Knowing the Risk: Crickets Distinguish between Spider Predators of Different Size and Commonness

Predators unintentionally release chemical and other cues into their environment that can be used by prey to assess predator presence. Prey organisms can therefore perform specific antipredator behavior to reduce predation risk, which can strongly shape the outcome of trophic interactions. In contrast to aquatic systems, studies on cue‐driven antipredator behavior in terrestrial arthropods cover only few species to date. Here, we investigated occurrence and strength of antipredator behavior of the wood cricket Nemobius sylvestris toward cues of 14 syntopic spider species that are potential predators of wood crickets. We used two different behavioral arena experiments to investigate the influence of predator cues on wood cricket mobility. We further tested whether changes in wood cricket mobility can be explained by five predator‐specific traits: hunting mode, commonness, diurnal activity, predator–prey body–size ratio, and predator–prey life stage differences. Crickets were singly recorded (1) in separate arenas, either in presence or absence of spider cues, to analyze changes in mobility on filter paper covered with cues compared with normal mobility on filter paper without cues; and (2) in subdivided arenas partly covered with spider cues, where the crickets could choose between cue‐bearing and cue‐less areas to analyze differences in residence time and mobility when crickets are able to avoid cues. Crickets either increased or reduced their mobility in the presence of spider cues. In the experiments with cues and controls in separate arenas, the magnitude of behavioral change increased significantly with increasing predator–prey body size ratio. When crickets could choose between spider cues and control, their mobility was significantly higher in the presence of cues from common spider species than from rare spiders. We therefore conclude that wood crickets distinguish between cues from different predator species and that spiders unintentionally release a species‐specific composition and size‐dependent quantity of cues, which lead to distinct antipredator behavior in wood crickets.     

Responses of an araneophagic assassin bug,Stenolemus bituberus,to spider draglines

Abstract 1. Animals, as they move through their environment, leave traces of their passage that can be informative to others and convey significant advantages to the animal producing them. However, such traces may also reveal presence, location or identity to enemies. 2. We studied an araneophagic (‘spider‐eating’) assassin bug, Stenolemus bituberus (Heteroptera, Reduviidae), testing whether it associated with areas containing chemotactile traces (e.g. draglines, excreta) left behind by nine sympatric spider species. Stenolemus bituberus were presented with a choice between a substrate containing draglines and a clean substrate. Each hour, for a duration of 12 h, we recorded which substrate was occupied. 3. Stenolemus bituberus tended to associate especially with draglines left by spiders from the genus Achaearanea, their most common prey in nature. 4. These results suggest that S. bituberus exploits draglines from these spiders as cues for indicating prey presence. We also found an increasing tendency to associate with draglines from some spider species through the day, which may be related to circadian patterns or slower response times of some individuals.     

Positive indirect effect of aquatic insects on terrestrial prey is not offset by increased predator density

1. Changes in one prey species' density can indirectly affect the abundance of another prey species if a shared predator eats both species. Sometimes, indirect effects occur when prey straddle habitats, including when riparian predator populations grow in response to emergent aquatic insects and increase predation on terrestrial prey. However, predators may largely switch to aquatic insects or become satiated, reducing predation on terrestrial prey. 2. To determine the net indirect effect of aquatic insects on terrestrial arthropods via generalist spider predators, a field experiment was conducted mimicking midge influx and a wolf spider numerical response inside enclosures near an Icelandic lake. Lab mesocosms were also used to assess per capita rates of spider predation u nder differing levels of midge abundance. 3. Midges always decreased sentinel prey predation, but this effect increased with predator density. When midges were absent, predation increased 30% at a high spider density, but predation was equal between spider treatments when midges were present. In situ arthropods showed no effect of midge or spider treatments, although non‐significant abundance patterns were observed congruent with sentinel prey results. 4. In lab mesocosms, prey survivorship increased ≥50% where midges were present and rapidly saturated; the addition of 5, 20, 50, and 100 midges equivalently reduced spider predation, supporting predator distraction rather than satiation as the root cause. 5. The present results demonstrate a strong positive indirect effect of midges and broadly support the concept that predator responses to alternative prey are a major influence on the magnitude and direction of predator‐mediated indirect effects.     

Preference for Chemical Cues Associated with Recent Prey in the Wolf Spider Hogna helluo (Araneae: Lycosidae)

In the wolf spider, Hogna helluo , we tested the response to insect and spider prey chemical cues and whether they show a preference for cues associated with prey consumed most recently. Thirty adult female H. helluo were maintained on a diet of either females of a smaller co-occurring wolf spider ( Pardosa milvina ) or domestic crickets ( Acheta domesticus ). A single P. milvina or cricket nymph was maintained on filter paper for 24 h, after which the papers from both prey sources were simultaneously presented to individual H. helluo from each diet treatment group. H. helluo locomotor behavior on each treatment and initial substrate preference was recorded (n = 15/treatment). H. helluo fed crickets showed significantly longer residence time and decreased mobility on filter paper previously occupied by a cricket; spiders fed P. milvina showed longer residence times and decreased mobility on filter paper previously occupied by P. milvina . H. helluo fed P. milvina exhibited an initial preference for substrates previously occupied by P. milvina but H. helluo fed crickets did not show a corresponding initial preference for crickets. Results suggest that H. helluo can detect distant cues associated with P. milvina but not crickets before contacting the substrate and that H. helluo respond to chemical cues from prey and show a preference for those cues associated with their most recent prey.     

Variation in active and passive resource inputs to experimental pools: mechanisms and possible consequences for food webs

1. Cross‐ecosystem movements of resources, including detritus, nutrients and living prey, can strongly influence food web dynamics in recipient habitats. Variation in resource inputs is thought to be driven by factors external to the recipient habitat (e.g. donor habitat productivity and boundary conditions). However, inputs of or by ‘active’ living resources may be strongly influenced by recipient habitat quality when organisms exhibit behavioural habitat selection when crossing ecosystem boundaries. 2. To examine whether behavioural responses to recipient habitat quality alter the relative inputs of ‘active’ living and ‘passive’ detrital resources to recipient food webs, we manipulated the presence of caged predatory fish and measured biomass, energy and organic content of inputs to outdoor experimental pools of adult aquatic insects, frog eggs, terrestrial plant matter and terrestrial arthropods. 3. Caged fish reduced the biomass, energy and organic matter donated to pools by tree frog eggs by ～70%, but did not alter insect colonisation or passive allochthonous inputs of terrestrial arthropods and plant material. Terrestrial plant matter and adult aquatic insects provided the most energy and organic matter inputs to the pools (40–50%), while terrestrial arthropods provided the least (7%). Inputs of frog egg were relatively small but varied considerably among pools and over time (3%, range = 0–20%). Absolute and proportional amounts varied by input type. 4. Aquatic predators can strongly affect the magnitude of active, but not passive, inputs and that the effect of recipient habitat quality on active inputs is variable. Furthermore, some active inputs (i.e. aquatic insect colonists) can provide similar amounts of energy and organic matter as passive inputs of terrestrial plant matter, which are well known to be important. Because inputs differ in quality and the trophic level they subsidise, proportional changes in input type could have strong effects on recipient food webs. 5. Cross‐ecosystem resource inputs have previously been characterised as donor‐controlled. However, control by the recipient food web could lead to greater feedback between resource flow and consumer dynamics than has been appreciated so far.     

Predicting Predatory Outcomes in the Context of Carryover Effects: Interactions between Juvenile Frogs and Spider Predators

As representatives of organisms with complex life histories, frogs provide an ideal system to study predator‐induced carryover effects: how the risk of predation in one life stage can impact predator–prey interactions in a later stage. Invertebrate predation on frogs has been widely reported, although studies of the behavioral mechanisms underlying their interactions in the terrestrial stage have been lacking. We made detailed observations of interactions between a wolf spider (Tigrosa helluo) and Blanchard's cricket frog (Acris blanchardi) to determine factors that predict capture success and to evaluate potential carryover effects from aquatic predation risk. Juvenile frogs, reared with or without dragonfly predator cues, were placed in an arena with or without spider cues and allowed to interact with a spider. Spiders captured frogs, and an interaction between frog size and activity predicted frog survival. We found no evidence that either aquatic or terrestrial cues altered frog behavior or survival. By preying upon a demographically important life stage, spiders may contribute to population dynamics in frogs.     

Sex‐Specific Response of Pardosa milvina (Araneae: Lycosidae) to Experience with a Chemotactile Predation Cue

Predators frequently leave behind chemical information (i.e., semiochemicals such as pheromones or kairomones) that can be detected by their prey and used to avoid areas where predators are likely present. Prey that have interacted indirectly with predators via chemical information thus may gain insight into their risk of being consumed that naïve individuals lack. Pardosa milvina (Araneae: Lycosidae) is a chemosensitive wolf spider that shows adaptive responses to chemotactile cues deposited by the larger wolf spider Tigrosa helluo. We raised offspring from P. milvina to examine the effect of experience with a predation cue on activity, foraging, and antipredator behavior. Spiders differed in activity and foraging behavior across ontogeny and between sexes, but there was no effect of experience with a predation cue. However, a sex‐specific effect of experience was found in antipredator behavior. Male spiders, but not females, used experience with a predator cue to increase their survival in the presence of a live predator. Specifically, naïve males were attacked sooner than experienced males, indicating that prior exposure to predator cues can modify Pardosa antipredator behavior. Intersexual differences in how spiders respond to experience with a predation cue likely reflect the risk of predation faced by males and females in nature.     

Chemical Mediation of Prey Recognition by Spider-Hunting Wasps

Predator–prey interactions are important in maintaining the structure and dynamics of ecological communities. Both predators and prey use cues from a range of sensory modalities to detect and assess one another; identification of these cues is necessary to understand how selection operates to shape predator–prey interactions. Mud-dauber wasps (Sphecidae) provision their larval nests with paralyzed spiders, and different genera of wasps specialize on particular spider taxa. Sceliphron caementarium (Drury 1773) wasps preferentially capture spiders that build two-dimensional (2D) webs, rather than those that construct three-dimensional (3D) webs, but the basis of this preference is not clear. Wasps may choose spiders based on an assessment of their web architecture, as 3D webs may provide better defenses against wasp predation than do 2D webs. However, because many hymenopterans use chemical cues to locate and recognize prey, it is also possible that mud-dauber wasps rely on chemical cues associated with the spider and/or the web to assess prey suitability. When we offered foraging S. caementarium wasps 2D and 3D spiders both on and off their webs, we found that in both cases the wasps took 2D spiders and avoided 3D spiders, demonstrating that the web itself is not the impediment. Results of a series of behavioral choice assays involving filter paper discs containing spider cues and chemically manipulated spiders or spider dummies corroborated the importance of spider chemical cues in mediation of prey recognition by mud-dauber wasps. We also discuss the relative importance of visual and chemical cues for prey recognition by wasps, examine the anti-predator behaviors of 2D and 3D spiders, and consider the role of wasp predation in spider diversification.     

Sensory Basis of Food Detection in Wild <Emphasis Type="BoldItalic">Microcebus murinus</Emphasis>

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.     

Ecology of Arachnida alien to Europe

The ecology of selected species of spiders (Araneae), harvestmen (Opiliones), and the neglected tropical order Schizomida, alien to Europe, is discussed. Their geographic origins and pathways of introduction, by transportation with goods, are similar to other predatory terrestrial arthropods. Occurrence in buildings (synanthropy) is a prerequisite for range expansion in many arachnid species. Thelytokous parthenogenesis facilitated spread of a few spider, harvestman and schizomid species outside their native range. Both prey generalists and specialists (woodlice-eating Dysdera crocata and ant-eating Zodarion rubidum) are among species successfully expanding their range. Alien arachnids include individual species belonging to many different families. We stress the absence of true invasiveness of alien arachnids in Europe. Some unusual adverse effects of alien arachnids were recorded, such as pollution of buildings and clogged car fuel system ventilation tubes. Frequency of painful biting and threat to native biota are low.     

Cooperative foraging in neotropical pseudoscorpions: effects of prey changes on behavioral adjustments of colonies

The pseudoscorpion Paratemnoides nidificator is a generalist predator that captures large arthropods that live on tree trunks. Few pseudoscorpions species show some degree of sociality. We investigated how colonies of the pseudoscorpion P. nidificator adjust their cooperative capture behavior under a situation of changing prey types as a simulation of variation in prey availability. We hypothesized that colonies would be more efficient at prey capture under repeated exposure to the same prey, and that the change in the availability of prey would be followed by new behavioral adjustments to adequately exploit the new prey. Eight experimental colonies housed in the laboratory received repetitions of three different ant species as prey. The number of pseudoscorpions attacking the prey, the number of behavioral acts, and the time expended subduing prey were evaluated as measures of prey capture performance, in relation to repetitive exposure to the same prey and also in relation to prey type changes. However, only individuals’ recruitment significantly responded to prey type exposure. Prey capture behavior was heterogeneous among colonies, resulting in highly variable behavioral responses. Colonies showed a tendency toward increasing capture success through repeated prey type exposure. However, 50% of the colonies were unable to capture the new prey type and died of starvation. Although it is a generalist predator, prey capture behavior could depend on different coordination components for subduing and handling large prey. Therefore, changes in prey availability could cause the attenuation of a cooperative relationship in some colonies, making them more prone to failure during capture.     

Tradeoffs involved in site selection and foraging in a wolf spider: effects of substrate structure and predation risk

Understanding how animals weigh habitat features, exposure to predators and access to resources is important to determining their life history and distribution across the landscape. For example, when predators accumulate in structurally complex habitats, they face an environment with different competitive interactions, foraging opportunities and predatory risks. The wolf spider Pardosa milvina inhabits the soil surface of highly disturbed habitats such as agricultural fields throughout eastern North America. Pardosa displays effective antipredator behavior in the presence of chemical cues produced by a larger coexisting wolf spider, Hogna helluo . We used those cues to simulate predation risk in laboratory and field experiments designed to test the effects of habitat substrate and predation risk on site selection and prey consumption of Pardosa . In general, Pardosa preferred more complex substrates over bare dirt but those preferences were eliminated or reversed when cues from Hogna were present. Feeding trials revealed that substrate alone had few effects on Pardosa prey consumption, which we measured by documenting the change in the abdomen width. Although the presence of Hogna cues reduced prey consumption overall in field feeding trials, the negative effect of predation risk on prey consumption was only observed in grass and bare dirt substrates in the laboratory. We also found that prey capture was negatively affected by habitat complexity for both spider species but that same complexity offered Pardosa protection from predation by Hogna. This study provides insight into how two predator species interact to balance site selection and feeding in order to avoid predation. Shifts in foraging and distributional patterns of predators can have profound implications for their role in the food web.     

Temperature dependency of predation: Increased killing rates and prey mass consumption by predators with warming

Temperature dependency of consumer–resource interactions is fundamentally important for understanding and predicting the responses of food webs to climate change. Previous studies have shown temperature‐driven shifts in herbivore consumption rates and resource preference, but these effects remain poorly understood for predatory arthropods. Here, we investigate how predator killing rates, prey mass consumption, and macronutrient intake respond to increased temperatures using a laboratory and a field reciprocal transplant experiment. Ectothermic predators, wolf spiders (Pardosa sp.), in the lab experiment, were exposed to increased temperatures and different prey macronutrient content (high lipid/low protein and low lipid/high protein) to assess changes in their killing rates and nutritional demands. Additionally, we investigate prey mass and lipid consumption by spiders under contrasting temperatures, along an elevation gradient. We used a field reciprocal transplant experiment between low (420 masl; 26°C) and high (2,100 masl; 15°C) elevations in the Ecuadorian Andes, using wild populations of two common orb‐weaver spider species (Leucauge sp. and Cyclosa sp.) present along the elevation gradient. We found that killing rates of wolf spiders increased with warmer temperatures but were not significantly affected by prey macronutrient content, although spiders consumed significantly more lipids from lipid‐rich prey. The field reciprocal transplant experiment showed no consistent predator responses to changes in temperature along the elevational gradient. Transplanting Cyclosa sp. spiders to low‐ or high‐elevation sites did not affect their prey mass or lipid consumption rate, whereas Leucauge sp. individuals increased prey mass consumption when transplanted from the high to the low warm elevation. Our findings show that increases in temperature intensify predator killing rates, prey consumption, and lipid intake, but the responses to temperature vary between species, which may be a result of species‐specific differences in their hunting behavior and sensitivity to temperature.     

Can species‐specific prey responses to chemical cues explain prey susceptibility to predation?

The perception of danger represents an essential ability of prey for gaining an informational advantage over their natural enemies. Especially in complex environments or at night, animals strongly rely on chemoreception to avoid predators. The ability to recognize danger by chemical cues and subsequent adaptive responses to predation threats should generally increase prey survival. Recent findings suggest that European catfish (Silurus glanis) introduction induce changes in fish community and we tested whether the direction of change can be attributed to differences in chemical cue perception. We tested behavioral response to chemical cues using three species of freshwater fish common in European water: rudd (Scardinius erythrophthalmus), roach (Rutilus rutilus), and perch (Perca fluviatilis). Further, we conducted a prey selectivity experiment to evaluate the prey preferences of the European catfish. Roach exhibited the strongest reaction to chemical cues, rudd decreased use of refuge and perch did not alter any behavior in the experiment. These findings suggest that chemical cue perception might be behind community data change and we encourage collecting more community data of tested prey species before and after European catfish introduction to test the hypothesis. We conclude that used prey species can be used as a model species to verify whether chemical cue perception enhances prey survival.     

Effects of Predation Risk on Vertical Habitat Use and Foraging of Pardosa milvina

Animals face the risk of predation while engaging in regular activities, such as foraging, mate‐seeking, and reproducing. In order to avoid predation, prey can modify behavior to prevent capture. Pardosa milvina may climb in response to chemotactile cues of Hogna helluo, a larger cooccurring wolf spider, to avoid predation. The purpose of this study was to test the effects of the location of predator cues on the climbing response of P. milvina and to test how this antipredator behavior affected foraging success. In experimental arenas, when cues were on the bottom of the containers, P. milvina moved upward, and when cues were on the walls, individuals moved downward. These results suggest that P. milvina respond to H. helluo cues with general avoidance and do not automatically climb in response to the cues. As H. helluo spend most of their time on the ground, P. milvina may avoid predation by spending more time climbing in areas with H. helluo cues. The presence of predator cues significantly decreased foraging by P. milvina. But within the predator cue treatments, climbing ability had no effect on foraging, possibly due to the short height of the feeding arenas. Future studies are needed to determine if climbing by P. milvina in response to cues of H. helluo has direct and indirect negative effects on herbivores in the field.     

The non-consumptive effects of predators and personality on prey growth and mortality

Individual organisms vary in personality, and the ecological consequences of that variation can affect the strength of predator–prey interactions. Prey with bolder tendencies can mitigate the strength of species interactions by altering growth and initiating ontogenetic niche shifts (ONS). While the link between personality and growth has been established, recent research has highlighted the important interplay between ONS and predator cues in community ecology. The objective of this study was to evaluate the effects of prey personality and predator cues on prey growth and ONS. We predicted growth–mortality trade-offs among personalities with higher survival, larger size, and accelerated ONS for bold individuals in comparison with shy individuals. To evaluate this objective, we conducted behavioral assays and a mesocosm experiment to test how southern leopard frog (Rana sphenocephala) tadpole personality and predatory fish (bluegill, Lepomis macrochirus) cues affects tadpole growth and metamorphosis. On average, bold tadpoles had higher mortality across all treatments in comparison with shy tadpoles. The effects of fish cues were dependent on tadpole personality with shy tadpoles metamorphosing significantly later than bold tadpoles. Bold tadpoles were larger than shy tadpoles at metamorphosis; however, that pattern reversed with fish cues as shy individuals metamorphosed larger than bold individuals. Our results suggest personality may be useful for predicting growth and life history for some prey species with predators. Specifically, the threat of predation can interact with personality to incur a benefit (earlier ONS) while also incurring a cost (size at metamorphosis). Hence by incorporating predator cues with personality, ecologists will be able to elucidate growth–mortality trade-offs mediated by personality.     

Prenatal Chemosensory Learning by the Predatory Mite Neoseiulus californicus

Background

Prenatal or embryonic learning, behavioral change following experience made prior to birth, may have significant consequences for postnatal foraging behavior in a wide variety of animals, including mammals, birds, fish, amphibians, and molluscs. However, prenatal learning has not been previously shown in arthropods such as insects, spiders and mites.

Methodology/Principal Findings

We examined prenatal chemosensory learning in the plant-inhabiting predatory mite Neoseiulus californicus. We exposed these predators in the embryonic stage to two flavors (vanillin or anisaldehyde) or no flavor (neutral) by feeding their mothers on spider mite prey enriched with these flavors or not enriched with any flavor (neutral). After the predators reached the protonymphal stage, we assessed their prey choice through residence and feeding preferences in experiments, in which they were offered spider mites matching the maternal diet (neutral, vanillin or anisaldehyde spider mites) and non-matching spider mites. Predator protonymphs preferentially resided in the vicinity of spider mites matching the maternal diet irrespective of the type of maternal diet and choice situation. Across treatments, the protonymphs preferentially fed on spider mites matching the maternal diet. Prey and predator sizes did not differ among neutral, vanillin and anisaldehyde treatments, excluding the hypothesis that size-assortative predation influenced the outcome of the experiments.

Conclusions/Significance

Our study reports the first example of prenatal learning in arthropods.     

The role of prey availability in aggregative behaviour of the orb weaving spider Tetragnatha elongata

Like many spider species, Tetragnatha elongata exhibits considerable flexibility in its spacing pattern as a response to variable levels of prey abundance. This study examines the extent and form of spider aggregation at high prey density. In experiments in which their respective densities were manipulated, when spider density was high, excess prey allowed individuals (1) a significant reduction in web building, and (2) indiscriminate use of pre-laid silk. These effects were not observed at low spider density. These results are discussed in the context of ‘risk-sensitive’ foraging theory, which shows how this type of behaviour in an aggregation might be adopted as a means for reducing resource variance. Such an approach indicates a possible means through which sociality might be initiated.     

Opportunistic foraging strategy of rainbow lizards at a seaside resort in Togo

Rainbow lizards (Agama agama) are common in suburban areas throughout Africa, and have an opportunistic foraging strategy, with arthropods being the main prey source. In a coastal resort in southern Togo, West Africa, several individuals in a population were observed while feeding regularly upon non-natural human-made food (pizza) and showing a clear preference for a given type of food versus others that were offered (‘four cheeses’ being the preferred one). The fact that all monitored individuals fed upon a same type of pizza suggests that they may have some chemical cues attracting them.     

Synchronized and rhythmical activity during the prey capture in the social spiderAnelosimus eximius (Araneae,Theridiidae)

Summary Anelosimus eximius is a social spider species of South America. Many individuals share the same web and participate in prey capture, taking some ten seconds to locate the prey in the silky structures. In the laboratory, we analyzed the movements of each spider which took part in the pursuit, and showed that they were both synchronized and rhythmical. Spiders alternate simultaneous periods of immobility (involving 100% of the attacking individuals) and activity (involving at least 70% of the spiders).The results are discussed with reference to the model developed by Goss and Deneubourg (1988) suggesting that autocatalysis may be the motor of certain synchronized and rhythmical activities in social arthropods.