). Females give birth to one young at a time and show an
interbirth interval of 3 years (Rylands et al. 1998) (see Appendix A). Muriquis
live in large groups comprised of more than 50 individuals (Strier 1993/1994).
Males are philopatric whereas females generally disperse into other groups as
they reach adolescence at about 5–7 years of age (Strier 1990, b; Printes and
Strier 1999; Strier and Ziegler 2000).
PVA model
VORTEX (version 8.21) is a PVA software package that models the impact of
deterministic forces and stochastic events on wildlife population dynamics
(Miller and Lacy 1999). This package is one of the most often used for PVA
focusing endangered populations, including in workshops with officers from
conservation and land management agencies (Lindenmayer et al. 1995). A
detailed description of the package and its features is given in Lacy (1993,
2000) and Miller and Lacy (1999).
Scenarios and sensitivity analysis
The dynamics of single isolated populations of 10, 20, 30, 40, 50, 100, 200, 300,
400, 500, 600 and 700 B. hypoxanthus were simulated. Five hundred iterations
were run for each scenario and a time frame of 1000 years has been used.
Demographic parameters used as input for the model, were based on previously
published data on B. hypoxanthus (Strier 1991b, 1993/1994, 2000; Rylands et al.
1998), and a summary of the data set is provided in the Appendix A.
Sensitivity analysis measures the extent of change in the modeled population
output values due to a known change in assumptions. It identifies those
assumptions that are important to accurately estimate, those to which the model
is particularly sensitive, and those which are less influential (McCarthy et al.
1995). Sensitivity analysis provides an indication of the impact that errors in
assumptions, or real changes due to management or threats, could have on the

4200
outcome. Sensitivity analysis will be run for the two population sizes identified
as quasi-extinction thresholds for demographic and genetic modeling of B.
hypoxanthus populations. The significance of the difference in output between
the basic scenario and changed models is tested using a Students two-tailed
t-test (Zar 1996). The model was examined for sensitivity to variation in mor-
tality rate, sex ratio, percentage of reproductive females and inbreeding
depression. Sensitivity to mortality was examined by increasing mortality rate
by 5, 10 and 20% (Rylands et al. 1998). Scenarios evaluating sex ratio sensitivity
were run using values of 0.500 and 0.650 males/females (Rylands et al. 1998).
Regarding percentage of reproductive females, sensitivity analysis was run with
scenarios of 20 and 33% of females reproducing at any given year (Rylands
et al. 1998). The effect of inbreeding was examined by introducing inbreed-
ing depression to the scenarios. As the actual impact of inbreeding on
B. hypoxanthus populations is unknown, the standard lethal equivalent median
value for juvenile mammal survival of 1.57 per haploid genome was used (Ralls
et al. 1988). As VORTEX only models inbreeding impact on juvenile survival,
the simulated effect of inbreeding is probably conservative (Lacy 1993).
Results
Analysis of simulation results
Data derived from the computer simulation analysis using VORTEX were: (1)
deterministic growth rate (k); (2) population growth rate (r) (±1SD); (3)
probability of population extinction (±1SE); (4) mean time to extinction
(±1SD); (5) mean population size (±1SD); and (6) decline in genetic variability,
expressed as the expected heterozygosity or gene diversity (He). The probability
of extinction is the number of simulations that went extinct divided by the total
number of simulations (Ballou 1992). Extinct populations were not included in
calculations of mean population growth, population size or levels of He. A
population is considered as demographic viable if it has a 99% probability of
persistence for 1000 years (Shaffer 1981), and genetically viable when popu-
lations had a 10% or lower decrease in He (Foose et al. 1986; Foose 1993).
Such a long time frame is considered appropriate for species with long
generation times (Armbruster and Lande 1999), such as B. hypoxanthus
($: 19.57 years; #: 17.87 years).
Minimum viable population sizes and quasi-extinction thresholds
Typically, in populations with fewer than 20 animals, demographic stochas-
ticity may lead to extinction (Possingham 1996). At smaller population sizes,
increased demographic fluctuations, reflected by the values for SD (r),
depressed population growth and led to substantial probabilities of extinction
(Table 1). There was a reduced likelihood of extinction among larger

4201
populations of B. hypoxanthus, and more gene diversity was conserved in such
populations than in smaller ones (Table 1). Extinctions occurred among small
isolated populations of B. hypoxanthus even when no inbreeding depression
was incorporated in the analyses (Table 1). Demographic stochasticity alone
jeopardized population stability in these scenarios. Given this, populations of
40 or more B. hypoxanthus might be necessary to achieve more than 99%
probability of demographic persistence over 1000 years (Table 1). However,
there was a significant (>10%) loss of genetic variability from populations of
this size, and only populations with about 700 animals might be genetically
stable during a 1000 year period (Table 1). Therefore, a population size of 40
individuals should be set as a quasi-extinction threshold for demographic
analysis, whereas the quasi-extinction threshold taking into account genetic
modeling should be set at 700 animals.
Minimum area of suitable habitat
Taking into account the mean density of 0.0605±0.0889 individuals/ha esti-
mated for B. hypoxanthus (Strier and Fonseca 1996/1997), it is possible to
estimate that demographically and genetically MVPs of B. hypoxanthus would
need MASHs about 661 and 11,570 ha, respectively. Although 661 and
11,570 ha are recommended as MASHs for the maintenance of viable popu-
lations of B. hypoxanthus, forest remnants might be much larger than the
estimated MASHs due to seasonal variations in habitat quality and habitat
heterogeneity. Besides that, many factors that may play an important role in
promoting extinctions, such as catastrophes, hunting, edge effects and meta-
population structure, have not been incorporated into this analysis (Mace and
Lande 1991).
Sensitivity analysis
Inbreeding scenarios resulted in depressed r and population size, but an in-
crease in He for the population threshold size of 40, and depressed population
size and increased He for populations of 700 individuals (Table 2). The basic
scenario modeled populations with female-biased sex ratio (0.356). Equal sex
ratio scenarios (0.500) depressed r and population size, and increased He for
both population threshold sizes (40 and 700) (Table 2). Male-biased sex ratios
(0.650) also increased extinction probability for populations of 40 animals
(Table 2). The scenario with 20% of females breeding resulted in decreased r
and final population sizes, and increased He (Table 2). The scenario with
greater numbers of reproductive females (33%), on the other way, produced
increased r and population sizes, but decreased He (Table 2). Scenarios eval-
uating mortality rates showed no significant results for most of the output

4202
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4203
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4204
parameters with the exception of a decrease in final population size with a 10%
increase in the mortality rate for the population size of 40 (Table 2).
Discussion
Inbreeding depression critically influences the persistence of small populations
(Mills and Smouse 1994; Bijlsma et al. 2000; Hedrick and Kalinowski 2000).
Under some circumstances, however, inbreeding will tend to purge populations
of enough deleterious recessive mutations to reduce inbreeding depression
(Byers and Waller 1999; Hedrick and Kalinowski 2000). Even if purging is
reasonably effective, it has recently been shown that its effectiveness is envi-
ronment dependent and restricted to the environment in which the purging
occurred (Bijlsma et al. 1999). Changing and deteriorating environments can
evoke previously concealed genetic load to become expressed, resulting in
increased inbreeding depression in these situations. Purging thus, possibly may
be effective in mitigating the immediate fitness effects of inbreeding, but might
not be effective at all in the long run (Bijlsma et al. 1999).
Preliminary genetic studies on muriquis revealed some of the highest levels of
polymorphism and heterozygosity known for any primate (Pope 1998). The
high levels of genetic heterozygosity still found today may persist because
muriqui population sizes declined rapidly relative to their generation length
(Strier 1997; Pope 1998), and may be one of the factors contributing to the
apparent ability of at least one isolated population at Estac¸a˜o Biolo´gica de
Caratinga (Caratinga Biological Station) to avoid the deleterious effects of
inbreeding depression (Strier 1993/1994). Recent PVAs using VORTEX found
surprisingly low extinction probabilities for Caratinga’s population (90 indi-
viduals) over the next 100 years (5.3 generations), with no evidence of delete-
rious inbreeding effects (Strier 1993/1994; Rylands et al. 1998). Comparing the
results of the modeled population size of 100 individuals for the present study,
we observed a He of 0.932 for a time period of 100 years (5.3 generations).
However, estimated He for the time period of 1000 years (53 generations) was
only 0.527. Such results are in accordance with the statements that genetic
effects would be felt only after a longer time period (45–50 generations)
(Gilligan et al. 1997), and that longer time frames should be used to model
species with long generation times (Armbruster et al. 1999). Therefore, results
suggest that Caratinga’s population is viable in 100 years, but it is not genet-
ically viable in a longer time frame.
Any deviation of sex ratio from equality increases inbreeding. Therefore, the
conservation of more genetic diversity under equal sex ratio scenarios may be
the result of an increase in Ne (Wedekind 2002). Male-biased sex ratio scenarios
reduced Ne and increased inbreeding. Therefore, the conservation of genetic
diversity on male-biased sex ratio scenarios may be the result of purging. An
optimal sex ratio manipulation with respect to the genetic quality of a popu-
lation means sending it first through a genetic bottleneck to achieve increased

4205
Ne, and hence decreased rates of inbreeding, in the long run (Wedekind 2002).
Female-biased sex ratios facilitate population expansion while male-biased sex
ratios increase the probability of extinction (Gabriel et al. 1991), and the
results presented here agree with such statement (Table 2). At high population
densities, local resource competition should favor the production of dispersing
daughters over philopatric sons. In contrast, at the low population densities
that prevail in the larger undisturbed forests, relaxation of local resource
competition should reduce the benefits of producing daughters, and even favor
the production of philopatric sons (Strier 2000).
The scenario with smaller number of breeding females would increase Ne,
since sex ratio is female-biased (0.3560), and consequently result in an increase
in He. More breeding females (33%) benefit demographic parameters, whereas
less breeding females benefit genetic diversity for both modeled population
sizes of B. hypoxanthus (Table 2).
In order to maintain and improve muriqui’s genetic diversity it is of para-
mount importance the increase of population sizes, and management options
to achieve this goal should deal with: (1) habitat conservation and restoration.
The Atlantic Forest has a long history of habitat destruction and degradation
(Dean 1996), therefore the preservation of forest remnants and the establish-
ment of programs dealing with habitat restoration, recovering forest habitat
for B. hypoxanthus would greatly benefit the persistence and genetic health of
muriqui’s populations. Adequate management of existing habitat, the creation
of new protected areas (both private and public) and the restoration of
degraded habitat are goals of strategic importance. (2) Supplementation of
existing populations through translocation. There are several small popula-
tions inhabiting reserves and protected areas that would support a larger
number of muriquis. The translocation of new individuals for these areas
would result in demographic and genetic benefits for the local populations.
Reserves with large and growing populations, which are already near their
carrying capacity, could be the source for individuals for the genetic
reinforcement of the smaller populations, rescuing them from genetic impov-
erishment. For example, Rio Doce State Park has a small population of mu-
riquis and would support a much larger population whereas Caratinga
Biological Station has a growing population of B. hypoxanthus, viable within
the next 100 years, being near its carrying capacity. Therefore, Caratinga could
be used as a source of individuals for translocation to the Rio Doce popula-
tion. A detailed monitoring program must be established in order to evaluate
the advances and success of translocation schemes. (3) Establishment of cor-
ridors. Due to the high rate of habitat destruction and fragmentation in the
Atlantic Forest, insularization and isolation may be a serious threat to the
persistence and the genetic health of wildlife populations (e.g. Brito and Grelle
2004; Brito and Fonseca in press). Improving connectivity among populations
would help mitigating genetic deterioration by allowing dispersing individuals,
sources of new genetic material, to reach other populations and consequently
improving genetic diversity in the populations which are receiving them. There

4206
is a management plan to improve habitat connectivity in the Atlantic Forest
with the creation of three regional ecological corridors, and one of them, the
Central Atlantic Forest Corridor, would benefit B. hypoxanthus preservation.
The creation of corridors on a local spatial scale should be a complementary
approach for the regional corridor network.
Fewer than 500 B. hypoxanthus are thought to survive today, distributed in
small populations (Strier and Fonseca 1996/1997; Strier et al. 2002). Although
new populations have been discovered in recent years (e.g. Hirsch et al. 2002),
the 890 ha forest at Estac¸a˜o Biolo´gica de Caratinga is still the largest popu-
lation known (171 individuals) and the only one considered to be viable for the
next 100 years (Rylands et al. 1998; Strier 2000). However, the results observed
here suggest that Caratinga’s muriqui population will suffer from loss of
genetic diversity in a longer time frame (1000 years). Muriquis have managed
to persist, despite severe habitat disturbance, in part because of their adaptable
way of life, which includes their ability to exploit secondary as well as primary
forest (Fonseca 1986; Strier 1987). However, our results suggest that even if all
234 B. hypoxanthus individuals (Strier and Fonseca 1996/1997) were grouped
into one population, it would not be genetically viable in the long run (0.7261
He in 1000 years, see Table 1). Therefore, the high levels of genetic polymor-
phism and heterozygosity of muriqui populations (Pope 1998) may quickly
deteriorate in the next centuries or tens of generations if management actions
are not implemented in order to help mitigate or reverse the trend in loss of
heterozygosity.
Acknowledgements
We thank the support from the U.S. Fish and Wildlife Service and Fundac¸a˜o
Biodiversitas. Conservation International Brasil provided funds. Daniel Brito
was supported by a Ph.D. scholarship from FAPEMIG.
Appendix A
B. hypoxanthus demographic data used as input values to VORTEX
VORTEX 8.21 – simulation of genetic and demographic stochasticity
1 population(s) simulated for 1000 years, 500 iterations.
Extinction is defined as no animals of one or both sexes.
No inbreeding depression.
First age of reproduction for females: 9 for males: 7.
Maximum breeding age (senescence): 35.
Sex ratio at birth (percent males): 35.600000.
Polygynous mating;
100.00% of adult males in the breeding pool.

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