The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly

Summary Caterpillars of Maculinea arion are obligate predators of the brood of Myrmica sabuleti ants. In the aboratory, caterpillars eat the largest available ant larvae, although eggs, small larvae and prepupae are also palatable. This is an efficient way to predate. It ensures that newly-adopted caterpillars consume the final part of the first cohort of ant brood in a nest, before this pupates in early autumn and becomes unavailable as prey. At the same time, the fixed number of larvae in the second cohort is left to grow larger before being killed in late autumn and spring. Caterpillars also improve their feeding efficiency by hibernating for longer than ants in spring, losing just 6% of their weight while the biomass of ant larvae increases by 27%. Final instar caterpillars acquire more than 99% of their ultimate biomass in Myrmica nests, growing from 1.3 mg to an estimated 173 mg. A close correlation was found between the weights of caterpillars throughout autumn and the number of large ant larvae they had eaten. This was used to calculate the number of larvae eaten in spring, allowing both for the loss of caterpillar weight during winter and the increase in the size of their prey in spring. It is estimated that 230 of the largest available larvae, and a minimum nest size of 354 M. sabuleti workers, is needed to support one butterfly. Few wild M. sabuleti nests are this large: on one site, it was estimated that 85% of nests were too small to produce a butterfly, and only 5% could support two or more. This prediction was confirmed by the mortalities of 376 caterpillars in 151 wild M. sabuleti nests there. Mortalities were particularly high in nests that adopted more than two caterpillars, apparently due to scramble competition and starvation in autumn. Survival was higher than predicted in wild nests that adopted one caterpillar. These caterpillars seldom exhaust their food before spring, when there is intense competition among Myrmica for nest sites. Ants often desert their nests in the absence of brood, leaving the caterpillar behind. Vacant nests are frequently repopulated by a neighbouring colony, carrying in a fresh supply of brood. Maculinea arion caterpillars have an exceptional ability to withstand starvation, and sometimes survive to parasitize more than one Myrmica colony. Despite these adaptations, predation is an inefficient way to exploit the resources of a Myrmica nest. By contrast, Maculinea rebeli feeds mainly at a lower trophic level, on the regurgitations of worker ants. Published data show that Myrmica nests can support 6 times more caterpillars of Maculinea rebeli than of M. arion in the laboratory. This is confirmed by field data.     

Chemical disguise as particular caste of host ants in the ant inquiline parasite Niphanda fusca (Lepidoptera: Lycaenidae)

The exploitation of parental care is common in avian and insect 'cuckoos' and these species engage in a coevolutionary arms race. Caterpillars of the lycaenid butterfly Niphanda fusca develop as parasites inside the nests of host ants (Camponotus japonicus) where they grow by feeding on the worker trophallaxis. We hypothesized that N. fusca caterpillars chemically mimic host larvae, or some particular castes of the host ant, so that the caterpillars are accepted and cared for by the host workers. Behaviourally, it was observed that the host workers enthusiastically tended glass dummies coated with the cuticular chemicals of larvae or males and those of N. fusca caterpillars living together. Cuticular chemical analyses revealed that N. fusca caterpillars grown in a host ant nest acquired a colony-specific blend of cuticular hydrocarbons (CHCs). Furthermore, the CHC profiles of the N. fusca caterpillars were particularly close to those of the males rather than those of the host larvae and the others. We suggest that N. fusca caterpillars exploit worker care by matching their cuticular profile to that of the host males, since the males are fed by trophallaxis with workers in their natal nests for approximately ten months.     

The effect of queen ants on the survival of Maculinea arion larvae in Myrmica ant nests

Summary The mortality of Maculinea arion caterpillars was measured in both laboratory and wild Myrmica nests, and found to be nearly 3 times higher in nests that had queen ants present. This is attributed to queen effect, which causes worker ants in nests with queens to attack large ant larvae (gynes) that would otherwise develop into new queens. Maculinea arion caterpillars mimic Myrmica larvae, and are usually attacked during the first 10 days after adoption, when they pass through the size range of ant gyne larvae. Caterpillars are also likely to be attacked during this period because their nethod of feeding brings them into close contact with the skins of large ant larvae, which contain gyne larval pheromones; older caterpillars are large enough to eat larvae without their exposed surfaces contacting the larval skin. In the wild, many caterpillars of Maculinea arion die in ant nests, and this has been shown in previous work to be the key factor that determines changes in their abundance from year to year. It is suggested that queen effect can be an important cause of these deaths, and one that particularly affects populations of butterflies that breed on sites with long-established plagioclimaxes of short turf rather than short-lived grass-land successions.     

Chemical mimicry and host specificity in the butterfly Maculinea rebeli,a social parasite of Myrmica ant colonies

Although it has always been assumed that chemical mimicry and camouflage play a major role in the penetration of ant societies by social parasites, this paper provides the first direct evidence for such a mechanism between the larvae of the parasitic butterfly Maculinea rebeli and its ant host Myrmica schencki. In the wild, freshly moulted fourth-instar caterpillars, which have no previous contact with ants, appear to be recognized as ant larvae by foraging Myrmica workers, which return them to their nest brood chambers. Three hypotheses concerning the mechanism controlling this behaviour were tested: (i) the caterpillars produce surface chemicals that allow them to be treated as ant larvae; (ii) mimetic compounds would include hydrocarbons similar to those employed by Myrmica to recognize conspecifics and brood; and (iii) the caterpillars'' secretions would more closely mimic the profile of their main host in the wild, M. schencki, than that of other species of Myrmica. Results of behavioural bioassays and chemical analyses confirmed all three hypotheses, and explained the high degree of host specificity found in this type of highly specialized myrmecophile. Furthermore, although caterpillars biosynthesized many of the recognition pheromones of their host species (chemical mimicry), they later acquired additional hydrocarbons within the ant nest (chemical camouflage), making them near-perfect mimics of their individual host colony''s odour.     

THE COMPONENTS OF KIN COMPETITION

It is well known that competition among kin alters the rate and often the direction of evolution in subdivided populations. Yet much remains unclear about the ecological and demographic causes of kin competition, or what role life cycle plays in promoting or ameliorating its effects. Using the multilevel Price equation, I derive a general equation for evolution in structured populations under an arbitrary intensity of kin competition. This equation partitions the effects of selection and demography, and recovers numerous previous models as special cases. I quantify the degree of kin competition, α, which explicitly depends on life cycle. I show how life cycle and demographic assumptions can be incorporated into kin selection models via α, revealing life cycles that are more or less permissive of altruism. As an example, I give closed‐form results for Hamilton's rule in a three‐stage life cycle. Although results are sensitive to life cycle in general, I identify three demographic conditions that give life cycle invariant results. Under the infinite island model, α is a function of the scale of density regulation and dispersal rate, effectively disentangling these two phenomena. Population viscosity per se does not impede kin selection.     

Determinants of predation on phytophagous insects: the importance of diet breadth

To evaluate the role of predation in the evolution of diet specialization and to determine the effectiveness of various larval defenses, we offered lepidopteran larvae to colonies of the tropical ant Paraponera clavata. We recorded behavioral and physical characteristics of prey items and used log-linear models to analyze their importance as deterrents to predation by P. clavata. The most important determinant of probability of prey rejection by P. clavata was a prey's diet breadth; specialists were rejected by the ants significantly more than generalists. Other less important, but significant, predictors of prey rejection included ontogeny, morphology and chemistry. Late instar caterpillars were rejected more frequently than early instars, hairy caterpillars were rejected more frequently than caterpillars with other morphologies, and one caterpillar species with an unpalatable extract was rejected more frequently than two species with palatable extracts.     

Evolution of influence: signaling in a lycaenid-ant interaction

Some phytophagous insects gain defense from natural enemies by associating with otherwise potentially harmful top predators. Many lycaenid butterfly caterpillars are involved in such interactions with ants: larvae provide carbohydrate rewards from the dorsal nectary organ (DNO) to associated ants in return for protection from natural enemies. The stability of these interactions involves signals that identify the lycaenid caterpillar as a mutualist. However, larvae of some lycaenid species, such as Lycaena xanthoides, are found in close association with ants but do not possess the reward producing DNO. Evaluating the relationship in a phylogenetic framework, we show that the association between L. xanthoides and ants likely evolved from a non-ant-associated ancestor. Behavioral trials also show that L. xanthoides larvae are capable of influencing ant behavior to increase ant tending when faced with a simulated predator attack, without providing DNO-derived rewards to ant associates. These results demonstrate that the DNO is not necessary to maintain associations between lycaenid larvae and ants. Third-party interactions may affect the evolution of mutualisms and consideration of underlying evolutionary history is necessary to understand contemporary species associations.     

Kin discrimination and altruism in the larvae of a solitary insect

Kin selection theory predicts altruism between related individuals, which requires the ability to recognize kin from non-kin. In insects, kin discrimination associated with altruistic behaviour is well-known in clonal and social species but in very few solitary insects. Here, we report that the solitary larvae of a non-social insect Aleochara bilineata Gyll. (Coleoptera; Staphylinidae) show kin discrimination and sibling-directed altruistic behaviour. Larvae superparasitize more frequently the hosts parasitized by non-kin individuals than those hosts parasitized by siblings. Kin discrimination probably occurs by self-referent phenotype matching, where an individual compares its own phenotype with that of a non-familiar related individual, a mechanism rarely demonstrated in animals. The label used to recognize kin from non-kin corresponds to substances contained in the plug placed on the hosts by the resident larvae during the parasitization process. Kin competition induced by a limited larval dispersion may have favoured the evolution of kin recognition in this solitary species.     

Contest competition among Maculinea rebeli butterfly larvae in ant nests

Abstract.

• 1 Caterpillars of the myrmecophilous butterfly Maculinea rebeli showed strong evidence of contest competition when introduced at high densities to laboratory nests of Myrmica ants.
• 2 This is attributed to the direct feeding of caterpillars by workers, which select a few individuals to nurture when food or ant numbers are limiting. It contrasts with published data for a congener, Maculinea arion, which has predacious larvae and experiences scramble competition in crowded ant nests.
• 3 Worker ants from two Myrmica rubra colonies (I and II) were used to found the laboratory nests hosting Maculinea rebeli. Nests from each source reared a similar biomass of Maculinea, but whereas those containing M. rubra I workers reared eight to ten lightweight caterpillars each, cultures from colony II reared half as many caterpillars, each of about double the weight.
• 4 Differences in nest capacity may be due to the different social structures of colonies I and II at the start of the experiment.

     

Florivorous myrmecophilous caterpillars exploit an ant–plant mutualism and distract ants from extrafloral nectaries

Females of myrmecophilous butterflies tend to oviposit in plants visited by ant species that engage in stable associations with its larvae. In Banisteriopsis malifolia, caterpillars are attended by the same ants that feed on extrafloral nectaries. A conflict may arise when both the plant and caterpillars compete for ant attention, and ants are assumed to forage on the highest quality resource. By attending caterpillars, ants can be indirectly detrimental to plant fitness because florivorous larvae feed intensively until pupation. In this study, we specifically investigated (i) whether the occurrence of facultative myrmecophilous Synargis calyce (Riodinidae) caterpillars in B. malifolia was based on ant species (Camponotus blandus or Ectatomma tuberculatum) and abundance; (ii) the monopolization of ants by the butterfly larvae and (iii) the florivory rates incurred by the caterpillars on inflorescences. The abundance of S. calyce was six‐fold greater in plants with C. blandus, compared to E. tuberculatum treatments. Caterpillars monopolized up to 50% of C. blandus on the plants, indicating that the resources offered by S. calyce were more attractive to ants than extrafloral nectaries. Florivory by riodinids incurred losses of almost 60% of flower buds. Myrmecophilous riodinids exploited an ant–plant mutualism by attracting aggressive ants that become larvae bodyguards. Thus, this ecological interaction is potentially detrimental to B. malifolia, since the ants, which can provide protection against herbivores, shift to provide defence for one of these herbivores.     

Absence of kin discrimination in a ponerine ant

Kinship theory implies that individual social Hymenoptera should be able to identify kin. We tested kin discrimination in the polygynous ponerine ant Gnamptogenys striatula. Mate choice experiments showed that individuals did not pair according to kinship. Experiments on matriline discrimination revealed that workers did not preferentially groom, transport (after nest disturbance) or cannibalize (after starvation) larvae on the basis of kin, when both related and unrelated larvae were present. These results show the absence of kin discrimination for the criteria and experimental conditions used. The lack of kin discrimination during mate choice in G. striatula can be explained by male dispersion and female philopatry, which reduces the likelihood of mating between siblings and of kin-based mate choice reflected in incest avoidance. The lack of matriline discrimination by workers may reflect permanent intracolony mutualism or the high cost of discrimination. Finally, it appears that the absence of kin discrimination in such contexts in G. striatula is not incompatible with kinship theory and may have been secondarily selected during social evolution. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Kin recognition in immatures of <Emphasis Type="Italic">Heliconius erato phyllis</Emphasis> (Lepidoptera; Nymphalidae)

Females of the neotropical butterfly Heliconius erato phyllis lay eggs individually, which, after hatching into caterpillars, can be cannibalistic towards neighboring eggs. Laboratory experiments were conducted to test for kin recognition between first instar caterpillars and eggs. Two experiments were performed, putting three eggs in the vertices of an equilateral triangle made of green paper with side length of 0.5 cm. In the first experiment, two of the three eggs were full siblings; in the second experiment, one group consisted of three eggs from three independent nonrelated females, and in the other group all three eggs were full siblings. The frequency of cannibalism in experiment 1 (SSN, sibling–sibling–nonsibling) was 66% for nonrelated eggs and 34% for sibling eggs (P = 0.0018). In experiment 2, in group NNN (three nonsibling eggs) it was 83%, and for group SSS (three sibling eggs), the frequency of cannibalism was 53% (P < 0.0001). These results indicate kin recognition (caterpillar–egg). This recognition may have been important in the evolution of some of the butterfly’s adaptations, and possibly as an opportunity for kin selection.     

Intra- and interspecific competition and host race formation in the apple maggot fly,Rhagoletis pomonella (Diptera: Tephritidae)

Intra- and interspecific resource competition are potentially important factors affecting host plant use by phytophagous insects. In particular, escape from competitors could mediate a successful host shift by compensating for decreased feeding performance on a new plant. Here, we examine the question of host plant-dependent competition for apple (Malus pumila)- and hawthorn (Crataegus mollis)-infesting larvae of the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae) at a field site near Grant, Michigan, USA. Interspecific competition from tortricid (Cydia pomonella, Grapholita prunivora, and Grapholita packardi) and agonoxenid (subfamily Blastodacninae) caterpillars and a curculionid weevil (Conotrachelus crataegi) was much stronger for R. pomonella larvae infesting the ancestral host hawthorn than the derived host apple. Egg to pupal survivorship was estimated as 52.8% for fly larvae infesting hawthorn fruit without caterpillars and weevils compared to only 27.3% for larvae in harthorns with interspecific insects. Survivorship was essentially the same between fly larvae infesting apples in the presence (44.8%) or absence (42.6%) of interspecific insects. Intraspecific competition among maggots was also stronger in hawthorns than apples. The order or time that a larva exited a hawthorn fruit was a significant determinant of its pupal mass, with earlier emerging larvae being heavier than later emerging larvae. This was not the case for larvae in apples, as the order or time that a larva exited an apple fruit had relatively little influence on its pupal mass. Our findings suggest that decreased performance related to host plant chemistry/nutrition may restrict host range expansion and race formation in R. pomonella to those plants where biotic/ecological factors (i.e. escape from competitors and parasitoids) adequately balance the survivorship equation. This balance permits stable fly populations to persist on novel plants, setting the stage for the evolution of host specialization under certain mitigating conditions (e.g. when mating is host specific and host-associated fitness trade-offs exist).     

Do Maculinea rebeli caterpillars provide vestigial mutualistic benefits to ants when living as social parasites inside Myrmica ant nests?

Caterpillars of the lycaenid butterfly Maculinea rebeli Hirschke (Lepidoptera: Lycaenidae) live for 11–23 months as social parasites in Myrmica (Hymenoptera: Formicidae) red ant nests, a trait that is believed to have evolved from mutualistic myrmecophilous ancestry. Although Maculinea rebeli caterpillars harm Myrmica larvae, they simultaneously produce copious secretions which the adult worker ants imbibe, perhaps representing a vestige of the ancestral mutualism. We report the results of laboratory experiments designed to test alternative hypotheses: (i) Maculinea rebeli caterpillars provide a beneficial source of sugar in return for being tended by Myrmicaworkers; (ii) Maculinea rebeli harms its host by stressing the workers by competing for available sugar. Comparisons were made of Myrmica worker fitness after 90–450 days under all possible combinations of three experimental treatments: ± M. rebeli caterpillars, ± sucrose and ± ant brood. Caterpillars always reduced the survival of both ant workers and their larvae, even when sugar was not provided, suggesting that M. rebeli is wholly parasitic on all stages in its host colony. The results also confirmed the importance of sucrose in the diet of Myrmica, and showed that M. rebeli caterpillars which eat ant brood to supplement their normal trophallactic feeding by workers develop more quickly - but have the same survival and pupal weights – as caterpillars that are fed solely by worker ants.     

Ants benefit from attending facultatively myrmecophilous Lycaenidae caterpillars: evidence from a survival study

Workers of three ant species (Lasius niger, Lasius flavus, Myrmica rubra) were caged in the laboratory together with caterpillars and pupae of five species of lycaenid butterflies. Mortality of ants was 3–5 times higher when the ants were confined with larvae lacking a dorsal nectar organ (Lycaena phlaeas, Lycaena tityrus) rather than with caterpillars which possess a nectar gland (Aricia agestis, Polyommatus bellargus, P. icarus). For all five species, ant survival was always lower at the pupal stage (where a nectar organ is always absent) than at the caterpillar stage and was largely equivalent for the butterfly species tested. The experimental data confirm earlier estimates that ants can derive nutritive benefits from tending facultatively myrmecophilous lycaenid caterpillars, even though these caterpillars produce nectarlike secretions at low rates.     

Myrmecophily in Hesperiidae. The case of Vettius tertianus in ant gardens

The larvae of the hesperiid butterfly Vettius tertianus develop by eating the leaves of Aechmea mertensii, a bromeliad epiphyte restricted to ant gardens. The relationships between ants and V. tertianus larvae highlight the preferential association of the caterpillars with Pachycondyla goeldii (Ponerinae), an ant-garden initiator. The oviposition strategy of V. tertianus may thus imply the identification of the inhabiting ant species and not only the identification of the host plant. The caterpillars neither provide secretions to the ants, nor possess defensive devices (i.e. hairs or appendices) against ants. Their activity rhythm does not isolate them from foraging workers of P. goeldii and their shelters are also attainable by the ants. Moreover, as the cuticular lipid profiles of V. tertianus larvae are clearly different from those of the ants and also from the leaf-surface of A. mertensii, acceptance is not due to mimicry between larvae and plants or ants. However, the caterpillars deposit, on the leaf they eat, silk containing a mixture of substances very similar to those found on their own cuticle. No interaction with ants was recorded during observations, even though the ant gardens were patrolled by numerous P. goeldii individuals during their activity period. But when confronted with the caterpillar, none of the tested ant species reacted aggressively. These results suggest the existence of compounds, other than cuticular lipids, responsible for the absence of aggressiveness in the ants. The case of V. tertianus is relatively new as myrmecophily within Hesperiidae has been described only once. Moreover, it preferentially involves a member of the Ponerinae, a subfamily in which interactions with other arthropods are exceptional.     

The effect of plant chemistry on the acceptability of caterpillar prey to the argentine antIridomyrmex humilils (Hymenoptera: Formicidae)

Experiments were performed to test the acceptability of two palatable, cryptic caterpillars, the tobacco hornworm,Manduca sexta, and the cabbage looper,Trichoplusia ni, reared on different diets, to the Argentine ant,Iridomyrmex humilis. Ants preferred larvae reared on artificial diet, groundcherry, or cowpea to tobacco-reared larvae. Ants also preferred larvae reared on artificial diet without nicotine to larvae reared on diet containing nicotine (5% dry wt). Experiments were also performed to test the response of ants to larval extracts and chemicals applied to the surface of palatable prey. Ants did not respond differently to larvae of the potato tuber moth,Phthorimaea operculella, treated with larval extracts or regurgitate from tobacco-reared larvae compared to artificialdiet-reared larvae, but ants were deterred byP. operculella larvae treated with nicotine compared to untreated larvae. The results of this study indicate that caterpillars can derive at least some degree of chemical protection from their food plant without sequestering and storing plant compounds and without the development of elaborate aposematic characteristics.     

Behavioural ecology of defence in a risky environment: caterpillars versus ants in a Neotropical savanna

1. Predatory ants may reduce infestation by herbivorous insects, and slow‐moving Lepidopteran larvae are often vulnerable on foliage. We investigate whether caterpillars with morphological or behavioural defences have decreased risk of falling prey to ants, and if defence traits mediate host plant use in ant‐rich cerrado savanna. 2. Caterpillars were surveyed in four cerrado localities in southeast Brazil (70–460 km apart). The efficacy of caterpillar defensive traits against predation by two common ant species (Camponotus crassus, C. renggeri) was assessed through experimental trials using caterpillars of different species and captive ant colonies. 3. Although ant presence can reduce caterpillar infestation, the ants' predatory effects depend on caterpillar defence traits. Shelter construction and morphological defences can prevent ant attacks (primary defence), but once exposed or discovered by ants, caterpillars rely on their size and/or behaviour to survive (secondary defence). 4. Defence efficiency depends on ant identity: C. renggeri was more aggressive and lethal to caterpillars than C. crassus. Caterpillars without morphological defences or inside open shelters were found on plants with decreased ant numbers. No unsheltered caterpillar was found on plants with extrafloral nectaries (EFNs). Caterpillars using EFN‐bearing plants lived in closed shelters or presented morphological defences (hairs, spines), and were less frequently attacked by ants during trials. 5. The efficiency of defences against ants is thus crucial for caterpillar survival and determines host plant use by lepidopterans in cerrado. Our study highlights the effect of EFN‐mediated ant‐plant interactions on host plant use by insect herbivores, emphasizing the importance of a tritrophic viewpoint in risky environments.     

Competition between the gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids

The gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis, overlap geographically as well as in their host ranges. Adult female swallowtails are incapable of distinguishing between damaged and undamaged leaves, and the opportunities for competition between these two species are numerous. We designed field and laboratory experiments to look for evidence of indirect competition between P. canadensis and L. dispar larvae. Swallowtail caterpillars were reared in the laboratory on leaves from gypsy-moth-defoliated and undefoliated trees to explore host-plant effects. We tested for pathogen-mediated interactions by rearing swallowtail larvae on both sterilized and unsterilized leaves from defoliated and undefoliated sources. In addition, we measured the effects of known gypsy moth pathogens, as well as gypsy moth body fluids, on the growth and survival of swallowtail larvae. Field experiments were designed to detect the presence of parasitoid-mediated competition, as well: we recorded parasitism of swallowtail caterpillars placed in the field either where there were no gypsy moth larvae present, or where we had artificially created dense gypsy moth populations. We found evidence that swallowtails were negatively affected by gypsy moths in several ways: defoliation by gypsy moths depressed swallowtail growth rate and survival, whether leaves were sterilized or not; sterilization significantly reduced the effect of defoliation, and gypsy moth body fluids proved lethal; and swallowtail caterpillars suffered significantly increased rates of parasitism when they were placed in the field near gypsy moth infestations.     

Mutualism between Thisbe irenea butterflies and ants, and the role of ant ecology in the evolution of larval-ant associations

A facultative mutualism between the riodinid butterfly Thisbe irenea and the ponerine ant Ectatomma ruidum is described from Panama. Ants protect larvae against attacks of predatory wasps, but not against tachinid parasitoids. Several potential sources of ecological variation affecting the larval survival of Thisbe irenea are noted. A preliminary means of testing the ability of larvae to appease ants is described that may be applied to all butterfly-ant systems. Observations and literature records indicate that ant taxa which tend butterfly larvae are the same taxa that tend extrafloral nectaries and Homoptera. A general hypothesis for the evolution of myrmecophily among butterflies suggests that ant taxa which utilize secretions in their diet are major selective agents for the evolution of the larval ant-organs, and hence, ant-larval mutualisms. This idea is extended to suggest how appeasement of predaceous ant taxa through the use of larval ant-organs can influence an ant-larval relationship, eventually leading to mutualism.