Publications of Marie-Claude Huynen
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See detailNorthern pigtailed macaques rely on old growth plantations to offset low fruit availability in a degraded forest fragment
Gazagne, Eva ULiege; José‐Domínguez, Juan Manuel; Huynen, Marie-Claude ULiege et al

in American Journal of Primatology (2020)

Space‐use and foraging strategies are important facets to consider in regard to the ecology and conservation of primates. For this study, we documented movement, ranging, and foraging patterns of northern ... [more ▼]

Space‐use and foraging strategies are important facets to consider in regard to the ecology and conservation of primates. For this study, we documented movement, ranging, and foraging patterns of northern pigtailed macaques (Macaca leonina) for 14 months in a degraded habitat with old growth Acacia and Eucalyptus plantations at the Sakaerat Biosphere Reserve in northeastern Thailand. We used hidden Markov models and characteristic hull polygons to analyze these patterns in regard to fruit availability. Macaques' home range (HR) was 599 ha and spanned through a natural dry‐evergreen forest (DEF), and plantation forest. Our results showed that active foraging increased with higher fruit availability in DEF. Macaques changed to a less continuous behavioral state during periods of lower fruit availability in DEF, repeatedly moving from foraging to transiting behavior, while extending their HR further into plantation forest and surrounding edge areas. Concomitantly, macaques shifted their diet from fleshy to dry fruit such as the introduced Acacia species. Our results showed that the diet and movement ecology adaptations of northern pigtailed macaques were largely dependent on availability of native fruits, and reflected a “high‐cost, high‐yield” foraging strategy when fresh food was scarce and dry fruit was available in plantation forest. Conversely, wild‐feeding northern pigtailed macaque populations inhabiting pristine habitat approached a “low‐cost, low‐yield” foraging strategy. Our results outline the effects of habitat degradation on foraging strategies and show how a flexible species can cope with its nutritional requirements. [less ▲]

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See detailBirth control in urban macaques: Description of a tubectomy program and post-op monitoring in Macaca fascicularis, Indonesia
Brotcorne, Fany ULiege; Deleuze, Stefan ULiege; Huynen, Marie-Claude ULiege et al

Conference (2020, February 10)

In Asia, primates and humans are increasingly forced to share space, and often enter in conflict when primates proliferate in anthropogenic environments. Reproductive control is increasingly used to limit ... [more ▼]

In Asia, primates and humans are increasingly forced to share space, and often enter in conflict when primates proliferate in anthropogenic environments. Reproductive control is increasingly used to limit population growth but very few monitoring data are available. Therefore, the efficiency and implications of such programs require a careful examination. Our research aims to assess the adequacy and implications of a three-year sterilization program in wild female long-tailed macaques in Ubud, Bali. We present the rationales behind the selected methods (surgical approach of endoscopic tubectomy and giant trapping cages for captures) and we describe the demographic population model used to establish the objectives of population growth control. We then present the outcomes of this program and the postoperative monitoring results. 137 females underwent tubectomy over four successive campaigns between 2017 and 2019, which represented 45% of the sexually mature females of the population. The survival rate was very high (96%) six months after sterilization and no major postoperative complication were recorded. No novel pregnancy in treated females was observed, reflecting a 100% success rate of the procedure. Moreover, the surgical approach was also applicable for pregnant females since 26% of the treated females were pregnant at the time of the surgery and 77% of them experienced term delivery. Overall, this study case demonstrates the safety and efficiency of tubectomy sterilization as mean of population control in wild macaques. A demographical and behavioural monitoring is currently in progress to provide a global evaluation of the implications of such programs [less ▲]

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See detailWhen pigtailed macaques cannot select for optimal sleeping sites in degraded habitat
Gazagne, Eva ULiege; Savini, Tommaso ULiege; Ngoprasert, Dusit et al

Conference (2019, October 10)

Primates spend half of their lives in sleeping sites and should select them carefully to maximize fitness. Sleeping site selection in degraded habitat, with reduced availability and quality of resources ... [more ▼]

Primates spend half of their lives in sleeping sites and should select them carefully to maximize fitness. Sleeping site selection in degraded habitat, with reduced availability and quality of resources, is therefore likely to play a leading role in primates’ survival. We aimed to assess the impact of habitat degradation on sleeping site selection patterns in a troop of northern pigtailed macaques, using 3 non-mutually exclusive hypotheses: null hypothesis of random selection, predation avoidance, and food proximity. We identified 107 sleeping sites with only 15 reused sites selected at random in the Sakaerat Biosphere Reserve, northeastern Thailand. After analyzing forest structure at sleeping sites and random sites, we found a general low availability of large and tall trees. Our results show that macaques did not select sleeping sites at random; probability of site selection increased in familiar areas with a high number of stems and with emergent trees. Following the predator avoidance hypothesis, these characteristics are likely to facilitate macaques escape in case of predator attack and also to decrease predator detection at their sleeping sites. Additionally, the food proximity hypothesis seems to be the leading strategy in explaining sleeping sites selection of this degraded habitat. Macaques multiplied their sleeping sites following food distribution, and slept inside or in close proximity to their feeding area, which is likely to maximize their energy intake. Our results highlight the impact habitat degradation may have on sleeping site selection in a flexible species. [less ▲]

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See detailBirth control in urban macaques: Description of an endoscopic tubectomy procedure and post-op monitoring
Deleuze, Stefan ULiege; Polet, Roland ULiege; Gede, Soma et al

Conference (2019, October 10)

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See detailFaire face à une faible disponibilité en fruits dans un habitat dégradé : rôle des plantations chez les macaques à queue de cochon (Macaca leonina) en Thaïlande.
Gazagne, Eva ULiege; José Domínguez, Juan Manuel; Huynen, Marie-Claude ULiege et al

Conference (2019, October 04)

Etudier les facteurs impactant l’utilisation de l’habitat ainsi que les stratégies de recherche alimentaire chez les primates résidents dans des habitats dégradés, est indispensable pour pouvoir mettre en ... [more ▼]

Etudier les facteurs impactant l’utilisation de l’habitat ainsi que les stratégies de recherche alimentaire chez les primates résidents dans des habitats dégradés, est indispensable pour pouvoir mettre en place des stratégies de conservation efficaces. Nous avons étudié l’écologie du mouvement, le domaine vital et les stratégies de recherche alimentaire pendant 14 mois, d’une troupe de macaques à queue-de-cochon du nord (Macaca leonina) de 141± 10 individus dans le fragment forestier dégradé de la réserve de biosphère Sakaerat, située au Nord-Ouest de la Thaïlande. Nous avons analysé ces objectifs en utilisant les méthodes récentes suivantes en fonction de la disponibilité en fruit : les modèles d’Hidden Markov et les polygones caractéristiques de Hull. Nos résultats montrent que la troupe étudiée a un domaine vital total de 599 ha qui couvre la Forêt native Sèche Sempervirente (FSS) et de vieilles plantations d’acacias et d’eucalyptus. Lors des périodes de forte disponibilité en fruits natifs, les macaques recherchent activement de la nourriture à l’intérieur de la FSS (i.e. mouvements lents et variables). A l’inverse, lors des périodes de faibles disponibilités en fruits natifs, les macaques passent plus fréquemment d’un état de recherche alimentaire à un état de transit (i.e. mouvements rapides et orientés). Ils élargissent leurs déplacements aux plantations et zone lisières avec une plus faible fidélité au site quotidienne, bien que les domaines vitaux et trajet parcourus journaliers ne soient pas significativement plus grands. En revanche, les macaques adaptent leur régime alimentaire en consommant significativement plus de fruits secs exotiques comme les graines d’acacia. En combinant pour la première fois de nouvelles analyses sur l’écologie du mouvement et le domaine vital, notre étude montre que les macaques à queue-de-cochon adaptent la dynamique de leur mouvement, leur profil de déplacement ainsi que leur régime alimentaire en fonction de la disponibilité en fruit natif. Ces patrons indiquent que les macaques consomment les ressources prédictibles des plantations et ont tendance à suivre la stratégie de maximisation de l’énergie pour faire face à de faibles disponibilités alimentaires. Cette stratégie énergétique est différente de celle utilisé par leurs congénères habitant la forêt pristine du parc national de Khao Yai située près de Sakaerat, qui ont tendance à minimiser leurs dépenses énergétiques lors de faibles disponibilités en fruit, en diminuant leur domaine vitaux et déplacement quotidiens. Ces résultats approfondissent les connaissances sur l’écologie de cette espèce vulnérable et peu connue, et révèlent un des effets potentiels de la dégradation de l’habitat : la modification des stratégies énergétiques chez les macaques. [less ▲]

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See detailForaging strategies underlying bird egg predation by macaques: A study using artificial nests
Kaisin, Olivier ULiege; Gazagne, Eva ULiege; Savini, Tommaso ULiege et al

in American Journal of Primatology (2018), 80(11),

Bird egg predation is widespread in non-human primates. Although nest predation is often described as opportunistic, little is known about foraging strategies and nest detection in primates. Since it is ... [more ▼]

Bird egg predation is widespread in non-human primates. Although nest predation is often described as opportunistic, little is known about foraging strategies and nest detection in primates. Since it is the prevalent cause of nest failure in the tropics, birds select nest sites within specific microhabitats and use different nest types to increase nesting success. Identifying the nests targeted by the northern pigtailed macaques (Macaca leonina), an omnivorous cercopithecine species, and known nest predator, will shine light on nest foraging strategies in primates. The aim of this research was to reveal if nest predation is a selective or opportunistic feeding behavior. We studied, using artificial nests and camera traps, the influence of nest type (open-cup vs. cavity), microhabitat (i.e., understory density, canopy cover, canopy height, ground cover, and presence vs. absence of thorns and lianas), and nest height, on nest predation by a troop of northern pigtailed macaques in the Sakaerat Biosphere Reserve (Thailand), a degraded environment. In our study, macaque predation on artificial nests was high; out of the200nests thatwereset up, 112were plunderedbymacaques. Althoughpredation ratesdecreasedwithnest height,nest type,andmicrohabitathadnosignificant effecton predation by macaques. Nest detectability and accessibility did not affect predation rates. Macaques actively searched for nests in different microhabitats, suggesting that nest predation by this primate might be considered a selective feeding behavior in this degraded habitat. Consequently, nest predation by this primate might have important conservation implications on the population dynamics of forest-dwelling bird species. Behavior observation methods, such as instantaneous scan sampling, may underesti- mate nest predation by primates, a furtive and cryptic behavior. [less ▲]

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See detailAnalyser les avantages et inconvénients des stérilisations de primates en milieux anthropisés: une étude de cas des macaques balinais
Brotcorne, Fany ULiege; Broens, Damien ULiege; Delooz, Sophie ULiege et al

Conference (2018, October 18)

Les macaques et les hommes sont aujourd’hui contraints de partager leurs habitats, conduisant souvent à des situations conflictuelles lorsque ces premiers prolifèrent en milieux urbains. Ce phénomène ... [more ▼]

Les macaques et les hommes sont aujourd’hui contraints de partager leurs habitats, conduisant souvent à des situations conflictuelles lorsque ces premiers prolifèrent en milieux urbains. Ce phénomène s’accroit en Asie où certaines espèces survivent et tirent profit des habitats anthropisés et de leurs ressources, alors que d’autres sont en déclin. Récemment, les programmes de contrôle des naissances (via stérilisation permanente ou contraception) se multiplient afin de contrôler l’expansion locale de certaines populations dites « à problème ». Cette approche représente une alternative plus éthique à l’élimination, voire dans certains cas à la translocation. Cependant, les effets et les implications de ces programmes restent largement méconnus. Très peu d’études décrivent la manière dont la stérilité provoquée impacte ou non l’environnement social et le comportement des individus traités, ainsi que de leur groupe. L’objectif de notre recherche est d’investiguer les réponses physiologiques, comportementales et sociales de macaques à longue-queue (Macaca fascicularis) femelles adultes inclues depuis 2017 dans un programme de stérilisation (par ligature des trompes) dans le sanctuaire Monkey Forest Ubud à Bali, en Indonésie. A travers un monitoring éthologique comportemental (basé sur +/- 1000 heures de données focales collectées depuis 2017 via la méthode du focal individuel de 15 minutes combiné à des scans de groupe à intervalle de 5 minutes) et démographique (via comptages mensuels systématiques) à long-terme, nous mesurons le niveau d’activités que les femelles mobilisent au regard de leur condition (stérilisées vs. contrôles) et nous quantifions les indicateurs comportementaux d’anxiété (agressions et comportements autodirigés) afin d’évaluer également les implications des stérilisations en termes de bien-être. Pour cette communication, nous décrirons dans un premier temps le contexte de la population cible (i.e., forte densité démographique, et intensification du conflit humain-macaque et de la tension sociale au sein des groupes de macaques), les objectifs du programme de stérilisation (i.e., taux de croissance visé et modélisation du nombre de femelles à stériliser), et les méthodologies utilisées pour les captures et les stérilisations. Dans un second temps, nous présenterons les résultats préliminaires sur le suivi des femelles stérilisées et les différences éventuelles observées avec les femelles contrôles. Lors la première année qui suit leur stérilisation, les femelles montrent des budgets d’activités globalement similaires aux femelles contrôles. Ce résultat à court-terme s’explique par la technique de stérilisation sélectionnée (i.e., ligature des trompes) qui n’annule pas la production de stéroïdes ovariens, et ainsi n’impacte pas directement le comportement. La seconde étape de nos recherches consiste maintenant à analyser l’évolution du profil comportemental sur le long-terme afin d’évaluer l’impact éventuel des cycles non-féconds répétés et de l’absence permanente de nouveaux jeunes chez les femelles stérilisées. Ces implications seront discutées à travers une analyse des avantages et des inconvénients de ce type de programme. [less ▲]

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See detailSurviving in a degraded forest environment: foraging strategies and space use of northern pigtailed macaques (Macaca leonina) in Sakaerat Biosphere reserve, Northeastern Thailand
Gazagne, Eva ULiege; Hambuckers, Alain ULiege; Savini, Tommaso ULiege et al

Conference (2018, July 05)

Space-use patterns and foraging strategy in degraded habitat are crucial to understand the ecology, adaptation, and conservation of primates. However, detailed ranging and behavioral data are scarce for ... [more ▼]

Space-use patterns and foraging strategy in degraded habitat are crucial to understand the ecology, adaptation, and conservation of primates. However, detailed ranging and behavioral data are scarce for many species, especially from Southeast Asia. We aimed to determine the northern pigtailed macaques (Macaca leonina) dietary, ranging, and habitat use patterns in the Sakaerat Biosphere reserve in Northeastern Thailand, a degraded habitat with ancient plantations and sub-optimal resources availability. We studied these patterns for eleven months in regard of fruit availability in a wild troop of these macaques. We used Characteristic Hull Polygons (CHP) combined with spatial statistics to estimate home ranges and core areas. We ran a monthly phenology survey to measure fruit availability over the study period. We predicted that macaques would increase their ranging during low fruit abundance to gather enough food (i.e. energy-maximizing strategy) and would use more intensively plantation and edge areas. We found a total home range of 535.5 ha and an average core area of 219.3 ha, with an average daily path length of 2,226 m. During high fruit abundance, macaques spent more time around fruit-tree species in the dry evergreen forest. During low fruit abundance, they extended their home range to plantations forest and edge areas. Fruit consumption was positively correlated to fruit abundance and there was a clear shift from flesh and pulp to dry fruit during low fruit abundance season. While the portion of home range used decreased in period of high fruit availability, daily path length and core area size did not change. Overall, as predicted, our preliminary data shows that the study troop used an energy-maximizing strategy and was able to expand the range of resources consumed in fruit scarcity period. Conversely, a study done using the same method on the same species in the nearby pristine Khao Yai National park found an energy-minimizing strategy, that is, decreased ranging area in periods of food scarcity. In conclusion, as in previous studies, our results show indeed that northern pigtailed macaques adapt their diet, monthly range and habitat use according to food abundance. However, they indicate they adapt it in an opposite way. In a degraded forest environment, the northern pigtailed macaques seem to change their survival strategy by increasing their range in periods of food scarcity to seek additional resources. These findings pose the question of substantial modification of ecological strategies by species constrained by human alteration of their habitat. [less ▲]

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See detailGastrointestinal Parasites in Captive and Free-ranging Cebus albifrons in the Western Amazon, Ecuador.
Martin, Sarah ULiege; Carrillo Bilbao, Gabriel Alberto; Ramirez, William et al

in International Journal for Parasitology: Parasites and Wildlife (2017)

Currently, there is a lack of surveys that report the occurrence of gastrointestinal parasites in the white-headed capuchin monkey (Cebus albifrons). We therefore assessed the presence and richness ... [more ▼]

Currently, there is a lack of surveys that report the occurrence of gastrointestinal parasites in the white-headed capuchin monkey (Cebus albifrons). We therefore assessed the presence and richness (= number of different parasite genera) of parasites in C. albifrons in wildlife refuges (n = 11) and in a free-ranging group near a human village (n = 15) in the Ecuadorian Amazon. In the 78 samples collected (median of 3 samples per animal), we identified a total of 6 genera of gastrointestinal parasites, representing protozoa, nematodes, acantocephalan and cestodes. We observed a high prevalence (84%) across the 26 individuals, with the most prevalent parasite being Strongyloides sp. (76.9%), followed by Hymenolepis sp. (38.5%) and Prosthenorchis elegans (11.5%). We found Entamoeba histolytica/dispar/moskovskii/nuttalli and Capillaria sp. in only a minority of the animals (3.8%). In addition, we observed unidentified strongyles in approximately one-third of the animals (34.6%). We found a total of 6 parasite genera for the adult age group, which showed higher parasite richness than the subadult age group (5) and the juvenile age group (3). Faecal egg/cyst counts were not significantly different between captive and free-ranging individuals or between sexes or age groups. The free-ranging group had a higher prevalence than the captive group; however, this difference was not significant. The only genus common to captive and free-ranging individuals was Strongyloides sp. The high prevalence of gastrointestinal parasites and the presence of Strongyloides in both populations support results from previous studies in Cebus species. This high prevalence could be related to the high degree of humidity in the region. For the free-ranging group, additional studies are required to gain insights into the differences in parasite prevalence and intensity between age and sex groups. Additionally, our study demonstrated that a serial sampling of each individual increases the test sensitivity. [less ▲]

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See detailIntergroup variation in robbing and bartering by long-tailed macaques at Uluwatu Temple (Bali, Indonesia)
Brotcorne, Fany ULiege; Giraud, Gwennan ULiege; Gunst, Noelle et al

in Primates: Journal of Primatology (2017)

Robbing and bartering (RB) is a behavioral practice anecdotally reported in free-ranging commensal macaques. It usually occurs in two steps: after taking inedible objects (e.g., glasses) from humans, the ... [more ▼]

Robbing and bartering (RB) is a behavioral practice anecdotally reported in free-ranging commensal macaques. It usually occurs in two steps: after taking inedible objects (e.g., glasses) from humans, the macaques appear to use them as tokens, returning them to humans in exchange for food. While extensively studied in captivity, our research is the first to investigate the object/food exchange between humans and primates in a natural setting. During a 4-month study in 2010, we used both focal and event sampling to record 201 RB events in a population of long-tailed macaques (Macaca fascicularis), including four neighboring groups ranging freely around Uluwatu Temple, Bali (Indonesia). In each group, we documented the RB frequency, prevalence and outcome, and tested the underpinning anthropogenic and demographic determinants. In line with the environmental opportunity hypothesis, we found a positive qualitative relation at the group level between time spent in tourist zones and RB frequency or prevalence. For two of the four groups, RB events were significantly more frequent when humans were more present in the environment. We also found qualitative partial support for the male-biased sex ratio hypothesis [i.e., RB was more frequent and prevalent in groups with higher ratios of (sub)adult males], whereas the group density hypothesis was not supported. This preliminary study showed that RB is a spontaneous, customary (in some groups), and enduring population-specific practice characterized by intergroup variation in Balinese macaques. As such, RB is a candidate for a new behavioral tradition in this species. [less ▲]

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See detailReproduction control as management strategy for local overpopulation of primates in tropical human-dominated habitats: a review
Brotcorne, Fany ULiege; Wandia, Nengah; Poncin, Pascal ULiege et al

Conference (2017, February 08)

Today, anthropogenic pressures are posing major challenges to Asian primates, forced either to adapt ecologically and behaviourally to the human massive encroachment into natural habitats, or to disappear ... [more ▼]

Today, anthropogenic pressures are posing major challenges to Asian primates, forced either to adapt ecologically and behaviourally to the human massive encroachment into natural habitats, or to disappear. Species ability to survive in human-modified habitats greatly varies, with generalist species, such as Cercopithecines, being more likely to thrive. Several macaque species in particular proliferate in situations of commensal association with humans, which leads sometimes to local overpopulation. High density of primates, resulting from the combined effect of population spatial compression and positive demographics, systematically induces conflicts with humans over crop-raiding and nuisance issues. Different management strategies have been deployed these last decades, going from culling or trapping programmes to sterilization campaigns. Sterilization is an ethical and flourishing solution to mitigate the human-macaque conflict by limiting the population expansion, but very few empirical data are available about their efficiency and potential side effects. We propose here to review various macaque sterilization programmes conducted in Asia, highlighting the pros and cons as well as the short- and long-term effects. As a study case, we will present data on population dynamics and side behavioural effects, as the base for an ongoing sterilization programme in a population of long-tailed macaques (M. fascicularis) in Bali (Indonesia). This population has experienced a tenfold increase over the last 30 years. Vasectomy undergone by several males in a former approach was not efficient to limit births. With others, we argue that macaque’s reproductive profile requires female sterilization. The goal here is to stimulate discussion over management of forced coexistence scenarios between human and primates, since this phenomenon is an integrative part of conservation in this rapidly changing world. [less ▲]

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See detailPersistence of the effec of frugivore identity on post-dispersal seed fate: consequences for the assessment of functional redundancy
Lugon, Ana Paula; Boutefeu, Marion; Bovy, Emilie et al

in Biotropica (2017)

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