Howling on the edge: Mantled howler monkey (Alouatta palliata) howling behaviour and anthropogenic edge effects in a fragmented tropical rainforest in Costa Rica

The function of long calling is a subject of interest across animal behaviour study, particularly within primatology. Many primate species have male‐specific long‐distance calls, including platyrrhines like the folivorous howler monkey (Alouatta spp.). Howler monkeys may howl to defend resources such as feeding trees or areas of rich vegetation from other monkey groups. This study tests the ecological resource defence hypothesis for howling behaviour in the mantled howler monkey (Alouatta palliata) and investigates how anthropogenic forest fragmentation may influence howling behaviour. More specifically, this study examines how howling bout rate, duration, precursors and tree species richness, DBH, and canopy cover vary in 100 m anthropogenic edge and interior forest zones at La Suerte Biological Research Station (LSBRS), a fragmented tropical rainforest in Costa Rica. Results show that tree species richness and canopy cover are higher in forest interior at this site, suggesting that monkeys should howl at greater rates in the interior to defend access to these higher‐quality vegetation resources. Overall, our results supported the ecological resource defence hypothesis. The main howl precursor was howling from neighbouring groups. Although howling rate did not differ between forest zones, howling bouts from forest interior were longer, had a greater number of howls per bout and were preceded by different precursors than howls from anthropogenic edge zones, including more howls from neighbouring groups. Our findings provide some of the first evidence for behavioural edge effects in primate vocal communication behaviour.     

Blood groups of the mantled howler monkey (Alouatta palliata).

Fifty-two howler monkeys were tested for their human-type A-B-O blood groups. All were group B, as shown by the presence of B and H in their saliva, and anti-A in serum. The B-like agglutinogen of their red cells is common to all New World monkey species tested, and is of different origin and significance than their true A-B-O blood group. Differences among the B-like agglutinogens of the red cells of howler monkeys, marmosets, rabbits and humans group B were demonstrated, and limited tests have also been performed to study the biochemical basis of the anti-B reactions.     

Grooming in the mantled howler monkey,Alouatta palliata Gray

Dominant individuals groom subordinates in the mantled howler monkey. This relationship is previously unreported for the species and is a characteristic that howler monkeys share with many birds and mammals.     

Mechanical defenses in leaves eaten by Costa Rican howling monkeys (Alouatta palliata)

Primate species often eat foods of different physical properties. This may have implications for tooth structure and wear in those species. The purpose of this study was to examine the mechanical defenses of leaves eaten by Alouatta palliata from different social groups at Hacienda La Pacifica in Costa Rica. Leaves were sampled from the home-ranges of groups living in different microhabitats. Specimens were collected during the wet and dry seasons from the same tree, same plant part, and same degree of development as those eaten by the monkeys. The toughness of over 300 leaves was estimated using a scissors test on a Darvell mechanical tester. Toughness values were compared between social groups, seasons, and locations on the leaves using ANOVA. Representative samples of leaves were also sun-dried for subsequent scanning electron microscopy and energy dispersive x-ray (EDX) analyses in an attempt to locate silica on the leaves. Both forms of mechanical defense (toughness and silica) were found to be at work in the plants at La Pacifica. Fracture toughness varied significantly by location within single leaves, indicating that measures of fracture toughness must be standardized by location on food items. Monkeys made some food choices based on fracture toughness by avoiding the toughest parts of leaves and consuming the least tough portions. Intergroup and seasonal differences in the toughness of foods suggest that subtle differences in resource availability can have a significant impact on diet and feeding in Alouatta palliata. Intergroup differences in the incidence of silica on leaves raise the possibility of matching differences in the rates and patterns of tooth wear.     

Non-visual senses in fruit selection by the mantled howler monkey (Alouatta palliata)

Primates - There is extensive knowledge about the visual system and the implications of the evolution of trichromatic color vision in howler monkeys (genus Alouatta) related to food selection;...     

Intestinal parasites in howler monkeys Alouatta palliata (Primates: Cebidae) of Costa Rica

Fecal samples of 102 howler monkeys (Alouatta palliata) from several sites of Costa Rica were studied for intestinal parasites. The zones studied were: Central Valley (San Ramón, Alajuela), Central Pacific (Chomes and Manuel Antonio National Park. Puntarenas), North Pacific (Palo Verde Park and Playa Potrero, Guanacaste). Chira Island in the Nicoya Gulf and Caribean area (Cahuita. Limón). Animals were anesthetized with dards containing Telazol in order to collect the fecal material; some monkeys defecated spontaneously and others by direct stimulation. Samples were studied in saline solution (0.85%) and a Iodine solution, or stained with Haematoxylin. The material was also cultured in Dobell culture medium to determine the presence of amoeba and flagellates. Strongvloides. Controrchis. Trypanoxyuris genera were found in 3.4% of the samples. In addition 16.7% to 80% of the animals showed protozoa infection with Endolimax, Entamoeba, Trichomonas and Giardia. It is discussed the relationships of parasite infection with environmental conditions, animal population and human presence, specially in the monkey conservation programs point of view.     

Visual detection and fruit selection by the mantled howler monkey (Alouatta palliata)

Howler monkeys (platyrrhini) have evolved routine trichromatic color vision independently from catarrhines, which presents an opportunity to test hypotheses concerning the adaptive value of distinguishing reddish from greenish hues. A longstanding hypothesis posits that trichromacy aids in the efficient detection of reddish-ripe fruits, which could be an advantage for the detection of the nutritional content of the fruit, such as sugars. In the present study, we assessed fruit visual conspicuity and selection based on color and sucrose content by wild mantled howler monkeys (Alouatta palliata) on Agaltepec Island, Mexico. We used colorimetry to classify dietary fruits as cryptic (greenish) or conspicuous (reddish) against their background leaves. Species-specific color models indicate that trichromatic howler monkeys should be more efficient in discriminating the conspicuous ripe fruits from leaves compared to detecting cryptic ripe fruits from leaves. We found howler monkeys consume more cryptic fruits compared to conspicuous fruits, and that they consume more unripe fruits than ripe fruits. The consumption (acceptance) of fruit was independent of sucrose content, and thus this disaccharide may not play an essential role in mantled howler food selection. Our findings suggest that routine trichromatic color vision may aid in the detection and discrimination of conspicuously colored fruits, but that the final decision whether to accept or reject a fruit probably involves the use of other senses in addition to vision.     

Exploration and play in howler monkeys (Alouatta palliata)

Exploration and play were observed in eight troops of howler monkeys (Alouatta palliata) containing 56 young and 95 adults. The behavior patterns of seven age classes are described. There was a clear trend for animals to spend less time in nonsocial exploration with increasing age, and for the frequency of social play to follow an inverted “U” pattern, peaking in the early juvenile stage at 15–30 min per day. The howlers' specialization for eating large quantities of difficult to digest plant matter affected their play: as the young became increasingly dependent on plant food around the infants stage, there was a shift in their playtimes to allow for the energy demanding activity of digestion. This and other aspects of howler behavior are related to a reinforcement theory of exploration and play.     

Rates of fermentative digestion in the howler monkey, Alouatta palliata (primates: ceboidea)

1. Caecal material of wild howler monkeys was analyzed by gas chromatography for evidence of fermentation activity and rates of production and absorption of volatile fatty acids. 2. Results showed a high rate of production of acetic acid and lesser production of propionic, butyric and isobutyric acids. The VFA content of the blood was increase in passage through the caecal vascular system. 3. We estimate that howler monkeys may obtain as much as 31% of their required daily energy from fermentation end products. 4. Energy rich fatty acids may be of particular importance to howlers when they are living on diets high in leaves, which have high cell wall contents and low contents of nonstructural carbohydrates.     

Patterns of infection by intestinal parasites in sympatric howler monkey (Alouatta palliata) and spider monkey (Ateles geoffroyi) populations in a tropical dry forest in Costa Rica

In primate populations, endoparasite species richness and prevalence are associated with host traits such as reproductive and social status, age, sex, host population density, and environmental factors such as humidity. We analyzed the species richness and prevalence of intestinal parasites in two sympatric primate populations, one of Alouatta palliata and one of Ateles geoffroyi, found in a tropical dry forest in Costa Rica. We identified three species of intestinal parasites (Controrchis sp., Trypanoxyuris sp., and Strongyloides sp.) in these two primate species. We did not find any differences in species richness between the primate species. However, the prevalences of Controrchis sp. and Trypanoxyuris sp. were higher in Alouatta palliata. Similarly, males and lactating females of Alouatta palliata showed higher Controrchis sp. prevalences. We did not observe any differences in parasite richness and prevalence between seasons. Infectious diseases in endangered primate populations must be considered in conservation strategies, especially when defining protected areas.     

Longitudinal Assessment of Immature-to-Adult Ratios in Two Groups of Costa Rican Alouatta palliata

We used immature-to-adult female ratios (IFR), which indicate replacement rates, to assess changes in and viabilities of nonhuman primate groups and populations. Heltne et al. (1975) concluded that the howling monkey (Alouatta palliata) population at La Pacifica (Guanacaste, Costa Rica) was declining, as the IFR was <1.5, the ratio thought needed for a sustainable population. Our population surveys of 1984, 1991, and 1998 revealed that the number of monkeys in the population was stable, but the number of groups had increased and mean group size decreased. To examine these group-level changes, we present the IFR and immature-to-adult (IAR) ratios for La Pacifica Groups 2 and 18, which we have studied longitudinally for 18 and 10 years, respectively. Group 2 was larger than Group 18, but both groups showed similar mean IFRs for the study periods. The mean IFR for each group exceeded the population IFR. The annual IFRs varied more in the smaller group than in the larger group, and the IARs for these groups varied more than the IFRs did. All annual IFRs in the groups were below the hypothesized critical value of 1.5. Given these group and population values, we examined this critical IFR value with respect to mantled howler life history characteristics, particularly interbirth intervals and juvenile emigration, both of which preclude ratios 1.5, and compared the La Pacifica mantled howler population ratios with those of other populations. Group size, in conjunction with these ratios, might be more predictive of sustainable groups and populations.     

Parasitic infections of three Mexican howler monkey groups (Alouatta palliata mexicana) living in forest fragments in Mexico

In order to better understand how patterns of parasitism in howler monkeys are affected by forest fragmentation, we carried out a 1 year survey of gastrointestinal parasites in fecal samples from three groups of Mexican howler monkeys inhabiting different forest fragments in the Los Tuxtlas Biosphere Reserve, Mexico. The study groups were chosen because the conditions in which they lived suggested a potentially negative gradient for parasite richness and a positive gradient for levels of parasitism. We report for the first time the presence of Entamoeba coli in Alouatta palliata mexicana and of hookworms (Family Ancylostomidae) in A. palliata. A reduction in home range size and an increase in disturbance was associated with a loss of parasite richness, which in general was high. Parasite prevalence and the proportion of contaminated samples in which each parasite taxon was present was also high in general and there were no differences between groups. A factor related to the generally high levels of parasitism in our study groups could be the high humidity in the study area, because this favors the survival of parasitic free forms and increases the chances of infection. This would also account for the tendency towards higher levels of parasitism observed in the rainy season. Finally we did not find a pattern relating sex and parasitism.     

Behavioural development of howling monkey twins (Alouatta palliata) in Santa Rosa National Park,Costa Rica

Twins born to a young female howling monkey in Santa Rosa National Park, Costa Rica were observed during the first 96 days of their life. The comparison of their development to that of single infants and the comparison of the behaviour of the mother of the twins to that of mothers of single infants revealed few differences. However, qualitative observations suggests that high costs are associated with maternal care of infant twins. The mother had difficulty carrying both infants and was the only female observed to become sick during the study. Increased costs of lactation were not compensated for by an increase in foraging time. It would seem that howling monkey mothers possess a maternal care system which is capable of providing suitable care to twins. However, the costs on the mother of raising twins is suggested as a factor selecting for a litter size of one.     

Natural selection on molar size in a wild population of howler monkeys (Alouatta palliata)

Dental traits have long been assumed to be under selection in mammals, based on the macroevolutionary correlation between dental morphology and feeding behaviour. However, natural selection acting on dental morphology has rarely, if ever, been documented in wild populations. We investigated the possibility of microevolutionary selection on dental traits by measuring molar breadth in a sample of Alouatta palliata (mantled howler monkey) crania from Barro Colorado Island (BCI), Panama. The age at death of the monkeys is an indicator of their fitness, since they were all found dead of natural causes. Howlers with small molars have significantly decreased fitness as they die, on average, at an earlier age (well before sexual maturity) than those with larger molars. This documents the existence of phenotypic viability selection on molar tooth size in the BCI howlers, regardless of causality or heritability. The selection is further shown to occur during the weaning phase of A. palliata life history, establishing a link between this period of increased mortality and selection on a specific morphological feature. These results provide initial empirical support for the long-held assumption that primate molar size is under natural selection.     

Limited genetic diversity in the critically endangered Mexican howler monkey (Alouatta palliata mexicana) in the Selva Zoque,Mexico

The Mexican howler monkey (Alouatta palliata mexicana) is a critically endangered primate, which is paleoendemic to Mexico. However, despite the potential significance of genetic data for its management and conservation, there have been no population genetic studies of this subspecies. To examine genetic diversity in the key remaining forest refuge for A. p. mexicana, the Selva Zoque, we amplified full-length mitochondrial control region sequences (1,100 bp) from 45 individuals and found 7 very similar haplotypes. Haplotype diversity (h = 0.486) and nucleotide diversity (π = 0.0007) were extremely low compared to other Neotropical primates. Neutrality tests, used to evaluate demographic effects (Tajima’s D = ?1.48, p = 0.05; Fu’s F _s = ?3.33, p = 0.02), and mismatch distribution (sum of squares deviation = 0.006, p = 0.38; raggedness index = 0.12, p = 0.33) were consistent with a recent and mild population expansion and genetic diversity appears to be historically low in this taxon. Future studies should use a combination of mitochondrial and nuclear markers to fully evaluate genetic diversity and to better understand demographic history in A. p. mexicana. These studies should be undertaken throughout its geographic range in order to evaluate population structure and identify management units for conservation. Due to the limited distribution and population size of A. p. mexicana, future conservation strategies may need to consider genetic management. However, a more detailed knowledge of the population genetics of the subspecies is urgently recommended to maximise the conservation impact of these strategies.