Host-Specific Myrmecophily and Myrmecophagy in the Tropical Coccinellid Diomus thoracicus in French Guiana (original) (raw)
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Host-specific myrmecophily and myrmecophagy in the tropical coccinellid Diomus thoracicus
HAL (Le Centre pour la Communication Scientifique Directe), 2010
A variety of arthropods, particularly insects, have developed myrmecophilous interactions with ants to gain access to resources and/or for protection. Among these myrmecophiles, only a few examples have been documented in the Coccinellidae, most of them involving species able to feed on ant-tended Hemiptera. We report here a new case of obligate myrmecophily in the coccinellid Diomus thoracicus. Larvae are invariably and exclusively found in the nests of the ant Wasmannia auropunctata and seem to rely on ant brood as their only food source. Not only do ant workers show no aggressiveness toward the D. thoracicus larvae in their behavioral interactions at the colonial level, but also at the species level; while coccinellid adults are always attacked. The integration of the larvae inside of the ant nests is based on their chemical mimicry of the host's cuticular cues. Therefore, given the presence of the D. thoracicus larvae inside of the ant's nest, their predation on Wasmannia brood and their chemical mimicry, this species can be considered a specific parasite of W. auropunctata. Overall, this new case of myrmecophily not only specifically involves a highly invasive ant species, but also provides insights into the evolution of myrmecophily and myrmecophagy in coccinellids.
Proceedings of the Royal Society of London. Series B: Biological Sciences, 1999
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.
Host specificity pattern and chemical deception in a social parasite of ants
Scientific Reports
In natural ecosystems, relationships between organisms are often characterised by high levels of complexity, where vulnerabilities in multi-trophic systems are difficult to identify, yet variation in specific community modules can be traceable. Within the complex community interactions, we can shed new light on dynamics by which co-evolutionary outcomes can inform science-led conservation. Here we assessed host-ant use in six populations of the butterfly Phengaris (=Maculinea) rebeli, an obligate social parasite of Myrmica ants and a model system in evolutionary and conservation ecology. Starting from the initial distribution of eggs, we estimated the survival of the parasite in the wild in nests of seven Myrmica ant species, and analysed the chemical cues evolved by the parasites to subvert its host defences. We found local variations in host specificity that are consistent with similarities found in the chemical profiles of hosts and parasites on different sites. At some sites, only one ant species is successfully exploited; at others, multiple-host populations are used. Understanding how stable or adaptable these associations are is essential knowledge when devising conservation measures to maintain keystone species of ant and locally adapted populations of Phengaris butterfly species, which are rare, threatened and a high priority for conservation worldwide. Although many generalist insect species can respond rapidly to environmental changes 1,2 , closely-coupled assemblages of interacting specialists are often more vulnerable, because survival may depend upon the maintenance of obligate co-adaptations or interactions within the community 3. An estimated ~100000 species of insect are myrmecophiles that interact with ants 4 ; most being facultative, often mutualistic, and displaying similar diffuse co-evolutionary patterns. About 10000 species are obligatory myrmecophiles, including many with antagonistic interactions in the form of social parasitism, where we expect to find tighter co-evolution between parasite and host, potentially in a geographical mosaic 5,6. The European Phengaris (=Maculinea) (P. arion, P. teleius, P. nausithous, P. alcon, P. rebeli-we considered the two latter taxa as separate following 7) are already the most studied ant-parasitic butterflies, and have become a model system in evolutionary and conservation ecology 8. P. rebeli adults, the focal species of this study, are on the wing from late June to mid-July and females oviposit on Gentiana cruciata. About four days after egg-laying, P. rebeli larvae hatch and feed for 10-14 days on their specific food plant. After the third moult, larvae leave the plant and drop to the ground where they are found by a Myrmica worker and carried into an ant nest 9. The adoption of caterpillars by ants is primarily mediated by chemical deception 6,10-13. As demonstrated for P. rebeli in SouthWestern Europe, pre-adoption caterpillars synthesise a simple mixture of surface hydrocarbons that weakly mimics those of Myrmica species in general, but has the closest match to the hydrocarbon signature of its host ant M. schencki 14. Yet the low level of chemical similarity, coupled with poor discrimination by foraging workers, means that P. rebeli pre-adoption caterpillars are retrieved into nests by workers of any foraging Myrmica species that happen to encounter them 10,11,14,15. Once inside ant colonies, the mimetic cocktail of hydrocarbons synthesised by caterpillars becomes more complex 11,15,16 , which, aided by acoustical mimicry 17-19 , not only enables the parasites to integrate closely with the societies of their primary ant host species but also identifies them as intruders to "non-host" species, where, in due course, either all or the large majority of individuals are killed or ejected by the more discriminatory nurse-workers 11,15,20,21 .
Declassifying myrmecophily in the Coleoptera to promote the study of ant-beetle symbioses
Psyche
The symbiotic associations between beetles and ants have been observed in at least 35 beetle families. Among myrmecophiles, beetles exhibit the most diverse behavioral and morphological adaptations to a life with ants. These various associations have historically been grouped into discrete but overlapping behavioral categories, many of which are still used in the modern literature. While these behavioral classifications provide a rich foundation for the study of ant-beetle symbioses, the application of these systems in future studies may be less than effective. Since morphological characteristics often provide the only information of myrmecophilous beetles, they should be studied in a species-by-species fashion, as behavioral data are often limited or unavailable. Similarly, behavioral studies should focus on the target species at hand, avoiding discrete classification schemes. I formally propose the rejection of any classification scheme, in order to promote future studies of myrmecophily in both taxonomic and evolutionary studies.
Three beetles—three concepts. Different defensive strategies of congeneric myrmecophilous beetles
Behavioral Ecology and Sociobiology, 2011
Myrmecophiles, i.e., organisms associated with ants live in a variety of ecological niches in the vicinity or inside ant colonies and employ different strategies to survive ant encounters. Because different niches are characterized by different encounter rates with host ants, strategies used to avoid ant aggressions should depend on these niches. This hypothesis was studied with three rove beetle species of the genus Pella, which are myrmecophiles of the ant Lasius fuliginosus and the non-myrmecophilous relative Drusilla canaliculata. Behavioral tests in the field revealed that Pella species are better adapted to interactions with ants than D. canaliculata, but that they use speciesspecific strategies in ant interactions. Pella cognata and Pella funesta avoid encounters with ants by swift movements. Chemical analyses of the defensive tergal gland secretions showed that P. cognata has replaced the aggression inducing undecane by the behaviorally neutral tridecane. P. funesta repels the ants by releasing the panic alarm pheromone sulcatone from its tergal gland resulting in an "ant free space" around the beetles. Finally, Pella laticollis uses a specific and unique appeasing behavior. Behavioral and chemical data did not reveal any indication for the mimicry of the ants" cuticular hydrocarbon profiles by any of the beetle species. It is discussed that the employed strategies correlate with the ecological niches of the beetles. P. cognata and P. funesta are living along ant trails with ample space to escape and the employed strategies are probably sufficient to escape from dangerous conflicts. In contrast, P. laticollis lives in refuse areas of ant nests with frequent ant encounters, and its appeasement strategy allows it to stay at the encounter site.
Ethology Ecology & Evolution, 2009
Siagona europaea Dejean 1826, a carabid beetle living in clay soils of Mediterranean open lands, has been found to be an exclusive ant predator. Some morphological variations in body form are evidently adaptations to the habitat, favouring in the meantime the myrmecophagous life style. After capturing an ant, the beetle waves the prey held in its mandibles all around its dorsal forebody by arching its head and pronotum; the ants apparently spray a secretion over the beetle while being waved. The cuticular profile of beetles without contact with ants, beetles after capture and consumption of ants and of two ant species, Tapinoma nigerrimum and Messor capitatus, was recorded. Gas chromatography analyses revealed that more component are present on the carabid cuticle after predation and that they correspond to those of the tested ants. We suggest that this may be an intermediate evolutionary stage towards a true myrmecophilous life style as present in other tropical carabids. Moreover behavioural tests proved the diet (ants) which the beetle was fed triggers different reactions in ants of the same, or of a different, species. key word: cuticular profile, ants, myrmecophagy, carabid beetles.
A temporary social parasite of tropical plant-ants improves the fitness of a myrmecophyte
Naturwissenschaften, 2010
Myrmecophytes offer plant-ants a nesting place in exchange for protection from their enemies, particularly defoliators. These obligate ant–plant mutualisms are common model systems for studying factors that allow horizontally transmitted mutualisms to persist since parasites of ant–myrmecophyte mutualisms exploit the rewards provided by host plants whilst providing no protection in return. In pioneer formations in French Guiana, Azteca alfari and Azteca ovaticeps are known to be mutualists of myrmecophytic Cecropia (Cecropia ants). Here, we show that Azteca andreae, whose colonies build carton nests on myrmecophytic Cecropia, is not a parasite of Azteca–Cecropia mutualisms nor is it a temporary social parasite of A. alfari; it is, however, a temporary social parasite of A. ovaticeps. Contrarily to the two mutualistic Azteca species that are only occasional predators feeding mostly on hemipteran honeydew and food bodies provided by the host trees, A. andreae workers, which also attend hemipterans, do not exploit the food bodies. Rather, they employ an effective hunting technique where the leaf margins are fringed with ambushing workers, waiting for insects to alight. As a result, the host trees’ fitness is not affected as A. andreae colonies protect their foliage better than do mutualistic Azteca species resulting in greater fruit production. Yet, contrarily to mutualistic Azteca, when host tree development does not keep pace with colony growth, A. andreae workers forage on surrounding plants; the colonies can even move to a non-Cecropia tree.
Myrmica ants host highly diverse parasitic communities: from social parasites to microbes
Insectes Sociaux, 2014
Myrmica ants have been model species for studies in a variety of disciplines, including insect physiology, chemical communication, ant social dynamics, ant population, community ecology, and ant interactions with other organisms. Species belonging to the genus Myrmica can be found in virtually every habitat within the temperate regions of the northern hemisphere and their biology and systematics have been thoroughly studied. These ants serve as hosts to highly diverse parasitic organisms from socially parasitic butterfly caterpillars to microbes, and many Myrmica species even evolved into parasitizing species of their own genus. These parasites have various impacts both on the individuals and on the social structure of their hosts, ranging from morphological malformations to reduction in colony fitness. A comprehensive review of the parasitic organisms supported by Myrmica and the effects of these organisms on individuals and on whole ant colonies has not yet been compiled. Here, we provide a review of the interactions of these organisms with Myrmica ants by discussing host and parasite functional, behavioral or physiological adaptations. In addition, for all "symbiont groups" of Myrmica ants described in this paper, we examine the present limitations of the knowledge at present of their impact on individuals and host colony fitness. In conclusion, we argue that Myrmica ants serve as remarkable resource for the evolution of a wide variety of associated organisms.
Journal of Insect Conservation, 2011
Larvae of the obligate myrmecophilous social parasite Maculinea alcon (Lepidoptera: Lycaenidae) were found exclusively using Myrmica aloba (Hymenoptera: Formicidae) ant hosts in NE-Portugal. This is the first record of the host ant usage of any Maculinea species in Portugal, and of any Maculinea using M. aloba nests. These results on such peripheral European populations confirm that knowledge of the local host ant species is crucial for the successful protection of these endangered butterflies, and vital for examining the evolution of such interactions.