The Experts below are selected from a list of 360 Experts worldwide ranked by ideXlab platform
Alejandro Estrada - One of the best experts on this subject based on the ideXlab platform.
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cognitive maps in the wild revealing the use of metric information in Black Howler monkey route navigation
The Journal of Experimental Biology, 2021Co-Authors: Alejandro Estrada, Miguel De Guinea, Anneisola K Nekaris, Sarie Van BelleAbstract: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.
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socially mediated overlap in vocal interactions between free ranging Black Howler monkeys
American Journal of Primatology, 2021Co-Authors: Alban Lemasson, Alejandro Estrada, Margarita Brisenojaramillo, Melissa Berthet, Veronique BiquandAbstract:"Conversation rules" such as overlap avoidance and coordinated overlap have been reported in nonhuman animals, and seem to be adaptive responses to the requirements of social life. Some species display both patterns in an apparently flexible way, but the social factors mediating their respective usage remain poorly documented. We investigated the potential social factors guiding the usage of these temporal rules during collective howling in six free-ranging groups of Black Howler monkeys (Alouatta pigra). First, we found that adult males' vocalizations rarely overlap those of other callers while most adult females' calls overlap other members' calls, especially that of other females. Second, whereas some call types (notably affiliative calls) are typically emitted without overlap, roars (agonistic loud calls) overlap more frequently. Third, coordinated overlap is more frequent during intergroup competition. Our findings support the hypothesis that overlap avoidance and coordinated overlap are two different (here sex-related) vocal alliance social behaviors, at least for some nonhuman primates. More comparative investigations are now needed to explore further their evolutionary trajectories in this lineage.
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effects of variation in forest fragment habitat on Black Howler monkey demography in the unprotected landscape around palenque national park mexico
PeerJ, 2020Co-Authors: Keren Klass, Sarie Van Belle, Alvaro Camposvillanueva, Fernando Mercado Malabet, Alejandro EstradaAbstract: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.
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demographic population structure of Black Howler monkeys in fragmented and continuous forest in chiapas mexico implications for conservation
American Journal of Primatology, 2020Co-Authors: Keren Klass, Sarie Van Belle, Alejandro EstradaAbstract: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.
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The Influence of Loud Calls on Intergroup Spacing Mechanism in Black Howler Monkeys (Alouatta pigra)
International Journal of Primatology, 2019Co-Authors: Sarie Belle, Alejandro EstradaAbstract:Long-distance vocalizations form an integral part of intergroup spacing mechanisms. The decision to approach, retreat, or ignore loud calls of neighboring groups might be influenced by resource availability, location in the home range, presence of fertile females or infants, or differential resource-holding potentials, and can alter intergroup encounter rates. During a 19-mo study (February 2016–August 2017), we examined navigation decisions relative to neighbor’s loud calls for five groups of Black Howler monkeys ( Alouatta pigra ) in Palenque National Park, Mexico. Study groups encountered any of their neighbors at a mean rate of one every 3.5 days and the same neighbor at a mean rate of one every 16.7 days, which was significantly more frequent than would be expected based on a simulation model that randomized observed daily paths. These results are consistent with mutual attraction. Based on 368 travel bouts relative to nearby (50–300 m) calls of neighbors, study groups were more likely to approach calls of neighbors than would be expected by chance, but only when neighbors were close by (50–150 m), suggesting that the imminence of threat by opponents played a role. Of the nine social and ecological predictor variables considered, availability of ripe fruits and of flowers was an important driver of their navigation choices and groups were more likely to move toward neighbors’ calls when ripe fruits were scarce and to move away when flowers were abundant. We found no evidence that the presence of fertile females or unweaned infants influenced navigation decisions. Nor did relative competitive abilities of opposing groups, measured as numeric superiority in group size or male group size, affect navigation decisions. This study provides evidence that Black Howler monkeys incorporate information on resource availability and neighbors’ current locations into their navigation decisions and intergroup spacing patterns.
Sarie Van Belle - One of the best experts on this subject based on the ideXlab platform.
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cognitive maps in the wild revealing the use of metric information in Black Howler monkey route navigation
The Journal of Experimental Biology, 2021Co-Authors: Alejandro Estrada, Miguel De Guinea, Anneisola K Nekaris, Sarie Van BelleAbstract: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.
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effects of variation in forest fragment habitat on Black Howler monkey demography in the unprotected landscape around palenque national park mexico
PeerJ, 2020Co-Authors: Keren Klass, Sarie Van Belle, Alvaro Camposvillanueva, Fernando Mercado Malabet, Alejandro EstradaAbstract: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.
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demographic population structure of Black Howler monkeys in fragmented and continuous forest in chiapas mexico implications for conservation
American Journal of Primatology, 2020Co-Authors: Keren Klass, Sarie Van Belle, Alejandro EstradaAbstract: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.
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individual participation in intergroup contests is mediated by numerical assessment strategies in Black Howler and tufted capuchin monkeys
Philosophical Transactions of the Royal Society B, 2015Co-Authors: Sarie Van Belle, Clara J ScarryAbstract:Asymmetries in resource-holding potential between opposing groups frequently determine outcomes of intergroup contests. Since both numerical superiority and high intergroup dominance rank may confer competitive advantages, group members should benefit from assessing the relative strength of rivals prior to engaging in defensive displays. However, differences in individual assessment may emerge when cost-benefit trade-offs differ among group members. We examine the influence of numerical superiority and intergroup dominance relationships on individual participation in intergroup encounters in Black Howler monkeys (Alouatta pigra) and tufted capuchin monkeys (Sapajus nigritus). Black Howlers responded with longer vocal displays during encounters with neighbours with an equal number of resident males, while tufted capuchins increased their participation with increasing relative male group size. Within each species, males and females responded similarly to varying numerical odds, suggesting that despite pay-off asymmetries between males and females, both sexes were similarly influenced by numerical asymmetries in deciding to participate in collective group defence. Whereas the outcome of contests among tufted capuchins was determined by relative male group size, reflected in a pronounced intergroup dominance hierarchy, the absence of dominance relationships among Black Howler groups may have provoked prolonged vocal displays in order to assess rival groups with matching competitive abilities.
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female participation in collective group defense in Black Howler monkeys alouatta pigra
American Journal of Primatology, 2015Co-Authors: Sarie Van BelleAbstract: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. Am. J. Primatol. 77:595–604, 2015. © 2015 Wiley Periodicals, Inc.
Paul A. Garber - One of the best experts on this subject based on the ideXlab platform.
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switching between food patches suggests a need to balance nutrients while foraging in wild Black Howler monkeys alouatta pigra
Revista Mexicana De Biodiversidad, 2020Co-Authors: Nicoletta Righini, Paul A. Garber, Jessica M Rothman, Minerva Sarai Santillanrivera, Antonio LopezespinozaAbstract:Studies of feeding patch choice in primates have traditionally analyzed individual foraging decisions in relation to patterns of social foraging, dominance, and feeding competition. However, information on detailed ecological and nutritional characteristics of the patches also is needed to understand the basis of feeding patch preferences. In particular, recent models of nutritional ecology have stressed the importance of nutrient balancing as a primary driver of individual foraging decisions. Here we investigated the behavioral and nutritional factors affecting feeding patch choice in Black Howler monkeys (Alouatta pigra) during a 15-month field study in Campeche, Mexico. We collected 1300 hours of behavioral data on 14 focal animals, including full-day follows of one individual/day recording all feeding activities. We carried out nutritional analyses of foods from feeding trees and calculated daily nutrient intake. A total of 690 trees (i.e., patches) were visited throughout the study period. The time spent feeding and the amount of food consumed differed significantly according to patch type. Individuals consumed more food in mature and immature fruit patches than in mature leaf, young leaf, and flower patches. Protein intake rates (kJoule/min) were similar in young and mature leaf patches, and higher than in mature fruit, immature fruit, and flower patches, among which the rate was similar. In the majority of the cases (80.3%), the focal animals left the feeding patch prior to satiation. On those occasions, resource mixing, or moving from one food type to another food type, accounted for 49.4% of the patch leaving events. The fact that Black Howler monkeys alternated feeding bouts between fruit and leaf patches, as well as alternating bouts of higher and lower protein intake, suggest that this pattern could be dictated by the need to balance nutrients.
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the relative effects of reproductive condition stress and seasonality on patterns of parasitism in wild female Black Howler monkeys alouatta pigra
American Journal of Primatology, 2017Co-Authors: Rodolfo Martinezmota, Paul A. Garber, Rupert Palme, Thomas R GillespieAbstract:Parasitic infections in wildlife are shaped by host-related traits including individual reproductive condition. It has been argued that female primates are more susceptible to infectious diseases during pregnancy due to short-term changes in immune function that result in reduced ability to combat infections. Likewise, lactation, which is the most energetically expensive state, may affect immunity and infection risk due to tradeoffs between milk production and maintenance of immune function. Here, we examine the degree to which parasite prevalence and parasite richness are affected by female reproductive condition and stress levels in wild female Black Howler monkeys (Alouatta pigra). Over the course of one year, we collected fresh fecal samples from 15 adult females belonging to seven Black Howler groups living in Escarcega, Mexico. Fecal samples were used for parasitological analysis and for measuring fecal glucocorticoid metabolites (i.e., stress biomarker). We found that the prevalence of intestinal parasites and parasite richness did not differ among non-pregnant, pregnant, and lactating females. Fecal glucocorticoid metabolite levels increased significantly during pregnancy and during the first month of lactation, and positively predicted the probability of Controrchis biliophilus infection. Parasite prevalence and richness decreased during the months of increased rainfall. We conclude that reproductive physiology has limited consequences on intestinal parasitic infection risk in female Black Howler monkeys and that seasonal environmental fluctuations have greater effects.
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the effects of plant nutritional chemistry on food selection of mexican Black Howler monkeys alouatta pigra the role of lipids
American Journal of Primatology, 2017Co-Authors: Nicoletta Righini, Paul A. Garber, Jessica M RothmanAbstract:Understanding the nutritional basis of food selection is fundamental to evaluate dietary patterns and foraging strategies in primates. This research describes the phytochemical composition of the foods consumed by two groups of Mexican Black Howler monkeys (Alouatta pigra) during a 15-month field study, and examines how plant nutritional chemistry affected food choice. Based on indices of selectivity that reflected seasonal changes in the amount of different phenophases of the most consumed plant species and their availability in the environment, we found that, in general, Howlers did not preferentially select food items based on their concentrations of protein, sugar, energy, or their protein-to-fiber ratio. During only one season of the year, the nortes (October–January), there was evidence for selectivity. During this period, selectivity indices correlated positively with the lipid content of foods ingested. However, a strategy of selecting fruits high in lipids (21–41% dry matter) coincided with the consumption of a leaf-based diet (based on estimates of the dry weight of food ingested), suggesting that during this season Howlers interchanged lipids with sugars to obtain energy and possibly to balance the higher protein intake obtained by the increased leaf consumption. Overall, these data did not support the prediction that food choice in this Howler population was strongly correlated with particular nutrients, and suggest that balancing a suite of nutrients by consuming plants that vary widely in their composition may be an important strategy for Howler monkeys. Am. J. Primatol. 9999:XX–XX, 2015. © 2015 Wiley Periodicals, Inc.
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Metabolomic data suggest regulation of Black Howler monkey (Alouatta pigra) diet composition at the molecular level.
American journal of primatology, 2016Co-Authors: Katherine R Amato, Alexander V. Ulanov, Kou San Ju, Paul A. GarberAbstract:In addition to macronutrients, foods consist of a complex set of chemical compounds that can influence dietary selectivity and consumer physiology. Metabolomics allow us to describe this complexity by quantifying all small molecules, or metabolites, in a food item. In this study we use GC-MS based metabolomics to describe the metabolite profiles of foods consumed by one population of Mexican Black Howler monkeys (Alouatta pigra) over a 10-month period. Our data indicate that each food exhibited a distinct metabolite profile, and the average weekly intake of metabolites such as neochlorogenic acid and serotonin (5-hydroxytryptamine) was correlated with the consumption of certain plant parts. We speculate that these patterns result in temporal changes in Howler monkey physiology such as food retention time. In contrast, variation in the weekly intake of metabolites such as oxalic acid was 70% less than variation in the concentration of the same metabolites across food items, suggesting that Howler monkeys regulated the intake of these metabolites, possibly to avoid physiological consequences such as kidney stone formation. Finally, seasonal variation in the consumption of individual nutrient and non-nutrient metabolites were correlated with changes in the relative abundances of associated gut microbial taxa, implying indirect effects of food item metabolites on Howler monkey nutritional ecology that likely drive foraging decisions. While additional research is needed to validate these findings, the patterns we report serve as important baseline data for understanding the effects of plant metabolites on the food choice in primates.
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social and genetic factors mediating male participation in collective group defence in Black Howler monkeys
Animal Behaviour, 2014Co-Authors: Sarie Van Belle, Alejandro Estrada, Paul A. Garber, Anthony Di FioreAbstract:Cooperative group defence can provide benefits both to participants in the collective actions and to free-riding group members. The study of individual strategies used during collective action is thus useful for our understanding the nature and evolution of cooperation in animal societies. Here, we examine social and genetic factors influencing the participation of adult and subadult males in naturally occurring howling bouts of five multimale-multifemale groups of Black Howler monkeys, Alouatta pigra, at Palenque National Park, Mexico during a 28-month study. Among Howler monkeys, howling bouts are often used in the context of intergroup spacing as a form of cooperative group defence. For howling bouts in which all resident males were in view at least 80% of the time (N = 387 bouts), we calculated the percentage of time that each male participated and the percentage of time that each intragroup male–male dyad participated mutually. Male participation was significantly greater during howling bouts that were part of intergroup encounters compared to spontaneous calls or calls in response to nearby calls when there was no visual contact with rival groups. Adult males initiated and participated during howling bouts significantly more than subadult males. Among adult males, those that had sired offspring in the group initiated and participated significantly more than males without offspring in the group. Kinship and proximity patterns among pairs of males did not influence the percentage of time that those dyads howled mutually. Together, these findings suggest that cooperative group defence in male Black Howler monkeys evolved principally through mutualism in which participants gain direct fitness benefits.
Alban Lemasson - One of the best experts on this subject based on the ideXlab platform.
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socially mediated overlap in vocal interactions between free ranging Black Howler monkeys
American Journal of Primatology, 2021Co-Authors: Alban Lemasson, Alejandro Estrada, Margarita Brisenojaramillo, Melissa Berthet, Veronique BiquandAbstract:"Conversation rules" such as overlap avoidance and coordinated overlap have been reported in nonhuman animals, and seem to be adaptive responses to the requirements of social life. Some species display both patterns in an apparently flexible way, but the social factors mediating their respective usage remain poorly documented. We investigated the potential social factors guiding the usage of these temporal rules during collective howling in six free-ranging groups of Black Howler monkeys (Alouatta pigra). First, we found that adult males' vocalizations rarely overlap those of other callers while most adult females' calls overlap other members' calls, especially that of other females. Second, whereas some call types (notably affiliative calls) are typically emitted without overlap, roars (agonistic loud calls) overlap more frequently. Third, coordinated overlap is more frequent during intergroup competition. Our findings support the hypothesis that overlap avoidance and coordinated overlap are two different (here sex-related) vocal alliance social behaviors, at least for some nonhuman primates. More comparative investigations are now needed to explore further their evolutionary trajectories in this lineage.
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Vocal repertoire of free-ranging Black Howler monkeys’ (Alouatta pigra): call types, contexts and sex-related contributions
American Journal of Primatology, 2017Co-Authors: Margarita Briseño-jaramillo, Alejandro Estrada, Véronique Guyot-biquand, Alban LemassonAbstract:Alouatta species utter the most powerful primate vocalizations in the Neotropics and are well-known for their loud and long-lasting male howling bouts. However, the diversity of acoustic structures used in these howling bouts, as well as in non-howling contexts, and the relative contribution of the different group members to the entire vocal repertoire, needed to be explored further. This report provides the first detailed description of the vocal repertoire of Black Howler monkeys (Alouatta pigra), focusing on acoustic structures and contexts of emission of both loud and soft calls as well as on the contribution rate of males and females to the different call types. Three free-ranging social groups of Black Howler monkeys living in Palenque National Park, Mexico were monitored. We identified twelve acoustically discriminable call types, eight described previously and four described here for the first time. A few call types were systematically emitted either isolated or during howling bouts, but most of them could be heard in both calling contexts. Three call types were emitted only by females and two only by males. Adult males’ call rates (for the seven shared call types) were higher than those of females but only when considering calls emitted within howling bouts. Our contextual analysis enabled us to divide call types into potential functional categories, according to their degree of contribution, to intra-group versus inter-group interactions and to neutral-positive versus negative situations. We then discussed how socio-ecological factors, notably sex differences in social behaviors, may explain the variability found in the vocal repertoire of this species and compared our findings with the literature on other primate species.
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behavioural innovation and cultural transmission of communication signal in Black Howler monkeys
Scientific Reports, 2015Co-Authors: Margarita Brisenojaramillo, Alban Lemasson, Alejandro EstradaAbstract:Social traditions based on communication signals are widespread in birds, cetaceans and humans, but surprisingly rare in nonhuman primates known for having genetically-determined vocal repertoires. This study presents the first description of a singular case of behaviour associated with calling (placing a hand in front of the mouth while vocalizing: HFM) in Black Howler monkeys. We showed, first, that HFM was found only in a subset of the groups observed, at the same geographical location, and was age- and sex-specific. There was an audience effect on HFM, with highest rates when a neighbouring group was visible. HFM was non-randomly combined with audio-visual signals and always performed while roaring. High HFM rates triggered more vocal responses from group members and male neighbours, and HFM signalers temporally synchronized their behaviour in a predictable way. Finally, the positioning of the hand systematically modified the call’s auditory structure. Altogether these results support the idea that HFM is an innovated, culturally transmitted communication signal that may play a role in inter-group competition and intra-group cohesion. This study opens new lines of research about how nonhuman primates developed strategies to overcome their constraints in acoustic plasticity very early in the primate lineage.
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Individual voice recognition and an auditory map of neighbours in free-ranging Black Howler monkeys (Alouatta pigra)
Behavioral Ecology and Sociobiology, 2015Co-Authors: Margarita Briseño-jaramillo, Alejandro Estrada, Alban LemassonAbstract:Recognizing individuals auditorily is of primal importance in maintaining socio-spatial cohesion among conspecifics within a social group as well as for regulating space use among neighbours, particularly for species dwelling in forests where visual communication is constrained. This study evaluates the capacity of Black Howler monkeys ( Alouatta pigra ) in the Palenque National Park, Mexico, to recognize the voices of individual neighbours, using a violation-of-expectation paradigm based on the spatial congruence of voices. First, we assessed intra- vs inter-individual acoustic variations by comparing the acoustic structures of the loud calls of six adult males from three different social groups. Although the acoustic structures of barks were more individually discriminative than those of roars, both loud call types presented significant individual variations. Second, playbacks of sequences composed of barks and roars were studied in order to assess the auditory recognition capacity of six neighbouring groups. Two test situations were presented to each study group: the spatial location of the speaker was either congruent (in the appropriate neighbouring territory) or incongruent (in a territory on the opposite side) with the voice broadcast. Monkeys reacted significantly more (e.g. faster approach, more vocal responses) in incongruent situations. Our data suggest that Black Howler monkeys display individual acoustic variations and are capable of recognizing the voices of non-group members. Our experimental paradigm is an easily replicable way to investigate inter-group voice recognition in animals and to test the extent of socio-spatial cognitive abilities.
Katherine R Amato - One of the best experts on this subject based on the ideXlab platform.
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Metabolomic data suggest regulation of Black Howler monkey (Alouatta pigra) diet composition at the molecular level.
American journal of primatology, 2016Co-Authors: Katherine R Amato, Alexander V. Ulanov, Kou San Ju, Paul A. GarberAbstract:In addition to macronutrients, foods consist of a complex set of chemical compounds that can influence dietary selectivity and consumer physiology. Metabolomics allow us to describe this complexity by quantifying all small molecules, or metabolites, in a food item. In this study we use GC-MS based metabolomics to describe the metabolite profiles of foods consumed by one population of Mexican Black Howler monkeys (Alouatta pigra) over a 10-month period. Our data indicate that each food exhibited a distinct metabolite profile, and the average weekly intake of metabolites such as neochlorogenic acid and serotonin (5-hydroxytryptamine) was correlated with the consumption of certain plant parts. We speculate that these patterns result in temporal changes in Howler monkey physiology such as food retention time. In contrast, variation in the weekly intake of metabolites such as oxalic acid was 70% less than variation in the concentration of the same metabolites across food items, suggesting that Howler monkeys regulated the intake of these metabolites, possibly to avoid physiological consequences such as kidney stone formation. Finally, seasonal variation in the consumption of individual nutrient and non-nutrient metabolites were correlated with changes in the relative abundances of associated gut microbial taxa, implying indirect effects of food item metabolites on Howler monkey nutritional ecology that likely drive foraging decisions. While additional research is needed to validate these findings, the patterns we report serve as important baseline data for understanding the effects of plant metabolites on the food choice in primates.
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the gut microbiota appears to compensate for seasonal diet variation in the wild Black Howler monkey alouatta pigra
Microbial Ecology, 2015Co-Authors: Carl J Yeoman, Katherine R Amato, Angela D Kent, Rebecca M Stumpf, Roderick I. Mackie, Steven R Leigh, Brenda A Wilson, Karen E Nelson, Bryan A WhiteAbstract:For most mammals, including nonhuman primates, diet composition varies temporally in response to differences in food availability. Because diet influences gut microbiota composition, it is likely that the gut microbiota of wild mammals varies in response to seasonal changes in feeding patterns. Such variation may affect host digestive efficiency and, ultimately, host nutrition. In this study, we investigate the temporal variation in diet and gut microbiota composition and function in two groups (N = 13 individuals) of wild Mexican Black Howler monkeys (Alouatta pigra) over a 10-month period in Palenque National Park, Mexico. Temporal changes in the relative abundances of individual bacterial taxa were strongly correlated with changes in host diet. For example, the relative abundance of Ruminococcaceae was highest during periods when energy intake was lowest, and the relative abundance of Butyricicoccus was highest when young leaves and unripe fruit accounted for 68 % of the diet. Additionally, the Howlers exhibited increased microbial production of energy during periods of reduced energy intake from food sources. Because we observed few changes in Howler activity and ranging patterns during the course of our study, we propose that shifts in the composition and activity of the gut microbiota provided additional energy and nutrients to compensate for changes in diet. Energy and nutrient production by the gut microbiota appears to provide an effective buffer against seasonal fluctuations in energy and nutrient intake for these primates and is likely to have a similar function in other mammal species.
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the role of gut microbes in satisfying the nutritional demands of adult and juvenile wild Black Howler monkeys alouatta pigra
American Journal of Physical Anthropology, 2014Co-Authors: Carl J Yeoman, Katherine R Amato, Angela D Kent, Rebecca M Stumpf, Roderick I. Mackie, Steven R Leigh, Brenda A Wilson, Karen E Nelson, Bryan A WhiteAbstract:In all mammals, growth, development, pregnancy, and lactation increase nutritional demands. Although primate field studies tend to focus on shifts in activity and diet as mechanisms to compensate for these demands, differences in digestive efficiency also are likely to be important. Because the gut microbiota can impact host digestive efficiency, we examined differences in activity budget, diet, and the gut microbial community among adult male (N = 4), adult female (N = 4), and juvenile (N = 5) wild Black Howler monkeys (Alouatta pigra) across a ten-month period in Palenque National Park, Mexico to determine how adult females and juveniles compensate for increased nutritional demands. Results indicate that adult females and juveniles consumed more protein and energy than adult males. Adult males, adult females, and juveniles also possessed distinct gut microbial communities, unrelated to diet. Juveniles exhibited a gut microbiota characterized by bacteria from the phylum Firmicutes, such as Roseburia and Ruminococcus, and demonstrated high fecal volatile fatty acid content, suggesting increased microbial contributions to host energy balances. Adult females possessed a higher Firmicutes to Bacteroidetes ratio, also suggesting increased energy production, and their gut microbiota was characterized by Lactococcus, which has been associated with folate biosynthesis. On the basis of these patterns, it appears that the gut microbiota differentially contributes to Howler monkey nutrition during reproduction and growth. Determining the nutritional and energetic importance of shifts in activity, diet, and the gut microbiota in other nonhuman primate taxa, as well as humans, will transform our understanding of these life history processes and the role of host-microbe relationships in primate evolution. Am J Phys Anthropol 155:652–664, 2014. © 2014 Wiley Periodicals, Inc.
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nutrition and foraging strategies of the Black Howler monkey alouatta pigra in palenque national park mexico
American Journal of Primatology, 2014Co-Authors: Katherine R Amato, Paul A. GarberAbstract:Food resources consumed by primates vary markedly in nutritional content. As a result, foragers must develop a feeding strategy to select resources that balance energy and macronutrient intake and reduce the consumption of fiber and toxins. In this study, we collected data on dietary patterns, rates of food consumption, and weight of food items consumed and combined them with published values of the nutritional content of Neotropical foods to estimate energy and nutrient intake during a 10-month period in two groups (N = 16 individuals) of Black Howler monkeys (Alouatta pigra) inhabiting Palenque National Park, Mexico. Although Howler monkeys are generally assumed to exploit a leaf-dominated diet and be energy-limited, our results indicated that Black Howlers met their estimated energy requirements, consuming an average of 0.58 MJ of overall energy per metabolic body mass per day. The Howlers also surpassed protein requirements by consuming an average of 8.2 g of protein per metabolic body mass per day. The amount of time they spent resting was not correlated with the amount of leaves or fruit in the diet or with overall energy intake. Therefore, despite consuming a leaf-heavy diet during some months of the year, Black Howlers do not appear to be energy-limited. Additionally, the Howlers maintained a relatively consistent level of average daily protein energy intake regardless of diet composition, while non-protein energy intake varied in response to the amount of ripe fruits consumed. Although our use of published nutritional data introduces error, these findings suggest that Black Howler feeding ecology is more similar to other fruit-eating atelines than previously suspected, and several common assumptions regarding Howler behavior and feeding ecology need to be reexamined. Am. J. Primatol. 76:774–787, 2014. © 2014 Wiley Periodicals, Inc.
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habitat degradation impacts Black Howler monkey alouatta pigra gastrointestinal microbiomes
The ISME Journal, 2013Co-Authors: Katherine R Amato, Carl J Yeoman, Angela D Kent, Nicoletta Righini, Franck Carbonero, Alejandro Estrada, Rex H Gaskins, Rebecca M Stumpf, Suleyman YildirimAbstract:The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican Black Howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of Howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of Howlers occupying suboptimal habitats, which may impact host health.