Introduction

Among primates, only the five genera of the family Atelidae (Alouatta, Lagothrix, Oreonax, Brachyteles and Ateles) have fully prehensile tails. Numerous studies (e.g., Mendel, 1976; Gebo, 1992; Bergeson, 1998; Lawler and Stamps, 2002) have shown that prehensile tails aid in locomotion, help to maintain balance while resting or sleeping, especially on smaller branches, and improve the efficiency of foraging by enlarging the monkey's feeding sphere.

Howling monkeys use their fully prehensile tails from birth, and infants often wrap their tails around the base of their mothers' tails for extra security, especially while traveling (Baldwin and Baldwin, 1978). Prehensile tail-use continues in older, more independent infants and juveniles, particularly during play and environmental exploration. Adult howlers also use their tails in most activities, especially foraging and traveling. However, activity budgets differ greatly between adults and immatures, with the latter being much more active.

This study addresses the age-related differences in tail-use by mantled howling monkeys (Alouatta palliata). Many previous studies have focused on the positional and postural behavior of howling monkeys (e.g., Bicca-Marques and Calegaro-Marques, 1993; Estrada et al., 1999; Gebo, 1992; Lawler and Stamps, 2002), but none has focused on age as an independent variable, and only one article (Wheeler and Ungar, 2001) addressed sex differences. Many of these studies have used the same independent variables, such as the size and type of substrate, the monkeys' location in the trees, and general activity, but the dependent variables differ greatly across reports.

Methods

The study was carried out at the Ometepe Biological Field Station, Isla de Ometepe, Nicaragua (11°24′N, 85°50′W) at the beginning of the wet season, 4–22 July 2004. This tropical, semideciduous, dry forest has many groups of mantled howling monkeys, Alouatta palliata, at three main sites: Beach Forest, Spider Forest, and Volcano Forest. The latter two are fragmented and crosscut by agricultural fields or trails, while Beach Forest is an isolated fragment (about 1 ha) bounded by Lake Nicaragua and the main road on the island. Howlers come to the ground to cross this road, but were not seen doing so during this study. For more details of the study site, see Garber et al. (1999) and Winkler et al. (2004).

The study had two parts: an extensive nine-day period in which six groups (five in Spider Forest, one in Volcano Forest) were observed, and an intensive six-day period in which the single group in Beach Forest was observed. This yielded 10 data-collection days with over 53 contact hours and over 22 hours of data. Seventy samples (700 minutes of data) and 65 samples (650 minutes of data) were collected in the first and second periods, respectively. The groups varied in their composition but generally had 2– 4 adult males, 3– 6 adult females, 1– 4 juveniles, and 0 – 2 infants.

Instantaneous, focal-subject sampling at 15-second intervals was used over 10-minute sampling periods. Individuals were chosen at random, so that no subject was the focus of two samples in a row. Data were collected on adults and immatures, but only adults could be sexed. If the focal-subject was lost from view for over a minute, the sample was dropped; if the monkey was out of sight for less than a minute, it was noted on the data sheet, and the behavior recorded for that period was the last seen behavior for that subject. All observations occurred when the monkeys were in the trees, usually at 10–20 m; binoculars were occasionally used.

For each sample, I recorded the starting time, one of the four general behavioral contexts (Table 1), size of substrate, and location in the canopy. Travel for dependant infants was recorded when the mother carried them them dorsally or ventrally while traveling herself. Data were analyzed as rates (the frequency of scans per sample) for both immatures and adults. These numbers were then compared using a binomial test (two-tailed, α= 0.05).

Table 1.

Behavior variables recorded.

Results

Adults used their tails most while feeding on terminal branches and resting, and in both contexts used their tails more than immatures did (Table 2). Immature howlers used their tails most when playing, followed by resting and feeding. Adults were not recorded playing.

Table 2.

Rates (scans/sample) in four contexts of five behavioral categories.

Sixteen of 20 combinations of context and tail-use showed differences between adults and immatures; of these, immatures had greater rates than adults for 12 categories (n = 16, x = 4, p = 0.038). Rates of tail-use for immatures did not differ from adult rates for four of 20 combinations. Within contexts and across tail-use categories, the only statistically significant difference between immatures and adults was in play (n = 5, x = 0, p = 0.31), for the simple reason that adults never played.

Neither adults nor immatures rested by hanging by their tails. Similarly, Tail-Forelimb Suspension was never seen in adults and was seen only in juveniles during play. Both immatures and adults preferred to use Tail-Wrap during resting, feeding, and travel, and this is the most common use of the tail.

Discussion

Howlers are habitual inhabitants of the uppermost canopy and spend most of the day resting. This behavior likely reflects the mostly folivorous diet of howlers that requires them to spend much time digesting large amounts of lowquality plant material, making them more sedentary and less socially active than many other species (Baldwin and Baldwin, 1978). Our results show a clear difference in the activity budget and tail-use of immatures and adults. While playing, immatures exhibited a wide range of tail-use but most often hung only by their tails. This confirms previous findings that as howler infants mature into more skillful juveniles, they spend more time playing while hanging by the tail, which allows them to grapple with a play partner from any angle with less effort than a sitting animal expends (Baldwin and Baldwin, 1978). Their play allows young howlers to gain motor and behavioral experience that may later be helpful for hanging from small branches while they eat and for learning how to use their tails efficiently for other purposes, such as locomotion, resting, or sleeping.

While feeding, juveniles hung by their tails more often than adults, but showed less tail-use overall. The former result agrees with findings by, for example, Bicca-Marques and Calegaro-Marques (1993), who recorded that smaller individuals use an extended reach gained by hanging more often, making them more competitive with larger individuals. On the other hand, immatures often failed to use their tails more than adults, especially when traveling or resting. One might think that inexperienced young howlers would be cautious, and so use their tails for extra support and security. Their low rate of tail-use may be because immatures are uncertain as to what they can do with their tails, while still acquiring behavioral experience and knowledge.