Biochemical prey recognition by planktonic protozoa

Planktonic flagellates and ciliates are the major consumers of phytoplankton and bacterioplankton in aquatic environments, playing a pivotal role in carbon cycling and nutrient regeneration. Despite certain unicellular predators using chemosensory responses to locate and select their prey, the biochemical mechanisms behind prey reception and selection have not been elucidated. Here we identify a Ca(2+)-dependent, mannose-binding lectin on the marine dinoflagellate Oxyrrhis marina, which is used as a feeding receptor for recognizing prey. Blocking the receptor using 20 microM mannose-BSA inhibited ingestion of phytoplankton prey, Isochrysis galbana, by 60%. In prey selection studies, O. marina ingested twice as many 6 mum diameter beads coated with mannose-BSA as those coated with galNac-BSA. When pre-incubated with mannose-BSA, O. marina was no longer able to discriminate between different sugar-coated beads. Thus, these findings reveal molecular mechanisms of protozoan prey recognition. Our results also indicate the functional similarity between cellular recognition used by planktonic protozoa to discriminate between different prey items, and those used by metazoan phagocytic blood cells to recognize invading microorganisms.     

Evolution of cannibalism: referring to costs of cannibalism

A rational explanation for cannibalism is that it would be favored under conditions of crowding of conspecific individuals and/or low availability of alternative prey with the fear of starvation, so as to maximize individual fitness. Cannibalism has, however, not evolved and is not maintained by a simple individual optimization, while it has evolved and is maintained as a game among population members. We analysed the attainable state of an evolutionary cannibalism game within a framework that reflects the minimum essence of cause-effect in the cannibalism phenomenon. Cannibalism is predator-prey interaction among conspecifics. Immediate direct payoffs (survival in the interaction among conspecifics) and indirect payoffs (growth results in potential productivity and survival against the threat of starvation) would be included. No morphological specialization and no size priority of cannibalism individuals are assumed as conservative situations in which we analyse the possibility of cannibalism. Cannibalism would be possible under the conservative condition, if initially the wild population's cannibalism rate is not sufficiently lower than a threshold value. Crowding and/or low availability of alternative prey with the fear of starvation facilitates cannibalism evolution. Energy gain from conspecific prey would be attenuated by costs of counterattacks by conspecific victims and by challenge cost of its own. Discounting net intake energy required in the arms race for cannibalism challenge result in a relative disadvantage of having a high cannibalism rate and makes an evolutionary equilibrium of low cannibalism rate, even when potential profitability of conspecific prey is high.     

Easy Visualization of the Protist <Emphasis Type="Italic">Oxyrrhis</Emphasis><Emphasis Type="Italic">marina</Emphasis> Grazing on a Live Fluorescently Labelled Heterotrophic Nanoflagellate

Planktonic heterotrophic flagellates are ubiquitous eukaryotic microorganisms that play a crucial role in carbon and nutrient fluxes through pelagic food webs. Here we illustrate for the first time a grazing model of planktonic dinoflagellate, Oxyrrhis marina, on the heterotrophic nanoflagellate Goniomonas amphinema, using the DNA-binding fluorescent dye Hoechst 33342. A solution of 1 microg/mL of the fluorochrome allowed viability of the prey for at least 48 hours, provided low fluorescence quenching, and labelled the flagellate without masking the cytoplasm. After 2 hours of contact between the fluorescent prey and the predator, O. marina population had preyed on live G. amphinema at an ingestion rate of 2.2 prey Oxyrrhis (-1) h(-1). Results show that this model is a time-effective and inexpensive approach for the direct observation of heterotrophic flagellate grazing. The fact that prey remain alive while predation occurs, as well as the low rate of quenching, could be of help in studying the fate of real-time trophic interactions between protists in microbial webs.     

Emergent impacts of cannibalism and size refuges in prey on intraguild predation systems

Many organisms undergo ontogenetic niche shifts due to considerable changes in size during their development. These ontogenetic shifts can alter the trophic position of individuals, the type and strength of ecological interactions across species, and allow for cannibalism within species. In this study we ask if and how the interaction of a size refuge and cannibalism in the prey alters the dynamics of intraguild predation (IGP) systems. By manipulating the composition of large cannibalistic (Aeshna umbrosa) and predatory (Anax junius) dragonfly larvae in mesocosms we show that the interaction of cannibals and predators was non-linear and increased the survival of prey. The structure of the final resource community shared by prey and predator differed between small and large dragonfly treatments but not within size classes across species. In general, the small prey stage showed similar shifts in microhabitat use and refuge use when exposed to either conspecific cannibals or predators, while large cannibals showed no clear anti-predator response. However, further behavioral experiments revealed that specific behavioral components, such as distances between individuals or number of movements, differed when individuals were exposed to either cannibals or predators. This indicates that individuals discriminated between conspecific or heterospecific predators. Furthermore, in similar experiments large cannibals and predators showed different behaviors when exposed to conspecifics rather than to each other. These changes in behavior are consistent with the observed increase in prey survival. In general, the results indicate that cannibalism and ontogenetic niche shifts can result in behavior-mediated indirect interactions that reduce the impact of the predator on the mortality of its prey and alter the interactions of IGP systems. However, they also indicate that size is not the sole determinant and that we also need to account for the species identity when predicting the dynamics of communities.     

Plant and Prey Consumption Cause a Similar Reductions in Cannibalism by an Omnivorous Bug

Cannibalism is usually more intense when other food sources are scarce, be it prey or plant-based foods. We hypothesized that feeding on plants would reduce cannibalism to a lesser extent than feeding on prey, because plants are considered nutritionally inferior compared to prey. We used the omnivorous bug Orius laevigatus Say (Heteroptera: Anthocoridae) to test this prediction. Starved female bugs were individually held with five second-instar conspecific nymphs and offered (i) Helicoverpa armigera eggs (prey); (ii) pollen (plant); (iii) H. armigera eggs and pollen (prey+plant); or (iv) no eggs or pollen. Fewer cannibalistic events and shorter feedings on conspecifics were recorded in the presence of pollen, prey or both than in their absence. Data therefore do not support our hypothesis that cannibalism is differentially affected by foods of different nutritional values. It seems that omnivorous feeding habits enable predators to sustain themselves on plant sources in the absence of prey, without the need to resort to cannibalism.     

Sibling cannibalism among juvenile vundu under controlled conditions. I. Cannibalistic behaviour, prey selection and prey size selectivity

Sibling cannibalism among vundu Heterobranchus longifilis larvae started at the age of 4 days, with the prey caught tail-first then swallowed up to the head, which was eventually discarded (type I cannibalism). At 17 days old, this type of cannibalism vanished and was replaced by the ingestion of the whole prey (type II cannibalism), which could only be exerted by predators six times as heavy as their prey. Type II cannibalism consisted of a seemingly opportunistic ambush attack by a formerly passive predator towards a disorientated prey. It required no preliminary aggression or chase, or even contact with the prey, suggesting that the attack was not mediated by the tactile sense, and that cannibalism was independent of aggressive behaviour. When alternative food resources (formulated feed, live tilapia prey) were available, the intensity of cannibalism decreased but pellet-eaters or tilapia predators always achieved lower growth rates than those feeding on conspecifics, suggesting that cannibalism was the most advantageous foraging tactic. Losses to cannibalism among populations of 30-day old juvenile vundu with an initial ratio of 4% of cannibals were as high as 75·5–79·9% over 15 days. Predation peaked during the first days (up to 2·8 prey C⁻¹ day⁻¹), then vanished progressively as surviving prey grew faster than cannibals and escaped their predation. Cannibals preferred consuming the largest prey available with respect to the logistics of cannibalism (body weight ratio of 6·0). This preference for large prey was interpreted both as a foraging tactic aiming to maximize the energetic return, and as foraging strategy enabling the cannibals to exploit their prey as long as possible. Based on these data, comprehensive models of the impact of cannibalism on vundu populations were developed.     

Direct and indirect effects of predation on mosquitofish behavior and survival

Predation can have strong direct and indirect effects on the behavior of prey. We investigated whether predation by chain pickerel (Esox niger) caused adult eastern mosquitofish (Gambusia holbrooki) to alter their habitat use and whether pickerel predation influenced survival of adult and neonate mosquitofish. The number of adult mosquitofish using the riskier of three habitats was lowest when two predators occupied the risky habitat, intermediate in the treatment with one predator, and highest when no predators occurred there. More mosquitofish neonates survived high predation treatments than treatments lacking pickerel. We conclude that pickerel predation causes adult mosquitofish to shift to refuge habitats. The pattern of neonate survival suggests that adult habitat use may create a refuge from cannibalism for neonate mosquitofish, resulting in higher neonate survival in treatments with more pickerel. Hence, pickerel predation has a direct effect on adult mosquitofish behavior and a strong indirect effect on neonate survival. Both interspecific and intraspecific predation can effect prey populations and can interact to produce important indirect effects.     

Influence of prey availability and conspecifics on patch quality for a cannibalistic forager: laboratory experiments with the wolf spider Schizocosa

 Because cannibals are potentially both predator and prey, the presence of conspecifics and alternative prey may act together to influence the rate at which cannibals prey upon each other or emigrate from a habitat patch. Wolf spiders (Lycosidae) are cannibalistic-generalist predators that hunt for prey with a sit-and-wait strategy characterized by changes in foraging site. Little information is available on how both prey abundance and the presence of conspecifics influence patch quality for these cursorial, non-web-building spiders. To address this question, laboratory experiments were conducted with spiderlings and older juveniles of the lycosid genus Schizocosa. The presence of insect prey consistently reduced rates of spider emigration when spiders were housed either alone or in groups. Solitary juvenile Schizocosa that had been recently collected from the field exhibited a median giving-up time (GUT) of 10 h in the absence of prey (Collembola); providing Collembola increased the median GUT to 64 h. For solitary spiders, the absence of prey increased by about fourfold the rate of emigration during the first 24 h. In contrast, for spiders in patches with a high density of conspecifics, the absence of prey increased the 24-h emigration rate by only 1.6-fold. For successful cannibals in the no-prey patches, the presence of conspecifics improved patch quality by providing a source of food. Mortality by cannibalism was affected by both prey availability and openness of the patch to net emigration. In patches with no net emigration, the presence of prey reduced rates of cannibalism from 79% to 57%. Spiders in patches open to emigration but not immigration experienced a rate of cannibalism (16%) that was independent of prey availability. The results of these experiments indicate that for a cannibalistic forager such as the wolf spider Schizocosa, (1) the presence of conspecifics can improve average patch quality when prey are absent, and (2) cannibalism has the potential to be a significant mortality factor under natural field conditions because cannibalism persisted in prey patches that were open to emigration. Received: 12 April 1996 / Accepted: 14 August 1996     

Influence of a dorsal trash-package on interactions between larvae of Mallada signata (Schneider) (Neuroptera: Chrysopidae)

Abstract Larvae of the native Australian chrysopid Mallada signata use discarded prey items and environmental debris ('trash'), carried on the dorsal abdominal segments, as camouflage. Larvae that carry trash were confirmed experimentally to experience lower rates of cannibalism, an effect attributed to the camouflage conferred by the package. Larvae preferred physically hard material over normal dietary items when constructing their trash-package. The inclusion of these materials in the package may provide both physical and chemical camouflage from predator and prey alike. When encounter rates between conspecifics were low, larvae that carried trash increased their activity rates as they aged. In contrast, trash-denuded larvae decreased activity rates as they aged. Among first-instar larvae, as the density of larvae increased and encounters became more frequent, those with trash moved further than those without. Larvae with trash packages exhibited lower cannibalism and higher activity rates, which may subsequently enhance foraging capacity.     

Refuge from cannibalism in complex-structured habitats: implications for the accumulation of invertebrate predators

Abstract.  1. Like many invertebrate predators, the wolf spider Pardosa littoralis Banks (Araneae: Lycosidae) accumulates in complex-structured habitats replete with leaf litter (thatch). Here we test the hypothesis that P. littoralis accumulates in complex habitats to gain refuge from cannibalism.
2. A laboratory experiment examined the effects of habitat complexity (thatch present or absent) and size-class pairing of conspecific spiders (large vs. small, small vs. small, and large vs. large) on the incidence of cannibalism. Spider survival was significantly higher (22%) in complex-structured habitats with thatch than in simple-structured habitats lacking thatch. Furthermore, cannibalism occurred more frequently in P. littoralis when the size of conspecifics was asymmetric (large vs. small spiders) than when spiders were of equal size. There was no interactive effect of habitat complexity and size-class pairing on spider survival.
3. A field experiment examined the effects of habitat complexity, conspecific density, and access to alternative prey on the prevalence of cannibalism in P. littoralis . Access to alternative prey significantly increased the number of spiders recovered from field enclosures, as did the presence of leaf litter thatch. That fewer spiders were recovered when thatch and alternative prey were absent suggests that cannibalism was most prevalent under these conditions.
4. Overall, results suggest that habitat complexity reduces agonistic interactions and cannibalism among wolf spiders, providing encouragement to pest managers that the structure of agricultural habitats can be managed to maximise densities of generalist predators for enhanced pest suppression.     

Genotyping confirms significant cannibalism in northern Gulf of Mexico invasive red lionfish, <Emphasis Type="Italic">Pterois volitans</Emphasis>

DNA barcoding is used in a variety of ecological applications to identify organisms, including partially digested prey items from diet samples. That particular application can enhance the ability to characterize diet and predator–prey dynamics but is problematic when genetic sequences of prey match those of consumer species (i.e., self-DNA). Such a result may indicate cannibalism, but false positives can result from contamination of degraded prey samples with consumer DNA. Here, nuclear-encoded microsatellite markers were used to genotype invasive lionfish, Pterois volitans, consumers and their prey (n?=?80 pairs) previously barcoded as lionfish. Cannibalism was confirmed when samples exhibited two or more different alleles between lionfish and prey DNA across multiple microsatellite loci. This occurred in 26.2% of all samples and in 42% of samples for which the data were considered conclusive. These estimates should be considered conservative given rigorous assignment criteria and low allelic diversity in invasive lionfish populations. The highest incidence of cannibalism corresponded to larger sized consumers from areas with high lionfish densities, suggesting cannibalism in northern Gulf of Mexico lionfish is size- and density-dependent. Cannibalism has the potential to influence population dynamics of lionfish which lack native western Atlantic predators. These results also have important implications for interpreting DNA barcoding analysis of diet in other predatory species where cannibalism may be underreported.     

Predator cannibalism can shift prey community composition toward dominance by small prey species

Cannibalism among predators is a key intraspecific interaction affecting their density and foraging behavior, eventually modifying the strength of predation on heterospecific prey. Interestingly, previous studies showed that cannibalism among predators can increase or reduce predation on heterospecific prey; however, we know less about the factors that lead to these outcomes. Using a simple pond community consisting of Hynobius retardatus salamander larvae and their associated prey, I report empirical evidence that cannibalism among predators can increase predation on large heterospecific prey but reduce that on small heterospecific prey. In a field‐enclosure experiment in which I manipulated the occurrence of salamander cannibalism, I found that salamander cannibalism increased predation on frog tadpoles but reduced that on aquatic insects simultaneously. The contrasting effects are most likely to be explained by prey body size. In the study system, frog tadpoles were too large for non‐cannibal salamanders to consume, while aquatic insects were within the non‐cannibals’ consumable prey size range. However, when cannibalism occurred, a few individuals that succeeded in cannibalizing reached large enough size to consume frog tadpoles. Consequently, although cannibalism among salamanders reduced their density, salamander cannibalism increased predation on large prey frog tadpoles. Meanwhile, salamander cannibalism reduced predation on small prey aquatic insects probably because of a density reduction of non‐cannibals primarily consuming aquatic insects. Body size is often correlated with various ecological traits, for instance, diet width, consumption, and excretion rates, and is thus considered a good indicator of species’ effects on ecosystem function. All this considered, cannibalism among predators could eventually affect ecosystem function by shifting the size composition of the prey community.     

Eat or Not to Eat: Reversed Sexual Cannibalism as a Male Foraging Strategy in the Spider Micaria sociabilis (Araneae: Gnaphosidae)

Reversed sexual cannibalism represents an unusual situation in which a male kills and consumes a female. We examined this rare phenomenon in the spider Micaria sociabilis, whose males were observed to regularly cannibalise old females. In this study, we investigated male motivation for such behaviour in the light of ecological conditions such as mate availability and prey availability. We found that male cannibalism is not affected by short‐term starvation but rather by male feeding history during the ontogenetic development in combination with prey availability during the adult stage. Males from the summer generation reached bigger sizes than males from the spring generation and females from both generations. They developed in the period with exceptionally high prey occurrence, but when they reached the adult stage, the prey availability decreased. In this period, we observed the highest frequency of cannibalism, however, only when the sex ratio was female biased. Reversed sexual cannibalism in M. sociabilis seems to represent an advantageous male foraging strategy, which is affected by prey availability and male feeding history, tuned by sex ratio and directed towards females of inferior quality.     

A survey of intraspecific predation within the class Mammalia

The occurrence of cannibalism in mammals was studied during a general review of cannibalism (Polis, 1981). In total, there were 146 references documenting intraspecific predation in 75 species of mammals distributed between seven orders. Of these references, 138 refer to cannibalism whereas eight studies refer to intraspecific killing unaccompanied by cannibalism. Of the papers that specified the identity of both the predator and the prey, approximately 80% referred to infanticide (including cannibalism). It appears that infanticide often functions as part of a reproductive strategy. Juveniles and adults are occasional intraspecific prey for some species of Insectivora, Chiroptera, Primates, Lagomorpha, Rodentia, Carnivora, and Artio-dactyla. Cannibalism was best documented for the carnivores, rodents and primates. In general, cannibalism often occurs during normal predatory activities and is a function of low food availability, environmental stress, and a high density of conspecifics.     

Feeding strategy and cannibalism of the Argentine hake Merluccius hubbsi

The diet composition and feeding strategy of the Argentine hake Merluccius hubbsi in the San Matías Gulf were analysed in order to use this information for the sustainable management of the fishery. Merluccius hubbsi behaved as an opportunistic predator. Small M. hubbsi consumed planktonic crustaceans, whereas medium and large fish ate numerous prey taxa with low frequency of occurrence and variable specific abundance. Intra- and intercohort cannibalism were detected in all size groups and were particularly significant in large M. hubbsi. Medium-sized M. hubbsi consumed small conspecifics and large-sized M. hubbsi consumed both small and medium M. hubbsi. These results indicate that the removal of large M. hubbsi by fishing may increase the risk of overfishing by two combined effects: a direct effect of recruitment-overfishing and an indirect effect of growth-overfishing through an enhanced cannibalism of medium M. hubbsi on small M. hubbsi. Intra- and intercohort cannibalism and other trophic relationships in the M. hubbsi should therefore be considered explicitly in stock assessment models.     

Conceptual Bases for Prey Biorecognition and Feeding Selectivity in the Microplanktonic Marine Phagotroph <Emphasis Type="Italic">Oxyrrhis marina</Emphasis>

It is suspected that phagotrophic marine protozoa might possess feeding receptors that enable them to discern the nutritional quality of individual prey items (during prey-handling) on the basis of their cell-surface biochemistry. This article reviews advances in our understanding of the molecular mechanisms that mediate the biorecognition and selection of nonself (microalgal) prey items by the microplanktonic marine phagotroph Oxyrrhis marina. The potential importance of lectin–glycan interactions is first considered in view of findings which demonstrate that O. marina possesses lectin-like feeding receptors specific for prey-surface (mannose) glycoconjugates. Secondly, some conceptual bases for indirect or ‘opsonic’ modes of prey biorecognition mediated by soluble prey-labelling proteins are presented. Finally, the possibility that some accounts of selective feeding in O. marina might result from the noxious effects of prey-associated chemicals rather than active ‘distaste’ by phagotrophic cells is discussed. Recent evidence for toxic superoxide (O₂ ⁻) production by marine microalgae is afforded particular attention given that release of O₂ ⁻ anions can be exacerbated by the binding of mannose-specific lectins to the microalgal cell wall; a novel model for grazing-activated chemical defence is proposed.     

Costs and benefits of interlarval cannibalism in Harmonia axyridis

Cannibalism, which is rather common in ladybirds, has been usually studied at the individual level: benefits of cannibalism for cannibals were estimated. Our study was conducted at the group level: we evaluated the overall effect of interlarval cannibalism on a group of Harmonia axyridis larvae of the fourth instar deprived of food, including both cannibals and their victims. Experiments showed that the probability of pupation in larvae which were kept individually was significantly higher than in larvae kept in groups of five, other conditions being the same. The proportion of samples in which at least one of five individuals pupated among the larvae kept individually was also higher than among those kept in groups suggesting that the eventual benefit of cannibalism was outweighed by the negative impact of aggressive interlarval interactions. The mean and minimum survival time in samples where none of five larvae pupated were longer when larvae were kept individually than when larvae were kept in groups. However, the maximum survival time (the survival time of the last larva in a sample) increased when larvae were kept in groups, which was the only one benefit of cannibalism found in our study. Under natural conditions, the possible adaptive value of this effect is that in the absence of natural prey, longer larval survival time proportionally increases the possibility of finding a new prey patch thereby ensuring survival of the population.     

Functional responses of five cyprinid species to planktonic prey

Synopsis The functional responses of five species of cyprinids (Chalcalburnus chalcoides, Vimba vimba, Abramis brama, Rutilus rutilus, and Scardinius erythrophthalmus) feeding on four planktonic prey types were measured in the laboratory. Although no alternative prey types were present, the response curves were sigmoid in most cases, because attack rates were not independent of prey density. The findings are explained as being the overt expression of the fishes& foraging tactics. The chief way of maximizing food uptake, according to our interpretation, is accelerating attack rates with increasing prey density. The ability of prey to escape or relative prey size may interfere with this strategy. C. chalcoides, the only obligatory planktivore among the species studied, attacks at higher rates and responds most markedly to changes in prey density.     

Cannibalistic Behavior and Functional Response in Chrysomya albiceps (Diptera: Calliphoridae)

Chrysomya albiceps is a facultative predator and cannibal species during the larval stage. Very little is known about cannibalism and prey size preference, especially in blowflies. The purpose of this investigation was to determine the influence of prey size and larval density on cannibalism by third-instar larvae of C. albiceps under laboratory conditions. Our results indicate that no cannibalism occurs by third-instar larvae on first- and second-instar larvae, but third-instar larvae do eat second-instar larvae. The functional response on second-instar larvae is consistent with Holling type II. The consequences of consuming second-, compared to first- or third-, instar larvae as well as the implications of cannibalism for the population dynamics of C. albiceps are discussed.     

Cannibalism as an evolutionary strategy

Mathematical models of predator-prey systems in which the prey species has a three-stage life cycle are studied. Certain stages of the prey life history are allowed to use younger stages as food. It is shown that sufficiently restricted cannibalism can result in an increase in the numbers of adult prey on a sustained basis when cannibalism decreases the vulnerability of a stage subject to predation or increases overall productivity.