Balancing contest competition,scramble competition,and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus)

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within‐group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as “single female dominance,” with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.     

Reproductive output, maternal age, and survivorship in captive common marmoset females (Callithrix jacchus)

Common marmosets (Callithrix jacchus) demonstrate significant variation in reproductive output on both a yearly and lifetime basis in comparison to other anthropoid primates. We explore the factors that may be most important in determining reproductive variation in captive common marmosets. Studies have found that maternal age, maternal condition, and dam survivorship are related to reproductive output; however, these reports are not in agreement and are far from conclusive. With the use of a large, multicolony, demographic database pooling data across five marmoset colonies, we examined litter information for 1,649 litters, and reproductive summaries for 400 dams to assess 1) how reproductive output variation (total production, total weaned production) is determined by litter size, interbirth interval (IBI), age at first birth, and dam survival age; 2) the relationship between maternal age and reproductive output variables; and 3) relationship between the reproductive output variables and survival. We used stepwise regression procedures to describe the amount of variation in lifetime reproductive output among dams, and found that mean litter size accounted for 18% of the variance in total production, survival age accounted for 10.6%, age at first birth accounted for 8.8%, and mean IBI accounted for 5%. For total (nonzero) weaned production, survival age accounted for 7.6% of variance, age at first birth accounted for 7.2%, mean IBI accounted for 2%, and mean litter size accounted for 1.6%. We identified significant effects (P<0.05) of maternal age on litter size and IBI length, but no effect of dam age on weaned litter size. Cox proportional hazards regression analyses revealed significant effects (P<0.01) of number of litters, age at first birth, and site on dam survivorship. Dams that produced more litters showed higher survivorship. Age at first birth showed a positive relationship with dam survivorship, i.e., dams that delayed first reproduction had higher survival. Our findings about reproductive variation in marmosets may have practical applications for the management of marmoset breeding colonies.     

Use of Alternative Plant Resources by Common Marmosets (Callithrix jacchus) in the Semi‐Arid Caatinga Scrub Forests of Northeastern Brazil

The common marmoset (Callithrix jacchus) is amply distributed in the Brazilian Northeast, but little is known of its ecology in the semi‐arid Caatinga scrublands. The present study provides the first detailed data on the composition of the diet of C. jacchus in Caatinga ecosystems, derived from observations at four sites in the state of Sergipe. While exudate sources were gouged at all four sites in a manner typical of the species, fruit was the principal component of the diet at the main study site during most months, and a number of unusual items were eaten, including leaves, and the reproductive parts of cacti and bromeliads. These plants are rarely recorded in marmoset diets, but are common in caatinga habitats. Leaves were ingested during 5 of the 8 months monitored at the main study site, reaching 39.74% of the diet in 1 month, and appeared to be an alternative fallback food to plant exudates during periods when fruit was scarce. Three species of cactus provided both flowers and fruits, while the terrestrial bromeliad, Encholirium spectabile, provided nectar (30.81% of the diet in November). Approximately half of the plant species (and three families) identified in this study had not been recorded previously in the diet of Callithrix. Overall, the data suggest that, while the marmosets exploit the same types of plant foods in the Caatinga, the resource base is quite distinct from that of the Atlantic Forest. Other differences, such as relatively small groups and large home ranges, may contribute to divergent ecological patterns, which require more systematic investigation. Am. J. Primatol. 75:333‐341, 2013. © 2012 Wiley Periodicals, Inc.     

Post-conception reproductive competition in cooperatively breeding common marmosets

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.     

Female striped mice (Rhabdomys pumilio) change their home ranges in response to seasonal variation in food availability

Animals may respond to seasonally changing environments withphysiological and behavioral strategies. Whereas migration isa behavioral strategy used by many taxa, it may not be an optionfor small mammals. However, small mammals can seasonally varythe area of habitat in which they are active. The striped mouseRhabdomys pumilio in the semiarid Succulent Karoo of South Africalives in a seasonal environment, characterized by hot, dry summerswith low food abundance and cold, wet winters, followed by highfood abundance in spring. We radio tracked a total of 28 femalesduring the 2004 dry season, the following breeding season inspring, and the following dry season in 2005 and tested theprediction that females shift their home ranges in relationto food availability. Females shifted their home ranges froman area characterized by evergreen succulent shrubs in the vicinityof a dry riverbed in the dry season to sandy areas that werecharacterized by new plant growth of annuals in spring. Homeranges during the breeding season in spring had a higher percentageof annuals than dry season home ranges measured in spring. Femalehome range size increased during the breeding season. We suggestthat female striped mice shift their home ranges seasonallyto gain access to protein-rich young plant material, which isimportant for breeding.     

The Role of Edaphic Environment and Climate in Structuring Phylogenetic Pattern in Seasonally Dry Tropical Plant Communities

Seasonally dry tropical plant formations (SDTF) are likely to exhibit phylogenetic clustering owing to niche conservatism driven by a strong environmental filter (water stress), but heterogeneous edaphic environments and life histories may result in heterogeneity in degree of phylogenetic clustering. We investigated phylogenetic patterns across ecological gradients related to water availability (edaphic environment and climate) in the Caatinga, a SDTF in Brazil. Caatinga is characterized by semiarid climate and three distinct edaphic environments – sedimentary, crystalline, and inselberg –representing a decreasing gradient in soil water availability. We used two measures of phylogenetic diversity: Net Relatedness Index based on the entire phylogeny among species present in a site, reflecting long-term diversification; and Nearest Taxon Index based on the tips of the phylogeny, reflecting more recent diversification. We also evaluated woody species in contrast to herbaceous species. The main climatic variable influencing phylogenetic pattern was precipitation in the driest quarter, particularly for herbaceous species, suggesting that environmental filtering related to minimal periods of precipitation is an important driver of Caatinga biodiversity, as one might expect for a SDTF. Woody species tended to show phylogenetic clustering whereas herbaceous species tended towards phylogenetic overdispersion. We also found phylogenetic clustering in two edaphic environments (sedimentary and crystalline) in contrast to phylogenetic overdispersion in the third (inselberg). We conclude that while niche conservatism is evident in phylogenetic clustering in the Caatinga, this is not a universal pattern likely due to heterogeneity in the degree of realized environmental filtering across edaphic environments. Thus, SDTF, in spite of a strong shared environmental filter, are potentially heterogeneous in phylogenetic structuring. Our results support the need for scientifically informed conservation strategies in the Caatinga and other SDTF regions that have not previously been prioritized for conservation in order to take into account this heterogeneity.     

High diversity of arbuscular mycorrhizal fungi in natural and anthropized sites of a Brazilian tropical dry forest (Caatinga)

Arbuscular mycorrhizal fungi (AMF) establish symbiotic associations with higher plants, which support the establishment and maintenance of plant communities across a range of environments, including those adversely affected by anthropogenic activity as well as natural sites. This study aimed at determining the diversity and distribution of AMF in areas of the tropical semi-arid region of Caatinga, Brazil, and compare areas in a naturally preserved state with anthropized sites. We characterized AMF communities in soil samples (n = 108), based on morphological taxonomy, at three sampling occasions and from six areas (typical Caatinga, extremely sandy Caatinga, stony Caatinga, rocky Caatinga, and two typical Caatinga areas that had been modified by human activities), at the National Park of Catimbau, Northeast Brazil. Eighty AMF species were recorded, with Glomus and Acaulospora predominating at all sites. There were significant differences in the composition of AMF communities between natural and anthropized sites, and among sampling occasions. Habitat-types also influenced AMF communities in Caatinga. Extensive tropical dry forest areas, such as the Catimbau National Park possess distinct niches, which maintain diverse AMF communities that are determined by anthropogenic activities, as well as vegetation types and environmental conditions.     

Primate Group Size and Abundance in the Caatinga Dry Forest, Northeastern Brazil

The Caatinga dry forest poses a series of ecological challenges for mammals in general and primates in particular. The erratic rainfall pattern impacts on plant diversity and phenological patterns; from year to year there is marked variability in fruit production and failure to fruit is common. The harshness apparently accounts for the impoverished mammalian fauna. However, data on primate abundance, distribution, and possible environmental effects on primate density are lacking in this type of dry forest. I censused the primate community in 3 habitats of the Serra da Capivara National Park, Piaui, NE Brazil, over a total distance of 318 km. Overall, the abundance of primates in the Caatinga dry forest is very low as a consequence of low abundance of food resources both in space and time. Alouatta caraya (predominantly folivorous) occurs at extremely low density, and during the dry season are apparently confined to canyon areas, where trees retain their leaves. Callithrix jacchus has morphological feeding specializations for gum-eating, and gum is an important resource during food bottleneck periods. Nonetheless, Callithrix jacchus occurs at comparatively low densities. Group sizes for howlers and marmosets in the Caatinga are significantly smaller than in other forest types. Contrarily, Cebus apella libidinosus had an average group size within the range reported for Amazonian and Atlantic forests. Researchers consider the generalized diet of capuchins as the explanation for their similar abundance in different habitats, indicating relative independence from ecological constraints. However, I suggest that capuchin foraging style and cognitive abilities are important factors accounting for their unreduced group size and density even under extreme conditions.     

The use of time and space by the Panamanian tamarin, Saguinus oedipus.

Tamarin activity patterns and habitat utilization strategies in the Tropical Dry Forest of the Panama Canal Zone were monitored quantitatively using radio-location telemetry. The daily tamarin activity pattern differed from that of other Neotropical primates in that early morning and late afternoon activity normally did not occur. Total daily activity time averaged 676 +/- 62 min. Sleeping trees, and behaviors associated with their use, were documented. Daily path length averaged 2,061 +/- 402 m. Mean travel distance was 468 +/- 66 m. Approximately one-third of the home range was utilized on a given day. Wet season home ranges for two social groups were 26 and 32 ha in area. Areas of low brush, forest edge, and vine-entangled second growth were heavily used by foraging tamarins. Large shade trees, particularly evergreens, were important as refuges from solar radiation. Open-canopy forest types and areas of grass were avoided. Social groups on resource-stable lowland sites defended territories; those on unstable upland sites used a system of time-space segregation. Upland groups became seminomadic during the dry season. Suitability of home range site may affect social group stability, natality, and infant survivorship.     

Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest

Mammals that live in seasonal environments may adjust their reproductive cycles to cope with fluctuations in food availability. Because lemurs in Madagascar experience highly seasonal variation in food availability, we examined the effects of fluctuating food availability on body condition and reproduction in one of the larger living species, Verreaux's sifaka (Propithecus verreauxi verreauxi), in the Kirindy Forest of western Madagascar. Seven years of demographic data were combined with an intensive study of 25 individuals over the course of 18 months. In contrast to other populations of Verreaux's sifaka, females were found to have greater body mass than males. Both male and female sifaka exhibited significant losses of body mass and fat during the dry season. Females were more likely to give birth and successfully wean an infant when they had higher body mass during the mating season. They mated during the periods of high and declining food availability, gave birth during the lean season, and then timed mid/late lactation with the period of increasing food availability. Thus, we conclude that sifaka follow the "classic" reproductive strategy (sensu van Schaik and van Noordwijk [Journal of Zoology (London) 206:533-549, 1985]).     

Cross-generic Food Sharing in Tamarins

Adult-infant food-sharing behavior is a major component of the infant care strategies of callitrichids (marmosets and tamarins). It is particularly well-developed in cotton-top tamarins (Saguinus Oedipus) and lion tamarins (Leontopithecus spp), which show frequent adult-initiated food offering, as well as sharing of food in response to begging by infants. This report documents a case of cross-generic food sharing, in which a male golden-headed lion tamarin (Leontopithecus chrysomelas) shared food with an infant cotton-top tamarin. The lion tamarin provided more food to the infant than its mother did. This emphasizes the importance of this behavior in the reproductive strategies of the communally-rearing Callitrichidae and raises questions about mechanisms that underly it.     

Body Weight of Wild and Captive Common Marmosets (Callithrix jacchus)

Captive studies and occasional trappings of wild individuals indicate that callitrichids have small size and body weight and lack sexual dimorphism. We compared body weights of captive and wild Callithrix jacchus obtained by repeatedly weighing subjects from two populations in Brazil. We obtained captive data by routinely weighing 138 individuals from the Universidade Federal do Rio Grande do Norte colony and wild data via regular trapping of 243 individuals in 15 free-ranging groups from IBAMA's field site in Nísia Floresta. We assigned all subjects to one of four age classes—infant, juvenile, subadult, and adult—according to their birth dates or size, reproductive status, and dental development. There is no significant difference between males and females in any of the four age classes, but captive subjects were heavier than wild ones in all age classes but infant. Reproductive and nonreproductive adult females showed no statistical difference in weight. These results accord with previous reports of lack of body size sexual dimorphism in common marmosets and suggest that differences between wild and captive common marmosets are not constitutional, but are instead a consequence of diet and physical activity. The absence of weight difference between reproductive and nonreproductive females suggests that any possible advantage from high rank is outweighed by the costs of reproduction in common marmosets.     

Resource Utilization and Temporal Segregation of Scarabaeinae (Coleoptera,Scarabaeidae) Community in a Caatinga Fragment

We characterized dung beetles food preference and diel activity and examined the way such characteristics may structure a Scarabaeinae community in a dry forest. We sampled a fragment of Arboreal Caatinga in Milagres, Bahia, Brazil, during the dry and wet seasons, using baited pitfall (bovine spleen, human feces, cow dung, and rotten banana). Species were classified by activity (nocturnal and diurnal) and food preference (coprophagous, necrophagous, saprophagous, copro-necrophagous, and generalist). In total, 1,581 individuals belonging to 16 morphospecies were sampled, with six new records for Caatinga. The dung beetles were mainly from generalist and coprophagous species; seven species presented nocturnal activity, and five were diurnal. There was higher species richness during the day and greater abundance during the night. Species composition differences were influenced by functional guilds and beetle size according to temporal segregation. These factors may be related to physiological, morphological, and behavioral differences.     

Comparison of Development and Life History in Pan and Cebus

We examined growth and development in capuchins and chimpanzees in relation to weaning, onset of reproduction, and reproductive life span. Striking differences are evident in neurobehavioral status at birth (more mature in capuchins), the relative duration of infancy (longer in chimpanzees), and the proportional weight of the infant at the time of weaning (greater in capuchins). Although capuchins and chimpanzees spend a similar proportion of life in a weaned but reproductively immature state, chimpanzees spend so much more of their lives as nursing infants that reproductive output per individual is much lower than in capuchins. Discussion centers around tolerated transfers of food (food-sharing) as a potential adaptation to limited foraging success by immature foragers. Perhaps food transfers from adult to infant, which is a more prominent feature of behavior in chimpanzees than in capuchins in natural environments, allow a very small weanling chimpanzee to survive.     

Diversity of reproductive modes in anurans communities in the Caatinga (dryland) of northeastern Brazil

Anuran reproductive activities in xeric environments are strongly influenced by local rainfall and temperatures. Anuran species that inhabit the Caatinga biome in northeastern Brazil demonstrate numerous behavioral and reproductive strategies that avoid or minimize the negative effects of elevated temperatures and scarce water resources on egg development. Among the various anuran species found in the Caatinga region, members of the family Leptodactylidae demonstrate the greatest number of reproductive modes adapted to a terrestrial life style while most of the Hylidae species are more susceptible to variations in water availability. Laying eggs in foam nests is a common strategy among species that inhabit environments with open vegetation forms and water resources that are restricted to only short periods during the year. Data concerning anuran communities in the localities examined here indicated a greater diversity of reproductive modes in ponds with more diverse vegetation structures and longer periods of water availability indicating that the deeper the temporary ponds (permitting a longer hydroperiod) the more diverse will be the aquatic and bordering vegetation, and the richer will be the diversity of anuran species observed and the number of reproductive modes encountered there.     

Differences in ingestive balance of two populations of neotropical Thrichomys apereoides (Rodentia, Echimyidae)

Thrichomys apereoides is widely distributed in the Caatinga, a semi-arid region in Brazil, but is presumed to lack capabilities for water conservation. In the present study, we compared two populations of adult individuals living under different precipitation conditions (700 and 450 mm year(-1)). Animals from the less dry area were twice as heavy as those from the drier locality. Under ad libitum water regimen, there were differences between populations in relative food intake as well as in water intake and urine concentration, but not in normalized body mass water intake. Under short-term water deprivation, both populations presented similar body mass loss. Whereas individuals from the more arid locality maintained food consumption, urine volume and urine osmolality, Thrichomys from the less dry locality reduced food consumption and urine volume. The occurrence of anuria in 75% of animals from this population indicates that the limits of their ability to deal with water shortage had been reached. The morphological and physiological difference and the non-allometric similarities found between the two populations of T. apereoides fulfill the criteria for physiological adaptations to differences in annual rainfall. Our data challenge the hypothesis that the irregularity of annual rainfall in the Caatinga precludes the evolution of adaptations to this semi-arid climate.     

Ranging behaviour and habitat preference of a wild marmoset group, Callithrix humeralifer (Callitrichidae, Primates)

The ranging behaviour of a group of marmosets ( Callithrix humeralifer ) in seasonal Amazonian rain forest was studied during one year. Range sizes (monthly and daily), day range lengths and patterns of range use are examined for correlations with feeding behaviour and the distribution of three forest types within the marmoset's range. Seasonal differences in ranging are associated with changes in the abundance and distribution of plant food sources. The marmosets ranged more widely and used more sources of a greater diversity of plant food species, which were distributed over a wider area, in the wet season than in the dry season. In the dry season, they ranged over a smaller area and, although they used fewer sources of a reduced diversity of plant species overall, they exploited a larger number of sources of the five highest ranked plant species in the diet. Throughout the year, they showed a preference for disturbed primary forest, characterized by dense understoreys and abundant second growth patches. Reasons for this preference are discussed, taking into account their use of fruits of typical pioneer species (particularly in the dry season), insect prey abundance, sleeping site availability and defence against predators.     

Plant sexual systems and a review of the breeding system studies in the Caatinga, a Brazilian tropical dry forest

BACKGROUNDS AND AIMS: The reproductive biology of a community can provide answers to questions related to the maintenance of the intraspecific pollen flow and reproductive success of populations, sharing and competition for pollinators and also questions on conservation of natural habitats affected by fragmentation processes. This work presents, for the first time, data on the occurrence and frequency of plant sexual systems for Caatinga communities, and a review of the breeding system studies of Caatinga species. METHODS: The sexual systems of 147 species from 34 families and 91 genera occurring in three Caatinga areas in north-eastern Brazil were analysed and compared with worldwide studies focusing on reproductive biology of different tropical communities. KEY RESULTS: The frequency of hermaphrodite species was 83.0 % (122 species), seven of these (or 4.8 % of the total) being heterostylous. Monoecy occurred in 9.5 % (14) of the species, and andromonoecy in 4.8 % (seven). Only 2.7 % (four) of the species were dioecious. A high percentage of hermaphrodite species was expected and has been reported for other tropical ecosystems. With respect to the breeding system studies with species of the Caatinga, the authors' data for 21 species and an additional 18 species studied by others (n = 39) revealed a high percentage (61.5 %) of obligatory self-incompatibility. Agamospermy was not recorded among the Caatinga studied species. CONCLUSIONS: The plant sexual systems in the Caatinga, despite the semi-arid climate, are similar to other tropical dry and wet forest communities, including those with high rainfall levels, except for the much lower percentage of dioecious species. The high frequency of self-incompatible species is similar to that reported for Savanna areas in Brazil, and also for dry (deciduous and semideciduous) and humid tropical forest communities.     

Fitness consequences of alternative life histories in water striders,Aquarius remigis (Heteroptera: Gerridae)

Using field and laboratory observations and experiments over 3 years, I investigated whether reproductive trade-offs shape individual life histories in two natural populations of the water strider, Aquarius remigis, in which univoltine and bivoltine life cycles coexist. Both later eclosion dates and food shortages, even after adult eclosion, induced diapause in females, thus deferring reproduction to the following spring. Adult body size was positively affected by food availability during juvenile development. Higher food levels also increased the reproductive output of females, but not their longevity or oviposition period. When compared to spring breeders (univoltine life cycle), direct (summer) breeders (bivoltine life cycle) experienced reduced lifetime egg numbers and longevity, as well as reduced survivorship of their second-summer-generation offspring; these reproductive costs offset, at least in part, the advantage in non-decreasing populations of having two generations per year. Fecundity was correlated with body size, and among summer-generation females direct breeders were larger than non-breeders. The time remaining before the onset of winter and/or the time since adult eclosion augmented cumulative energy uptake, and consequently the lipid reserves and winter survival probability of non-breeding (diapausing) summer adults approaching hibernation. Overwintered spring reproductives died at faster rates than non-reproductive summer individuals despite greater food availability in spring, indicating a mortality cost of reproduction. Body length correlated with absolute and not with proportional lipid content but showed no consistent relationship with survivorship in the field. These results are in agreement with current theory on the evolution of insect voltinism patterns, and further indicate high degrees of life history flexibility (phenotypic plasticity) in the study populations in response to variable environmental factors (notably photoperiod and food availability). This may be related to their location in a geographic transition zone from uni- to bivoltine life cycles.     

Wide home ranges for widely foraging lizards

Space usage by animals may be influenced by a range of factors. In this study we investigate whether foraging behaviour affects the home range size of lizards. Two distinct tactics of foraging have been recognized in predators: sit-and-wait foraging (SW) and active foraging (AF). Foraging activity level of a data set of lizard species, mainly compiled from literature, is compared with their home range sizes. Two opposite predictions can be made about foraging in connection with home range area: on the one hand, SW species may exhibit larger home ranges due to their mating system; on the other hand, AF species have higher metabolic energy and thus food requirements and can be expected to have larger home ranges that have to yield this food. This study shows that percentage of the time moving (as an index of foraging mode) correlates positively with home range, even after correcting for body mass, and these patterns remain when phylogenetic relationships are taken into account. We thus conclude that home range areas parallel activity levels in lizards.