Liliam P. Pinto

Diet of Alouatta belzebul discolor in an Amazonian Rain Forest of Northern Mato Grosso State, Brazil

Prior field studies of Alouatta showed the highest frugivory in A. belzebul. During 10 mo between October 1999 and October 2000, we studied the feeding ecology of a group of 7–9 red-handed howlers (Alouatta belzebul discolor) in a primary forest on the banks of a tributary of the Teles Pires River, near Paranaíta, MT, Brazil (9°34′S; 56°19′W). The howlers used 3 types of habitat: upland (terra firme) forest, flood plain forest (igapó) and palm forest (açaizal). During 45 complete days of observation, the group fed on 67 plant species (N = 2039 feeding records) in 24 families. The 2 most used families were Leguminosae and Moraceae, with 17 species each. Fruits predominated (40–80%) in every month, except June, when young leaves accounted for 54% of the diet. Dialium guianense (Leguminosal, Caesalpinioideae) was the most consumed species. Flower (6%) and mature leaf (5%) consumptions were low. Tree bark, live and decayed wood, and woody twig monthly consumption varied from 0 to 26%, and occurred only in igapó, where they used mostly Macrolobium acaciaefolium (Leguminosae, Caesalpinioideae), Clitoria amazonum (Leguminosae, Papilionoideae) and Licania cf. canescens (Chrysobalanaceae). Our study on Alouatta belzebul discolor complements the high frugivory in A. b. belzebul and documents uncommon dietary items for the species. Although there is intraspecific variation in howler diets and new studies have shown higher frugivory for more folivorous species, Alouatta belzebul seems to be the most frugivorous howler species, in spite of its wide geographical distribution and, in this case, sympatry with Ateles chamek, a frugivore.

Primary seed dispersal by three Neotropical seed-predating primates ( Cacajao melanocephalus ouakary , Chiropotes chiropotes and Chiropotes albinasus )

The Neotropics house two guilds of large arboreal vertebrate seed predators: parrots and the pitheciin primates. Both have diets dominated by immature fruits. The possibility of members of the Pitheciinae (genera Cacajao, Chiropotes and Pithecia) acting as occasional seed dispersers has been mooted, but not experimentally shown. We combined primate behavioural data and seed germination data from three separate field studies in the Brazilian states of Amazonas and Para to analyse patterns of post-consumption seed survivorship for seeds discarded by three pitheciin species (Cacajao melanocephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus). We then calculated the frequency of dispersal events for four species eaten by C. m. ouakary. All three primate species dropped intact seeds while feeding, and 30.7% of 674 dropped seeds germinated ex situ. Undamaged seeds from unripe and ripe samples germinated (29.3% and 42.7%. respectively), and all three primate species carried some fruits up to 20 m from the parent tree before consuming them. Potential seed-dispersal events varied from 1 (Macrolobium acaciifolium) per fruiting cycle to more than 6500 (Duroia velutina), suggesting that there are differences in dispersal potential. In summary, although they are highly specialized seed predators, these primates may also act as important dispersers for some plant species, and effective dispersal is not restricted to ripe fruits, as immature fruits removed from a tree may continue to mature and the seeds later germinate, a much-neglected aspect of dispersal ecology. The possibility that similar events occur in parrots should be experimentally investigated.

Terrestrial Activity in Pitheciins (Cacajao, Chiropotes, and Pithecia)

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a “local pattern” of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types. Am. J. Primatol. 74:1106‐1127, 2012.

Evolutionary Biology and Conservation of Titis, Sakis and Uacaris: Why we know so little: the challenges of fieldwork on the Pitheciids

Introduction Possessing a suite of unusual and interesting features, Pitheciids are at the extremes of many of primatology’s ecological and sociological continua (see Norconk 2011). Pitheciids should provide acute tests of many primatological models; however, this is frequently thwarted by the lack of even the most basic quantitative information concerning ecology, behavior and social organization. Such gaps are due not only to the small number of studies, but also to difficulties in obtaining data. This chapter considers why, given that these primates possess such aesthetic and intellectual appeal and high conservation value, they have been so little studied. The peculiarities of pitheciids, combined with their native habitats’ inherent challenges, have often undermined potentially successful fieldwork. Some researchers who began working with species of Callicebus or Chiropotes, for example, simply gave up because of problems habituating the animals or because the study was so difficult that the quality and quantity of gained data would not be worth the effort. Several researchers who persisted were either unable to obtain the expected volume of data or were incapable of answering many of their initial research questions, sometimes both. Using field experiences from a variety of research projects across a range of habitat types and pitheciid taxa, this chapter reports on the problems that arose during these studies and presents suggestions to minimize similar difficulties in the future.

Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia.

Pitheciids are known for their frugivorous diets, but there has been no broad‐scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both. Am. J. Primatol. 78:493–506, 2016.

Run, hide, or fight: anti-predation strategies in endangered red-nosed cuxiú (Chiropotes albinasus, Pitheciidae) in southeastern Amazonia

Although primate predation is rarely observed, a series of primate anti-predation strategies have been described. Energetic costs of such strategies can vary from high-cost mobbing, via less costly alarm calling, to low-cost furtive concealment. Here we report the anti-predation strategies of red-nosed cuxiú, Chiropotes albinasus, based on direct observations from four study sites in southeastern Brazilian Amazonia. Over a collective period of 1255 fieldwork hours, we observed nine direct interactions between raptors (all potential predators) and red-nosed cuxiús. Of these, one (11%) resulted in predation. Raptors involved were: Harpia harpyja (four events), Leucopternis sp. (two events), Spizaëtus tyrannus (one event), and unidentified large raptors (two events). Predation attempts occurred in flooded-forest and terra firme rainforest, were directed at both adult and non-adult cuxiús, and involved both adult and juvenile raptors. Anti-predation strategies adopted by the cuxiús included: (1) group defence and mobbing behaviour (two occasions), (2) dropping into dense sub-canopy (seven occasions), (3) alarm calling (eight occasions), and (4) fleeing to, and hiding in, dense vegetation (eight occasions). During each encounter at least two of these behaviours were recorded. These are the first published records of predation, predation attempts, and anti-predator behaviour involving red-nosed cuxiú.