Fallback foraging as a way of life: Using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation

The genus Cebus is one of the best extant models for examining the role of fallback foods in primate evolution. Cebus includes the tufted capuchins, which exhibit skeletal features for the exploitation of hard and tough foods. Paradoxically, these seemingly “specialized” taxa belong to the most ubiquitous group of closely related primates in South America, thriving in a range of different habitats. This appears to be a consequence of their ability to exploit obdurate fallback foods. Here we compare the toughness of foods exploited by two tufted capuchin species at two ecologically distinct sites; C. apella in a tropical rainforest, and C. libidinosus in a cerrado forest. We include dietary data for one untufted species (C. olivaceus) to assess the degree of difference between the tufted species. These data, along with information on skeletal morphology, are used to address whether or not a fallback foraging species exhibits a given suite of morphological and behavioral attributes, regardless of habitat. Both tufted species ingest and masticate a number of exceedingly tough plant tissues that appear to be used as fallback resources, however, C. libidinosus has the toughest diet both in terms of median and maximal values. Morphologically, C. libidinosus is intermediate in absolute symphyseal and mandibular measurements, and in measures of postcranial robusticity, but exhibits a higher intermembral index than C. apella. We propose that this incongruence between dietary toughness and skeletal morphology is the consequence of C. libidinosus' use of tools while on the ground for the exploitation of fallback foods. Am J Phys Anthropol 140:687–699, 2009. © 2009 Wiley-Liss, Inc.     

Stone tool use by adult wild bearded capuchin monkeys (Cebus libidinosus). Frequency, efficiency and tool selectivity

Chimpanzees have been the traditional referential models for investigating human evolution and stone tool use by hominins. We enlarge this comparative scenario by describing normative use of hammer stones and anvils in two wild groups of bearded capuchin monkeys (Cebus libidinosus) over one year. We found that most of the individuals habitually use stones and anvils to crack nuts and other encased food items. Further, we found that in adults (1) males use stone tools more frequently than females, (2) males crack high resistance nuts more frequently than females, (3) efficiency at opening a food by percussive tool use varies according to the resistance of the encased food, (4) heavier individuals are more efficient at cracking high resistant nuts than smaller individuals, and (5) to crack open encased foods, both sexes select hammer stones on the basis of material and weight. These findings confirm and extend previous experimental evidence concerning tool selectivity in wild capuchin monkeys ( [Visalberghi et?al., 2009b] and [Fragaszy et?al., 2010b]).Male capuchins use tools more frequently than females and body mass is the best predictor of efficiency, but the sexes do not differ in terms of efficiency. We argue that the contrasting pattern of sex differences in capuchins compared with chimpanzees, in which females use tools more frequently and more skillfully than males, may have arisen from the degree of sexual dimorphism in body size of the two species, which is larger in capuchins than in chimpanzees. Our findings show the importance of taking sex and body mass into account as separate variables to assess their role in tool use.     

Interactions between aroids and arboreal mammals in the Brazilian Atlantic rainforest

The Brazilian Atlantic rainforest harbours at least 129 non-volant mammal species. There is also a diverse and numerous epiphytic flora associated with this Neotropical rainforest, including several species of Araceae. Nevertheless, knowledge of the ecology of this group of plants and its interaction with animals is poor. In this study we investigated the interactions between epiphytic aroids and arboreal mammals in the Atlantic forest. We carried out the field work between November 1995 and June 1997 in the Parque Estadual Intervales, southeastern Brazil, a still well preserved forest area of approximately 490 km². We analysed faecal samples from primates (Cebus apella and Brachyteles arachnoides), collected during observations in the field, and marsupials (Didelphis aurita, Micoureus demerarae, Gracilinanus microtarsus), collected from animals captured monthly or bi-monthly in live-traps. We recorded 17 species of Araceae in the study area. The seeds of eight species occurred in the faecal samples: Anthurium harrissi, Monstera adansonii, Philodendron corcovadense, P. appendiculatum, P. exymium, P. crassinervium, P. obliquifolium, and Heteropsis oblongifolia. Aroids were present in faecal samples of the primates during most of the year, with a mean monthly percentage of occurrence of about 56.2%. For marsupials, aroids also were a seasonally important food source, as between November and June the mean monthly percentage of occurrence in faecal samples was about 26.5%. Our data indicate that aroids are an important food source for arboreal and semi-arboreal mammals and that these animals may play an important role as seed dispersers of this group. Aroids and arboreal mammals appear to interact more strongly in Atlantic forest than in other Neotropical forests.     

Anting in a Semifree-ranging Group of <Emphasis Type="Italic">Cebus apella</Emphasis>

Capuchins apply many organic materials, especially leaves, to their skin. Protection against ectoparasites is the most commonly discussed explanation for the behavior. We describe fur rubbing with carpenter ants(Camponotus rufipes) by semifree-ranging tufted capuchins(Cebus apella) in the Tietê Ecological Park, S?o Paulo, Brazil. Carpenter ants produce and secrete high concentrations of formic acid, which repels tick nymphs. Anting occurred significantly more often during months of seasonal incidence of nymphs of the tick Amblyomma cajennense, and the behavior was not related to ant-eating. We argue that anting behavior in tufted capuchins fits the hypothesis of protection against ectoparasites.     

Personality and behavioural syndrome in <Emphasis Type="Italic">Necromys lasiurus</Emphasis> (Rodentia: Cricetidae): notes on dispersal and invasion processes

Recent studies showed that behavioural individual features are related to species invasion and occupation abilities. In particular, the recent literature on animal personality has pointed to a correlation between behavioural profiles and the success in different phases of the invasion. In the present study, we investigated personality traits in the Neotropical species Necromys lasiurus. This wild rodent is expanding its original distribution to disturbed areas in the Atlantic Forest biome in response to anthropogenic impacts, acting as an invasive species (broad sense). In order to evaluate personality, we performed three behavioural assays as follows: open field, aversive open field and holeboard field. We extracted three personality domains—activity, exploration, and neophilia—using principal component analysis. There was significant positive correlation between these personality domains characterising a behavioural syndrome. We discussed the implications of this behavioural profile to dispersal and potential invasion abilities in this species.     

Universal stress proteins are important for oxidative and acid stress resistance and growth of Listeria monocytogenes EGD-e in vitro and in vivo

Background

Pathogenic bacteria maintain a multifaceted apparatus to resist damage caused by external stimuli. As part of this, the universal stress protein A (UspA) and its homologues, initially discovered in Escherichia coli K-12 were shown to possess an important role in stress resistance and growth in several bacterial species.

Methods and Findings

We conducted a study to assess the role of three homologous proteins containing the UspA domain in the facultative intracellular human pathogen Listeria monocytogenes under different stress conditions. The growth properties of three UspA deletion mutants (Δlmo0515, Δlmo1580 and Δlmo2673) were examined either following challenge with a sublethal concentration of hydrogen peroxide or under acidic conditions. We also examined their ability for intracellular survival within murine macrophages. Virulence and growth of usp mutants were further characterized in invertebrate and vertebrate infection models.Tolerance to acidic stress was clearly reduced in Δlmo1580 and Δlmo0515, while oxidative stress dramatically diminished growth in all mutants. Survival within macrophages was significantly decreased in Δlmo1580 and Δlmo2673 as compared to the wild-type strain. Viability of infected Galleria mellonella larvae was markedly higher when injected with Δlmo1580 or Δlmo2673 as compared to wild-type strain inoculation, indicating impaired virulence of bacteria lacking these usp genes. Finally, we observed severely restricted growth of all chromosomal deletion mutants in mice livers and spleens as compared to the load of wild-type bacteria following infection.

Conclusion

This work provides distinct evidence that universal stress proteins are strongly involved in listerial stress response and survival under both in vitro and in vivo growth conditions.