Interactions between tayras (<Emphasis Type="Italic">Eira barbara</Emphasis>) and red-handed howlers (<Emphasis Type="Italic">Alouatta belzebul</Emphasis>) in eastern Amazonia

Two tayras (Eira barbara) were observed attacking an infant red-handed howler (Alouatta belzebul) on an island in eastern Brazilian Amazonia, as a nearby adult male watched passively. In a separate incident, four tayras were seen attacking a subadult female on the ground. Tayras were also observed in the vicinity of the two howler study groups on a number of occasions over a 9-month period. During this same period, the two groups lost a third of their members, including infants and subadults, and the remains of six animals were found at the study site. While tayras were the only predators seen attacking the howlers, it remains unclear to what extent they were responsible for apparently high mortality rates in this high-density, isolated howler population.     

Survey of Helminth Parasites in Populations of <Emphasis Type="Italic">Alouatta palliata mexicana</Emphasis> and <Emphasis Type="Italic">A. pigra</Emphasis> in Continuous and in Fragmented Habitat in Southern Mexico

The 2 howler species that occur in southern Mexico, Alouatta palliata mexicana and Alouatta pigra are endangered, mainly as a result of habitat loss and fragmentation from human activity. Little is known about the gastrointestinal parasite communities affecting their populations, and lack of baseline information for populations of howler species in continuous forest habitats, makes evaluations of gastrointestinal parasite prevalence in populations in fragmented landscapes difficult. We report the results of a one-time broad survey of gastrointestinal parasites in fecal samples of individuals from several demographically stable populations of Alouatta palliata mexicana and A. pigra existing in continuous and/or protected forests. We further report similar data for populations of both species in human-fragmented landscapes. We detected 6 parasites for each howler monkey species, but only 3 of them (Trematode I, Controrchis biliophilus, Trypanoxyuris sp.) were common to both species. While parasitic prevalence in populations of both howler species was, in general, higher in the fragmented habitat than in continuous and/or protected forests. The difference is only marginally significant in Alouatta pigra. Some parasites (Coccidia and Strongylid) only appeared in populations in fragmented landscapes. Preliminary data suggest that adult males tended to have higher parasite prevalence values than those of adult females in both howler species. Parasite prevalence is associated to average group size, but not to population density in Alouatta pigra.     

Skeletal Pathologies in a Population of Alouatta palliata: Behavioral, Ecological, and Evolutionary Implications

We examined the pathological conditions in a sample of 200 skulls of Alouatta palliata recovered from Barro Colorado Island (BCI), Panama, to investigate the prevalence of disease and injury in a free-ranging monkey population. Forty-five individuals (22.5%) have some type of nondental pathological condition, indicating that illness and injury are relatively common in this population. Ten individuals, all older adult males, exhibit clear signs of antemortem trauma in the form of healed fractures. We attribute the trauma primarily to fighting, and its frequency (16.4% of adult males) contradicts previous assertions that BCI howlers are nonaggressive. Nine of the 37 scorable immature individuals (24%) have signs of a larval infestation, supporting the suggestion that ectoparasites play an important role in BCI howler mortality. Other pathological conditions in the sample include shifted muscle attachments, periostitis, arthritis, neoplasm, periapical abscesses, and facial deformity, as well as various dental abnormalities.     

Interspecific interaction and predator avoidance behavior in response to tayra (<Emphasis Type="Italic">Eira barbara</Emphasis>) by mantled howler monkeys (<Emphasis Type="Italic">Alouatta palliata</Emphasis>)

This paper reports the response of one howler monkey group (Alouatta palliata) to a group of potential predators, the tayra (Eira barbara). The apparently successful predator avoidance behavior of the monkeys was recorded in detail. We observed a group of four adult tayras moving around theAlouatta group displaying a species-typical aggressive behavioral pattern. The two adult females of the howler group successfully chased the tayras away by repeatedly moving closer to the mustelids and even following them until the predators moved off.     

Population Characteristics of Howlers: Ecological Conditions or Group History

We examined the relative importance of ecological parameters—habitat productivity and seasonality—and group history—episodic predation, disease, and sudden habitat deterioration—to explain variation in the density and group structure of howlers (Alouatta spp.). We use data from a census of Guanacaste National Park, Costa Rica, and a literature review characterizing 80 howler populations. In Guanacaste National Park both habitat type and degree of protection affect howler density and group structure. Howlers were found at the highest density and in the largest groups in areas of semievergreen forest, which ecological sampling indicates have the most consistent level of food production. Differences in density between the sector of the park that first received protected status and more recently protected areas may be due partially to the degree of protection the areas received. We test the prediction that howler density and group structure would be influenced by habitat productivity as indexed by rainfall. Average group size and sex ratios differ among species, but female-to-immature ratios do not. Considering all censuses at one site to be independent, there are significant interspecific differences in density, with Alouatta pigra occurring at lower densities than the other species. In spite of such variability, there is no relationship between annual rainfall and howler density, and rainfall had a variable effect on group size depending on the level of independence that was considered. While such ecological comparisons are unrefined, e.g., rainfall must be used as a surrogate for habitat production, the fact that so few relationships were documented suggests that factors other than the ecological factors considered here are responsible for the observed differences in population characteristics. We suggest that much of the variability in howler population characteristics is related to events occurring in the recent history of the groups, such as habitat alteration, hunting, food tree crop failure, and disease.     

Effective Solutions for Howler Conservation

All species of howlers are at risk due to habitat destruction. I review the three most serious threats to howler survival—agricultural disturbance, logging disturbance, and hunting—both in a general context and in species accounts. Withal, the adaptability of howlers has allowed them to be a widespread genus throughout Central and South America. Alouatta is especially adaptable due to its generalized folivorous diet. I discuss how this adaptability relates to survival in situations of habitat destruction. In addition, I examine howler preference for riverine habitats and their ability to capitalize on secondary forests and secondary growth. I take a practical approach, suggesting some solutions for species survival, which include habitat management and reintroductions. Successful conservation models highlighted are the Community Baboon Sanctuary in Belize, in which villagers manage their lands for the benefit of the black howler and for their own economic benefit from ecotourism, and a village-sustainable logging system in Quintana Roo, Mexico, which has reduced levels of deforestation while benefiting both villagers and howlers, as well as other wildlife. A successful translocation of black howlers in Belize in order to reestablish a viable population is also described. The paper concludes with further suggestions to encourage howler conservation.     

Geographic Distribution of Red Howlers (Alouatta seniculus) in Southwestern Brazilian Amazonia, with Notes on Alouatta caraya

We surveyed howler (Alouatta) populations at 36 sites throughout the Brazilian state of Rondônia, in southwestern Amazonia, using quantitative (line transect surveys) and qualitative (interviews) methods. We recorded the red howler (Alouatta seniculus) at only one- third of the sites, and the species was relatively rare at most of them, especially in comparison with sympatric atelids (Ateles chamek and Lagothrix cana). In addition to local discontinuities, Alouatta was absent from a wide area (possibly as much as 100,000 km²) of northern Rondônia, south of the upper Madeira river. This lacuna apparently contradicts the typical association of the species with flooded forest ecosystems, but the ecological factors that may underlie it remain unclear. Competition with sympatric atelids does not appear to be a significant factor anywhere within the study area. Also, there is no evidence to suggest that the distribution patterns are related to recent human colonization of the state. We collected indirect evidence of the presence of a second howler species – Alouatta caraya – at two sites in southern Rondônia, where they are associated with highland savanna habitats and gallery forests in the Guaporé grasslands.     

Infant–Nonmother Interactions of Free-Ranging Mantled Howlers (Alouatta palliata) in Costa Rica

Proximate and ultimate explanations of interactions between infants and nonmothers vary depending upon the relatedness of the interactors. We investigated interactions of infants and nonmothers from a 22-month continuous study and from the long-term monitoring of the mantled howler population of La Pacifica, Guanacaste Province, Costa Rica. Relatedness is low or absent in these mantled howler groups. Juvenile females appeared to practice care skills with older infants, but as most first infants died, they failed to benefit. Infant positive interactions with adults occurred with the mother and probable father. Other adult females behaved aggressively toward the youngest infants. Mothers were retentive of infants and responded negatively to these interactions, suggesting that they perceived them as threatening. Interactions with infants appear to reflect competition in groups of unrelated adults. A review of other populations of Alouatta palliata and other species of howlers indicate variability in social group size and suggest variability in intragroup relatedness. We suggest that further study will confirm that social behavior (including interactions with infants) will vary by resource availability (group size) and associated demographic patterns (male and female migration) that affect relatedness in howler social groups.     

Gastrointestinal parasites of Howler monkeys (Alouatta palliata) inhabiting the fragmented landscape of the Santa Marta mountain range,Veracruz, Mexico

In recent years populations of howler monkeys (Alouatta palliata) in southeastern Mexico have decreased substantially due to the transformation and loss of natural habitats. This is especially evident in the Santa Marta mountain range, Veracruz, Mexico where several studies have evaluated the impact of fragmentation on howler monkey populations in order to propose management programs for their conservation. The conditions generated by fragmentation likely change the rates of parasitic infection and could decrease howler survival. In this study, gastrointestinal parasite species richness, prevalence, and egg density of infection were determined in howler groups inhabiting five forest fragments at the Santa Marta mountain range. Two hundred and seventy‐eight fresh fecal samples were collected between October 2002 and April 2003. Three parasite species were found during the dry and the wet season in all forest fragments sampled: one unidentified species of Eimeriidae; Trypanoxyuris minutus (Oxyuridae); and Controrchis biliophilus (Dicrocoeliidae). Both the prevalence of T. minutus and infection density for all parasites differed between seasons and fragments (the largest fragment consistently differed from other fragments). Host density, distance to the nearest town, fragment size, fragment shape, and total basal area of food trees explained parasite prevalence, but each species had a different pattern. Although parasite richness was lower, prevalence and density were higher than values reported for howlers in conserved forests. These results suggest that the establishment of biological corridors and animal translocation programs must take into account the parasite ecology of each fragment to avoid higher infection rates and preclude potential consequent mortality. Am. J. Primatol. 72:539–548, 2010. © 2010 Wiley‐Liss, Inc.     

Recruitment of Black Howler Fruit Trees in Fragmented Forests of Northern Belize

We examined recruitment of trees whose seeds are dispersed by black howler monkeys (Alouatta pigra) in forest fragments within the Community Baboon Sanctuary in north-central Belize. In the fragments, most other large frugivores are absent and howlers dominate the large frugivore community. Consequently, we expected to observe an increased representation of howler fruit trees among the sapling community. To test this prediction preliminarily we observed howler feeding behavior for one year and conducted adult tree and sapling transects in 6 locations where howlers were present. We sampled a seventh site where howlers were absent for vegetation only. We found that in 4 of 6 sites there were proportionately fewer howler fruit saplings when compared to adult tree samples. However, when recruitment of howler fruit trees in the 6 sites was compared to a site where howlers were absent, 11 of 12 species had relatively higher recruitment. The lack of recruitment among howler fruit trees in general likely reflects differences in responses of individual species, as well as disruptions from human activities to natural processes within the forests. The observed lower recruitment patterns of howler trees suggest that over time, the abundance of the trees will likely decline and thus affect the foraging behavior and possibly survival of howlers in the fragmented forests.     

Survey of the black howler monkey,<Emphasis Type="Italic">Alouatta pigra</Emphasis>, population at the Mayan site of Palenque,Chiapas, Mexico

A survey of the population of the black howler monkey (Alouatta pigra) present at the Mayan site of Palenque was conducted during 2000. A total of 911 man/hours, spread over 112 days were spent surveying the 600 ha area of pristine forest at the site for howler troops. We detected the presence of 136 individuals of which 131 were members of 20 troops, the rest were 3 solitary adult males and 2 adult males travelling as a pair. Ecological density was estimated at 23 individuals/km². Mean troop size was 7.0 individuals and it ranged from 2–12 individuals; 60% of the troops were multimale. All sighting of howler monkeys were in evergreen rain forest and 75% were in trees ≥20 m in height. The reported densities and mean troop size are higher than those reported for the species in Guatemala and in central Quintana Roo, Mexico. The vegetation of the forest contains tree species reported to be used by species ofAlouatta in the Moraceae, Sapotaceae, Leguminosae, and Lauraceae plant families. Protection of a large perimeter area (ca 1700 ha) around the archeological site by the Mexican government ensures the conservation of the forest and of the black howler monkey population present at the site.     

Seed predation ofCariniana estrellensis (Lecythidaceae) by black howler monkeys,Alouatta caraya

Seed predation by howler monkeys is poorly documented. Here we report the seed predation onCariniana estrellensis (Lecythidaceae) fruits by the black howler monkeyAlouatta caraya in south-east Brazil during an intense dry season. This observation suggests that even non-specialized seed predators such as howlers can use seeds in critical periods of dry season.     

Mandible/basihyal relationships in red howler monkeys (Alouatta seniculus): A craniometrical approach

The morphological relationships between the cranium and basihyal of red howler monkeys (Alouatta seniculus) were analyzed based on measurements of 36 cranial and 3 basihyal dimensions and observations of the female specimen in spirits. In this study, 115 crania from 111 red howler monkeys and 4 mantled howler monkeys (Alouatta palliata) were used. The analyses from the standpoints of the correlation coefficients, principal component analysis, discriminant function analysis, age changes and sex differences were performed and the following results were obtained: (1) The cranial measurements closely related to the basihyal measurements were mandibular length, occipital breadth, facial length, ramus height, cranial base length, bigonial breadth and pr-i length. (2) Age changes for the mandibular measurements in males of red howler monkeys were remarkable, and, in particular, the development of the gonion toward posterior and lateral directions were characteristic. (3) The largest sex differences were found in the mandibular measurements of red howler monkeys among the Anthropoidea of seven genera compared. (4) The existence of a “cline” in the cranial measurements of the red howler monkey was recognized. (5) The inter-species differences in the crania between the red howler monkey and mantled howler monkey are obvious, metrically and non-metrically. Based on the results mentioned above, the morphological relationships between the mandible and basihyal in the red howler monkey are discussed.     

Mortality of Herring Eggs on Different Algal Substrates (Furcellaria spp. and Cladophora spp.) in the Baltic Sea – An Experimental Study

In the Baltic Sea, herring (Clupea harengus membras) spawns in the littoral zone, where its eggs are attached to algae or vascular plants. Field studies indicate that egg mortality can be very high (up to 100%) in eggs that are attached to red algae (Rajasilta et al., 1989, 1993). Because high mortality can be due to allelochemical effects of the algae, we studied the mortality of herring eggs on different algal substrates experimentally. Four types of substrates were tested: fresh Cladophora and Furcellaria, and Furcellaria that had decomposed six days or 23 days. The incubation time in the experiments was 3 days and incubation temperature 12–13 ^oC (ca. 700–800 h-degrees). The results were in accordance with observations made in field studies and indicated significant differences among the substrate types. In eggs attached to fresh Cladophora, mortality was significantly lower (mean=2.8%; n=20) than in those attached to Furcellaria, independently of the treatment of the algae. The highest values of mortality (mean=14.4%; n=20) were found in eggs attached to Furcellaria that had decomposed over a six days’ period. This suggested that Furcellaria contain some chemical substances, which can cause mortality in herring embryos and the effect seems to be dependent on the state of decomposition of the algae.     

Tool use by a red howler monkey (Alouatta seniculus) towards a two-toed sloth (Choloepus didactylus)

Among New World monkeys, spontaneous tool use and object manipulation are commonly descirbed inCebus species only. We report here an occurrence of tool manipulation by a wild male red howler monkey (Alouatta seniculus), observed using a stick to softly but repeatedly hit a two toed sloth (Choloepus didactylus) resting in the same tree. The ecological context of this unusual behavior for this quiet species generally showing very little manipulative propensity is discussed.     

Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus).

We monitored the birth patterns of sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus) during a 4‐yr period from October 1996 to August 2000 at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Brown howler monkey births (n = 34) occurred throughout the year, and birth frequencies did not differ between rainy and dry season months. The aseasonal birth patterns of the howler monkeys differed significantly from the dry season concentration and dry month peak in muriqui births (n = 23). We found no effects of infant sex or the number of females on interbirth intervals (IBIs) in our 10 howler monkey study troops. IBIs of brown howler monkeys averaged 21.2 ± 2.5 mo (n = 8, median = 21.0 mo), and were significantly shorter following dry season births than rainy season births. Their IBIs and yearling survivorship (74%) were similar to those reported for other species of howler monkeys, but yearling survivorship was much lower than that of muriquis (94%), whose IBIs were more than 12 mo longer than those of the howler monkeys. Our study extends comparative knowledge of birth patterns in Alouatta to a poorly known species, and provides insights into the different ways in which diet and life history may affect the timing of births in large‐bodied platyrrhines under the same seasonal ecological conditions. Am. J. Primatol. 55:87–100, 2001. © 2001 Wiley‐Liss, Inc.     

In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini,Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes

We hybridized whole human chromosome specific probes to metaphases of the black-and-red howler monkey Alouatta belzebul in order to establish chromosomal homology between humans and black-and-red howlers. The results show that the black-and-red howler monkey has a highly rearranged genome and that the human chromosome homologs are often fragmented and translocated. The number of hybridization signals we obtained per haploid set was 40. Nine human chromosome probes gave multiple signals on different howler chromosomes, showing that their synteny is disturbed in A. Belzebul. Fourteen black-and-red howler autosomes were completely hybridized by one human autosomal paint, six had two signals, three had three signals, and one chromosome had four signals. Howler chromosomes with multiple signals have produced 12 chromosomal syntenies or hybridization associations which differ from those found in humans: 1/2, 2/20, 3/21, 4/15, 4/16, 5/7, 5/11, 8/18, 9/12, 10/16, 14/15, and 15/22. The hybridization pattern was then compared with those found in two red howler taxa and other mammals. The comparison shows that even within the genus Alouatta numerous interchromosomal rearrangements differentiate each taxa: A. belzebul has six unique apomorphic associations, A. seniculus sara and A. seniculus arctoidea share seven derived associations, and additionally A. seniculus sara has four apomorphic associations and A. seniculus arctoideaseven apomorphic associations. A. belzebul appears to have a more conserved karyotype than the red howlers. Both red and black-and-red howlers are characterized by Y-autosome translocations; the peculiar chromosomal sex system found in the red howler taxa could be considered a further transformation of the A. belzebul sex system. The finding that apparently morphologically similar or even identical taxa have such extreme genomic differences has important implications for speciation theory and neotropical primate conservation. Am. J. Primatol. 46:119–133, 1998. © 1998 Wiley-Liss, Inc.     

Mortality in reared hydropsychid pupae (Trichoptera: Hydropsychidae)

Cases containing pupae of Hydropsychidae (Trichoptera) were collected from sampling-stations along the length of the Credit and Humber Rivers, Ont., and reared at 18°C. Mortality was high; about 33% of the cases produced adults. Up to 24% of collected cases had been infested with chironomid larvae. Within a station, emergence success and mortality due to chironomid infestation were about the same for the species of Hydropsyche Pictet present; Cheumatopsyche Wallengren suffered less chironomid-related mortality than Hydropsyche. There were significant between-station differences in chironomid-related mortality for H. sparna Ross, H. bronta Ross, H. morosa Hagen, and H. slossonae Banks. Chironomid-related mortality was lowest for pupae from upper Credit R. stations, highest for pupae collected from a lower Credit R. station. Pupae from all Humber R. stations suffered about the same amount of chironomid-related mortality. Chironomid infestation was significantly higher for prepupae than for pupae.     

Temporal variation in abundance of the egg predator Carcinonemertes epialti (Nemertea) and its effect on egg mortality of its host,the shore crab,Hemigrapsus oregonensis

An outbreak of the nemertean, Carcinonemertes epialti, was observed on Hemigrapsus oregonensis during October, 1982 at Campbell Cove, Bodega Harbor, California. Mean worm intensity (296 worms/crab) was the highest recorded for this nemertean egg predator on H. oregonensis. During the outbreak, male crabs were found to harbor more worms than both non-ovigerous and ovigerous females. Crab egg mortality was substantial; 83% of the ovigerous females experienced 75–100% brood mortality. The seasonal peak in worm abundance coincided with the seasonal low in crab reproduction at this locality. A method for estimating the impact of C. epialti on H. oregonensis natality was developed using crab size and fecundity, and worm prevalence and intensity. For a non-outbreak sampling period, a mean of 5.6% egg mortality was experienced by infested crabs for the period selected. Thus, brood mortality during the outbreak was much greater than that experienced at non-outbreak periods. Heavy fishing pressure on some commercially important crab species has been suggested as a possible factor inducing worm outbreaks and facilitating their continued persistence. These observations suggest that fisheries are not necessarily responsible for the outbreaks of nemerteans on commercially important crab species. However, fishing pressure may still be a sufficient condition to promote nemertean outbreaks.     

Selective mortality of a coral reef damselfish: role of predator–competitor synergisms

Phenotypic variability within cohorts of juvenile organisms can serve as the basis for selective mortality. Previous studies have demonstrated the important role that predators play in this process but not the impact of competitors on selective predation. We use a combination of lab and field studies to evaluate the effect of the presence of adult competitor damselfish (Dascyllus aruanus and Pomacentrus moluccensis; family Pomacentridae) on the selective mortality of newly-arrived (settled) lemon damselfish (P. moluccensis) by resident predator fishes (Pseudochromis fuscus Pseudochromidae and Cheilodipterus quinquelineatus Apogonidae). Lab trials consisted of mesocosm experiments in which the behaviour, mortality, and physiological condition (measured as lipid content) of surviving P. moluccensis settlers from each of three treatments: (1) predators absent, (2) predators present, and (3) predators and competitors present, were compared. The field study involved stocking newly settled P. moluccensis on natural bommies (patch reefs) which had either been subject to a partial removal of resident fish (predators and competitors) or left alone. Results indicated there was very strong condition-based selective mortality in both the lab and field trials. In both cases there was a strong positive relationship between mortality and the lipid content of surviving fish; implying low-condition fish were selectively removed. The mesocosm trials indicated that the strength of mortality as well as condition selectivity was higher when competitors were present than when they were absent. Behavioural observations in the mesocosm study suggest that attention by juvenile P. moluccensis to the movements and occasional chases of the competitors (especially D. aruanus) reduced their vigilance to the predators. These results suggest the important and interactive roles which condition of newly settled reef fish and interspecific competition can play in the outcomes of post-settlement predation. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.