Few studies of wild animal performance account for parasite infections: A systematic review.


Journal

The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574

Informations de publication

Date de publication:
04 2023
Historique:
received: 01 07 2022
accepted: 29 11 2022
medline: 6 4 2023
pubmed: 9 12 2022
entrez: 8 12 2022
Statut: ppublish

Résumé

Wild animals have parasites. This inconvenient truth has far-reaching implications for biologists measuring animal performance traits: infection with parasites can alter host behaviour and physiology in profound and sometimes counterintuitive ways. Yet, to what extent do studies on wild animals take individual infection status into account? We performed a systematic review across eight scientific journals primarily publishing studies in animal behaviour and physiology over a 5-year period to assess the proportion of studies which acknowledge, treat or control for parasite infection in their study design and/or analyses. We explored whether parasite inclusion differed between studies that are experimental versus observational, conducted in the field vs the laboratory and measured behavioural vs physiological traits. We also investigated the importance of other factors such as the journal, the trait category (e.g. locomotion, reproduction) measured, the vertebrate taxonomic group investigated and the host climatic zone of origin. Our results show that parasite inclusion was generally lacking across recent studies on wild vertebrates. In over 680 filtered papers, we found that only 21.9% acknowledged the potential effects of infections on animal performance in the text, and only 5.1% of studies treated animals for infection (i.e. parasite control) or considered infection status in the statistical analyses (i.e. parasite analysis). Parasite inclusion, control and analysis were higher in laboratory compared to field studies and higher for physiological studies compared to behavioural studies but did not differ among journals, performance trait categories and taxonomic groups. Among climatic zones, parasite inclusion, control and analysis were higher in tropical, subtropical and temperate zones than in boreal and polar zones. Overall, our literature review suggests that parasites are sorely under-acknowledged by researchers in recent years despite growing evidence that infections can modify animal performance. Given the ubiquity of parasites in the environment, we encourage scientists to consider individual infection status when assessing performance of wild animals. We also suggest ways for researchers to implement such practices in both experimental and observational studies.

Identifiants

pubmed: 36480357
doi: 10.1111/1365-2656.13864
doi:

Types de publication

Systematic Review Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

794-806

Informations de copyright

© 2022 The Authors. Journal of Animal Ecology © 2022 British Ecological Society.

Références

Albery, G. F., Watt, K. A., Keith, R., Morris, S., Morris, A., Kenyon, F., Nussey, D. H., & Pemberton, J. M. (2020). Reproduction has different costs for immunity and parasitism in a wild mammal. Functional Ecology, 34(1), 229-239. https://doi.org/10.1111/1365-2435.13475
Arnal, A., Droit, A., Elguero, E., Ducasse, H., Sánchez, M. I., Lefevre, T., Misse, D., Bédèrina, M., Vittecoq, M., Daoust, S., & 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(Sep), 1-7. https://doi.org/10.3389/fevo.2015.00109
Arnold, S. J. (1983). Morphology, performance and fitness. American Zoologist, 23(2), 347-361. https://doi.org/10.1093/icb/23.2.347
Aryes, J. S., & Schneider, D. S. (2012). Tolerance of infections. Annual Reviews of Immunology, 30, 271-294. https://doi.org/10.1146/annurev-immunol-020711-075030
Barber, I., Hoare, D., & Krause, J. (2000). Effects of parasites on fish behaviour: A review and evolutionary perspective. Reviews in Fish Biology and Fisheries, 10, 131-165.
Barber, I., & Huntingford, F. A. (1995). The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour, 132(15), 1223-1240.
Barber, I., & Wright, H. A. (2005). Effects of parasites on fish behaviour: Interactions with host physiology. In K. A. Sloman, R. W. Wilson, & S. Balshine (Eds.), Behaviour and physiology of fish (Fish Physiology, Vol. 24, pp. 109-149). Elsevier.
Behrens, J. W., Seth, H., Axelsson, M., & Buchmann, K. (2014). The parasitic copepod Lernaeocera branchialis negatively affects cardiorespiratory function in Gadus morhua. Journal of Fish Biology, 84(5), 1599-1606. https://doi.org/10.1111/jfb.12362
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., 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
Booth, D. T., Clayton, D. H., & Block, B. A. (1993). Experimental demonstration of the energetic cost of parasitism in free-ranging hosts. Proceedings of the Royal Society of London B: Biological Sciences, 253, 125-129. https://royalsocietypublishing.org/
Bradley, C. A., & Altizer, S. (2005). Parasites hinder monarch butterfly flight: Implications for disease spread in migratory hosts. Ecology Letters, 8(3), 290-300. https://doi.org/10.1111/j.1461-0248.2005.00722.x
Brusch, G. A., Gavira, R. S. B., Viton, R., DupoueÌ, A., Leroux-Coyau, M., Meylan, S., le Galliard, J. F., & Lourdais, O. (2020). Additive effects of temperature and water availability on pregnancy in a viviparous lizard. Journal of Experimental Biology, 223(19), 1-10. https://doi.org/10.1242/jeb.228064
Caballero, I. C., Sakla, A. J., Detwiler, J. T., le Gall, M., Behmer, S. T., & Criscione, C. D. (2015). Physiological status drives metabolic rate in mediterranean geckos infected with pentastomes. PLoS ONE, 10(12), e0144477. https://doi.org/10.1371/journal.pone.0144477
Careau, V., Garant, D., & Humphries, M. M. (2012). Free-ranging eastern chipmunks (Tamias striatus) infected with bot fly (Cuterebra emasculator) larvae have higher resting but lower maximum metabolism. Canadian Journal of Zoology, 90(3), 413-421. https://doi.org/10.1139/Z2012-008
Careau, V., Thomas, D., Humphries, M. M., & Réale, D. (2008). Energy metabolism and animal personality. Oikos, 117(5), 641-653. https://doi.org/10.1111/j.0030-1299.2008.16513.x
Choudhury, A., & Dick, T. A. (2000). Richness and diversity of helminth communities in tropical freshwater fishes: Empirical evidence. Journal of Biogeography, 27, 935-956.
Chrétien, E., De Bonville, J., Guitard, J., Binning, S. A., Barou-Dagues, M., Melis, É., Kack, A., Côté, A., Gradito, M., Papillon, A., Thelamon, V., Levet, M., & Barou-Dagues, M. (2022). Data from: Few studies of wild animal performance account for parasite infections: A systematic review (version v1). Zenodo. https://doi.org/10.5281/zenodo.7296510
Christensen, E. A. F., Norin, T., Tabak, I., van Deurs, M., & Behrens, J. W. (2021). Effects of temperature on physiological performance and behavioral thermoregulation in an invasive fish, the round goby. Journal of Experimental Biology, 224(1), 1-10. https://doi.org/10.1242/jeb.237669
Claireaux, G., & Lefrançois, C. (2007). Linking environmental variability and fish performance: Integration through the concept of scope for activity. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1487), 2031-2041. https://doi.org/10.1098/rstb.2007.2099
Debeffe, L., Morellet, N., Verheyden-Tixier, H., Hoste, H., Gaillard, J. M., Cargnelutti, B., Picot, D., Sevila, J., & Hewison, A. J. M. (2014). Parasite abundance contributes to condition-dependent dispersal in a wild population of large herbivore. Oikos, 123(9), 1121-1125. https://doi.org/10.1111/oik.01396
Greenhall, A. M. (2018). In A. M. Greenhall & U. Schmidt (Eds.), Natural history of vampire bats. CRC Press.
Guitard, J. J., Chrétien, E., De Bonville, J., Roche, D. G., Boisclair, D., & Binning, S. A. (2022). Increased parasite load is associated with reduced metabolic rates and escape responsiveness in pumpkinseed sunfish. Journal of Experimental Biology, 225(15), 1-12. https://doi.org/10.1242/jeb.243160
Holmstad, P. R., Jensen, K. H., Skorping, A., Holmstad, P. R., Jensen, K. H., & Skorping, A. (2008). Ectoparasite intensities are correlated with endoparasite infection loads in willow ptarmigan. Oikos, 117, 515-520. https://doi.org/10.1111/j.2007.0030-1299.16219.x
Kamiya, T., O'Dwyer, K., Nakagawa, S., & Poulin, R. (2014). What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological Reviews, 89(1), 123-134. https://doi.org/10.1111/brv.12046
Kingsolver, J. G., & Huey, R. B. (2003). Introduction: The evolution of morphology, performance, and fitness 1. Integrative and Comparative Biology, 43, 361-366. https://academic.oup.com/icb/article/43/3/361/623023
Krause, J., & Godin, J. J. (1994). Influence of parasitism on the shoaling behaviour of banded killifish, Fundulus diaphanus. Canadian Journal of Zoology, 72, 1775-1779.
Kuris, A. M., Hechinger, R. F., Shaw, J. C., Whitney, K. L., Aguirre-Macedo, L., Boch, C. A., Dobson, A. P., Dunham, E. J., Fredensborg, B. L., Huspeni, T. C., Lorda, J., Mababa, L., Mancini, F. T., Mora, A. B., Pickering, M., Talhouk, N. L., Torchin, M. E., & Lafferty, K. D. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature, 454(7203), 515-518. https://doi.org/10.1038/nature06970
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., de Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T. J., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, P. A., McLaughlin, J. P., Mordecai, E. A., Pascual, M., Poulin, R., & Thieltges, D. W. (2008). Parasites in food webs: The ultimate missing links. Ecology Letters, 11(6), 533-546. https://doi.org/10.1111/j.1461-0248.2008.01174.x
Lefebvre, F., Mounaix, B., Poizat, G., & Crivelli, A. J. (2004). Impacts of the swimbladder nematode Anguillicola crassus on Anguilla anguilla: Variations in liver and spleen masses. Journal of Fish Biology, 64(2), 435-447. https://doi.org/10.1111/j.0022-1112.2004.00309.x
Lind, C. M., Agugliaro, J., & Farrell, T. M. (2020). The metabolic response to an immune challenge in a viviparous snake, Sistrurus miliarius. Journal of Experimental Biology, 223(10), 1-10. https://doi.org/10.1242/jeb.225185
Marcogliese, D. J. (2004). Parasites: Small players with crucial roles in the ecological theater. EcoHealth, 1(2), 151-164. https://doi.org/10.1007/s10393-004-0028-3
Martins, P. M., Poulin, R., & Gonçalves-Souza, T. (2021). Integrating climate and host richness as drivers of global parasite diversity. Global Ecology and Biogeography, 30(1), 196-204. https://doi.org/10.1111/geb.13213
McElroy, E. J., & de Buron, I. (2014). Host performance as a target of manipulation by parasites: A meta-analysis. Journal of Parasitology, 100(4), 399-410. https://doi.org/10.1645/13-488.1
Meadows, D. W., & Meadows, C. M. (2003). Behavioral and ecological correlates of foureye butterflyfish, Chaetodon capistratus, (Perciformes: Chaetodontidae) infected with Anilocra chaetodontis (Isopoda: Cymothoidae). Revista de Biología Tropical, 51, 77-81. www.rbt.ac.cr, www.ucr.ac.cr
Mota-Rojas, D., Wang, D., Titto, C. G., Gómez-Prado, J., Carvajal-De la Fuente, V., Ghezzi, M., Boscato-Funes, L., Barrios-García, H., Torres-Bernal, F., Casas-Alvarado, A., & Martínez-Burnes, J. (2021). Pathophysiology of fever and application of infrared thermography (Irt) in the detection of sick domestic animals: Recent advances. Animals, 11(8) MDPI AG, 1-33. https://doi.org/10.3390/ani11082316
Oppliger, A., Celerier, M. L., & Clobert, J. (1996). Physiological and behaviour changes in common lizards parasitized by haemogregarines. Parasitology, 113, 433-438.
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., McDonald, S., … Moher, D. (2021). The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. International Journal of Surgery, 88(March), 105906. https://doi.org/10.1016/j.ijsu.2021.105906
Palstra, A. P., Heppener, D. F. M., van Ginneken, V. J. T., Székely, C., & van den Thillart, G. E. E. J. M. (2007). Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus. Journal of Experimental Marine Biology and Ecology, 352(1), 244-256. https://doi.org/10.1016/j.jembe.2007.08.003
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: A theoretical analysis. Parasitology, 109, 109-118.
Poulin, R. (2001). Another look at the richness of helminth communities in tropical freshwater fish. Journal of Biogeography, 28, 737-743.
Poulin, R. (2010). Latitudinal gradients in parasite diversity: Bridging the gap between temperate and tropical areas. Neotropical Helminthology, 4(2), 169-177.
Poulin, R. (2011). Evolutionary ecology of parasites. In In evolutionary ecology of parasites (2nd ed., pp. 96-133). Princeton University Press.
Poulin, R., & Morand, S. (2000). The diversity of parasites. The Quarterly Review of Biology, 75(3), 277-293.
Poulin, R., & Rohde, K. (1997). Comparing the richness of metazoan ectoparasite communities of marine fishes: Controlling for host phylogeny. Oecologia, 110, 278-283.
R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Rangel, R. E., & Johnson, D. W. (2018). Metabolic responses to temperature in a sedentary reef fish, the bluebanded goby (Lythrypnus dalli, Gilbert). Journal of Experimental Marine Biology and Ecology, 501, 83-89. https://doi.org/10.1016/j.jembe.2018.01.011
Rew-Duffy, M., Cameron, S. F., Freeman, N. J., Wheatley, R., Latimer, J. M., & Wilson, R. S. (2020). Greater agility increases probability of survival in the endangered northern quoll. The Journal of Experimental Biology, 223, 1-9. https://doi.org/10.1242/jeb.218503
Rohde, K., & Heap, M. (1998). Latitudinal differences in species and community richness and in community structure of metazoan endo-and ectoparasites of marine teleost fish*. International Journal for Parasitology, 28, 461-474.
Ryberg, M. P., Skov, P. v., Vendramin, N., Buchmann, K., Nielsen, A., & Behrens, J. W. (2020). Physiological condition of Eastern Baltic cod, Gadus morhua, infected with the parasitic nematode Contracaecum osculatum. Conservation Physiology, 8(1), 1-14. https://doi.org/10.1093/conphys/coaa093
Sayre, R., Karagulle, D., Frye, C., Boucher, T., Wolff, N. H., Breyer, S., Wright, D., Martin, M., Butler, K., van Graafeiland, K., Touval, J., Sotomayor, L., McGowan, J., Game, E. T., & Possingham, H. (2020). An assessment of the representation of ecosystems in global protected areas using new maps of world climate regions and world ecosystems. Global Ecology and Conservation, 21, e00860. https://doi.org/10.1016/j.gecco.2019.e00860
Spagnoli, S., Xue, L., & Kent, M. L. (2015). The common neural parasite Pseudoloma neurophilia is associated with altered startle response habituation in adult zebrafish (Danio rerio): Implications for the zebrafish as a model organism. Behavioural Brain Research, 291, 351-360. https://doi.org/10.1016/j.bbr.2015.05.046
Timi, J. T., & Poulin, R. (2020). Why ignoring parasites in fish ecology is a mistake. International Journal for Parasitology, 50(10-11), 755-761. https://doi.org/10.1016/j.ijpara.2020.04.007
Townsend, A. K., Sewall, K. B., Leonard, A. S., & Hawley, D. M. (2022). Infectious disease and cognition in wild populations. Trends in Ecology & Evolution, 37(10), 899-910. https://doi.org/10.1016/j.tree.2022.06.005
Twyford, A. D. (2018). Parasitic plants. Current Biology, 28(16), R857-R859. https://doi.org/10.1016/j.cub.2018.06.030
Umberger, C. M., de Buron, I., Roumillat, W. A., & McElroy, E. J. (2013). Effects of a muscle-infecting parasitic nematode on the locomotor performance of their fish host. Journal of Fish Biology, 82(4), 1250-1258. https://doi.org/10.1111/jfb.12061
Wagner, G. N., McKinley, R. S., Bjørn, P. A., & Finstad, B. (2003). Physiological impact of sea lice on swimming performance of Atlantic salmon. Journal of Fish Biology, 62(5), 1000-1009. https://doi.org/10.1046/j.1095-8649.2003.00091.x
Weinstein, S. B., & Kuris, A. M. (2016). Independent origins of parasitism in Animalia. Biology Letters, 12(7), 20160324. https://doi.org/10.1098/rsbl.2016.0324
Wickham, H. (2011). The split-apply-combine strategy for data analysis. Journal of Statistical Software, 40(1), 1-29. http://www.jstatsoft.org/
Wickham, H. (2016). Ggplot 2 elegant graphics for data analysis. Springer-Verlag.

Auteurs

Emmanuelle Chrétien (E)

Eau Terre Environnement, Institut National de la Recherche Scientifique (INRS-ETE), Québec, Québec, Canada.
Département de Sciences Biologiques, Groupe Interuniversitaire en Limnologie et Environnement Aquatique (GRIL), Montréal, Québec, Canada.

Jérémy De Bonville (J)

Département de Sciences Biologiques, Groupe Interuniversitaire en Limnologie et Environnement Aquatique (GRIL), Montréal, Québec, Canada.
Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Joëlle Guitard (J)

Institut des Sciences de la Mer (ISMER), Université du Québec à Rimouski, Rimouski, Québec, Canada.

Sandra A Binning (SA)

Département de Sciences Biologiques, Groupe Interuniversitaire en Limnologie et Environnement Aquatique (GRIL), Montréal, Québec, Canada.
Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Élizabeth Melis (É)

Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Alexandra Kack (A)

Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Ariane Côté (A)

Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Maryane Gradito (M)

Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Amélie Papillon (A)

Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Victoria Thelamon (V)

Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Marie Levet (M)

Département de Sciences Biologiques, Groupe Interuniversitaire en Limnologie et Environnement Aquatique (GRIL), Montréal, Québec, Canada.
Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

Marie Barou-Dagues (M)

Centre d'Études Biologiques de Chizé, CNRS-ULR, UMR 7372, Villiers en Bois, France.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH