The capuchin, the howler, and the Caatinga: seed dispersal by monkeys in a threatened Brazilian forest

Regeneration of the Brazilian Caatinga forest may be restricted by the naturally low diversity and density of fruit-eating animals, which has been aggravated by local faunal extinction induced by human activities. We made a preliminary evaluation of the potential seed-dispersal role of capuchin (Cebus apella libidinosus) and howler monkeys (Alouatta caraya) in Serra da Capivara National Park. The monkeys dispersed at least 26 species. Alouatta dispersed larger seeds than Cebus, and the two species apparently dispersed seeds in different local habitats. Seed dispersal by monkeys potentially makes a significant contribution to Caatinga regeneration.     

Mammal assemblages in forest fragments and landscapes occupied by black howler monkeys

Species assemblages in disturbed habitats vary as a function of the interaction between species requirements and the spatial configuration of the habitat. There are many reports accounting for the presence of howler monkeys in fragments where other mammals are absent, suggesting that they are more resilient. In the present study we explored this idea and predicted that if howler monkeys were more resilient to habitat loss and fragmentation than other mammals, mammal assemblages in fragments occupied by howler monkeys should include fewer species with decreasing amount of habitat (smaller fragment size and less habitat in the landscape) and increasing number of forest fragments. We explored these relationships by additionally considering the feeding and life habits of mammal species, as well as the isolation and proximity of each fragment to human settlements and roads. We sampled the presence of mammals in five fragments occupied by black howler monkeys (Alouatta pigra) in the Mexican state of Campeche. Through direct sights performed during 240 h in each fragment, we observed 23 species. At the landscape scale, higher fragmentation was associated with a decrease in herbivores, omnivores and total number of species. At the fragment scale semiarboreal, omnivore, and total number of species increased with increasing fragment size. This study supports the idea that howler monkeys are more resilient to forest loss and fragmentation than other native mammals, and our exploratory analyses suggest that the specific mammal assemblages that are found in fragments are related to both landscape and fragment scale spatial attributes, as well as with species-specific characteristics.     

Effects of forest fragmentation on the physiological stress response of black howler monkeys

Habitat loss and fragmentation can create severe environmental problems for forest species, and may ultimately lead to local population extinction. One mechanism that might play a role in this process is the physiological stress response of individuals, because animals that experience chronic stress might show reduced rates of reproduction and survival. In this study, we investigated whether black howler monkeys Alouatta pigra inhabiting forest fragments experienced greater physiological stress than those in continuous forest. Faecal cortisol metabolite levels were compared between monkeys inhabiting fragmented and continuous forests in Southern Mexico. The sex of the animals was taken into consideration, while activity patterns and aggressive events were also recorded to examine differences in behaviour and sociality. A chemiluminescent enzyme immunoassay was utilized to determine faecal cortisol metabolite levels. Our results showed that cortisol metabolite levels were higher in howler monkeys from forest fragments, and that they vary through time. Patterns of locomotion also differed between forest types, as monkeys from fragments travelled at higher frequencies, while monkeys from continuous forests performed more of their movements within tree crowns. There was no difference in the frequency of feeding, resting and social interactions between fragmented and continuous forest monkeys. Higher faecal cortisol metabolite levels in fragmented areas are likely the result of suboptimal environments and could have long-term adverse effects on monkey health, fertility and survival. We propose that faecal cortisol metabolite measurements can be a useful conservation tool for monitoring populations of long-lived species subsisting under suboptimal conditions.     

Male reproductive strategies in black and gold howler monkeys (Alouatta caraya)

Behavioral and demographic factors such as group size, social structure, dispersal patterns, and mating systems affect male reproductive success. In the present study, we analyze the relationship between social structure, genetic relatedness of adult males and offspring paternity in one population of Alouatta caraya inhabiting a continuous forest in Northern Argentina. After 14 months of behavioral studies and genotyping 11 microsatellites, we found that dominant or central males achieved greater mating success and fathered all the offspring conceived during our study in two multimale–multifemale groups (both including three adult males). Although skewed toward the dominant males, females copulated with almost all resident males and with extra group males. We found significantly fewer agonistic interactions between adult males in the group with fewer females and where males were more genetically related to each other (average relatedness r = 0.237; 0.015 int/ind/hr vs. r = 0.02; 0.029 int/ind/hr). Paternity was also analyzed in two other neighboring groups which also showed strong skew to one male over a 2‐year period. These results reveal that even though female black and gold howlers mate with many males, infants are typically fathered by one dominant male. Am. J. Primatol. 76:43–55, 2014. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

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.     

Demographic population structure of black howler monkeys in fragmented and continuous forest in Chiapas,Mexico: Implications for conservation

For wild primates, demography studies are increasingly recognized as necessary for assessing the viability of vulnerable populations experiencing rapid environmental change. In particular, anthropogenic changes such as habitat loss and fragmentation can cause ecological and behavioral changes in small, isolated populations, which may, over time, alter population density and demographic structure (age/sex classes and group composition) in fragment populations relative to continuous forest populations. We compared our study population of Endangered black howler monkeys (Alouatta pigra) in 34 forest fragments around Palenque National Park (PNP), Mexico (62 groups, 407 individuals), to the adjacent population in PNP, protected primary forest (21 groups, 134 individuals), and to previous research on black howlers in fragments in our study area (18 groups, 115 individuals). We used χ² and Mann–Whitney U tests to address the questions: (a) what is the current black howler demographic population structure in unprotected forest fragments around PNP? (b) How does it compare to PNP's stable, continuous population? (c) How has it changed over time? Compared to the PNP population, the fragment populations showed higher density, a significantly lower proportion of multimale groups, and significantly fewer adult males per group. The population's age/sex structure in the fragmented landscape has been stable over the last 17 years, but differed in a higher proportion of multifemale groups, higher density, and higher patch occupancy in the present. In the context of conservation, some of our results may be positive as they indicate possible population growth over time. However, long-term scarcity of adult males in fragments and associated effects on population demographic structure might be cause for concern, in that it may affect gene flow and genetic diversity. The scarcity of adult males might stem from males experiencing increased mortality while dispersing in the fragmented landscape, whereas females might be becoming more philopatric in fragments.     

Isolation,characterization and evaluation of 11 autosomal STRs suitable for population studies in black and gold howler monkeys Alouatta caraya

We identified 11 polymorphic microsatellite markers for Alouatta caraya. Three markers were isolated from an enriched genomic library of A. caraya (AC14, AC17, AC45), five were previously described in Homo sapiens (TGMS1, TGMS2, D5S117, D8S165, D17S804), and three were identified for Lagothix lagotricha (1110, 1118, 157). Forty‐eight individuals from one Argentinean population were genotyped, yielding heterozygosity values between 0.146 and 0.792. These markers provide an exclusion power of 0.922 when neither parent is known (0.992 when one parent is known) and are suitable for parentage analysis, population genetics and phylogeographical studies of A. caraya, the southernmost primate in the New World.     

Roaring rhythms in black howler monkeys (Alouatta pigra) of Belize

Roaring was recorded during 15-min intervals for 55 days from April 29 to July 14, 1981 in the area around Bermuda Landing, Belize. Roaring profiles were compiled to represent four three-week periods in which roaring was graphed against the time of day. Rates of roaring were also calculated for three troops. Results indicate a gradual change in the daily profile of roaring from dry to rainy season. The marked bimodality of roaring at dawn and dusk in the dry season changed to a more dampened bimodality with reduced dawn and dusk peaks and more roaring during the midday in the rainy season. This seems related to the decreased hours of sun and the amount of rain during the wet season. Additionally, literature on monkeys with long range vocalizations suggests that bimodal peaks in calling may be more prevalent in species which display territorial defense.     

Physiological and analytical validations of fecal steroid hormone measures in black howler monkeys

The measurement of hormones in fecal samples allows for the noninvasive assessment of the endocrine status of free-ranging primates. However, procedures and techniques for hormone analysis in feces must be validated, both analytically and physiologically. Few studies have addressed the endocrinology of black howler monkeys (Alouatta pigra). Due to its conservation status, direct handling of individuals from this species and invasive sample collection are highly regulated, and therefore traditional methods for the validation of hormone assays, such as pharmacological challenges, are not allowed. As a consequence, sometimes studies of the fecal hormones of free-ranging black howler monkeys do not report physiological validations and therefore the biological reliability of such measurements cannot be assessed. In order to stimulate future research with this species, the present study aimed at providing methodological bases for fecal endocrine monitoring. Specifically, we compared the validity of two immunoassays (radioimmunoassays, RIA; solid-phase chemiluminescent enzyme immunoassay, SPCEI) performed with commercial kits to measure cortisol, testosterone, estradiol, and progesterone; and demonstrate how the physiological functions of these steroid hormones can be determined through non-pharmacological validations. We found no differences between the analytical validity of RIA and SPCEI assays to measure cortisol and testosterone, whereas for estradiol and progesterone RIA showed better results. Concerning the physiological validation of our assays, we demonstrated that: (1) comparisons between pre- and post-stress situations may be used to assess cortisol response, (2) comparisons between females and males may be used to assess variation in testosterone levels, and (3) comparisons between pregnant and non-pregnant females may be used to determine variation in estradiol and progesterone activity. The analytical and physiological validations that we performed demonstrate that there are currently commercial kits that allow for correct endocrine monitoring of this species, and that there are non-pharmacological alternatives to assess the biological validity of hormone measurements.     

The role of seed dispersal in the natural regeneration of rain forest after strip-cutting in the Peruvian Amazon

Seed dispersal and forest regeneration were studied on a 30×150 m strip cleared by strip-cutting, a system of forest management designed for sustained yield (Hartshorn 1989), in high terrace rain forest in the Department of Loreto, Peru. After one year the strip was dominated by seedlings of a few bat- and bird-dispersed pioneer tree species (Cecropia spp., Melastomataceae, and Alchornea triplinervia); stump sprouts from cut trees and saplings that survived the clearing were less numerous. The density of saplings (>2 m in height) surviving the clearing was 903 per hectare; 94% of these survived the subsequent 18 months. About 30% of 417 stumps (>7.5 cm diameter at breast height) resprouted within 3 months, with an additional 10% sprouting in the subsequent 10 months. Sprouting frequency was greater for small stumps than large and varied greatly among plant families. Seed deposition over this year was much lower in the interior of the strip, both in species richness and numbers of seeds, than within the forest; strip edges were intermediate in richness and number. The decline in seed input from forest to edge to strip, both in species and in numbers of seeds, was most pronounced for bird-dispersed taxa (primarily Melastomataceae); bat- and wind- dispersed taxa were more evenly distributed. The similarity in bat species composition between the strip and nearby primary forest was higher than the similarity in bird species composition between these habitats, reflecting a failure of many forest bird species to venture into the strip. The predominance of Cecropia spp. and other pioneers of minimal commercial value in the regeneration question the sustainability of strip-cutting. Subsequent succession and future tree species composition on the cleared strip will depend not only on the survivorship and growth of sprouts, survivors, and seedlings, but also on responses of different seed-dispersing animal taxa to changes in the species composition and structure of the vegetation in the strip.     

Parasites of free-ranging black howler monkeys (Alouatta pigra) from Belize and Mexico

Parasites are important members of the ecological web within which an animal lives, and can be used as indicators of ecosystem health. However, few baseline parasitological data are available for free-ranging animals, particularly for the black howler monkey (Alouatta pigra). In this study a total of 283 fecal samples were collected from 50 individually identified A. pigra during 2003 and 2004 and examined for parasites. The samples were processed using standard quantitative centrifugation concentration techniques, with sugar and zinc sulfate used as flotation media. The slides were examined using bright-field and phase microscopy. Antigen capture enzyme-linked immunosorbent assays (ELISAs) were used to detect protozoa. Four parasites were detected: 1) Controrchis biliophilus (Dicrocoeliidae), 2) Trypanoxyuris minutus (Oxyuridae), 3) Giardia sp. (Hexamitidae), and 4) Entamoeba sp. (Endamoebidae). Controrchis biliophilus was detected in 80% (wet season) and 81% (dry season) of the A. pigra samples; Trypanoxyuris minutus was detected in 8% (wet season) and 27% (dry season) of samples; and Giardia sp. was detected in 40% (wet season) and 27% (dry season) of samples. For the first time, DNA from Giardia sp.-positive fecal samples was extracted from A. pigra. Alouatta pigra individuals that lived near human settlements in Belize were infected with Giardia duodenalis (syn. G. lamblia, G. intestinalis) Assemblages A and B. These results suggest that G. duodenalis is transmitted from people and/or domestic animals to A. pigra.     

Effects of black howler monkey (Alouatta caraya) seed ingestion on insect larvae

Fig (Ficus monckii) and laurel (Ocotea puberula) seeds were obtained from Alouatta caraya feces (ingested seeds) and from trees (noningested) in northeastern Argentina. Seeds were examined to detect the presence (infested) or absence (noninfested) of larvae. Sixty percent (N = 315) of noningested fig seeds were galls with insect larvae inside, while 23% (N = 331) were encountered in the ingested group. Eighty-two percent (N = 28) of noningested laurel seeds were infested, and only 19% (N = 63) of ingested seeds were infested. According to the present data, the insects' larvae are digested by howlers intaking animal protein, but the laurel seeds were not destroyed. Am. J. Primatol. 45:411–415, 1998. © 1998 Wiley-Liss, Inc.