Population Survey and Demographic Features of a Coastal Island Population of Alouatta clamitans in Atlantic Forest, Southeastern Brazil

Abstract

Brown howlers (Alouatta clamitans) are endemic to the Atlantic Forest. Because only 7.5% of this fragmented forest remains in Brazil, there is an urgent need for studies of its ecology. Understanding island populations, still poorly researched in the relatively well-studied Alouatta, can provide important information for understanding habitat fragmentation and conservation. We studied brown howlers on the northern portion of the coastal and protected island, Ilha do Cardoso State Park. We used distance sampling methods on 5 transects to estimate population density of the howlers. Estimated howler density on the island is 10.6 individuals/km2, with a total of 36 (21-62) individuals in a 3.4 km2 area. The density is low, but similar to that of other large and preserved areas. By triangulating on vocalization and following groups, we estimate that there are 10 groups with an average of 4.5 individuals per group. Groups comprise 42% adult females, 27% adult males, 20% juveniles, 7% infants, and the remaining 4% subadult males. Howlers apparently use all appropriate habitats, including Atlantic Forest of plains and slopes. We believe that the howler population is maintaining a typical replacement on the island, with low birth rates and high survival rates, but long-term studies are required to test this. Small group size and associated social structure may be due to the particular environmental conditions on Ilha do Cardoso State Park.

Full text

Population Survey and Demographic Features
of a Coastal Island Population of Alouatta
clamitans in Atlantic Forest, Southeastern Brazil
Bianca Ingberman &Roberto Fusco-Costa &
Emygdio Leite de Araujo Monteiro-Filho
Received: 22 June 2008 / Accepted: 23 July 2008 /
Published online: 20 January 2009
#Springer Science + Business Media, LLC 2009
Abstract Brown howlers (Alouatta clamitans) are endemic to the Atlantic Forest.
Because only 7.5% of this fragmented forest remains in Brazil, there is an urgent
need for studies of its ecology. Understanding island populations, still poorly
researched in the relatively well-studied Alouatta, can provide important information
for understanding habitat fragmentation and conservation. We studied brown
howlers on the northern portion of the coastal and protected island, Ilha do Cardoso
State Park. We used distance sampling methods on 5 transects to estimate population
density of the howlers. Estimated howler density on the island is 10.6 individuals/km
2
,
with a total of 36 (21–62) individuals in a 3.4 km
2
area. The density is low, but
similar to that of other large and preserved areas. By triangulating on vocalization
and following groups, we estimate that there are 10 groups with an average of 4.5
individuals per group. Groups comprise 42% adult females, 27% adult males, 20%
juveniles, 7% infants, and the remaining 4% subadult males. Howlers apparently use
Int J Primatol (2009) 30:1–14
DOI 10.1007/s10764-008-9324-z
B. Ingberman
Programa de pós-graduação em Ecologia e Conservação, UFPR, Centro Politécnico, C.P. 19020,
Curitiba, Paraná 81531-990, Brazil
B. Ingberman (*):R. Fusco-Costa :E. L. de Araujo Monteiro-Filho
Instituto de Pesquisas Cananéia (IPeC), Rua Tristão Lobo 199, Cananéia, São Paulo 11990-000,
Brazil
e-mail: bibugio@yahoo.com.br
E. L. de Araujo Monteiro-Filho
Department of Zoology, and Programa de pós-graduação em Ecologia e Conservação, Federal
University of Paraná (UFPR), Centro Politécnico, C.P. 19020 Curitiba, Paraná 81531-990, Brazil
Present address:
B. Ingberman :R. Fusco-Costa :E. L. de Araujo Monteiro-Filho
Instituto de Pesquisas Cananéia (IPeC), Rua Tristão Lobo 199, Cananéia, São Paulo 11990-000,
Brazil

all appropriate habitats, including Atlantic Forest of plains and slopes. We believe
that the howler population is maintaining a typical replacement on the island, with
low birth rates and high survival rates, but long-term studies are required to test this.
Small group size and associated social structure may be due to the particular
environmental conditions on Ilha do Cardoso State Park.
Keywords Alouatta clamitans .coastal island .group composition .linear transect .
population density
Introduction
Alouatta includes the most widespread monkeys in the New World, with 10 species
in Brazil (Gregorin 2006). The southern brown howler, Alouatta clamitans
Cabrera,1940, endemic to the Atlantic Forest (Kinzey 1982), occurs from Misiones
in Argentina in the south (Di Bitetti et al.1994) to its northeastern limit at the Serra
do Espinhaço, Brazil (Gregorin 2006). In Brazil, its range extends from Rio Grande
do Sul in the south (Printes et al.2001) to the Rio Jequitinhonha River in the north
in Minas Gerais (Rylands et al.1996).
Few studies of population dynamics, in comparison to many behavioral studies,
for most primates belie the fact that just such studies are required for understanding
the populations and their possible conservation management (Cullen and Valladares-
Padua 1997; Roper 2006).
In addition to population density, we must also understand how the howlers are
distributed within this habitat. Accordingly, we must also study interactions between
ecology, demographic history and population structure (Chapman and Balcomb
1998). For example, group size and composition are important components of the
dynamics that influence population density (Crockett and Eisenberg 1987) that, like
patterns of space use, can reflect needs of a particular habitat. These data are very
important to shape future studies.
Today, the Atlantic Forest is reduced to ca. 8% of its original extent, and that
which remains is very fragmented. Of the 91,930 km
2
that remain, only 36%
(33,084 km
2
) is protected, even though it is a conservation hotspot because of its
species richness and number of endemic species (Ministério do Meio Ambiente
2000;Myerset al.2000). Island populations in threatened ecosystems may
represent an important extreme condition for understanding population dynamics.
Studies of island population dynamics arenonexistentatIlhadoCardosoState
Park, even though it is an important conservation unit. Yet, the island population is
not necessarily isolated because the distance to the mainland is small and howlers
can move between the 2. The single study on howlers only estimated the
total population size on the island (São Bernardo 2004).Thus,hereweestimate
population density, group size, and organization to understand the island
population better, providingimportantandusefulinformation for management,
and to examine how population information may inform primate conservation
strategies for fragmented populations.
2 B. Ingberman et al.

Materials and Methods
Study Area
The Parque Estadual Ilha do Cardoso (PEIC) is an island (25°03′05′′ to 25°18′18′′S
and 47°53′48′′ to 48°05′42′′W; Fig. 1) and state park that comprises 151 km
2
(Sampaio et al. 2005), of which 74% is Atlantic Forest (111 km
2
; Melo and
Montovani 1994). The island is within the municipality of Cananéia, on the coast of
the State of São Paulo, in southeastern Brazil. Topography here is variable, from sea
level to 800 m (Pfeifer 1981–82). Without a dry season, rainfalls peak from
December to March, with peaks reaching 1.673–3.014 mm/yr (Funari et al.1987);
there is a wet season (October–March) and a less wet season (April–September).
In the island, there are well preserved terrestrial, coastal, and marine ecosystems
with ca. 400 species of birds and 80 species of mammals (CONSEMA 2001).
Among the mammals highlights the presence of medium and large mammals as the
ocelots (Leopardus pardalis), cougars (Puma concolor), white-lipped peccaries
(Tayassu pecari), collared peccaries (Pecari tajacu), agutis (Dasyprocta leporina),
capybaras (Hydrochaeris hydrochaeris), pacas (Agouti paca), coatis (Nasua nasua),
and brown howlers (Alouatta clamitans), the only primate specie on the island
(Nakano-Oliveira 2006; São Bernardo 2004; Almeida 1946).
Before its establishment as a protected area in 1962, traditional communities
comprising descendents of European colonists occupied Ilha do Cardoso. The
communities used simple agriculture and fishing on a small scale, especially from
the 18th to the 20th centuries (Almeida 1946). Today they occur only on the margins
of the southern, eastern, and northern coastal plains, living by fishing and tourism.
Beginning in the 1990s, Guarani Mbya Indians moved to the northwestern part of
Fig. 1 The study area showing the location of the trails used in the linear transect method to estimate
howler population size on the northern part of Ilha do Cardoso, in São Paulo, southeastern Brazil.
Demography of Brown Howlers in Southeastern Brazil 3

the island, where 30 people live today (Marcos Campolin, pers. comm.). The
population changes altered the natural vegetation, with primary forest occurring only
in the middle of the island, in the more mountainous region that is still difficult to
reach (Melo and Montovani 1994). Today, the Guarani Mbya still clear forests
occasionally to build houses and for cultivation (Marcos Campolin, pers. comm.).
The study area comprises pluvial tropical forest. In the coastal plains, the canopy
reaches ≤20 m, whereas the understory varies from 8 to 10 m, mostly in the northern
and eastern part of the island (Barros et al.1991). On the slopes of the highlands, the
understory is denser at ≤10 m, though emergent trees of the canopy can occasionally
reach 35 m (Melo and Montovani 1994).
Methods
We studied howlers from December 2005 to December 2006 on 5 trails (total length
8050 m), used for line transects in the northern part of the island (Fig. 1). Trail A
(2000 m) is relatively level, on the coastal plains, and 500 m of it at one end are used
for ecotourism. Trail B (2050 m), also on the coastal plains, west of the first, has
almost daily human activity, usually due to the indigenous people. Trail C (1500 m)
extends from the coastal plains up to 360 m altitude and is used only by researchers.
The first 500 m includes secondary growth on an abandoned road. Trail D (1200 m)
also ascends the foothills, with elevation ranging from near sea level to 240 m and
seldom shows signs of human activity. The region of the Trail E (1300 m) was clear-
cut for local agriculture ca. 45 yr ago (Zilda Cardoso, pers. comm.). Currently,
secondary growth is typical, with some tall grasses [Scleria secans (L.) Urban
(Cyperaceae)] and emergent trees (<15 m) of Leguminoseae (Selmo Bernardo, pers.
comm.). Trail E varies from 0 to 220 m elevation and the last 70 m has several fig
trees (Ficus spp.) and is near habitations of the local indigenous people.
We estimated population density via distance methods with linear transects per
Buckland et al.(1993). To orient better along the trails and to estimate distances, we
marked trails every 50 m with colored flagging and the points with GPS (Garmin
E-trex, datum SAD 69′; Cullen and Rudran, 2003;Peres,1999). One or 2
researchers counted howlers twice (once in the morning and once in the evening)
per month, weather permitting, with ≥2.5 h between counts (Ferrari 2002). Bad
weather interferes with detection probabilities. To count howlers, we walked trails at
a constant velocity of 0.5–1.0 km/h (Brockelman and Ali 1987; Chiarello 2000;
Cullen and Valladares-Padua, 1997; Pinto et al.,1993) with stops for an average of
30 s every 100 m. Morning walks were from 0800 to 1200 h and afternoon walks
from 1400 to 1800 h, per Peres (1999) and Cullen and Rudran (2003).
We counted howlers only when we sighted them. We recorded time, date, location,
height, behavior (traveling, resting, vocalizing, feeding) of the first individual at the time
of sighting and group composition at each encounter, as well as the perpendicular linear
distance to the transect. We either measured or estimated the perpendicular distance to
the trail from the individualor group observed. When necessary to determine group size
and compositions, we followed individuals for ≤30 min.
We collected other data at different times. Occasionally we found groups and
recorded number and composition (sex and age class). We identified sex clearly only
4 B. Ingberman et al.

in mature individuals when sexual dichromatism is evident (Crockett and Eisenberg
1987; Neville et al.1988). We based age class on size-scaling (NRC 1981) and
behavior. We considered individuals infants if held by the mother or carried on her
back when traveling. We noted GPS coordinates (latitude, longitude) at all
encounters. Thus, we easily identified each group based on group structure,
individual markings, numbers of individuals, location where last sighted. When we
only heard the group, we used triangulation to estimate its location. We performed
triangulation via 3 compass bearings from the trail toward the sound and later
mapping the points and estimating their coordinates.
For estimating population size, we used the area in which we either observed
individuals and groups or heard their vocalizations and established their positions via
triangulation. The area encompassed within the limits measured 3.4 km
2
and was a
reliable area.
Data Analysis
We used distance methods to estimate population density per Buckland et al.(1993).
We either measured perpendicular distances of the subjects to the transect line either
directly (rangefinder), or if the topography did not allow the measure, via
triangulation with a compass. We analyzed distance data via DISTANCE 4.0
(Buckland et al.1993) as follows:
D¼nf
0s=2L
wherein D=density of the population, n= number of encounters; f
0
=probability
density function for encounters, s=average group size, and L= total transect length.
In distance methods, population density is estimated via 2 parameters: encounter
probability, g(x), and the number of encounters.
We compared the number of encounters between sampling periods (morning and
afternoon) and the 2 seasons of the year. We also compared behaviors to test whether
some resulted in encounters more often than expected. We gathered expected values
from published data (Chiarello 1992; Jardim 2005; Lunardelli 2000; Mendes 1989).
We also compared slopes with plains to test whether howlers were more likely to be
found at one than the other. Tests were significant at p<0.05.
To calculate group location and triangulation we used Arc View GIS 3.1 (ESRI
1998) with the azimuth extension.
Results
Density
A total of 175,000 m traversed (91,950 m in the plains, 83,050 in the slopes; Table I)
in 225 h of effort during 111 transect walks resulted in 26 encounters. We used the
part of the northern region of the island (3.4 km
2
) in which we could accurately
estimate sightings and locations of vocalizing individuals (reliable area) to estimate
the population size because of the heterogeneous topography and vegetation of the
Demography of Brown Howlers in Southeastern Brazil 5

rest of the island. Owing to the thick vegetation, the maximum detection distance
from the trail to an individual or group was ca. 50 m (Fig. 2). Through the analysis
of data via DISTANCE the hazard-rate with a cosine adjustment best fit the detection
function.
We estimated density at 10.6 individuals/km
2
(CV=25.9%) with group density at
2.4 groups/km
2
(CV=25.7%). This provides a population size estimate of 36
individuals in the 3.4km
2
study area. We estimated average group size at 4.5
individuals/group (Table II). The numbers of encounters were similar in the morning
and afternoon (χ
2
=0.02, df=1, p>0.05) and within 30 min intervals in the morning
(χ
2
=4.27, df=7, p>0.05) or evening (χ
2
=5.69, df=8, p>0.05). Encounter rate was
also similar among seasons (χ
2
=5.6, df=3, p>0.05). However, groups differed in
their detectability due to their behavior (χ
2
=12.2, df=3; p<0.05; Fig. 3).
Group Distribution
Though groups may have differed in detectability, the difference is not due to being
on the slopes or the plains (χ
2
=0.5; GL= 1; p > 0.05). We encountered groups 19
times (61%) on the slopes and 12 times (39%) on the plains, including 5 additional
sightings not during transect counts.
Fig. 2 Encounter probability function for perpendicular distances. The histogram represents observed
values and the curve the expected values.
Table I Distances of transects and total distance traveled in five transects on northern Ilha do Cardoso for
the distance sampling methods used to estimate abundance of the Alouatta clamitans
Transect Length (m) Topography Number of visits Total distance (m)
A 2050 Plains 24 46,300
B 2000 Plains 24 45,650
C 1500 Slope 23 34,600
D 1200 Slope 24 28,000
E 1300 Slope 16 20,450
6 B. Ingberman et al.

Table II Estimates of population density for Alouatta clamitans in different areas of the Atlantic Forest
Location Area
(km
2
)
Density Encounter rate
(per 10 km)
Individuals /
10 km
Estimated
population
Method (duration
in months)
Distance
walked (km)
Group
size
References
a
(latitude)
Groups Individuals
RB Alberto Ruschi–ES 40 2.4 (0.6–9.5) 10.1 (1.8–40.0) 1.87 404 (72–1,600) Linear transect (12) 165 3.7 (2–6)
c
4 (19°38′S)
EB Caratinga–MG 1.1 17.2 117 –129 Intensive study area (11) –6.79 (3–10)
c
6 (19°50′S)
5.7 17.2 667
Serra do Brigadeiro
(Fazenda Neblina)–MG
3.2 –7.5 –– Linear transect (12) ––7 (20°34′S)
Morro do Diabo–SP 350
b
–15.6 0.71 1,029–28,812
b
Linear transect (20) 2,287 (161–618 /local) –11 (22°30′S)
b
Fazenda Tucano–SP 20
b
–10.9 0.71 111–266
b
Linear transect (20) 2,287 (161–618 /local) –11 (22°30′S)
b
Lageadinho –SP 0.48 –98 –Home range –7 ha (?) –6–12
c
10 (22°41′S)
FBR (Viraeiro/
Tabatingüera)–SP
1.15 3.48 22 (14–38) –25 (16–44) Intensive study area (13) –6.4 (4–11) 10 (22°41′S)
Viraeiro/ Tabatingüera
(FBR)–SP
14.5 –27.1 (23.4–33.4) 1.4 –Linear transect (10) 131.4 3.4 +6.4 12 (22°41′S)
Sara (FBR)–SP 5 –34.6 (29.8–42.6) 2.2 –Linear transect (10) 68.3 2.7 +6.3 12 (22°41′S)
Água Sumida (FBR)–SP 2.4 –10.42 (9–12.9) 1 –Linear transect (10) 40 1.8 +3.5 12 (22°41′S)
Monal (FBR)–SP 3.74 –8.32 (7.1–10.2) 0.6 –Linear transect (10) 35.1 2.5 12 (22°41′S)
Fazenda Mosquito–SP 21
b
–36.3 0.71 125–220
b
Linear transect (20) 2,287 (161–618 /local) –11 (22°44′S)
b
EE Caetetus–SP 21.78
b
–0.6 0.71 296–425
b
Linear transect (20) 2,287 (161–618 /local) –11 (22°44′S)
b
Fazenda Rio Claro–SP 17
b
–16.3 0.71 112–267
b
Linear transect (20) 2,287 (161–618 /local) –11 (22°46′S)
b
RM Santa Genebra –SP 2.3 24.3–36.08 119–177 –274–407 Home range (12) –4.9 (2–9) 3 (22°49′S)
Mata Doralice–PR 1.7 31–39 82–102 –140–175 Home range (12) –3–6
c
13 (23°16′S)
Reserva da Cantareira–SP 54 8.75 80.9 +32.5 –4,369 +1,755 Linear transect (17 days) 32 5.76 (2–11)
c
5 (23°30′S)
Demography of Brown Howlers in Southeastern Brazil 7

Table II (continued)
Location Area
(km
2
)
Density Encounter rate
(per 10 km)
Individuals /
10 km
Estimated
population
Method (duration
in months)
Distance
walked (km)
Group
size
References
a
(latitude)
Groups Individuals
PE Intervales–SP 498.88 –18–22 –10,975 Quadrants (25) –5.83 (4–8)
c
2 (24°12′S)
Paranapiacaba–SP 1,000 0.39 +0.17 0.8 +0.4 0.25 +0.08 789 (299–2,083) Linear transect (1) 352.4 1.8 +0.4 1 (24°20′S)
PE Ilha do Cardoso–SP 3.4 2.35 (1.3–4.5) 10.6 (6.1–18.3) 1.48 36 (21–62) Linear transect (12) 175 4.5 (3–6)
c
This study (25°03′S)
PE Ilha do Cardoso–SP 111 3.4 (2.6–4.4) 8.9 (6.9–11.6) 1.3 997 (769–1,291) Linear transect (15) 273.05 2.6 (?–6) 8 (25°03′S)
Bugre.Balsa Nova–PR 0.9 –38 –266 Home range (12) –6.3 (4–10)
c
16 (25°29′S)
FLONA de Três Barras–SC 0.94 10.68 64 –60 Home range (26) –6(5–7) 9 (26°12′S)
Morro da Extrema–RS 0.86 –100 –– No. of ind. × total used area (24) –8(4–12)
c
15 (30°12′S)
Restinga do Lami–RS 0.14 –260 –– No. of ind. × total used area (24) –9.4 (7–13)
c
15 (30°15′S)
PE Itapuã. Morro da
Fortaleza–RS
1.71 –110 –– No. of ind. × total used area (24) –7.4 (5–11)
c
15 (30°23′S)
PE Itapuã. Morro do
Campista–RS
8–74.8 –600 Linear transect (8) 107 6.8 (5–9)
c
14 (30°23′S)
RM= Reserva Municipal; EB=Estação Biológica; FLONA=Floresta Nacional; RF= Reserva Florestal; FBR =Fazenda Barreiro Rico; PE=Parque Estadual; RB =Reserva
Biológica; EE= Estação ecológica.
a
1, González-Sólis et al. (2001); 2, Steinmetz (2001); 3, Chiarello (1992); 4, Pinto et al. (1993); 5, Silva (1981); 6, Mendes (1989); 7, Consenza and Melo (1998); 8, São
Bernardo (2004); 9, Perez (1997); 10, Torres de Assumpção (1983); 11, Cullen et al. (2001); 12, Martins (2005); 13, Aguiar et al. (2003); 14, Buss (2001); 15, Jardim (2005); 16,
Miranda (2004).
b
apud Chiarello (2003).
c
Studies that show group structure.
8 B. Ingberman et al.

We twice encountered 2 groups at the same time. In the first instance, on trail C,
the individuals went their separate ways after an antagonistic interaction between the
males, i.e., vocalizations, threat displays. In the second instance, at the end of trail E,
1 group vocalized while the other remained quiet, hidden in the canopy of a tree.
When the vocalizing group quieted, the hidden group came out of hiding and moved
away, while the other group remained but a short time later moved away as well.
We identified 10 groups and 2 solitary males, with overlapping areas of 4 groups
(2 each on E trail and C trail). We located individuals 15–25 m above the ground,
with 55% at 15 m, 36% at 20 m, and only 9% at 25 m in the emergent trees (χ
2
=
31.4; df=2, p<0.05).
Social organization in 80% of the groups had 1 adult male. Groups comprised
42% adult females, 27% adult males, 4% subadult males, 20% juveniles, and 7%
infants. The sex ratio of adult females to adult males was 1.58:1. There were 0.6
immatures per adult female (IFR) and 0.16 infants per adult female (IAR). No group
comprised only adults, and in 70% of the groups, nonadults were only juveniles and
in 20% of the groups, nonadults were only infants.
Discussion
To compare densities among studies, it is very important that the studies be
conducted following the same methodologies (Cullen and Valladares-Padua 1997).
Nonetheless, population density of howlers is variable in the literature (0.6–80.9
individuals/km
2
) and here, 10.6 individuals/km
2
. The island howler density is
relatively low vs. an average among published studies, many of which are in
fragmented landscapes (22 individuals/km
2
, Table II); however, it is similar to that of
large forest reserves (Chiarello and Galetti 1994) or in large forest tracts (Crockett
1998; Marsh et al.2003). Perhaps lower densities are normal in large, protected
areas. If so, low densities may not indicate low-quality habitat or a negative impact
on the population.
To date, disease is unknown. Potential predators are ocelots (Leopardus pardalis)
and cougars (Puma concolor), yet there is no report of predation by either of them
on howlers on the island (Nakano-Oliveira 2006). The possibility of hunting also
Fig. 3 Behavioral categories and the percentage of the time that individuals were engaged in each. Black,
observed values at Ilha do Cardoso; white, expected values based on the literature.
Demography of Brown Howlers in Southeastern Brazil 9

seems ruled out because the local people on the island apparently seldom or never
hunt howlers (pers. obs.) and because it is a conservation unit, hunting should be
lower.
Thus, we suggest that the relatively large, protected area of Ilha do Cardoso and
the life history patterns of Alouatta (long life, low birth rate; Kappeler et al.2003),
result in the observed low, but natural and probably healthy, density. To gain more
insight into the possibilities, we need to study not only population size, but also
distribution patterns on a local scale and habitat use to understand population
dynamics, ecology, and behavior of the island howler population.
If we extrapolate our density estimates to the northern area of the island with
similar vegetation and habitat characteristics (20.5 km
2
), where howlers are also
present (pers. obs.), then the total population size is estimated at 217 (95%
confidence interval: 125–374). The extrapolation for the entire island is not possible
because of the huge variability of the vegetation on the island (Giulietti et al. 1983
apud Melo and Montovani, 1994). Nevertheless, the density we estimated is within
the range of most studies (Table II) and similar to the value of São Bernardo (2004)
on Ilha do Cardoso, the first study of the species on an island.
On the island, howlers apparently use all appropriate habitat, which includes
Atlantic Forest of plains and slopes and excludes areas in regeneration for <50 yr.
For instance, based on personal observations of many researchers, residents, and
environmental monitors, howlers apparently never use restinga —coastal, low
savannah—vegetation. Thus, while not using restinga as they use the forest, the
restinga may still serve as a bridge for their travels. For example, it occurs in some
individuals feeding in a small hill covered by Atlantic Forest (Morro do Trapiche,
pers. obs.; Fig. 1) that is isolated from the central plain and slope forest of the island
by restinga vegetation.
Howler life history strategy is one of energy conservation (Milton 1980 apud
Crockett and Eisenberg 1987), and travel is usually to find an individual food source,
such as fruits, that are seasonally available (Estrada and Coates-Estrada 1986;
Limeira 2000; Lunardelli 2000). Figs of Ficus are a favored food (Bicca-Marques
2003; Chitolina and Sander 1981; Estrada and Coates-Estrada 1986; Lunardelli
2000; Nagy and Milton 1979; Serio-Silva et al.2002;) and, in some places, are
followed in preference by some species of Leguminosae (Bicca-Marques 2003;
Lunardelli 2000). Fig density is greatest on the plains (Coelho 2005), yet howler
encounter rate is not greater. Also, in the areas of regeneration <45 yr old without
large trees, we noted only signs (fresh feces) of howlers. Perhaps, because there are
some trees in the Leguminoseae, the howlers travel rapidly to forage, returning
quickly to the more mature forest.
Group Composition
Social organization is variable among Alouatta spp. (Neville et al.1988) but seems
to be similar within individual species. On the island, 80% of the groups had 1 male,
which is typical for the species (Mendes 1989). In Alouatta seniculus, males
apparently monopolize the social group dependent on its size (Rudran and
Fernandez-Duque 2003). This is not true for Alouatta clamitans, in which, though
density varies enormously [≤260 individuals/km
2
(Jardim 2005) and 10.6
10 B. Ingberman et al.

individuals/km
2
on Ilha do Cardoso], social structure is very similar among groups
of different sizes, viz.,group structure of Alouatta clamitans is typically unimale.
When the number of individuals does not allow it, the group tends to split,
reestablishing the unimale structure, as registered once by Miranda in 2004.
The ratio of immatures to adult females (IFR) on the island is lower than at other
sites. The highest IFR was 1.7 (Jardim 2005) and the lowest was 0.6 (this study).
The birth rate of infants to adult females (IAR) at Ilha do Cardoso was 0.16, the
second lowest recorded for the species (0.14, Miranda 2004), suggesting a low birth
rate.
All groups had nonadult individuals, with juveniles only in 70% of the groups
and infants only in 20%. Only the largest group (6 individuals) contained both, 1
juvenile and 1 infant. This difference is because the infant age class is ephemeral:
infants become juvenile at 12 mo, while it takes another 40 mo for the juveniles to
become subadult (Neville et al.1988). Consequently, one expects there to be more
juveniles than infants.
In summary, we believe that the Ilha do Cardoso population of brown howlers is
healthy and natural, possibly maintaining a typical replacement based on low
mortality and low birth rates, but long-term studies are required to test this. The low
density does not appear to be a problem, or caused by negative human impacts on
the environment, but instead seems typical for large, well-protected forest regions,
like Ilha do Cardoso. Therefore, we believe that it is adequate for the maintenance of
the howler population and that small group size with similar structure may be merely
the response to the environmental conditions on the island.
Acknowledgments We thank the Instituto Florestal of São Paulo for permission to conduct this research
in PEIC, Parque Estadual Ilha do Cardoso for logistic support, Idea Wild for equipment, and Fundação o
Boticário de Proteção à Natureza for financial support. We thank James J. Roper, Julio César Bicca-
Marques, Mauricio Moura, and 2 anonymous referees for valuable suggestions. James J. Roper translated
the paper from Portuguese.
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