Trap-building Predators Research Articles

Convergent evolution of antlions and wormlions: similarities and differences in the behavioural ecology of unrelated trap-building predators

Convergent evolution of antlions and wormlions: similarities and differences in the behavioural ecology of unrelated trap-building predators

Efficiency of antlion trap design and larval behavior in capture success

Abstract Traps constructed by an animal reduce the amount of energy required to seek prey. The main risk of trap-building predators is the greater uncertainty of encountering prey, owing to their immobility. Sometimes environmental characteristics do not allow them to build efficient traps, resulting in lower capture success. We observed prey escape, capture success, and behavior of two antlion species, Cueta lineosa, a habitat specialist, and Myrmeleon hyalinus, a generalist, building geometrically different traps. The traps of C. lineosa are elaborate and deep, consisting of two inverted cones, while M. hyalinus builds simple inverted cones. Prey escape was observed from traps with antlion larvae present and from artificially constructed traps without antlions. We used a 3D printer to create a replica model of both trap types, pressing the model onto the substrate surface to create a trap. The C. lineosa artificial trap slowed prey escape more effectively than the simpler artificial trap of M. hyalinus. Prey escape time was four times longer for two ant species and three times longer for woodlice from C. lineosa traps. Escape time also decreased with increasing prey length. We also found behavioral differences between these two antlion species. The behavior of M. hyalinus is much more efficient in catching prey than that of C. lineosa. The results indicate that both species are efficient trap-building predators; however, it appears that capture success depends not only on trap design but also on larval behavior.

Evidence for competition and cannibalism in wormlions

Trap-building predators, such as web-building spiders and pit-building antlions, construct traps to capture their prey. These predators compete over sites that either enable the construction of suitable traps, are prey rich, or simply satisfy their abiotic requirements. We examined the effect of intraspecific competition over suitable space in pit-building wormlions. As expected, the ability of wormlions to select their favorable microhabitats—shaded or deep sand over lit or shallow sand—decreased with increasing density. Favorable microhabitats were populated more frequently by large than by small individuals and the density of individuals in the favorable microhabitat decreased with their increase in body mass. The advantage of large individuals in populating favorable microhabitats is nevertheless not absolute: both size categories constructed smaller pits when competing over a limited space compared to those constructed in isolation. The outcome of competition also depends on the type of habitat: deep sand is more important for large wormlions than small ones, while shade is similarly important for both size classes. Finally, in contrast to previous reports, cannibalism is shown here to be possible in wormlions. Its prevalence however is much lower compared to that documented in other trap-building predators. Our findings show that the advantage of large individuals over small ones should not be taken for granted, as it can depend on the environmental context. We present suggestions for the relative lack of competitive advantage of large wormlion individuals compared to other trap-building predators, which may stem from the absence of obvious weaponry, such as sharp mandibles.

Plasticity in extended phenotypes: how the antlion Myrmeleon crudelis adjusts the pit traps depending on biotic and abiotic conditions

Abstract The physical structures built by animals are considered extended phenotypes that reflect how organisms make decisions and deal with changes in their biotic and abiotic environment. We summarize the results of several studies on Myrmeleon crudelis, a neuropteran larva that digs pit-traps in the soil to capture small arthropods (mostly ants) in the tropical dry forests of Costa Rica. Specifically, we showed how this species responds to varying biotic and abiotic conditions with changes in the design and/or location of its pit traps. Several experiments and field comparisons indicate that: 1) antlions adjust the pit design according to the abundance and type of prey. When prey is scarce, antlions increased trap diameter, an architectural adjustment that enhances the probability of prey encounter. Antlions that experienced high prey abundance, but the prey easily escaped, then increased pit depth, an adjustment that increases the chance of prey retention; 2) soil compaction strongly reduced pit-trap size and abundance; 3) antlions preferred soils with high proportion of fine-particle size to build pits. In fine-grained soil, pit-traps are larger and more efficient to capture prey than traps in coarse-grained soils; and 4) pit-traps may also be affected through indirect effects of soil structure and vegetation cover. Areas with fine-soil presented less plant cover, and plant cover could be beneficial for antlions because it acts as a shelter against direct sunlight and rainfall, or it may represent a cost because it is a source of leaflitter falling in the pits. The works summarized here how trap-building predators can exhibit considerable flexibility in trap construction in response to various biotic and abiotic factors, emphasizing how the study of extended phenotypes can be a useful approach to better understand the flexibility of foraging behaviors.

Sit-and-wait prey: first field observations of scorpions preying on antlions (Neuroptera)

Abstract Antlions (Neuroptera) are a group of sit-and-wait predator insects, with some species further specializing in digging conical pit-traps in the ground in order to catch prey. Studies on antlions’ predators are scarce with only few generalist predators known to feed on them. Here we report for the first time on field observations of antlions’ predation by three scorpion genera. We suggest that scorpions may be common predators of antlions, at least in the hyper-desert environment of southern Israel. The effects of predation risk on the behavior of sit-and-wait and particularly on trap-building predators received little attention in the literature. In light of our observations, we posit that predation risk must be taken into serious consideration in future research of antlions in particular, and sit-and-wait predators in general.

The dynamics of prey selection by the trap-building predatorGasteracantha hasselti

AbstractPrey selection by generalist predators can be highly dynamic depending on the prey community structure. However, the dynamics of prey selection at the stage of prey entrapping are rarely investigated in trap-building predators, probably because their traps have been previously considered to intercept mobile prey proportionally to its availability in environment. Here we investigated the dynamics of prey selection by the orb-weaving spiderGasteracantha hasselti(Araneidae) depending on the composition of the available prey in tropical lowland forests located in north-eastern Thailand. We found thatGasteracanthacaptured a wide variety of prey but selected, on average, mostly Coleoptera and Diptera. The selectivity ofGasteracantha’s webs for Coleoptera was constant across the changes in overall prey availability and prey composition. The web selectivity for Hemiptera decreased rapidly with increasing relative densities of Hemiptera in the environment. The selectivity for Diptera and Hymenoptera increased and decreased, respectively, with their absolute densities in the environment. The relative selectivity ofGasteracantha’s traps for a particular prey type was driven by the presence and density of the highly selected prey rather than overall prey density. The results show that the selectivity ofGasteracantha’s traps for prey had both fixed and dynamic components and the dynamic component was determined by the relative as well as absolute densities of the particular prey types in the environment.

Wormlions prefer both fine and deep sand but only deep sand leads to better performance.

Wormlions are small fly larvae that dig pits in loose soil to trap their prey. Similar to other trap-building predators, like spiders and antlions, they depend on the habitat structure for successful trap construction and prey catch. We examined whether sites at which wormlions are present differ in sand depth and particle size from nearby sites, at which wormlions are absent. Next, in the laboratory we manipulated both sand depth and type (fine vs. coarse) to determine their joint effect on microhabitat preference, the size of the constructed pit, wormlion movement, and their latency to respond to prey. We expected better performance by wormlions in fine and deep sand, and the sand in wormlions’ natural sites to be finer and deeper. However, in only partial agreement with our expectations, wormlion sites featured finer sand but not deeper sand. In the laboratory, wormlions preferred both fine and deep sand, and moved more in shallow and coarse sand, which we interpret as an attempt to relocate away from unfavorable conditions. However, only deep sand led to larger pits being constructed and to a faster response to prey. The preference for fine sand could, therefore, be related to other benefits that sand provides. Finally, body mass was a dominant factor, interacting with the preference for both deep and fine sand: deep over shallow sand was more favored by large wormlions and fine over coarse sand by smaller ones. Our results suggest that several factors should be incorporated when studying microhabitat selection.

The contribution of shelter from rain to the success of pit-building predators in urban habitats

Trap-building predators are sit-and-wait predators that construct a trap and wait for other arthropods to be captured in their trap. The abiotic features of their microhabitat play a significant role in their foraging success, and trap relocation can be costly and risky. Wormlions are fly larvae that construct pits in loose soil to catch prey that fall into their pit-traps and serve as a fine example of a trap-building predator. Wormlions flourish in cities and often occur under buildings that provide shelter from direct sunlight and rain. Here, we studied in the laboratory and in the field the effect of simulated rain and soil moisture on wormlion (Vermileo sp.) habitat choice, response to prey and prey escape success. Wet soil had a strong negative effect on the wormlion pit size and its response to prey, and a positive effect on the probability of ant prey escaping the pit-trap. All these limitations led to a strong avoidance by wormlions of wet soil both before and after a pit was constructed, even at the cost of pit relocation. A field experiment comparing wet and dry plots nevertheless failed to show the expected directional relocation from wet to dry plots, and we provide several explanations as to why the patterns detected in the laboratory were less clear in the field. We suggest that rain presents a considerable limiting factor for wormlion hunting success, and that rain-shielding artificial structures could be responsible for the success of these predators in urban environments. It remains to be tested whether our results hold true for other trap-building predators and whether their preference for dry habitats is as strong as that of wormlions.

The complex effect of illumination, temperature, and thermal acclimation on habitat choice and foraging behavior of a pit-building wormlion

Habitat selection has consequences for an animal’s fitness, especially for sit-and-wait predators with limited mobility, and which cannot always correct earlier suboptimal choices. Environmental change may nevertheless lead individuals to relocate to another site, although such relocations can be energetically costly or risky. Temperature and illumination are two important factors that undergo change in seasonal and daily cycles that may impact habitat quality. Animals must therefore either acclimate to the new conditions or relocate. Wormlions are sit-and-wait, trap-building predators whose success in foraging is highly dependent on their surroundings. Here, we manipulated temperature (high, low, and moderate) and let the wormlions choose between lit and shaded conditions. We found that the typical wormlion preference for shaded microhabitats decreased with increasing temperature. We then followed wormlion behavior under a full-factorial design of two constant illumination conditions (light vs. shade) and three temperatures. Although both constant light and high temperature reduced foraging performance, expressed in pit construction tendency and pit area, the two conditions had a non-additive effect. Acclimation to extreme thermal conditions moderated the negative effects of such temperatures, expressed in a higher tendency to construct a pit, and equalized performance across temperatures. Finally, the high temperature reduced behavioral consistency while acclimation increased it, suggesting that consistency is impaired by unfavorable environmental change. To conclude, while an environmental change usually affects several environmental factors simultaneously, the induced behavioral change is neither synergic nor additive and can even differ from the response to each unfavorable environmental factor in isolation. Choosing a suitable habitat is essential for survival and reproduction, especially for sedentary organisms, and requires the consideration of various environmental conditions. Acclimating to suboptimal conditions, however, might conduce to improving performance in a less suitable habitat. Testing the effect of several environmental conditions on habitat choice and foraging behavior, before and after acclimation, has rarely been carried out. Here, we tested the combined effects of temperature, illumination, and their interaction, on habitat choice and foraging performance of a sit-and-wait predator, the wormlion. Wormlions usually prefer shade, but their preference for light increases with decreasing temperature. Both temperature and illumination affect behavior but their joint effect is not additive. Acclimation, which took place for temperature but not for illumination, improved certain foraging behaviors. Our findings highlight the importance of evaluating several environmental conditions and behaviors when studying habitat choice and foraging behavior.

Group dynamics and relocation decisions of a trap-building predator are differentially affected by biotic and abiotic factors.

Most habitats in nature are heterogeneous, incorporating favorable and unfavorable microhabitats for different animals, based on their ecological niche. Unsuitable microhabitats have negative consequences for individual growth and survival. Animals, therefore, should fine-tune their location within the habitat by dispersing away from such microhabitats. We studied the suitability of different constant microhabitat conditions for wormlion larvae, a trap-building predator, tested in groups under laboratory conditions. Wormlions construct pit-traps in loose soil and capture small arthropod prey. As wormlions occur in high densities in nature, testing in groups is thus more indicative of their natural behavior than testing individuals. Wormlions responded strongly to biotic conditions—high conspecific density, starvation, and large body mass of conspecifics—by either increasing pit-relocation events or moving away from the microhabitat center to the periphery of the arena, probably opting for a way out. In other instances, individuals increased their distance to the nearest neighbor, thereby changing the spatial pattern toward a more regular pattern, potentially indicating interference competition. The only abiotic condition apparently perceived by wormlions as unsuitable was shallow sand, which led to frequent relocations. The two other abiotic factors—illumination and sand particle size—had no observable effect on behavior, although wormlions in nature always occur under shade in fine sand, and prefer both shade and fine sand particle size under laboratory conditions when given a choice. Under the fine spatial scale of the present experiment, biotic factors appear to be more influential than abiotic ones.

The effect of previous experience on trap construction and movement distance in a pit-building predator

Wormlion larvae are sit-and-wait predators that construct cone-shaped pits in sandy patches to capture prey. Wormlions select microhabitats that feature favorable conditions for pit construction, in a similar way to other trap-building predators, like spiders and antlions. We investigated whether wormlions exhibit an experience-based behavioral plasticity in their pit construction behavior. In a laboratory experiment, pit sizes and relocation distances were compared between larvae that experienced either a period of unfavorable conditions, i.e., surface obstacles, shallow or coarse sand, or a period of favorable conditions, i.e., clear, deep, and fine sand and were able to construct pits undisturbed. We expected that wormlions experiencing improving conditions would build larger pits than those experiencing deteriorating conditions. In addition, we expected that larvae experiencing unfavorable conditions would be less choosy in their new microhabitat and move over shorter distances. We observed a certain effect of recent experience on the trap-building behavior; however, it was not consistent among treatments. Additionally, we detected a correlation between larval body mass, relocation distance, and pit area. These findings might suggest that past experience does not influence wormlion foraging behavior in a simple manner but that different types of experience induce different behavioral responses.

Spider web and silk performance landscapes across nutrient space.

Predators have been shown to alter their foraging as a regulatory response to recent feeding history, but it remains unknown whether trap building predators modulate their traps similarly as a regulatory strategy. Here we fed the orb web spider Nephila pilipes either live crickets, dead crickets with webs stimulated by flies, or dead crickets without web stimulation, over 21 days to enforce spiders to differentially extract nutrients from a single prey source. In addition to the nutrients extracted we measured web architectures, silk tensile properties, silk amino acid compositions, and web tension after each feeding round. We then plotted web and silk “performance landscapes” across nutrient space. The landscapes had multiple peaks and troughs for each web and silk performance parameter. The findings suggest that N. pilipes plastically adjusts the chemical and physical properties of their web and silk in accordance with its nutritional history. Our study expands the application of the geometric framework foraging model to include a type of predatory trap. Whether it can be applied to other predatory traps requires further testing.

Habitat choice and complex decision making in a trap-building predator

The selection of a suitable habitat may maximize the survival and reproduction chances of individuals. We examined the habitat choice of wormlions, small sand-dwelling insects that construct pit-traps to capture prey. Unlike the well-studied antlions, which employ a similar hunting strategy, wormlion behavior has not been thoroughly studied. We first determined whether wormlions prefer 1) shaded versus lit, 2) deep versus shallow sand, and 3) surface-obstructed versus clear microhabitats. The first option of each of the three pairs was highly preferred. In unfavorable microhabitats, larvae were also less likely to construct a pit, mainly in shallow sand, and moved over longer distances. Next, we sought to determine whether the choice is additive (taking more than a single factor into account), hierarchical (ranking the factors according to an order of preference), or based on a threshold rule (accepting a microhabitat that crosses a quality threshold). Combining shade with one of 3 environmental factors – surface obstacles, shallow sand, or high conspecific density – led to lower proportions of wormlions choosing shade. In other words, a combination of shade and any factor was no longer preferred over lit and otherwise favorable microhabitats. We thus conclude that the wormlions’ microhabitat choice is additive, taking more than a single factor into account, and that favorable conditions of any sort are traded-off against one another.

Optimal range of prey size for antlions

1. Antlions are opportunistic trap building predators that cannot control prey encounter. Their trap should ideally retain a great diversity of prey. However, building a single trap that captures many prey with varying characteristics can be challenging.2. A series of five different ant species ranging from thin to large, of sizes ranging from 2.75 to 6.5 mm, and a mean weight ranging from 0.54 to 6.00 mg were offered in a random succession to antlions. The state of satiation of the antlions was controlled, and their mass and the depth of their pit were recorded. The reaction of antlion to the prey, the probability of capture as well as the time to escape were recorded.3. The probability of an antlion reaction is an increasing function of the pit depth and a decreasing function of antlion mass. The probability of capture is highest for intermediate prey mass and is an increasing function of pit depth. The time to escape is a declining function of prey mass and an increasing function of pit depth.4. There is an upper limit to prey mass given that large prey escape out of the pit. There is a lower limit to prey mass given the difficulty to apprehend the smallest, thin species. Consequently, there is a range of prey mass, corresponding to a medium‐sized ant of 2 mg, for which the pit functions best. The physics of insect locomotion on sandy slopes was identified as the key to understanding the functioning of antlion pits.

Can differential nutrient extraction explain property variations in a predatory trap?

Predators exhibit flexible foraging to facilitate taking prey that offer important nutrients. Because trap-building predators have limited control over the prey they encounter, differential nutrient extraction and trap architectural flexibility may be used as a means of prey selection. Here, we tested whether differential nutrient extraction induces flexibility in architecture and stickiness of a spider's web by feeding Nephila pilipes live crickets (CC), live flies (FF), dead crickets with the web stimulated by flies (CD) or dead flies with the web stimulated by crickets (FD). Spiders in the CD group consumed less protein per mass of lipid or carbohydrate, and spiders in the FF group consumed less carbohydrates per mass of protein. Spiders from the CD group built stickier webs that used less silk, whereas spiders in the FF group built webs with more radii, greater catching areas and more silk, compared with other treatments. Our results suggest that differential nutrient extraction is a likely explanation for prey-induced spider web architecture and stickiness variations.

Foraging behaviour of a neglected pit-building predator: the wormlion

Wormlion larvae (Diptera: Vermileonidae) construct conical pits in fine loose soils and ambush arthropod prey. Their hunting strategy resembles that of pit-building antlions (Neuroptera: Myrmeleontidae), offering a classical example of convergent evolution, as they belong to different orders of insects. However, compared with other trap-building predators, spiders and antlions, the foraging behaviour of wormlions is almost unknown. In this study we used a combination of field observations and laboratory experiments to close this gap and investigate how hunger and ecological factors such as density and spatial pattern affect pit size, that is, how they shape investment in foraging and indicate competition between neighbouring larvae. We found slight, mainly decreasing, changes in pit size with hunger, with no change in response to prey. Surprisingly, body mass and length were not tightly correlated with pit size, unlike in antlions and spiders. Other factors, in addition to body mass and size, affect pit size, as the correlation between pits constructed in the field and in the laboratory was strong. The evidence for competition was mixed. On the one hand, we detected, in the laboratory, a change towards a regular spatial pattern with increasing pit densities, as expected, suggesting interference competition. On the other hand, we detected, in the field, a positive correlation between the sizes of neighbouring pits, and a negative correlation in the laboratory between pit size and distance to the nearest neighbour, both indicating clustering in favourable microhabitats, and not supporting strong competition. We discuss our findings in comparison with other trap-building predators and locate them within the general framework of foraging theory.

Nutrient-Mediated Architectural Plasticity of a Predatory Trap

BackgroundNutrients such as protein may be actively sought by foraging animals. Many predators exhibit foraging plasticity, but how their foraging strategies are affected when faced with nutrient deprivation is largely unknown. In spiders, the assimilation of protein into silk may be in conflict with somatic processes so we predicted web building to be affected under protein depletion.Methodology/Principal FindingsTo assess the influence of protein intake on foraging plasticity we fed the orb-web spiders Argiope aemula and Cyclosa mulmeinensis high, low or no protein solutions over 10 days and allowed them to build webs. We compared post-feeding web architectural components and major ampullate (MA) silk amino acid compositions. We found that the number of radii in webs increased in both species when fed high protein solutions. Mesh size increased in A. aemula when fed a high protein solution. MA silk proline and alanine compositions varied in each species with contrasting variations in alanine between the two species. Glycine compositions only varied in C. mulmeinensis silk. No spiders significantly lost or gained mass on any feeding treatment, so they did not sacrifice somatic maintenance for amino acid investment in silk.Conclusions/SignificanceOur results show that the amount of protein taken in significantly affects the foraging decisions of trap-building predators, such as orb web spiders. Nevertheless, the subtle differences found between species in the association between protein intake, the amino acids invested in silk and web architectural plasticity show that the influence of protein deprivation on specific foraging strategies differs among different spiders.

Microhabitat evaluation and utilization by a foraging predator

Sit-and-wait foraging is a distinct strategy that involves significant investments prior to prey encounters. However, the complexity of decisions involved in selecting, maintaining and abandoning ambush sites provides considerable opportunity for learning and flexibility, particularly for trap-building predators, such as web-building spiders. Most research into the behaviour of trap-building predators has focused on the initiation and completion of foraging bouts (site selection and site abandonment, respectively), and less consideration has been given to the ecological significance of behaviours that occur between these end points. In this study, we sought to determine whether an interim behaviour, flexible trap-construction, is a means of real-time decision making during foraging, and test a new hypothesis that site selection is not a single decision, but a cumulative series of several, distinct decisions based on evaluation of relevant site characteristics. In a laboratory assay, web-building spiders were allowed to choose between microhabitats with and without prey, and site utilization and web construction behaviours were evaluated over a foraging period, to determine how prey cues impact the evaluation and selection of foraging sites by predators. Spiders responded to prey availability across successive phases of site searching and web construction, demonstrating that multiple, distinct decision-making steps are involved in foraging site selection. These results indicate that site maintenance behaviours, such as multiple phases of trap construction, are an integral part of the decision-making framework of foraging predators.

Foraging strategy switching in an antlion larva

Antlion larvae are typically considered as trap-building predators, but some species of antlions always forage without using pits or only sometimes use pits to capture prey; they can ambush prey without pits. This study examined a species that switches its strategy between pit-trapping and ambushing and asked the mechanism behind the switching behaviour. A dynamic optimization model incorporating tradeoffs between the two strategies was built. The tradeoffs were prey capture success and predation risk (both are higher when pit-trapping). The model predicted that antlions should use the trap-building strategy when their energy status is low and should use the ambush strategy when their energy status is high. These predictions as well as an assumption (i.e., predation risk associated with pit-trapping is higher than that associated with ambushing) of the model were empirically confirmed. The results suggest that antlions flexibly switch between pit-trapping and ambushing to maximize their fitness by balancing the costs and benefits of the two strategies.

Multiple prey cues induce foraging flexibility in a trap-building predator

Predators must be behaviourally flexible to counter the temporal and spatial stochastic fluctuations and response variability of their prey. To ensure behaviours are adequate across environments, animals must regularly assess environmental cues. Spider orb webs are an example of a flexible foraging trait in a predator, as web architectural components vary in response to exposure to different prey types and prey traits. The cues used by orb web spiders to initiate changes in web architecture are not known. Current research predicts that prey nutrients and vibratory stimuli are potential candidates, but how they combine to affect spider foraging decisions is not clear. We performed experiments exposing the giant wood spider, Nephila pilipes, to different prey nutrients and vibratory stimuli. Spiders were fed either large profitable prey with high kinetic energy (crickets) or small prey with low kinetic energy (flies). In two treatments the prey nutrients and vibratory cues came from live prey, but in the other two treatments spiders received dead crickets with webs stimulated by flies and vice versa. The spiders fed on live flies built larger webs with more radii that were less stiff and had greater vibration damping. These web characteristics did not differ between the other three treatment groups. Our results show that in the absence of nutrient and vibratory cues from profitable prey, spiders alter their web architecture to build webs better able to capture the less profitable prey at a cost of more material investment, greater web visibility and reduced vibratory signal clarity.