Foraging activity of a dominant epigeal predator: molecular evidence for the effect of prey density on consumption

Despite the widely held assumption that ‘generalist’ predators consume most prey available to them, there is a growing body of evidence suggesting otherwise. Generalists are expected to perform well in disturbed areas because they can switch between prey pathways when one food source becomes depleted. Indeed, these predators have the potential to promote diversity by switching to prey in a frequency dependent manner and consume prey groups in relation to local abundance. It is therefore important to understand how predation rates fluctuate as local availability changes. We performed open‐field and mesocosm experiments in a corn and soybean agroecosystem to delineate the role prey density plays in determining predation frequency of a dominant epigeal predator. To track trophic pathways, molecular gut‐content analysis using enzyme‐linked immunosorbent assay (ELISA) was performed to track foraging behavior of the wolf spider Pardosa milvina feeding on dipterans, flies. Extensive monitoring of foraging activity and prey populations revealed that predation varied temporally. Importantly, the frequency of individuals testing positive for flies was lower than predicted when flies were extremely abundant but higher when they were scarce, relative to the prey community as a whole. Furthermore, isolating predators in mesocosms revealed an effect of Diptera density on the likelihood of consumption, as determined by ELISA, only when flies were at low levels (12.5% of prey provided). The molecular results suggest that these spiders do not appear to be consuming flies in a frequency‐dependent manner where the decision to switch between different prey pathways is driven by relative abundance. Rather, selectivity of prey is somewhat independent of variation of other prey groups, which is indicative of their consistent reliance on dipterans and may be related to nutritional requirements and/or capture success.     

Foraging responses of predators to novel toxic prey: effects of predator learning and relative prey abundance

Learning to avoid toxic prey items may aid native predators to survive the invasion of highly toxic species, such as cane toads Bufo marinus in tropical Australia. If the predators’ initial aversion is generalized, native prey that resemble the toxic invader may receive a benefit through accidental mimicry. What ecological factors influence the acquisition of learned avoidance (and hence, the impact of invasion on both predators and native prey)? We conducted laboratory experiments to evaluate how the relative abundance of toad tadpoles compared to palatable native tadpoles (Litoria caerulea and L. rubella) affected the ability of native aquatic predators to discriminate between these two prey types. Both fish (northern trout gudgeon, Mogurnda mogurnda) and frogs (Dahl's aquatic frog, Litoria dahlii) learned to discriminate between toads and frogs within an eight‐day period. Higher abundance of toad tadpoles relative to frog tadpoles enhanced rates of predator learning, and thus reduced predation on toads and increased predation on native tadpoles. In the field, spatial and temporal variation in the relative abundance of cane toads compared to native frogs may influence the rates at which these novel toxic items are deleted from predator diets, and the duration of predator protection afforded to natives that resemble the invader.     

The impact of a sit-and-wait predator: separating consumption and prey emigration

Reviews of the impact of invertebrate predators in enclosure/exclosure experiments suggest that much of the apparent depletion of prey is due to prey emigration induced by the predators. However, these generalisations derive mainly from studies of invertebrate predators that are predominantly active searchers (usually stoneflies) and of prey with strong avoidance responses (mainly mayflies).
We examined the impact of a large sit-and-wait predator, the nymph of the dragonfly Cordulegaster boltonii , which has recently invaded Broadstone Stream as a new top predator. Field enclosure/exclosure experiments were conducted to assess the impact of the invader on the benthos. Depletion of prey varied seasonally and among taxa, and was highest when prey density and encounter rates were high. Mobile prey, although least likely to show a statistically significant response because of high exchange rates, were those most strongly depleted.
Experimental channels were used to separate the relative contribution of consumption and emigration to total impact for the two most depleted prey species. Depletion of prey was due solely to consumption and predators did not induce emigration. We therefore urge caution in making generalisations about the impacts of invertebrate predators, since sit-and-wait and searching predators potentially have very different impacts.     

Land cover diversity increases predator aggregation and consumption of prey

A lower diversity of land cover types is purported to decrease arthropod diversity in agroecosystems and is dependent on patterns of land use and fragmentation. Ants, important providers of ecosystem services such as biological control, are susceptible to landscape‐level changes. We determined the relationships between land cover diversity and fragmentation on the within‐field spatial associations of ants to pests and resulting predation events by combining mapping and molecular tools. Increased land cover diversity and decreased fragmentation increased ant abundance, spatial association to pests and predation. Land cover diversity and fragmentation were more explanatory than land cover types. Even so, specific land cover types, such as deciduous forest, influenced ant and pest diversity more so than abundance. These results indicate that geospatial techniques and molecular gut content analysis can be combined to determine the role of land use in influencing predator–prey interactions and resulting predation events in agroecosystems.     

Structural evidence why males of Panorpa liui offer prey rather than salivary mass as their nuptial gift

Ma, N. and Hua, B. 2010. Structural evidence why males of Panorpa liui offer prey rather than salivary mass as their nuptial gift. —Acta Zoologica (Stockholm) 92 : 398–403. The scorpionflies are considered as ideal model animals for the study of mating systems in insects. The males generally offer both prey and salivary mass as nuptial gifts to the females during copulation. Our field observations show that Panorpa liui is peculiar because the males offer only prey rather than salivary secretions as nuptial gift. Through anatomical and histological examinations, the salivary glands of P. liui were found to be devoid of sexual dimorphism in Panorpa for the first time. Both the male and female P. liui bear simple salivary glands, which are only composed of a common duct and two short sac‐like glands. This is the first attempt to explore the relationship between the salivary glands and the mating tactics from the structural aspect in Panorpa, speculating that the simple structure of the male salivary glands in P. liui might be responsible for its failing to produce salivary mass as a nuptial gift during copulation. Compared with Boreidae, Meropidae, Bittacidae and Panorpidae, we presume that the absence of sexual dimorphism of the salivary glands might represent a plesiomorphy in P. liui. The origin and evolutionary process of the nuptial gift behaviour are tentatively speculated in Panorpa.     

Effects of chronic exposure to a toxic prey in a generalist predator

Abstract.  Generalist predators experience large differences in prey quality, and eating toxic prey may affect their fitness even if the toxic prey constitutes only a small fraction of a mixed diet. Feeding and life history parameters were examined in the wolf spider Pardosa prativaga during continuous exposure to the toxic collembolan Folsomia candida . Spiderlings were divided into a control group fed adult Drosophila melanogaster , a group fed only F. candida , and a mixed diet group fed both types of prey. Folsomia candida reduced survival, developmental stage attained and growth rate of all exposed spiders. Spiders chronically exposed to F . candida increased their consumption of D. melanogaster compared to control spiders. Folsomia candida thus inhibited the utilization of the high-quality food and/or increased the respiration rate. The intake of F . candida remained at a constant low level throughout the experiment, indicating that P. prativaga was unable to develop an absolute aversion against this prey. Half of the control group was also given the mixed diet after a large juvenile instar was attained. These spiders were not affected to the same extent as the newly hatched spiderlings, indicating an ontogenetically increased tolerance. Comparison of laboratory-raised and field-caught spiders confirmed that tolerance to F. candida was size-dependent and thus not an induced response. A differential survival in the mixed diet group, based partly on maternal effects, indicated possible genetic variability in the physiological tolerance to F. candida .     

Beyond ecological opportunity: Prey diversity rather than abundance shapes predator niche variation

1. Ecological opportunity (i.e. the diversity of available resources) has a pivotal role in shaping niche variation and trophic specialisation of animals. However, ecological opportunity can be described with regard to both diversity and abundance of resources. The degree to which these two components contribute to niche variation remains unexplored.
2. To address this, we used an extensive dataset on fish diet and benthic invertebrate diversity and density from 73 sampling events in three Norwegian rivers in order to explore realised trophic niches and the response of dietary niche variation along gradients of resource diversity (potential trophic niches), resource density (as a proxy of resource abundance) and fish density (as a proxy of inter‐ and intra‐specific competition) in a freshwater top predator (the brown trout, Salmo trutta L.).
3. Linear models indicated that individual and population niche variation increased with increasing ecological opportunity in terms of prey diversity. However, no simple cause‐and‐effect associations between niche indices and prey abundance were found. Our multiple regression analyses indicated that the abundance of certain resources (e.g. Chironomidae) can interact with prey diversity to determine individual and population realised trophic niches. Niche variation (within‐individual component and inter‐individual diet variation) decreased with increasing inter‐ and intra‐specific competition.
4. This study extends prevailing trophic ecology theory by identifying diversity, rather than density, of available prey resources as a primary driver of niche variation in fish of temperate riverine systems with no extensive resource limitation. The study also shows that ecological opportunity may mask the direction of the effect (compression or expansion) of competition on niche variation when food resources are diverse.
5. Our study provides novel empirical insight to the driving forces behind niche variation and reveals that diversity, rather than density, of available prey resources may be a primary driver of niche variation in freshwater fish. Our study supports the view that a broader potential trophic niche promotes broader realised trophic niche variation by individuals, which leads to individual niche diversification by opening access to alternatives resources, resulting in a concomitant rise in the realised trophic niche width of the population.

     

Taphonomic evidence of a Paleogene mammalian predator–prey interaction

A taphonomic study has been undertaken on an assemblage of bones and teeth of Isoptychus sp. and Thalerimys fordi (extinct rodent family Theridomyidae) from a single bed in a coastal plain setting, in the Late Eocene (Priabonian) Osborne Member, Headon Hill Formation (Hampshire Basin, UK). The vertebrate fossils show good preservation and do not bear the marks of obvious long distance transport. The two theridomyid species show similar patterns of mortality, element representation and surface modifications, which indicate similar mechanisms of accumulation. There is high mortality of juvenile and old individuals indicating accumulation of the assemblage by the action of attritional not catastrophic agents. The postcranial elements show fragmentary states and very low relative abundances. The vast majority of elongate bones (limb bones, phalanges and metapodials) are broken and exhibit a spiral irregular type of fracture with rounded fracture edges indicating that the bones were broken when they were fresh and have subsequently undergone additional modification. The enamel of most of the cheek teeth and incisors shows localized etching to various degrees and most of the bones show etching. By elimination of other modifying agents the observed etching is attributed to digestive corrosion. Collectively, these data indicate that the majority of the theridomyid individuals were eaten and digested by an animal that could cause high fragmentation during ingestion and with stomach juices of relatively high acidity. Both these features characterize mammalian carnivores. The presence of puncture marks on bones of both theridomyid species and comparisons with sizes of bite marks caused by extant mammalian carnivores suggest predation by a small mammalian carnivore about the size of an arctic fox. The extinct amphicyonid carnivoran Cynodictis cf. lacustris occurs in the same bed and the sizes of some of its teeth match well with the sizes of the puncture marks on the theridomyid bones. A predator–prey interaction is, therefore, deduced for the amphicyonid and the two theridomyid species, thereby reconstructing a small part of the continental Paleogene food chain.     

Dynamics of predator and modular prey: effects of module consumption on stability of prey–predator system

In traditional models of predator–prey population dynamics, it is usually assumed that consumed prey are immediately removed from the population. However, in plant–herbivore interactions, damaged plants are generally alive after attacks by herbivores. This can result in successive or simultaneous attacks by multiple predators on a single prey item (here, the term prey is expanded to include plants). We constructed a mathematical model with two time scales, taking into account predation processes within a generation, considering post‐predation survival and the modularity of prey. We assumed that a prey item can be divided into modules and that it can be fed on by multiple predators or parasitized by multiple parasites at the same time. The model includes two essential factors: the modularity of prey for predators (n) and the detaching/attaching ratio of predators to prey (ε). Based on the formulae, we revealed a general property of realistic dynamics in plant–herbivore and host–parasite interactions. The analysis showed that the model could be approximated by models with the type I, type II or Beddington–DeAngelis functional responses by taking appropriate limits to the situations. When modularity is low or the detaching/attaching ratio is high, population dynamics tend to be stabilized. These stabilizing effects may be related to interference competition among predator individuals or increases in free prey modules and free predator individuals. In the limit of high modularity, the ratio of the attached prey modules to the total prey modules becomes negligible and the dynamics tend to be destabilized. However, if quantity and quality of prey modules are negatively correlated, the equilibrium is likely to be stabilized at high modularity as long as it remains feasible. These results suggest that considering post‐predation survival and modularity of prey is crucial to understand predator–prey interactions.     

Generalist caterpillar prey are more palatable than specialists for the generalist predator Iridomyrmex humilis

Summary Experiments are described which test the hypothesis that more host-specific species of caterpillars should be less aceptable to a generalist predator than polyphagous species. Caterpillars of all species were tested in paired choice tests with the Argentine ant, Iridomyrmex humilis. Experiments were replicated ten times, videotaped and later analyzed. Brightly colored specialist species (normally considered to be aposematic) were clearly the least palatable, while more cryptic specialists were also significantly less acceptable than generalists overall. Leaf-tying species were considered separately; all were highly palatable independent of host range. The results indicate that among caterpillars that do not construct leaf shelters, those with a wide post range are more acceptable than those with a narrow host range. This is consistent with the notion that generalist predators provide selection pressure favoring narrow host range in their herbivorous prey.     

Behavioural responses of native predators to an invasive toxic prey species

One important impact of invasive species may be to modify the behaviour of native taxa. For example, the invasion of highly toxic cane toads (Bufo marinus) kills many anurophagous native predators, but other predators learn to recognize and avoid the toxic invader. We exposed native fish (northern trout gudgeons, Mogurnda mogurnda) and Dahl's aquatic frogs (Litoria dahlii) to cane toad tadpoles, then monitored the predator's responses during subsequent trials. Both the frogs and fish initially attacked toad tadpoles, but rapidly learned not to do so. Fish and adult frogs retained their aversion for at least a week, whereas recently metamorphosed frogs did not. Clearly, the spread of cane toads through tropical Australia can modify feeding responses of native aquatic predators. For predators capable of rapid avoidance learning, the primary impact of cane toads may be on foraging behaviour rather than mortality.     

Sublethal costs associated with the consumption of toxic prey by snakes

Costs of plant defences to herbivores have been extensively studied, but costs of chemical defences to carnivores are less well understood. We examine the costs to Australian keelback snakes (Tropidonophis mairii, Gray 1841) of consuming cane toads (Bufo[Rhinella]marinus Linnaeus 1758). Cane toads (an invasive species in Australia) are highly toxic. Although keelbacks can consume toads without dying (unlike most Australian snakes), we show that cane toads are poor quality prey for keelbacks. Toads are of low net nutritional value, take longer to consume than do native frogs and reduce the snake's locomotor performance for up to 6 h after ingestion of a meal. These latter effects may increase a snake's vulnerability to predation. Nutritional content of vertebrate prey is not the only factor driving the evolution of foraging behaviour; other more subtle costs, such as risk of predation, may be widespread.     

Variable but predictable prey availability affects predator breeding success: natural versus experimental evidence

Food supply is a major source of variation in breeding success for predators, and to what extent individuals are able to cope with temporal variability in food availability remains an outstanding question in life-history studies. We confronted the natural variation in clutch size and breeding success with results from a food supplementation experiment during egg formation, conducted over several contrasted years of natural food supply in an avian specialist predator, the Montagu's harrier Circus pygargus . This raptor mainly preys on common vole Microtus arvalis a cyclic microtine under temperate latitudes. Vole abundance together with timing of breeding accounted for most of the variance in clutch size and number of fledglings. Results from empirical and experimental data were overall in agreement. Fed pairs consistently increased clutch size compared with controls in all experimental years, whereas no effect of food supplementation on egg volume was detected. Supplemented pairs, however, did not fledge significantly more chicks than controls. The costs entailed by the increase in clutch size appear nevertheless to be limited compared with previous studies. Food supply seemed therefore to display sufficient predictability throughout a breeding season to afford individuals the opportunity to adjust their breeding effort to an optimal number of offspring, in agreement with Lack's anticipation hypothesis.     

Experimental evidence for emergent facilitation: promoting the existence of an invertebrate predator by killing its prey

1. Recent theoretical insights have shown that predator species may help each other to persist by size-selective foraging on a shared prey. By feeding on a certain prey stage, a predator may induce a compensatory response in another stage of the same prey species, thereby favouring other predators; a phenomenon referred to as emergent facilitation. 2. To test whether emergent facilitation may occur in a natural system, we performed an enclosure experiment where we mimicked fish predation by selectively removing large zooplankton and subsequently following the response of the invertebrate predator Bythotrephes longimanus. 3. Positive responses to harvest were observed in the biomass of juvenile individuals of the dominant zooplankton Holopedium gibberum and in Bythotrephes densities. Hence, by removing large prey, we increased the biomass of small prey, i.e. stage-specific biomass overcompensation was present in the juvenile stage of Holopedium. This favoured Bythotrephes, which preferentially feed on small Holopedium. 4. We argue that the stage-specific overcompensation occurred as a result of increased per capita fecundity of adult Holopedium and as a result of competitive release following harvest. If shown to be common, emergent facilitation may be a major mechanism behind observed predator extinctions and patterns of predator invasions.     

Specificity of thrombin: evidence for selectivity in acylation rather than binding for p-nitrophenyl alpha-amino-p-toluate.

The lysyl ester analogue p-nitrophenyl alpha-amino-p-toluate hydrobromide was synthesized, and its reactions with thrombin, trypsin, and plasmin were studied by stopped-flow and conventional methods. Kinetic parameters were compared with those determined for the arginyl ester analogue, p-nitrophenyl p-guanidinobenzoate hydrochloride, with these enzymes. By following nitrophenol release or proflavin absorption changes in the stopped-flow spectrophotometer, the constants Ks (enzyme-substrate binding), k2 (acylation), and k3 (deacylation) were determined. The major findings were: (1) Ks values were similar regardless of the substrate or the enzyme; (2) k3 was approximately the same for the reaction of the lysyl ester analogue with any enzyme; (3) k2 for the lysyl ester analogue was 1100 times greater with trypsin than with thrombin; and (4) k2 with thrombin was 60 times greater for the arginyl than for the lysyl ester analogue. The results suggest that the limited cleavage of lysyl bonds by thrombin is due in part to restricted acylation rather than substrate binding. The active site of thrombin, compared with that of trypsin, appears to have a more stringent requirement for the spatial relationship between the cationic group and the bond cleaved in substrates.