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Vocal complexity is central to many evolutionary hypotheses about animal communication. Yet, quantifying and comparing complexity remains a challenge, particularly when vocal types are highly graded. Male Bornean orangutans (Pongo pygmaeus wurmbii) produce complex and variable "long call" vocalizations comprising multiple sound types that vary within and among individuals. Previous studies described six distinct call (or pulse) types within these complex vocalizations, but none quantified their discreteness or the ability of human observers to reliably classify them. We studied the long calls of 13 individuals to: (1) evaluate and quantify the reliability of audio-visual classification by three well-trained observers, (2) distinguish among call types using supervised classification and unsupervised clustering, and (3) compare the performance of different feature sets. Using 46 acoustic features, we used machine learning (i.e., support vector machines, affinity propagation, and fuzzy c-means) to identify call types and assess their discreteness. We additionally used Uniform Manifold Approximation and Projection (UMAP) to visualize the separation of pulses using both extracted features and spectrogram representations. Supervised approaches showed low inter-observer reliability and poor classification accuracy, indicating that pulse types were not discrete. We propose an updated pulse classification approach that is highly reproducible across observers and exhibits strong classification accuracy using support vector machines. Although the low number of call types suggests long calls are fairly simple, the continuous gradation of sounds seems to greatly boost the complexity of this system. This work responds to calls for more quantitative research to define call types and quantify gradedness in animal vocal systems and highlights the need for a more comprehensive framework for studying vocal complexity vis-à-vis graded repertoires.
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Vocalización Animal , Animales , Vocalización Animal/fisiología , Masculino , Pongo pygmaeus/fisiología , Reproducibilidad de los Resultados , Aprendizaje Automático , Acústica , Espectrografía del Sonido , BorneoRESUMEN
Uncontrolled fires place considerable burdens on forest ecosystems, compromising our ability to meet conservation and restoration goals. A poor understanding of the impacts of fire on ecosystems and their biodiversity exacerbates this challenge, particularly in tropical regions where few studies have applied consistent analytical techniques to examine a broad range of ecological impacts over multiyear time frames. We compiled 16 y of data on ecosystem properties (17 variables) and biodiversity (21 variables) from a tropical peatland in Indonesia to assess fire impacts and infer the potential for recovery. Burned forest experienced altered structural and microclimatic conditions, resulting in a proliferation of nonforest vegetation and erosion of forest ecosystem properties and biodiversity. Compared to unburned forest, habitat structure, tree density, and canopy cover deteriorated by 58 to 98%, while declines in species diversity and abundance were most pronounced for trees, damselflies, and butterflies, particularly for forest specialist species. Tracking ecosystem property and biodiversity datasets over time revealed most to be sensitive to recurrent high-intensity fires within the wider landscape. These megafires immediately compromised water quality and tree reproductive phenology, crashing commercially valuable fish populations within 3 mo and driving a gradual decline in threatened vertebrates over 9 mo. Burned forest remained structurally compromised long after a burn event, but vegetation showed some signs of recovery over a 12-y period. Our findings demonstrate that, if left uncontrolled, fire may be a pervasive threat to the ecological functioning of tropical forests, underscoring the importance of fire prevention and long-term restoration efforts, as exemplified in Indonesia.
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Mariposas Diurnas , Incendios , Animales , Ecosistema , Suelo , Bosques , Árboles , BiodiversidadRESUMEN
Tropical peatlands are the sites of Earth's largest fire events, with outsized contributions to greenhouse gases, toxic smoke, and haze rich with particulate matter. The human health risks from wildfire smoke are well known, but its effects on wildlife inhabiting these ecosystems are poorly understood. In 2015, peatland fires on Borneo created a thick haze of smoke that blanketed the region. We studied its effects on the long call vocalizations of four adult male Bornean orangutans (Pongo pygmaeus wurmbii) in a peat swamp forest. During the period of heavy smoke, orangutans called less often and showed reduced vocal quality-lower pitch, increased harshness and perturbations, and more nonlinear phenomena-similar to changes in human smokers. Most of these changes persisted for two months after the smoke had cleared and likely signal changes in health. Our work contributes valuable information to support non-invasive acoustic monitoring of this Critically Endangered primate.
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Among non-human primates, alloparental infant care is most extensive in callitrichines, and is thought to be particularly costly for tamarins whose helpers may suffer increased energy expenditure, weight loss, and reduced feeding time and mobility. The costs and benefits of infant care likely vary among group members yet very few wild studies have investigated variable infant care contributions. We studied infant care over an 8-month period in four wild groups of saddleback tamarins in Bolivia to evaluate: (a) what forms of infant care are provided, by whom, and when, (b) how individuals adjust their behavior (activity, vigilance, height) while caring for infants, and (c) whether individuals differ in their infant care contributions. We found that infant carrying, food sharing, and grooming varied among groups, and immigrant males-those who joined the group after infants were conceived-participated less in infant care compared to resident males. Adult tamarins fed less, rested more, and increased vigilance while carrying infants. Although we did not detect changes in overall activity budgets between prepartum and postpartum periods, tamarins spent more time scanning their environments postpartum, potentially reflecting increased predation risk to both carriers and infants during this period. Our study provides the first quantitative data on the timing and amount of infant carrying, grooming, and food transfer contributed by all individuals within and among multiple wild groups, filling a critical knowledge gap about the factors affecting infant care, and highlighting evolutionary hypotheses for cooperative breeding in tamarins.
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Conducta Materna , Conducta Paterna , Saguinus/psicología , Animales , Bolivia , Femenino , Masculino , Conducta SocialRESUMEN
The use of urine test strips (e.g., Roche Chemstrip®) has become the standard for quickly assessing the physiological condition and/or health of wild primates. These strips have been used to detect ketosis as a marker of fat catabolism in several primate taxa in their natural environments in response to changing food availability. However, the use of urine strips to determine ketosis has only been validated in human studies, and thus it remains unclear whether these strips accurately detect and quantify ketone bodies in nonhuman primates. We examined variations in ketone body concentrations in urine samples collected from wild Bornean orangutans at the Tuanan Orangutan Research Station. We assessed the accuracy of qualitative results from Chemstrip test strips in the field (i.e., negative, small, moderate, and large) using an enzyme-linked assay in the laboratory to determine the concentrations of acetoacetate of the same urine samples. Urine samples that tested positive for ketones in the field had significantly higher levels of ketones in the enzymatic assay compared to those that tested negative. There was significant variation in acetoacetate concentrations among the 4 Chemstrip values; however, post hoc tests revealed no significant differences between negative and small samples. We conclude that urinary test strips provide a useful tool for determining ketotic state in wild orangutans, but caution should be taken when interpreting results from samples showing only small levels of ketones on these strips.
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Enfermedades del Simio Antropoideo/diagnóstico , Cetosis/veterinaria , Pongo pygmaeus , Urinálisis/veterinaria , Animales , Borneo , Indonesia , Cetosis/diagnóstico , Urinálisis/instrumentación , Urinálisis/métodosRESUMEN
Since Darwin (), scientists have been puzzled by how behaviors that impose fitness costs on helpers while benefiting their competitors could evolve through natural selection. Hamilton's () theory of inclusive fitness provided an explanation by showing how cooperative behaviors could be adaptive if directed at closely related kin. Recent studies, however, have begun to question whether kin selection is sufficient to explain cooperative behavior in some species (Bergmüller, Johnstone, Russell, & Bshary, ). Many researchers have instead emphasized the importance of direct fitness benefits for helpers in the evolution of cooperative breeding systems. Furthermore, individuals can vary in who, when, and how much they help, and the factors that affect this variation are poorly understood (Cockburn, ; Heinsohn, ). Cooperative breeders thus provide excellent models for the study of evolutionary theories of cooperation and conflict (Cant, ).
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Evolución Biológica , Callitrichinae/fisiología , Conducta Cooperativa , Conducta Materna , Animales , Antropología Física , Femenino , Masculino , Selección GenéticaRESUMEN
The spatial and temporal variation in food abundance has strong effects on wildlife feeding and nutrition. This variation is exemplified by the peatland forests of Central Kalimantan, which are characterized by unpredictable fruiting fluctuations, relatively low levels of fruit availability, and low fruit periods (<3% of trees fruiting) that can last nearly a year. Challenged by these environments, large, arboreal frugivores like orangutans must periodically rely on non-preferred, lower-quality foods to meet their nutritional needs. We examined variation in nutrient intake among age-sex classes and seasons over a 7-year period at the Tuanan Orangutan Research Station in Central Kalimantan. We conducted 2,316 full-day focal follows on 62 habituated orangutans (Pongo pygmaeus wurmbii). We found differences in total energy and macronutrient intake across age-sex classes, controlling for metabolic body mass. Intake of both total energy and macronutrients varied with fruit availability, and preference of dietary items increased with their nutritional quality. Foraging-related variables, such as day journey length, travel time, and feeding time, also varied among age-sex classes and with fruit availability. Our results add to the growing body of literature suggesting that great variation in foraging strategies exists among species, populations, and age-sex classes and in response to periods of resource scarcity. RESEARCH HIGHLIGHTS: The spatial and temporal variation in food abundance has strong effects on wildlife feeding and nutrition. Here we present the first long term study of the effects of variation in fruit availability and age/sex class on nutritional ecology of wild Bornean orangutans. We examined variation in nutrient intake of wild orangutans in living in a peat swamp habitat over a 7-year period at the Tuanan Orangutan Research Station in Central Kalimantan. We conducted 2,316 full-day focal follows on 62 habituated orangutans (Pongo pygmaeus wurmbii). We found differences in total energy and macronutrient intake across age-sex classes, controlling for metabolic body mass. Intake of both total energy and macronutrients varied with fruit availability, and preference of dietary items increased with their nutritional quality. Foraging-related variables, such as day journey length, travel time, and feeding time, also varied among age-sex classes and with fruit availability. Our results add to the growing body of literature suggesting that great variation in foraging strategies exists among species, populations, and age-sex classes and in response to periods of resource scarcity.
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Conducta Alimentaria , Pongo pygmaeus , Humedales , Animales , Ecosistema , Pongo , Estaciones del Año , SueloRESUMEN
OBJECTIVES: Male vocal displays play an important role in sexual selection in many species. If there are costs or constraints, calls may convey honest information about the caller. We studied the loud calls of male simakobu (Simias concolor), a sexually dimorphic primate that resides in one-male groups, on Siberut Island, Indonesia. MATERIALS AND METHODS: We combined behavioral and ecological data with acoustic analysis to determine the influence of energy costs and status on calling effort. Based on all-day follows (n = 107) and loud-call recordings (n = 186), we determined how calling rates and durations varied in relation to short-term (time of day, temperature, travel distance) and long-term (fruit availability, physical condition) measures of energy availability and expenditure. RESULTS: We found that males avoided calling at the hottest times of the day, and produced shorter calls at higher temperatures, supporting the hypothesis that calls are influenced by thermoregulation costs. A peak of longer duration calls just before sunrise, however, could not be explained by energy constraints, but we hypothesize that this pattern is related to the fact that dawn calls occur in choruses, motivating males to call longer than their neighbors. Contrary to predictions, calling rates increased with decreasing fruit availability and did not appear to be energetically costly. DISCUSSION: We hypothesize that calling rates instead reflect strategies involving feeding and/or mate competition, signaling the motivation, rather than fighting ability, of the caller. Overall, results only weakly support the hypothesis that the timing and duration-but not rate-of simakobu loud calls are influenced by energy costs. Am J Phys Anthropol 161:44-52, 2016. © 2016 Wiley Periodicals, Inc.
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Colobinae/fisiología , Vocalización Animal/fisiología , Animales , Ritmo Circadiano , Masculino , Factores de TiempoRESUMEN
Primate loud calls have the potential to encode information about the identity, arousal, age, or physical condition of the caller, even at long distances. In this study, we conducted an analysis of the acoustic features of the loud calls produced by a species of Asian colobine monkey (simakobu, Simias concolor). Adult male simakobu produce loud calls spontaneously and in response to loud sounds and other loud calls, which are audible more than 500 m. Individual differences in calling rates and durations exist, but it is unknown what these differences signal and which other acoustic features vary among individuals. We aimed to describe the structure and usage of calls and to examine acoustic features that vary within and among individuals. We determined the context of 318 loud calls and analyzed 170 loud calls recorded from 10 adult males at an undisturbed site, Pungut, Siberut Island, Indonesia. Most calls (53%) followed the loud call of another male, 31% were spontaneous, and the remaining 16% followed a loud environmental disturbance. The fundamental frequency (F0) decreased while inter-unit intervals (IUI) increased over the course of loud call bouts, possibly indicating caller fatigue. Discriminant function analysis indicated that calls were not well discriminated by context, but spontaneous calls had higher peak frequencies, suggesting a higher level of arousal. Individual calls were distinct and individuals were mainly discriminated by IUI, call duration, and F0. Loud calls of older males had shorter IUI and lower F0, while middle-aged males had the highest peak frequencies. Overall, we found that calls were individually distinct and may provide information about the age, stamina, and arousal of the calling male, and could thus be a way for males and females to assess competitors and mates from long distances.
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Colobinae/fisiología , Vocalización Animal/fisiología , Acústica , Factores de Edad , Animales , Nivel de Alerta , Femenino , Individualidad , Masculino , Resistencia FísicaRESUMEN
Asian colobines typically live in small one-male groups (OMGs) averaging five adult females, but Simias concolor (simakobu or pig-tailed langur) is considered an exception because mostly adult male-female pairs have been reported. However, based on their phylogenetic position and marked sexual dimorphism, simakobu are also expected to form OMGs with multiple females. The preponderance of small groups could be the result of human disturbance (hunting or habitat disturbance) reducing group size in the recent past. To investigate this possibility, we documented the demography of ten wild simakobu groups from January 2007 until December 2008 at an undisturbed site, the Peleonan Forest, Siberut Island, Indonesia. We assessed the population-specific size and composition of groups and documented demographic changes due to births, disappearances, and dispersals throughout our 2-year study. We found OMGs with 3.0 adult females on average in addition to all-male groups, but no adult male-female pairs. The ratio of 0.5 infants per adult female (and 0.64 births per female-year in focal groups) suggested that birth rates were similar to those of other Asian colobines. In 5.1 group-years, we observed six dispersal events and six temporary presences (i.e., less than 3 months' residency). Both males and females dispersed, and juveniles seemed to disperse more frequently than adults. To assess the impact of human disturbance on simakobu demography, we compiled data for seven additional populations from the literature and compared them using multiple regressions. Adult sex ratio and the number of immatures per group were influenced negatively by hunting and positively by habitat disturbance while reproductive rates were not significantly affected by either variable. These findings suggest that adult male-female pairs may result from hunting pressure reducing group size, and that conservation action to reduce hunting in the Mentawai Islands is needed to ensure the survival of this critically endangered species.