Slow growth improves compensation ability: examining growth rate and starvation endurance in pit-building antlions from semi-arid and hyper-arid regions

Different environments are expected to exert differential selective pressures, often generating distinct sets of traits in organisms inhabiting different geographic regions. Starvation endurance is an important trait for organisms in harsh (i.e., extreme climate and/or biotically poor) and unpredictable environments. This is especially true for sit-and-wait predators, such as antlions, which experience stronger fluctuations in prey arrivals than do actively searching predators. We conducted an experimental comparison of starvation endurance in pit-building antlions, originating from semi-arid and hyper-arid environments. We hypothesized that individuals from the climatically harsher and biotically poor environment (i.e., hyper-arid) should be better adapted to endure long starvation periods. Additionally, we posited that faster-growing individuals are expected to be more sensitive to starvation because of their need to sustain higher metabolic rates. We found that antlions originating from the semi-arid region maintained higher activity levels, which led to slightly higher mass loss rates during starvation, but enabled faster recovery when food supply was renewed. Conversely, antlions originating from the hyper-arid region had lower activity levels, consistent with their lower rate of mass loss during starvation, but this came at the expense of decreased response to prey and lower growth rate when food became available again. Each strategy holds its advantages for coping with long starvation periods, and we cannot say decisively which strategy is better. Results from both regions were consistent with the predictions of the growth compensation phenomenon: antlions that were fed less frequently pre-starvation grew at faster rates when food supply was renewed. Our study demonstrates that individuals originating from different environments adopt different strategies in order to endure starvation, exemplifying antlions’ ability to compensate for mass lost during starvation.     

Examining growth rate and starvation endurance in pit‐building antlions from Mediterranean and desert regions

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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.     

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).     

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.

     

Comparative study on the behavioral response to starvation in three species of antlion larvae (Neuroptera: Myrmeleontidae)

To clarify how pit-building antlion larvae behave during prolonged periods of low resource abundance, pit relocation rate, giving-up time, and respiration rate under starvation conditions were examined, using three species of antlion larvae. Most larvae ofMyrmeleon bore never relocated their pits before they starved to death, while larvae ofHagenomyia micans relocated more often thanMyrmeleon formicarius (average number of pit relocations 0.04 forM. bore, 0.19 forM. formicarius, and 0.62/individual/10 days forH. micans). The relative respiration rate, a ratio of respiration rate at starvation to that at satiation, was lower inM. bore andM. formicarius than in H. micans. Thus, there was an inversely proportional relationship between the pit relocation rate and the decrease in respiration rate under starvation conditions in the three species of antlion larvae.     

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.     

Thermal dependence of trap building in predatory antlion larvae (Neuroptera: Myrmeleontidae)

Trap-building predators remain under strong selection from thermal microenvironments. To address how soil temperature and body size affect trap building, we conducted a laboratory experiment using larvae of the antlion Myrmeleon bore at six ecologically relevant temperatures. Larger larvae built larger traps, and warmer soil led to more and larger traps. Body mass did not alter the dependence of trap building on temperature. Our results suggest that the physiological capacity of antlion larvae, which is affected by larval size and body temperature, is the major determinant of trap building. This effect should be considered when assessing interactions between antlions and prey.     

四种昆虫饵料对穴蚁蛉幼虫生长发育及消化利用的影响

选择4种可规模化饲养的昆虫——米蛾Corcyra cephalonica、家蝇Musca domestica、斜纹夜蛾Spodoptera litura、甜菜夜蛾Spodoptera exigu幼虫来饲养穴蚁蛉Myrmeleon sagax(Walker)幼虫(俗称蚁狮),研究这4种饵料对蚁狮生长发育及消化利用的影响。结果显示,用家蝇幼虫饲养的蚁狮,其体重增长、相对生长率、化蛹率、蛹重均显著高于用斜纹夜蛾和甜菜夜蛾幼虫饲养的蚁狮,而幼虫历期则比斜纹夜蛾和甜菜夜蛾幼虫饲养的短;用米蛾幼虫饲养,虽然蚁狮体重增长、化蛹率和蛹重与用家蝇幼虫饲养的差异不显著,但其相对生长率却显著低于用家蝇幼虫饲养的蚁狮,幼虫历期也比用家蝇幼虫饲养的明显延长。同时食物消化利用的结果显示,用4种饵料饲养蚁狮,它们的近似消化率差异不显著,但食物利用率和食物转化率均以家蝇幼虫饲养的蚁狮最高。经分析比较,在4种饵料昆虫中,以用家蝇幼虫每4d喂蚁狮1次的饲养效果最佳。     

Utilisation of prey by antlion larvae (Neuroptera: Myrmeleontidae) in terms of energy and nutrients

Prey utilisation at low prey densities was determined for third instar Cueta sp., Furgella intermedia (Markl) and Palpares annulatus (Stitz) larvae in terms of wet weight, dry weight, energy and nutrients. Prey utilisation was similar to other insects on a wet weight (42-47%), dry weight (46-49%), energetic (40-58%) and nutritive basis (62-79%). Lipids (33-36%) provided energetically the highest contribution of the nutrients ingested. The quantities of water, proteins, nucleic acids, lipids and carbohydrates extracted by the antlion larvae were in proportion to their availability in their prey, the Hodotermes mossambicus larvae. The quantities of nutrients extracted by the antlion larvae at low prey densities were not significantly influenced by the differences in mandible size, antlion body weight or the trapping method (building a pit or not) of the antlion species. It is proposed that a low metabolic rate and the accumulation of fat reserves, and not the extent of prey utilisation, enable P. annulatus larvae to tolerate a 123-d starvation period in which 22.3% of their body weight is lost.     

Pit relocation by antlion larvae: A simple model and laboratory test

Summary We generated a computer model to analyse the effects of shadow competition for sit-and-wait predators, particularly antlion larvae. The model used a simple foraging assessment rule to determine the quality of an antlion's location, and antlions relocated randomly in their habitat when a location proved to be of low quality. Shadow competition, or competition for food caused when one sit-and-wait predator intercepts moving prey before a second sit-and-wait predator is encountered, was incorporated into the model by restricting antlions to a bounded arena, and having prey for the antlions enter from the arena periphery. Antlions responded to shadow competition by relocating their pits to peripheral areas of their habitat. This peripheral accumulation of pits was most pronounced when antlion densities were high, and when prey availabilities were intermediate. An experimental test with the antlionMyrmeleon immaculatus supported the importance of shadow competition as a cause of observed pit distributions. Only the treatment which incorporated shadowing had pit distributions near the periphery, while the pit distributions in the control treatments did not differ from randomly generated distributions. We conclude that shadowing can influence sit-and-wait predator distributions when the prey distributions and movement patterns generate the conditions necessary for shadowing. But when prey availability is unpredictable, making assessment of patches difficult, or when prey do not originate in the periphery of the habitat, other factors, such as temperature or moisture, could be more important.     

异色瓢虫幼虫的食物搜索行为

本试验采用Nakamuta(1982)装置研究两种光照条件下异色瓢虫幼虫的食物搜索行为,结果表明：(1)摄食刺激均能激发搜索行为由广域型转换为地域集中型;(2)摄食时间越长,地域集中型搜索时间(GUT)值越大;(3)摄食的最后一个食饵大小决定GUT的长短;(4)光照对搜索行为有影响;(5)饥饿度对GUT的长短有一定影响。     

Phenotypic plasticity and variation in morphological and life-history traits of antlion adults across a climatic gradient

We report here on two complementary experiments examining the effect of climate on morphological and life-history traits of antlion adults. We first examined whether body size and wing loading of emerging adults are plastic by raising larvae, collected from five antlion populations along Israel's sharp climatic gradient, in two environmental chambers simulating temperature and humidity of desert and Mediterranean climates. The variance in adult morphology was mostly related to body size, with adults of Mediterranean populations being larger than those of desert populations. Wing-to-thorax ratio was negatively correlated with temperature, compensating for the decrease in wing-beat frequency in colder environments. Differences between climatic treatments were significant for body size but not for the wing-to-thorax ratio, suggesting that body size is more plastic than the ratio between different body components. We next investigated how the exposure of antlion pupae to different climatic conditions influences the emerging adults. Adult body mass increased with final larval body mass at a faster rate when exposed to Mediterranean rather than desert conditions. Duration of the pupa stage was positively correlated with final larval mass, but only under Mediterranean conditions. Adult survival increased with initial mass (after eclosion), but was lower under desert conditions. Similarly, adults lost mass at a faster rate when exposed to desert conditions. Notably, the exposure of the pupae to varying climatic conditions had no effect on adult morphology. Climate is a major factor affecting insect life span and body size. Since body size is strongly linked to fecundity and survival, climate thus has a twofold effect on fitness: directly, and indirectly through body size.     

Feeding resumption, morphological changes and mortality during starvation in Japanese flounder larvae

Japanese flounder Paralichthys olivaceus larvae established first feeding 3 days after hatching (DAH) at c . 17° C. Non-fed fish reached irreversible starvation at age 5 DAH. Non-fed fish showed similar feeding rate and feeding intensity as the fed fish when they were provided with prey before 5 DAH, after which the starved larvae did not feed even when prey became available. None of the six morphological measurements examined (total length, body height, eye height, head height, gut height and myotome height) showed significant differences between the non-fed and fed larvae until 5 DAH. Normal development continued only in the fed group, and the non-fed larvae showed reverse growth or body collapse after 5 DAH. Owing to the shrinkage and collapse at the top of head due to starvation, head height could be a sensitive indicator of starvation in Japanese flounder larvae. In the fed treatments, high mortality occurred from first feeding (3 DAH) to irreversible starvation (5 DAH), accounting for about two-thirds to three-quarters of the overall mortality (46–52%) throughout the experiments. This mortality was not prey density or larval density dependent. Mortality during the same period in the non-fed larvae accounted for about a third of the overall mortality (100%).     

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.     

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.     

Insecticidal bacteria isolated from predatory larvae of the antlion species Myrmeleon bore (Neuroptera: Myrmeleontidae)

Various bacterial species were isolated from the crop (digestive organ) of the antlion species Myrmeleon bore and tested for their insecticidal activity against caterpillars by injection. Sixty-eight isolates from the antlion crop were grouped into twenty-four species based on homologies of 16S rRNA gene sequences and biochemical properties. Isolated Bacillus cereus, Bacillus sphaericus, Morganella morganii, Serratia marcescens and a Klebsiella species killed 80% or more cutworms when injected at a dose of 5x10(5)cells per insect. In addition, cutworms killed by these isolates resembled observations made of caterpillars attacked by antlions. A culture-independent analysis showed that the isolated bacterial species are likely to be frequently present in the antlion crop. These results suggest that insecticidal microorganisms associate with antlions, and may promote the death of prey.     

Sand as a medium for transmission of vibratory signals of prey in antlions Euroleon nostras (Neuroptera: Myrmeleontidae)

Abstract.  European pit-building antlions ( Euroleon nostras / Geoffroy in Fourcroy/) detect their prey by sensing the vibrations that prey generate during locomotory activity. The behavioural reactions and some of the physical properties of substrate vibrations in sand are measured to observe signal transmission through the substrate. The frequency range of the signals of four arthropod species ( Tenebrio molitor , Pyrrhocoris apterus , Formica sp. and Trachelipus rathkei ) is 0.1–4.5 kHz and acceleration values are in the range 400 μm s⁻² to 1.5 mm s⁻². Substrate particle size and the frequency of prey signals both influence the propagation properties of vibratory signals. The damping coefficient at a frequency 300 Hz varies from 0.26 to 2.61 dB cm⁻¹ and is inversely proportional to the size of the sand particle. The damping coefficient is positively correlated with the frequency of the pulses. Vibrations in finer sand are attenuated more strongly than in coarser sand and, consequently, an antlion detects its prey only at a short distance. The reaction distance is defined as the distance of the prey from the centre of the pit when the antlion begins tossing sand as a reaction to the presence of prey. The mean reaction distance is 3.3 cm in the finest sand (particle size ≤ 0.23 mm) and 12.3 cm in coarser sand (particle size 1–1.54 mm). The most convenient sands for prey detection are considered to be medium particle-sized sands.     

Prey detection in antlions: propagation of vibrational signals deep into the sand

Trap‐building antlion larvae detect their prey according to the substrate vibrations produced during movement of the prey on the sand surface. Although most studies are devoted to surface vibrational waves, in the present study, we determine the role of vibrations travelling through deeper sand layers. A behavioural experiment confirms that vibrational stimuli from prey insects on the surface of the sand stimulate the antlions buried in deeper sand layers to move towards the surface. Sand depth and particle size both have a strong effect on signal transmission. The damping coefficient (α₁₀) varies from 0.49 dB to 3.30 dB cm^?1 and depends on frequency (in the range from 100 to 300 Hz), particle size (from finest to coarse sand) and distance from the source of the vibrations. The deeper the sand, the narrower the frequency range of the signal becomes. Sand is a filter for higher frequencies. The smaller the sand particles, the more intense the filtering becomes. Fine sand with a mean sand particle size of 360 μm is a more efficient filter than coarse sand; consequently, high frequencies (> 2.5 kHz) are eliminated at a depth of 3 cm. Mean frequency depends on both depth and particle size. However, low frequency signals still propagate at a certain distance, which is biologically important in prey detection. Although the most efficient signal propagation appears to occur in coarse sand, it contains overly large particles that are inconvenient for relatively small antlion larvae. Predators seek a compromise between fine and coarse sand choosing medium sand.     

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.