Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-05-08T09:13:25.374Z Has data issue: false hasContentIssue false

Let's go swimming: mermithid-infected earwigs exhibit positive hydrotaxis

Published online by Cambridge University Press:  28 August 2019

Ryan Edward Harper Herbison*
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin 9016, New Zealand
Steven Evans
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin 9016, New Zealand
Jean-François Doherty
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin 9016, New Zealand
Robert Poulin
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin 9016, New Zealand
*
Author for correspondence: Ryan Edward Harper Herbison, E-mail: RyanEHHerbison@gmail.com

Abstract

Certain species of parasites have the apparent ability to alter the behaviour of their host in order to facilitate the completion of their own life cycle. While documented in hairworms (phylum Nematomorpha), the ability for mermithid parasites (from the sister phylum Nematoda) to force hosts to enter water remains more enigmatic. Here, we present the first experimental evidence in a laboratory setting that an insect which normally never enters open water (the European earwig Forficula auricularia) will readily enter the water when infected with a mermithid nematode (Mermis nigrescens). Only adult mermithids appear capable of inducing this polarising shift in behaviour, with mermithid length being a very strong predictor of whether their host enters water. However, mermithid length was only weakly associated with how long it took an earwig to enter water following the beginning of a trial. Considering the evidence presented here and its alignment with a proteomic investigation on the same host–parasite system, this study provides strong evidence for adaptive behavioural manipulation and a foundational system for further behavioural and mechanistic exploration.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adamo, SA (2013) Parasites: evolution's neurobiologists. Journal of Experimental Biology 216, 310.Google Scholar
Baylis, HA (1944) Observations on the nematode Mermis nigrescens and related species. Parasitology 36, 122132.Google Scholar
Baylis, HA (1947) The larval stages of the nematode Mermis nigrescens. Parasitology 38, 1016.Google Scholar
Biron, DG, Marché, L, Ponton, F, Loxdale, HD, Galéotti, N, Renault, L and Thomas, F (2005) Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach. Proceedings of the Royal Society of London B: Biological Sciences 272, 21172126.Google Scholar
Biron, DG, Ponton, F, Marché, L, Galeotti, N, Renault, L, Demey-Thomas, E and Thomas, F (2006) ‘Suicide’ of crickets harbouring hairworms: a proteomics investigation. Insect Molecular Biology 15, 731742.Google Scholar
Capinera, JL (1987) Observations on natural and experimental parasitism of insects by Mermis nigrescens Dujardin (Nematoda: Mermithidae). Journal of the Kansas Entomological Society 60, 159162.Google Scholar
Christie, JR (1937) Mermis subnigrescens, a nematode parasite of grasshoppers. Journal of Agricultural Research 55, 353364.Google Scholar
Crumb, S, Eide, P and Bonn, A (1941) The European Earwig. Technical Bulletin, United States, Department of Agriculture, 766, 76.Google Scholar
Gat, JR (2000) Atmospheric water balance – the isotopic perspective. Hydrological Processes 14, 13571369.Google Scholar
Herbison, RE, Kleffman, T, Algie, M, Evans, S and Poulin, R (2019) A Molecular War: convergent and ontogenetic evidence for adaptive host manipulation in related parasites infecting divergent hosts. Submitted.Google Scholar
Hughes, D (2013) Pathways to understanding the extended phenotype of parasites in their hosts. Journal of Experimental Biology 216, 142147.Google Scholar
Kaushik, M, Knowles, SCL and Webster, JP (2014) What makes a feline fatal in Toxoplasma gondii’s fatal feline attraction? Infected rats choose wild cats. American Zoologist 54, 118128.Google Scholar
Libersat, F, Delago, A and Gal, R (2009) Manipulation of host behavior by parasitic insects and insect parasites. Annual Review of Entomology 54, 189207.Google Scholar
Maeyama, T, Terayama, M and Matsumoto, T (1994) The abnormal behavior of Colobopsis sp. (Hymenoptera: Formicidae) parasitized by Mermis (Nematoda) in Papua New Guinea. Sociobiology 24, 115119.Google Scholar
Nickle, WR (1972) A contribution to our knowledge of the Mermithidae (Nematoda). Journal of Nematology 4, 113.Google Scholar
Poinar, G Jr, Latham, ADM and Poulin, R (2002) Thaumamermis zealandica n. sp. (Mermithidae: Nematoda) parasitising the intertidal marine amphipod Talorchestia quoyana (Talitridae: Amphipoda) in New Zealand, with a summary of mermithids infecting amphipods. Systematic Parasitology 53, 227233.Google Scholar
Poulin, R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41, 151186.Google Scholar
Poulin, R and Latham, M (2002) Parasitism and the burrowing depth of the beach hopper Talorchestia quoyana (Amphipoda: Talitridae). Animal Behaviour 63, 269275.Google Scholar
Poulin, R and Maure, F (2015) Host manipulation by parasites: a look back before moving forward. Trends in Parasitology 31, 563570.Google Scholar
Presswell, B, Evans, S, Poulin, R and Jorge, F (2015) Morphological and molecular characterization of Mermis nigrescens Dujardin, 1842 (Nematoda: Mermithidae) parasitizing the introduced European earwig (Dermaptera: Forficulidae) in New Zealand. Journal of Helminthology 89, 267276.Google Scholar
Sanchez, MI, Ponton, F, Schmidt-Rhaesa, A, Hughes, DP, Misse, D and Thomas, F (2008) Two steps to suicide in crickets harbouring hairworms. Animal Behaviour 76, 16211624.Google Scholar
Schmidt-Rhaesa, A (2001) The life cycle of horsehair worms (Nematomorpha). Acta Parasitologica 46, 151158.Google Scholar
Thomas, F, Schmidt-Rhaesa, A, Martin, G, Manu, C, Durand, P and Renaud, F (2002) Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology 15, 356361.Google Scholar
Vance, SA (1996) Morphological and behavioural sex reversal in mermithid-infected mayflies. Proceedings of the Royal Society of London B: Biological Sciences 263, 907912.Google Scholar
Webb, EK, Pearman, GI and Leuning, R (1980) Correction of flux measurements for density effects due to heat and water vapour transfer. Quarterly Journal of the Royal Meteorological Society 106, 85100.Google Scholar
Webster, JP (2007) The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophrenia Bulletin 33, 752756.Google Scholar