Context-dependent crypsis: a prey’s perspective of a color polymorphic predator

Many animals use body coloration as a strategy to communicate with conspecifics, prey, and predators. Color is a trade-off for some species, since they should be visible to conspecifics but cryptic to predators and prey. Some flower-dwelling predators, such as crab spiders, are capable of choosing the color of flowers where they ambush flower visitors and pollinators. In order to avoid being captured, visitors evaluate flowers visually before landing. The crab spider Mecaphesa dubia is a polymorphic species (white/purple color morphs), which inhabits the flower heads of a dune plant, Palafoxia lindenii. Using full-spectrum photography of spiders and flowers, we evaluated how honeybees perceived the spiders at different distances. Using visual modeling, we obtained the chromatic and achromatic contrasts of the spiders on flower heads as perceived by honeybees. Purple morphs were found mainly on the receptacle area and white morphs were equally likely to be found in the flowers and receptacle. According to theoretical modeling, white morphs were visible to honeybees from a distance of 10 cm in receptacle area but appeared to be cryptic in the flower area. Purple morphs were cryptic on the receptacle and less so when they were on the flowers. Spiders on flower heads are predicted to be more easily detected by honeybees using chromatic contrast. Our study shows that the conspicuousness of flower dwelling spiders to honeybees depends on the color morph, the distance of observation, and the position of spider on the flower head.     

From repulsion to attraction: species- and spatial context-dependent threat sensitive response of the spider mite Tetranychus urticae to predatory mite cues

Prey perceiving predation risk commonly change their behavior to avoid predation. However, antipredator strategies are costly. Therefore, according to the threat-sensitive predator avoidance hypothesis, prey should match the intensity of their antipredator behaviors to the degree of threat, which may depend on the predator species and the spatial context. We assessed threat sensitivity of the two-spotted spider mite, Tetranychus urticae, to the cues of three predatory mites, Phytoseiulus persimilis, Neoseiulus californicus, and Amblyseius andersoni, posing different degrees of risk in two spatial contexts. We first conducted a no-choice test measuring oviposition and activity of T. urticae exposed to chemical traces of predators or traces plus predator eggs. Then, we tested the site preference of T. urticae in choice tests, using artificial cages and leaves. In the no-choice test, T. urticae deposited their first egg later in the presence of cues of P. persimilis than of the other two predators and cue absence, indicating interspecific threat-sensitivity. T. urticae laid also fewer eggs in the presence of cues of P. persimilis and A. andersoni than of N. californicus and cue absence. In the artificial cage test, the spider mites preferred the site with predator traces, whereas in the leaf test, they preferentially resided on leaves without traces. We argue that in a nonplant environment, chemical predator traces do not indicate a risk for T. urticae, and instead, these traces function as indirect habitat cues. The spider mites were attracted to these cues because they associated them with the existence of a nearby host plant.     

Habitat segregation mediates predation by the benthic fish <Emphasis Type="Italic">Cottus gobio</Emphasis> on the exotic amphipod species <Emphasis Type="Italic">Gammarus roeseli</Emphasis>

Predation is often considered as one of the most important biotic factor determining the success of exotic species. The freshwater amphipod Gammarus roeseli has widely colonized Western Europe, where it is frequently found in sympatry with the native species (Gammarus pulex). Previous laboratory experiments revealed that G. roeseli may have an advantage over G. pulex through differential predation by native fish (brown trout). Morphological anti-predator defences (spines) were found responsible for lower rates of predation on the invasive G. roeseli. Here, using both field surveys and laboratory experiments, we tested if a differential of predation exists with other fish predators naturally encountered by gammarids. The main predators present in our field site were nocturnal benthic feeders (mainly bullheads, Cottus gobio). Fish diet analysis showed that, compared to its global availability in the river, G. roeseli was less consumed than G. pulex. In the field, however, G. roeseli was found mainly in the aquatic vegetation whereas G. pulex was found in all habitat types. Laboratory experiments in microcosms revealed that G. roeseli was less prone to predation by C. gobio only when vegetation was present. Depending on the type of predator, the differential of predation could therefore be mediated by antipredator behaviour, and a better usage of refuges, rather than by morphological defences.     

Spatial separation from family in the mobile young of a biparental fish: risks and dynamics of returning home

In species with extended parental care, mobile dependent young are potentially more vulnerable to predators when they stray and become separated from their parents. We would expect that the likelihood of, and latency time for, a separated young to safely return to its ‘family unit’ (i.e. parents and brood mates) to be, respectively, inversely and positively related to the initial distance of separation and potentially mediated by its age or body size. Using the biparental convict cichlid fish (Amatitlania siquia), we tested these predictions by capturing individual young and displacing them at varying distances from their family unit in both the field and laboratory. As expected, displaced fish were less likely, and took longer, to return to their family with increasing separation distance from the family unit. The body length of displaced young mediated these relationships and their antipredator behaviour; larger young refuged more than smaller ones and were also less likely to be eaten by predators. These results suggest that selection should favour strong affiliative behaviour in mobile young animals towards their brood mates and protective parents because straying from the family unit leads to increased exposure to predation and a reduced likelihood of returning home with increasing separation distance.     

Field vole (Microtus agrestis) seasonal spacing behavior: the effect of predation risk by mustelids

There are numerous studies showing that predation risk may change different aspects of the behavior of prey, such as habitat use, activity pattern, and foraging. Prey should exhibit the strongest antipredatory response against their most deadly predator. Small mustelids are considered the most important mammalian predators of voles. Nevertheless, there is no general agreement as to whether strong antipredatory reactions exist in natural free-living populations of voles. Here, we studied the field vole Microtus agrestis spatial reaction to high predation risk from small mustelids in the breeding (August) and nonbreeding (October) seasons under natural conditions. Voles were exposed to a caged weasel (Mustela nivalis) and a stoat (Mustela erminea), as well as to the odors of these predators. The reactions of 30 field voles were monitored with radiotelemetry. The field voles were found to display antipredator reactions that varied with season. In the breeding period, in response to predation risk, voles reduced locomotory activity and daily-range size, whereas in the nonbreeding period they did not. Changes in home range position were similar for control and treatment voles, in both the breeding and nonbreeding periods. The results indicate that mustelid predators modify the spatial behavior of small rodents in natural conditions depending on season. This might be a reflection of differences in state-dependent responses to predation from sexually active or inactive individuals. This suggests that the basic antipredatory reaction of voles under high predation risk from small mustelids limits their locomotory activity.     

Male Enchenopa treehoppers (Hemiptera: Membracidae) vary mate-searching behavior but not signaling behavior in response to spider silk

Finding and attracting mates can impose costs on males in terms of increased encounters with, and attraction of, predators. To decrease the likelihood of predation, males may modify mate-acquisition efforts in two main ways: they may reduce mate-searching efforts or they may reduce mate-attraction efforts. The specific behavior that males change in the presence of predator cues should depend upon the nature of risk imposed by the type of predator present in the environment. For example, sit-and-wait predators impose greater costs to males moving in search of mates. Here, we test whether cues of the presence of a sit-and-wait predator lead to a reduction in mate-searching but not mate-acquisition behavior. We used a member of the Enchenopa binotata complex of treehoppers—a clade of vibrationally communicating insects in which males fly in search of mates and produce mate-attraction signals when they land on plant stems. We tested for changes in mate-searching and signaling behaviors when silk from a web-building spider was present or absent. We found that males delayed flight when spider silk was present but only if they were actively searching for mates. These results suggest that males have been selected to reduce predation risk by adjusting how they move about their environment according to the cues of sit-and-wait predators.     

An estimated 400–800 million tons of prey are annually killed by the global spider community

Spiders have been suspected to be one of the most important groups of natural enemies of insects worldwide. To document the impact of the global spider community as insect predators, we present estimates of the biomass of annually killed insect prey. Our estimates assessed with two different methods suggest that the annual prey kill of the global spider community is in the range of 400–800 million metric tons (fresh weight), with insects and collembolans composing >90% of the captured prey. This equals approximately 1‰ of the global terrestrial net primary production. Spiders associated with forests and grasslands account for >95% of the annual prey kill of the global spider community, whereas spiders in other habitats are rather insignificant contributors over a full year. The spider communities associated with annual crops contribute less than 2% to the global annual prey kill. This, however, can be partly explained by the fact that annual crop fields are “disturbed habitats” with a low buildup of spider biomass and that agrobiont spiders often only kill prey over short time periods in a year. Our estimates are supported by the published results of exclusion experiments, showing that the number of herbivorous/detritivorous insects and collembolans increased significantly after spider removal from experimental plots. The presented estimates of the global annual prey kill and the relative contribution of spider predation in different biomes improve the general understanding of spider ecology and provide a first assessment of the global impact of this very important predator group.     

Multicomponent floral signals elicit selective foraging in bumblebees

Flower constancy, or the tendency of individual pollinators to visit sequentially a single flower type even when other equally rewarding types are available, has important implications for animal-pollinated plants. Yet, the proximal reason for the behaviour still remains poorly understood. Here I show that bumblebees visiting equally rewarding flowers that differ in size and odour are more flower constant and less efficient (visited fewer flowers per minute) than bees visiting flowers that differ in size only and odour only. These results are consistent with the view that flower constancy in pollinators is related to their inability to perceive, process or recall multicomponent floral signals. I discuss these findings in the context of pollinator behavioural mechanisms and the evolution of floral diversity.     

Armoured spiderman: morphological and behavioural adaptations of a specialised araneophagous predator (Araneae: Palpimanidae)

In a predator–prey system where both intervenients come from the same taxon, one can expect a strong selection on behavioural and morphological traits involved in prey capture. For example, in specialised snake-eating snakes, the predator is unaffetced by the venom of the prey. We predicted that similar adaptations should have evolved in spider-eating (araneophagous) spiders. We investigated potential and actual prey of two Palpimanus spiders (P. gibbulus, P. orientalis) to support the prediction that these are araneophagous predators. Specific behavioural adaptations were investigated using a high-speed camera during staged encounters with prey, while morphological adaptations were investigated using electron microscopy. Both Palpimanus species captured a wide assortment of spider species from various guilds but also a few insect species. Analysis of the potential prey suggested that Palpimanus is a retreat-invading predator that actively searches for spiders that hide in a retreat. Behavioural capture adaptations include a slow, stealthy approach to the prey followed by a very fast attack. Morphological capture adaptations include scopulae on forelegs used in grabbing prey body parts, stout forelegs to hold the prey firmly, and an extremely thick cuticle all over the body preventing injury from a counter bite of the prey. Palpimanus overwhelmed prey that was more than 200% larger than itself. In trials with another araneophagous spider, Cyrba algerina (Salticidae), Palpimanus captured C. algerina in more than 90% of cases independent of the size ratio between the spiders. Evidence indicates that both Palpimanus species possesses remarkable adaptations that increase its efficiency in capturing spider prey.     

Prey detection without successful capture affects spider’s orb-web building behaviour

Animals obtain information from past foraging experience to adjust their foraging activity according to their environment. The ability of spiders to obtain information from unsuccessful predation experiences was investigated by examining the effects on web building, a significant foraging investment, of prey detection without successful capture in the orb-web spider Cyclosa octotuberculata. Four treatments were employed: (1) successful capture and feeding: one syrphid fly was allowed to be captured and consumed by the spider on the web; (2) single prey-item detection: a syrphid fly was placed on the web to lure the spider, but was removed before capture; (3) five prey-item detection: above prey-item detection stimulus was given five times; and, (4) control: neither prey nor feeding on the web. While control spiders decreased the total thread length and capture area of their webs, prey-item detection spiders in both conditions increased them, indicating that the spider obtained information from unsuccessful predation experience to adjust their foraging investment. The fed spiders exhibited a significantly greater increase than the prey-detection-only spiders, suggesting that prey detection alone and prey detection with consumption had different informational effects. Total thread length did not differ between single and five prey-item detection spiders, but distance between two adjacent sticky spirals increased only in the former spiders, possibly because five times unsuccessful predations prevented spiders to reduce web stickiness. It suggests that the spider changed web morphology according to the number of prey detection.     

Defensive responses by a social caterpillar are tailored to different predators and change with larval instar and group size

Gregariousness in animals is widely accepted as a behavioral adaptation for protection from predation. However, predation risk and the effectiveness of a prey's defense can be a function of several other factors, including predator species and prey size or age. The objective of this study was to determine if the gregarious habit of Malacosoma disstria caterpillars is advantageous against invertebrate natural enemies, and whether it is through dilution or cooperative defenses. We also examined the effects of larval growth and group size on the rate and success of attacks. Caterpillars of M. disstria responded with predator-specific behaviors, which led to increased survival. Evasive behaviors were used against stinkbugs, while thrashing by fourth instar caterpillars and holding on to the silk mat by second instar caterpillars was most efficient against spider attacks. Collective head flicking and biting by groups of both second and fourth instar caterpillars were observed when attacked by parasitoids. Increased larval size decreased the average number of attacks by spiders but increased the number of attacks by both stinkbugs and parasitoids. However, increased body size decreased the success rate of attacks by all three natural enemies and increased handling time for both predators. Larger group sizes did not influence the number of attacks from predators but increased the number of attacks and the number of successful attacks from parasitoids. In all cases, individual risk was lower in larger groups. Caterpillars showed collective defenses against parasitoids but not against the walking predators. These results show that caterpillars use different tactics against different natural enemies. Overall, these tactics are both more diverse and more effective in fourth instar than in second instar caterpillars, confirming that growth reduces predation risk. We also show that grouping benefits caterpillars through dilution of risk, and, in the case of parasitoids, through group defenses. The decreased tendency to aggregate in the last larval instar may therefore be linked to decreasing predation risk.     

Role of post-dispersal seed and seedling predation in establishment of dandelion (Taraxacum agg.) plants

Dandelion Taraxacum agg. (formerly Taraxacum officinale G.H. Weber ex Wiggers) is a common weed species associated with pastures, grasslands and no-tillage cropping systems throughout its native range in Europe, and more recently introduced into North America, Australasia and elsewhere. Following wind-dispersal from the parent plant, its seeds are subject to predation from a host of invertebrate predators. Similarly, seedling predation may also significantly limit dandelion recruitment. Although such post-dispersal mortality is central to our understanding of dandelion population dynamics and therefore weed control, the precise spatio-temporal role played by different putative seed and seedling predators is poorly understood. Here we studied how seed viability, and seed and seedling predation influenced dandelion recruitment at two contrasting sites in central Europe. The abundance in the field and seed and seedling consumption in the laboratory were determined for the main groups of predators—ground beetles (Coleoptera: Carabiade), terrestrial isopods (Isopoda: Oniscidea) and molluscs (Gastopoda: Pulmonata). At particular sites, seed viability and seedling predation were negatively correlated while the percentage of seeds that succumbed to seed predation was similar. Combined factors accounted for the death of 98% and 87% of exposed seeds. Ground beetles (particularly Amara spp.) and terrestrial isopods (Armadillidium vulgare) were efficient and dominant seed predators, while slugs (Arion lusitanicus) and isopods were important predators of seedlings. While there was no seasonal trend in the intensity of seed predation it decreased towards autumn in parallel with the feeding activity of the declining population of A. lusitanicus. The mortality factors thus varied in their importance, largely between sites and less with the course of the season. Although seed inviability, seed and seedling predation did not stop the recruitment of dandelion seedlings they are crucial factors limiting dandelion populations. Methods of increasing the efficiency of predation of seed as a means of managing weeds are worthy of further study, particularly in areas where dandelion is an invasive species.     

Time management and nectar flow: flower handling and suction feeding in long-proboscid flies (Nemestrinidae: Prosoeca)

A well-developed suction pump in the head represents an important adaptation for nectar-feeding insects, such as Hymenoptera, Lepidoptera and Diptera. This pumping organ creates a pressure gradient along the proboscis, which is responsible for nectar uptake. The extremely elongated proboscis of the genus Prosoeca (Nemestrinidae) evolved as an adaptation to feeding from long, tubular flowers. According to the functional constraint hypothesis, nectar uptake through a disproportionately elongated, straw-like proboscis increases flower handling time and consequently lowers the energy intake rate. Due to the conspicuous length variation of the proboscis of Prosoeca, individuals with longer proboscides are hypothesised to have longer handling times. To test this hypothesis, we used field video analyses of flower-visiting behaviour, detailed examinations of the suction pump morphology and correlations of proboscis length with body length and suction pump dimensions. Using a biomechanical framework described for nectar-feeding Lepidoptera in relation to proboscis length and suction pump musculature, we describe and contrast the system in long-proboscid flies. Flies with longer proboscides spent significantly more time drinking from flowers. In addition, proboscis length and body length showed a positive allometric relationship. Furthermore, adaptations of the suction pump included an allometric relationship between proboscis length and suction pump muscle volume and a combination of two pumping organs. Overall, the study gives detailed insight into the adaptations required for long-proboscid nectar feeding, and comparisons with other nectar-sucking insects allow further considerations of the evolution of the suction pump in insects with sucking mouthparts.     

Pollen foraging: learning a complex motor skill by bumblebees (<Emphasis Type="Italic">Bombus terrestris</Emphasis>)

To investigate how bumblebees (Bombus terrestris) learn the complex motor skills involved in pollen foraging, we observed naïve workers foraging on arrays of nectarless poppy flowers (Papaver rhoeas) in a greenhouse. Foraging skills were quantified by measuring the pollen load collected during each foraging bout and relating this to the number of flowers visited and bout duration on two consecutive days. The pollen standing crop (PSC) in each flower decreased drastically from 0530 to 0900 hours. Therefore, we related foraging performance to the changing levels of pollen available (per flower) and found that collection rate increased over the course of four consecutive foraging bouts (comprising between 277 and 354 individual flower visits), suggesting that learning to forage for pollen represents a substantial time investment for individual foragers. The pollen collection rate and size of pollen loads collected at the start of day 2 were markedly lower than at the end of day 1, suggesting that components of pollen foraging behaviour could be subject to imperfect overnight retention. Our results suggest that learning the necessary motor skills to collect pollen effectively from morphologically simple flowers takes three times as many visits as learning how to handle the most morphologically complex flowers to extract nectar, potentially explaining why bees are more specialised in their choice of pollen flowers.     

The use of heterospecific scent marks by the sweat bee <Emphasis Type="Italic">Halictus aerarius</Emphasis>

To forage effectively amongst flowers, some bee species utilize olfactory cues left by previous visitors in addition to direct assessment of visual cues to identify rewarding flowers. This ability can be more advantageous if the bees can recognize and use scent marks left by heterospecifics, not just marks left by members of their own species. We conducted field experiments to investigate whether the sweat bee Halictus aerarius avoids visiting flowers of trailing water willow Justicia procumbens emptied by other bee species. We found that H. aerarius rejected the flowers visited by both heterospecifics and conspecifics. They also rejected visited flowers artificially replenished with nectar. Our results demonstrate that social bees outside the Apidae can detect marks left on flowers by heterospecifics but that (on this plant species) they are unable to discriminate against flowers by directly detecting nectar volume. H. aerarius exhibited different rejection rates according to the identity of the previous bee species. We suggest that the frequency of rejection responses may depend on the amount of chemical substances left by the previous bee. In general, the use of scent marks left by previous visitors is almost certainly advantageous, enabling foragers to avoid flowers with depleted nectar levels and thereby improving their foraging efficiency.     

The effects of different predator species on antipredator behavior in the Trinidadian guppy, Poecilia reticulata

Different types of predators often elicit different antipredator responses in a common type of prey. Alternatively, some prey species may adopt a general response, which provides limited protection from many different types of predator. The Trinidadian guppy, Poecilia reticulata, is faced with a wide range of different predators throughout its range and is known to display varying levels of antipredator behavior depending on the predator assemblage. Pike cichlids, Crenicichla frenata, are regarded as the primary aquatic guppy predator in streams in the northern mountain range in Trinidad. As such, they are seen to be responsible for many of the differences in morphology, life history traits, and behavior between guppy populations from areas with few predators and those from areas with many pike cichlids. In this study we investigated how guppies responded when faced with different predator species using three common aquatic predators. We exposed shoals of ten guppies to one out of four treatments: no predator (control), pike cichlid, acara cichlid (Aequidens pulcher), and wolf fish (Hoplias malabaricus); and we made behavioral observations on both focal individuals and the shoal as a whole. Guppies showed significantly greater levels of predator inspection and shoaling behavior, foraged less, spent more time in the surface water, and stayed in significantly larger shoals when faced with pike cichlids than in other treatments. We discuss these results in the context of multiple predator effects.     

Predation risk increases dispersal distance in prey

Understanding the ecological factors that affect dispersal distances allows us to predict the consequences of dispersal. Although predator avoidance is an important cause of prey dispersal, its effects on dispersal distance have not been investigated. We used simple experimental setups to test dispersal distances of the ambulatory dispersing spider mite (Tetranychus kanzawai) in the presence or absence of a predator (Neoseiulus womersleyi). In the absence of predators, most spider mites settled in adjacent patches, whereas the majority of those dispersing in the presence of predators passed through adjacent patches and settled in distant ones. This is the first study to experimentally demonstrate that predators induce greater dispersal distance in prey.     

Giant honeybees (Apis dorsata) mob wasps away from the nest by directed visual patterns

The open nesting behaviour of giant honeybees (Apis dorsata) accounts for the evolution of a series of defence strategies to protect the colonies from predation. In particular, the concerted action of shimmering behaviour is known to effectively confuse and repel predators. In shimmering, bees on the nest surface flip their abdomens in a highly coordinated manner to generate Mexican wave-like patterns. The paper documents a further-going capacity of this kind of collective defence: the visual patterns of shimmering waves align regarding their directional characteristics with the projected flight manoeuvres of the wasps when preying in front of the bees’ nest. The honeybees take here advantage of a threefold asymmetry intrinsic to the prey–predator interaction: (a) the visual patterns of shimmering turn faster than the wasps on their flight path, (b) they “follow” the wasps more persistently (up to 100 ms) than the wasps “follow” the shimmering patterns (up to 40 ms) and (c) the shimmering patterns align with the wasps’ flight in all directions at the same strength, whereas the wasps have some preference for horizontal correspondence. The findings give evidence that shimmering honeybees utilize directional alignment to enforce their repelling power against preying wasps. This phenomenon can be identified as predator driving which is generally associated with mobbing behaviour (particularly known in selfish herds of vertebrate species), which is, until now, not reported in insects.     

Post-dispersal weed seed predation by avian and non-avian predators

Seed predation by avian and non-avian predators was quantified in the boundaries and cropped areas of cereal fields by presenting known quantities of seed with and without exclusion cages. Predator encounter-rates with the dishes exceeded 99%. Birds removed on average 6.7% seed from the dishes during the seven-day trials compared to 51% by non-avian predators. A comparison was made of the causal factors responsible for predation of Avena fatua, Chenopodium album and Cirsium arvense seeds. A. fatua seeds were preyed most heavily by both avian and non-avian predators. Seed removal by birds was greater in the cropped area than in the field boundary, non-avian predators being generally more active in the field boundary. Seed predation by birds was greater in spring than in any other season, whilst losses to other animals were greater during autumn and winter. Although, birds were not the main seed predators in cereal fields, they may contribute to weed seed depletion, of relevance to reduced-input farming systems where herbicides use is restricted.     

Wind speed affects prey-catching behaviour in an orb web spider

Wind has previously been shown to influence the location and orientation of spider web sites and also the geometry and material composition of constructed orb webs. We now show that wind also influences components of prey-catching behaviour within the web. A small wind tunnel was used to generate different wind speeds. Araneus diadematus ran more slowly towards entangled Drosophila melanogaster in windy conditions, which took less time to escape the web. This indicates a lower capture probability and a diminished overall predation efficiency for spiders at higher wind speeds. We conclude that spiders’ behaviour of taking down their webs as wind speed increases may therefore not be a response only to possible web damage.