Vol.:(0123456789) 1 3
Primates (2021) 62:199–206
https://doi.org/10.1007/s10329-020-00859-6
ORIGINAL ARTICLE
For emergency only: terrestrial feeding in Coimbra-Filho’s titis reflects
seasonal arboreal resource availability
João Pedro Souza-Alves
1,6,7
· Fabricio B. Baccaro
2
· Isadora P. Fontes
3
· Marcela A. Oliveira
4
·
Nichollas Magalhães O. Silva
5
· Adrian A. Barnett
1,6
Received: 15 April 2020 / Accepted: 14 August 2020 / Published online: 29 August 2020
© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2020
Abstract
Terrestriality in Platyrrhine primates is primarily associated with low arboreal resource availability, low predation risk
when on the ground and increased contact time with human observers. To test the relationship between these variables and
ground use frequency, we studied a group of endangered Coimbra-Filho’s titi monkeys (Callicebus coimbrai) in a 14-ha for-
est fragment in north-eastern Brazil. Terrestriality data were collected on a monthly basis (33 months) using scan sampling
procedures from July 2008 to July 2012. Overall, Coimbra-Filho’s titi monkeys were recorded during 0.6% of observation
time (113 out of 18,164 scans) on the ground. Most of the time on the ground was spent feeding on young leaves (71 records)
and the least amount of time on fruits (14 records). Availability of arboreal foods, rainfall, and time of contact with human
observers did not influence overall terrestrial behaviour (ground use). However, the timing and nature of the monkeys’ terres-
trial feeding was strongly related to the absence of arboreal fruit (β-estimate = −3.078) and young leaf (β-estimate = −3.515)
food resources. We suggest that terrestrial feeding by Coimbra-Filho’s titi monkeys could be an adaptation to low arboreal
fruit availability and the exploitation of alternative food resources.
Keywords Arboreal food resources · Brazil · Callicebus coimbrai · Human habituation · Predation risk · Predator-sensitive
foraging
Introduction
Within the landscape of fear (sensu Laundré et al., 2001:
topic review Bleicher 2017), the presence and disper-
sion of predators may have a profound effect on primate
behaviour. This includes the period when researchers are
habituating study animals so that their presence even-
tually causes minimal stress and impact on the primate
study group (Williamson and Feistner 2003). During this
time, the presence of humans can affect the behaviour of
unhabituated or partially habituated animals, provoking
alarm calling (Bezerra and Souto 2008), reducing the
time spent feeding, grooming, and resting, and increasing
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s10329-020-00859-6) contains
supplementary material, which is available to authorized users.
* João Pedro Souza-Alves
souzaalves1982@gmail.com
1
Programa de Pós-graduação em Ciências Biológicas
(Zoologia), Universidade Federal da Paraíba,
João Pessoa 58051-900, Brazil
2
Departamento de Biologia, Universidade Federal
do Amazonas, Manaus, Amazonas 69067-005, Brazil
3
Secretaria Municipal de Meio Ambiente de Sergipe, Aracaju,
Sergipe 49097-270, Brazil
4
Programa de Pós-graduação de Biodiversidade e
Biotecnologia da Amazônia Legal, Universidade Federal de
Rondônia, Campus José Ribeiro Filho, Porto Velho, Brazil
5
Programa de Pós-graduação Em Desenvolvimento Regional e
Meio Ambiente, Universidade Federal de Rondônia, Campus
José Ribeiro Filho, Porto Velho, Brazil
6
Laboratório de Ecologia, Comportamento e Conservacão
(LECC), Departamento de Zoologia, Universidade Federal
de Pernambuco, Recife, Brazil
7
Present Address: Department of Zoology, Post-Graduate
Program in Animal Biology, Federal University
of Pernambuco, Av. Professor Morais Rego, 1235, Cidade
Universitária, Recife, PE 50670-901, Brazil
Author's personal copy