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

Abstract

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 Myrmica workers; (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.

Interspecific differences in cuticular hydrocarbon profiles of Myrmica ants are sufficiently consistent to explain host specificity by Maculinea (large blue) butterflies

“…In the case of M. rebeli, a "chemically insignificant" signal at adoption followed by active synthesis of species-specific hydrocarbons would explain why: (1) despite apparently successful adoption by other species so few caterpillars survive to maturity in non-host ant species' nests (Elmes et al 1991b;Thomas and Elmes 1998); (2) why certain individuals are preferred by host ants to others when too many caterpillars are adopted ) -by chance some are better "matched" to a particular host colony; (3) why some caterpillars take a "first meal" of ant larvae before being fully accepted by the host ants (Wardlaw et al 2000) -perhaps a quick source of energy "kick-starts" the chemical activity; (4) why in the laboratory, M. rubra and some M. ruginodis colonies generally integrate with caterpillars more readily than M. sabuleti and M. scabrinodis (Elmes et al 1991b) -the profiles of M. rubra and M. ruginodis are closer to those of M. schencki (Fig. 1B); and (5) why in the wild, very small numbers of Maculinea rebeli survive with non-host species but never with Myrmica sabuleti, even though M. sabuleti adopts the majority of M. rebeli larvae Thomas et al 1997) -M. sabuleti is the most chemically distinct species from M. schencki (Fig.…”

Phylogeny ofMaculineablues (Lepidoptera: Lycaenidae) based on morphological and ecological characters: evolution of parasitic myrmecophily

“…In contrast to the vast majority of myrmecophilous lycaenid butterflies who receive protection from ants, Maculinea species have evolved an intricate form of nest parasitism. Their early larval instars are mono‐ to oligophagous feeders on flowers and developing seeds of herbs, but later parasitize the nests of ant genera Myrmica Latreille, 1804, and Aphaenogaster Mayr, 1853 (see, e.g., Fiedler, 1991; Wardlaw et al., 2000). This ecological complex has attracted much research on butterfly myrmecophily (e.g., Hochberg et al., 1994; Fiedler, 1998; Akino et al., 1999; Pierce et al., 2002).…”

Differences in oviposition strategies between two ecotypes of the endangered myrmecophilous butterfly Maculinea alcon (Lepidoptera: Lycaenidae) under unique syntopic conditions

“…In the ant nest, they either feed on the ant brood (predatory species like Maculinea teleius Bergsträsser, 1779, Maculinea nausithous Bergsträsser, 1779 and Maculinea arion Linnaeus, 1758), or they are fed by the ant workers (cuckoo species like Maculinea alcon Denis & Schiffermüller, 1775 and Maculinea ‘ rebeli ’ Hirsche, 1904; see Elmes et al ., ; Thomas & Wardlaw, ). After spending most of the next year (or 2 years) in the ant nest, and gaining about 98% of their final biomass, they pupate during summer (Thomas et al ., ; Wardlaw et al ., ; Elmes et al ., ). This lifestyle make Maculinea species a perfect candidate for studies of evolutionary and behavioural ecology (e.g., Thomas & Elmes, ; Als et al ., ; Van Dyck & Regniers, ; Jansen et al ., ; Ugelvig et al ., ; Sielezniew et al ., ).…”