Although it has always been assumed that chemical mimicry and camou£age play a major role in the penetration of ant societies by social parasites, this paper provides the ¢rst direct evidence for such a mechanism between the larvae of the parasitic butter£y 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 conspeci¢cs and brood; and (iii) the caterpillars' secretions would more closely mimic the pro¢le of their main host in the wild, M. schencki, than that of other species of Myrmica. Results of behavioural bioassays and chemical analyses con¢rmed all three hypotheses, and explained the high degree of host speci¢city 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 camou£age), making them near-perfect mimics of their individual host colony's odour.
Here we report direct evidence that cuticular hydrocarbons are responsible for nestmate recognition in Formica japonica distributing in Southern Honshu in Japan. Workers showed aggressive behavior against foreign workers but not against nestmates. A similar response was observed when a glass dummy was treated with isolated hydrocarbons from foreign workers or nestmates. Among the isolated hydrocarbons, ten hydrocarbon components were identified: five nalkanes and five (Z)-9-alkenes with odd number of carbons from 25 to 33, in different ratios in different colonies. When synthetic hydrocarbons blended in the same ratio as natural blends were presented to workers, they showed aggressive responses against foreign blends but paid less attention to those of nestmates. Neither n-alkane nor (Z)-9-alkene blends, however, caused aggression response in foreign workers. Thus, both n-alkanes and (Z)-9-alkenes are necessary to discriminate nestmates from foreign conspecifics.
Mating behavior of the scarab beetle Dasylepida ishigakiensis was observed in a sugar cane field in Miyako Is., Okinawa, Japan. In field observations of tethered females on 6 February 2002, calling behaviors were observed only within 30 min of sunset time (18:25-18:55, JST), when light intensity decreased from ca. 500 lx to 1 lx. Mating was strongly affected by temperature: adults appeared and subsequent mating occurred when the temperature at 18:00 was higher than 18°C. Females appeared from the soil, flew to settle on sugar cane leaves and commenced rhythmical abdominal expansion and contraction. Males were attracted to the calling females from leeward, landed on or near the calling female, and immediately mounted. After genital connection, the male raised his legs and suspended himself with his genitalia. Mating lasted for ca 2 h. Most mated D. ishigakiensis females neither appeared from the soil nor attracted males until the end of March, so are considered monogamous. In contrast, males appeared from the soil after mating on evenings warmer than 18°C and probably repeat mating if females are available.
The chemical signatures on the cuticles of five common Myrmica ant species were analysed (49 colonies of M. rubra, M. ruginodis, M. sabuleti, M. scabrinodis and M. schencki), each ant being the specific host of one of the five threatened European species of Maculinea butterfly. The cuticular hydrocarbon profile (based on the relative abundance of each chemical) of each ant species was highly distinctive, even between the morphologically similar species M. sabuleti and M. scabrinodis. There was no significant difference in the chemical profiles of workers and larvae from any colony. Nor was there much pattern in the intraspecific variation: colonies from the same populations were significantly, but only slightly, more similar to each other than to colonies from distant populations. M. rubra showed remarkably little variation between populations sampled widely from northern Russia, Ukraine, Scotland and southern England. The data were compared with published profiles of M. rubra and two North American Myrmica species, and with a quantitative reanalysis of data for Maculinea rebeli caterpillars. We conclude that the hydrocarbon profiles of Myrmica species are sufficiently and consistently different for chemical mimicry to explain the pattern of host specificity recorded for the European Maculinea butterflies. The optimum strategy for chemical mimicry in each of the two life-styles of Maculinea larvae is discussed: we suggest that predatory species might benefit from mimicking the median profile of their model whereas the "cuckoo" species would benefit when variation between siblings encompasses a large range of the variation recorded within a local population of the model species.
The white grub Dasylepida ishigakiensis has a 2‐year life cycle and spends approximately 9 months as a nonfeeding larva, pupa and adult on a subtropical island. Evidence is presented indicating that this beetle has two diapauses that appear to synchronize this long life cycle with the seasons. Larvae exposed to 20, 22.5, 25 and 27.5 °C late in the third (last) stadium pupate rapidly except for some individuals kept at the highest temperature. The latter pupate upon transfer to 22.5 °C, indicating that larval diapause is maintained at high temperature but terminates upon transfer to a lower temperature. Pupal development is directly temperature‐dependent in the range 20–30 °C. Adults develop reproductive organs (i.e. the ovary in females and the seminal vesicles and accessory glands in males) rapidly at 15 and 20 °C, whereas those kept at 25 °C take a long time to do so. Ovarian development is completely suppressed at 30 °C but initiated upon transfer to 20 °C. In the laboratory, males with well‐developed reproductive organs mate even with sexually immature females, whereas females with undeveloped ovaries show no sexual behaviour. Although the two diapauses of this species are thermally regulated (i.e. a characteristic commonly expressed by insects in summer diapause), adults of this beetle emerge from pupae late in the autumn and remain in the soil for 2 months. Adult diapause effectively serves to synchronize the time of sexual maturation with the coldest month of the year.
Chemical components that attract males in the laboratory were extracted from the female elytra of the white-spotted longicorn beetle, Anoplophora malasiaca (Thomson) (Coleoptera: Cerambycidae), and found to be comprised of several sesquiterpene hydrocarbons. Males located females that had fed on the bark of the host plant Citrus unshiu more frequently than those fed on an artificial diet in the laboratory. Male attraction was also confirmed in the corresponding sesquiterpene fractions of the host plant. The sesquiterpene fractions of female elytra and C. unshiu leaves showed quite similar GC profiles. In the field, the beetles were found on C. unshiu trees baited with intact females or males as frequently as those baited with the leaf extracts containing the sesquiterpenes at different purification levels. The beetles were found on those baited trees significantly more frequently than on unbaited control trees. Males, as well as females attracted both sexes, and the male elytra also contained the sesquiterpenes that were identical with those in female and C. unshiu. This indicated that active components in the elytra are acquired from C. unshiu by feeding, contact and/or adsorption. These sesquiterpenes may serve for intraspecific communication in A. malasiaca. The major sesquiterpenes from the C. unshiu leaves were isolated and elucidated by NMR analyses of four sesquiterpene hydrocarbons, b-elemene, b-caryophyllene, a-humulene, and a-farnesene.
Regulation via interspecific communication is an important for the maintenance of many mutualisms. However, mechanisms underlying the evolution of partner communication are poorly understood for many mutualisms. Here we show, in an ant-lycaenid butterfly mutualism, that attendant ants selectively learn to recognize and interact cooperatively with a partner. Workers of the ant Pristomyrmex punctatus learn to associate cuticular hydrocarbons of mutualistic Narathura japonica caterpillars with food rewards and, as a result, are more likely to tend the caterpillars. However, the workers do not learn to associate the cuticular hydrocarbons of caterpillars of a non-ant-associated lycaenid, Lycaena phlaeas, with artificial food rewards. Chemical analysis revealed cuticular hydrocarbon profiles of the mutualistic caterpillars were complex compared with those of non-ant-associated caterpillars. Our results suggest that partner-recognition based on partner-specific chemical signals and cognitive abilities of workers are important mechanisms underlying the evolution and maintenance of mutualism with ants.
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.
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