Germination success of large-seeded plant species ingested by howler monkeys in tropical rain forest fragments.

PREMISE: Primates are important seed dispersers, especially for large-seeded (>1 cm long) tropical species in continuous and fragmented rainforests. METHODS: In three forest fragments within the Montes Azules Biosphere Reserve, southern Mexico, we investigated the effect of seed passage through the gut of howler monkeys (Alouatta pigra) on the germination rate and maximum germination (%) of native, large-seeded species. One group of howler monkeys, per fragment, was followed and fresh feces collected. Large seeds were removed to compare their germination success with non-ingested seeds of the same species collected underneath parent plants. RESULTS: Feces contained large seeds from seven tree species (Ampelocera hottlei, Castilla elastica, Dialium guianense, Garcinia intermedia, Pourouma bicolor, Spondias mombin, Trophis racemosa) and one liana species (Abuta panamensis). Except for G. intermedia, ingested seeds germinated significantly faster than non-ingested seeds, which had negligible germination. Ingested seeds of D. guianense, P. bicolor, S. mombin, T. racemosa, and A. panamensis had significantly greater germination, while G. intermedia had significantly lower germination and seed ingestion had no apparent effect for A. hottlei and C. elastica. CONCLUSIONS: In general, seed ingestion by howler monkeys confers faster germination compared with non-ingested seeds. Faster germination reduces predation probabilities and increases seedling establishment in forest fragments. Primate dispersal services contribute to germination heterogeneity within plant populations of old-growth forest species and to their persistence in forest fragments.

Cognitive maps in the wild: revealing the use of metric information in black howler monkey route navigation.

When navigating, wild animals rely on internal representations of the external world - called 'cognitive maps' - to take movement decisions. Generally, flexible navigation is hypothesized to be supported by sophisticated spatial skills (i.e. Euclidean cognitive maps); however, constrained movements along habitual routes are the most commonly reported navigation strategy. Even though incorporating metric information (i.e. distances and angles between locations) in route-based cognitive maps would likely enhance an animal's navigation efficiency, there has been no evidence of this strategy reported for non-human animals to date. Here, we examined the properties of the cognitive map used by a wild population of primates by testing a series of cognitive hypotheses against spatially explicit movement simulations. We collected 3104 h of ranging and behavioural data on five groups of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico, from September 2016 through August 2017. We simulated correlated random walks mimicking the ranging behaviour of the study subjects and tested for differences between observed and simulated movement patterns. Our results indicated that black howler monkeys engaged in constrained movement patterns characterized by a high path recursion tendency, which limited their capacity to travel in straight lines and approach feeding trees from multiple directions. In addition, we found that the structure of observed route networks was more complex and efficient than simulated route networks, suggesting that black howler monkeys incorporate metric information into their cognitive map. Our findings not only expand the use of metric information during route navigation to non-human animals, but also highlight the importance of considering efficient route-based navigation as a cognitively demanding mechanism.

Effects of variation in forest fragment habitat on black howler monkey demography in the unprotected landscape around Palenque National Park, Mexico.

Habitat loss and fragmentation are leading threats to biodiversity today, and primates are particularly vulnerable to anthropogenic habitat disturbance. However, few studies have examined how differential effects of variation in forest fragment characteristics on males and females in a primate population may affect demography and population persistence. We quantified the effects of variation in forest fragment characteristics on the within-fragment demography of black howler monkeys (Alouatta pigra) in forest fragments around Palenque National Park, Mexico, and how these effects differed between adult males and females. We quantified forest loss in the landscape between 2000 and 2017, and used a redundancy analysis to examine the effects of 15 variables quantifying fragment dimensions, forest composition and physical structure, and isolation on fragment population size and density, the proportion of adult males and females in the fragment population, and the mean number of adult males and females per group in 34 fragments (N = 393 monkeys). We hypothesized that (i) population size is positively correlated with fragment area, while population density is negatively correlated, and (ii) the composition of fragment populations results from differential effects of fragment variables on adult males and females. Forest cover decreased by 23.3% from 2000 to 2017. Our results showed a significant effect of fragment variables on population demography in fragments, accounting for 0.69 of the variance in the demographic response variables. Population size increased with fragment area and connectivity, while density decreased. Larger, less isolated fragments with better connectivity, characteristics indicative of abundant secondary growth, and those with more diverse vegetation but lower Simpson's evenness indices tended to have more adult females per group and a higher proportion of adult females in the population. In contrast, fragments that were largely similar in characteristics of forest composition and structure, but that were more isolated from nearby fragments, had more adult males per group and a higher proportion of adult males. These results may stem from black howler females preferentially remaining in natal groups and fragments when possible, and dispersing shorter distances when they disperse, while males may be more likely to disperse between fragments, traveling longer distances through the matrix to more isolated fragments. These differential effects on males and females have important conservation implications: if females are more abundant in larger, less isolated fragments, while males are more abundant in more isolated fragments, then to effectively conserve this population, both landscape connectivity and fragment areas should be maintained and increased.

From Mexico to Michigan and back: An international collaboration investigating primate behavior, ecology, and evolution from multiple perspectives.

Evolutionary research benefits form the integration of laboratory and field components to determine factors and processes that affect the evolutionary trajectories of species. Our shared interest in understanding hybridization with genetic admixture as a process that may impact social, behavioral, and ecological features of primates, brought us together in a collaborative project aimed at addressing how vocal variation in two species of howler monkeys in Mexico affects and is affected by hybridization. To achieve this goal, we joined our academic expertise in studying primate genetics, ecology, and behavior under different natural and experimental conditions. We took advantage of decades of experience studying and handing wild howler monkeys for translocation projects to safely sample and study wild populations for this project. Here, we describe the history of our collaboration highlighting how our different perspectives, academic realities, and individual strengths built the foundation for our successful collaboration. We also share our perspectives on how this collaboration opened up new academic venues, broadened our individual perspectives on the integration of different research approaches to address a complex topic, and allowed us to recognize the strength of international collaboration.

Molecular detection of Bifidobacterium spp. in faeces of black howler monkeys (Alouatta pigra).

BACKGROUND: Bifidobacterium genus are considered to be beneficial bacteria for their hosts; however, knowledge about the specific species that are part of the gut microbiome of howler monkeys is scarce. Polymerase chain reaction (PCR) is a useful technique for the identification of non-cultivable or difficult to grow bacterial species. With the goal of detecting species of the genus Bifidobacterium in black howler monkeys, we used PCR on DNA derived from faecal samples. METHODS: We collected and extracted DNA from 40 faecal samples. Using specific primers, we performed PCR and nested PCR to detect members of the Bifidobacterium genus and a subset of species: Bifidobacterium adolescentis, Bifidobacterium bifidum, Bifidobacterium infantis, Bifidobacterium longum and Bifidobacterium animalis subsp. animalis. RESULTS: 97.5% (39/40) of the samples were positive for Bifidobacterium spp. We found B longum in 100% of the analysed samples. CONCLUSIONS: This is the first report of B longum in black howler monkey faeces.

Integrating expert knowledge and ecological niche models to estimate Mexican primates' distribution.

Ecological niche modeling is used to estimate species distributions based on occurrence records and environmental variables, but it seldom includes explicit biotic or historical factors that are important in determining the distribution of species. Expert knowledge can provide additional valuable information regarding ecological or historical attributes of species, but the influence of integrating this information in the modeling process has been poorly explored. Here, we integrated expert knowledge in different stages of the niche modeling process to improve the representation of the actual geographic distributions of Mexican primates (Ateles geoffroyi, Alouatta pigra, and A. palliata mexicana). We designed an elicitation process to acquire information from experts and such information was integrated by an iterative process that consisted of reviews of input data by experts, production of ecological niche models (ENMs), and evaluation of model outputs to provide feedback. We built ENMs using the maximum entropy algorithm along with a dataset of occurrence records gathered from a public source and records provided by the experts. Models without expert knowledge were also built for comparison, and both models, with and without expert knowledge, were evaluated using four validation metrics that provide a measure of accuracy for presence-absence predictions (specificity, sensitivity, kappa, true skill statistic). Integrating expert knowledge to build ENMs produced better results for potential distributions than models without expert knowledge, but a much greater improvement in the transition from potential to realized geographic distributions by reducing overprediction, resulting in better representations of the actual geographic distributions of species. Furthermore, with the combination of niche models and expert knowledge we were able to identify an area of sympatry between A. palliata mexicana and A. pigra. We argue that the inclusion of expert knowledge at different stages in the construction of niche models in an explicit and systematic fashion is a recommended practice as it produces overall positive results for representing realized species distributions.

Elección diferencial de frutos en dos especies simpátricas de monos y murciélagos frugívoros en el sureste de México / Differential fruit choice in two simpatric monkey species and frugivorous bats in southern mexico

ABSTRACT In order to identify the role played by plant species as a food source in the fruit election of dispersing agents (Alouatta pigra Lawrence 1933, Atelesgeoffroyi Kuhl 1820 and frugivorous bats), we developed a study in dry tropical forests in Yucatan, Mexico. We recorded the fruits consumed by frugivorous bats using collectors and, for monkeys, we implemented the focal animal method. The number of fruits consumed by primates (A. pigra and A. geoffroyi) and bats were recorded, 342 and 386, respectively. It was determined that bats deposited fruits with some percentage of pulp, while monkeys contributed more with a fruits without pulp (pairwise LSD contrast p < 0.05). Among the variety of fruit species in the diet of primates, we detected that A. pigra chose mostly not an abundant species such as Enterolobium cyclocarpum Jacq. Griseb. (1860) instead of those more abundant (Manilkara zapota (L.) P. Royen (1953) and Brosimum alicastrum Sw. subsp. alicastrum C.C. Berg (1972)). The type of fruit and seed handling caused by primates would be more beneficial to seed germination than those applied by bats. Moreover, this election and fruit handling could depend on the characteristics of fruits and space-temporal availability of plant species as a food source.

RESUMEN Con el objetivo de examinar el papel que juegan las especies vegetales como fuentes alimenticias en la selección de frutos de agentes dispersores (Alouatta pigra, Ateles geoffroyi y murciélagos frugívoros), se realizó un estudio en selvas secas en el sureste de Yucatán, México. Se registraron los frutos consumidos por murciélagos usando colectores y, en el caso de los monos, se implementó el método de animal focal. El número de frutos consumidos registrados para ambas especies de primates y murciélagos fueron 342 y 386, respectivamente. Se determinó que los murciélagos depositaron frutos con pequeñas cantidades de pulpa, mientras que los monos contribuyeron mayormente con frutos totalmente despulpados (contrastes por pares LSD p < 0.05). Entre la variedad de especies de frutos en la dieta de los primates se detectó que A. pigra eligió frutos de las especies menos abundantes como Enterolobium cyclocarpum Jacq. Griseb. (1860) en vez de aquellas más abundantes (Manilkara zapota (L.) P. Royen (1953) y Brosimum alicastrum Sw. subsp. alicastrum C.C. Berg (1972)). El tipo de manejo de frutos y semillas causado por los primates sería más beneficioso para la germinación de las semillas que los aplicados por los murciélagos. Además, esta elección y manejo del fruto podría depender de sus características y la disponibilidad espacio-temporal de las especies de plantas como fuente de alimento.

New Entamoeba group in howler monkeys (Alouatta spp.) associated with parasites of reptiles.

Our knowledge of the parasite species present in wildlife hosts is incomplete. Protozoans such as amoebae of the genus Entamoeba infect a large variety of vertebrate species, including NHPs. However, traditionally, their identification has been accomplished through microscopic evaluation; therefore, amoeba species have not always been identified correctly. We searched for Entamoeba spp. using a fragment of the small subunit rDNA in free-ranging howler monkeys (Alouatta palliata and A. pigra) from southeast Mexico. One hundred fifty five samples were collected, with 46 from A. palliata and 109 from A. pigra and 8 of the total samples were positive. We detected a new clade of Entamoeba, which was separated from other described species but closer to E. insolita, as well as an unnamed sequence typically found in iguana species with low shared identity values (<90%). We designated this new clade as conditional lineage 8 (CL8) and we have shown that members of this group are not exclusive to reptiles.

The role of sex and age in the architecture of intrapopulation howler monkey-plant networks in continuous and fragmented rain forests.

We evaluated the structure of intrapopulation howler monkey-plant interactions by focusing on the plant species consumed by different sex and age classes in continuous and fragmented forests in southern Mexico. For this we used network analysis to evaluate the impact of fragmentation on howler population traits and on resource availability and food choice. A total of 37 tree and liana species and seven plant items (bark, immature fruits, flowers, mature fruits, immature leaves, mature leaves and petioles) were consumed, but their relative consumption varied according to sex and age classes and habitat type. Overall, adult females consumed the greatest number of plant species and items while infants and juveniles the lowest. For both continuous and fragmented forests, we found a nested diet for howler monkey-plant networks: diets of more selective monkeys represent subsets of the diets of other individuals. Nestedness was likely due to the high selectivity of early life stages in specific food plants and items, which contrasts with the generalized foraging behaviour of adults. Information on the extent to which different plant species and primate populations depend on such interactions in different habitats will help to make accurate predictions about the potential impact of disturbances on plant-animal interaction networks.

Female participation in collective group defense in black howler monkeys (Alouatta pigra).

Many group-living animals actively defend a home range against neighboring groups. In many of these societies, males are the primary participants during group defense, while female participation ranges from seldom to frequent. Among howler monkeys (Alouatta spp.), loud calls (i.e., howling) are often used in the context of intergroup spacing as a form of cooperative group defense. Males initiate and lead these howling bouts, but females occasionally participate as well. During a 28-month study, I examined social and ecological factors influencing the participation of adult females in naturally occurring howling bouts of five multimale-multifemale groups of black howler monkeys (A. pigra) at Palenque National Park, Mexico. I calculated the percentage of time each female participated during howling bouts for which the participation of all resident females could be recorded ≥80% of the time (N = 287). At least one female was observed to participate in 53% of the vocal displays. Female participation was significantly greater during howling bouts that were part of visual intergroup encounters compared to spontaneous calls or calls in response to nearby calls when there was no visual contact with rival groups. Female calling behavior was not influenced by the presence of infants vulnerable to infanticide or by the proximity to food resources. Nonetheless, in four of the five study groups, one female called significantly more than the other resident female(s), suggesting that these females played a special role within the group's social dynamics, not previously recognized for this species.

Primate extirpation from rainforest fragments does not appear to influence seedling recruitment.

Primates are important seed dispersers, especially of large-seeded tree species, but the impact that these animals have on seedling recruitment is unclear. Evidence suggests that forest regeneration might be disrupted in forest fragments in which primates were extirpated. We tested this hypothesis by assessing seedling recruitment in 3 forest fragments occupied (OF) by primates, 3 fragments unoccupied (UF) by primates, and 3 areas within a continuous forest (CF) in the Lacandona rainforest, Mexico. Species and stem densities of tree, palm and liana seedlings were recorded over 16 months. Individuals were classified according to dispersal mode: large-seeded animal-dispersed (LS), small- and medium-seeded animal-dispersed (SS), and abiotically-dispersed species (AD). We assessed the influence of primate presence, adult tree assemblage, and fragment spatial metrics (size, age, distance to nearest fragment, and distance to continuous forest) on seedling assemblages. We recorded 6879 seedlings belonging to 90 species, and 59 genera in 405 1-m(2) plots. Both seedlings and adults showed similar differences in species and stem densities of LS, SS and AD species among forest types, suggesting that seedling assemblages were strongly influenced by the adult assemblages. The recruitment of each LS species varied among study sites, but evidence supporting higher recruitment enhancement of these species in continuous forest and occupied fragments was weak. Distance to continuous forest was the unique fragment spatial metric related (negatively) to the recruitment of LS species. Thus, primate extirpation does not appear to disrupt seedling assemblages in the Lancandona rainforest. Nevertheless, we cannot reject the hypothesis that certain LS species such as Spondias radlkoferi may be affected by the extirpation of primates.

Seed source, seed traits, and frugivore habits: Implications for dispersal quality of two sympatric primates.

• Premise of the study: Frugivore selection of fruits and treatment of seeds together with seed deposition site are crucial for the population dynamics of vertebrate-dispersed plants. However, frugivore species may influence dispersal quality differently even when feeding on the same fruit species and, while animals disperse some seeds, others simply fall beneath the parent plant.• Methods: In southern Mexico, we investigated to see if within-species seed traits (i.e., length, width, weight, and volume) and germination success differed according to seed source. For five tropical tree species we obtained ingested seeds from two sources, howler monkey (Alouatta pigra) and spider monkey (Ateles geoffroyi) feces; and noningested seeds from two sources, the ground and tree crowns (with predispersed seeds used as control).• Key results: A principal components' analysis showed that traits of seeds ingested by howler monkeys differed from other sources while seeds ingested by spider monkeys were similar to noningested seeds. Howlers consumed on average the larger seeds in Ampelocera hottlei, Brosimum lactescens, and Dialium guianense. Both primate species consumed the smaller seeds in Spondias mombin, while no seed trait differences among seed sources were found in Spondias radlkoferi. For all five tree species, germination rate was greatest for seeds ingested by howler monkeys.• Conclusions: For the studied plant species, seed ingestion by howler monkeys confers higher dispersal quality than ingestion by spider monkeys or nondispersal. Dispersal services of both primate species, however, are not redundant and may contribute to germination heterogeneity within plant populations in tropical forests.

Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids.

Social differences between primate species may result from both flexible responses to current conditions or fixed differences across taxa, yet we know little about the relative importance of these factors. Here, we take advantage of a naturally occurring hybrid zone in Tabasco, Mexico to characterize the variation in social structure among two endangered howler monkey species, Alouatta pigra and A. palliata, and their hybrids. Work in pure populations has suggested that A. pigra females maintain closer proximity, exhibit higher rates of affiliation, and lower rates of agonism than A. palliata females, but we do not know what accounts for this difference. Using identical data collection and analysis methods across three populations, we first seek to confirm previously reported interspecific differences in social structure across all sexes. We next examine: (1) how female social relationships changed with ancestry (by comparing pure and hybrid individuals); (2) how female social relationships changed with group size (A. pigra have smaller groups than A. palliata); and (3) whether female social relationships differed between two taxonomic groups within a single forest fragment (thus controlling for ecological variation). We confirmed previously described species differences, including closer proximity among females than among males in all populations. We also found that smaller groups maintained closer proximity. However, even after accounting for variation in group size, A. pigra females had closer proximity and more affiliation than A. palliata females. Furthermore, differences between pigra-like and palliata-like hybrids paralleled differences between pure populations and persisted even after controlling for ecological variation. Together, our results suggest that flexibility cannot account for all of the social differences between A. pigra and A. palliata and indicate an important genetic component in primate social behavior.

Anotaciones de la ecología alimentaria de monos aulladores negros en un fragmento con condiciones de hacinamiento (Balancán, Tabasco, México) / Anotações sobre a ecologia alimentar de bugios num fragmento superlotado (Balancán, Tabasco, México) / Annotations on the feeding ecology of black howler monkeys in an overcrowded fragment in Balancán, Tabasco, México

Se describió el comportamiento de alimentación del mono aullador negro centroamericano (Alouatta pigra) en un fragmento de menos de una hectárea de selva húmeda perennifolia rodeada de pastizales de uso ganadero, árboles dispersos y huertos de mango en la región de Balancán (Tabasco, México). Objetivo: reportar la dieta y actividad del mono aullador negro en condiciones de hacinamiento durante el mes más lluvioso en Balancán, Tabasco, México. Materiales y métodos: las observaciones conductuales (81 h) se hicieron mediante la metodología animal focal de una tropa de A. pigra constituida por tres individuos (un macho adulto, un hembra adulta y un infante). Resultados: del tiempo total de observación, la alimentación representó el 15,97%, el descanso el 78% y la locomoción el 4,57%. En el área de estudio se registraron 14 especies de plantas, de las cuales 10 fueron consumidas por los monos aulladores. El 55% del tiempo de alimentación fue invertido al consumo de frutos, 27% a las hojas, 17% al tallo y 1% a los retoños. La especie de árbol más consumida fue Spondias mombin, con el 61% del tiempo invertido. Conclusión: al igual que otros estudios, se confirmó la tendencia alimentaria folívoro-frugívora del género Alouatta. Se provee información sobre la flexibilidad que tienen los monos aulladores negros para vivir y mantenerse en condiciones de extrema perturbación donde su hábitat es de 0,1 hectáreas con pocas especies de árboles para utilizar, lo que además obliga a los individuos a hacer uso del suelo para trasladarse. Palabras clave: Alouatta pigra, Dieta, Patrón de actividad, Frugivoría, Hábitat fragmentado...

Annotations on the feeding ecology of black howler monkeys in an overcrowded fragment in Balancán, Tabasco, México. We described the feeding behavior of Central-American black howler monkey (Alouatta pigra) in a fragment of less than one hectare of humid evergreen forest surrounded by grassland for livestock use, isolated trees and mango orchards, in the region of Balancán (Tabasco, México). Objective: To record the diet and activity of black howler monkeys in crowded conditions during the wettest month in Balancán (Tabasco, México). Methods and methods: The behavioral observations (81 h) were made using the focal animal methodology with an A. pigra troop made up of three individuals (1 adult male, 1 adult female and 1 infant). Results: Feeding time represented 15.97%, rest 78% and locomotion 4.57% of total time. In the study area we recorded 14 plant species, with 10 being consumed by howler monkeys. 55% of feeding time was devoted to the consumption of fruits, 27% to leaves, 17% to stems, and 1% to sprouts. Spondias mombin was the tree species most consumed, with 61% of the time invested on it. Conclusion: Like other studies, we confirmed the frugivore-folivore feeding tendency of the genus Alouatta. We provide information on the black howler monkey flexibility to live and maintain themselves in extreme perturbation conditions, where their habitat is 0.1 ha with few tree species to use, forcing individuals to move around the ground...

Anotações sobre a ecologia alimentar de bugios num fragmento superlotado (Balancán, Tabasco, México). Descreve-se o comportamento alimentar do bugio centro-americano (Alouatta pigra) num fragmento menor que 1 ha de floresta úmida perenifólia rodeada por pastos para uso do gado, árvores dispersas e pomares de manga na região de Balacán (Tabasco, México). Objetivo: Registrar a dieta e atividade do bugio em condições de superlotação durante o mês mais chuvoso em Balacán, Tabasco, México. Materiais e métodos: As observações de comportamento (81 h) se fizeram por abordagem animal focal de um grupo de A. pigra constituído por três indivíduos (um macho adulto, uma fêmea adulta e um infante). Resultados: Do tempo total de observação, a alimentação representou 15,97%, o descanso 78% e a locomoção 4,57%. Na área de estudo se registraram 14 espécies de plantas das quais 10 foram consumidas pelos bugios. O 55% do tempo de alimentação foi gasto para o consumo de frutas, 27% às folhas, 17% ao caule e 1% aos brotos. A espécie de árvores mais consumida foi Spondias mombin, com 61% do tempo investido. Conclusão: Assim como outros estudos confirma-se a tendência alimentaria folívora-frugívora do gênero Alouatta. Fornece-se informação sobre a flexibilidade que têm os bugios para viver e ficar em condições de extrema perturbação, onde seu habitat é de 0,1 ha com poucas espécies de árvores para seu uso. Forçando, além disso, aos indivíduos a usar o terreno para se deslocar...

Some observations on the present distribution and conservation of Alouatta and Ateles in Southern Mexico.

Some information on the past and present distribution of Alouatta and Ateles in southern Mexico and on the impact of habitat destruction on their future existence is presented. Three surveys of primate populations and forest habitats were carried out between 1981 and 1983 in southeastern Mexico. Rapid destruction of the forest is reducing the number of forested areas where Alouatta and Ateles can exist and co-occur. Illegal hunting of the two primates also contributes to their rapid decline. Alouatta and Ateles live a precarious existence in a few large and small islands of forest, and efforts are needed to set aside some of these areas as reserves so that their future survival is ensured.