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The effect of waterfowl signals and Pseudocorynosoma enrietti infection on the behaviour of the amphipod Hyalella patagonica

Published online by Cambridge University Press:  31 July 2023

N. Figueroa
Affiliation:
Laboratorio de Parasitología (LAPAR), INIBIOMA (CONICET – Universidad Nacional del Comahue), Avda. Quintral 1250, 8400 San Carlos de Bariloche – Río Negro, Argentina
V. Flores*
Affiliation:
Laboratorio de Parasitología (LAPAR), INIBIOMA (CONICET – Universidad Nacional del Comahue), Avda. Quintral 1250, 8400 San Carlos de Bariloche – Río Negro, Argentina
C. Rauque
Affiliation:
Laboratorio de Parasitología (LAPAR), INIBIOMA (CONICET – Universidad Nacional del Comahue), Avda. Quintral 1250, 8400 San Carlos de Bariloche – Río Negro, Argentina
*
Corresponding author: V. Flores; Email: veronicaroxanaflores@gmail.com

Abstract

In the present study, we sought to determine whether i) a waterfowl signal induces avoidance behaviour of the amphipod Hyalella patagonica, ii) infection by the acanthocephalan Pseudocorynosoma enrietti affects the behaviour of the amphipod, and iii) the parasite interferes with the amphipod response to waterfowl. We evaluated amphipod behaviour experimentally by measuring activity levels, phototaxis, geotaxis, and clinging behaviour. The main findings of this study indicate that uninfected amphipods show avoidance behaviour by reducing their activity in the presence of a predator signal. Secondly, infected amphipods show altered behaviour, such as swimming in bright areas near the water surface, which makes them more visible to predators in nature. Lastly, the presence of predatory cues causes infected amphipods to drop to the bottom, which increases their visibility to predators. The present research allows us to perceive the intricate interplay among predators, parasites, and their intermediate hosts and advance our understanding of these complex ecological dynamics.

Type
Research Paper
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Arnal, A, Anaïs, D, Elguero, E, Ducasse, H, Sánchez, M, Lefevre, T, Dorothée, M, Bédèrina, M, Vittecoq, M, Daoust, S, and Thomas, F (2015) Activity level and aggregation behavior in the crustacean gammarid Gammarus insensibilis parasitized by the manipulative trematode Microphallus papillorobustus. Frontiers in Ecology and Evolution 3, 109.CrossRefGoogle Scholar
Bakker, T, Frommen, J, and Thünken, T (2017) Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology 123, 779784.CrossRefGoogle Scholar
Bauer, A, Haine, E, Perrot-Minnot, M, and Rigaud, T (2005) Acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli. Journal of Zoology 267, 3943.CrossRefGoogle Scholar
Benesh, D, Kitchen, J, Pulkkinen, K, Hakala, I, and Valtonen, T (2008) The effect of Echinorhynchus borealis (Acanthocephala) infection on the anti-predator behavior of a benthic amphipod. Journal of Parasitology 94, 542545.CrossRefGoogle ScholarPubMed
Casalins, L, Brugni, N, and Rauque, C (2015) The behavior response of amphipods infected by Hedruris suttonae (Nematoda) and Pseudocorynosoma sp. (Acanthocephala). Journal of Parasitology 101, 647650.CrossRefGoogle ScholarPubMed
Cézilly, F, Thomas, F, Médoc, V, and Perrot-Minnot, M (2010) Host-manipulation by parasites with complex life cycles: adaptive or not? Trends in Parasitology 26, 311317.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Maynard, BJ, and Wellnitz, TA (2003) Activity levels and predator detection by amphipods infected with an acanthocephalan parasite, Pomphorhynchus laevis. Folia Parasitologica 50, 129134.CrossRefGoogle ScholarPubMed
del Hoyo, J, Elliott, A, and Sartagal, J (1992) Family Anatidae (ducks, geese and swans). pp. 536628 in del Hoyo, J, Elliott, A, and Sartagal, J (Eds), Handbook of the birds of the world, vol. 1. Barcelona, Lynx Edicions.Google Scholar
Fayard, M, Dechaume‐Moncharmont, FX, Wattier, R, and Perrot‐Minnot, MJ (2020) Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans. Biological Reviews 95, 12331251.CrossRefGoogle ScholarPubMed
Friesen, O, Poulin, R, and Lagrue, C (2017) Differential impacts of shared parasites on fitness components among competing hosts. Ecology and Evolution 7, 46824693.CrossRefGoogle ScholarPubMed
Jacquin, L, Mori, Q, Pause, M, Steffen, M, and Medoc, V (2014) Non-specific manipulation of gammarid behaviour by P. minutus parasite enhances their predation by definitive bird hosts. PLoS ONE 9, e101684.CrossRefGoogle ScholarPubMed
Jermacz, Ł and Kobak, J (2018) The braveheart amphipod: a review of responses of invasive Dikerogammarus villosus to predation signals. PeerJ 6, e5311.CrossRefGoogle ScholarPubMed
Jermacz, Ł, Nowakowska, A, Kletkiewicz, H, and Kobak, J (2020) Experimental evidence for the adaptive response of aquatic invertebrates to chronic predation risk. Oecologia 192a, 341350.CrossRefGoogle Scholar
Lagrue, C, Heaphy, K, Presswell, B, and Poulin, R (2016) Strong association between parasitism and phenotypic variation in a supralittoral amphipod. Marine Ecology-Progress Series I 553, 111123.CrossRefGoogle Scholar
Lagrue, C, Güvenatam, A, and Bollache, L (2013) Manipulative parasites may not alter intermediate host distribution but still enhance their transmission: field evidence for increased vulnerability to definitive hosts and non host predator avoidance. Parasitology 140, 258265.CrossRefGoogle Scholar
MacDonald, EC, Frost, EH, MacNeil, SM, Hamilton, DJ, and Barbeau, MA (2014) Behavioral response of Corophium volutator to shorebird predation in the upper Bay of Fundy, Canada. PLoS ONE 9, e110633.CrossRefGoogle Scholar
Moore, J (2002) Parasites and the behavior of animals. 1st edn. New York, Oxford University Press. 315 pp.Google Scholar
Narosky, T and Izurieta, D (2010) Aves de Argentina y Uruguay. Guía de identificación. 16th edn. Buenos Aires, Vazquez Mazzini Editores. 432 pp.Google Scholar
Paterson, RA, Dick, JT, Pritchard, DW, Ennis, M, Hatcher, MJ, and Dunn, AM (2015). Predicting invasive species impacts: a community module functional response approach reveals context dependencies. Journal of Animal Ecology 84, 453463.CrossRefGoogle ScholarPubMed
Perrot-Minnot, MJ, Kaldonski, N, and Cézilly, F (2007) Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod. International Journal of Parasitology 37, 645651.CrossRefGoogle Scholar
Poulin, R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. pp. 151186 in Brockmann, HJ, Roper, TJ, Naguib, M, Wynne-Edwards, KE, Mitani, JC, and Leigh, WS (Eds), Advances in the Study of Behavior. Burlington, Academic Press Burlington.Google Scholar
Rauque, C and De Los Ríos Escalante, P (2013) Patagonian inland water malacostracans as hosts for parasites. Crustaceana 86, 15201526.CrossRefGoogle Scholar
Rauque, C and Semenas, L (2007) Infection pattern of two sympatric acanthocephalan species in the amphipod Hyalella patagonica (Amphipoda: Hyalellidae) from Lake Mascardi (Patagonia, Argentina). Parasitology Research 100, 12711276.CrossRefGoogle ScholarPubMed
Rauque, C and Semenas, L (2009) Effects of two acanthocephalan species on the reproduction of Hyalella patagonica (Amphipoda, Hyalellidae) in an Andean Patagonian Lake (Argentina). Journal of Invertebrate Pathology 100, 3539.CrossRefGoogle Scholar
Rauque, C, Paterson, R, Poulin, R, and Tompkins, D (2011) Do different parasite species interact in their effects on host fitness? A case study on parasites of the amphipod Paracalliope fluviatilis. Parasitology 138, 11761182.CrossRefGoogle ScholarPubMed
Rauque, C, Flores, V, and Semenas, L (2022) Pseudocorynosoma enrietti (Molfi & Freitas Fernandes, 1953) (Acanthocephala: Polymorphidae) from Patagonia (Argentina): life cycle, localities, and new host records. Journal of Helminthology 96, e38.CrossRefGoogle Scholar
Thünken, T, Baldauf, A, Bersau, N, Bakker, TCM, Kullmann, H, and Frommen, JC (2010) Impact of olfactory non-host predator cues on aggregation behaviour and activity in Polymorphus minutus infected Gammarus pulex. Hydrobiologia 654, 137145.CrossRefGoogle Scholar
Wellnitz, T, Giari, L, Maynard, B, and Dezfuli, BS (2003) A parasite spatially structures its host population. Oikos 100, 263268.CrossRefGoogle Scholar
Williams, M, Donohue, I, Picard, J, and O’Keeffe, F (2019) Infection with behaviour-manipulating parasites enhances bioturbation by key aquatic detritivores. Parasitology 146, 15281531.CrossRefGoogle ScholarPubMed
Wilhelm, FM and Lasenby, DC (1998) Seasonal trends in the head capsule length and body length/weight relationships of two amphipod species. Crustaceana 71, 399410.CrossRefGoogle Scholar