Understanding gregariousness in a larval Lepidopteran: the roles of host plant, predation, and microclimate

Abstract.  1. Many moth and butterfly larvae are gregarious early in development, but become solitary in late instars. This ontogenetic variation in behaviour is probably the result of temporal changes in the costs and benefits associated with gregariousness. This study provides observational and experimental evidence that, in one particular moth species, a series of different ecological factors influence larval behaviour at different times during development.
2. Field observations show that young caterpillars of the limocodid Doratifera casta form large aggregations while foraging, but that mature larvae are largely solitary.
3. A field experiment revealed that individual first to third instar larvae in larger groups develop more rapidly, but that group size had no detectable influence on survival. The developmental advantage associated with gregariousness is affected by host plant species, but not by predator exclusion, suggesting that group living in these cryptic early instar larvae promotes feeding facilitation, but does not provide individuals with protection from natural enemies.
4. Laboratory experiments revealed that aposematic fourth instar caterpillars in large groups were less likely to be attacked by a generalist insect predator than those in small groups.
5. Field observations provided no evidence that group living affects body temperature, suggesting that microclimatic factors do not favour gregariousness in this species.
6. It is concluded that gregariousness in D. casta confers at least two different advantages on larvae at different stages early in development, but that these advantages disappear, or are outweighed by costs associated with intraspecific competition, in final instars.     

Predatory risk increased due to egg‐brooding in Armadillidium vulgare (Isopoda: Oniscidea)

Cost of reproduction is associated with a reduction in subsequent survival or future breeding success. A decrease in survival rate of parents during or after reproduction reduces the probability of their future reproduction. However, few studies have demonstrated such survival costs to parents. Females of Armadillidium vulgare hold their eggs in a marsupium and brood these until the young hatch. Caring for eggs in a marsupium seems to place a large burden on brooding females, and it restricts their predator avoidance behaviour. As such, costs of care may increase the mortality rates of brooding females. To reveal the costs of parental care, we examined the effects of egg brooding on behaviour and predation risk. Egg‐brooding females decreased speed of locomotion and rolling duration, and were killed by predators at a higher rate. Our results indicate that egg brooding in A. vulgare has costs in the form of predation risk.     

Nest, but Not Egg, Fidelity in a Territorial Salamander

Egg recognition and subsequent egg brooding are costly forms of parental investment in many species of vertebrates. Life history factors, such as coloniality or risk of brood parasitism, may constrain egg recognition in vertebrates. Female red-backed salamanders ( Plethodon cinereus ) from my study site are territorial and do not share nest sites with other females. They are terrestrial and neither they nor their eggs are likely to be displaced by environmental factors such as flooding. I experimentally tested, in the laboratory, the hypothesis that female red-backed salamanders can discriminate between their own eggs and the eggs of unfamiliar females. Each female was allowed to move about a test chamber containing two clutches of eggs, one clutch with which it was found in the forest and one that had been found with a distant female. Most females remained with one clutch of eggs, which they brooded during the entire observation period. However, they did not significantly prefer to brood their own eggs over the eggs of another female. In a corollary field experiment, I tested whether brooding females that were displaced 1 m from their nest sites would return to their territories and commence brooding behaviour within 3 d. All 10 displaced females returned to their own nest within this time period and were found brooding their eggs. Because female red-backed salamanders at my study site do not tend to share nest sites with other females and because their eggs remain in stationary nests, selection may not have favoured egg recognition. However, the results suggest that female salamanders indirectly recognize their own eggs by actively recognizing their territorial nest sites.     

Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence

Many aposematic species have evolved an aggregated lifestyle, and one possible advantage of grouping in warningly coloured prey is that it makes the aposematic signal more effective by generating a greater aversion in predators. Here we investigate the effect of prey group size on predator behaviour, both when prey are aposematic and when they are not aposematic, to separate the effects of warning coloration and prey novelty. Naive domestic chicks (Gallus gallus domesticus) were presented with either solitary or groups of 3, 9 or 27 live larvae of the aposematic bug Tropidothorax leucopterus. Other naive chicks were presented with larvae of the non-aposematic bug Graptostethus servus either solitary or in groups of 27. Attack probability decreased with increasing group size of aposematic prey, both when birds were naive and when they had prior experience, whereas prey gregariousness did not affect the initial attack probability on the G. servus larvae. In a separate experiment, groups of mealworms were shown to be even more attractive than solitary mealworms to naive chicks. We conclude that the aversiveness of prey grouping in this study can be explained as increased signal repellence of specific prey coloration, in this case a classical warning coloration. These experiments thus support the idea of gregariousness increasing the signalling effect of warning coloration.     

Do caterpillars disperse their damage?: larval foraging behaviour of two specialist herbivores,Euphydryas phaeton (Nymphalidae) and Pieris rapae (Pieridae)

Abstract. 1. To examine ecological and evolutionary aspects of caterpillar foraging behaviour, this study focused on observation of the individual foraging behaviour of two lepidopteran species, Pieris rapae L. and Euphydryas phaeton (Drury), on their respective host plants.
2. Periodic observations over the course of a day showed that the larvae move considerable distances, forage on the upper surfaces of leaves, and often immediately leave areas from which they have fed, leaving a pattern of dispersed herbivory.
3. Differences in foraging behaviour were not found between the two species, even though one species is aposematic and the other is cryptically coloured, but there were significant differences in the foraging patterns of P.rapae on the two host plants, broccoli and radish.     

A within-species warning function for an aposematic signal

Aposematic, or warning, signals are generally interspecific in form: one species advertises noxiousness to a predator or parasite species. In a study of the pipevine swallowtail butterfly (Battus philenor), we show that a pattern of colouration in the caterpillars that is considered to be aposematic in the context of attack by natural enemies also deters oviposition by conspecific females. In field and laboratory assays, females avoided oviposition on plants bearing live conspecific larvae. Females avoided oviposition on plants bearing artificially constructed models identical to larvae in shape, size and colour pattern. Finally, oviposition on plants harbouring a model bearing the larval colour pattern was reduced relative to plants bearing a leaf-green model, suggesting that the larval colour pattern was essential for avoidance. We discuss how intraspecific and interspecific processes might interact in the evolution of an aposematic signal.     

Prey stage preference and feeding behaviour of Oligota kashmirica benefica (Coleoptera: Staphylinidae), an insect predator of the spider mite Tetranychus urticae (Acari: Tetranychidae)

We studied the prey stage preference and feeding behaviour of the first to third instar larvae and adult females of Oligota kashmirica benefica Naomi (Coleoptera: Staphylinidae), a predator of the spider mite Tetranychus urticae Koch (red form) (Acari: Tetranychidae), on leaves of the kudzu vine (Pueraria lobata (Wild.) Ohwi (Leguminosae)) under laboratory conditions. The number of mites eaten increased with the growth of predator larvae. Third instar larvae preyed on all stages of spider mite, whereas first instar larvae preyed mainly on immobile stages (eggs and quiescent stages). The predator larvae showed two types of foraging behaviour (active searching and ambush behaviour) when targeting the mobile stages (larval, nymph and adult stages of prey). Although no difference was found in the number of prey consumed by adult females and third instar larvae of the predator, the adult females mainly attacked and consumed the immobile stages.     

Density reductions by predatory trout increase adult size and fecundity of surviving caddisfly larvae in a detritus-based stream food web

1. In some situations, individuals surviving in environments where predation is intense can grow faster because the benefits of release from intraspecific competition outweigh costs associated with anti-predator responses. Whether these 'thinning' effects of predation occur in detritus-based food webs where resource renewal occurs independently of consumption by consumers was studied. We investigated how effects of predatory brown trout ( Salmo trutta ) on the larvae of the detritivorous stream caddisfly, Zelandopsyche ingens , influenced the size and fecundity of the caddisfly adults.
2. Trout substantially reduced the abundance of Z. ingens larvae, but adult male and female Z. ingens were significantly larger in trout streams compared to fishless streams. Females in trout streams had 33% more eggs than fishless stream females, and egg sizes were not significantly different. In mesocosms, Z. ingens larvae in low density treatments reflecting trout stream abundances grew significantly faster than larvae in high density treatments that were characteristic of fishless stream abundances. Non-lethal trout presence did not influence case building behaviour, feeding rates or growth or Z. ingens larvae, indicating non-lethal effects of predators were negligible.
3. Increased adult size and fecundity associated with trout stream individuals were probably a result of predator thinning of larval density indirectly releasing surviving Z. ingens from intraspecific competition. Thus, predator thinning did influence interactions between larvae in this detritus-based food web as larval growth was strongly density-dependent. However, extrapolating the total number of eggs potentially produced indicates the increased fecundity of females in trout streams would not compensate for losses of larvae to trout predation.     

Laboratory breeding studies of freshwater crayfish, Austropotamobius pallipes (Lereboullet)

SUMMARY. 1. Mature crayfish, collected from an Irish lake before breeding had started, were held in breeding combinations and their mating and brooding activities observed.
2. All mating attempts were initiated by the male. A single mating led to spawning within 6 days but a subsequent mating cancelled the effects of the first. Males mated more often when there were more females present. Males lacking a major cheliped mated less often than did normal males.
3. Larger males mated more often than did smaller males, and although males showed no female size preference, matings were less frequent and generally unsuccessful when males were much larger than females; the female was usually killed. Large females mated successfully with smaller males.
4. Females held at high densities with a larger male mated earlier than at low densities. However, aggression also increased with density; at high densities males fought and killed females.
5. Males held in pairs without females fought; in occasional mating attempts spermatophores were not positioned correctly. Paired females rarely fought; all spawned normally although unmated. Although their eggs soon died and were removed during grooming, brooding behaviour continued for at least 2 months.
6. Brooding females held in pairs shed pleopodal eggs during aggressive encounters. Females held singly showed a lower initial rate of egg loss.     

Prey stage preference and feeding behaviour ofOligota kashmirica benefica (Coleoptera: Staphylinidae), an insect predator of the spider miteTetranychus urticae (Acari: Tetranychidae)

We studied the prey stage preference and feeding behaviour of the first to third instar larvae and adult females ofOligota kashmirica benefica Naomi (Coleoptera: Staphylinidae), a predator of the spider miteTetranychus urticae Koch (red form) (Acari: Tetranychidae), on leaves of the kudzu vine (Pueraria lobata (Wild.) Ohwi (Leguminosae)) under laboratory conditions. The number of mites eaten increased with the growth of predator larvae. Third instar larvae preyed on all stages of spider mite, whereas first instar larvae preyed mainly on immobile stages (eggs and quiescent stages). The predator larvae showed two types of foraging behaviour (active searching and ambush behaviour) when targeting the mobile stages (larval nymph and adult stages of prey). Although no difference was found in the number of prey consumed by adult females and third instar larvae of the predator, the adult females mainly attacked and consumed the immobile stages.     

Experiments on predation and substratum choice by larvae of the muscid fly, Limnophora riparia

Larvae of the muscid fly Limnophora riparia live in lake outlets and prey on other invertebrates living there. In experiments, we demonstrated that larvae prefer moss as a substratum, though they will bury themselves in any suitable material to avoid light. The substratum is used to anchor Limnophora larvae as they attack their prey. When given a choice of prey they preferred chironomid and black fly larvae to oligochaetes and psyehodid larvae. Larvae of the black fly Simulium noelleri were used in laboratory experiments to test the interaction of predator and prey. Limnophora larvae attacked black fly larvae of all sizes, but preferred small larvae, the body contents of which were often removed completely. Increasing prey or predator density did not affect this latter preference, though an increase in predator density, or a decrease in prey density, did cause the predator to take prey of medium size as well as small prey. Limnophora larvae showed the same size preference when attacking dead (freshly-killed) prey and they preferred to attack larvae rather than pupae when both were available. They did not attack black fly eggs.     

Foraging behaviour influences the outcome of predator–predator interactions

Abstract.  1. Interactions among predators may influence the total efficiency of a predator complex. The effect of intra- and interspecific interactions of the generalist predators Orthotylus marginalis (Heteroptera: Miridae) and Anthocoris nemorum (Heteroptera: Anthocoridae) was investigated in a laboratory experiment. Outcomes of the interactions were determined by comparing predation rates on eggs and larvae of the blue willow beetle Phratora vulgatissima of single individuals with those of two individuals of the same or different species.
2. A non-additive, antagonistic effect on predation rates due to intraspecific interactions was found between individuals of A. nemorum . No such effect was found in O. marginalis . These results are as expected as a consequence of differences in behaviour of the two predator species: A. nemorum is a much more active and mobile predator than O. marginalis .
3. Contrary to expectation, interspecific interactions between A. nemorum and O. marginalis did not affect the total predation rate.
4. An observation from the field corroborated the results obtained in the laboratory study; there was no negative relationship between the densities of the two predator species, indicating that the two species do not interact negatively in the field at their natural densities.
5. It is concluded that the additive effect of multiple predator species is of potential value in biological control.     

Influence of prey density, species and developmental stages on the predatory behaviour ofAmblyseius longispinosus (Acari: Phytoseiidae)

The influence of prey density, species and developmental stages on the predatory behaviour ofAmblyseius longispinosus (Evans) was studied. A 24 h exposure revealed that gravid females were more voracious compared to young females. The trends in the number of eggs and larvae consumed by each young and gravid female predator were about the same, showing an increase with density of the red and the yellow strains ofT. urticae levelling off at a prey density of 40 per predator. The highest mean number of eggs consumed in 24 h was 16.7 for the young female and 33.3 for the gravid female, and a mean high of 17 larvae in 24 h for the young female and 27.8 for the gravid female. With adult prey, however, the predators reached satiation point at a lower density of five to ten adult prey per female. In general, the response curves were adequately described by the Holling’s Type II model. Under continuous exposure for five days, a significant reduction in consumption was observed with the gravid female from the second day onwards, to a level similar to the number of eggs and larvae consumed by a young female predator.     

Extended Mother–Offspring Relationships in Crayfish: The Return Behaviour of Juvenile Procambarus Clarkii

Crayfish shows a relatively complex parental behaviour compared with other invertebrates, but the literature provides only anecdotal accounts of this phenomenon. In Procambarus clarkii, we described the ‘return’ behaviour of third‐stage juveniles when offered four types of adults: biological mothers, foster mothers, non‐brooding females and males. Then, we analysed the posture and behaviour of the adults to understand the role played by the putative mother in attracting the juveniles. Contrary to non‐brooding individuals, both biological and foster mothers displayed a relatively rare locomotion, executed few cleaning and feeding acts, and never attempted to prey on juveniles. They often assumed a ‘spoon‐like telson posture’ that seemed to facilitate offspring’s approaches. Juveniles increased the frequency of tail‐flips away in the presence of non‐brooding adults; conversely, they accepted foster mothers, along with biological mothers, but not as fast as the latter. Taken together, these results suggest that mother–offspring relationships in P. clarkii are more refined than previously thought, being possibly a key factor enabling this species to thrive in harsh environmental conditions.     

Dynamic switching in predator attack and maternal defence of prey

Predator and prey relationships are dynamic and interrelated. Thus, any offensive behaviour will vary according to differing defensive behaviours, or vice versa, within each species in any predator–prey system. However, most studies are one‐sided as they focus on just one behaviour, that of either the predator or prey. Here, we examine both predatory behaviour of an oophagus katydid and antipredator behaviour by a frog with egg‐stage parental care. Katydid offensive behaviour and predation success was greater in females and increased with predator maturity and size. Frog defensive behaviour was sex specific, probably because only mothers provide parental care. Defensive behaviour could be active, such as charging predators, or passive, such as sheltering eggs, with greater active defence against larger predators; neither was influenced by offspring age. These results are contrary to existing theory, which argues parental investment ought to be negatively correlated with parental predation risks and affected by offspring age. This study highlights the use of antipredator behaviour to test predictions of parental investment theories in amphibians. In addition, it illustrates the need to consider factors that influence both species concurrently when examining the complex interaction between predators and parents.     

Attacks by predators on artificial cryptic and aposematic insect larvae

Colour and colour patterns seem to be especially important visual warning signals for predators, which might have innate or learned ability to avoid aposematic prey. To test the importance of larval colour pattern of the aposematic ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), an invasive alien species in Europe, we presented the plasticine models of aposematic larvae to wild and naïve birds. We studied the attacks on aposematic larvae of various patterns and colours in nature and in an outdoor aviary. The larvae were cryptic (green), aposematic (resembling those of the H. axyridis larvae), and semi-aposematic (i.e., black but missing the typical orange patches of H. axyridis larvae). We detected attacks on 71 larvae out of 450 (i.e., 2.6% daily predation). Twenty-nine attacks were made by birds, 37 by arthropods, and five by gastropods. Wild birds attacked green and black larvae significantly more often than aposematic larvae. Colour did not have an effect on attacks by arthropods. The experiment with naïve birds was conducted in an outdoor aviary, where naïve great tits, Parus major L., were offered the same artificial larvae as in the first experiment. In total, 57 of 90 exposed larvae were attacked by birds (i.e., 28% daily predation), and green larvae were attacked significantly more than the aposematic larvae (but not more than black larvae). Our results imply that aposematic larvae of H. axyridis are more than 12× less likely to be predated by birds than green larvae in nature. The aposematic pattern represented a more effective signal than the semi-aposematic signal. The ability to reject aposematic prey seemed to be innate in our birds.     

Context-dependent aggregation in Common Frog Rana temporaria tadpoles: influence of developmental stage, predation risk and social environment

1. This study examines the aggregation behaviour and activity of larvae of the Common Frog Rana temporaria in relation to the early social environment, ontogeny and the presence of chemical cues from a predatory fish to address three main questions: (i) Does previous social interaction influence aggregation behaviour in later developmental stages? (ii) To what extent does aggregation behaviour depend upon the risk level perceived by the individual? (iii) Does aggregation behaviour change through ontogeny?
2. Tadpoles were reared from eggs either in small groups or in complete isolation. In relatively early stages of development, tadpoles showed no preference for the side of the test container containing siblings over the side containing no larvae regardless of the social context experienced (isolation or contact with siblings).
3. The presence of chemical cues from a potential predator did not trigger the aggregation behaviour of tadpoles, but it had a remarkable effect on their activity and spatial distribution. Tadpoles exposed to water preconditioned by a predator spent significantly less time swimming and avoided the central area of the test container more frequently than did controls exposed to unconditioned water.
4. Tadpoles were more active, avoided the central section and associated preferentially with conspecifics (siblings) at later stages of development regardless of the social conditioning they had previously experienced.
5. Individuals reared in groups were twice as active as individuals reared in isolation. This suggests that the early social environment experienced by larvae can influence future behaviour and thereby growth and development rates.
6. The expression of conspecific attraction is probably linked to an ontogenetic shift in larval behaviour. However, reduced activity, rather than aggregation, appears to be the basic antipredator mechanism in larval Common Frog.     

Higher survival of an aposematic than of a cryptic form of a distasteful bug

Summary An experiment was performed to assess the relative survival of two forms of 5th instar larvae of Lygaeus equestris (Heteroptera, Lygaeidae) — the normal red form, called aposematic, and a mutant grey form, called cryptic — when given to hand-raised great tits (Parus major).Sixteen birds were presented with aposematic larvae and 16 were presented with cryptic larvae in 10 consecutive trials. One attack per trial was allowed. Both larval forms were presented against a background matching the grey larvae, but since both prey types were presented in a specific place known to the predator, detection rate for both was assumed to be unity.Birds learned to avoid both prey types. However, the survival of the aposematic larvae was higher than that of the cryptic ones due to three aspects of predator behaviour: i) a greater initial reluctance to attack, ii) a more rapid avoidance learning, and iii) a lower frequency of killing in an attack, when the prey was aposematic. Moreover, a greater number of birds learned to avoid prey without killing any individual, when the prey was aposematic. This result is considered to be due to prey coloration alone, since, in a separate test, no difference in prey distastefulness could be detected.This experiment shows that individual prey can benefit from being aposematic and indicates that individual selection can be a sufficient explanation for the evolution of aposematic coloration. It was concluded that, since the survivorship was 6.4 times higher for the aposematic prey, it could have a detection rate that is correspondingly higher than the cryptic in order for the two forms to have equal fitness.     

A quantified ethogram for oviposition behavior and oviposition preference in the hemipterophagous butterfly Spalgis epius (Westwood) (Lepidoptera: Lycaenidae)

In this study, we examined the oviposition behavior and preference of Spalgis epius, a potential predator of mealybug crop pests. An ethogram of oviposition behavior was constructed based on observations made in an oviposition cage. Ovipositional behavioral acts were catalogued and separated into two behavioral repertoires: searching and egg laying. Gravid females of S. epius oviposited similar numbers of eggs on three mealybug species. Females preferred eggs and adults to nymphs of mealybugs for oviposition. Among three species of mealybugs attended by ants, females laid fewer eggs in the mealybug mass attended by Oecophylla smaragdina than on mealybugs attended by Tapinoma melanocephalum and Camponotus variegatus. Females preferred mealybug masses already containing conspecific eggs to mealybug masses containing conspecific larvae or Cryptolaemus montrouzieri larvae for egg deposition. Gravid females laid larger numbers of eggs under bright sunlight than in diffused sunlight or shade. The results of this study showed that S. epius can effectively attack any species of mealybugs, avoid intra- and interspecific competition, and co-exist with some species of ants attending mealybugs. With the knowledge of these behaviors, this predator can be effectively utilized as a major biological control agent of mealybugs.     

Variance in number of eggs per patch: oviposition behaviour and population dispersion in a seed parasitic moth

ABSTRACT. 1. The relationship between oviposition behaviour and population dispersion was analysed for Grey a subalba Braun (Lep., Incurvariidae), a species in which females usually, but not invariably. lay eggs in only a few schizocarps (seed-pairs) on each umbellet they visit on Lomatium dissectum (Umbelliferae). During each of four years females exhibited a constant probability of leaving an umbellet after each egg was laid. Hence, some umbellets received more eggs than others and the behaviour matched a geometric distribution of eggs among umbellets.
2. The variance in number of schizocarps attacked per umbellet by individual females did not result from females choosing schizocarps of particular sizes or avoiding schizocarps that already contained eggs or larvae. A potential, but speculative, explanation of the variance is that females distribute their eggs among umbellets in a way that maximizes unpredictability on larval dispersion to a searching parasitoid, The pattern of oviposition by Greya females fits the truncated geometric distribution that is predicted if information, as indexed by the Shannon-Wiener entropy measure, is minimized. None the less, other measures of unpredictability or minimum information are possible, and the results highlight the problem of how to identify patterns of movement that may result from selection for unpredictability to enemies.
3. In systematic surveys of the L.dissectum population during three consecutive years, virtually all plants had between 10% and 65% of their seeds attacked. Hence, the separation of oviposition bouts between umbellets and the constant probability of leaving an umbellet after each egg was laid resulted in a broad distribution of Greya attack among L.dissectum plants.