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With the dead under the mat: the zombie ant extended phenotype under a new perspective

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Abstract

Some parasitic fungi can increase fitness by modifying the behavior of their hosts. These behaviors are known as extended phenotypes because they favor parasitic gene propagation. Here, we studied three lineages of Ophiocordyceps, a fungus that infects ants, altering their conduct before death. According to fungal strategy, ants may die in leaf litter, with entwined legs in branches, under the moss mat, or biting plant tissue. It is critical for parasites that the corpses stay at these places because Ophiocordyceps exhibit iteroparity, possibly releasing spores in multiple life cycles. Thus, we assumed substrate cadaver permanence as a fungi reproductive proxy and corpse height as a proxy of cadaver removal. We hypothesize that biting vegetation and dying in higher places may increase the permanence of ant corpses while avoiding possible corpse predation on the forest floor. We monitored over a year more than 4000 zombie ants in approximately 15 km2 of undisturbed tropical forest in central Amazonia. Our results show a longer permanence of corpses with increasing ground height, suggesting that the parasites may have better chances of releasing spores and infecting new hosts at these places. We found that the zombie ants that last longer on the substrate die under the moss mat in tree trunks, not necessarily biting vegetation. The biting behavior appears to be the most derived and complex mechanism among Ophiocordyceps syndromes. Our results put these findings under a new perspective, proposing that seemingly less complex behavioral changes are ecologically equivalent and adaptative for other parasite lineages.

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Acknowledgements

We are thankful to J. da Silva Lopes for fieldwork assistance, to L. O. Demarchi and S. P. de Lima for the helpful comments on the manuscript, and to N.M. Kinap for the study area figure. Also, we acknowledge the Brazilian Biodiversity Research Program (PPBio) and the National Institute for Amazonian Biodiversity Research (CENBAM). This work was only possible due to 20 years of research under the Brazilian LTER – CHAMADA PÚBLICA Nº 021/2020 – PELD/CNPq/FAPEAM.

Funding

This study was financed in part by the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM)—POSGRAD/scholarship/ financial support and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. The Fieldwork was financed by CHAMADA PÚBLICA Nº 021/2020—PELD/CNPq/FAPEAM. FBB receives continuous support by CNPq grant (#313986/2020–7).

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Authors and Affiliations

  1. Instituto Nacional de Pesquisas da Amazônia - INPA, Coordenação de Biodiversidade - COBIO, Av. André Araújo 2936, PetrópolisManaus, AM, 69083-000, Brazil

    Fernando Sarti Andriolli & José Wellington de Morais

  2. Instituto Federal de Educação, Ciência e Tecnologia do Amazonas – IFAM/CMA, Estradas Dos Moraes, S/N, Senador José Esteves, Maués, AM, 69190-000, Brazil

    José Aragão Cardoso Neto

  3. Departamento de Biologia, Universidade Federal Do Amazonas (UFAM), Av. General Rodrigo Octávio, Manaus, AM, 620069.080-900, Brazil

    Fabricio Beggiato Baccaro

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  1. Fernando Sarti Andriolli
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  2. José Aragão Cardoso Neto
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  3. José Wellington de Morais
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  4. Fabricio Beggiato Baccaro
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Contributions

FSA and FBB contributed to the study’s conception and design. JACN conducted the data collection. FSA and FBB performed the analysis. JWM and FBB supervised the project and reviewed versions of the manuscript. All authors contributed, commented, and approved the submitted manuscript.

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Correspondence to Fernando Sarti Andriolli.

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Communicated by: Sean O'Donnell

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Andriolli, F.S., Cardoso Neto, J.A., de Morais, J.W. et al. With the dead under the mat: the zombie ant extended phenotype under a new perspective. Sci Nat 111, 33 (2024). https://doi.org/10.1007/s00114-024-01920-w

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