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Dispersal among male ring-tailed lemurs (Lemur catta) on St. Catherines Island

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American Journal of Primatology 70:650–660 (2008)
RESEARCH ARTICLE
Dispersal Among Male Ring-Tailed Lemurs (Lemur catta)
on St. Catherines Island
J. A. PARGA1 AND R. G. LESSNAU2,3
1
Department of Social Sciences, University of Toronto at Scarborough, Scarborough, Ontario, Canada
2
St. Catherines Island Foundation Center, Midway, Georgia
3
Department of Biology, Armstrong Atlantic State University, Savannah, Georgia
Male dispersal patterns were analyzed across a nine-year period in a population of ring-tailed lemurs
(Lemur catta) on St. Catherines Island (SCI), USA, to evaluate two ultimate explanations for
male dispersal: inbreeding avoidance and intrasexual mating competition. As part of this analysis,
we also compared patterns of dispersal at this site with data from wild populations. Overall, we
found that patterns of male intertroop movement on SCI are similar to the wild with respect to the
frequency and seasonality of male transfer. In Madagascar, males move between groups every 3.1–3.5
years [Sussman, International Journal of Primatol 13:395–413, 1992; Koyama et al., Primates
43:291–314, 2002] as compared with every 3.2 years on SCI. The majority of transfers on SCI occurred
during the birth season, as occurs at one site in Madagascar, Berenty [Budnitz & Dainis, Lemur biology.
New York: Plenum Press, p 219–235, 1975; Jones, Folia Primatologica 40:145–160, 1983].
One difference is that males perform natal transfers 1–2 years earlier on SCI than in the wild, which
may be related to food provisioning on SCI. Males never transferred back into their natal troops,
which is remarkable given the small number of groups on SCI. Although this pattern of movement
can indicate inbreeding avoidance by males, the fact that male troop tenure was in many cases long
enough to overlap with the sexual maturation of potential daughters did not support the inbreeding
avoidance hypothesis for male secondary dispersal. Instead, the intrasexual competition hypothesis
was strongly supported, because males were significantly more likely to transfer into groups
having fewer adult males and a more favorable sex ratio than their pretransfer groups.
Males therefore appear to be bypassing groups in which they would experience a greater degree
of intrasexual mating competition during the breeding season. Am. J. Primatol. 70:650–660, 2008.
c
2008 Wiley-Liss, Inc.
Key words: male dispersal; intertroop transfer; Lemur catta; inbreeding avoidance
INTRODUCTION
Dispersal behavior can help maintain genetic
variation within populations by causing gene flow
[Howard, 1960; Lindburg, 1969]. Several proximate
forces can drive dispersal, including competition for
resources [Waser, 1985] or increased mating opportunities for individuals who disperse [Dobson, 1982].
Inbreeding avoidance is one commonly noted function of dispersal [Clutton-Brock, 1989; Packer, 1979],
although whether dispersal is a specific adaptation to
protect against inbreeding depression is debatable
[Dobson & Jones, 1985; Moore & Ali, 1984, 1985;
Packer, 1985; Pusey, 1987].
Among mammals, male-biased dispersal is more
common than female-biased dispersal [Greenwood,
1980, 1983], and the same generally holds true for
primates [Pusey & Packer, 1987; Pusey, 1992]. When
primate males disperse, transfer decisions can often
be influenced by mating opportunities and by the
r 2008 Wiley-Liss, Inc.
intensity of male–male competition. Males frequently
transfer into groups due to the presence of cycling
females [e.g., mangabeys, Lophocebus albigena: Olupot and Waser, 2001; baboons, Papio hamadryas:
Packer, 1979; Manzolillo, 1986; langurs, Presbytis
entellus: Borries, 2000], or transfer into groups having
more favorable sex ratios or fewer males than in their
previous group of residence [e.g., white-faced capuContract grant sponsors: University of Texas at Austin; US
National Science Foundation; Ford Foundation.
Correspondence to: J. A. Parga, Department of Social Sciences,
University of Toronto at Scarborough, 1265 Military Trail,
Scarborough, Ont., Canada M1C 1A4.
E-mail: j.parga@utoronto.ca
Received 26 August 2007; revised 15 February 2008; revision
accepted 26 February 2008
DOI 10.1002/ajp.20542
Published online 13 May 2008 in Wiley InterScience (www.
interscience.wiley.com).
Male Dispersal in Lemur catta / 651
chin, Cebus capucinus: Jack & Fedigan, 2004b; rhesus
macaque, Macaca mulatta: Drickamer & Vessey,
1973; baboon, P. hamadryas: Alberts & Altmann,
1995; Henzi et al., 1998]. A recent review by Jack
[2003] found much evidence among primates that
male secondary, or non-natal, dispersal is driven by
intrasexual competition, whereas there is less support
for inbreeding avoidance as an explanation for
secondary male dispersal.
This article analyzes patterns of male dispersal
in a group-living prosimian primate across a
nine-year period to investigate two frequently suggested ultimate explanations for male dispersal:
inbreeding avoidance and intrasexual mating
competition [Jack, 2003]. If non-natal male dispersal
functions primarily in inbreeding avoidance, males
would be expected to disperse from a social group
before potential daughters become reproductively
mature and would not be expected to transfer back to
their natal groups after leaving. Conversely, we
evaluated the intrasexual mating competition hypothesis for male non-natal dispersal by specifically
testing the following variables for their effects on
patterns of male intertroop movement: the number
of adult females per group, the number of adult
males per group, and group sex ratio. If the
intrasexual mating competition hypothesis for male
secondary dispersal is to be supported, males should
move to groups having greater numbers of females,
fewer males, or a more favorable sex ratio (fewer
males per female) than their previous group of
residence. Because our study population is a nonendemic colony of free-ranging ring-tailed lemurs
(Lemur catta) maintained on St. Catherines Island
(SCI), USA, we first compared male intertroop
movement patterns at this location to data on wild
individuals of the species.
In the wild, L. catta groups have approximately
equal numbers of males and females, and dispersal is
typically performed by males [Budnitz & Dainis,
1975; Gould, 1994, 1997, 2006a; Jolly, 1966; Jones,
1983; Koyama et al., 2002; Sauther, 1991; Sauther
et al., 1999; Sussman, 1991, 1992]. Male dispersal in
this species does not appear to be the result of
‘‘eviction’’ due to intragroup aggression, but instead
appears to be voluntary [Gould, 2006a; Sussman,
1991]. Previous work has shown that the lemurs on
SCI exhibit species-typical social [Keith-Lucas et al.,
1999] and reproductive behavior [Parga, 2003; Parga
et al., 2006], but no study has previously analyzed
male dispersal patterns at this site. In this study, we
considered whether male intertroop movement on
SCI is similar to male transfer in the wild with
respect to: (1) age at natal dispersal, (2) frequency of
male transfer, (3) seasonality of dispersal, and (4) the
occurrence of single-male vs. group transfers. We
then used these data to evaluate the inbreeding
avoidance and intrasexual competition hypotheses
for male dispersal.
MATERIALS AND METHODS
Definitions
In this article, an animals’ dispersal behavior is
defined as, ‘‘...movements away from its own (or
group) home range into another area’’ [Bekoff, 1977;
p 715]. Whereas Bekoff’s [1977] definition applies
to adults, we apply the term regardless of age,
and use dispersal to describe individuals who
emigrate from natal and non-natal groups. Dispersal
events were those in which males stayed in their new
groups for at least one month or more before
transferring again. Such movements were consistently recorded across the study. Short-term male
extra-troop ‘‘visits’’ (lasting from less than a day
to a week in length) were not considered dispersal
events due to their short duration and the fact that
males returned to the group from which they came.
Visits were not consistently recorded during the
study, and were not included in the present analyses.
Incidentally, no male stayed in a new group for more
than one week but less than one month [Lessnau,
unpublished data].
Study Site and Study Animals
SCI is a largely forested barrier island off the
coast of Georgia, USA [Thomas et al., 1978]. A colony
of L. catta was started at this site by the Wildlife
Conservation Society (WCS) with the release of a
founder group of six lemurs in 1985 [Keith-Lucas
et al., 1999]. Although most lemurs in the SCI
population are descendants of the founder population, several unrelated males have been added
throughout the years to increase genetic diversity
in the population. This colony was deemed particularly apt for a study of dispersal because all adults
wear uniquely colored Telonics radio collars (Mesa,
AZ) and can therefore be located via radio-telemetry.
Also, because the colony is on an island, animals are
unable to transfer out of the research area, a
frequent difficulty in wild studies of dispersal.
L. catta on SCI forage on naturally occurring
vegetation, show group ranging behavior, and have
established home range areas [Dierenfeld &
McCann, 1999; Keith-Lucas et al., 1999]. The lemurs
on SCI show breeding seasonality [Jolly, 1966];
however, due to photoperiodic control [Evans &
Goy, 1968; Rasmussen, 1985; Van Horn, 1975; Van
Horn & Eaton, 1979], reproduction is shifted
approximately 6 months from Madagascar [Parga &
Lessnau, 2005]. Each lemur group is provisioned
once daily with food (monkey chow, fresh fruits, and/
or vegetables) and water at heated shelter sites that
the lemurs are able to enter and exit freely. The
composition of each group per study year is shown in
Table I.
Of the males that have resided in the SCI colony
(n 5 87), 70 were born into the colony, and 17 were
Am. J. Primatol.
652 / Parga and Lessnau
born at other institutions and were released into the
island population. At its peak size, the colony was
composed of four distinct lemur groups [Parga &
Lessnau, 2005]. One of these groups was relocated in
October 2002 to a zoo, leaving three troops in the
island population. Because relatedness in the population is estimated to be fairly high, colony management occasionally removes individuals to reduce
inbreeding. Records of all births and deaths since
the colony’s start in 1985 allow for determination of
matrilineal relatedness among individuals. In 1997,
R.G.L. began keeping daily records on the composition of all lemur groups (including data on male
intertroop movement). These records were used in
TABLE I. Group Composition in October of Each
Year, Showing M:F Sex Ratio, Including All Natal
Females and Non-Natal Males Two Years of Age and
Older
Year
Group
] males:
] females
1997
1
2
3
1
2
3
1
2
3
1
2
3
4
1
2
3
4
3:4
1:3
5:4
2:5
3:3
3:5
1:6
2:4
3:6
4:5
1:6
3:8
1:4
4:5
4:7
4:6
1:4
Year
Group
] males:
] females
2002
1
2
3
4
2
3
4
2
3
4
2
3
4
5
3:7
4:6
4:6
3:4
4:5
2:8
2:4
2:5
2:5
4:8
2:7
2:6
1:4
2:3
the present analysis along with behavioral observations conducted by J. A. P. across five mating seasons
between 2000 and 2004.
Data Analysis
Analyses included all male dispersal events
between August 1997 and July 2005. Only males
born in 2003 and earlier were included in the
calculation of mean male age at natal dispersal.
When comparing the number of males within (and
the group sex ratios of) pre- and post-transfer
groups, the dispersing male was excluded from both
groups. The following non-parametric tests were
employed: binomial, w2 goodness of fit, Kolmogorov–Smirnov, and Wilcoxon signed-rank sum. All tests
were two-tailed, and the level of significance was set
at 0.05. All means are reported with the standard
error of the mean (SEM). Statistical tests were
performed using Statistica, version 5.5 (Stat Soft
Inc., 1999, Tulsa, OK).
RESULTS
1998
1999
2000
2001
2003
2004
2005
Fig. 1. Male age at natal dispersal (n 5 17).
Am. J. Primatol.
Natal Dispersal, Frequency of Transfer, and
Group Tenure Duration
We recorded a total of 30 transfer events.
Approximately half of these (n 5 17) were instances
of natal dispersal (Table II). Males transferred out of
their natal groups between 1.6 and 3 years of age,
with a mean age at natal transfer of 2.270.1 years
(Fig. 1). The majority of males (88.2%) left their
natal groups before reaching 3 years of age. All
remaining males transferred out of their natal group
shortly after reaching age 3. Only a single male
remained in his natal group beyond age 3, but he was
removed from the colony for management purposes
at 3.6 years. Adult males (age 2 years and older,
n 5 9) transferred between non-natal groups approximately every 3.2 years. Group tenure duration
1
3
3
2
2
2
2
4
4
Rangingb
3
Rangingb
Rangingb
2
2
3
4
Seasonality of Male Dispersal
–
Unknowna
No
No
–
Yes
Yes
Yes
Yes
No
No
No
No
Yes
Yes
No
No
–
Unknowna
No
Yes
–
Yes
Yes
Yes
Yes
Yes
Yes
No
Yes
Yes
Yes
Yes
No
3
2
2
3
3
3
3
3
3
4
2
3
4
4
4
2
2
A peak in both types of male dispersal (natal and
non-natal) occurred between the months of March
and June, during which time 80% of all transfers
took place (Fig. 2). This peak in male dispersal
coincides with the peak in births on SCI [Parga &
Lessnau, 2005]. Only three male transfers occurred
during the breeding season: two in November and
one in January (Fig. 2). The two November transfers
deserve special mention, as they were facilitated by
management intervention in group dynamics. Following an aggressive interaction over an estrous
female, two resident adult males of one group
became injured and were removed from the group
by management and placed within the shelter that
serves as the location of daily food provisioning. The
injured males were not allowed to free-range with
the group for several days. Within 2 days of the
captivity of these injured males, two young males
(aged 1 and 2 years) immigrated from a neighboring
group, and remained in this group for the duration of
the breeding season.
Not recorded in WCS records.
These males transferred to a part of the island where no free-ranging lemur groups reside.
b
a
02-May-2000
01-Aug-1997
08-Apr-2001
05-Apr-2001
02-Mar-2000
24-Jun-2001
24-Jun-2001
01-Mar-2002
01-Mar-2002
05-Apr-2003
05-Nov-2003
05-May-2003
05-Apr-2003
31-Mar-2005
31-Mar-2005
05-Nov-2003
02-Mar-2004
EK
BY
MN
BR
JH
RY
CH
DA
LE
CL
CP
WD
RI
TD
GA
MX
FZ
2.1
2.3
2.1
3.0
2.8
2.3
1.9
1.9
1.9
3.0
2.6
2.1
1.9
2.0
2.0
1.6
1.8
0
Unknowna
1
1
0
1
1
1
1
1
1
1
1
1
1
1
2
None
Unknowna
KL
Subadult male
None
CH
RY
LE
DA
RI
MX
BY
CL
GA
TD
CP
BR, ED
Do Males Disperse Alone or Together?
Date of transfer
Age at 1st
] of individuals with whom Identity of male
transfer (yrs)
this male transferred
transfer partner(s)
between non-natal transfers was highly variable
(range: 0.1–5.8 years; n 5 9; Table III).
Male
TABLE II. List of Natal Male Transfers
Was the transfer partner Was the transfer partner
a cohort member?
a natal male?
Group of
origin
Group transferred
into
Male Dispersal in Lemur catta / 653
Males that ‘‘transferred together’’ to a new
group traveled to their new group on the same day in
pairs or as a triplet (Tables II and III). Whether or
not males dispersed alone or with other males was
known for 16 of the 17 natal male transfers
(Table II). In natal dispersal events, males were
significantly more likely to transfer with 1–2 other
males than alone (binomial test: n 5 16, x 5 2,
P 5 0.0018). In particular, natal males were more
likely to disperse with one transfer partner rather
than disperse alone or with two other males (goodness of fit: w2 5 16.63, df 5 2, Po0.0003; Fig. 3). In
contrast, non-natal transfers were no more likely to
involve groups of males than lone males (binomial
test: n 5 13, x 5 5, P 5 0.157, NS), and such males
were equally likely to disperse alone, or with one or
two other males (goodness of fit: w2 5 2.00, df 5 2,
Po0.368, NS; Table III). Male age was not the
driving force for these trends, because age did not
significantly affect whether males transferred alone
or with other males (Kolmogorov–Smirnov: n1 5 7,
n2 5 22, P40.10, NS).
Next, we considered the relatedness of transfer
partners. Natal males transferred with a same-aged
birth cohort member in 38% of cases, and with an
older or younger matrilineally related male in 69% of
natal transfers (Table II). In all other instances,
natal males transferred with older males whose
relatedness to them is unknown. It is possible that
some natal males may have transferred with their
fathers, as the older male transfer partners were old
Am. J. Primatol.
1:3
2:6
1:7
1:3
1:3
N/Ab
1:6
1:8
1:8
3:5
0:4
N/Ab
N/Ab
Sex ratio of pretransfer group
(M:F)
4:5
2:7
1:6
3:7
4:5
2:8
2:8
3:5
3:5
2:4
2:6
2:7
2:7
2
3
2
4
2
Rangingb
2
4
4
2
4
Rangingb
Rangingb
A striking trend was that no male ever transferred back to his natal group, despite the fact that
some males transferred several times during the
study period (e.g., male KL transferred four times in
eight years: Table III). Six males even traveled
beyond the home ranges of the L. catta groups into
areas of the island with no lemurs (presumably, in
search of lemur groups), which necessitated their
removal from the island population by colony
management.
3
2
3
2
3
3
3
2
2
4
2
2
2
Intrasexual Competition Hypothesis and Male
Dispersal Behavior
Am. J. Primatol.
c
b
a
Male troop tenure began prior to data collection on troop composition.
These males transferred to a part of the island where no free-ranging lemur groups reside.
These values do not include transfer partners.
MK
MN
None
None
KL
WD
None
BR, FZ
ED, FZ
None
None
GA
TD
5.3
8.1
12
12.1
11.2
8.1
9.9
13
6
3.1
3
2.1
2.2
1
1
0
0
1
1
0
2
2
0
0
1
1
19-Jul-1998
8-Apr-2001
30-Mar-2005
23-Apr-2005
19-Jul-1998
5-May-2003
26-Jan-2001
2-Mar-2004
2-Mar-2004
22-Apr-2003
11-Apr-2000
9-May-2005
9-May-2005
KL
KL
KL
KL
MK
BY
ED
ED
BR
LE
JH
TD
GA
Unknowna
2.7
4.1
0.1
4.3
5.8
Unknowna
3.1
2.9
1.1
0.1
0.1
0.1
Date of transfer
Duration of troop
tenure prior to
dispersal (years)
] of individuals
Age at this
Identity of
with whom this transfer (years) male transfer
male transferred
partner(s)
Pre-transfer
group
Avoidance of Natal Groups as Dispersal
Destinations
Male
TABLE III. List of Non-Natal Male Transfers
enough to sire the natal male in question and were in
the group at the time of their conception.
Post-transfer
group
Sex ratio of posttransfer group
(M:F)c
654 / Parga and Lessnau
If intrasexual male mating competition is a
driving force for non-natal male dispersal, three
variables should be potentially important to male
transfer decisions: the number of females per group,
the number of males per group, and overall group sex
ratio. Although the numbers of adult females (aged 2
years and older) per group did not differ significantly
between males’ pre- and post-transfer groups (Wilcoxon: Z 5 0.66, n 5 10, Po0.51, NS), males were
more likely to transfer into a group having fewer
non-natal males than the group which they left
(Wilcoxon: Z 5 2.31, n 5 10, Po0.02).
Similarly, the M:F sex ratio of pre- and posttransfer groups differed significantly, with males
tending to move into groups having a more favorable
sex ratio (fewer non-natal males per adult female)
than in pre-transfer groups (Wilcoxon: Z 5 2.09,
n 5 10, Po0.037). Interestingly, this relationship is
only significant when excluding a male’s transfer
partners from the sex ratio of the post-transfer
group. If transfer partners were included in the
calculation of sex ratio for both groups, the sex ratio
did not differ significantly between pre- and posttransfer groups (Wilcoxon: Z 5 1.68, n 5 10, Po0.1,
NS); this trend would be expected if transferring
males do not ‘‘count’’ their transfer partners when
assessing the number of males in a prospective group
of entry.
DISCUSSION
Age at Natal Dispersal
On SCI, most males (over 88%) leave their natal
groups by the age of 2, with almost all other males
leaving at the age of 3. In contrast, only 46% of natal
males disperse between the ages of 2 and 3 in
Berenty, Madagascar [Koyama et al., 2002]. Males in
Beza Mahafaly, Madagascar leave their natal groups
even later, between the ages of 3 and 5 [Sussman,
1992]. Berenty’s rich habitat or the history of tourist
Male Dispersal in Lemur catta / 655
Fig. 2. Seasonality of male dispersal for natal (n 5 17) and non-natal (n 5 13) transfers on SCI between 1997 and 2005. Male dispersal
behavior showed a seasonal peak, which coincided with the birth season at this location.
Fig. 3. Natal males were significantly more likely to transfer with one or two other males than alone (binomial test: n 5 16, x 5 2,
P 5 0.0018). The majority of natal males dispersed from their natal group with a single transfer partner. In contrast, non-natal transfers
were no more likely to involve groups of males than lone males (binomial test: n 5 13, x 5 5, P 5 0.157, NS). The number of transfers of
each type is listed above each bar.
provisioning at this site [Koyama et al., 2001, 2002]
may be the reason for the earlier natal transfer of
males from Berenty in comparison with Beza. Even
with this variation among wild L. catta males, male
natal dispersal is an event that generally occurs
earlier on SCI than in the wild.
This earlier age at natal dispersal on SCI is
likely due to advanced male maturation as a result of
provisioning. Sexual maturation is a common correlate of animal dispersal [Baker, 1978; Smale et al.,
1997], with the timing of dispersal frequently being
controlled by body condition or fat reserves [Dufty &
Belthoff, 2001; Smale et al., 1997]. In male Belding’s
ground squirrels, for example, experimentally provisioned males disperse at an earlier age than
unprovisioned males [Nunes & Holekamp, 1996].
Indeed, female sexual maturation occurs more
rapidly on SCI than among wild L. catta. Females
on SCI reach primiparity at age 2 [Parga & Lessnau,
2005] earlier than the typical primiparous age for
females in Madagascar, which is age 3 in Beza
[Sussman, 1991] but which can occasionally occur at
age 2 in Berenty [Koyama et al., 2001].
Other factors that may lead to earlier male
dispersal on SCI include decreased predation pressure or increased familiarity with neighboring
troops. Although lemur predators do exist on SCI
[Parga & Lessnau, 2005], young males may be more
likely to disperse at an earlier age if there is
decreased predation pressure at this site as compared with the wild. Also, because the number of
potential groups in which to transfer in the wild far
exceeds the numbers of groups available to transferring males on SCI, males in this island colony may be
Am. J. Primatol.
656 / Parga and Lessnau
more familiar with neighboring groups than are
males in Madagascar, and as a result may be more
likely to attempt transfers at an earlier age.
Troop Tenure Duration: Lack of Support for
the Inbreeding Avoidance Hypothesis
Considering both natal and non-natal dispersal
events, males on SCI transfer between groups about
as frequently as do males in Madagascar. Adult
males transfer between groups about once every 3.5
years in Beza Mahafaly [Sussman, 1992], once every
3.1 years in Berenty [Koyama et al., 2002], and once
every 3.2 years on SCI. The frequency of male
transfer on SCI clearly falls well within the species’
range. It is important to note, however, that at all
three sites there is a great deal of interindividual
variation in male troop tenure length. In Beza
Mahafaly, some males remain in groups for many
years whereas others transfer almost every year
[Gould, 1994, 2006b]. Similarly, in Berenty, male
troop tenure ranged between 1 and 7 years [Koyama
et al., 2002]. On SCI, male troop tenure was also
highly variable. Some males remained in non-natal
groups for several years before transferring while
others stayed for just weeks before transferring
again. Such short tenure lengths have been noted
among wild males in Madagascar [Gould, 1994;
Jones, 1983; Sauther, 1991; Sussman, 1991, 1992].
Dispersing every few years may help some males
produce a more genetically diverse set of offspring
across their lifetime [Gladstone, 1979; Williams,
1975].
In order for the inbreeding avoidance hypothesis
for male secondary dispersal to be supported, males
should transfer from a group before potential
daughters become sexually mature [Cheney &
Seyfarth, 1983]. For male L. catta who remain in a
troop for a very short period of time and then
transfer, their departure would occur around the
time potential daughters would reach sexual maturity [Sussman, 1992]. However, on SCI, females can
mate for the first time at the age of 1, and can have
their first infant at age 2 [Parga & Lessnau, 2005].
Consequently, there is much overlap in male troop
tenure duration and the attainment of sexual
maturity by potential daughters. This finding does
not support the inbreeding avoidance hypothesis for
secondary male dispersal.
Seasonality of Male Dispersal
Among seasonally breeding primates with male
dispersal, male intertroop movement often occurs
during the mating season [e.g., vervet monkeys,
Cercopithecus aethiops: Henzi & Lucas, 1980; Cheney, 1983; Hanuman langurs, P. entellus: Borries,
2000; Japanese macaque, M. fuscata: Sprague, 1992;
rhesus macaque, M. mulatta: Boelkins & Wilson,
1972]. Instead, among L. catta on SCI, the majority
Am. J. Primatol.
of male dispersal events on SCI coincided with the
birth peak at this site, which occurs from March
through June [Parga & Lessnau, 2005]. Only a few
instances of male dispersal occurred during the
mating season on SCI. This pattern is most similar
to Berenty, Madagascar, where male dispersal
primarily occurs during the birth season [Budnitz
& Dainis, 1975; Jones, 1983]. Studies of male
transfer in L. catta (including temporary male visits)
conducted at Beza Mahafaly have shown that
transfer can also occur in the months before and
during the mating season, and the birth and
lactation seasons [Gould, 1994, 1997, 2006a; Sauther,
1991; Sussman, 1991, 1992]. Therefore, although the
overall seasonality of male transfer behavior on SCI
is most similar to that described in Berenty [Budnitz
& Dainis, 1975; Jones, 1983], the mating season
transfers on SCI are also within the range documented for wild L. catta males.
A potential adaptive explanation for why male
dispersal events occur during the birth season at
some locations is that this pattern of dispersal
provides opportunities for males to commit infanticide of other male’s offspring [Pereira & Weiss, 1991;
van Schaik, 1996]. Male L. catta attacks on infants
have been observed at Berenty [Hood, 1994; Ichino,
2005; Jolly et al., 2000], and in captivity at the Duke
Lemur Center [formerly, the Duke University
Primate Center; Jolly et al., 2000; Pereira & Weiss,
1991]. However, infanticide as an adaptive male
strategy in this species has been questioned for
several reasons [Sauther et al., 1999; Sussman,
1999]. Because infanticide by males has not been
observed on SCI [Parga & Lessnau, 2005], we
conclude that there is no direct support from our
study location at present to suggest that male
dispersal is functionally related to opportunities for
infanticide.
Instead, it appears that males on SCI transfer
primarily during the birth season (when no female is
sexually receptive) because they are apt to receive
lower levels of aggression from resident group males
at this time. The occurrence of two young males
transferring into a group during the mating season
only after the two injured adult resident males had
been enclosed in the group’s shelter provides
anecdotal but supporting evidence for this idea. In
fact, these two males were the only individuals to
ever transfer during the first estrus cycle of the
mating season, which takes place during OctoberNovember annually on SCI [Parga & Lessnau, 2005],
when rates of aggression among males are extremely
high, especially on days of estrus [Parga, 2006]. The
only other male who was observed to transfer during
the mating season entered a group having a single
resident adult male, and entered late in the breeding
season (during January). Hence, the birth season
appears to be an optimal time for males to disperse,
as it likely minimizes the amount of aggression
Male Dispersal in Lemur catta / 657
received from resident males of the group they are
attempting to join.
The proximate mechanism stimulating males to
transfer during the birth season is unknown. Also
unknown is why male L. catta on SCI do not transfer
more frequently during the mating season and
accept the cost of aggression from resident males
during this time, as do males of other primate species
[e.g., vervet monkeys, C. aethiops: Henzi & Lucas,
1980], including wild L. catta males in Beza Mahafaly
[Sauther, 1991; Sussman, 1992]. Males in this study
did emigrate voluntarily, however, and were not
aggressively evicted by any resident group members
[Parga, personal observation], which is also the case
among wild L. catta [Gould, 2006a; Sussman, 1991].
Males Dispersing Together Vs. Alone:
Functional Explanations
Males in this study frequently transferred
between groups in pairs or triplets. Less than onequarter of transfers were performed by lone males.
Natal males in particular were more likely to
transfer between groups with at least one other male
than alone. Wild L. catta males also tend to transfer
in pairs or triplets [Budnitz & Dainis, 1975; Gould,
1994, 1997, 2006a; Jones, 1983; Sussman, 1991,
1992], as do males of several other primate species
[e.g., vervets, C. aethiops: Henzi & Lucas, 1980;
Japanese macaques, M fuscata: Sugiyama, 1976;
long-tailed macaques, M. fascicularis: van Noordwijk
& van Schaik, 1985, 2001; de Ruiter & Geffen, 1998;
rhesus macaques, M. mulatta: Drickamer and Vessey, 1973; squirrel monkeys, Saimiri sciureus:
Mitchell, 1994]. Transferring with a partner can be
highly adaptive, as the partner (or partners) can help
provide protection against predators or against
aggression from resident individuals of the group
the males are attempting to enter [i.e., capuchin
monkeys, Cebus capucinus: Jack & Fedigan, 2004a,b;
vervet monkeys, C. aethiops: Cheney, 1983, Cheney
& Seyfarth, 1983].
Transferring L. catta males in the wild receive
aggression from resident individuals in the troop
that they are attempting to join, and a transfer
partner can help males to spot impending attacks
from these individuals or from predators [Gould,
1994, 1997, 2006a; Sussman, 1992]. Similarly, males
on SCI must also contend with aggression from
members of the group they are attempting to join
[Parga, unpublished data], and risk attack from a
number of potential lemur predators, both aerial and
terrestrial [Keith-Lucas et al., 1999; Parga &
Lessnau, 2005]. Therefore, as previously suggested
by Sussman [1992] and Gould [1994, 1997, 2006a],
the strategy of transferring with other males may
provide L. catta males with a much safer passage
than transferring alone.
Transferring into groups with related males may
also be functionally related to kin selection [Meikle &
Vessey, 1981]. In this study, several groups of males
transferring together were known to be closely
related through matrilineal lines. Males frequently
dispersed out of their natal groups with same-year
birth cohort members or with other males born into
their natal group who were close in age. Some
younger natal males may have also transferred out
of their natal groups with their fathers, as the older
males with whom they transferred were in the troop
when the natal male was conceived, and were also old
enough to have fathered them. This speculative idea
must await the completion of paternity analyses
currently in progress to be properly evaluated.
Regardless of relatedness, travelling with an
older male may be particularly important because
the experience of the older male can aid the
successful integration of a younger male into a new
social group [Gould, 1994]. A transfer partner (or
partners) can also provide dispersing males with
valuable affiliative relationships while they are
making the transition from one group to another
[Gould, 1994, 1997, 2006a]. Indeed, male transfer
partners on SCI have been observed mutual grooming and huddling together during resting periods
while on the periphery of a new group [Parga,
personal observation].
Avoidance of Natal Groups as Dispersal
Destinations
Notably, no male ever returned to his natal
group, despite the fact that some males transferred
several times during the study period. This is similar
to other cases in which males rarely or never return
to their natal group to breed [e.g., capuchins, Cebus
capucinus: Jack & Fedigan, 2004b; baboons,
P. hamadryas, Packer, 1979; macaques, Macaca
spp.: Dittus, 1979; Sugiyama, 1976; Drickamer &
Vessey, 1973]. This pattern of avoidance of returning
to the natal group is even more striking when one
considers the small number of lemur groups on SCI
(3–4 throughout much of the colony’s history). As a
consequence, the degree of inbreeding on SCI is
likely to be lower than it otherwise would be if males
did not avoid their natal groups as transfer destinations.
Intrasexual Competition Hypothesis: Group
Composition and Male Dispersal
If male–male competition drives secondary male
dispersal, non-natal males might be expected to
transfer into groups with greater numbers of
females, or groups having more favorable sex ratios
than their previous group of residence [e.g., whitefaced capuchin, Cebus capucinus: Jack & Fedigan,
2004b; rhesus macaque, M. mulatta: Drickamer &
Vessey, 1973; baboon, P. hamadryas: Packer, 1979;
Am. J. Primatol.
658 / Parga and Lessnau
Alberts & Altmann, 1995]. Among wild L. catta
males in Beza Mahafaly, Madagascar, Sussman
[1992] found that males were more likely to leave
groups with higher male-to-female sex ratios. In this
study, there was not a significant difference in males’
pre- and post-transfer groups in the numbers of
adult females. Neither was there a difference in the
sex ratio of males’ pre- and post-transfer groups
when a male’s transfer partners were included in the
calculation of sex ratio (for both pre- and posttransfer groups). However, group sex ratios were
found to differ significantly between males’ pre- and
post-transfer groups when males’ transfer partners
were excluded from the post-transfer group-male
count. We interpret this as support for the intrasexual mating competition hypothesis for secondary
male dispersal. Furthermore, these findings suggest
that transferring males do not include current
transfer partners when assessing the composition
of a prospective group of entry.
We also found that male L. catta on SCI were
significantly more likely to join a group having fewer
non-natal males than in their previous group. This
trend was noted among wild L. catta in Berenty,
Madagascar, and was interpreted as male avoidance
of groups with a greater number of potential
competitors [Jones, 1983]. The number of males per
group is indicative of the amount of competition a
male will likely experience because females commonly mate with multiple males during estrus, and
male dominance rank shows much instability at this
time [Gould, 1994, 1997; Jolly, 1966; Koyama, 1988;
Sauther, 1991; Taylor & Sussman, 1985]. There is
also a strong positive correlation between the number
of male mates per female and the rate of male–male
aggression during estrus [Parga, 2006]. Furthermore,
after male transfers have occurred during the spring
and summer months on SCI, troop composition tends
to remain stable until the fall mating season. Thus,
secondary male dispersal in L. catta (dispersal
between two non-natal groups) appears to be driven
by avoidance of the natal group as a transfer
destination, as well as by avoidance of groups in
which a male would experience more intense
male–male competition during the mating season.
ACKNOWLEDGMENTS
We thank the SCI Foundation and the WCS for
their maintenance of the L. catta colony throughout
the years. L. Gould, P. Henzi, R. R. Lawler, R. J.
Lewis, D. J. Overdorff, L. Shapiro, and one anonymous reviewer kindly provided comments that
greatly improved this article. A. Henry helped
compile records on male intertroop movement and
S.J. Lozano aided in figure formatting. During the
writing of this paper, J. A. Parga was supported
by a Ford Foundation Dissertation Fellowship and by
a US National Science Foundation Postdoctoral
Am. J. Primatol.
Fellowship. All research reported in this article
adhered to the American Society of Primatologists’
Principles for the Ethical Treatment of Non Human
Primates, was approved by both the WCS and the
IACUC at the University of Texas at Austin, and
adhered to the legal requirements of the United
States.
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