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Infection with behaviour-manipulating parasites enhances bioturbation by key aquatic detritivores

Published online by Cambridge University Press:  10 June 2019

Maureen A. Williams Open the ORCID record for Maureen A. Williams [Opens in a new window] ,
Ian Donohue Open the ORCID record for Ian Donohue [Opens in a new window] ,
Juliette Picard ,
Floriane O'Keeffe  and
Celia V. Holland Open the ORCID record for Celia V. Holland [Opens in a new window]
Maureen A. Williams*
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland
Ian Donohue
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland
Juliette Picard
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland
Floriane O'Keeffe
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland
Celia V. Holland
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland
*
Author for correspondence: Maureen A. Williams, E-mail: [email protected]
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Abstract

The ecological ubiquity of parasites and their potential impacts on host behaviour have led to the suggestion that parasites can act as ecosystem engineers, structuring their environment and physical habitats. Potential modification of the relationship between parasites and their hosts by climate change has important implications for how hosts interact with both their biotic and abiotic environment. Here, we show that warming and parasitic infection independently increase rates of bioturbation by a key detritivore in aquatic ecosystems (Gammarus). These findings have important implications for ecosystem structure and functioning in a warming world, as alterations to rates of bioturbation could significantly modify oxygenation penetration and nutrient cycling in benthic sediments of rivers and lakes. Our results demonstrate a need for future ecosystem management strategies to account for parasitic infection when predicting the impacts of a warming climate.

Keywords

Acanthocephalabehaviourbioturbationecosystem engineerGammarushost-parasite interactionsparasitetemperaturewarming
Type
Research Article
Information
Parasitology , Volume 146 , Issue 12 , October 2019 , pp. 1528 - 1531
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Copyright
Copyright © Cambridge University Press 2019 

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References

Abram, PK, Boivin, G, Moiroux, J and Brodeur, J (2017) Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity. Biological Reviews 92, 1859–1876.Google Scholar
Agatz, A and Brown, CD (2014) Variability in feeding of Gammarus pulex: moving towards a more standardised feeding assay. Environmental Sciences Europe 26, 15–23.Google Scholar
Amundsen, PA, Lafferty, KD, Knudsen, R, Primicerio, R, Klemetsen, A and Kuris, AM (2009) Food web topology and parasites in the pelagic zone of a subarctic lake. Journal of Animal Ecology 78, 563–572.Google Scholar
Bailly, Y, Cézilly, F and Rigaud, T (2018) Stage-dependent behavioural changes but early castration induced by the acanthocephalan parasite Polymorphus minutus in its Gammarus pulex intermediate host. Parasitology 145, 260–268.Google Scholar
Bakker, TCM, Mazzi, D and Zala, S (1997) Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 1098–1104.Google Scholar
Baranov, V, Lewandowski, J and Krause, S (2016) Bioturbation enhances the aerobic respiration of lake sediments in warming lakes. Biology Letters 12, 20160448.Google Scholar
Barton, K (2016) Package ‘MuMIn: Multi-Model Inference’.Google Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Bauer, A, Haine, ER, Perrot-Minnot, MJ and Rigaud, T (2005) The 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, 39–43.Google Scholar
Croel, RC and Kneitel, JM (2011) Ecosystem-level effects of bioturbation by the tadpole shrimp Lepidurus packardi in temporary pond mesocosms. Hydrobiologia 665, 169–181.Google Scholar
De Nadaï-Monoury, E, Lecerf, A, Canal, J, Buisson, L, Laffaille, P and Gilbert, F (2013) A cost-effective method to quantify biological surface sediment reworking. Hydrobiologia 713, 115–125.Google Scholar
Dell, AI, Pawar, S and Savage, VM (2011) Systematic variation in the temperature dependence of physiological and ecological traits. Proceedings of the National Academy of Sciences of the United States of America 108, 10591–10596.Google Scholar
Dell, AI, Pawar, S and Savage, VM (2014) Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. Journal of Animal Ecology 83, 70–84.Google Scholar
Dobson, A, Lafferty, KD, Kuris, AM, Hechinger, RF and Jetz, W (2008) Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America 105, 11482–11489.Google Scholar
Donohue, I and Garcia-Molinos, J (2009) Impacts of increased sediment loads on the ecology of lakes. Biological Reviews 84, 517–531.Google Scholar
Donohue, I, Donohue, L, Ní Ainín, B and Irvine, K (2009) Assessment of eutrophication pressure on lakes using littoral invertebrates. Hydrobiologia 633, 105–122.Google Scholar
Dunne, JA, Lafferty, KD, Dobson, AP, Hechinger, RF, Kuris, AM, Martinez, ND, McLaughlin, JP, Mouritsen, KN, Poulin, R, Reise, K, Stouffer, DB, Thieltges, DW, Williams, RJ and Zander, CD (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biolgy 11, e1001579.Google Scholar
Galaktionov, KV (2017) Patterns and processes influencing helminth parasites of Arctic coastal communities during climate change. Journal of Helminthology 91, 387–408.Google Scholar
Grant, J and Daborn, G (1994) The effects of bioturbation on sediment transport on an intertidal mudflat. Netherlands Journal of Sea Research 32, 63–72.Google Scholar
Hoberg, EP and Brooks, DR (2007) How will global climate change affect parasite–host assemblages? TRENDS in Parasitology 23, 571–574.Google Scholar
Hunting, ER, Whatley, MH, van der Geest, HG, Mulder, C, Kraak, MHS, Breure, AM and Admiraal, W (2012) Invertebrate footprints on detritus processing, bacterial community structure, and spatiotemporal redox profiles. Freshwater Science 31, 724–732.Google Scholar
Issartel, J, Hervant, F, Voituron, Y, Renault, D and Vernon, P (2005) Behavioural, ventilatory and respiratory responses of epigean and hypogean crustaceans to different temperatures. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 141, 1–7.Google Scholar
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.Google Scholar
Jones, CG, Lawton, JH and Shachak, M (1996) Organisms as ecosystem engineers. In Samson, Fred B. and Knopf, Fritz L. (eds), Ecosystem Management: Selected Readings. New York, NY: Springer, pp. 130–147.Google Scholar
Jorge, F and Poulin, R (2018) Poor geographical match between the distributions of host diversity and parasite discovery effort. Proceedings of the Royal Society B: Biological Sciences 285, 20180072.Google Scholar
Kelly, DW, Dick, JTA and Montgomery, WI (2002) The functional role of Gammarus(Crustacea, Amphipoda): shredders, predators, or both? Hydrobiologia 485, 199–203.Google Scholar
Kordas, RL, Harley, CDG and O'Connor, MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. Journal of Experimental Marine Biology and Ecology 400, 218–226.Google Scholar
Kuris, AM, Hechinger, RF, Shaw, JC, Whitney, KL, Aguirre-Macedo, L, Boch, CA, Dobson, AP, Dunham, EJ, Fredensborg, BL, Huspeni, TC, Lorda, J, Mababa, L, Mancini, FT, Mora, AB, Pickering, M, Talhouk, NL, Torchin, ME and Lafferty, KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.Google Scholar
Kutz, SJ, Hoberg, EP, Polley, L and Jenkins, EJ (2005) Global warming is changing the dynamics of Arctic host-parasite systems. Proceedings. Biological sciences/The Royal Society 272, 2571–2576.Google Scholar
Labaude, S, Rigaud, T and Cézilly, F (2016) Additive effects of temperature and infection with an acanthocephalan parasite on the shredding activity of Gammarus fossarum (Crustacea: Amphipoda): the importance of aggregative behavior. Global Change Biology 23, 1415–1424.Google Scholar
MacNeil, C and Briffa, M (2009) Replacement of a native freshwater macroinvertebrate species by an invader: implications for biological water quality monitoring. Hydrobiologia 635, 321–327.Google Scholar
Maire, O, Lecroart, P, Meysman, F, Rosenberg, R, Duchêne, J and Grémare, A (2010) Quantification of sediment reworking rates in bioturbation research: a review. Aquatic Biology 2, 219–238.Google Scholar
McDonald, ME (1988) Key to acanthocephala reported in waterfowl, Washington, DC, USA: United States Department of the Interior, Fish and Wildlife Service.Google Scholar
Mermillod-Blondin, F, Gaudet, JP, Gerino, M, Desrosiers, G, Jose, J and Châtelliers, MCD (2004) Relative influence of bioturbation and predation on organic matter processing in river sediments: a microcosm experiment. Freshwater Biology 49, 895–912.Google Scholar
Morley, NJ and Lewis, JW (2014) Temperature stress and parasitism of endothermic hosts under climate change. TRENDS in Parasitology 30, 221–227.Google Scholar
Mouritsen, KN and Jensen, KT (1997) Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Marine Ecology Progress Series 151, 123–134.Google Scholar
Mouritsen, KN and Poulin, R (2005) Parasites boost biodiversity and change animal community structure by trait-mediated indirect effects. Oikos 108, 344–350.Google Scholar
Mydlarz, LD, Jones, LE and Harvell, CD (2006) Innate immunity, environmental drivers, and disease ecology of marine and freshwater invertebrates. Annual Review of Ecology, Evolution, and Systematics 37, 251–288.Google Scholar
O'Gorman, EJ, Pichler, DE, Adams, G, Benstead, JP, Cohen, H, Craig, N, Cross, WF, Demars, BOL, Friberg, N, Gíslason, GM, Gudmundsdóttir, R, Hawczak, A, Hood, JM, Hudson, LN, Johansson, L, Johansson, MP, Junker, JR, Laurila, A, Manson, JR, Mavromati, E, Nelson, D, Ólafsson, JS, Perkins, DM, Petchey, OL, Plebani, M, Reuman, DC, Rall, BC, Stewart, R, Thompson, MSA and Woodward, G (2012) Impacts of warming on the structure and functioning of aquatic communities. Advances in Ecological Research 47, 81–176.Google Scholar
Ouellette, D, Gaston, D, Gagne, J-P, Gilbert, F, Poggiale, J-C, Blier, PU and Stora, G (2004) Effects of temperature on in vitro sediment reworking processes by a gallery biodiffusor, the polychaete Neanthes virens. Marine Ecology Progress Series 266, 185–193.Google Scholar
Perrot-Minnot, MJ, Sanchez-Thirion, K and Cézilly, F (2014) Multidimensionality in host manipulation mimicked by serotonin injection. Proceedings of the Royal Society B: Biological Sciences 281, 20141915.Google Scholar
Perrot-Minnot, MJ, Maddaleno, M, Cézilly, F and Woods, A (2016) Parasite-induced inversion of geotaxis in a freshwater amphipod: a role for anaerobic metabolism? Functional Ecology 30, 780–788.Google Scholar
R Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Reid, DM (1938) Forms of Gammarus from Ireland. Nature 141, 690.Google Scholar
Studer, A, Thieltges, DW and Poulin, R (2010) Parasites and global warming: net effects of temperature on an intertidal host–parasite system. Marine Ecology Progress Series 415, 11–22.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, 356–361.Google Scholar
Torchiano, M (2018) effsize: Efficient Effect Size Computation. doi: 10.5281/zenodo.1480624.Google Scholar
Vadher, AN, Stubbington, R and Wood, PJ (2015) Fine sediment reduces vertical migrations of Gammarus pulex (Crustacea: Amphipoda) in response to surface water loss. Hydrobiologia 753, 61–71.Google Scholar
Vannatta, JT and Minchella, DJ (2018) Parasites and their impact on ecosystem nutrient cycling. TRENDS in Parasitology 34, 452–455.Google Scholar
Wohlgemuth, D, Solan, M and Godbold, JA (2017) Species contributions to ecosystem process and function can be population dependent and modified by biotic and abiotic setting. Proceedings of the Royal Society B: Biological Sciences 284, 20162805.Google Scholar
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