American Journal of Primatology 21:279-294 (1990)

Alouatta caraya: Population Density and Demography Northern Argentina

DAMIAN I. RUMIZ Department of Wildlife and Range Sciences, and Program for Studies in Tropical Conseruation, University of Florida Gainesuille

A long-term study was carried out on a black howler monkey (Alouatta caraya) population living in 150 ha of forest patches spread out in a 3,000 ha rural area in Northern Argentina. A total of 22 different groups were located between 1980 and 1984 and 11 of these were monitored regularly during 28 months.

Ecological density varied between 12.14 and 12.93 groups per sq km of tall dense forest (0.80 to 1.15 ind.iha; biomass 306 to 365 kgisq km). Sol- itaries and small associations of adult or subadult individuals of both sexes were also recorded but occupied habitats of inferior quality. Mean sizes of reproductive groups varied from 6.4 to 8.4 and the range was 3 to 15 individuals. Reproductive groups had 1 to 3 adult males, 1 to 3 adult females, and several immatures. Sex ratio was biased toward females among the adults but it varied in other age classes. Births occurred throughout the year showing a peak in the colder and drier season. Sub- adult or young adult males and females dispersed from suspected natal groups and became solitaries or joined associations. Males invaded groups and displaced or coexisted with resident males. Infanticides and disappear- ances of infants were associated with male changes.

Comparative censuses on an island not far from the main study area showed higher density and biomass (2.8 ind./ha; 1,117 kg/sq km) and dif- ferent group sizes and composition. Habitat features as well as the history of each study site may account for the observed demographic differences.

Key words: howler monkeys, group composition, population changes

INTRODUCTION The study of population structure and composition provides the link between

the behavior of individual animals and the population level phenomena that give rise to evolutionary change [Dunbar, 19871. Although much field work has been done on howler monkeys (Alouatta), the evolutionary implications of group size and demography are still difficult to interpret due to the ample intra- and inter- specific variability they show [Crockett & Eisenberg, 19871. A pattern is apparent, however, in the best studied species: A. palliata and A. seniculus. Both species

Received for publication February 3, 1989; revision accepted April 3, 1990.

Address reprint requests to D. Rumiz, 118 Newins-Ziegler Hall, University of Florida, Gainesville, FL 32611.

0 1990 Wiley-Liss, Inc.

280 / Rumiz

appear to have larger groups at higher densities than at lower ones, but A. palliata typically exists in larger groups, with more adult females per male than A. senic- ulus [Crockett & Eisenberg, 19871.

It is not clear how much of the extant information from these two species can be generalized to the whole genus Alouatta, or even from a single population to an entire species [Eisenberg, 19791. Group size and composition are the result of demographic processes that take years to occur [Altmann & Altmann, 1979; Rob- inson, 19881, and short-term studies of few groups may lead to misconceptions about primate social organization [Crockett, 19851.

Data for A. caraya (black howler) are limited to Pope's [1968] analysis of an island population which was totally collected and to Thorington et al.'s [1984] field study on the Argentine bank of the Paraguay River which was interrupted before 1 year of sampling. Based on these studies it is possible to infer that A. caraya is similar to A. seniculus in group size and composition, but many other aspects remain to be examined. Basic population and demographic data on relatively less known species such as A. caraya are important to understanding the comparative biology of these platyrrhines. This study presents long-term data on density, changes in group composition, and reproduction of a black howler population living in a fragmented habitat, as well as short-term comparative observations on density and group composition from a continuous habitat.

MATERIALS AND METHODS Study Area

The black howler inhabits riverine and inland forests of Brazil, Paraguay, Bolivia, and northeastern Argentina. Its southernmost populations occur at about 29" S [Colillas & Coppo, 19761, along the Rio Parana and tributaries.

The main study was carried out in a 3,000 h a area of grasslands and forest patches on both sides of the Rio Riachuelo (27" 30' S and 58" 41' W) (Fig. 1). Situated south from the Tropic of Capricorn, this area has a mean annual temper- ature of 21.7" C (with extremes of 44.4" C and 1.1" C) and a rainfall average of 1,200 mm (50 yr record, Estaci6n Corrientes). Rains occur throughout the year but de- crease in quantity from June to August. In contrast to other howler study sites, the dry season is the coldest period of the year and frosts can occur.

The vegetation is a mosaic of forest and clear-cut areas that are dominated by grazing fields that developed after the semideciduous forest of Schinopsis balansae, Astronium balansae (Anacardiaceae), and Tabebuia avellanedae (Bignoniaceae) was cut. Patches of dense tall forest [Morello, 19681 around 15 m in height and ranging from 1 to 10 ha in size remain on some flat hillocks and along the creeks and banks of the Rio Riachuelo. These areas contain trees of the above-mentioned species as well as Ficus enormis (Moraceae), Phytolacca dioica (Phytolaccaceae), Enterolobium contortisiliquum, Gleditsia amorphoides (Fabaceae), and a common exotic species, Melia azedarach (Meliaceae). Most of these tree species and several vines are important food sources for the howlers [Rumiz et al., 19861. Stands of forest still occur in highly disturbed areas but the individual trees of the above species are not as tall, and bamboo (Guadua angustifolia) as well as thorny tree species also are present. Open forests with palm trees (Copernicia australis) occupy temporarily flooded areas near lagoons. A vegetation map of the Riachuelo area and maps of the main forest patches were drawn from aerial photographs. Tall forest accounted for only 150 ha (5%) of the total 3,000-ha study area.

For comparative purposes, censuses of howlers were conducted on Isla Guas- cara, a 600-ha island in the Rio Parana, located 40 km North of the Riachuelo area. The island vegetation is a seasonally flooded forest dominated by Nectandra fal-

Caraya Howler Density and Demography / 281

Fig. 1. Geographic location of the study areas

I

cifolia, Ocotea suaveolens (Lauraceae), Banara arguta (Flacourtiaceae), and Cecro- pia adenopus (Moraceae).

Study Population A total of 22 different howler groups were located in the Riachuelo area. Only

a few animals were captured and tagged, but most of the individuals could be individually recognized, at least when they were in their group. Study groups and group members were identified by the location where they were found, the pres- ence of ear tags or natural marks (scars, broken fingers, particular colors), and the age and sex classes of the individuals.

The sexes are dichromatic in the adults (males are black and females blonde). Subadult and juvenile males are darker than similar-sized females. There is a progressive darkening which occurs as males mature. Infants could be sexed as early as 1 month old, but for some individuals it was impossible to assign a sex until they were several months old.

Age classes were initially assigned following Rudran’s [19791 criteria for red howlers, but modifications were made after observing animals of known age.

Infants. Infants were light brown color; I assumed they were up to 1 yr. old. Juveniles (1 yr. to 3 yr. in females and 1 yr. to 4 yr. in males). Three sizes

were distinguished (small, medium, and large), males were larger than females in the same category. Females have a long and thin clitoris, vulvar lips are also thin, body color usually paler than adult females. Males become darker in a consistent pattern, beginning with the forehead, shoulders, hands, and feet and ending when they become homogeneously dark (darker than most of the adult females).

Subadults (3 to 4-5 yr. for females and 4 to 5 yr. for males). Female

TABLE I. Mean Weight (kg f 1 sd) of Wild Alouatta curuya (CAPRIM)

Adult males (n = 58) 6.42 f 1.147 Adult females (n = 117) 4.33 r?l 0.764 Juvenile males (n = 33) 2.36 f 0.968 Juvenile females (n = 33) 2.32 ? 0.652 Infants (n = 20) 0.68 2 0.203

genitalia begin to change; clitoris becomes shorter and broader, body size is still smaller than for adult females. Male size similar to adult females, with whitish testicles, coat almost all brownish black or black with golden shines (brown hairs still present in the dorsum), ventrally brown.

Adults (females after the first birth, about 4-5 yr.; males after 5 yr.). Females with clitoris hardly noticeable, broad vulvar lips with irregular pigmentation, signs of nursing. Body color blonde but with the back darker and grayish. Males entirely black, no brown in dorsal surfaces, orange testicles, ven- trally some brown hairs but less than subadults. Noticeably larger than females.

Body weights were obtained from captures performed by staff of CAPRIM (Argentine Primate Center) a t sites close to the study area (Table I).

Population Censuses Censuses in the Riachuelo began in May 1980 with two study groups. The

number of groups censused increased progressively to 22 by November 1984 (Fig. 2). Groups were counted monthly or bimonthly by walking a fixed transect through the forest patches. A complete census required about 2 weeks of field work. Trans- portation among forest patches and from the base building of CAPRIM was ac- complished with a Honda three-wheeler and a canoe. On each encounter with monkeys the group composition by sex and age was recorded and its location plotted on a map.

Ecological density, or the number of groups per area of suitable habitat [Eisen- berg, 19791, was estimated using the area of the forest patches where the groups were located. Biomass was estimated by assigning weights from Table I to each age and sex class. The weight for subadult males was assumed to be equal to adult females and that for subadult females was an average of juvenile and adult female weights.

Records were kept of 11 Riachuelo groups from early 1982 to November 1984. Life history diagrams of the groups were drawn from the census data showing the ontogenetic trajectories of individuals. Births, infant mortality, interbirth inter- vals, dispersals, and other parameters were calculated from these graphs. In July 1987 ten of the study groups were recensused.

Eleven groups were censused on Isla Guascara during June-August 1981. In this area, the subadult age class was not recognized and these individuals were lumped with large juveniles.

RESULTS Social Units and Differential Use of Habitat in the Riachuelo Area

Black howlers were found in bisexual reproductive groups of 3 t o 15 individ- uals (groups 1-15 and 19-22), as adult or subadult solitary individuals of both sexes, and in small unisexual or bisexual associations of two or four adult or subadult individuals which had not successfully reproduced (groups 16-18).

Group #

1 2 3 4 5 6 7 8 9

10 11 12 13 14 15 16 17 18 19 20 21 22

44 51 54 40 35 34 32 34 33 33 30 21 21 15 8 o * o * 2 20 14

o * 2

* means one contact.

Fig. 2. Periods of study of Riachuelo groups

A total of 425 of the 440 group locations corresponded to reproductive groups, and 404 of these group counts (95%) were located in patches of tall forest. Only 5% were found in low forest. All but two of the locations of extragroup associations (13 of remaining 15) were found in low forest patches. The exception was a small association that later became a reproductive group (group 10). Solitaries were found in both tall and low forest. The usual group locations in the forest patches are shown in Figure 3.

Population Density and Biomass Ecological density varied between 12.14 and 12.93 groups per sq km depending

on the set of groups considered (Table 11). As mean group size increased during the study, ecological density of individuals also increased from 0.80 to 1.15 individuals per hectare for a set of 9 groups. Density between forest patches did not vary, shown by comparing the density estimate from these 9 bisexual groups to one from a different set of 10 groups (1.04 and 0.97 ind. per ha, respectively) obtained by splitting the values of 19 groups from November 1984 into two sets (Table 11).

The crude density for the total 3,000-ha study area varied from 0.040 to 0.052 ind. per ha (4 to 5.2 ind. per sq km). Adding the solitaries and small associations from some patches of low forest and extrapolating to the total amount of low forest in the area, the crude density only increases to 5.7 individuals per sq km.

The resulting biomass figures for different censuses varied between 306 and 365 kg per sq km of tall forest.

On Isla Guascara, a total of 11 groups with 112 individuals occupied 40 ha of tall flooded forest at one end of the island. The ecological density was estimated to

284 I Rumiz

Fig. 3. Group location in the Riachuelo forest patches

be as high as 27.5 groups per sq km or 2.8 ind. per ha. Biomass was calculated to be 1,117 kg per sq km.

Group Sizes and Composition Group sizes in the Rio Riachuelo were smaller in JuneJuly 1982 (X = 6.4

ind.; Table 111) than in January 1984 (X = 8.4 ind.; Table IV) (Wilcoxon matched- pairs signed-rank test, T = 2, N = 10, P < .01, two tailed [Siegel, 19561). Group composition also changed during the study. Table V contains demographic param- eters for these groups on six different dates. Group size increased gradually from 1982 through January 1984, and then decreased slightly. The increase was due to newborns and the decrease is best explained by disappearances or mortality of all classes of individuals. A decrease in the adult sex ratio in 1984 was due to the immigration of 3 new males and the disappearance of 2 adult females. Sex ratio among juveniles favored females at the beginning but changed later toward a predominance of males. There are no apparent trends in the rest of the life history parameters.

Group size on Isla Guascara had a mean of 10.2 individuals but its size dis- tribution was rather bimodal, with either small (5 to 7 ind.) or large (9 to 15 ind.) groups (Table VI). Although group sizes were greater than for Riachuelo at the beginning of the study (Mann-Whitney U Test, U = 28.5, n l = n2 = 11, P < .05, two tailed; Siegel, 1956), the difference was not significant when Riachuelo groups became larger (U = 43, n l = n2 = 11, P > .lo, two tailed). Nevertheless, com- parisons between group composition on Isla Guascara and Rio Riachuelo result in contrasts for some parameters (see Table V). On the island there were more mul- timale groups and, therefore, more adult males per group (X = 2.7 males) than in

Caraya Howler Density and Demography / 285

TABLE 11. Ecological Density in the Riachuelo Area

n Area n Density Density Date (groups) (ha)" (ind.) gr.lsq km ind./ha

Jan. '82 9 69.60 56 12.93 0.80

Jul. '82 9 69.60 58 12.93 0.83 11 86.48 70 12.72 0.81

Jan. '83 9 69.60 66 12.93 0.94 11 86.48 78 12.72 0.90

Jul. '83 9 69.60 75 12.93 1.08 11 86.48 87 12.72 1.01

Jan. '84 9 69.60 80 12.93 1.15 11 86.48 92 12.72 1.06 17 140.00 147 12.14 1.05

Jun. '84 9 69.60 75 12.93 1.08 11 86.48 88 12.71 1.02 17 140.00 138 12.14 0.99

Nov. '84 9 69.60 73 12.93 1.05 11 86.48 86 12.72 0.99 17 140.00 140 12.14 1.00 19 150.00 151 12.67 1.01

"Accumulated area of forest patches used by combinations of 9, 11, 17, and 19 howler groups.

TABLE 111. Group Composition of 11 Riachuelo Groups in June-JuIy 1982*

Subad. L. Juv. M. Juv. S. Juv. Infants Group No. M F M F M F M F M F M F

~ ~ - - ~ Adults

1 1 3 1 1 2 1 2 1 1 1 3 1 2 1 2 4 1 2 1 1 5 1 3 1 1 6 1 2 2 1 2 1 7 2 2 2 1 1 8 2 2 1 1 1 9 2 1 1 1

10 1 1 11 2 3 1 1 1 1 1

Total 15 22 3 2 2 4 5 4 1 5 5 2 Mean 1.4 2.0 0.5 1.9 0.6

Total

9 3 6 5 6 9 8 7 5 2

10

70 6.4

*Subad. = subadults: L. = large; M. = medium: S. = small; Juv. = juveniles; M = males; F = females.

the Riachuelo (X = 1.4) but the adult sex ratio (1:1.40) fell within the range observed in the Riachuelo (1:1.29 to 1:1.78). Also, there were many more juvenile males than females and a lower proportion of infants and juvenile + infants to adult females on the island.

Demographic Changes in the Riachuelo Area Population trends. The sample of 11 groups showed a finite annual rate of

increase of 1.14 between JuneJuly 1982 and 1983, and 1.01 between 1983 and

286 / Rumiz

TABLE IV. Group Composition of 11 Riachuelo Groups in January 1984*

Subad. L. Juv. M. Juv. S. Juv. Infants _ _ _ _ _ _ _ - - _ _ _ Adults Group No. M F M F M F M F M F M F T o t a l ~~~ ~ ~ ~

1 1 3 1 1 1 2 1 1 11 2 2 2 1 5 3 1 2 1 2 1 7 4 1 2 1 1 1 1 1 8 5 1 3 1 1 1 3 10 6 1 3 1 1 2 1 1 1 2 13 7 1 2 2 1 1 1 2 10 8 1 2 1 1 1 1 7 9 2 1 1 1 1 1 7

10 1 2 2 5 11 3 3 1 1 1 9 Total 15 25 6 4 6 2 8 4 3 3 11 5 92 Mean 1.4 2.3 0.9 2.4 1.4 8.4

"Subad. = subadults; L. = large; M. = medium; S. = small; Juv. = juveniles; M = males; F = females

TABLE V. Demographic Parameters for 11 Groups From Isla Guascara and 11 Groups From Rio Riachuelo

Rio Riachuelo Isla Guascara Jun-Aug J u n J u l Jan J u n J u l Jan J u n J u l Nov

1981 1982 1983 1983 1984 1984 1984

Inf. born betw.dates 1nf.dead betw.dates Immigrations Emig. +deaths n = ind. Finite rate of increase Mean group size Density indiha One male to multimale

groups Adults to immatures Males to females Ad. males to

ad. females Juv. males to

juv. females Ad. females t o juv.

+infants Ad. females to infants

8 11 0 3 1 2 1 1

1.14 7.1 0.90

78

8:3

6 9 3 4 4 0 2 9

87 92 1.01

7.9 8.4 1.01 1.06

8:3 8:3

9 4 1 8

86 112 70 88

8.0 1.02

7:4

7.8 0.99

714

10.2

3:8 2.80

6.4 0.81

7:4

1:0.55 1:0.87 1:1.40

1:0.89 1:1.25 1:1.47

1:0.90 1:1.37 1:1.78

1:1.23 1:1.30 1:1.12 1:0.94 1:1.78 1:1.67

1:1.28 1:0.98 1:1.47

1:1.20 1:1.05 1:1.29

1:0.17 1:1.62 1:0.91 1:0.71 1:0.62 1:0.71 1:0.50

L0.95" 1:1.27 1:1.40 1:1.60 1:1.76 1:1.70 1:1.82

1:0.31 1:0.32 1:0.56 1:0.64 1:0.64 1:0.39 1:0.45

"Includes subadults as juveniles.

1984. The number of newborns (19) mainly explains the increase observed in the first 12-month period (Table V) because immigrations (3) were counterbalanced with infant mortality (3) and emigrations plus deaths (2). In the 2nd year, even though births continued steadily, disappearance of adults, emigration, and infant mortality decreased the population size. This also occurred during the final months of the study.

Caraya Howler Density and Demography / 287

TABLE VI. Group Composition of 11 Groups on Isla Guascara

Subadults + Adults juveniles Group

No. M F M F Infants Total

1 4 2 2 1 9 2 4 5 3 1 13 3 1 3 1 1 6 4 3 6 1 3 13 5 3 6 4 1 1 15 6 2 2 2 1 7 7 3 5 3 2 13 8 5 5 4 1 15 9 1 3 1 5

10 1 2 2 5 11 3 3 3 1 1 11 Total 30 42 23 4 13 112 Mean 2.7 3.8 2.5 1.2 10.2

There was a progressive increase in the proportion of immatures to adults and of juveniles + infants to adult females.

A census performed in July 1987 of ten identified groups revealed a similar number of individuals as in 1984 (68 and 69, respectively) without a significant difference in group size (Wilcoxon matched-pairs signed-ranks test, T = 9, N = 6, P > .05, two tailed). Proportions between adults and immatures in 1987 (Ad.: Imm. = 1:1.03; Ad.F:juv.+inf. = 1:1.27; Ad.F:inf. = 1:0.36) were similar to the ones obtained for the same ten groups in 1984 (Ad.:Imm. = 1:0.94; Ad.F:juv. + inf. = 1:1.29; Ad.F:inf. = 1:0.33).

Reproduction Seventy-four reliably dated births were recorded from 16 Ri- achuelo groups. Births occur throughout the year but with a peak in the dry season (June to August) (Fig. 4). Analysis of birth seasonality by the “direct method” [Caughley, 19771, for which I assumed 12 equal month-long periods, showed a mean in mid June with a standard deviation of 3 months and 13 days (variance almost 12 mo). Following Caughley, this scheme does not fit a birth pulse, but some seasonality appears evident.

The sex ratio of 64 young infants (34 males and 30 females) was not signifi- cantly different from 50:50 [Binomial test, z = 0.37, P = .35, Siegel, 19561.

Thirty-one females from 14 Riachuelo groups gave birth to 70 infants and 30 interbirth intervals (IBIS) were reliably measured (Table VII). For these females, the average birth rate was 0.89 infants per female per year considering the 31 females, while the mean IBI was 15.93 mo. (sd = 3.73) after surviving infants and 15.80 months (sd = 3.74) including infants that died. The shortest IBI (with a previous surviving infant) was 12 months.

Dispersal and disappearances. Males and females were seen to emigrate from suspected natal groups and become solitaries. In 11 Riachuelo groups, 4 adult and 2 subadult females disappeared and two of them (1 young adult and 1 sub- adult) were found later not far from their groups before being recorded as missing. Only one case of female “immigration” was confirmed when one adult female joined a pair of adults (male and female). Infants were born in this association resulting in a new group (group 10) of 7 individuals.

At least 4 adult and 4 subadult males disappeared from seven groups. Some of

288 / Rumiz

Number of births

14

12

10

8

6

4

2

0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 4. Monthly distribution of 74 births recorded in 16 groups from the Riachuelo area.

them left their groups when they became mature and one or more larger males were in the group. In the other cases the males left when adult males immigrated or “invaded” groups. At least 7 adult males joined 3 groups during 4 male inva- sions. Former resident males disappeared from the groups (3 cases) or coexisted with invaders (1 case). Fights during invasions and findings of solitary males with wounds suggested that residents were evicted.

The disappearance of juvenile individuals was noted, but their fate was un- known. Three juvenile males and three juvenile females disappeared from their natal groups. Natural mortality in adults and juveniles, even when suspected in some cases, was confirmed only once (one juvenile male died, unknown cause).

Of 43 births recorded in the 11 Riachuelo groups, 15 infants (35%) died. Two of them were confirmed cases of infanticide associated with male changes in groups 1 and 5 [Zunino et al., 19851. Three more infants disappeared from these groups after being observed with injuries. In group 11, four infants were missing on the dates of male changes or their disappearance coincidenced with observations of fights between males. The sample of dead infants (4 males, 5 females, and 6 un- sexed) did not suggest a particular trend of differential mortality by sex. Data of this sort were not collected for the island population.

DISCUSSION The study of the Riachuelo population confirmed some suspected demographic

and behavioral characteristics of black howler monkeys and provided possible explanations for the population features observed on Isla Guascara. Comparisons among the Riachuelo, Isla Guascara, and other howler populations allow for some generalizations and improve our understanding of howler demographics.

General Demography in the Riachuelo Area In the Rio Riachuelo, howlers may be found living in established groups, in

small extragroup associations, or as solitary individuals corroborating other re-

Caraya Howler Density and Demography / 289

TABLE VII. Infants Produced Per Female and Interbirth Intervals (IBIs) in the Riachuelo Area

Group Female Obs. period Infants born IBIs No. ID No. (months) per female (months)

1 1 44 3 15/22 2 33 2 19 3 40 2 19

2 1 51 2 20 3 1 53 3 22/26

4 1 40 4 14/12/13 2 50 4 i a / i 3 m

2 40 3 20/15 5 1 30 3 13/14

2 35 3 12“/14 3 34 3 16/17

6 2 34 3 7 1 32 3 15/13

2 30 3 12/12 a 1 34 2

2 34 2 21 9 1 33 2 12

10 1 17 2 14 2 21 2 13

11 1 30 2 2 30 2 3 30 1

12 1 21 2 2 21 1

13 1 21 1 2 21 2 3 21 2 4 21 2

14 1 15 1 2 15 2 3 15 1

Total 31 females 946 mo. 70 inf. 30 IBIs Mean 0.89 inf/female/v 15.8 mo.

15

_ _ _ _ _ _ _ _ _ ~

“First infant died.

ports for A. palliata, A. pigra, and A. seniculus [Crockett & Eisenberg, 19871. Solitaries are males and females that dispersed from their natal groups. These subadult or young adult individuals may join other established groups or try to form new ones to become reproductive. Additions of male immigrants into estab- lished groups are viewed as “invasions,” with fights between males and eviction or coexistence with residents. Infanticides and infant disappearances can occur asso- ciated with male changes, as reported for other howlers [e.g., Rudran, 1979; Clarke, 1983; Crockett & Sekulic, 19841. Female immigration in established groups was not confirmed, but I documented females joining small associations. This pattern was also reported for A. seniculus by Crockett [19841.

290 / Rumiz

Births occur throughout the year but show a peak in the dry season and a valley in the early wet season. A similar seasonal pattern was found in red howlers which may minimize unfavorable conditions at weaning time [Crockett & Rudran, 1987al. Sex ratio a t birth does not seem to depart from 5050, confirming the findings from other howler populations [Glander, 1980; Crockett & Rudran, 1987bl. Interbirth intervals (X = 15.93 mo, sd = 3.73) are shorter than ones recorded for Alouattupalliutu in Costa Rica [X = 22.5 mo, sd = 2.0; Glander, 19801 but not for A. seniculus in Venezuela [X = 17 mo, sd = 3.72; Crockett & Rudran, 1987bl. Data from captive A. carayu [Shoemaker, 19821 showed remarkably short intervals (7, 8, and 9 mo) with a previous surviving infant. These figures suggest a wide flexibility in the reproductive capacity of female howlers, which is maxi- mized under captive conditions. Data from the island or other habitats are not available, but I would expect that if resources abound, female howlers will maxi- mize reproduction and shorten interbirth intervals.

Group Formation in Riachuelo and Isla Guascara The two populations compared in this paper occupied different habitats and

demonstrated differences in density and group composition. Isla Guascara sus- tained higher population densities than Rio Riachuelo. Rumiz et al. [1986] argued that the island is a highly dynamic and productive environment where fast- growing trees are suspected of having little antiherbivore defenses and thus are high-quality food for an arboreal folivore. This kind of environment is continuously changing. Periodic floods bring large amounts of nutrients, and deposition of sed- iments continually enlarge the island downstream, providing a place for rapid colonization with fast growing trees without chemical defenses. This new habitat may become usable by monkeys in a very short time and populations may grow fast, but atypical high levels of the river may eventually erode parts of the island, sweeping the forest and the monkeys downstream. Occasional sustained high wa- ter levels may also kill many of the trees and abruptly modify food availability. All of this produces dramatic changes in black howler populations and, depending on historical events, a few “founders” may be found on one island at one time and a large high-density population on another.

In the Riachuelo area I found reproductive groups living in tall forest patches while small associations used lower-quality habitats. Several interactions between large and small groups suggest that large established groups usually displace small ones. An association that occupied a tall forest patch where no large group used to go later became reproductive. It appears that habitat availability in the Riachuelo area strongly limits the establishment of new groups because of its patchy configuration: groups fully utilize their forest patches whereas the inter- stices between home ranges usually consist of grassland. Therefore, if the best quality habitat is used by large groups, small associations cannot become repro- ductive and new groups are not formed.

At the high population density phase of the island, mean group size was larger than during the low population stages in the Riachuelo, agreeing with previous generalizations about density and group size in howler monkeys [Eisenberg et al., 1972; Eisenberg, 1979; Crockett & Eisenberg, 19871. However, not all the island groups were homogeneously large, and the distribution of group size was bimodal with either small or large groups. A long-term study of an increasing population of red howlers has shown that temporary associations tend to become established and reproductive, resulting in the formation of new groups [Crockett, 1984; Rudran, unpublished; Rumiz, pers. observ.] which are smaller than the older ones [Crock- ett, 19851. It is plausible that the large groups of the island represent the old

Caraya Howler Density and Demography / 291

established groups and the small groups are the recently formed ones, which are not yet old enough to have experienced recruitment. In this habitat, the existence of a nearly continuous forest allows the settlement of new groups in the suitable interstitial areas between home ranges of large groups.

Sex and Age Ratios in Riachuelo and Isla Guascara Adult sex ratio was similar in both areas but among juveniles plus subadults

more males were observed on the island. A preponderance of subadults and juve- nile males was also observed in the last census of the Riachuelo and in censuses of red howlers [Rudran, 1979; Rumiz pers. obs.]. This ratio may vary over time, even showing the reverse situation due to variations in sex ratio a t birth if the sample size is small, but there are reasons to believe that this difference is consistent over time. Females mature faster than males and therefore there is a greater probabil- ity of finding males in the juvenile and subadult age classes. A less probable reason may be that sexual dimorphism and food competition produce higher infant and juvenile mortality in females, as stated for macaques [Dittus, 19771, but there are insufficient data to test this.

However, differences in male-female emigration rates may also account for the wide difference between immature male and female numbers on the island. Males emigrate from natal groups as subadults or large juveniles. In the Riachuelo these individuals left the study groups and several were located later in other forest patches. The dispersal stage may be particularly risky for them because they are in unfamiliar habitats of lower quality food, and a poor diet appears to be an important cause of mortality when combined with diseases or injuries [Milton, 19821. Also they are more exposed to predators (domestic dogs in this study area) when moving on the ground between forest patches. Although females also dis- perse, and should be exposed to the same risks as males, females leave the natal groups at lower rates because there are more available positions for them in the groups (adult sex ratio favors females). On the island, dispersers cannot easily leave the area (howlers are known to swim, but it seems unlikely that they would venture to cross strong streams several hundreds meters wide such as the Parana River), and due to the high density they do not have to go far to monitor potentially receptive groups in familiar habitat. As a result, there are more dispersers around the established groups on the island and they are easier to find. As these groups were not monitored long-term and group members were not individually recog- nized, dispersers could have been recorded as members of the groups when they were actually peripheral to them. A similar situation may have happened in Pope’s [19681 study of another insular population of A. caraya. This was the only howler study where the adult sex ratio favored males, which was explained by the inclu- sion of a number of peripheral young adult males. Thorington et al. [1984] sug- gested that it was not a representative sample of the population because some females with infants were not captured. However, if part of Pope’s “adult I” males were considered as subadults [the small ones in the range of weight: 4.1 to 7.4 kg; Stahl et al., 19681 both insular populations would have similar agehex distribu- tions.

The Ad.:Imm. and the Ad.F.:juv. + inf. ratios were larger in the high-density population of the island than in the Riachuelo, suggesting a decrease in population growth. In the Riachuelo, however, there was a trend to decrease these proportions during the increase in population density (e.g., more juveniles per adult female), and a hypothetical high-density population at Riachuelo would not show the same age structure as on the island.

Proportions among adult females and immatures are often used to evaluate

292 i Rumiz

population trends in howler monkeys, but there have not been many opportunities to test them. Heltne, Turner, and Scott [19761, based on their “7 year model,” predicted that the La Pacifica howler population in Costa Rica would decline be- cause it had an Ad.F.:juv. +inf. ratio below 1:1.5. Further censuses by Clarke et al. [1986] showed that this population kept its density and structure for more than a decade despite a “distressed” picture. If Heltne et al.’s “11 year model” is used instead, La Pacifica’s and also the long-term stable Santa Rosa’s howler popula- tions fit the predicted female to immature ratios [Fedigan, 19861. The Riachuelo population had an Ad.F.:juv.+inf. ratio between 1:1.27 and 1:1.82, but instead of growing as expected according the 11 y model, it was the same size 3 years later. Female life span probably does not vary between howler species from 7 to 11 years, but changes in fecundity or mortality rates of immatures are more likely to occur. It is possible that mortality factors operate differentially by sex and age in differ- ent habitats and population densities, thus producing the observed variation in population structure. Reliable predictions about these demographic processes will only be available after more comparative long-term studies are completed.

CONCLUSIONS

howlers, particularly with A. seniculus: A. caraya shares demographic and behavioral features with other studied

a) Both sexes emigrate and form extragroup associations; b) Male invasions may lead to fights and infanticides; c) Births occur throughout the year but show a peak in the dry season; d) Sex ratio a t birth does not differ significantly from 5050; e) The Riachuelo population had IBIS similar to A. seniculus from the Vene-

zuelan llanos but shorter than A . palliata from the Costa Rican dry forest. In a fragmented habitat, the large established groups occupied the best forest

patches while small associations were restricted to lower quality habitat. It seems that small associations may become successfully reproductive only if better habitat is available.

Different populations living in habitats with features that may modify pat- terns of mortality, dispersal, and population growth show different demographic characteristics.

ACKNOWLEDGMENTS I conducted this study as a fellowship trainee of CONICET (Argentine Re-

search Council) at CAPRIM (Argentine Primate Center). Field expenses and equipment were covered by CAPRIM-CONICET and personal funds. I am grateful to Dr. Orestes J. Colillas and Dr. Rudy Rudran who encouraged and advised me during the undertaking of this project. The help of CAPRIM staff, especially Mr. S. Pitteri and Drs. A. Brown and G. Zunino, was of vital importance in the logistics and discussion of the ongoing project. Drs. K. Glander, J. Robinson, J. Whitehead, C. Crockett, and three anonymous reviewers provided insightful comments on different versions of the manuscript.

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