Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars

1. Aposematism is a widely used antipredator strategy in which an organism possesses both warning coloration and unprofitable characters. Theoretical evidence suggests that aposematic colour should develop when high opportunity costs imposed by crypsis force an organism to engage in conspicuous behaviours. Hence, it is expected that ontogenetic colour change (OCC) in larval insects should include aposematism when foraging needs compel behavioural modifications that preclude a continued state of crypsis. 2. To test this idea, I first investigated whether OCC in caterpillars of the panic moth Saucrobotys futilalis was indicative of a switch from cryptic to aposematic coloration. I then examined the context of panic moth OCC as it related to foraging patterns and behavioural conspicuousness. 3. Early Saucrobotys instars are a cryptic green, but later instars become progressively more orange and develop black spots. Early instar larvae forage cryptically on the inner parenchyma of silked-together host plant leaves to avoid predation, but are rapidly forced to engage in conspicuous foraging behaviours as they outgrow the resources afforded by their shelters. Both coloration and behaviour reach maximal conspicuousness in final instar larvae. 4. As predicted, OCC encompassed a change from crypsis to aposematism in Saucrobotys. Aposematic function was demonstrated by changes in both antipredator behaviour patterns and effectiveness of predator deterrence in early and late instars. Moreover, increased opportunity costs of crypsis and behavioural conspicuousness coincided with the onset of aposematic coloration. 5. This pattern of OCC suggests that aposematic coloration in Saucrobotys develops as a response to constraints imposed by crypsis. Moreover, my study illustrates the importance of the study of ontogenetic patterns in determining how behaviour, morphology, and predator responses interact to influence the initial evolution of phenomena such as aposematism.     

Interaction of a solitary larval endoparasitoid, Microplitis mediator, with its host, Mamestra brassicae: host acceptance and host suitability

Abstract:  Microplitis mediator (Haliday) (Hym., Braconidae) is an important parasitoid of early instar larvae of the European cabbage moth, Mamestra brassicae L. (Lep., Noctuidae). In the laboratory, we examined attack responses of female M. mediator to the first three larval instars of M. brassicae . Females were presented with M. brassicae larvae either one individual at a time in a no-choice experiment, or three individuals, one from each instar, simultaneously in a choice experiment. Whether or not there was choice, naïve female parasitoids attacked a high proportion of larvae and did not discriminate among instars. In the no-choice experiment, attacked larvae were reared, and parasitoid cocoons were produced from about 76% of larvae attacked as first and second instars, but from only 19% of larvae attacked as third instars. Dissections of attacked larvae from the choice experiment showed that about 79% of attacks on first and second instars resulted in oviposition compared with only 49% for third instars. When given choice, frequency and number of attacks on first instar larvae increased with increasing parasitoid experience. Our results suggest that first and second instar larvae of M. brassicae are suitable hosts for M. mediator , but that third instar larvae are suboptimal both because oviposition attempts were frequently unsuccessful and because immature parasitoids failed to complete development. Nevertheless, naïve attacking parasitoids exhibited minimal discrimination among instars, although experienced parasitoids most frequently attacked first instar larvae. The host selection behaviour of M. mediator is discussed in the context of optimal foraging theory and implications for biological control.     

Behavioural responses of larval container mosquitoes to a size-selective predator

Abstract.  1. The hypothesis that size-selective predation and species-specific prey behaviours facilitate the coexistence between larvae of invasive Aedes albopictus (Skuse) and U.S.A.-native Ochlerotatus triseriatus (Say) was tested experimentally with the predator Corethrella appendiculata (Grabham).
2. Larval behaviours associated with a higher risk of predation were identified, and prey behavioural responses were tested in either the physical presence of predators or in water containing predation cues. Larvae that thrashed on container bottoms had a higher risk of being captured by fourth instar C. appendiculata than did larvae resting on the water surface. Ochlerotatus triseriatus , but not A. albopictus , adopted low-risk behaviours in response to water-borne cues to predation. Both prey species reduced risky behaviours in the physical presence of the predator, but O. triseriatus showed a stronger response.
3. The vulnerability of 2nd and 3rd instar prey to predation was compared, and behavioural responses were correlated with prey vulnerability. Second instars of both species were more vulnerable to predation by C. appendiculata than were 3rd instars, and the 3rd instar A. albopictus was more vulnerable than O. triseriatus of the same stage. All instars of O. triseriatus showed a similar reduction of risky behaviours in response to the presence of C. appendiculata despite 4th instar prey being relatively invulnerable to size-selective predation.
4. Weaker predator avoidance, coupled with superior competitive ability, of invasive A. albopictus is likely to contribute to its coexistence with O. triseriatus in containers of the south-eastern U.S.A., where C. appendiculata can be abundant.     

Dropping behaviour of larvae of aphidophagous ladybirds and its effects on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas

Abstract.  1. Two experiments were performed in the laboratory to assess the behaviour of dropping from a host plant as a defence against intraguild predation in aphidophagous ladybird larvae.
2. In the first experiment, encounters were observed on bean plants between fourth instars of the intraguild predator species, Harmonia axyridis , and first instars of two other ladybird species, Adalia bipunctata (L.) and Coccinella septempunctata (L.). The percentages of first instars of the latter two species that dropped from the plant in response to attack differed dramatically, with 47.5% of C. septempunctata first instars dropping vs. 0% of A. bipunctata .
3. In the second experiment, first instars of A. bipunctata or C. septempunctata and a fourth instar of H. axyridis were allowed to forage together on bean plants for 3 h. During this time, 44.3% of C. septempunctata larvae dropped from the plant, but less than 2% of A. bipunctata larvae did so. In contrast, 95.0% of A. bipunctata larvae fell victim to intraguild predation by H. axyridis vs. only 54.5% of C. septempunctata larvae.
4. The significance of dropping behaviour of ladybird larvae as a defence against intraguild predation, and the relationship of dropping behaviour to species-specific habitat affinity of ladybirds, is discussed.     

Gregariousness affects performance and defensive reactions in swallowtail caterpillars

1. Group living in caterpillars may enhance individual performance due to sharing of costs associated with individual tasks when dealing with biotic or abiotic ecological factors. 2. In the gregarious caterpillar Battus polydamas archidamas (Papilionidae) egg clusters and caterpillar groups vary in size. We hypothesized that individual survival would be higher in larger groups and that group living would enhance individual performance: shorter development time and/or reduced frequency of (presumably costly) defensive reactions in larvae and larger adult size. We also tested whether the group size conferring the highest survival to laboratory-reared caterpillars matched the most frequent egg clutch size in the field. 3. We collected egg clutches in the field and reared caterpillars in groups of 1, 6, 10, and 14 individuals. We quantified larval survival and stage duration as well as adult mass under laboratory conditions, excluding natural enemies. We also recorded the frequency of larval defensive reactions (thrashing and osmeterium display) against a tactile stimulus of first-instar larvae. 4. Group living enhanced caterpillar survival, particularly during the first instars, when caterpillars are 100% gregarious. Groups of intermediate size reduced larval development time but group living did not affect adult mass. Individual caterpillars in groups showed defensive reactions less frequently than solitary individuals, revealing a cost-saving feature of gregariousness for this swallowtail species. The most frequent clutch size in the field (9–10 eggs) did not match the larval group with highest survival (14 individuals), but did match the group with shortest development time.     

Where to stay by night and day: Size-specific and seasonal differences in horizontal and vertical distribution of Chaoborus flavicans larvae

1. Data on the distributions of pelagic and benthic Chaoborus flavicans larvae were gathered in 1994 and tested for their agreement with the predator avoidance hypotheses. The development of all Chaoborus life stages, as well as the horizontal and vertical distribution in the four larval instars, was followed from May until October. We expected the largest larvae to dwell deeper by day, thus avoiding predation by visually foraging fish.
2. In agreement with this prediction body size increased with daytime depth, and this was true both between and within instars. The migration amplitude consequently increased with larval instar.
3. There was also evidence for horizontal migration, mainly in the third but also in the fourth instar.
4. Along a horizontal transect with increasing depth, locations with many benthic larvae had fewer pelagic larvae. Oxygen concentration was a good predictor of maximum benthic larval depth for most of the season but failed to predict their distribution in autumn.     

Factors influencing aggregation between nymphs of the lime aphid, Eucallipterus tiliae (L.)

Abstract. 1. Aggregation in the lime aphid is influenced by the newly-born nymphs staying close to their mother.
2. The aggregations are brought about by gregariousness between the first instar nymphs and their reluctance to move far from their birthplace.
3. As the nymphs mature they become more wide-ranging and leave the aggregation. Dispersal is also promoted by a lack of gregariousness between different instars.
4. Such aggregations remain intact only as long as the adult continues to reproduce the relatively sedentary first instars.
5. The significance of this behaviour in the spacing of the lime aphid is discussed.     

Gregariousness and repellent defences in the survival of phytophagous insects

Group living has both costs and benefits for plant‐feeding insects, but defence against predators is the most widely acknowledged benefit. Gregarious folivores typically have warning coloration and elaborate anti‐predator defences. Do these defences protect these species from predation? To see if protection from predators generally results from gregariousness, I compared the shapes of published survivorship curves of externally feeding, gregarious and solitary Lepidoptera and Symphyta. Gregarious species are less likely than solitary species to die in the larval stages. However, solitary species that have anti‐predator defences do not have higher larval survival compared to gregarious species. This result, along with evidence from experimental manipulations of group size, suggests that repellent defences per se do not increase survival of gregarious larvae. Group behaviour is undoubtedly important in affecting the higher larval survival of gregarious species, but we currently cannot determine whether predator learning, dilution of risk, or rapid development contribute most to increasing survival.     

Fruit abscission by Physalis species as defense against frugivory

Fruit abscission as a response to herbivory is well-documented in many plant species, but its effect on further damage by mobile herbivores that survive fruit abscission is relatively unstudied. Physalis plants (Solanaceae) abscise fruit containing feeding larvae of their main frugivore, Heliothis subflexa Guenée (Lepidoptera: Noctuidae), a specialist moth. We tested the ability of H. subflexa larvae placed under the plant canopy to find and climb onto two architecturally different Physalis species. Physalis pubescens L., a low, shrub-like, spreading plant, abscises its fruit at a higher rate than Physalis angulata L., a tall arborescent plant. As a result, small larvae are more often dropped from P. pubescens . Third and fifth instars located P. pubescens faster and with a higher probability than P. angulata . Although fifth instars outperformed third-instar caterpillars at finding P. angulata , P. pubescens was located equally fast by the two instars. Heliothis subflexa located Physalis plants more successfully and more quickly than a close relative, the generalist Heliothis virescens Fabricius. The higher fruit abscission rates in P. pubescens may be an evolved response to its greater susceptibility to searching caterpillars.     

Factors affecting host selection in an insect host–parasitoid interaction

1. Many parasitoids can develop successfully in different stages of the same host but the costs of parasitism may vary between the stages. The stage of host attacked has generally been determined when there is no choice, giving a misleading impression of host selection or preference.
2. The rate of parasitism by a solitary endoparasitoid, Venturia canescens , of each larval stage of the Indian meal moth, Plodia interpunctella , was examined with and without a host refuge from parasitism. In addition, when given a choice of host stages, with and without a refuge, the influence of parasitoid age on host selection was examined.
3. Wasps were able to parasitize all except the first instar, but second instars experienced significantly reduced parasitism, in both refuge treatments, compared with third to fifth instars. Whilst parasitoid emergence was always significantly less when all host stages had a refuge, the reduction was only marginally significant when second instars were attacked.
4. When given a choice of second- and fifth-instar larvae, wasps consistently parasitized more fifth instars, both with and without a refuge. Moreover, significantly fewer second-instar larvae were parasitized in the presence of fifth instars than when presented alone to the wasps. This pattern of parasitism was unaffected by the increasing age of the parasitoids.
5. Host selection by V. canescens is discussed in terms of host–parasitoid population dynamics and structure.     

Ontogenetic shifts in the functional response and interference interactions of Rhyacophila dorsalis larvae (Trichoptera)

1. Ontogenetic shifts in predator behaviour can affect the assessment of food‐web structure and the development of predator–prey models. Therefore, it is important to establish if the functional response and interference interactions differ between life‐stages. These hypotheses were tested by (i) comparing the functional response of second, third, fourth and fifth larval instars of Rhyacophila dorsalis, using three stream tanks with one Rhyacophila larva per tank and one of 10 prey densities between 20 and 200 larvae of Chironomus sp.; (ii) using other experiments to assess interference within instars (two to five larvae of the same instar per tank), and between pairs of different instars (one, two or three larvae per instar; total predator densities of two, four or six larvae per tank). 2. The first hypothesis was supported. The number of prey eaten by each instar increased with prey density, the relationship being described by a type II model. The curvilinear response was stronger for fourth and fifth instars than for second and third instars. Mean handling time did not change significantly with prey density, and increased with decreasing instar number from 169 s for fifth instars to 200 s for second instars. Attack rate decreased progressively with decreasing instar number. Handling time varied considerably for each predator–prey encounter, but was normally distributed for each predator instar. Variations in attack rate and handling time were related to differences in activity between instars, fourth and fifth instars being more active and aggressive than second and third instars, and having a higher food intake. 3. The second hypothesis was partially supported. In the interference experiments between larvae of the same instar or different instars, mean handling time did not change significantly with increasing predator density, and attack rate did not change for second and third instars but decreased curvilinearly for fourth and fifth instars. Interference between some instars could not be studied because insufficient second instars were available at the same time as fourth and fifth instars, and most third instars were eaten by fourth and fifth instars in the experiments. Prey capture always decreased with decreasing attack rate. Therefore, interference reduced prey consumption in fourth and fifth instars, but not in second and third instars. The varying feeding responses of different instars should be taken into account when assessing their role in predator–prey relationships in the field.     

Cohort studies on mosquito (Diptera: Culicidae) larvae living in the water-filled floral bracts of Heliconia aurea (Zingiberales: Musaceae)

Abstract. 1. An experimental and observational study of the three species of mosquito larvae living in the water-filled floral bracts of Heliconia aurea at Rancho Grande, Venezuela, was designed to determine if each mosquito species forms instar cohorts and excludes conspecifics of younger instars. This study was motivated by a statement of Maguire (1971) who suggested that mosquito larvae in Puerto Rican Heliconia inflorescences form instar cohorts and exclude younger mosquitoes from the floral bracts.
2. Field observations of naturally occurring populations of mosquito larvae from fifty-three H.aurea inflorescences give no indication that cohorts are formed for Wyeomyia felicia and Culex bihaicolus . However, there is strong evidence that cohorts of Trichoprosopon digitatum occur. These cohorts are not structured by larval competition but by female preference of the youngest bracts as oviposition sites and by large T.digitatum larvae feeding on smaller con-specifics.
3. Field experiments show that first instar W.felicia and C.bihaicolus survive as well over a 6 day period in the presence of third instar conspecifics as they do when all mosquito larvae in an experimental bract are first instars.     

Foliage‐age mixing within balsam fir increases the fitness of a generalist caterpillar

1. Manipulative field studies were carried out to evaluate the foliage age preference–performance relationship for an extreme generalist herbivore, the whitemarked tussock moth (Orygia leucostigma Smith) (Lepidoptera: Lymantriidae), within balsam fir [Abies balsamea (L.) Mill]. 2. Field surveys indicated that early instar caterpillars fed almost exclusively on young (i.e. current‐year) foliage, whereas late instars caterpillars fed on both young and mature (i.e. 1‐ and 2‐year‐old) foliage. 3. Survival of early instar caterpillars was highest in treatments where current‐year and/or 1‐year old foliage were available, but decreased significantly on older foliage. In contrast, late instar caterpillars had the highest survival when allowed to feed on all age classes of foliage, whereas potential fecundity was highest for late instars that fed on young foliage. 4. Overall, caterpillars had 32–65% higher fitness when able to feed on all rather than just one age class of foliage. 5. These results support both the ‘complementary diet' hypothesis, which states that dietary mixing of different‐aged foliage can increase nutrient uptake and/or dilute harmful secondary plant chemicals, and the ‘ontogeny’ hypothesis, which attributes changes in diet to changes in the nutritional needs and/or tolerance to plant defences of juvenile insects as they develop.     

Achieving high sexual size dimorphism in insects: females add instars

Abstract.  1. In arthropods, the evolution of sexual size dimorphism (SSD) may be constrained by a physiological limit on growth within each particular larval instar. A high SSD could, however, be attained if the larvae of the larger sex pass through a higher number of larval instars.
2. Based on a survey of published case studies, the present review shows that sex-related difference in the number of instars is a widespread phenomenon among insects. In the great majority of species with a sexually dimorphic instar number, females develop through a higher number of instars than males.
3. Female-biased sexual dimorphism in final sizes in species with sexually dimorphic instar number was found to considerably exceed a previously estimated median value of SSD for insects in general. This suggests a causal connection between high female-biased SSD, and additional instars in females. Adding an extra instar to larval development allows an insect to increase its adult size at the expense of prolonged larval development.
4. As in the case of additional instars, SSD is fully formed late in ontogeny, larval growth schedules and imaginal sizes can be optimised independently. No conflict between selective pressures operating in juvenile and adult stages is therefore expected.
5. In most species considered, the number of instars also varied within the sexes. Phenotypic plasticity in instar number may thus be a precondition for a sexual difference in instar number to evolve.     

Leaf toughness changes the effectiveness of larval aggregation in the butterfly Byasa alcinous bradanus (Lepidoptera: Papilionidae)

Two subspecies of the papilionid butterfly Byasa alcinous , B. a. bradanus and B. a. alcinous , have varying degrees of larval aggregation. Early instar larvae of ssp. bradanus always occur in aggregations. To determine the functions of larval aggregation in this subspecies, we examined the effects of leaf toughness on larval performance when caterpillars were reared alone and in aggregations. Newly hatched larvae were reared either individually or in groups of 10 and were fed either tough or tender leaves of Aristolochia debilis . When fed tough leaves, more gregarious larvae survived the first instar. This difference between solitary and aggregated larvae did not occur when caterpillars were fed soft leaves. The effects of aggregation on larval weight and duration were not significant between leaf-toughness treatments. Larval aggregation of B. a. bradanus improves larval survivorship in early instars that use host plants with tough leaves.     

Host tree influences on the dispersal of first instar gypsy moths, Lymantria dispar (L.)

Abstract. 1. In laboratory tests, first instar gypsy moths attempted dispersal more frequency when exposed to less acceptable foliage.
2. First instars from small eggs attempted dispersal less frequently than larvae from large eggs when exposed to foliage from highly acceptable or marginally acceptable hosts. Dispersal rates of larvae from medium sized eggs were intermediate.
3. These results (1–2) confirm and expand upon the findings of Capinera & Barbosa (1976).
4. In the field, data on the relative densities of larvae on different host species support the conclusion that the frequency of dispersal attempts is inversely related to host acceptability.
5. The implications of these findings for the population dynamics of the gypsy moth are discussed.     

The consequences of larval aggregation in the butterfly Chlosyne lacinia

1. Females of Chlosyne lacinia (Geyer) (Lepidoptera: Nymphalidae, Melitaenae), the bordered patch butterfly, clump eggs in a few large clusters on their host plant, Helianthus annuus. Resulting larvae form sibling aggregations to at least the third instar.
2. The effect of group size on survival and development of C. lacinia larvae was tested experimentally in the field. Larvae developed faster and survived better in larger groups.
3. The effects of various predator guilds (ground-dwelling arthropods, aerial arthropods and avian predators) on survival of larvae was then tested while controlling group size. Ground-dwelling arthropods, mainly fire ants Solenopsis xyloni , reduced larval survival greatly but other solitary invertebrate and avian predators did not alter survival. Group defences and aposematism of C. lacinia larvae are probably ineffective against predatory ants that attack en masse and recruit other colony members.
4. In laboratory experiments, two possible mechanisms underlying faster development of larvae in larger groups were tested: (i) overcoming the physical toughness of host plant leaves, and (ii) social stimulus to feed. Results support the physical toughness hypothesis but not the social stimulus hypothesis.
5. Feeding in large groups by C. lacinia larvae confers multiple advantages, including protection from solitary predators and increased feeding efficiency because grouped, early-instar larvae can initiate feeding wounds on tough sunflower leaves. These advantages of larval gregariousness, coupled with reduced desiccation at the egg stage, apparently outweigh disadvantages of aggregation, such as interference and exploitative competition among larvae.     

Higher productivity at the cost of increased host-specificity when Maculinea butterfly larvae exploit ant colonies through trophallaxis rather than by predation

Abstract .1. Field studies were made of the benefits and costs of two feeding strategies in the genus Maculinea, whose final-instar larvae parasitise Myrmica ant colonies. Maculinea arion is an obligate predator of ant brood, whereas M. rebeli and M. alcon mimic ant larvae and are fed (like cuckoos) directly by the workers.
2. Samples of > 1500 Myrmica nests confirmed laboratory-based predictions that, by feeding at a lower trophic level, many (4.7-fold) more individuals of M. rebeli and M. alcon are supported per ant colony than M. arion.
3. Because of their efficient feeding, cuckoo species often occupied sites where their phytophagous early larval populations coincided to only a small extent (> 10%) with host Myrmica colonies, whereas all sites supporting M. arion had 50–100% of the phytophagous stages within foraging range of the host Myrmica species.
4. Greater host-specificity was identified as another consequence of cuckoo-feeding. The ecological cost of this is discussed .
5. The feeding of other Maculinea species had not been fully described: the data suggest that M. nausithous is a predator of ant brood and confirm that M. teleius is predacious .     

Dynamics of handling time and functional response by larvae of Chrysomya albiceps (Dipt., Calliphoridae) on different prey species

Abstract:  One way to understand the behavioural patterns exhibited by a predator in response to prey density is to evaluate its functional response. Such evaluation yields information about basic mechanisms of prey–predator dynamics, and is an essential component of prey–predator models. In this paper we analysed experimentally the functional response and the handling time spent by Chrysomya albiceps on different prey species and larval instars of blowflies. The type II functional response was observed when second instar larvae of Chrysomya megacephala and Chrysomya macellaria were consumed. The handling time spent by the predator was significantly different between instars and species. The implications of the functional response and handling time for the interaction dynamics of Brazilian Chrysomyinae species are discussed.     

Interactions with native mosquito larvae regulate the production of Aedes albopictus from bromeliads in Florida

Abstract. 1. Immatures of the invasive container mosquito Aedes albopictus occur in water-holding tanks and axils of ornamental bromeliads in Florida, where this species established and became abundant in the late 1980s and early 1990s.
2. The numbers of A. albopictus in bromeliads in gardens vary geographically in Florida, being significantly higher in northern sites where two species of Wyeomyia mosquitoes, native specialists of this microhabitat, are absent.
3. Causes of the negative relationship between abundances of A. albopictus and Wyeomyia spp. were investigated experimentally using Billbergia pyramidalis , an introduced bromeliad popular in Florida gardens.
4. Egg laying by A. albopictus in B. pyramidalis confined in a large outdoor cage was unaffected by the presence or absence of Wyeomyia spp. fourth instars, indicating that immatures of the native bromeliad mosquito species do not deter oviposition by the invasive species in this microhabitat.
5. Growth and survivorship of A. albopictus first instars in tanks of B. pyramidalis were negatively affected by the presence of fourth instar, but not first instar, Wyeomyia spp. larvae at natural densities. Stimulative effects of leaf litter on A. albopictus growth and survivorship in this microhabitat were independent of the presence or absence of Wyeomyia spp. immatures.
6. These results demonstrate that interspecific larval interactions regulate the production and explain the geographic patterns in abundance of A. albopictus from ornamental bromeliads in Florida.