The Natural History of Caterpillar-Ant Associations

Abstract

The caterpillars of many Lepidoptera are neither attacked nor tended by ants but nevertheless appear to be obligately ant-associated and benefit from the enemy-free space created by ants. Obligate myrmecophiles that do not attract ants through stridulatory or chemical signaling are limited to habitats where ants are reliably present for other reasons, either among ant-attended hemipterans, on ant-plants, or around ant nests. Particularly in the tropics, obligate ant associates that passively coexist with ants are more diverse than previously recognized, including, for example, hundreds of African species in the lycaenid subfamily Poritiinae. Mutualists and parasites of ants have been reported in eleven families: Tineidae, Tortricidae, Cyclotornidae, Coleophoridae, Crambidae, Erebidae, Notodontidae, Hesperiidae, Pieridae, Lycaenidae, and Riodinidae. Altogether, myrmecophily has originated at least 30 times in Lepidoptera, and many groups may remain undiscovered. The butterfly families Lycaenidae and Riodinidae contain the vast majority of ant-associated species: larvae of at least 3841 (71%) of the ~5390 described Lycaenidae and 308 (20%) of the ~1562 described Riodinidae are known or inferred to be ant-associated, and both families possess specialized, convergently developed exocrine glands and stridulatory devices to communicate with ants. Many caterpillar-ant relationships previously characterized as mutualisms may actually be parasitic, as caterpillars can manipulate ants and ultimately exert a fitness cost. In the family Lycaenidae, highly specialized and obligate ant associations are found largely in the Old World tropics, Australia, and Southern Africa, where the stoichiometry of soil micronutrients, particularly sodium and phosphorus, climate, host plants, and geography may all selectively shape caterpillar-ant associations.

Phylogeny of the Poritiinae (Lepidoptera: Lycaenidae), butterflies with ant associations and unusual lichenivorous diets

“…The paucity of available life history data does not allow evolutionary reconstruction of ant association in Poritiinae, but the wide phylogenetic distribution of species obligately associated with Crematogaster ants within the tribe Liptenini hints that this might be the ancestral state. Larvae of poritiines' likely sister group, the subfamily Aphnaeinae, are thought to have been ancestrally associated with Crematogaster ants (Boyle et al, 2015; Espeland et al, 2018), and all known aphnaeine species are obligately ant‐associated (Pierce & Dankowicz, 2022). Liptenini originated in African forests, and numerous clades colonized open habitats secondarily (Figure 3).…”

“…Another unusual characteristic of poritiines is their larval relationship with ants. Across the Lycaenidae as a whole, the immature stages of as many as 75% of the species associate with ants, with relationships ranging from mutualistic to parasitic, and from obligate to facultative (Fiedler, 2021; Pierce et al, 2002; Pierce & Dankowicz, 2022). While most ant‐associated lycaenid larvae produce attractive and manipulative secretions for ants to consume in exchange for defence from predators and parasitoids, larvae of Poritiinae are covered in long bristles that do not seem to attract or reward ants.…”

“…In contrast, little is known about the ant association or lack thereof in Poritiini—earlier reports suggest that they are not ant‐associated ostensibly because they lack overt mutualistic or parasitic interactions (Fiedler, 1991). However, it remains possible that species of Poritiini will prove to be ant‐associated in a manner similar to typical Liptenini (Pierce & Dankowicz, 2022).…”

Plant–treehopper convergence may trick butterflies into trophic oviposition mistakes

“…Butterflies can use information about the presence of other organisms to select the host plant. For example, myrmecophilous butterflies (Lepidoptera: Lycaenidae and Riodinidae) that live in symbiosis with ants can use visual and chemical cues for oviposition (Pierce & Dankowicz, 2022), and some of them prefer to oviposit near conspicuous ant–treehopper associations and exploit the enemy‐free space they provide (Kaminski et al, 2010). By contrast, nonmyrmecophilous butterfly species can use visual and chemical cues to avoid ovipositing near ant territories and to discriminate and choose between several host plant species (Dell'Aglio et al, 2016; Janz, 2003; Sendoya et al, 2009).…”

On the adaptive meaning of chemically insignificant cues in multitrophic caterpillar-ant-plant symbioses

“…Myrmecophilous butterflies (Lepidoptera: Lycaenidae and Riodinidae) live in association with ants during their immature stages (reviewed in [21]). In general, the ant- caterpillar interaction is trophobiotic, a kind of mutualistic interaction mediated by sugar- rich liquids that attract and serve as food resources for the ants, which in return offer protection against natural enemies or clean their partner caterpillars [1,20,22–23].…”