Age and seasonal effects on predator-sensitive foraging in squirrel monkeys (Saimiri sciureus): a field experiment

A field experiment was conducted to examine the effect of perceived predation risk on the use of foraging areas by juvenile and adult primates under different conditions of local food abundance. Wild squirrel monkeys, Saimiri sciureus, were observed in an experiment conducted during the dry and the wet seasons at a site in Eastern Amazonia, Brazil. Animals were presented with feeding platforms that differed in food quantity and exposure to aerial predators through varying vegetative cover. In the dry season, juveniles and adults chose platforms based solely on food quantity. However, in the wet season, juveniles foraged preferentially on high-reward platforms only if cover level also was high (i.e., potentially offered greater concealment from predators). In contrast, adults showed the same pattern of platform use regardless of season. These results indicate that age and local resource availability based on seasonality affect whether primates forage in a predator-sensitive manner. Juveniles may be more sensitive to predation risk when foraging, and individuals may take fewer risks when resource abundance is high in their environment.     

Synchronization of weaning time with peak fruit availability in squirrel monkeys (Saimiri collinsi) living in Amazonian Brazil

Many mammals coincide their reproductive activities with factors such as ambient temperature, rainfall, and food availability. In primates that invest immediate food intake into reproduction, the periods of maximum fruit production often coincide with the peak of lactation (to maximize maternal survival) or the occurrence of weaning (to maximize infant survival). This study investigates the relationship between reproductive periods and the availability of ripe fruit in the habitat of a population of wild squirrel monkeys (Saimiri collinsi) in Amazonian Brazil. We combine data from several years (2002–2003; 2011–2015) during which we followed the monkeys and quantified the occurrence of matings, gestations, births, and the number of lactating females. We also collected rainfall and plant phenological data for 24 months. Our results confirm that reproductive events are highly seasonal in S. collinsi. The period of weaning corresponded to the peak in the abundance of ripe fruits consumed by the monkeys. This indicates that the period of infant nutritional independence is optimally timed to coincide with periods of greater food production in this habitat. We suggest that seasonal breeding in these primates does not necessarily reduce maternal energetic stress, but likely improves infant survivorship.     

Spatial and temporal changes in bird assemblages in forest fragments in an eastern Amazonian savannah

We investigated the effects of forest fragmentation on bird assemblages in an Amazonian savannah landscape with forest fragments that have been isolated for more than 100 years. The study was conducted in areas surrounding the village of Alter do Chão (2°31′S, 55°00′W), Santarém, Brazil. Bird surveys and measurements of tree density were undertaken in 25 areas, with 19 plots in forest fragments of different sizes and six in an area of continuous forest. Data on forest‐fragment size, perimeter, and isolation were obtained from a georeferenced satellite image. Variation in number of bird species recorded per plot was not related to vegetation structure (tree density). The number of bird species recorded per plot increased significantly only with fragment area, but was not influenced by fragment shape or degree of isolation, even when considering species from the savannah matrix in the analysis. Fragments had fewer rare species. Multivariate ordination analyses (multiple dimensional scaling, [MDS]) indicated that bird species composition changed along a gradient from small to large forest fragments and continuous‐forest areas. In the Amazonian savannah landscapes of Alter do Chão, the organization and composition of bird assemblages in forest fragments are affected by local long‐term forest‐fragmentation processes. Differences in the number of bird species recorded per plot and assemblage composition between forest fragments and continuous forest were not influenced by forest structure, suggesting that the observed patterns in species composition result from the effects of fragmentation per se rather than from preexisting differences in vegetation structure between sites. Nevertheless, despite their long history of isolation, the forest fragments still preserve a large proportion (on average 80%) of the avifauna found in continuous‐forest areas. The fragments at Alter do Chão are surrounded by natural (rather than planted) grassland, with many trees in the savannah matrix and the landscape has vast areas covered by forest, which may have helped to ameliorate the influences of forest fragmentation.     

Responses of mother squirrel monkeys to dead infants

The responses of mother squirrel monkeys to infants were examined by testing the mothers with bodies of their own and other infants. Mothers whose infants were stillborn or died at one day of age showed strong and equivalent maternal responses to all the bodies with which they were presented, while those whose infants died after two weeks of age responded mainly to the body of their own infant. These results suggest that the female squirrel monkey becomes more selective in responding to the body of a dead infant with the passage of time after parturition. The female's post-parturient condition appears to be the prime cause for changes in her responsiveness, although other factors related to the infant's growth and development might also be important.Supported by Grant HD 04905 from the National Institute of Child Health and Human Development.     

Seasonal variation in the composition of fish assemblages in small Amazonian forest streams: evidence for predictable changes

1. The effects of seasonal inundation on the biology of fishes on floodplains of large Amazonian rivers are well studied. However, the small seasonal changes in headwater streams are generally considered to have little effect on fish assemblages. 2. In this study, we analysed seasonal changes in the species composition and abundance of fish in small Amazonian forest streams. We sampled fish with hand and seine nets in headwater streams in a 10 000 ha terra‐firme forest reserve near Manaus, Brazil. Each stream was surveyed at the end of the 2005 dry season, at the beginning of the 2006 rainy season and at the beginning of the 2006 dry season, by means of a standardized sampling effort. 3. The numbers of individuals and species caught were higher in the dry season, but rarefaction analyses indicated that greater species numbers could have been due simply to the larger number of individuals caught. 4. Between the dry and rainy season, the direction of changes in species composition in multivariate space varied among sites, especially for quantitative (abundance) data. However, the observed variation among sites was the less than expected if the directions of change were random. 5. Fish assemblages in the second dry season were more similar to those in the previous dry season than expected if changes in species composition among seasons were random. This indicates that a general seasonal pattern in fish assemblages can be detected, despite the existence of some erratic site‐specific changes. 6. Most of the species that showed large seasonal variations in density occupy temporary ponds during the rainy season, when much of the valley is inundated and pond networks form adjacent to streams. Short‐duration lateral migrations to these ponds may play an important role in the seasonal fish‐assemblage dynamics in Amazonian headwater streams. 7. Our results contrast with previous studies on small Amazonian streams, which have found little seasonal change in fish assemblages, and highlight the importance of the abundance of common species as an indicator of general fish assemblage structure in biological monitoring programmes.     

Food availability and breeding season as predictors of geophagy in Amazonian parrots

Geophagy, the consumption of soil, is common in many species, but the drivers of geophagy are not well understood. The best‐studied example of avian geophagy is the parrots of the western Amazon Basin, but even here, there is debate over what drives the behaviour. There are two possible explanations: (1) extra nutritional demands of reproduction drive an increase in geophagy, which would predict that geophagy should be highest during the breeding season, and (2) consumption of naturally toxic plant foods increases the need for the toxin protection effects of soil, which would predict that geophagy should be highest when food availability is low and animals are forced to consume more toxic foods. We used long‐term data from lowland Amazonia to compare seasonal fluctuations in rainfall, food availability, parrot breeding and parrot geophagy, and conducted novel tests of these hypotheses. Our analyses of annual patterns suggested that seasonal changes in rainfall drive plant fruiting, the resulting food availability patterns drive the timing of parrot breeding, and breeding drives seasonal patterns of geophagy. Surprisingly, chicks of the largest psittacine species fledged as food supplies approach their annual lows, suggesting that future climatic changes that alter peaks in food availability could have unexpected impacts on the reproduction of large psittacines in this system. Our tests found no evidence to support the toxin‐protection hypothesis. Instead, we found that the peak of geophagy occurred during species’ breeding seasons, which strongly supports the supplemental nutrients hypothesis. Our findings join a growing body of biochemical, physiological, behavioural, ecological and biogeographical evidence suggesting that a need for sodium is driving soil consumption in this classic model system of avian geophagy.     

Seasonality of reproduction in captive squirrel monkeys (Saimiri Sciureus)

Seasonality of reproduction is believed to be influenced by environmental factors such as humidity, temperature, and photoperiod. In primates, there has been much speculation about which environmental factors have the greatest influence on reproductive seasonality. To determine whether environmental factors affect seasonality of reproduction of squirrel monkeys in captivity, I used path analysis to compare number of births and matings per month with monkeys kept in indoor enclosures (maintained at optimal temperatures) and those kept in outdoor enclosures (exposed to the elements). Since a different pattern of seasonality was found to occur, I was able to test whether temperature, rainfall, or photoperiod could explain the temporal variation in reproduction. Squirrel monkeys raised in captivity displayed different patterns of seasonality of reproduction, depending on the conditions in which they are housed ( chi(2)3 25.12, P<0.001; G = 28.10, P<0.001). Temperature seemed to have a large impact on number of births and matings per month (matings: path coefficient = 0.799; births: path coefficient = -1.315). Understanding what factors regulate reproduction for animals and how these factors affect reproduction differently in wild versus captive populations are important to conservation and management of species.     

Pollen use by Megalopta sweat bees in relation to resource availability in a tropical forest

1. Spatial and temporal availability of pollen helps shape bee foraging behaviour and productivity, which has been studied in great detail at the landscape level, but never in a diverse tropical forest. 2. To study the effect of spatio‐temporal variation in resource distribution on pollen use and productivity, we identified pollen from spatially explicit nest collections of two generalist sweat bees, Megalopta genalis Meade‐Waldo and M. centralis Friese, from Barro Colorado Island, Panama, a 50‐ha forest dynamics plot during the 2007 dry and early wet seasons. Pollen from nests collected in 1998–1999 without spatial information was also identified. 3. Bees used pollen of at least 64 species; many of these occurred in only one collection. The 2007 collections contained pollen of 35 different species, but were dominated by five species, especially Hura crepitans L. and Pseudobombax septenatum (Jacq.) Dugand. 4. Temporal availability, but not distance from nest, influenced flower use at a 50‐ha scale. 5. Body size was not associated with minimum flight distance as inferred from pollen collections. 6. Nest productivity and pollen diversity decreased from the dry to wet seasons, mirroring community‐level availability of floral resources. 7. Results suggest that on a scale of 50 ha, bees are choosing certain host plant species regardless of distance from the nest, but adjusting foraging behaviour opportunistically based on the temporal availability of host flowers.     

Honeyeater population changes in relation to food availability in the Jarrah forest of Western Australia

The numbers of honeyeaters present at particular sites in the Jarrah forest varied significantly from month to month, with peak abundance occurring between May and September. Numbers also varied from site to site, depending upon the major plant species present. Honeyeater abundance was not limited by arthropod availability, but in many instances was closely correlated with the availability of nectar, particularly that produced by Dryandra sessilis. Large honeyeaters, such as Anthochaera chrysoptera and Phylidonyris novaehollandiae, were generally most abundant at times and sites of greatest nectar production. Small honeyeaters, such as Acanthorhynchus superciliosis, were never abundant but were present for most of the year. The production of nectar between October and December was such that more honeyeaters could have been supported than were actually present. Low numbers at these times can be explained in terms of reduced foraging efficiency that would have resulted from more widely dispersed flowers, and the possible availability of more rewarding nectar resources at other sites.     

Diel and seasonal patterns of foraging activity in the arboreal ant Crematogaster matsumurai Forel

The foraging habits of the arboreal ant Crematogaster matsumurai Forel were studied in natural and captive colonies in southern Kyushu, Japan. The nests of C. matsumurai are made mainly in the trunks of living trees. In the natural environment, the species mainly lives in decayed parts of relatively tall trees, such as Acer palmatum, Prunus jamasakura and Prunus yedoensis. Observation over a 24 h period showed that C. matsumurai foraged actively at night as well as during the day. The foraging of the workers out of the nest was seen from early spring to late autumn, both on the tree and on the ground. As protein sources, aphids were mainly collected by foragers from the tree, while small parts of dead insects or other arthropods were mainly collected from the ground surface. The foraging activity of workers is assumed to be influenced by the quantity and quality of food rather than seasonality.     

Climate change and seasonal reproduction in mammals

Seasonal reproduction is common among mammals at all latitudes, even in the deep tropics. This paper (i) discusses the neuroendocrine pathways via which foraging conditions and predictive cues such as photoperiod enforce seasonality, (ii) considers the kinds of seasonal challenges mammals actually face in natural habitats, and (iii) uses the information thus generated to suggest how seasonal reproduction might be influenced by global climate change. Food availability and ambient temperature determine energy balance, and variation in energy balance is the ultimate cause of seasonal breeding in all mammals and the proximate cause in many. Photoperiodic cueing is common among long-lived mammals from the highest latitudes down to the mid-tropics. It is much less common in shorter lived mammals at all latitudes. An unknown predictive cue triggers reproduction in some desert and dry grassland species when it rains. The available information suggests that as our climate changes the small rodents of the world may adapt rather easily but the longer lived mammals whose reproduction is regulated by photoperiod may not do so well. A major gap in our knowledge concerns the tropics; that is where most species live and where we have the least understanding of how reproduction is regulated by environmental factors.     

The reproductive phenology of an Amazonian ant species reflects the seasonal availability of its nest sites

In saturated tropical ant assemblages, reproductive success depends on queens locating and competing for scarce nest sites. Little is known about how this process shapes the life histories of tropical ants. Here I investigate the relationship between nest site availability and an important life history trait, reproductive phenology, in the common Amazonian ant species Allomerus octoarticulatus. A. octoarticulatus is a plant-ant that nests in the hollow, swollen stem domatia on Cordia nodosa. I provide evidence that nest sites are limiting for A. octoarticulatus. Most queens produced by A. octoarticulatus colonies died before locating suitable host plants, and most queens that located hosts died before founding colonies, probably from intraspecific competition among queens for control of host plants. I further show that the reproductive phenology of A. octoarticulatus closely matches the seasonal availability of its nest sites, domatia-bearing C. nodosa saplings. Both the production and flight of A. octoarticulatus reproductives, and the number of C. nodosa saplings available for colonization by ants, peaked from March to May. There was correlative evidence that A. octoarticulatus colonies use temperature as a cue to synchronize their reproduction to the availability of C. nodosa saplings: both the production of reproductives by ant colonies and the number of C. nodosa saplings available for colonization were correlated with temperature, and not with rainfall. All of these results suggest that nest site limitation constrains the reproductive phenology of A. octoarticulatus.     

Response of a traplining hummingbird to changes in nectar availability

Theory predicts that nectarivores respond to changes in profitabilityof patches of flowers or feeders by adjusting visitation rateto increase reward size. We conducted a set of experiments inan outdoor enclosure with seven feeders to determine how Phaethornislongirostris, a traplining hummingbird, adjusts its visitationrates in response to changes in sucrose solution delivery rates.Each experiment tested the response of P. longirostris to thefollowing changes in the timing and volume of sucrose solutiondelivery: (1) increases in sucrose solution abundance at allfeeders (mimicking seasonal increases in numbers of open flowersor nectar output); (2) large changes in sucrose solution availabilityat one feeder (mimicking increases or decreases of patch profitability);and (3) sudden unexpected decreases in sucrose solution availabilityat one feeder (mimicking loss of nectar to competitors). Wefound that P. longirostris (1) decreased visitation rates whenthe sucrose solution delivery rate was higher at all feeders,(2) increased visitation rates to individual feeders when their profitabilityincreased for whole days but did not significantly decrease visitationrates when feeder output decreased; and (3) responded to sudden foodlosses at a feeder (due to simulated competition) by increasinguse of that feeder for 1 or 2 h after the loss.     

The development of seasonal variation in gonadal hormones and body weight in the maturing squirrel monkey

Captive-born squirrel monkeys of three different subtypes (Colombian, Bolivian, Peruvian), ranging in age from 1 to 4.5 years for males and 1 to 3.5 years for females, were examined at 3-month intervals throughout the year for seasonal changes in levels of plasma testosterone and progesterone and in body weight. Cyclical activity of testosterone in males began between 2 and 3 years of age but became more defined by the time the animals were 3–4 years old. Peak values occurred in February and May and corresponded to the the time of year in which adults normally mate. Elevations of progesterone occurred initially at approximately 2.5 years of age in February and May, and mainly infernales of the Colombian subtype. However,unlike levels of testosterone in males of this age, which declined in August and November (following the typical breeding season), levels of progesterone in females continued to increase during these months. Seasonal changes in body weight were also found in males but these changes were less evident than, and did not correlate with, hormonal changes.     

Partner effects on food consumption in brown capuchin monkeys

It has been claimed that capuchin monkeys (Cebus apella) show inequity aversion in relation to food rewards for a simple exchange task. However, other factors may affect the willingness of a monkey to consume foods of high or low value in the presence of a conspecific. In this study, pairs of monkeys were presented with unequally valued foods, but without any task-performance: they simply received the food under four experimental conditions. By looking at the rate of collection and consumption of low-valued cucumber slices we expected to see variation dependent on whether the partner either had 1) cucumber (equity), 2) grape (inequity), 3) inaccessible cucumber or 4) inaccessible grape. Testing 12 adult capuchin monkeys, our findings differed from those of other authors in that the monkeys failed to show negative reactions to inequity, but rather responded with scramble competition (i.e., fast food collection) in the presence of a conspecific without access to food. They also showed facilitated consumption in the presence of a conspecific consuming high-valued food. Possibly, (in)equity plays a different role if food serves as a reward for a task rather than if it is simply made available for consumption.     

Intra-and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool use

Tool manufacture and use have been described for wild orangutans (Pongo pygmaeus), with appreciable interpopulational differences in tool complexes. The ecological factors that contribute to these differences require investigation. Significant interpopulational differences in diet suggest that ecological factors contribute to variation in tool-based insect foraging. Using 4 years of behavioral data from the Suaq Balimbing Research Station (Sumatra, Indonesia), we tested predictions of two ecological hypotheses for the invention of tool use for insect foraging. We found limited evidence for inter- and intrasexual differences, as well as temporal variation, in activity budget and diet. However, differences did not correspond to variation in either rate of tool use or specialization on tool-based insectivory. Compared to other populations, orangutans at Suaq Balimbing ate significantly more insects. Low temporal variation in insectivory and an abundance of social insects at Suaq Balimbing suggest that insects formed a staple in the diet rather than a fallback food. Our findings do not support the hypothesis that tool use is a response to the low availability of primary food sources. Rather, greater opportunities for invention likely contributed to insect-extraction tool use at Suaq Balimbing.     

Rainfall exclusion in an eastern Amazonian forest alters soil water movement and depth of water uptake

Deuterium-labeled water was used to study the effect of the Tapajós Throughfall Exclusion Experiment (TTEE) on soil moisture movement and on depth of water uptake by trees of Coussarea racemosa, Sclerolobium chrysophyllum, and Eschweilera pedicellata. The TTEE simulates an extended dry season in an eastern Amazonian rainforest, a plausible scenario if the El Ni?o phenomenon changes with climate change. The TTEE excludes 60% of the wet season throughfall from a 1-ha plot (treatment), while the control 1-ha plot receives precipitation year-round. Mean percolation rate of the label peak in the control plot was greater than in the treatment plot during the wet season (0.75 vs. 0.07 m/mo). The rate was similar for both plots during the dry season (ca. 0.15 m/mo), indicative that both plots have similar topsoil structure. Interestingly, the label peak in the control plot during the dry season migrated upward an average distance of 64 cm. We show that water probably moved upward through soil pores-i.e., it did not involve roots (hydraulic lift)-most likely because of a favorable gradient of total (matric + gravitational) potential coupled with sufficient unsaturated hydraulic conductivity. Water probably also moved upward in the treatment plot, but was not detectable; the label in this plot did not percolate below 1 m or beyond the depth of plant water uptake. During the dry season, trees in the rainfall exclusion plot, regardless of species, consistently absorbed water significantly deeper, but never below 1.5-2 m, than trees in the control plot, and therefore may represent expected root function of this understory/subcanopy tree community during extended dry periods.