Response of frugivorous primates to changes in fruit supply in a northern Amazonian forest

Abstract

Few attempts have been made to understand how spatiotemporal changes in fruit supply influence frugivores in tropical forests. The marked spatiotemporal variation in fruit supply can affect frugivore abundance and distribution, but studies addressing the effects of this variation on primates are scarce. The present study aimed to investigate how the spatiotemporal distribution of fruits influences the local distribution of three frugivorous primates in the eastern part of the Maracá Ecological Station, a highly seasonal Amazonian rainforest. Specifically, it was hypothesised that primate distribution will track changes in fruit supply, resulting that sites with high fruit availability should be heavily used by primates. During a 1-year study, fruit supply (ground fruit surveys) and primate density (line-transects) were monitored in twelve 2 km-long transects at monthly intervals. Fruit supply varied seasonally, being low during the dry season. The density of Ateles belzebuth was positively related to fruit supply during fruit shortage, but Cebus olivaceus and Alouatta macconnelli did not follow the same pattern. The supply of Sapotaceae fruit was an important component determining local distribution of A. belzebuth during the overall fruit shortage. Highly frugivorous primates such as A. belzebuth respond to seasonal decline in fruit supply by congregating at places with high fruit supply in this forest, particularly, those with many individuals of species of Sapotaceae. This study underscores the importance of small-scale spatiotemporal changes of fruit supply as a key component of frugivorous primate ecology in highly seasonal environments.Keywords: Amazonia, Maracá Ecological Station, primate distribution, seasonal fruit availability, fruit shortage. Resposta dos primatas frugívoros à variação na oferta de frutos em uma floresta do norte da Amazônia ResumoPoucas tentativas foram realizadas para entender como a variação espaço-temporal na oferta de frutos influencia os frugívoros nas florestas tropicais. A variação espaço-temporal dos frutos pode afetar a abundância e distribuição dos frugívoros, mas estudos abordando os efeitos desta variação nos primatas são escassos. Neste estudo, investigou-se como a oferta dos frutos afeta a distribuição local de três espécies de primatas frugívoros na parte leste da Estação Ecológica de Maracá, uma floresta sazonal na Amazônia. Especificamente, testou-se a hipótese de que a distribuição dos primatas acompanharia a variação na oferta de frutos, resultando em uma utilização mais frequente pelos primatas dos locais com maior disponibilidade deste recurso. A disponibilidade de frutos e a densidade dos primatas foram registradas mensalmente ao longo de um ano, em 12 transecções com 2 km de extensão. A oferta de frutos variou sazonalmente, sendo baixa durante a estação seca. A densidade de Ateles belzebuth se relacionou com a oferta dos frutos durante o período de escassez deste recurso, mas Alouatta macconnelli e Cebus olivaceus não seguiram o mesmo padrão. A oferta d...

Fruit availability drives the distribution of a folivorous–frugivorous primate within a large forest remnant

“…The relationship between their spatial distribution and the availability of fruit is compatible with such strategy. “Camping” behavior at productive fruit patches was also reported for other atelids [e.g., Alouatta palliata : Hopkins, ; A. caraya : Zunino, ; A. seniculus : Palacios & Rodríguez, ; Ateles belzebuth : Mourthé, ; Brachyteles arachnoides : Strier, ; B. hypoxanthus : Talebi & Lee, ; Lagothrix lagotricha : Di Fiore, ; Gonzalez, Clavijo, Betancur, & Stevenson, ], suggesting that it represents a common strategy for maximizing energy intake and/or monopolizing the access to valuable and highly seasonal foods.…”

“…The dependence of primates on their plant food sources might lead them to show patterns of habitat use, that reflect the spatial distribution (frequently clumped) of their preferred foods [e.g., ripe fruits and young leaves: Hopkins, ; Milton, ; van Schaik et al, ; Zimmerman et al, ]. This dependence explains why seasonal variations in fruit supply had a stronger influence on the spatial distribution of the highly frugivorous Ateles belzebuth , than on the less frugivorous Cebus olivaceus and Alouatta macconnelli (Mourthé, ). However, the frequent use of indirect estimators of food availability [e.g., tree species richness, vegetation type, and basal area of preferred food sources; see Anzures‐Dadda & Manson, ; Gómez‐Posada, Martínez, Giraldo, & Kattan, ; Hopkins, ; Thomas, ] have limited the power for testing how within‐site spatiotemporal differences in habitat quality influence primate spatial distribution, group size, and abundance, because they measure “potential,” not necessarily actual food availability.…”

Terrestrial Behavior in Titi Monkeys (Callicebus, Cheracebus, and Plecturocebus): Potential Correlates, Patterns, and Differences between Genera

“…Such variation is compatible with the hypothesis that other factors (probably local ones) are more influential than human contact. Changes in resource distribution and availability influence habitat choice (Camaratta et al 2017;Mourthé 2014), resource selection and foraging strategies (Nagy-Reis and Setz 2017), and forest strata use (Ding and Zhao 2004) by primates. Titi monkeys may also adjust diet composition in response to variations in fruit availability and often use the lower forest strata (0.5 to 10 m) during periods of fruit scarcity (Acero-Murcia et al 2018;Bicca-Marques and Heymann 2013;Caselli and Setz 2011;Souza-Alves et al 2011).…”

Effects of Local Habitat Variation on the Behavioral Ecology of Two Sympatric Groups of Brown Howler Monkey (Alouatta clamitans)

“…In turn, these environmental variables will affect the structure and composition of local plant communities contributing to the heterogeneity in local ecological resources and conditions available to primates [ 2 ]. Primates with large home ranges negotiate such fine-grained heterogeneity by traveling across the landscape seeking out patches of high quality habitat (e.g., [ 3 , 4 , 5 ]). Species with small home ranges however, may need to restrict their ranges to areas of higher quality habitats if they are to find their preferred foods while avoiding competitors and predators (e.g., [ 4 , 6 , 7 , 8 ]).…”

“…Primary consumers are challenged with the highly variable nutritional content and spatiotemporal distribution of their potential foods [ 3 , 4 , 24 – 26 ]. In a folivorous-frugivorous diet such as that of the howler monkeys, increased leaf consumption is hypothesized to lead to an increased feeding time because leaves are low in energy and more food is needed to achieve satiation [ 3 , 27 , 28 ].…”