Led by the nose: Olfaction in primate feeding ecology

Olfaction, the sense of smell, was a latecomer to the systematic investigation of primate sensory ecology after long years in which it was considered to be of minor importance. 1 This view shifted with the growing understanding of its role in social behavior 2 and the accumulation of physiological studies demonstrating that the olfactory abilities of some primates are on a par with those of olfactory‐dependent mammals such as dogs and rodents. 3 , 4 Recent years have seen a proliferation of physiological, behavioral, anatomical, and genetic investigations of primate olfaction. These investigations have begun to shed light on the importance of olfaction in the process of food acquisition. However, integration of these works has been limited. It is therefore still difficult to pinpoint large‐scale evolutionary scenarios, namely the functions that the sense of smell fulfills in primates’ feeding ecology and the ecological niches that favor heavier reliance on olfaction. Here, we review available behavioral and physiological studies of primates in the field or captivity and try to elucidate how and when the sense of smell can help them acquire food.     

Long-term consequences of changes in territory quality on feeding and reproductive strategies of vervet monkeys

1. Food availability and quality are important determinants of mammalian reproductive success, and long-term changes in food availability were assessed for their impact on diets and reproduction of three adjacent groups of vervet monkeys in Amboseli, Kenya in two periods spanning an interval of 9 years.
2. Diets were largely restricted to the products of two species of acacia trees ( Acacia xanthophloea and Acacia tortilis ), with food selection primarily determined by availability (tree density, size and seasonal production of foods).
3. Over this period the overall abundance of major foods, measured through absolute species density, declined while territory size increased.
4. Despite significant changes in food plant densities, diets remained relatively stable, suggesting a component of consistency in diet choice. Limited options or high costs for incorporation of novel foods are suggested as factors maintaining this stability, with deleterious consequences in the face of very long-term habitat changes.
5. This study suggests that the habitat deterioration, assessed by reduction in food densities, initiated local group extinction. An increased energy expenditure in foraging, high mortality and low reproductive rates ultimately led to a population crash under conditions of reduced food availability.     

Self-organized asymmetries in ant foraging: a functional response to food type and colony needs

The dominant paradigm to explain asymmetries in the spatialdistribution of foraging animals is that they track the spatialheterogeneity of their environment. However, in social insects,endogenous spatial asymmetries can emerge within a uniformenvironment as an outcome from the self-organizing processof trail recruitment. We studied how self-organized asymmetriescontribute to the exploitation of different food sources (carbohydrateor proteins) in colonies of the aphid-tending ant Lasius nigervarying in their nutritional needs (presence or absence ofbrood). Colonies with brood fed on sucrose sources exhibita higher mobilization of foragers than the other experimentalgroups. Foraging patterns differ greatly according to foodtype: colonies strongly focus their activity on only one dropletof sucrose, whereas they show a rather homogeneous distributionof foragers between proteinaceous sources. In addition, thepresence of brood in the colony enhances the asymmetry of collectiveforaging for both types of food. These spatial differencesin self-organized foraging patterns allow efficient exploitationof natural resources and play a role in the competitive strategyof this widespread palearctic ant.     

Mean-variance sets for dietary choice models: simplicity in a complex world

Summary This paper presents a series of simulations designed to determine optimal diet breadth under shortfall avoidance models. Profitability and encounter rate functions were varied, and means and variances of energy intake rate were generated using a simple simulation procedure. The resulting mean-variance sets assumed three distinct shapes: u-shaped, arched, and looped. These simulations show that certain mean-variance sets allow the forager to employ simple behavioural rules to determine the optimal diet breadth. This situation occurs when low ranking diet items have small handling times, and these conditions may be quite common. In other cases, mean-variance sets may be too complicated to allow for easy behavioural rules designed to minimize starvation probability. The ability to characterize foraging problems into a limited series of mean-variance set types benefits workers examining the evolution and maintenance of foraging strategies, since these sets have clear implications for the ability of animals to develop simple behavioural rules. Unfortunately data are lacking on the profitability and encounter rate distributions animals face in nature.     

Winter feeding ecology of cod (Gadus morhua) in a fjord of southern Norway

We investigated the winter feeding ecology of cod ( Gadus morhua ) in the Risørfjord and Flødevigen areas on the Skagerrak coast, southern Norway. Diets from the ice-covered Risørfjord were compared with diets from the more coastal Flødevigen area. In the Risørfjord area the diet featured numerically both decapods (56.0%) and fish (27.8%), but fish dominated by mass (75.1%). The most numerous dietary items from the Flødevigen area were decapods (48.1%) and isopods (30.6%), although fish still made up the bulk of the diet's mass (52.6%). Diets at Flødevigen shifted from winter to spring, as polychaetes became important numerically (67.8%) and also contributed substantially by weight (53.6%). Since cod feed opportunistically, differences between areas and seasons probably reflected differences in prey diversity and abundance. Prey size variability increased with increasing predator length, but maximum prey size relative to predator length was constant at about 9%. Prey fish increased in both length and numbers with the length of cod, particularly in the Risørfjord area, where fish were more important in the diet than at Flødevigen. However, the majority of fish consumed in both areas were small gobiids. Based on growth patterns observed in otoliths, with opaque zones (indicating faster growth) formed during winter, the quality and quantity of the winter diet may determine annual growth rates of cod on the Skagerrak coast. Fish and decapods constituted important, high energy food sources, and there was little indication that cod were food limited during winter in this area.     

Night and day: the comparative study of strepsirrhine primates reveals socioecological and phylogenetic patterns in olfactory signals

Studies of chemical signals in vertebrates typically target single species; however, a broader understanding of olfactory communication may derive from comparative studies. We collected urine from 12 species representing most families of strepsirrhine primates--an excellent model clade because of variation in scent marking and socioecology. Using SPDE/GC-MS, we identified the volatile chemical composition of male and female urine from six 'urine marking' species and six glandular or 'non-urine marking' species. We found no sex differences, but as predicted, urine markers expressed the most chemically complex and distinctive urine. More distantly related species had more dissimilar urinary profiles, suggesting gradual signal evolution. Reconstructing ancestral chemical profiles revealed different evolutionary trajectories for urine and non-urine markers. We suggest that urine marking is an ancestral behaviour related to solitary, nocturnal living and that parallel evolutionary shifts towards greater reliance on derived glandular marking occurred in a family (Lemuridae) characterized by diurnality and sociality.     

Genetic architecture of a feeding adaptation: garter snake (Thamnophis) resistance to tetrodotoxin bearing prey

Detailing the genetic basis of adaptive variation in natural populations is a first step towards understanding the process of adaptive evolution, yet few ecologically relevant traits have been characterized at the genetic level in wild populations. Traits that mediate coevolutionary interactions between species are ideal for studying adaptation because of the intensity of selection and the well-characterized ecological context. We have previously described the ecological context, evolutionary history and partial genetic basis of tetrodotoxin (TTX) resistance in garter snakes (Thamnophis). Derived mutations in a voltage-gated sodium channel gene (Na_v1.4) in three garter snake species are associated with resistance to TTX, the lethal neurotoxin found in their newt prey (Taricha). Here we evaluate the contribution of Na_v1.4 alleles to TTX resistance in two of those species from central coastal California. We measured the phenotypes (TTX resistance) and genotypes (Na_v1.4 and microsatellites) in a local sample of Thamnophis atratus and Thamnophis sirtalis. Allelic variation in Na_v1.4 explains 23 per cent of the variation in TTX resistance in T. atratus while variation in a haphazard sample of the genome (neutral microsatellite markers) shows no association with the phenotype. Similarly, allelic variation in Na_v1.4 correlates almost perfectly with TTX resistance in T. sirtalis, but neutral variation does not. These strong correlations suggest that Na_v1.4 is a major effect locus. The simple genetic architecture of TTX resistance in garter snakes may significantly impact the dynamics of phenotypic coevolution. Fixation of a few alleles of major effect in some garter snake populations may have led to the evolution of extreme phenotypes and an ‘escape’ from the arms race with newts.     

At-sea distribution and scale-dependent foraging behaviour of petrels and albatrosses: a comparative study

1. In order to study and predict population distribution, it is crucial to identify and understand factors affecting individual movement decisions at different scales. Movements of foraging animals should be adjusted to the hierarchical spatial distribution of resources in the environment and this scale-dependent response to environmental heterogeneity should differ according to the forager's characteristics and exploited habitats. 2. Using First-Passage Time analysis, we studied scales of search effort and habitat used by individuals of seven sympatric Indian Ocean Procellariiform species fitted with satellite transmitters. We characterized their search effort distribution and examined whether species differ in scale-dependent adjustments of their movements according to the marine environment exploited. 3. All species and almost all individuals (91% of 122 individuals) exhibited an Area-Restricted Search (ARS) during foraging. At a regional scale (1000s km), foraging ranges showed a large spatial overlap between species. At a smaller scale (100s km, at which an increase in search effort occurred), a segregation in environmental characteristics of ARS zones (where search effort is high) was found between species. 4. Spatial scales at which individuals increased their search effort differed between species and also between exploited habitats, indicating a similar movement adjustment for predators foraging in the same habitat. ARS zones of the two populations of wandering albatross Diomedea exulans (Crozet and Kerguelen) were similar in their adjustments (i.e. same ARS scale) as well as in their environmental characteristics. These two populations showed a weak spatial overlap in their foraging distribution, with males foraging in more southerly waters than females in both populations. 5. This study demonstrates that predators of several species adjust their foraging behaviour to the heterogeneous environment and these scale-dependent movement adjustments depend on both forager and environment characteristics.     

Wood anatomy of Penaeaceae (Myrtales): comparative, phylogenetic, and ecological implications

Wood samples of stems, lignotubers, and roots of the majority of species of Penaeaceae were analyzed with respect to qualitative and quantitative features. Virtually no data have hitherto been presented on xylem features of this family, restricted to Cape Province, South Africa. Presence of vestured pits in vessels, septate crystalliferous parenchyma in wood, intraxylary phloem, predominantly erect ray cells in the typically narrow, multiseriate rays and in the uniseriate rays, and amorphous deposits in ray cells place Penaeaceae securely in Myrtales and help to define that order. By comparison of ecological preferences of the species, as observed during field work, with quantitative analysis of conductive tissue, close correspondence of the wood structure to habit and habitat is demonstrated.     

Dynamic phenotypic plasticity for root growth in Polygonum: a comparative study

Species differences in patterns of phenotypic plasticity may be an important aspect of adaptive diversity. Plasticity for functionally important root traits was studied in inbred field lineages of Polygonum persicaria and P. cespitosum (Polygonaceae). Replicate seedlings were grown in plexiglass rhizotrons under a range of constant and temporally variable moisture treatments. Plasticity was determined for final whole-plant biomass, root biomass allocation, and absolute and proportional root length. The dynamic aspect of root plasticity was examined by digitizing weekly tracings of the proportional deployment of each plant's root system to different vertical soil layers. Plants of both species expressed significant functionally adaptive phenotypic plasticity in the relative allocation, length, and vertical deployment of root systems in response to contrasting moisture conditions. Plasticity patterns in these closely related species were in general qualitatively similar, but for most traits differed in the magnitude and/or the timing of the plastic response. Dynamic changes in root deployment were more marked as well as faster in P. persicaria. Species differences in patterns of individual plasticity were generally consistent with the broader ecological distribution of P. persicaria in diverse as well as temporally variable moisture habitats.     

Morphological integration and ontogenetic niche shift: a study of crested newt limbs

This study deals with the ontogenetic and evolutionary aspects of integration patterns in the limbs of crested newt species, which, like most amphibians, have a biphasic life history with two morphologically distinct stages (larval vs. juvenile and adult) that occupy different environments (aquatic vs. terrestrial). We analyzed the structure and pattern of correlation between limb skeletal elements at three ontogenetic stages (larval, juvenile, and adult) of four closely related species that differ in their preferences of aquatic habitats (more terrestrial and more aquatic). We found dynamic changes in the pattern of morphological integration between successive ontogenetic stages, as well as changes over the course of crested newt phylogeny. Generally, equivalent ontogenetic stages of different species of crested newts show higher concordance in the correlation pattern than successive ontogenetic stages within species. Among species, two opposing correlation patterns were observed: in more terrestrial species, homologous limb elements are less correlated and within-limb elements are more correlated; in aquatic species, the reverse pattern occurs. These results indicate that the function seems to be the covariance-generating factor, which has shaped the patterns of morphological integration of crested newt limbs.     

Adaptation in the African egg-eating snake: a comparative approach to a classic study in evolutionary functional morphology

A key component to any adaptive hypothesis is that the adaptive trait in question must confer a performance advantage and, in turn, an increase in fitness, relative to those animals displaying the phylogenetically antecedent condition. Among the most striking purported adaptations in vertebrates are those found in the African snake genus Dasypeltis . These snakes are unique in that they eat bird eggs to the exclusion of all other prey. Detailed functional morphological analysis dating back 50 years has highlighted a suite of morphological features in the head and trunk region hypothesized to assist these animals in eating bird eggs, and yet no comparative performance studies of egg-eating ability have ever been conducted in this group of snakes. The purpose of this study was twofold: first, we wanted to compare egg-eating performance in Dasypeltis with a facultative egg eater, the common king snake Lampropeltis getula . Second, we wanted to test the hypothesis that a selective regime exists in Africa conducive to the selection and subsequent fixation of the hypothesized egg-eating morphological adaptations. Our results show that a strong advantage exists in egg-eating ability for Dasypeltis . The difference is so large (only large Lampropeltis can eat small eggs) that analysis by analysis of covariance becomes difficult due to problems with collinearity. Our results examining potential selective regimes show that more birds lay eggs of a readily ingestible size in Africa than in a representative region in the United States. Additionally, the largest radiation of African ground-nesting birds existed in Africa before the colubrid explosion during the Miocene, which gave rise to Dasypeltis , giving further support to previous adaptive hypotheses regarding the unique morphology of these snakes.