On the evolution of omnivory in a community context

Omnivory is extremely common in animals, yet theory predicts that when given a choice of resources specialization should be favored over being generalist. The evolution of a feeding phenotype involves complex interactions with many factors other than resource choice alone, including environmental heterogeneity, resource quality, availability, and interactions with other organisms. We applied an evolutionary simulation model to examine how ecological conditions shape evolution of feeding phenotypes (e.g., omnivory), by varying the quality and availability (absolute and relative) of plant and animal (prey) resources. Resulting feeding phenotypes were defined by the relative contribution of plants and prey to diets of individuals. We characterized organisms using seven traits that were allowed to evolve freely in different simulated environments, and we asked which traits are important for different feeding phenotypes to evolve among interacting organisms. Carnivores, herbivores, and omnivores all coexisted without any requirement in the model for a synergistic effect of eating plant and animal prey. Omnivores were most prevalent when ratio of plants and animal prey was low, and to a lesser degree, when habitat productivity was high. A key result of the model is that omnivores evolved through many different combinations of trait values and environmental contexts. Specific combinations of traits tended to form emergent trait complexes, and under certain environmental conditions, are expressed as omnivorous feeding phenotypes. The results indicate that relative availabilities of plants and prey (over the quality of resources) determine an individual's feeding class and that feeding phenotypes are often the product of convergent evolution of emergent trait complexes under specific environmental conditions. Foraging outcomes appear to be consequences of degree and type of phenotypic specialization for plant and animal prey, navigation and exploitation of the habitat, reproduction, and interactions with other individuals in a heterogeneous environment. Omnivory should not be treated as a fixed strategy, but instead a pattern of phenotypic expression, emerging from diverse genetic sources and coevolving across a range of ecological contexts.     

Black-backed jackal diet at Mokolodi Nature Reserve, Botswana

We examined the feeding habits of black‐backed jackals at Mokolodi Nature Reserve, Botswana, by analysing 237 scats collected between November 1995 and February 1997. Jackal dietary habits reflected the availability of a wide variety of food items and the differential vulnerability of prey. Potential animal and plant food available to jackals varies throughout the year because of its seasonal character. Seasonality of prey occurrence in scats was pronounced for small mammals, miscellaneous fruits and invertebrates. Across all seasons, mammals were the most common food resource (32.4%, n = 168), followed by anthropogenic items (14.8%), fruits (12.9%), invertebrates (10.8%), birds (8.5%), unidentified items (3.5%) and reptiles (1.4%). The presence of domestic mammals and poultry remains in scats reveals their importance in the diet of jackals and the tendency of jackals to frequent human settlements in search of food. Some ecological implications of jackal dietary habits are also explored.     

Testing the validity of functional response models using molecular gut content analysis for prey choice in soil predators

Analysis of predator–prey interactions is a core concept of animal ecology, explaining structure and dynamics of animal food webs. Measuring the functional response, i.e. the intake rate of a consumer as a function of prey density, is a powerful method to predict the strength of trophic links and assess motives of prey choice, particularly in arthropod communities. However, due to their reductionist set‐up, functional responses, which are based on laboratory feeding experiments, may not display field conditions, possibly leading to skewed results. Here, we tested the validity of functional responses of centipede predators and their prey by comparing them with empirical gut content data from field‐collected predators. Our predator–prey system included lithobiid and geophilomorph centipedes, abundant and widespread predators of forest soils and their soil‐dwelling prey. First, we calculated the body size‐dependent functional responses of centipedes using a published functional response model in which we included natural prey abundances and animal body masses. This allowed us to calculate relative proportions of specific prey taxa in the centipede diet. In a second step, we screened field‐collected centipedes for DNA of eight abundant soil‐living prey taxa and estimated their body size‐dependent proportion of feeding events. We subsequently compared empirical data for each of the eight prey taxa, on proportional feeding events with functional response‐derived data on prey proportions expected in the gut, showing that both approaches significantly correlate in five out of eight predator–prey links for lithobiid centipedes but only in one case for geophilomorph centipedes. Our findings suggest that purely allometric functional response models, which are based on predator–prey body size ratios are too simple to explain predator–prey interactions in a complex system such as soil. We therefore stress that specific prey traits, such as defence mechanisms, must be considered for accurate predictions.     

Seasonal versatility in the feeding ecology of a group of titis (Callicebus coimbrai) in the northern Brazilian Atlantic Forest

The feeding behavior of a group of titis (Callicebus coimbrai) was monitored over an annual cycle at a site in northeastern Brazil. Behavioral data were collected in scan samples (1-min scan at 5-min intervals), and complementary data on fruit availability and new leaf cover were collected. Feeding time accounted for 28.9% of daily activity. Fruit was the principal item of the diet (61.2% of records) and the primary category in all months except September, when it was surpassed by leaves. Young leaves were the second most important category (20.0%). The consumption of seeds and insects was prominent in November and December. Fifty-two plant species were exploited, and the Elaeocarpaceae, Myrtaceae, Sapotaceae, and Passifloraceae provided the vast majority (86.0%) of plant feeding records. The phenological record did not provide a good measure of fruit availability, but a strong correlation (r(s) =0.902, P<0.0001, n=12) was found between the consumption of leaves and the exploitation of lianas each month. Lianas accounted for 28.2% of plant feeding records, and predominated between August and December. This suggests that lianas may represent a key factor in the ability of the species to tolerate the intense habitat fragmentation found throughout its geographic range.     

Predation of arthropods by southern bearded sakis (Chiropotes satanas) in Eastern Brazilian Amazonia

Bearded sakis are seed predators, but are also known to consume arthropods. This is the first detailed report of arthropod predation in southern bearded sakis (Chiropotes satanas). Two groups were monitored-one in continuous forest, and one on a small island-between January 2003 and February 2004. The arthropod prey included spiders and six insect orders. Island group members spent more time foraging for arthropods (3.8% vs. 2.6% of activity time) but ingested less prey (3.7% vs. 4.6% of feeding time). Arthropods accounted for a small proportion of feeding records in most months, but there were occasional sharp peaks due to the exploitation of temporary agglomerations of insects. In November, arthropods accounted for 26.6% and 14.2% of the feeding records of the mainland and island groups, respectively. The results suggest that bearded sakis actively seek arthropods as a dietary supplement, but that they represent a minor resource during most of the year, even under conditions of intense habitat fragmentation (island group).     

Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem

The planting of transgenic crops expressing Bacillus thuringiensis endotoxins is widespread throughout the world; the prolific increase in their application exposes nontarget organisms to toxins designed to control pests. To date, studies have focused upon the effects of Bt endotoxins on specific herbivores and detritivores, without consideration of their persistence within arthropod food webs. Here, we report the first quantitative field evaluation of levels of Bt endotoxin within nontarget herbivores and the uptake by higher order arthropods. Antibody-based assays indicated significant quantities of detectable Cry1Ab endotoxin within nontarget herbivores which feed on transgenic corn (including the corn flea beetle, Chaetocnema pulicaria, Japanese beetle, Popillia japonica and southern corn rootworm, Diabrotica undecimpunctata howardi). Furthermore, arthropod predators (Coccinellidae, Araneae, and Nabidae) collected from these agroecosystems also contained significant quantities of Cry1Ab endotoxin indicating its movement into higher trophic levels. This uptake by predators is likely to have occurred by direct feeding on plant material (in predators which are facultatively phytophagous) or the consumption of arthropod prey which contained these proteins. These data indicate that long-term exposure to insecticidal toxins occurs in the field. These levels of exposure should therefore be considered during future risk assessments of transgenic crops to nontarget herbivores and arthropod predators.     

Habitat selection,diet and food availability of European Golden Plover Pluvialis apricaria chicks in Swedish Lapland

Fennoscandian alpine tundra habitats support large numbers of breeding waders, but relatively little is known about their breeding ecology despite the fact that this habitat is threatened by climate change. We studied habitat selection, diet and prey availability of European (Eurasian) Golden Plover Pluvialis apricaria chicks at the Vindelfjällen Nature Reserve, Ammarnäs, Sweden. Information from 22 chicks tracked using radio‐transmitters was analysed. By analysing 149 faecal samples, four main prey taxa were identified, Coleoptera (40%), Bibionidae (31%), Hymenoptera (13%) and Tipulidae (10%). We found that chicks switched from feeding on Tipulidae to feeding on Bibionidae as they grew, and that this switch coincided with a shift from the use of the habitat where Tipulidae were abundant (alpine meadow/heathland) to the use of the habitat were Bibionidae were abundant (Willow shrub). Although chicks track food availability to some extent, the link between prey availability and habitat use was not perfect, indicating that additional factors other than food abundance, such as shelter from predators, determine habitat selection. Bibionidae are an important prey for Golden Plover chicks as it is the only prey group that has a late summer flush in abundance, in contrast to the general decline of total arthropod biomass during the chick‐rearing period. However, Bibionidae imagoes only occurred in 2011 and were virtually absent in 2013, which relates to the species’ ecology with 2‐ to 5‐year cycles in mass occurrence. Extreme annual variation in an essential food source such as Bibionidae imagoes might have an important effect on the condition and survival of Golden Plover chicks, an important subject for future studies. The foraging conditions for Golden Plover chicks in Fennoscandia appear to be different to those in the UK, where the chicks rely mainly on a Tipulidae flush only.     

Seasonal patterns in the foraging ecology of the harvester ant Pogonomyrmex naegelii (Formicidae, Myrmicinae) in a Neotropical savanna: daily rhythms, shifts in granivory and carnivory, and home range

The temporal dynamics of foraging, diet, and use of space is essential to understand the ecology of harvester ants. Here, we present an account of the foraging ecology of Pogonomyrmex naegelii in Brazilian cerrado savanna. Nests occur on bare ground and contain 166?C580 workers (N?=?3 colonies). Colony activity is unimodal year-round and peaks around the middle of the day. Foragers leave the nest independently and individually search for food in all directions. Ants ventured up to 15?m from nests, with most foraging occurring within 2?m of nests. Colonies tended to have larger home ranges in the dry/cold (April?CSeptember) than in the wet/warm season (October?CMarch). P. naegelii has a generalist and season-dependent diet comprised of many seed species and arthropod prey, and pieces of plant and animal matter. Foragers collected seeds from 34 plant species, predominantly grasses (genera Gymnopogon, Axonopus, Aristida). Over 6,700 seeds can be stored in nest granaries. Ants and termites were the main animal prey retrieved by P. naegelii. The proportion of seeds and arthropods foraged by P. naegelii changes year-round: in the dry/cold season, the diet is predominantly granivorous, whereas in the wet/warm season, seeds and arthropods are retrieved in more balanced proportions. Although food availability was not assessed, year-round diet of P. naegelii matches the pattern of seasonal abundance of grass seeds and arthropod prey in cerrado. Data on harvester ants come mostly from arid habitats; this study is a first assessment of the ecology of a Neotropical Pogonomyrmex from a moderately moist savanna environment.     

A meta-analytical review of the effects of elevated CO2 on plant-arthropod interactions highlights the importance of interacting environmental and biological variables

We conducted the most extensive meta-analysis of plant and animal responses to elevated CO(2) to date. We analysed > 5000 data points extracted from 270 papers published between 1979 and 2009. We examined the changes in 19 animal response variables to the main effect of elevated CO(2). We found strong evidence for significant variation among arthropod orders and feeding guilds, including interactions in the direction of response. We also examined the main effects of elevated CO(2) on: six plant growth and allocation responses, seven primary metabolite responses, eight secondary metabolite responses, and four physical defence responses. We examined these response variable changes under two-way and three-way interactions between CO(2) and: soil nitrogen, ambient temperature, drought, light availability, photosynthetic pathway, reproductive system, plant growth rate, plant growth form, tissue type, and nitrogen fixation. In general we found smaller effect sizes for many response variables than have been previously reported. We also found that many of the oft-reported main effects of CO(2) obscure the presence of significant two- and three-way interactions, which may help better explain the relationships between the response variables and elevated CO(2).     

Zoophytophagy in the plantbug Nesidiocoris tenuis

1 The zoophytophagy of Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae) was characterized in relation to prey availability and environmental factors by: (i) monitoring its population dynamics in tomato greenhouses; (ii) analysis of the influence of N. tenuis and whitefly density, temperature and humidity on the intensity of N. tenuis plant feeding; and (iii) laboratory assays under controlled conditions to determine the intensity of plant feeding in relation to prey availability, temperature and humidity. 2 A negative relationship was found between plant feeding and predated whiteflies in tomato greenhouses. Plant feeding was directly related to N. tenuis density and temperature and inversely related to whitefly density. The significance of prey availability and temperature was corroborated in laboratory assays. The intensification of plant feeding at low prey density indicates switching from zoophagy to phytophagy as prey become scarce. 3 Nesidiocoris tenuis showed a typical predator dynamic in relation to variance in prey density. Populations increased after whitefly outbreaks and decreased after whitefly had been depleted. The rapid decrease of N. tenuis populations after whitefly decreased, however, suggests that plants are a poorer nutrient source than whitefly for this species.     

Diet and Feeding Behavior of <Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis> (Callitrichidae) in Degraded Areas of the Atlantic Forest of South-Bahia,Brazil

Habitat disturbance alters plant diversity and food resource availability, affecting the ecology, and ultimately the survival and reproduction, of species depending on those plants. Studies in degraded areas serve to improve our understanding of the consequences of habitat modification for endangered species and to guide conservation actions. We studied diet composition, monthly variation in feeding behavior and fruit feeding time, and dietary diversity in two golden-headed lion tamarin (Leontopithecus chrysomelas) groups ranging in a degraded area of the Atlantic Forest in South-Bahia, Brazil, over a 12-mo period. We recorded feeding behavior and food items consumed through continuous observations and focal animal sampling, and performed dietary analyses on samples from consumed fruits. Substrate manipulation to search for animal prey was the feeding activity most frequently observed, followed by fruit consumption. We observed nectar drinking and exudate feeding at low frequencies from April through July. Bromeliads were the principal foraging substrate. We observed the use of 114 plant species, confirming the large dietary diversity reported for the species. Individual trees from the family Melastomataceae, common in degraded forests, accounted for the highest visiting frequencies (40%). Fruit availability was the main factor explaining variation in monthly fruit feeding time, despite the absence of climatic seasonality. Nutritional or energetic characteristics did not affect fruit choice. Differences in floristic composition appear to be a major determinant of the species’ diet in different study areas. Regional forest restoration programs should consider including advanced forest species, to improve both forest quality and animal mobility between fragments.     

Long-Term Changes in the Diet of Gymnogobius isaza from Lake Biwa,Japan: Effects of Body Size and Environmental Prey Availability

Body size and environmental prey availability are both key factors determining feeding habits of gape-limited fish predators. However, our understanding of their interactive or relative effects is still limited. In this study, we performed quantitative dietary analysis of different body sizes of goby (Gymnogobius isaza) specimens collected from Lake Biwa between 1962 and 2004. First, we report that the diet was composed mainly of zooplankton (cladocerans and copepods) before the 1980s, and thereafter, shifted to zoobenthos (gammarids). This foraging shift coincided with, and thus can be linked to, known historical events in the lake at that time: decrease in zooplankton abundance with the alleviation of eutrophication, increase in fish body size resulting from fish population collapse, and increase in gammarid abundance due to reduced fish predation pressure. Supporting this view, our data analyses revealed how the long-term changes in the diet composition would be co-mediated by changes in fish body size and environmental prey availability. Specifically, while zoobenthos abundance strongly affected the fish diet composition, larger (smaller) fish preferred zoobenthos (zooplankton). Furthermore, the body size effects were stronger than those of prey availability. These results provide the best long-term evidence that fish feeding habits vary over decades with its body size and prey community due to anthropogenic disturbances.     

A meta‐analysis of non‐consumptive predator effects in arthropods: the influence of organismal and environmental characteristics

Non‐consumptive effects (NCEs) – changes in prey behavior or physiology in response to predator threat – are common and can be as strong as consumptive effects. However, our knowledge of NCEs in arthropod systems is lacking. Factors related to study organism and environment have the potential to influence the occurrence and magnitude of NCEs in arthropod systems. While factors such as coevolutionary history of natural enemies and their prey, predator cue, predator or prey feeding mode, and refuge availability have been theoretically and empirically examined, no trends have been proposed for arthropods. We compiled 62 studies, yielding 128 predator–prey interactions, which explicitly examined NCEs in experiments where arthropods were identified to species, using a previously published database of papers from 1990 to 2005 and a new database of papers published from 2006 to 2015. Using these data, we conducted a meta‐analysis to explore the influence of organismal and environmental characteristics on the magnitude of predator NCEs. Our analysis addressed the following three questions. 1) Does predator–prey coevolution give rise to stronger NCEs than when predator and prey species did not coevolve? 2) What influence does habitat type and refuge availability have on NCEs? 3) How do predator characteristics (cue type, hunting mode and life stage) and prey characteristics (mobility, life stage, specialization, gregariousness and feeding mode) influence NCEs? We found that while NCEs were similar across most measured characteristics, NCEs on prey activity were significantly stronger when predator and prey shared an evolutionary history. Our results support growing evidence that NCEs have a negative effect on prey traits and that behavioral NCEs are stronger than physiological ones. Additional studies are needed to be confident in any emerging patterns, therefore we identify key gaps in the literature on NCEs in arthropod systems and discuss ideas for moving forward.     

Partitioning two- and three-trophic-level effects of resistant plants on the predator, Nabis roseipennis

Two- and three-trophic-level effects of resistant soybean plants on the development and fecundity of the predator Nabis roseipennis Reuter (Hemiptera: Nabidae) were determined. The nabids, like many hemipteran predators, feed on plants as well as arthropod prey. The life history traits of N. roseipennis when feeding on Pseudoplusia includens (Hübner) (Lepidoptera: Noctuidae) fed the resistant soybean cultivar PI 229358 or the susceptible Cobb' and while exposed to these resistant and susceptible soybean cultivars or a no-plant control were determined. Nymphal survival of N. roseipennis was unaffected by either prey or plant treatment. Development time was extended and fecundity of N. roseipennis was reduced by feeding on prey fed the resistant plant but not by exposure to resistant soybean plants. Thus, three-trophic-level effects of the resistant cultivar PI 229358 on prey quality were more important than two-trophic-level effects of direct plant feeding on development and fecundity of N. roseipennis. Consistency of these results with those of other predatory hemipterans and the potential impact of diet composition on the effects of resistant plants are discussed.     

On the myrmecomorph Coquillettia insignis Uhler (Hemiptera: Miridae): arthropod predators as operators in an ant-mimetic system

The nature of female-limited mimicry in the myrmecomorphic plant bug Coquillettia insignis Uhler is described, including aspects of its relation to possible ant models and to co-occurring visual arthropod predators. Twelve species of ants were collected with C. insignis on its host plant Lupinus caudatus Kell., of which six species were common: third instar to adult female mimics closely resemble four of these six species, in both morphology and behaviour. The mimetic significance of these close correspondences is indicated by the results of over 500 feeding trials, using the three most common species of co-occurring visual arthropod predators as operators. Two of these three species (Sussacus papenhoei Gertsch: Salticidae; and Sinea diadema (Fabricius): Reduviidae), classified C. insignis with corresponding models and not with closely related, non-mimetic plant bugs. Furthermore, after having had a single 'unpleasant' experience with the ant Formica fusca assassin bugs that had previously accepted C. insignis as prey rejected them in 19 out of 23 trials. These findings indicate that C. insignis is a Batesian mimic, with visual arthropod predators functioning as one class of potential operator. Implications for future research on perception and learning in arthropod predators is briefly discussed.     

Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod

Omnivorous arthropods make dietary choices according to the environment in which they forage, mainly availability/quality of plant and/or prey resources. Such decisions and their subsequent impacts on life‐history traits may be affected by the availability of nutrients and water to plants, that is, through bottom‐up forces. By setting up arenas for feeding behavior observation as well as glasshouse cages for plant preference assessment, we studied effects of the presence of prey (Lepidoptera eggs) and nitrogen/water availability to host tomato plants on the foraging behavior and life‐history traits in the omnivorous predator Macrolophus pygmaeus (Heteroptera: Miridae). In the absence of prey, the predator fed equally on the plants treated with various levels of nitrogen and water. In the presence of prey, however, the feeding rate on plants decreased when the plant received low water input. The feeding rate on prey was positively correlated with feeding rate on plants; that is, prey feeding increased with plant feeding when the plants received high water input. Moreover, plants receiving high water input attracted more M. pygmaeus adults compared with those receiving low water input. For M. pygmaeus fitness, the presence of prey enhanced its fertility and longevity, but the longevity decreased when plants received low compared with high water input. In conclusion, the omnivorous predator may be obliged to feed on plants to obtain water, and plant water status may be a limiting factor for the foraging behavior and fitness of the omnivorous predator.     

Meat eating in wild hamadryas baboons: Opportunistic trade‐offs between insects and vertebrates

The consumption of meat may provide herbivorous animals with important nutrients that are scarce in their plant‐based diet. Seasonal variation in plant food availability has been suggested to motivate dietary flexibility in a range of species and thus primates may seek more prey when key plant resources are unavailable. Alternatively, prey encounter rate may drive meat eating. Here we investigate patterns of meat eating in hamadryas baboons (Papio hamadryas) at Filoha, Awash National Park, Ethiopia. The Filoha baboons rely largely on doum palm fruit (Hyphaene thebaica), which are available most months of the year, and the young leaves of Acacia senegal, which are more abundant during the wet season. We hypothesized that the baboons would consume more meat when H. thebaica and A. senegal were less available, which we tested by comparing meat eating and consumption of these plant food species from March 2005 through February 2006. Our results reveal a high rate of vertebrate meat eating at Filoha (0.028/hour of observation) compared with other hamadryas sites. We found no relationship, however, between meat eating (either insect or vertebrate) and either rainfall or consumption of H. thebaica or A. senegal, indicating that availability of preferred plant resources does not drive meat consumption. Vertebrate consumption and time spent feeding were significantly negatively associated; there was no relationship, however, between the consumption of animal matter and either home range size or daily path length. Vertebrate and insect consumption alternated throughout the year such that the baboons maintained a small amount of animal matter in their diet year‐round. Our results suggest that the baboons do not often actively seek animal matter, but consume it opportunistically, with the presence of locust and dragonfly swarms driving insect consumption, and both prey availability and the availability of feeding time shaping vertebrate predation.     

Molecular scatology as a tool to study diet: analysis of prey DNA in scats from captive Steller sea lions

The DNA of prey present in animal scats may provide a valuable source of information for dietary studies. We conducted a captive feeding trial to test whether prey DNA could be reliably detected in scat samples from Steller sea lions (Eumetopias jubatus). Two sea lions were fed a diet of fish (five species) and squid (one species), and DNA was extracted from the soft component of collected scats. Most of the DNA obtained came from the predator, but prey DNA could be amplified using prey-specific primers. The four prey species fed in consistent daily proportions throughout the trial were detected in more than 90% of the scat DNA extractions. Squid and sockeye salmon, which were fed as a relatively small percentage of the daily diet, were detected as reliably as the more abundant diet items. Prey detection was erratic in scats collected when the daily diet was fed in two meals that differed in prey composition, suggesting that prey DNA is passed in meal specific pulses. Prey items that were removed from the diet following one day of feeding were only detected in scats collected within 48 h of ingestion. Proportions of fish DNA present in eight scat samples (evaluated through the screening of clone libraries) were roughly proportional to the mass of prey items consumed, raising the possibility that DNA quantification methods could provide semi-quantitative diet composition data. This study should be of broad interest to researchers studying diet since it highlights an approach that can accurately identify prey species and is not dependent on prey hard parts surviving digestion.     

Seasonal and taxonomic aspects of the size of arthropods in the tropics and its possible influence on size-selectivity in the prey of a tropical spider community

Summary During one year in Panama the size (=body length) of arthropods (representing the potential prey of a spider community) was determined by sampling with pitfall traps, bowl traps and sweep-netting. Most arthropods found were small and the distribution of their size is considerably skewed to the left (Figs. 1, 2). Pitfall traps and bowl traps yielded similar results but sweep-netting collected larger arthropods and may be size-selective. Although the variation of arthropod size is high, no seasonal influence on body size could be detected in the main prey groups of spiders (Figs. 3, 4). Differences in the size spectra of the actual prey of a tropical spider community are therefore not caused by seasonal variations in the availability of particular prey size classes. Species-specific prey size spectra, however, may be dependent on properties of the webs concerned, microhabitat selection or other, e.g. physiological or ethological differences between the spider species.