Parasite load, rather than parasite presence, decreases upstream movement in Trinidadian guppies Poecilia reticulata.
Gyrodactylus
ectoparasites
fish
guppies
rheotaxis
swimming behavior
swimming performance
Journal
Journal of fish biology
ISSN: 1095-8649
Titre abrégé: J Fish Biol
Pays: England
ID NLM: 0214055
Informations de publication
Date de publication:
29 Apr 2024
29 Apr 2024
Historique:
revised:
04
03
2024
received:
30
11
2023
accepted:
09
04
2024
medline:
30
4
2024
pubmed:
30
4
2024
entrez:
29
4
2024
Statut:
aheadofprint
Résumé
Several factors influence whether an organism remains in its local habitat. Parasites can, for example, influence host movement by impacting their behavior, physiology, and morphology. In rivers, fish that swim efficiently against the current are able to maintain their position without being displaced downstream, a behavior referred to as positive rheotaxis. We hypothesized that both the presence and number of ectoparasites on a host would affect the ability of fish to avoid downstream displacement and thus prevent them from remaining in their habitat. We used the guppy-Gyrodactylus host-ectoparasite model to test whether parasite presence and parasite load had an effect on fish rheotaxis. We quantified rheotaxis of sham-infected and parasite-infected fish in a circular flow tank in the laboratory prior to infection and 5-6 days postinfection. Both parasite-infected and sham-infected individuals expressed similar levels of positive rheotaxis prior to infection and after infection. However, with increasing parasite numbers, guppies covered less distance in the upstream direction and spent more time in slower flow zones. These results suggest that higher numbers of Gyrodactylus ectoparasites negatively influence rheotactic movements. Further research is needed to understand the ecological and evolutionary implications of this ectoparasite on fish movement.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fonds Québécois de la Recherche sur la Nature et les Technologies
Organisme : Natural Sciences and Engineering Research Council of Canada
Informations de copyright
© 2024 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd on behalf of Fisheries Society of the British Isles.
Références
Arnold, G. P. (1974). Rheotropism in fishes. Biological Reviews of the Cambridge Philosophical Society, 49(4), 515–576. https://doi.org/10.1111/j.1469-185X.1974.tb01173.x
Bakke, T. A., Cable, J., & Harris, P. D. (2007). The biology of gyrodactylid monogeneans: The “Russian‐Doll Killers”. Advances in Parasitology, 64(318), 161–460. https://doi.org/10.1016/S0065-308X(06)64003-7
Barber, I., Hoare, D., & Krause, J. (2000). Effects of parasites on fish behaviour: A review and evolutionary perspective. In. Reviews in Fish Biology and Fisheries, 10, 131–165.
Barnes, M., Ebanks, B., MacColl, A., & Chakrabarti, L. (2023). A common Anaesthetic, MS‐222, alters measurements made using high‐resolution Respirometry in the three‐Spined stickleback (Gasterosteus aculeatus). Fishes, 8(1), 1–9. https://doi.org/10.3390/fishes8010042
Binning, S. a., Roche, D. G., & Layton, C. (2013). Ectoparasites increase swimming costs in a coral reef fish. Biology Letters, 9(1), 20120927. https://doi.org/10.1098/rsbl.2012.0927
Binning, S. a., Barnes, J. I., Davies, J. N., Backwell, P. R. Y., Keogh, J. S., & Roche, D. G. (2014). Ectoparasites modify escape behaviour, but not performance, in a coral reef fish. Animal Behaviour, 93, 1–7. https://doi.org/10.1016/j.anbehav.2014.04.010
Binning, S. A., Shaw, A. K., & Roche, D. G. (2017). Parasites and host performance: Incorporating infection into our understanding of animal movement. Integrative and Comparative Biology, 57(2), 267–280. https://doi.org/10.1093/icb/icx024
Blasco‐Costa, I., Koehler, A. V., Martin, A., & Poulin, R. (2013). Upstream‐downstream gradient in infection levels by fish parasites: A common river pattern? Parasitology, 140(2), 266–274. https://doi.org/10.1017/S0031182012001527
Blondel, L., Klemet‐N'guessan, S., Scott, M. E., & Hendry, A. P. (2020). Asymmetric isolation and the evolution of behaviors influencing dispersal: Rheotaxis of guppies above waterfalls. Genes, 11(2), 1–15. https://doi.org/10.3390/genes11020180
Cable, J., Scott, E. C. G., Tinsley, R. C., & Harris, P. D. (2002). Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli. The Journal of Parasitology, 88(1), 183–184. https://doi.org/10.2307/3285412
Cable, J., & van Oosterhout, C. (2007). The impact of parasites on the life history evolution of guppies (Poecilia reticulata): The effects of host size on parasite virulence. International Journal for Parasitology, 37(13), 1449–1458. https://doi.org/10.1016/j.ijpara.2007.04.013
Chance, R. J., Cameron, G. A., Fordyce, M., Noguera, P., Wang, T., Collins, C., Secombes, C. J., & Collet, B. (2018). Effects of repeated anaesthesia on gill and general health of Atlantic salmon, Salmo salar. Journal of Fish Biology, 93(6), 1069–1081. https://doi.org/10.1111/jfb.13803
Chrétien, E., De Bonville, J., Guitard, J., Binning, S. A., Melis, É., Kack, A., Côté, A., Gradito, M., Papillon, A., Thelamon, V., Levet, M., & Barou‐Dagues, M. (2023). Few studies of wild animal performance account for parasite infections: A systematic review. The Journal of Animal Ecology, 92(4), 794–806. John Wiley and Sons Inc. https://doi.org/10.1111/1365-2656.13864
Cone, D. K., & Odense, P. H. (1984). Pathology of five species of Gyrodactylus Nordmann, 1832 (Monogenea). Canadian Journal of Zoology, 62(6), 1084–1088. https://doi.org/10.1139/z84-156
Croft, D. P., Albanese, B., Arrowsmith, B. J., Botham, M., Webster, M., & Krause, J. (2003). Sex‐biased movement in the guppy (Poecilia reticulata). Oecologia, 137(1), 62–68. https://doi.org/10.1007/s00442-003-1268-6
Fraser, B., & Neff, B. D. (2010). Parasite mediated homogenizing selection at the MHC in guppies. Genetica, 138(2), 273–278. https://doi.org/10.1007/s10709-009-9402-y
Friendly, M. (2010). HE plots for repeated measures designs. Journal of Statistical Software, 37, 1–40. https://doi.org/10.18637/jss.v037.i04
Gheorghiu, C., Marcogliese, D. J., & Scott, M. E. (2012). Waterborne zinc alters temporal dynamics of guppy Poecilia reticulata epidermal response to Gyrodactylus turnbulli (Monogenea). Diseases of Aquatic Organisms, 98(2), 143–153. https://doi.org/10.3354/dao02434
Grabowska, J., Zięba, G., Przybylski, M., & Smith, C. (2019). The role of intraspecific competition in the dispersal of an invasive fish. Freshwater Biology, 64(5), 933–941. https://doi.org/10.1111/FWB.13275
Harris, P. D. (1988). Changes in the site specificity of Gyrodactylus turnbulli Harris, 1986 (Monogenea) during infections of individual guppies (Poecilia reticulata Peters, 1859). Canadian Journal of Zoology, 66(12), 2854–2857. www.nrcresearchpress.com
Harris, P. D., & Lyles, a. M. (1992). Infections of Gyrodactylus bullatarudis and Gyrodactylus turnbulli on guppies (Poecilia reticulata) in Trinidad. The Journal of Parasitology, 78(5), 912–914. https://doi.org/10.2307/3283329
Hockley, F., Wilson, C. A. M. E., Brew, A., & Cable, J. (2014). Fish responses to flow velocity and turbulence in relation to size, sex and parasite load. Journal of the Royal Society Interface, 11(November 2013), 20130814. https://doi.org/10.1098/rsif.2013.0814
Jiang, Y., Torrance, L., Peichel, C. L., & Bolnick, D. I. (2015). Differences in rheotactic responses contribute to divergent habitat use between parapatric lake and stream threespine stickleback. Evolution, 69(9), 2517–2524. https://doi.org/10.1111/evo.12740
Jonsson, N. (1991). Influence of water flow, water temperature and light on fish migration in rivers. Nordic Journal of Freshwater Research, 66(1991), 20–35.
Karino, K., Orita, K., & Sato, A. (2006). Long tails affect swimming performance and habitat choice in the male guppy. Zoological Science, 23(3), 255–260. https://doi.org/10.2108/zsj.23.255
Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7(12), 1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x
Kennedy, C. E. J., Endler, J. A., Poynton, S. L., & Mcminn, H. (1987). Behavioral ecology and sociobiology parasite load predicts mate choice in guppies. Behavioral Ecology and Sociobiology, 21, 291–295.
Kent, M., & Ojanguren, A. F. (2015). The effect of water temperature on routine swimming behaviour of new born guppies (Poecilia reticulata). Biology Open, 4, 547–552. https://doi.org/10.1242/bio.20149829
Lehmann, T. (1993). Ectoparasites: Direct impact on host fitness. Parasitology Today, 9(1), 13–17. https://doi.org/10.1016/0169-4758(93)90154-8
Martin, C. H., & Johnsen, S. (2007). A field test of the Hamilton–Zuk hypothesis in the Trinidadian guppy (Poecilia reticulata). Behavioral Ecology and Sociobiology, 61(12), 1897–1909. https://doi.org/10.1007/s00265-007-0430-2
Meijering, E. (2006). MTrackJ: A Java program for manual object tracking.
Mohammed, R., van Oosterhout, C., Schelkle, B., Cable, J., & McMullan, M. (2012). Upstream guppies (Poecilia reticulata, Peters, 1859) go against the flow. Biota Neotropica, 12(3), 1–5.
Mohammed, R. S., Reynolds, M., James, J., Williams, C., Mohammed, A., Ramsubhag, A., van Oosterhout, C., & Cable, J. (2016). Getting into hot water: Sick guppies frequent warmer thermal conditions. Oecologia, 181, 911–917. https://doi.org/10.1007/s00442-016-3598-1
Montgomery, J., Coombs, S., & Halstead, M. (1995). Biology of the mechanosensory lateral line in fishes. Reviews in Fish Biology and Fisheries, 5(4), 399–416. https://doi.org/10.1007/BF01103813
Montgomery, J. C., Baker, C. F., & Carton, A. G. (1997). The lateral line can mediate rheotaxis in fish. Nature, 389(6654), 960–963. https://doi.org/10.1038/40135
Ojanguren, A. F., & Braña, F. (2000). Thermal dependence of swimming endurance in juvenile brown trout. Journal of Fish Biology, 56(6), 1342–1347. https://doi.org/10.1006/jfbi.2000.1253
Östlund‐Nilsson, S., Curtis, L., Nilsson, G. E., & Grutter, A. S. (2005). Parasitic isopod Anilocra apogonae, a drag for the cardinal fish Cheilodipterus quinquelineatus. Marine Ecology Progress Series, 287, 209–216. https://doi.org/10.3354/meps287209
Oufiero, C. E., & Garland, T. (2009). Repeatability and correlation of swimming performances and size over varying time‐scales in the guppy (Poecilia reticulata). Functional Ecology, 23(5), 969–978. https://doi.org/10.1111/J.1365-2435.2009.01571.X
Petkova, I., Abbey‐Lee, R. N., & Løvlie, H. (2018). Parasite infection and host personality: Glugea‐infected three‐spined sticklebacks are more social. Behavioral Ecology and Sociobiology, 72(173), 1–9. https://doi.org/10.1007/s00265-018-2586-3
Poulin, R. (1994). Meta‐analysis of parasite‐induced behavioral changes. Animal Behavior, 48, 137–146.
R Core Team. (2018). R: A language and environment for statistical computing (3.5.0). R Foundation for Statistical Computing.
Rasband, W. (2012). ImageJ. U. S. National Institutes of Health, Bethesda, Maryland, USA imagej.nih.gov/ij
Reynolds, M., Arapi, E. A., & Cable, J. (2018). Parasite‐mediated host behavioural modifications: Gyrodactylus turnbulli infected Trinidadian guppies increase contact rates with uninfected conspecifics. Parasitology, 145(7), 920–926. https://doi.org/10.1017/S0031182017001950
Reznick, D., Butler Iv, M. J., & Rodd, H. (2001). Life‐history evolution in guppies. VII. The comparative ecology of high‐ and low‐predation environments. The American Naturalist, 157(2), 126–140. https://doi.org/10.1086/318627
Reznick, D., & Endler, J. (1982). The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution, 36(1), 160–177.
RStudio Team. (2016). RStudio: Integrated Development for R (1.0.153; p. RStudio, Inc., Boston, MA). https://doi.org/10.1007/978-81-322-2340-5
Scott, M. (1982). Reproductive potential of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology, 85, 217–236. http://journals.cambridge.org/abstract_S0031182000055207
Stephenson, J. F. (2019). Parasite‐induced plasticity in host social behaviour depends on sex and susceptibility. Biology Letters, 15(11), 20190557. https://doi.org/10.1098/rsbl.2019.0557
Stephenson, J. F., van Oosterhout, C., Mohammed, R. S., & Cable, J. (2015). Parasites of Trinidadian guppies: Evidence for sex‐ and age‐specific trait‐mediated indirect effects of predators. Ecology, 96(2), 489–498. https://doi.org/10.1890/14-0495.1
Stewart, A., Hunt, R., Mitchell, R., Muhawenimana, V., Wilson, C. A. M. E., Jackson, J. A., & Cable, J. (2018). The cost of infection: Argulus foliaceus and its impact on the swimming performance of the three‐spined stickleback (Gasterosteus aculeatus). Journal of the Royal Society Interface, 15(147), 20180571. https://doi.org/10.1098/RSIF.2018.0571
Tadiri, C. P., Dargent, F., & Scott, M. E. (2013). Relative host body condition and food availability influence epidemic dynamics: A Poecilia reticulata‐Gyrodactylus turnbulli host‐parasite model. Parasitology, 140(3), 343–351. https://doi.org/10.1017/S0031182012001667
Tadiri, C. P., Scott, M. E., & Fussmann, G. F. (2016). Impact of host sex and group composition on parasite dynamics in experimental populations. Parasitology, 1–9, 523–531. https://doi.org/10.1017/S0031182016000172
van Oosterhout, C., Mohammed, R. S., Hansen, H., Archard, G., McMullan, M., Weese, D. J., & Cable, J. (2007). Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). International Journal for Parasitology, 37, 805–812. https://doi.org/10.1016/j.ijpara.2006.12.016
Vanschoenwinkel, B., Gielen, S., Seaman, M., & Brendonck, L. (2008). Any way the wind blows ‐ frequent wind dispersal drives species sorting in ephemeral aquatic communities. Oikos, 117(1), 125–134. https://doi.org/10.1111/j.2007.0030-1299.16349.x
Weese, D. J., Schwartz, A. K., Bentzen, P., Hendry, A. P., & Kinnison, M. T. (2011). Eco‐evolutionary effects on population recovery following catastrophic disturbance. Evolutionary Applications, 4(2), 354–366. https://doi.org/10.1111/j.1752-4571.2010.00169.x
Weetman, D., Atkinson, D., & Chubb, J. C. (1999). Water temperature influences the shoaling decisions of guppies, Poecilia reticulata, under predation threat. Animal Behaviour, 58, 735–741. http://www.idealibrary.comon
Weisser, W. W., McCoy, K. D., & Boulinier, T. (2001). Parastism and predation as causes of dispersal. In Dispersal: Vol. second (Issue 12, 452). Oxford University Press.
Wisenden, B. D., Goater, C. P., & James, C. T. (2019). Behavioral defenses against parasites and pathogens. In G. Zaccone, M. A. Perriere, B. G. Kapoor (Eds.), Fish defenses: Volume 2: Pathogens, parasites and predators (pp. 151–168). Science Publishers. https://doi.org/10.1201/b10189-6
Xavier, R., Faria, P. J., Paladini, G., Van Oosterhout, C., Johnson, M., & Cable, J. (2015). Evidence for cryptic speciation in directly transmitted gyrodactylid parasites of trinidadian guppies. PLoS One, 10(1), e0117096. https://doi.org/10.1371/journal.pone.0117096
Zarri, L. J., Palkovacs, E. P., Post, D. M., Therkildsen, N. O., & Flecker, A. S. (2022). The evolutionary consequences of dams and other barriers for riverine fishes. Bioscience, 72(5), 431–448. https://doi.org/10.1093/BIOSCI/BIAC004