Feeding rate as valuable information in primate feeding ecology

In this review I outline studies on wild non-human primates using information on feeding rate, which is defined as the food intake per minute on a dry-weight basis; further, I summarize the significance of feeding rate in primate feeding ecology. The optimal foraging theory has addressed three aspects of animal feeding: (1) optimal food patch choice, (2) optimal time allocation to different patches, and (3) optimal food choice. In order to gain a better understanding of these three aspects, the feeding rate itself or its relevance indices (e.g., rates of calorie and protein intake) could be appropriate measures to assess the quality of food and food patches. Moreover, the feeding rate plays an essential role in estimation of total food intake, because it varies greatly for different food items and the feeding time is not a precise measure. The feeding rate could also vary across individuals who simultaneously feed on the same food items in the same food patch. Body size-dependent and rank-dependent differences in the feeding rate sometimes cause individuals to take strategic behavioral options. In the closing remarks, I discuss the usefulness of even limited data on feeding rate obtained under adverse observational conditions in understanding primate feeding ecology.     

Particle handling during interception feeding by four species of heterotrophic nanoflagellates

High resolution video-microscopy was used to observe grazing patterns of the heterotrophic nanoflagellates Cafeteria roenbergensis, Bodo saltans, Spumella sp., and Ochromonas sp. Spumella and Ochromonas enclose food particles with pseudopodia while Cafeteria and Bodo engulf particles by invagination of the cell surface. The following parameters of the feeding process were quantified: frequency of flagellar beating, speed of particles in different positions of the feeding current, food size selection, feeding rate, and the time budget for the handling of particles. The mean handling times differed between 94 s for Cafeteria and 4 s for Ochromonas for ingested particles. Handling times for ingested particles were significantly longer than for non-captured particles. Long handling times were calculated to be disadvantageous only for flagellates which propel a high water volume per hour (esp. Ochromonas) or live in a bacteria-rich environment. Our model calculations may provide a reasonable theoretical explanation for a concentration-dependent behavioural variability of the feeding strategy of different heterotrophic nanoflagellates (HNF) species.     

Prolonging the arctic pulse: long-term exploitation of cached eggs by arctic foxes when lemmings are scarce

1. Many ecosystems are characterized by pulses of dramatically higher than normal levels of foods (pulsed resources) to which animals often respond by caching foods for future use. However, the extent to which animals use cached foods and how this varies in relation to fluctuations in other foods is poorly understood in most animals. 2. Arctic foxes Alopex lagopus (L.) cache thousands of eggs annually at large goose colonies where eggs are often superabundant during the nesting period by geese. We estimated the contribution of cached eggs to arctic fox diets in spring and autumn, when geese were not present in the study area, by comparing stable isotope ratios (delta(13)C and delta(15)N) of fox tissues with those of their foods using a multisource mixing model in Program IsoSource. 3. The contribution of cached eggs to arctic fox diets was inversely related to collared lemming Dicrostonyx groenlandicus (Traill) abundance; the contribution of cached eggs to overall fox diets increased from < 28% in years when collared lemmings were abundant to 30-74% in years when collared lemmings were scarce. 4. Further, arctic foxes used cached eggs well into the following spring (almost 1 year after eggs were acquired) - a pattern that differs from that of carnivores generally storing foods for only a few days before consumption. 5. This study showed that long-term use of eggs that were cached when geese were superabundant at the colony in summer varied with fluctuations in collared lemming abundance (a key component in arctic fox diets throughout most of their range) and suggests that cached eggs functioned as a buffer when collared lemmings were scarce.     

The predatory Chironomidae of an iron-rich stream: feeding ecology and food web structure

Abstract. 1. Three species of Tanypodinae (Chironomidae) were found in an acid and iron-rich stream in southern England. Maximum abundance was achieved in summer and they were sparse at other times. Individuals were aggregated on the stream bed and were overrepresented in accumulations of leaf litter.
2. The diets of all three species consisted of a mixture of prey (prominently detritivorous chironomid larvae) and detritus. More detritus and fewer prey were taken in winter than in summer.
3. When comparing large tanypod species with small and, intraspecifically, late instars with early, the proportion of guts containing prey increased with increasing body size.
4. Stonefly larvae were more prominent in the diet of Zavrelimyia barbatipes (Kieffer) in summer than in winter but for the other two species the reverse was true. A bigger proportion of Trissopelopia longimana (Staeger) guts contained prey in early summer than in August whereas more Macropelopia goetghebueri (Kieffer) guts contained prey in August. This was apparently a consequence of seasonal differences in the distribution of body size among the populations of these two species.
5. The stream contains two further common predators, Plectrocnemia conspersa (Curtis) and Sialis fuliginosa Pict. These are important predators of tanypod larvae but might also compete with them since they severely deplete populations of prey taken in common.
6. Analysis of the food-web in Broadstone Stream reveals remarkably high values of connectance (C and C_max) and of species richness times connectance (SC_max). Such characteristics are theoretically associated with fragile and dynamically unstable food webs, and may be found in 'constant' environments. There is also an apparently unusual prevalence of omnivory in the community.     

Mixed-species primate groups in the kibale forest: Ecological constraints on association

Five species of diurnal primates in the Kibale Forest of western Uganda— red colobus (Colobus badius),black- and- white colobus (Colobus guereza),redtail monkeys (Cercopithecus ascanius),blue monkeys (Cercopithecus mitis),mangabeys (Cercocebus albigena)-often associate in mixed- species groups that vary in size and composition from day to day. Across this range of species, we found no consistent effect of association on feeding rate. In addition, there is no systematic difference between the species- specific individual feeding rates when animals were in mixed- species groups feeding in a specific tree on one day and when individuals of one of the same species were feeding in the same individual tree on a subsequent day. If associating in a mixed- species group lowers the risk of predation, one might expect that the number of vigilant events would decrease in mixed- species groups. However, the only species to exhibit a consistent decrease in vigilant behavior when in association was the red colobus. Redtail monkeys were more vigilant when in association. We predicted that the density and distribution of food resources would both constrain the frequency of association and the size of mixed- species groups. Based on 22 months of data on food resources and bimonthly censuses, we found no relationship between the frequency of association (except mangabeys) or mean mixed- species group size and the density and distribution of food resources for all species. Finally, we examined the behavior of the monkeys in and out of association before and after the playback of a crowned hawk eagle call (Spizaetus coronatus),a known predator. When more species were in association, the amount of time they spent being vigilant following the playback was greater and the response more intense than when fewer species were in association or when the group was alone. The results of this study illustrate that the nature of the costs and benefits of polyspecific associations for these different monkey species are complex and vary from species to species.     

Foraging theory upscaled: the behavioural ecology of herbivore movement

We outline how principles of optimal foraging developed for diet and food patch selection might be applied to movement behaviour expressed over larger spatial and temporal scales. Our focus is on large mammalian herbivores, capable of carrying global positioning system (GPS) collars operating through the seasonal cycle and dependent on vegetation resources that are fixed in space but seasonally variable in availability and nutritional value. The concept of intermittent movement leads to the recognition of distinct movement modes over a hierarchy of spatio-temporal scales. Over larger scales, periods with relatively low displacement may indicate settlement within foraging areas, habitat units or seasonal ranges. Directed movements connect these patches or places used for other activities. Selection is expressed by switches in movement mode and the intensity of utilization by the settlement period relative to the area covered. The type of benefit obtained during settlement periods may be inferred from movement patterns, local environmental features, or the diel activity schedule. Rates of movement indicate changing costs in time and energy over the seasonal cycle, between years and among regions. GPS telemetry potentially enables large-scale movement responses to changing environmental conditions to be linked to population performance.     

Hunting at the highway: traffic noise reduces foraging efficiency in acoustic predators

Noise pollution from human traffic networks and industrial activity impacts vast areas of our planet. While anthropogenic noise effects on animal communication are well documented, we have very limited understanding of noise impact on more complex ecosystem processes, such as predator-prey interactions, albeit urgently needed to devise mitigation measures. Here, we show that traffic noise decreases the foraging efficiency of an acoustic predator, the greater mouse-eared bat (Myotis myotis). These bats feed on large, ground-running arthropods that they find by listening to their faint rustling sounds. We measured the bats' foraging performance on a continuous scale of acoustically simulated highway distances in a behavioural experiment, designed to rule out confounding factors such as general noise avoidance. Successful foraging bouts decreased and search time drastically increased with proximity to the highway. At 7.5 m to the road, search time was increased by a factor of five. From this increase, we predict a 25-fold decrease in surveyed ground area and thus in foraging efficiency for a wild bat. As most of the bats' prey are predators themselves, the noise impact on the bats' foraging performance will have complex effects on the food web and ultimately on the ecosystem stability. Similar scenarios apply to other ecologically important and highly protected acoustic predators, e.g. owls. Our study provides the empirical basis for quantitative predictions of anthropogenic noise impacts on ecosystem processes. It highlights that an understanding of the effects of noise emissions and other forms of 'sensory pollution' are crucially important for the assessment of environmental impact of human activities.     

Morphological integration and adaptation in the snake feeding system: a comparative phylogenetic study

A long-standing hypothesis for the adaptive radiation of macrostomatan snakes is that their enlarged gape--compared to both lizards and basal snakes--enables them to consume large prey. At first glance, this hypothesis seems plausible, or even likely, given the wealth of studies showing a tight match between maximum consumed prey mass and head size in snakes. However, this hypothesis has never been tested within a comparative framework. We address this issue here by testing this hypothesis in 12 monophyletic clades of macrostomatan snakes using recently published phylogenies, published maximum consumed prey mass data and morphological measurements taken from a large sample of museum specimens. Our nonphylogenetically corrected analysis shows that head width--independent of body size--is significantly related to mean maximum consumed prey mass among these clades, and this relationship becomes even more significant when phylogeny is taken into account. Therefore, these data do support the hypothesis that head shape is adapted to prey size in snakes. Additionally, we calculated a phylogenetically corrected morphological variance-covariance matrix to examine the role of morphological integration during head shape evolution in snakes. This matrix shows that head width strongly covaries with both jaw length and out-lever length of the lower jaw. As a result, selection on head width will likely be associated with concomitant changes in jaw length and lower jaw out-lever length in snakes.     

Seasonal variation of feeding patterns and food selection by crop-raiding elephants in Zimbabwe

Elephants and humans are increasingly coming into conflict because of the conversion of elephant habitat into agricultural areas. In order to identify trends that influence raiding behaviour, the nutritional makeup of food items consumed by crop‐raiding elephants over a 2‐year period were analysed and a trigger for crop raiding was identified. The point at which the quality of wild grasses declines below the quality of crop species corresponded to the movement of bull elephants out of a protected area and into fields. This finding may have wider implications for developing predictive models of elephant/human interactions.     

The subtlety of simple eyes: the tuning of visual fields to perceptual challenges in birds

Birds show interspecific variation both in the size of the fields of individual eyes and in the ways that these fields are brought together to produce the total visual field. Variation is found in the dimensions of all main parameters: binocular region, cyclopean field and blind areas. There is a phylogenetic signal with respect to maximum width of the binocular field in that passerine species have significantly broader field widths than non-passerines; broadest fields are found among crows (Corvidae). Among non-passerines, visual fields show considerable variation within families and even within some genera. It is argued that (i) the main drivers of differences in visual fields are associated with perceptual challenges that arise through different modes of foraging, and (ii) the primary function of binocularity in birds lies in the control of bill position rather than in the control of locomotion. The informational function of binocular vision does not lie in binocularity per se (two eyes receiving slightly different information simultaneously about the same objects from which higher-order depth information is extracted), but in the contralateral projection of the visual field of each eye. Contralateral projection ensures that each eye receives information from a symmetrically expanding optic flow-field from which direction of travel and time to contact targets can be extracted, particularly with respect to the control of bill position.     

Variation in the Nutritional Value of Primate Foods: Among Trees, Time Periods, and Areas

The study of nutritional ecology has proven to be useful for understanding many aspects of primate behavior and ecology and is a valuable tool in primate conservation. However, to date this approach has had limited application since chemical analyses of food items is very time-consuming and collections of perishable food material are often made in remote field locations. Such logistic difficulties have led to plant material being collected in a variety of fashions, and it is not known how variation in collection method might influence our understanding of the chemical basis of dietary selection. A standardization of collection methods is greatly needed to allow for direct comparison among studies. To develop an appropriate standardized method and to evaluate past research, it is necessary to understand along what dimensions plant chemistry varies. We evaluated variation in nutritional value—protein, fiber, digestibility, alkaloids, saponins, cyanogenic glycocides, and minerals—of leaf material from species eaten by red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza) of Kibale National Park, Uganda. We consider variation at 3-levels: among trees, time periods, and areas. While there was considerable variation among species with respect to protein, digestibility, and saponins, there was also variation among individuals of the same species; in fact, individuals may vary by as much as 20%. The average coefficients of variation (CV) among individuals of the same species are 13.4 for protein, 12 for digestibility, and 43 for saponins, while the average CV among species are 35, 31.3, and 82.4, respectively. No species showed a variable response with respect to testing for the presence or absence of cyanogenic glycocides, while 2 of 11 species tested for alkaloids showed a variable response. Over 2 years there was evidence of variation among time periods in the chemical composition of the same food items. The protein-to-fiber ratio of mature leaves of the same species collected from 4 sites separated by 12 km within Kibale was also variable and in some cases the variation among sites was greater than the differences among species. For example, while Funtumia latifolia had little variation in protein-to-fiber ratio at 3 sites (0.44 at all sites), the remaining site was 28% greater. Because temporal variation is less than variation among individuals, it is likely more important to sample from multiple trees at a single point in time than to sample across time. However, the most accurate assessment of nutrient intake is obtained by collecting plant material from the specific trees selected for consumption.     

Predation rates of nemertean predators: the case of a rocky shore hoplonemertean feeding on amphipods

Estimates of the predation rates of benthic nemerteans are often based on observations of single individuals, and consequently they may not be representative for all members of a population of these predators. Herein we conducted controlled and repeatable laboratory experiments on the predation rate of the hoplonemertean Amphiporus nelsoni Sánchez 1973, which is common at exposed rocky shores along the central Chilean coast. During the austral fall (April, May 2000), nemerteans were observed in relatively high numbers crawling in the intertidal zone during early morning or late-afternoon low tides. When these nemerteans were offered living amphipods held by a forceps, they immediately attacked the amphipods and fed on them. In the laboratory experiments, nemerteans preferred the amphipod Hyale maroubrae Stebbing, 1899, which is also very common in the natural habitat of A. nelsoni. The nemerteans preyed to a higher extent on small males and non-ovigerous females than would have been expected from their abundance. We suggest that these (non-reproductive) stages of H. maroubrae are very mobile and therefore have a high likelihood of encounters with nemerteans. Predation rates reached maxima when nemerteans were provided prey densities of four or more of their preferred prey species, H. maroubrae, furthermore indicating that encounter rates with prey may affect predation rates. In long-term laboratory experiments, A. nelsoni consumed more amphipods during low tide conditions than during high tide conditions. Many nemerteans in the field prefer particular environmental conditions (e.g. nocturnal low tides), which restricts the time available for successful feeding. In the long-term experiment, predation rates of A. nelsoni never exceeded 0.5 amphipods nemertean^–1 d^–1. Maximum feeding events were 3 or 4 amphipods nemertean^–1 d^–1, but this only occurred during 10 out of a possible 2634 occasions. Nemerteans that had consumed 3 or 4 amphipods during 1 day, consumed substantially less prey during the following days. Towards the end of the long-term experiment, average predation rates decreased to 0.2 amphipods nemertean^–1 d^–1, corresponding to predation rates reported for other nemertean species (0.1–0.3 prey items nemertean^–1 d^–1). We suggest that predation rates from laboratory experiments represent maximum estimates that may not be directly transferable to field populations. Additionally, low predator–prey encounter rates with preferred prey in the field may further limit the predation impact of nemertean predators in natural habitats.     

Aspects of the feeding ecology of Sargochromis codringtonii in Lake Kariba, Zimbabwe

Sargochromis codringtonii has always been considered a good candidate for the biological control of snails. However, there is lack of data on the feeding ecology of this species. The diet of S. codringtonii was examined by an analysis of stomach contents. The food of adult S. codringtonii in Lake Kariba is dominated by prosobranch snails. Pulmonate snails form a small insignificant component of the diet of S. codringtonii , and the reasons for this are discussed. Electivity indices were used to investigate prey selection. S. codringtonii does not show a particular preference for any snail species. It feeds on any snail species that is readily available. A morphometrical analysis of the feeding structures of S. codringtonii showed that the fish is well adapted to handling a molluscivorous diet. The daily food consumption of S. codringtonii was estimated over different seasons using the Elliot & Persson (1978 ) model [ J. Anim. Ecol. 47. 977–991]. Estimates of food consumption indicate that the fish consumed 14.0% of their dry body weight per day in summer and this falls to 4.5% in winter. The low consumption of pulmonates means that S. codringtonii cannot be a successful biological control agent against the vectors of schistosomiasis.     

Declining acceptability of a food plant for the polyphagous grasshopper Schistocerca americana: the role of food aversion learning

ABSTRACT Successive contacts with a food that was initially acceptable to the acridid Schistocerca americana (Drury) (Orthoptera: Acrididae) were monitored. It was found that acceptability, as measured by meal length, declined with experience until the food, spinach, was completely rejected. Reduced acceptability of spinach was maintained even after feeding for three meals on a fully acceptable and suitable food, a period of 2–3 h. Experiments with spinach-filled capsules placed in the gut suggested that the decline in acceptability was not due to direct feedback from the gut or haemolymph on the sensory or feeding control systems. Food aversion learning is indicated as the mechanism underlying the decline in acceptability.