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Mastozoología neotropical

versión impresa ISSN 0327-9383versión On-line ISSN 1666-0536

Mastozool. neotrop. vol.25 no.2 Mendoza dic. 2018



Examining individual risk-taking in Leontopithecus caissara (Primates, Callitrichidae): group order when arriving at and departing from sleeping sites


Rodrigo F. Moro-Rios1, 2, Andreas L. S. Meyer1, José E. Silva-Pereira1 and Gabriela Ludwig1, 3

1 Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil. [Correspondence: Rodrigo F. Moro-Rios <>].

2 Department of Anthropology, Durham University, Durham, United Kingdom.

3 Centro Nacional de Pesquisa e Conservação de Primatas Brasileiros, Paraíba, Brazil.


Monkey groups travel in line, exposing individuals to differential risks according to their position. We recorded events of arriving and departing from the sleeping site in a group of Leontopithecus caissara to investigate how the highest risk position is shared among group-mates during those events. We found the dominant male was the first to arrive and depart from the tree hole on most occasions. This finding suggests that the dominant adult male assumed higher risks and played a differential role in predator defense, possibly creating direct benefits for subordinate individuals to stay in the group.


Examinando a tomada de riscos em Leontopithecus caissara (Primates Callitrichidae): Ordem de entrada e saída do sítio de pernoite.

Grupos de primatas se deslocam em fila de maneira que cada indivíduo se encontra exposto a um risco de predação diferenciado de acordo com o lugar ocupado por ele. Nós registramos os eventos de chegada e saída do sítio de dormida de um grupo de Leontopithecus caissara de maneira a investigar quais indivíduos do grupo ocupam a posição de maior risco na fila. Nossos resultados demonstram o macho dominante como sendo o indivíduo a ocupar a posição de maior risco na maioria das ocasiões. Assim, o macho adulto dominante assumiu maiores riscos e um papel destacado no comportamento anti-predatório de maneira a criar benefícios diretos ao indivíduo subordinado que permaneceu no grupo em tal condição.

Key words: Individual roles; Mobbing; Predator avoidance; Sleeping sites; Social structure.

Palavras-chave: Comportamento anti-predatório; Estrutura social; Função social individual; Sítio de dormida.

Recibido 11 marzo 2017.
Aceptado 14 febrero 2018.

Editor asociado: M. Kowalewski

The probability of an individual in a social group being captured during a predation attempt is influenced by its within-group positioning (Hirsch 2007). In the case of traveling, the first individuals in a progression line are presumed to face higher risk of predation (Bumann et al. 1997). The same logic can be applied to retiring at night and arising the next day in species that use shelters, when the first individual to enter or leave faces higher risks (Heymann 1995; Day & Elwood 1999).

Predators have been observed taking advantage of a known sleeping site location, visiting the site often and choosing periods when their prey arrive at and/or depart from the shelter (Franklin et al. 2007; Emsens et al. 2014). Traveling in a coordinated line towards the sleeping site would increase the predation risk for the individual in front of the group, while it would give the remaining individuals a chance to escape (Heymann 1995; Day & Elwood 1999; Franklin et al. 2007). In this sense, understanding individual order in line under a risky context might lead to a better understanding of the roles played by each individual in a mammalian society, as well as the related costs and benefits of social life for individuals from different classes of age, sex and hierarchy.

Callitrichids are small primates (<700g) that suffer high predation pressure and frequently use tree holes as shelters (Stafford & Murad Ferreira 1995; Kappeler 1998). When retiring, callitrichids show cautious behaviors such as moving fast and in line towards the sleeping site, a highly coordinated behavior that hypothetically reduces the chances of predation (Heymann 1995; Day and Elwood 1999; Franklin et al. 2007). Predation risk is also high the next day as predators are likely to ambush their prey as they are arising (Smith et al. 2003; Emsens et al. 2014). Ocelots have already been observed in an attempt to hunt lion tamarins during arising time, pointing to the potential costs of being the first in line while retiring to and departing from the sleeping site (Nascimento 2008). Moreover, predation is not the only risk faced by the first individual to enter in the tree hole as animals such as bees, ants, snakes, and other potentially harmful species may compete for that hole (Moro-Rios personal observation).

As in most callitrichids, lion tamarins—genus Leontopithecus—live in small multi-male, multi-female groups with a cooperative infant care system (Garber et al.2015). Here, we investigate how individuals of a group of black-faced lion tamarins L. caissara shared the risks of assuming the front during arrival and departure from the sleeping sites. Our aim is to bring new insights to how the possible costs of predation are shared within a primate group.

We conducted this study at the Superagui National Park, Brazil (25°27¢S, 48°13¢W) between April 2008 and June 2009. The study group went through a process of habituation preceding the data collection period and was the focal group in 400 hours of direct observation. It was composed of one dominant male, one subordinate male, one dominant female, and two male juveniles. The individual hierarchical class was defined based on the index of combined attacks (Bayly et al. 2006) obtained from sampling all observed aggression. The dominant male was the only individual observed to mount and breed with the group female, suggesting he is also the putative breeding male.

To investigate the influence of individual identity on the position while departing and arriving, we performed a Generalized Linear Mixed Model (GLMM) assuming a Poisson distribution of the residuals. We set individual identity as a categorical predictor of the order of the animals in a line while arriving to and departing from a tree hole. We also added a control variable to account for the possible effects of the action performed (departing x arriving) on individuals’ ordination. Finally, we numbered each event and treated each event as a discrete variable to be included as a random factor in our full model and then allowed to test whether the group order varies case by case (by chance) or follows a pattern in the comparison between the full and the null model (see below). We found no evidence of overdispersal (χ2=35.7, P=1, p=0.27) and our model has shown good stability coefficients.

The results of a Mann-Whitney test between the positioning observed during arrivals and departures from the tree hole for all subjects showed no overall difference between the samples (BM: U=235.5, N=46, P=0.781; HM: U=289, N=46, P=0.314, BF: U=217.5, N=46, P=0.503, J1: U=270, N=46, P=0.585, J2: U=250.5, N=46, P=0.933). Based on this homogeneity, in all subsequent analyses the entire data set for each individual (entering and leaving) were combined into a single data set.

We then compared the fit of a full model with that of the null model comprising only the action performed and the random factor using a likelihood ratio test (Dobson 2002). All analyses were carried out in R 3.1.1 (R Core Team 2014) using the lme4 1.1-8 package, designed for GLMM analysis (Bates et al. 2015).

In our observations, males were recorded as the first individual to enter or to leave the tree hole on 87% of the occasions (Dominant male: 63% (n=29), subordinate male: 24% (n=11), female: 6.5 % (n=3), juveniles: 6.5 % (n=3)). The group was observed utilizing 8 sleeping sites. On all occasions individuals entered the tree hole one by one following the first, who always looked inside the hole several times before entering. In the next morning, the first individual to leave the tree hole always remained alone visually scanning all directions for a few moments, before he was joined by other individuals. On two occasions the sleeping site was rejected by the individual in the front following the inspection made from outside and a quick entrance into the hole. On one occasion a bee colony was occupying the tree hole and attacked the first individual in line during the inspection at the entrance of the hole.

The model explaining individuals position was significant (likelihood ratio test: χ2=13.51, df=3, p= 0.0043). There was a significant effect of the individual identity on the individuals order during the movements of arriving and departing from the tree hole and that effect is particularly significant due to the comparison between the female and the dominant male (Table 1).

Table 1
Estimated effect, standard error, confidence intervals and P-values for each individual from a group of Leontopithecus caissara as predictor of order in line while arriving to and departing from the tree hole. The results for the Dominant male are not presented because it was the dummy variable used as an index to test the effects of other classes in comparison to it.

In addition to our results, we made six observations of mobbing: one involving a black vulture (Coragyps atratus), one involving brown capuchin monkeys (Sapajus nigritus), one involving a tegu lizard (Tupinambis merianae), one involving azure jays (Cyanocorax caeruleus) and two involving unidentified forest raptors (Falconiformes). On all occasions, the animal who moved directly toward the potential threat was the dominant male. The subordinate helper male and the breeding female positioned themselves between one and three meters apart from BM, initiated alarm calls and moved either towards or away from BM. On all occasions, the juveniles moved to a position away from the threat, hidden behind a vertical tree trunk while occasionally staring in the direction of the treat. All episodes were not recorded near either sleeping sites or during retiring time.

The decision made by an individual on how to position itself relative to its group mates is an underappreciated factor that certainly modulates how different selective pressures define inclusive fitness (Schmitt & Di Fiore 2015). Here, we found that in a group of L. caissara the individual order during coordinated linear movements arriving at and departing from sleeping sites was not random. The following discussion aims to compare our results to the risk-taking patterns observed for other primate species and to build some hypothesis to explain the pattern observed here. However, we would like to emphasize that this study presents results from a short-term research on a single group. Thus, further research is needed to test any causal hypothesis related to the risk-taking pattern observed here.

Dominant individuals in primate groups have been reported to optimize their socio-spatial position in order to have better access to feeding resources and avoid predation (Teichroeb et al. 2015). Thus, one might hypothesize that dominant individuals would choose the best positions in line during highly coordinated movements. Here, we report a different pattern where the dominant animal assumed a higher risk position in a dangerous situation. Subtle forms of cooperation from a dominant animal, like taking certain positions during risky situations, may cause great benefits to its presumed offspring survival and subordinate individuals whose act as helpers (Snowdon & Ziegler 2007). Direct benefits to certain individuals staying in the group as subordinate helpers might have favored the evolution of cooperative infant care (Dunbar 1995). One of the proposed benefits to stay and help as a subordinate is the safety provided by group life (Dunbar 1995). Thus, one may hypothesize that the exchange of cooperative acts could be shaping risk-taking behaviors.

With highly dimorphic species, males often play an important role in deterring predators as an outcome of sexual-selection (Zuberbühler 2004). However, as callitrichids are non-dimorphic species (Garber et al. 2015), sexual selection is a weak explanation for our observations. A study on of S. mystax found no differences related to sex on individual socio-spatial decision during retiring for one group. The same study pointed to a female as the first to enter a sleeping site in six out of nine occasions in the other study group (Heymann 1995). In Callithrix geoffroyi, a female took the front of the group during mobbing (Passamani 1995) and both males and females mobbed predators in Mico humeraliffer (Rylands 1981). These observations suggest that individual roles vary across species, populations, and groups.

Individual traits, such as age and previous experience, were not evaluated here; however they might determine roles during coordinated movements and predator avoidance (Conradt & Roper 2003). Moreover, we cannot rule out the possibility that the observed pattern of positioning is related to the form of the animal’s huddle at night, rather than a pattern shaped by risk-taking. However, we made several observations that support the assumption of higher risks faced by the first individual in line, including a potential predator (owl) inside a formerly used tree hole, as well as two occasions where the first individual to enter the hole was attacked by insects (once by bees, and once by unidentified insects, which were possibly ants).

Assessing individual roles is the basis for understanding the trade of cooperative actions that shaped the evolution of the cooperative infant care system. We present data on only one group, restraining the possibilities of hypothesize on the role of sex and hierarchy on risk-taking. Nonetheless, we suggest further studies contrasting groups composed of individuals of known ages with different social organizations and breeding systems, which would shed light on whether group order while arriving and departing from sleeping sites is (1) part of labor sharing according to social organization and structure, (2) a matter of individual age and experience, or (3) a combination of both.


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