Evolutionary Biology and Conservation of Titis, Sakis and Uacaris: Insectivory and prey foraging techniques in Callicebus – a case study of Callicebus cupreus and a comparison to other pitheciids

Introduction For primates, animal prey and leaves represent alternative sources of protein, and no primate species combines large amounts of prey and leaves in the diet (Chivers & Hladik 1980; Martin 1990). These alternative dietary strategies can be explained by body-size constraints on the efficiency of prey foraging and by physiological constraints imposed on the digestion of leaves (Terborgh 1992). The absolute amount of obtainable prey does not increase with body size, thus making prey foraging unprofitable for large primate species, unless prey occurs in large clusters (like ant or termite mounds) (Terborgh 1983). The digestion of leaves through bacterial fermentation requires large amounts of space, which is not available in animals of small body size (Martin 1990). Consequently, primate diets show a predictable relationship with body mass (Martin 1990): while most extant primate species actually include fruit pulp in their diet, smaller species (below ca. 1–2 kg) usually supplement their diet with animal prey, while larger species (above ca. 1–2 kg) supplement with leaves (Harding 1981; Terborgh 1992). Additional factors such as the quality of leaves in the habitat or prey capture efficiency may, however, determine whether prey or leaves are used as source of protein. Kinzey (1978, 1997) compared the diets of two species of titi monkeys, and attributed the comparatively high amount of prey in the diet of Callicebus lucifer to leaves being very sclerophyllous and not readily available as a source of protein in its white-sand habitat, while very low capture efficiency was assumed to limit the amount of prey in Callicebus brunneus. He also suggested that “a ‘critical function’ . such as reducing the dietary protein source” (Kinzey 1978, p. 383) influences the molar structure of these otherwise basically frugivorous titi monkey species (Rosenberger & Kinzey 1996). Similarly, Rosenberger (1992) and Lambert (2007) emphasized that behavioral, morphological and physiological adaptations to the acquisition and consumption of minor food categories which may be vital for supplying certain essential nutrients, either throughout the year or as a fallback resource during critical periods of food scarcity, may be under strong selective pressure. Members of the Pitheciidae feed either principally on fruit pulp (titi monkeys) or seeds (sakis and uacaris), and are classified as “sclerocarpic frugivores” (Kinzey 1981; Norconk 2011; Rosenberger 1992). Neither fruit pulp nor seeds usually provide significant amounts of protein, so pitheciids have to exploit either prey or leaves to obtain proteins. In light of Kinzey’s (1978, 1997) hypothesis on the source of interspecific variation in prey consumption in titi monkeys, it is thus timely to review the available evidence for insectivory in the Pitheciidae. In this chapter we therefore examine (a) the contribution of prey to the diet and (b) the prey spectrum and prey foraging techniques, and analyze (c) whether a relationship exists between body mass and the contribution of prey to the diet, as predicted from theory. As a starting point for these comparisons and analyses, we provide detailed information on prey foraging in red titi monkeys, Callicebus cupreus.