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Macaques ( Macaca Leonina ): Impact on Their Seed Dispersal Effectiveness and Ecological Contribution in a Tropical Rainforest at Khao Yai National Park, Thailand

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Faculté des Sciences Département de Biologie, Ecologie et Environnement Unité de Biologie du Comportement, Ethologie et Psychologie Animale Feeding and ranging behavior of northern pigtailed macaques ( Macaca leonina ): impact on their seed dispersal effectiveness and ecological contribution in a tropical rainforest at Khao Yai National Park, Thailand ~ ~ ~ Régime alimentaire et déplacements des macaques à queue de cochon ( Macaca leonina ) : impact sur leur efficacité dans la dispersion des graines et sur leur contribution écologique dans une forêt tropicale du parc national de Khao Yai, Thaïlande Année académique 2011-2012 Dissertation présentée par Aurélie Albert en vue de l’obtention du grade de Docteur en Sciences Faculté des Sciences Département de Biologie, Ecologie et Environnement Unité de Biologie du Comportement, Ethologie et Psychologie Animale Feeding and ranging behavior of northern pigtailed macaques ( Macaca leonina ): impact on their seed dispersal effectiveness and ecological contribution in a tropical rainforest at Khao Yai National Park, Thailand ~ ~ ~ Régime alimentaire et déplacements des macaques à queue de cochon ( Macaca leonina ) : impact sur leur efficacité dans la dispersion des graines et sur leur contribution écologique dans une forêt tropicale du parc national de Khao Yai, Thaïlande Année académique 2011-2012 Dissertation présentée par Aurélie Albert en vue de l’obtention du grade de Docteur en Sciences Promotrice : Marie-Claude Huynen (ULg, Belgique) Comité de thèse : Tommaso Savini (KMUTT, Thaïlande) Alain Hambuckers (ULg, Belgique) Pascal Poncin (ULg, Belgique) Président du jury : Jean-Marie Bouquegneau (ULg, Belgique) Membres du jury : Pierre-Michel Forget (MNHN, France) Régine Vercauteren Drubbel (ULB, Belgique) Roseline C. Beudels-Jamar (IRSN, Belgique) Copyright © 2012, Aurélie Albert Toute reproduction du présent document, par quelque procédé que ce soit, ne peut être réalisée qu’avec l’autorisation de l’auteur et du/des promoteur(s). No part of this publication may be reproduced without written permission from the author and the advisor(s). Abstract Southeast Asia experiences an exceptional loss of natural habitat due to a deforestation rate that strongly increased during the last decades. The first consequence is the loss of many animal and plant species, threatened by their habitat degradation and by the loss of interactions necessary to the survival of the whole ecosystem. Large mammals and birds populations, the principal dispersal agent of some plant species, already collapsed massively due to hunting and habitat fragmentation and now threaten to die out. Among the large frugivorous species, primates are particularly vulnerable. Only few species, such as macaques, are able to survive in some man-made habitats, due to their opportunistic life-style. But, in the long term, habitat destruction, hunting and capture for local trade threaten their survival. The extinction of primates in Southeast Asian forests would be disastrous for many plant species as primates are among the major seed-dispersal agents. The study of Macaca , the only Cercopithecinae genus in Southeast Asia, could provide a better understanding of the role of cheek-pouched monkeys in tropical rainforest maintenance and restoration. In this study, we chose to focus on northern pigtailed macaques (Macaca leonina ) as few studies were carried out on this species, making data concerning its ecology and behavior highly limited. Their seed dispersal capacity, although unknown, is potentially high and pigtailed macaques could be as good seed dispersers as sympatric frugivores. They seem to eat a large number of fruits of many plant species, process seeds with care, and range daily over large areas. Moreover they could have a role in forest maintenance and regeneration given that they seem to eat species with all seed sizes, belonging to all plant life forms present in the forest, and they are able to cross various habitat types (primary as well as secondary forests). After providing an outline of our current knowledge on seed dispersal by Cercopithecinae species and their specific role in forest regeneration, our aim was to highlight the importance of northern pigtailed macaques on seed dispersal and thus on forest regeneration by studying (1) how their eco-ethological characteristics can make them effective dispersers, from a quantitative and a qualitative point of view, (2) how the influence of biotic factors, such as resources and predation, on their activities and movements may impact their seed dispersal effectiveness, and (3) what role Macaca spp. can have in a seed dispersal assemblage. While following a troop of northern pigtailed macaques habituated to humans in Khao Yai National Park, Thailand, we recorded their behavior, travels, and consumed items, from dawn to dusk. Moreover, we studied the spatio-temporal distribution of fruits included in their diet, and the characteristics of their sleeping sites. Finally, we performed germination and viability tests on ingested seeds. Results showed that northern pigtailed macaques could disperse thousands of seeds, up to 58 mm in length, coming from the 126 fruit species they eat. Especially, they could disperse them from primary to secondary forest, thanks to handling techniques such as swallowing, spitting and dropping. Finally, the seed passage through their digestive tract mostly had a neutral or positive effect on seed germination and viability. Macaques observed in this study satisfied therefore most requirements defining effective seed dispersers in both quantitative and qualitative terms and we can conclude to the potential importance of Macaca leonina in the tropical rainforest regeneration. To confirm the seed dispersal effectiveness of M. leonina , we needed to make sure that its ranging behavior did not negatively affect dispersed seeds. Moreover, given the importance of human food in their diet, we wondered if this resource had a negative impact on seed dispersal. Our results showed that northern pigtailed macaques adapted their ranging pattern according to fruit availability. Moreover, during fruit scarcity, they shifted their diet from frugivorous to omnivorous with an important part of human food. However, human food did not seem to have an impact on seed dispersal in high fruit abundance periods where macaques had a large home range, traveled long distances and ate mainly fruits. However, in low fruit abundance periods, macaques decreased their home range size, traveled shorter distances and ate mainly human food. This latter could have a negative impact on the seed dispersal of some rare fructifying species. However, these species were eaten by many other animal species able to provide good dispersal services. Then, we showed that sleeping sites characteristics and pre-sleep behavior in M. leonina were influenced by the proximity of resources and the risk of predation. Given that macaques used few sleeping sites, defecated when they woke up and that all troop members slept concentrated in a small area, we think that they created a high seed density below the sleeping trees. This may be harmful for some seed species but may be beneficial for the ecosystem. Moreover, this pattern may be shown in other effective seed dispersers in the park. So as harmful for seeds it may be, it does not make pigtailed macaques less effective than other frugivores. Finally, we demonstrated that Macaca species are important associates in the seed dispersal assemblage found in Southeast Asian forests. Indeed they may disperse most plant species, usually more efficiently dispersed by other frugivores, and thus provide a significant complement in term of dispersal quantity. Moreover, they are sometimes the only frugivores able to disperse the seeds of some species, mainly large-seeded and/or protected ones, and may thus bring them a vital dispersal service. Résumé La forte augmentation du taux de déforestation durant les dernières décennies a engendré une perte exceptionnelle d’habitat en Asie du sud-est. La première conséquence est la perte de nombreuses espèces animales et végétales, menacée par la dégradation de leur habitat et par la perte des interactions nécessaires à la survie de tout l’écosystème. Les populations de grands mammifères et oiseaux, agents de dispersion principaux de certaines espèces végétales, ont déjà fortement diminué en raison de la chasse et de la fragmentation de l’habitat, et sont désormais menacé d’extinction. Parmi les espèces de grands frugivores, les primates sont particulièrement vulnérables. Seules quelques espèces, telles que les macaques, sont capables de survivre dans des habitats façonnés par l’Homme, en raison de leur mode de vie opportuniste. Mais, à long terme, la destruction de leur habitat, la chasse et les captures pour le commerce local menacent leur survie. L’extinction des primates dans les forêts du sud-est asiatique serait désastreuse pour de nombreuses espèces végétales étant donné qu’ils font parti des principaux agents de dispersion des graines. L’étude des macaques, le seul genre de Cercopithecinae présent en Asie du sud-est, pourrait fournir une meilleure compréhension du rôle des singes à poches jugales dans le maintien et la restauration des forêts tropicales. Nous avons choisi de focaliser notre étude sur les macaques à queue de cochon du Nord ( Macaca leonina ) car peu d’études ont été effectuées sur cette espèce, rendant très limitées les données concernant son écologie et son comportement. Leur capacité à disperser
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