Out of the burrow and into the nest: Functional anatomy of three life history stages of Ozaena lemoulti (Coleoptera: Carabidae) reveals an obligate life with ants

Wendy Moore Brusca, Andrea Di Giulio

Research output: Contribution to journalArticle

Abstract

The carabid subfamily Paussinae contains many species known to be obligately associated with ants during at least one stage of their life history. Myrmecophilous larvae have been documented for members of the tribe Paussini as well as several genera in the tribes Ozaenini, including Physea and Eustra. Here we describe the first instar larva of Ozaena lemoulti, and find it to be the most highly modified ozaenine larva that we have examined to date. Many structures of the larva suggest that it is a myrmecophile. Unlike all other described ozaenine larvae, which live in burrows that they construct and seal with their terminal disk, the completely unique larval morphology suggests Ozaena has adapted to living without the protection of a burrow and therefore must have a completely different feeding strategy than the typical ambush strategy of burrow dwelling larvae. We hypothesize that Ozaena larvae live in association with ants and use their long legs for running within the nest, and modifications of the mouthparts suggest the larva feeds on soft lightly sclerotized prey, such as ant brood. Our findings support an earlier hypothesis that Ozaena is mymecophilous during the adult stage. Comparisons of the functional anatomy of the eggs, larvae and adult between Ozaena lemoulti and the closely related, non-myrmecophilous general arthropod predator, Goniotropis kuntzeni, provide complementary, yet independent, evidence suggestive of this shift in lifestyle. We also examine and molecularly identify gut contents, providing direct evidence that adult Ozaena exclusively eat Camponotus ants. We conclude that Ozaena represents an independent shift to adopting a life of myrmecophily among beetles classified within the carabid subfamily Paussinae and document the morphological changes at each life history stage associated with the shift to a nest parasite lifestyle.

Original languageEnglish (US)
Pages (from-to)e0209790
JournalPLoS One
Volume14
Issue number1
DOIs
StatePublished - Jan 1 2019

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Atrophic Rhinitis
Permethrin
Ants
Beetles
Carabidae
Life Cycle Stages
burrows
Seals
Larva
Anatomy
Formicidae
nests
life history
Coleoptera
larvae
lifestyle
Life Style
Parasites
Camponotus
feeding methods

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

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title = "Out of the burrow and into the nest: Functional anatomy of three life history stages of Ozaena lemoulti (Coleoptera: Carabidae) reveals an obligate life with ants",
abstract = "The carabid subfamily Paussinae contains many species known to be obligately associated with ants during at least one stage of their life history. Myrmecophilous larvae have been documented for members of the tribe Paussini as well as several genera in the tribes Ozaenini, including Physea and Eustra. Here we describe the first instar larva of Ozaena lemoulti, and find it to be the most highly modified ozaenine larva that we have examined to date. Many structures of the larva suggest that it is a myrmecophile. Unlike all other described ozaenine larvae, which live in burrows that they construct and seal with their terminal disk, the completely unique larval morphology suggests Ozaena has adapted to living without the protection of a burrow and therefore must have a completely different feeding strategy than the typical ambush strategy of burrow dwelling larvae. We hypothesize that Ozaena larvae live in association with ants and use their long legs for running within the nest, and modifications of the mouthparts suggest the larva feeds on soft lightly sclerotized prey, such as ant brood. Our findings support an earlier hypothesis that Ozaena is mymecophilous during the adult stage. Comparisons of the functional anatomy of the eggs, larvae and adult between Ozaena lemoulti and the closely related, non-myrmecophilous general arthropod predator, Goniotropis kuntzeni, provide complementary, yet independent, evidence suggestive of this shift in lifestyle. We also examine and molecularly identify gut contents, providing direct evidence that adult Ozaena exclusively eat Camponotus ants. We conclude that Ozaena represents an independent shift to adopting a life of myrmecophily among beetles classified within the carabid subfamily Paussinae and document the morphological changes at each life history stage associated with the shift to a nest parasite lifestyle.",
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