Feeding ecology, and ranging behavior of Callicebus nigrifrons (Primates: Pitheciidae)

Orientador: Eleonore Zulnara Freire SetzDissertação (mestrado) - Universidade Estadual de Campinas, Instituto de BiologiaResumo: O gênero Callicebus corresponde ao segundo maior gênero de primatas Neotropicais, sendo composto por 29 espécies. Embora bastante diverso, menos de um terço das espécies conhecidas foram sujeitas a estudos ecológicos e comportamentais. Para varias delas dispomos apenas de informações sobre sua distribuição geográfica. Este trabalho teve como principal objetivo estudar o comportamento alimentar e o uso do tempo e espaço por Callicebus nigrifrons, comparando os resultados aqui encontrados com aqueles disponíveis para outros Callicebus. Assim como as demais espécies do gênero, C. nigrifrons utilizou um grande numero de espécies (62) e famílias (28) vegetais como fonte de alimento, sendo os frutos os itens mais importantes em sua dieta (53%). As folhas corresponderam ao segundo item alimentar mais utilizado (16%) e, diferentemente de maioria das espécies de sauás, o consumo de invertebrados e flores representou uma grande parcela da dieta (20%). Como previsto pela teoria de forrageamento ótimo, C. nigrifrons parece preferir itens de maior valor energético (frutos carnosos), incluindo itens de menor valor a medida que a disponibilidade de itens de maior qualidade diminui no ambiente. No entanto, itens de menor qualidade, como folhas, estiveram sempre presentes na dieta, mesmo em períodos de grande abundancia de frutos, mostrando a importância da manutenção de uma dieta balanceada. Com relação ao uso de tempo, os sauás passam grande parte do dia se alimentando (35%), distribuindo o restante de seu tempo principalmente em descanso (30%) e deslocamento (24%). Nos meses com maior consumo de folhas os animais adotaram uma estratégia de baixo custo / baixo retorno, alocando mais tempo em descanso e deslocandose de forma mais lenta. A área de vida ocupada pelos animais, com cerca de 8 ha, esta dentro do que já foi estimado para outras espécies do gênero, assim como a distancia media percorrida diariamente (573 m). Embora o tamanho da área de vida utilizada não tenha variado entre as estações com maior e menor disponibilidade de frutos, os sauás concentraram suas atividades em regiões distintas em cada período. O uso dos diferentes tipos de vegetação ao longo do ano não parece ter sido determinado pela contribuição proporcional de cada uma, mas sim pela disponibilidade de recursos alimentares nestes ambientes. Tanto o comportamento do casal estudado como o dos grupos do entorno, dão indícios de que C. nigrifrons apresenta comportamento territorial sazonal, acompanhando a variação da disponibilidade de frutos zoocóricos.Abstract: With 29 species, Callicebus is the second largest genus of Neotropical primates. Although quite diverse, less than a third of the known species was subject to ecological and behavioral studies. For several of them we just have information about its geographical distribution. Here we study the activity pattern and the ranging and feeding behavior of Callicebus nigrifrons and compare these results with those available for other Callicebus. As well as other titi monkeys, C. nigrifrons feed on a wide range of plant species (62) and families (28), fruits being the most important items in its diet (53%). The leaves were the second most consumed food resource (16%) and, unlike most of Callicebus species, the invertebrate and flowers consumption represented a great portion of its diet (20%). As predicted by the optimal foraging theory, C. nigrifrons seems to prefer high-quality foods (like fleshy fruits), including low-quality foods as the availability of the first ones decreases. Items of lower quality, such as leaves, were always consumed, even in periods of great abundance of fruits, showing the importance of maintaining a balanced diet. These animals spend most of their time feeding (35%), followed by resting (30%) and moving (24%). In months with larger consumption of leaves the animals adopted a low cost/low return strategy, spending more time resting and moving more slowly. Titis ranged over an area of about 8 ha and traveled over an average path length of 573 m, which agrees with those already described for other species of the genus. Although home range did not vary among the different periods of fruit availability, the titis concentrated their activities in different areas in each period. The use of the different vegetation types along the year did not seem to be related with their proportional contribution, but with the availability of food resources in these. The behavior of the studied titi couple, as well as that of the groups surrounding them, indicates that C. nigrifrons exhibit seasonal territorial behavior, accompanying the fluctuation of flesh fruit supply.MestradoMestre em Ecologi

Territorial behavior of Callicebus nigrifrons Spix, 1823 (Pitheciidae) : influence of fruits availability and possible functions of long calls

Orientadores: Eleonore Zulnara Freire Setz, Júlio César Bicca-MarquesTese (doutorado) - Universidade Estadual de Campinas, Instituto de BiologiaResumo: A territorialidade corresponde a uma forma de competição na qual competidores expulsam uns aos outros de áreas contendo recursos, os territórios. A defesa de territórios pode ser flexível, sendo manifestada apenas quando existirem recursos críticos que limitem o crescimento da população (frequentemente representados pela disponibilidade de alimento) e quando estes forem economicamente defensáveis. Os primatas do gênero Callicebus são geralmente descritos como territoriais, embora esta caracterização baseie-se em estudos focados em apenas três das 30 espécies conhecidas desse gênero diverso de primatas Neotropicais. Ainda, a manifestação de comportamentos relacionados à territorialidade se mostrou bastante variável em estudos anteriores, podendo estar relacionada à curta duração desses trabalhos, os quais não contemplaram os efeitos da variação sazonal de recursos alimentares na manifestação desses comportamentos. Nesse contexto, investigamos o comportamento territorial de Callicebus nigrifrons, analisando a influencia da variação na disponibilidade de frutos sobre este comportamento. Buscamos também analisar o papel das vocalizações de longo alcance, geralmente associadas à defesa conjunta de território, mas que também pode estar relacionada a defesa de parceiros reprodutivos. Para isso monitoramos o comportamento de um grupo habituado de C. nigrifrons ao longo de 20 meses (Novembro/2009 - Junho/2011; 730 horas de observação) paralelamente ao monitoramento da disponibilidade de frutos de 22 espécies zoocoricas consumidas por estes primatas. Adicionalmente, analisamos a estrutura dos cantos de longo alcance de nove grupos de C. nigrifrons e relacionamos a estrutura desses cantos aos contextos nos quais estes são utilizados. Também realizamos experimentos com "playbacks" para investigar a importância das vocalizações de longo alcance na defesa conjunta de territórios e de parceiros. As vocalizações de C. nigrifrons apresentaram estrutura hierárquica, cuja combinação de unidades menores, as silabas, dá origem as frases, que são então combinadas em seqüências mais longas. Estas vocalizações de longo alcance são utilizadas tanto para comunicação entre membros do mesmo grupo, como para comunicação entre grupos vizinhos e, embora sejam compostas por unidades vocais semelhantes (mesmas silabas e frases), apresentam estruturas diferentes associadas a estes diferentes contextos comportamentais. Os cantos utilizados para comunicação entre grupos vizinhos foram utilizados principalmente para defesa de recursos alimentares importantes na dieta desses primatas. Diferente de outros Callicebus, C. nigrifrons não exibiu comportamento de defesa e patrulhamento das bordas de sua área de vida, mas focaram o comportamento de defesa em áreas com recursos alimentares importantes e economicamente defensáveis, como arvores frutíferas. Esse comportamento de defesa, tanto pela emissão de vocalizações de longo alcance, quanto pelo uso de outros comportamentos agressivos, resultaram na expulsão de grupos vizinhos que se aproximassem de sua área de uso, e variou em intensidade de acordo com a disponibilidade de frutos no ambiente. A baixa freqüência de encontros entre nosso grupo focal e grupos vizinhos sugere que os comportamentos adotados por C. nigrifrons são efetivos para garantir o acesso prioritário a recursos alimentares importantes em sua dietaAbstract: Territoriality is a form of competition in which competitors exclude each other from areas containing resources, the territories. Territorial behaviors are flexible and should be adopted only when there is critical resource shortage (which limits population growth) and when these are economically defensible. Callicebus monkeys are usually described as territorial, although this characterization is based on studies focused on three of the 30 known species of this diverse genus of Neotropical primates. Still, the expression of behaviors related to territoriality showed a variable pattern in previous studies. Part of these variations within Callicebus genus could be a result of the short duration of these studies, which did not contemplate the effects of seasonal variation of food resources on territorial behavior. Here we investigated the territorial behavior of Callicebus nigrifrons, evaluating the influence of fruit availability over it. We also evaluated the role of C. nigrifrons loud calls in intra and extra group communication, as well as on food and mate defense. We thus monitored the behavior of a habituated group of C. nigrifrons over a period of 20 months (November/2009 - June/2011; 730 observation hours in total). In parallel to behavioral data collection we monitored the availability of fruits from 22 species eaten by these primates. We also described the structure of loud calls of nine groups of C. nigrifrons and related the structure of these calls to the contexts in which they were used, and performed playback experiments to test the hypotheses of mate and joint territorial defense. Callicebus nigrifrons loud calls are higher hierarchical structures formed by different small units, the syllables, which are assembled to form phrases, which are then assembled to form long sequences, the loud calls. These calls are used in different contexts, involving the communication within and between groups. Although these calls are composed by basically the same syllable and phrase types, the proportional contribution of the different syllable and phrases and the way they are assembled differ between these different contexts. The loud calls used for extra group communication was more clearly associated to joint resource defense of important food recourses in C. nigrifrons diet, the fruits. Unlike previews studies of Callicebus spp., C. nigrifrons did not show the behavior of patrolling and marking range boundaries, but advertised the occupancy of its range via loud call emissions, especially from places close to important and economically defensible food sources, such as fruits. The intensity of the defensive behavior, via loud call emissions and aggressive approach and repulsion of neighboring groups, increased with fruit availability. The low frequency of inter-group agonistic encounter suggest that territories ownership advertisement by C. nigrifrons are effective in maintaining the priority access to important food resourcesDoutoradoEcologiaDoutora em Ecologi

Feeding Ecology And Activity Pattern Of Black-fronted Titi Monkeys (callicebus Nigrifrons) In A Semideciduous Tropical Forest Of Southern Brazil.

Most aspects of the ecology and behavior of Callicebus nigrifrons are still unknown. The information available about this species is mainly based on a few studies that also focused on other Callicebus. We examined the feeding behavior and activity pattern of a free-ranging pair of C. nigrifrons between March and November 2007 in an area of semideciduous tropical forest of southeastern Brazil. The study site is located at the southern limit of the Tropical Zone and is characterized by pronounced seasonality. As observed for other Callicebus monkeys, fruits were the most consumed food resource, accounting for 53% of the diet, which was complemented mainly by leaves (16%) but also by invertebrates and flowers (10% of each). A great variety of plant families (28) and species (62) were included in the diet. The titis spent 35% of their time feeding, distributing the remaining time between resting (30%) and traveling (24%). Data presented here indicate that C. nigrifrons prefer high-quality food items (fruit pulp), adding low-quality food items (such as leaves) as the availability of the higher-quality foods decreases. The amount of time spent traveling and resting did not change between seasons, but the time invested in feeding increased during the lean period. The activity pattern was not related to fruit availability, but in months with lower temperatures, monkeys spent more time feeding. We suggest that the feeding ecology and activity pattern of C. nigrifrons reflect adaptations related to annual fluctuations in food availability and temperature, respectively.52351-

From dropping to dropping: the contribution of a small primate to seed dispersal in Atlantic forest

The dynamic interaction between animals and plants through frugivory and seed dispersal is one of several ecological processes that modulates tropical biodiversity. Here we evaluated the potential role of a highly-frugivorous Neotropical primate, the black-fronted titi monkey (Callicebus nigrifrons), as seed disperser. We studied two titi monkey groups in semideciduous Atlantic Forest remnants. Each group fed on over 49 zoochorous plant species in about one year and ingested seeds from nearly a half of them, especially those with small seeds (< 0.5 cm). The groups of titi monkeys defecated a large number of seeds, reaching over 300 seeds per day (1-305). More than half of the total deposited seeds and seed species germinated after gut passage, however gut passage reduced germination success in three of five evaluated species. Feces were deposited in small clumps distributed across groups' home range. We suggest that the observed distribution pattern of feces may enhance plant reproductive fitness by increasing the probability of seeds being deposited far from parent plants, in novel and favorable sites. We concluded that the seed handling and deposition behavior of black-fronted titi monkey make this primate an important agent for Atlantic forest regeneration100CAPES - Coordenação de Aperfeiçoamento de Pessoal e Nível SuperiorFAPESP – Fundação de Amparo à Pesquisa Do Estado De São Paulosem informação2008/05127-0; 2010/04034-9; 2009/12124-

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

For arboreal primates, ground use may increase dispersal opportunities, tolerance to habitat change, access to ground-based resources, and resilience to human disturbances, and so has conservation implications. We collated published and unpublished data from 86 studies across 65 localities to assess titi monkey (Callicebinae) terrestriality. We examined whether the frequency of terrestrial activity correlated with study duration (a proxy for sampling effort), rainfall level (a proxy for food availability seasonality), and forest height (a proxy for vertical niche dimension). Terrestrial activity was recorded frequently for Callicebus and Plecturocebus spp., but rarely for Cheracebus spp. Terrestrial resting, anti-predator behavior, geophagy, and playing frequencies in Callicebus and Plecturocebus spp., but feeding and moving differed. Callicebus spp. often ate or searched for new leaves terrestrially. Plecturocebus spp. descended primarily to ingest terrestrial invertebrates and soil. Study duration correlated positively and rainfall level negatively with terrestrial activity. Though differences in sampling effort and methods limited comparisons and interpretation, overall, titi monkeys commonly engaged in a variety of terrestrial activities. Terrestrial behavior in Callicebus and Plecturocebus capacities may bolster resistance to habitat fragmentation. However, it is uncertain if the low frequency of terrestriality recorded for Cheracebus spp. is a genus-specific trait associated with a more basal phylogenetic position, or because studies of this genus occurred in pristine habitats. Observations of terrestrial behavior increased with increasing sampling effort and decreasing food availability. Overall, we found a high frequency of terrestrial behavior in titi monkeys, unlike that observed in other pitheciids. © 2019, Springer Science+Business Media, LLC, part of Springer Nature