The involvement of sand disturbance, cannibalism and intra-guild predation in competitive interactions among pit-building antlion larvae

Competition in trap-building predators such as antlion larvae is a complex biotic interaction, potentially involving exploitation competition, sand throwing (i.e., interference competition), cannibalism and intra-guild predation. We investigated the short-term behavioral and developmental responses of the strict sit-and-wait antlion predator Myrmeleon hyalinus to sand disturbance (i.e., quantification of the impact of severe sand throwing), and to con- and hetero-specific competition by a larger sit-and-pursue antlion species Lopezus fedtschenkoi. We found that antlions subjected to sand disturbances reduced their pit construction activity and relocated less often. Furthermore, the reduction in pit construction activity was stronger among antlions subjected to disturbances prior to feeding. Almost no death occurred during the sand disturbance experiment, but as expected, disturbances caused reductions in the relative growth rates of antlions. This negative effect was stronger in the group exposed to sand disturbances prior to feeding. The presence of the sit-and-pursue competitor led to reductions both in pit construction and in relocation activities of M. hyalinus. Although the per-capita food supply was identical in both experiments, only 48% of M. hyalinus larvae survived the competition experiment, and this pattern was consistent between the con- and hetero-specific treatments. However, in the presence of hetero-specific competitors, the relative growth rate of surviving larvae was significantly lower than that measured in the presence of con-specific competitors. Our study demonstrates that investigating the different components of complex biotic interactions can markedly improve our understanding of how these different factors interact to influence the behavior and life history of organisms.     

An experimental study on the foraging behavior of a pit-building antlion larva,Myrmeleon bore

Foraging behavior of a pit-building antlion larva, Myrmeleon boreTjeder was investigated experimentally to elucidate the relation between the feeding level and pit relocation.

1. In artificial sands constructed in the field the 3rd instar larvae of M. bore rarely changed the positions of their pits, though several antlions had moved actively until they constructed pits. The average feeding rate was 0.3 prey/day/pit, and about 60% of prey captured were ants.
2. To examine whether or not M. bore larvae concentrate into the area where they can capture more prey, 8 antlions were released into each of 6 boxes filled with sand. I divided the sand surface of each box into two half areas, then gave prey to the pits built in a half area and gave no prey to the pits built in the other half. During the 50-day observation period, nonfed antlions never moved into the area where prey were given.
3. The 3rd instar larvae were reared separately without food. Even under starved conditions they rarely relocated their pits until dealth. The average duration of survival period was 83.9 days.
4. The experimental results indicate that M. bore larvae adopt a tactic of sedentary ambushing. These larvae exhibit low movement rates which are independent of prey capture rates.

     

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.     

Factors Influencing Site Abandonment and Site Selection in a Sit-and-Wait Predator: A Review of Pit-Building Antlion Larvae

There is a large body of evidence indicating that predator behavior may strongly influence patterns and processes at the population and community level. Site selection is a major component of fitness in sit-and-wait predators, especially when relocation is rare. Although several review articles dealt with these issues in web-building spiders, this is the first attempt to summarize the effects of biotic and abiotic factors on site selection and relocation in another group of sit-and-wait predators, the pit-building antlions (Neuroptera: Myrmeleontidae). Our synthesis shows that prey abundance may have relatively little effect on pit relocation and that physical properties of the habitat or competition often override its effect. We suggest that owing to a variety of constraints such as physiological constraints or difficulties in assessing site quality, site selection and relocation are not necessarily optimal and thus food intake rate is not maximized. We call for a multi-factorial study on a single species in order to pinpoint the dominant factors and to assess to what extent they influence site selection and relocation. We conclude by proposing new research directions, such as studying whether pit relocation is an adaptive response, when controlling for possible phylogenetic effects.     

Cleaning Up After a Meal: The Consequences of Prey Disposal for Pit‐Building Antlion Larvae

Predators use a variety of strategies for capturing prey. Trap‐building predators can save on searching and encountering costs by investing in the construction and maintenance of traps such as webs and pits. However, what to do with partially consumed prey poses a potential problem. Antlion larvae (Myrmeleon acer) catch ants in conical pits, and dispose of partially consumed carcasses by flicking them a short distance away. We tested whether this prey‐disposal behaviour affects the effectiveness of antlion pits. We observed ant behaviour around artificially constructed pits and compared falls into pits with clean margins to those with conspecific ant carcasses or control objects around the pit edge. The presence of objects near pits affected the behaviour of live ants, and reduced the effectiveness of pits. Live ants spent the most time examining fresh ant carcasses, but the presence of any object near pits deterred pitfalls. Ants fell into pits significantly more often when pit edges were clean, suggesting that antlions could incur a prey capture cost from flicking carcasses from pits as well as from the accumulation of other debris around pit margins.     

Effects of larval antlions Euroleon nostras (Neuroptera, Myrmeleontidae) and their pits on the escape-time of ants

Abstract. Pit-building antlions are predators with a unique predation strategy, namely using pitfall traps constructed in loose sand to catch prey. Here, prey escape-time in the field is measured by introducing ants into one of four different treatment arenas. The first treatment lacks pits and antlions, the second includes 10 antlions that did not build pits, the third comprises eight artificially constructed pits, and the fourth is a treatment of eight antlions in pits and two without pits. Their pits are of a similar size to those used in the third treatment. When antlions are present without constructing pits, they impede the dispersal of prey. The mean escape-time for one half of the released ants is twice as long with antlions present as without them. When pits are present, the time taken for one half of the released ants to escape the predator is more than 10 times as long as when pits are absent. Escape-time from artificial pits is three times that from nonpit building antlions. Pits hinder the escape of ants and therefore increase the amount of time that the prey is available for capture. In the area where the pits are occupied by antlions, escape-time is four times longer than in a treatment with similar sized artificial pits. Thus, it appears that not only a pit, but also the presence of antlions influences the capture success.     

Effect of density on spatial distribution,pit formation and pit diameter of Myrmeleon acer Walker, (Neuroptera: Myrmeleontidae): patterns and processes

The effect of increasing population density on the formation of pits, their size and spatial distribution, and on levels of mortality was examined in the antlion Myrmeleon acer Walker. Antlions were kept at densities ranging from 0.4 to 12.8 individuals per 100 cm². The distribution of pits was regular or uniform across all densities, but antlions constructed proportionally fewer and smaller pits as density increased. Mortality through cannibalism was very low and only occurred at densities greater than five individuals per 100 cm². Antlions in artificially crowded situations frequently relocated their pits and when more space became available, individuals became more dispersed with time. Redistribution of this species results from active avoidance of other antlions and sand throwing associated with pit construction and maintenance, rather than any attempt to optimise prey capture per se.     

The effect of sand depth,feeding regime,density, and body mass on the foraging behaviour of a pit‐building antlion

Abstract 1. Pit‐building antlions are small sit‐and‐wait arthropod predators, which dig conical pits in sandy soils. We studied how biotic (conspecific density and feeding regime) and abiotic (sand depth) factors affect pit diameter and depth, while taking into account the larval body mass. 2. Pit diameter increased with larval body mass at a decelerating rate. In addition, larger larvae tended to relocate less frequently than smaller ones. 3. Sand depth positively affected overall pit size, while increasing conspecific density had a weaker but negative effect on pit size. 4. Feeding the antlions resulted in an increase in pit diameter compared with an unfed control group. However, as prey size increased this positive effect diminished. This result suggests that the existence of prey provides information about the quality of the microhabitat, triggering pit extension. However, similarly to the reduction in the foraging effort of saturated predators, antlions provided with large prey invested only little effort in pit enlargement. 5. Antlions were previously shown to be sensitive to prey and conspecific vibrations in the sand. We thus expected the feeding regime of the neighbour to affect antlion behaviour – surrogate of discriminating between local and global shortage of prey. Nevertheless, antlions with fed neighbours (a local prey shortage) did not show different behaviour compared with a control group in which both antlions were unfed (a global prey shortage).     

Variation in pit size of antlion (Myrmeleon carolinus) larvae: the importance of pit construction

Abstract.Larvae of several antlions build pits that vary in size across and within species. The influence of food limitation and pit building experience on variation in pit size of the larvae of Myrmeleon carolinus was investigated in the laboratory. Unfed larvae that were allowed to build pits had smaller pit diameters than fed larvae. However, fed antlions that had been previously prevented from pit building, initially did not build larger pits than unfed antlion larvae that, too, had been prevented from pit building. Therefore, physiological constraints associated with food limitation alone are not sufficient to explain the reduction in pit size of food limited antlions of this species.     

Microhabitat Selection by Antlion Larvae, Myrmeleon Crudelis: Effect of Soil Particle Size on Pit-Trap Design and Prey Capture

Selective pressure for choosing an adequate habitat should be strong in semisedentary animals because they have limited mobility once established. I examined microhabitat preferences and the adaptive value of these preferences in the antlion larva Myrmeloen crudelis, a semisedentary insect that digs pit traps in soils to capture small arthropods. I tested the habitat preferences of M. crudelis between two soil types in a tropical dry forest of Costa Rica. Specifically, I compared the soil particle composition size within and outside antlion aggregations and manipulated the availability of fine- and coarse-grained soil to assess how differences in soil grain size affect the design and performance of larval traps. Adjacent to antlion pits the soil was composed of a greater proportion of fine-grained particles (2 mm) than soil 1 m away from the pits. A set of experiments demonstrated that (1) in the presence of equal availability of fine- and coarse-grained soils, all larvae built their pits in fine-grained soil; (2) the larvae required less time to start and finish traps in fine-grained soil; (3) the larvae constructed larger and deeper pits in fine-grained soil; and (4) prey capture increased greatly in fine-grained traps compared with coarse-grained traps. Antlion larvae respond to variations in the proportion of fine particles in the soil, suggesting that antlion aggregations result from an active microhabitat selection. The preference for fine-grained soils is adaptive since pits constructed in such substrate are functional for longer periods and much more successful in trapping prey than pits in coarse-grained soil. Sit-and-wait predators that use sessile traps are spatially constrained to track prey abundance. Therefore, the ability to detect and select microhabitats with better conditions that enhance capture success may be under strong selection for this type of organism.     

Disadvantages of living in a populous neighborhood for sit-and-wait predators: Competition for space reduces pit-trap size in antlion larvae

The study of how trap design responds to biotic and abiotic conditions can help to understand the selective forces affecting the foraging of trap-building organisms. We experimentally tested whether pit design can be modified by intraspecific competition for space in larvae of Myrmeleon crudelis, a common sit-and-wait predator that digs conical pit traps in the soil to capture walking arthropods. In a tropical forest in Costa Rica, we measured pit dimensions, larval body size, and the level of competition (i.e., density of neighboring traps) in 40 antlion larvae. These larvae were then taken to the laboratory and allowed to build new traps in individual containers. We measured within-individual changes in the size of traps in the field and in the laboratory, and related these to the level of competition experienced in the field. Larvae with relatively high levels of competition in the field showed a greater increase in the size of their pits in the laboratory. This change was independent of larval size. Larvae with none or few neighbors in the field showed little change in their pit sizes, whereas those with higher competition levels increased their diameter and depth up to 1,400% and 1,000%, respectively. Our results demonstrate that, at least in high-density aggregations, pit design is restricted by competition in addition to the constraints imposed by body size. This work suggests that biotic interactions can play a role in the design of extended phenotypes in sit-and-wait predators that live in dense aggregations.     

Predator hunting modes and predator–prey space games

Predators and prey are often engaged in a game where their expected fitnesses are affected by their relative spatial distributions. Game models generally predict that when predators and prey move at similar temporal and spatial scales that predators should distribute themselves to match the distribution of the prey's resources and that prey should be relatively uniformly distributed. These predictions should better apply to sit-and-pursue and sit-and-wait predators, who must anticipate the spatial distributions of their prey, than active predators that search for their prey. We test this with an experiment observing the spatial distributions and estimating the causes of movements between patches for Pacific tree frog tadpoles (Pseudacris regilla), a sit-and-pursue dragonfly larvae predator (Rhionaeschna multicolor), and an active salamander larval predator (Ambystoma tigrinum mavortium) when a single species was in the arena and when the prey was with one of the predators. We find that the sit-and-pursue predator favors patches with more of the prey's algae resources when the prey is not in the experimental arena and that the prey, when in the arena with this predator, do not favor patches with more resources. We also find that the active predator does not favor patches with more algae and that prey, when with an active predator, continue to favor these higher resource patches. These results suggest that the hunting modes of predators impact their spatial distributions and the spatial distributions of their prey, which has potential to have cascading effects on lower trophic levels.     

Pitfall vs fence traps in feeding efficiency of antlion larvae

Larvae of pit-building antlions are expected to be more efficient at capturing prey than those of non-pit-builders. To test this prediction, feeding behaviors were compared in the same experimental conditions among pit-building Baliga micans and Myrmeleon bore, and non-pit-building Distoleon contubernalis. The number of prey eaten did not differ between species. D. contubernalis larvae used the walls of the experimental chamber as fence traps to capture prey. In the field, they were also found near edges of natural barriers, such as rocks, stones, tree roots, and plant stems. Artificial pitfall traps captured more arthropods near the edges of fences than farther from them. Larvae of the two pit-building species were located in the central part of the experimental chamber. In their natural habitats, the number of arthropods captured by artificial pitfall traps increased with pit size; thus, larger pits may be more efficient for capturing prey. In conclusion, pit-building and non-pit-building antlion larvae are both efficient hunters; the former hunt efficiently by making larger pitfall traps, and the latter do so by waiting for prey at the edge of the natural fences along which arthropods walk.     

The biophysics of pit construction by antlion larvae (Myrmeleon, Neuroptera)

An antlion pit is lined with fine particles during construction. This feature appears to increase the effectiveness of the pit in prey capture. Pit structure is influenced by physical properties of sand and the building behaviour of the antlion. Two physical properties of sand govern pit structure: the angle of repose and Stoke's Law drag force. These two properties complement each other as follows: (a) Since larger particles have a lower angle of repose than smaller particles, fine sand grains tend to stay on the pit walls, whereas larger particles fall to the pit's centre. (b) Large particles have a lower drag to momentum ratio than do small particles. Thus, larger particles are more likely to be thrown out of the pit than are smaller particles. Several behavioural modifications were demonstrated that increase the number of fine particles on the pit walls while reducing construction costs for the antlion. (a) A trajectory angle of 45° is used when the antlion throws particles out of the pit. This angle will maximize the distance to which larger particles are thrown. A trajectory angle of 60° is used at the end of pit construction when the antlion is throwing fine particles on the sides of the pit. This angle reduces the number of these fine particles leaving the pit. (b) Antlions can alter the velocity with which they throw particles. When discarding prey carcasses and debris that have accumulated during prey capture, they use a velocity that is approximately 39% higher than the velocity used during pit construction. (c) By vibrating their forelegs, antlions appear to sift out the finer particles before each throw. This increases the percentage of larger particles discarded from the pit.     

Evolutionarily Stable Relocation Strategy in an Antlion Larva

Antlion pits are often spatially aggregated even though there are potential negative effects associated with the aggregation (e.g., heightened competition and predation risk). This study investigated the possibility that a strategy leading to aggregation can be an evolutionarily stable strategy (ESS). In particular, the strategy considered was ‘decreasing relocation tendency when there are neighbors’. An individual based model showed that the strategy can be the unique ESS when the spatial distribution of prey is not completely random and antlions can learn it from their past foraging experiences. A laboratory experiment was conducted to examine the effects of the presence of neighbors and foraging success on the relocation behavior of antlion larvae. Antlions reduced their relocation tendency with respect to these factors, consistent with the predicted ESS. The results suggest that pit aggregations are formed because antlions reduce their relocation tendency when neighbors exist, and this strategy is an ESS.     

A trade-off between growth and starvation endurance in a pit-building antlion

Trade-offs have a central role in evolutionary ecology and life-history theory. Here, we present evidence for the existence of a rarely studied trade-off between growth rate and starvation endurance in larvae of a pit-building antlion. We first manipulated antlions’ feeding regime and obtained a spectrum of growth rates. Next, we starved the antlions and documented their rate of mass loss. Antlions growing faster during the feeding phase also lost mass faster during the successive starvation period, implying the existence of an induced trade-off between fast growth and starvation endurance. Finally, we fed all antlions with prey items of similar mass and measured both the giving-up prey mass (i.e. the remaining body mass of the prey that was not converted into predator body mass), and growth efficiency of antlions (i.e. proportion of prey consumed, negatively correlated with giving-up prey mass). The giving-up mass was negatively correlated with the growth rate of the antlions during the feeding phase, and positively correlated with their growth rate during the starvation phase (the opposite pattern was evident when examining growth efficiency), incongruently with the common phenomenon of growth compensation (i.e. extracting more of the prey after a starvation period). We suggest that antlion larvae can adopt a physiological mode bounded by two extremes: one extreme is adapted to starvation, involving reduced metabolic rates but also reduced capability to exploit prey, while the other is adapted to fast growth, allowing an efficient exploitation of prey, but at the expense of lowered starvation endurance.     

Variation in food availability influences prey‐capture method in antlion larvae

Abstract 1. Larvae of a Myrmecaelurus sp. are unique among antlions because they have two prey‐capture methods; they either ambush prey at the surface, or dig pit traps that prey fall in to. It was hypothesised that larvae will use the capture method that maximises their net rate of energy gain, which will be influenced by food availability (encounter rate) and by past energy inputs (body condition). 2. Costs were estimated by measuring resting and activity metabolic rates and determining the duration of pit maintenance at various encounter rates with ants that served as prey. Benefits were estimated from the energy gained per ant captured at different encounter rates. 3. Net energy gained was higher with a pit than without one, and was influenced more by the differences in prey capture rate between the two capture methods, and less by the differences in energy costs associated with each method. The proportion of larvae that constructed pits was higher when they were in intermediate body condition than when in good or in poor body condition. 4. Thus, the use of one capture method or the other depends on a combination of the influences of past net energy gain and the antlion’s most recent change in encounter rate with prey. Ambushing without a pit may serve as a default when physiological constraints limit the larvae’s ability to invest in pit construction and maintenance, or when larvae are sated, and saving the energy of pit construction and maintenance is worthwhile.     

Learning in a sedentary insect predator: Antlions (Neuroptera: Myrmeleontidae) anticipate a long wait

Pit-building antlions, the larvae of a winged adult insect, capture food by digging funnel-shaped pits in sand and then lying in wait, buried at the vertex, for prey to fall inside. The sedentary nature of this sit-and-wait predatory behaviour and, especially, antlions’ innate ability to detect prey arrival, do not fit the typical profile of insects that possess learning capabilities. However, we show, for the first time, that learning can play an important role in this unique form of predation. In three separate experiments, individual antlions received, once per training day, either a vibrational cue presented immediately before the arrival of food or that same cue presented independently of food arrival. Signalling of food not only produced a learned anticipatory behavioural response (Experiment 1), but also conferred a fitness advantage: Associative learning enabled antlions to dig better pits (Experiments 2 and 3), extract food more efficiently (Experiments 2 and 3), and, in turn, moult sooner (Experiment 3) than antlions not receiving the associative learning treatment.     

Food-web models that generate constant predator-prey ratios

Summary An approximately constant ratio of number of predator species/number of prey species is observed in several natural communities, although the exact value of the ratio may vary with habitat and the types of organisms in the food web. We test the hypothesis that a constant predator/prey ratio can be generated by what Holt (1977) terms apparent competition and what Jeffries and Lawton (1984) call competition for enemy-free space. We create simple, two trophic-level communities by drawing species of predators and prey at random from a species pool, simulating their interactions using Lotka-Volterra models. The simulated food webs converge over successive periods of invasion and extinction to locally stable systems with approximately constant ratios of number of predator species/number of prey species, despite varying initial conditions. As expected, predator/prey ratios take different values depending upon the biology of the simulated species. We conclude that apparent competition between prey species via shared enemies may be one mechanism whereby approximately constant predator/prey ratios are generated in natural communities.     

Partial prey consumption by antlion larvae

Predictions from two models of partial prey consumption were tested using antilion larvae (third instar Myrmeleon mobilis), a sit-and-wait predator. Griffiths' (1980) ‘Digestion Rate Limitation’ model correctly predicted decreased handling time and increased ingestion rate with increasing encounter rates. The model incorrectly predicted constant percentage extraction; percentage extraction changed significantly with encounter rate. An optimality model appropriate for ambush predators (Lucas & Grafen, in press) qualitatively matched observations, although antlions always discarded prey somewhat earlier than predicted. Thus neither of the models of partial prey consumption quantitatively fits observations. This reduction in handling time has a minor influence on the rate of energy intake, and therefore may be adaptive if other factors are taken into account. I show that discarding prey early is adaptive if prey that arrive when the predator is empty handed are more easily caught than those that arrive when the predator is eating. Preliminary results support this assumption.