Predaceous and Parasitic Lepidoptera

Braby MF, Espeland M, Müller CJ, Eastwood R, Lohman DJ, Kawahara AY, Maunsell SC, Pierce NE. Molecular phylogeny of the tribe Candalidini (Lepidoptera: Lycaenidae): systematics, diversification and evolutionary history. Systematic Entomology. 2020;45 (3) :703-722. braby_candalidini_2020.pdf
Whitaker MRL, Baker CCM, Salzman SM, Martins DJ, Pierce NE. Combining stable isotope analysis with DNA metabarcoding improves inferences of trophic ecology. PLOS ONE. 2019. whitaker_isotope_2019.pdf
Pohl S, Frederickson ME, Elgar MA, Pierce NE. Colony Diet Influences Ant Worker Foraging and Attendance of Myrmecophilous Lycaenid Caterpillars. Frontiers in Ecology and Evolution. 2016;4 (114). Publisher's Version fevo-04-00114.pdf
Whitaker MRL, Salzman S, Sanders J, Kaltenpoth M, Pierce NE. Microbial communities of lycaenid butterflies do not correlate with larval diet. Frontiers in Microbiology. 2016;7 (1920). Publisher's Version fmicb-07-01920.pdf
Mathew J, Travassos MA, Canfield M, Murawski D, Kitching RL, Pierce NE. The singing reaper: diet, morphology and vibrational signaling in the Nearctic species Feniseca tarquinius. Tropical Lepidoptera Research. 2008;18 :24-29.Abstract

Abstract – A survey at fourteen sites in Eastern North America of populations of the carnivorous lycaenid butterfly, Feniseca tarquinius, confirmed that the sole prey item on Alnus rugosa (Betulaceae) for this species in these regions was Paraprociphilus tessellatus (Homoptera: Aphidoidea: Pemphigidae). Overwhelmingly, these aphids were tended by ants in the subfamily Formicinae. These results are compiled with all earlier records of prey aphids, their host plants and attendant ants for this species. SEM examination of a 4th instar larva of F. tarquinius supported Cottrell’s (1984) observation that the dorsal nectary organ and tentacle organs are absent in the 4th instar of virtually all Miletinae. Larvae of F. tarquinius were found to produce substrate-borne vibrations that possess a long pulse length and narrow bandwidth when compared with other lycaenid calls. The possible function of these calls is briefly discussed.

Als TD, Vila R, Kandul NP, Nash DR, Yen SH, Hsu YF, Mignault AA, Boomsma JJ, Pierce NE. The evolution of alternative parasitic life histories in large blue butterflies. Nature. 2004;432 :386-390.Abstract

Large blue (Maculinea) butterflies are highly endangered throughout the Palaearctic region, and have been the focus of intense conservation research(1-3). In addition, their extraordinary parasitic lifestyles make them ideal for studies of life history evolution. Early instars consume flower buds of specific host plants, but later instars live in ant nests where they either devour the brood (predators), or are fed mouth-to-mouth by the adult ants (cuckoos). Here we present the phylogeny for the group, which shows that it is a monophyletic clade nested within Phengaris, a rare Oriental genus whose species have similar life histories(4,5). Cuckoo species are likely to have evolved from predatory ancestors. As early as five million years ago, two Maculinea clades diverged, leading to the different parasitic strategies seen in the genus today. Contrary to current belief, the two recognized cuckoo species show little genetic divergence and are probably a single ecologically differentiated species(6-10). On the other hand, some of the predatory morphospecies exhibit considerable genetic divergence and may contain cryptic species. These findings have important implications for conservation and reintroduction efforts.

Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annual Review of Entomology. 2002;47 :733-771.Abstract

The estimated 6000 species of Lycaenidae account for about one third of all Papilionoidea. The majority of lycaenids have associations with ants that can be facultative or obligate and range from mutualism to parasitism. Lycaenid larvae and pupae employ complex chemical and acoustical signals to manipulate ants. Cost/benefit analyses have demonstrated multiple trade-offs involved in myrmecophily. Both demographic and phylogenetic evidence indicate that ant association has shaped the evolution of obligately associated groups. Parasitism typically arises from mutualism with ants, arid entomophagous species are disproportionately common in the Lycaenidae compared with other Lepidoptera. Obligate associations are more common in the Southern Hemisphere, in part because highly ant-associated lineages make up a larger proportion of the fauna in these, regions. Further research on phylogeny and natural history, particularly of the Neotropical fauna, will be necessary to understand the rote ant association has played in the evolution of the Lycaenidae.

Pierce NE. Peeling the onion: Symbioses between ants and blue butterflies. In: Model systems in behavioral ecology. Princeton: Princeton University Press ; 2001. pp. 41-56. 2001_pierce_peeling_the_onion.pdf
Fraser AM, Axen AH, Pierce NE. Assessing the quality of different ant species as partners of a myrmecophilous butterfly. Oecologia. 2001;129 :452-460.Abstract

We assessed the quality of different ant species as partners of the facultatively myrmecophilous lycaenid butterfly Glaucopsyche lygdamus. We compared disappearance and parasitism rates of G. lygdamus larvae in the field, and development of non-feeding pre-pupae in the laboratory, when individuals were untended or tended by one of four ant species. Formica podzolica was the only ant species to provide a clear benefit to G. lygdamus, in the form of reduced larval parasitism relative to untended larvae. F. 'neogagates' (F. neogagates + F. lasioides) and Tapinoma sessile were essentially neutral partners, providing no significant cost or benefit for any of the parameters measured. Relative to untended individuals, association with F. obscuripes significantly increased larval disappearance and significantly decreased pupal mass. Thus, F. obscuripes may act as a parasite of the general association between G. lygdamus and ants under certain conditions. Ant species also differed in their persistence as tenders of G. lygdamus larvae once an interaction was established. Over the lifetime of a larva, F. podzolica and F. obscuripes usually remained as the attendant ant species on plants over consecutive census dates, while F. 'neogagates' and T. sessile were frequently replaced, most commonly by F. obscuripes. It remains to be determined if disappearance and developmental outcomes reported here reflect true fitness costs (i.e. reduced survivorship and lower reproductive success) for G. lygdamus. The potential and limitations for specialization in association between G. lygdamus and high quality ant partners are discussed.

Kitching R, Sheermeyer E, Jones R, Pierce NE. The Biology of Australian Butterflies (Monographs on Australian Lepidoptera Vol. 6). Sydney: CSIRO Press; 1999 pp. 395. brabynew1999.pdf
Pierce NE. Predatory and parasitic Lepidoptera: carnivores living on plants. Journal of the Lepidopterists' Society. 1995;49 :412-453.Abstract

Moths and butterflies whose larvae do not feed on plants represent a decided minority slice of lepidopteran diversity, yet offer insights into the ecology and evolution of feeding habits. This paper summarizes the life histories of the known predatory and parasitic lepidopteran taxa, focusing in detail on current researchin the butterfly family Lycaenidae, a group disprotionately rich in aphytophagous feeders and myrmecophilous habits.

Pierce NE. The evolution and biogeography of associations between lycaenid butterflies and ants. In: Oxford Surveys in Evolutionary Biology . Vol. IV. Oxford University Press ; 1987. pp. 89-116.Abstract

Many organisms make a living from seratching each other's backs. and many survive at the expense of othcrs. Once a complex interaction has arisen between two organisms. what elfect can such a relationship have on their subsequcnt cvolution·! This pllpcr will consider thc evolutionary conscquences of ussocintions UIllOlIg Iycllcnid buttcrflics, their host plants, unts. purusitoids. lind prcdators. Thc Lycacllidac llfC cspecially intcrc.'1ting from an ccologicul and evolutionary pcrspcctivc because they exhibit dramatic variety in their life histories. The larvae of many species associate with ants, and these relationships can be parasitic. commensal, or mutualistic. larvae cun be carnivorous or hcrbivorous: and some species interact with many species of ants, whereas others are species-specific. It is partly because of this complexity and diversity that the lycaenidae have not been studied as intensively as other buUerny families, and I will discuss at least three problems that have hampered our understanding of their ecology and evolution. In particular. more must be learned about the nature of the exocrine secretions of lycaenid larvae, and whether they function to reward. appease, and/or deceive their associated ants. The association between lycaenids and ants has had several important evolutionary consequences, and I will show how these relate to the question of why there are so many species of Iycaenid buuernies. Finally. I will discuss an unresolved pattern in the biogeography oflycaenid buuernies: association with ants in general, and species-specific interactions in particular, are far more common among Iycaenids found in Ethiopian, Oriental. and Australasian regions than among those from the Holarctic.