Parasites are inside “Everything and everywhere all at once”, yet not often considered in studies on wild animals. What’s the bug?

Authors: Jeremy De Bonville, Emmanuelle Chrétien, Joëlle J. Guitard, Marie Barou Dagues. This blog post tells the #Storybehindthepaper for Few studies of wild animal performance account for parasite infections: A systematic review.

What do we and wild animals all have in common? Parasites! As displeasing as this reality may sound, this fact is often overlooked by researchers conducting experiments on wild animals, either in the lab or on the field1. Parasites are defined as organisms living in or on another species (host) and are deriving resources from their host, harming them to some extent in the process. They are generally associated with a certain disgust, or are sometimes simply too small and considered “irrelevant” to be included in research questions. However, ignoring them could lead to erroneous conclusions, especially in ecology2. For one, wild animals are infected, at different levels, by parasites. Plus, parasites have this amazing capacity to influence their host performance in complex and various ways (Figure 1)3,4.

Figure 1.  Schematic summary of multiple performance traits that can be both impacted positively and negatively by the presence of parasites inside an individual.
         

As humans in the heart of the pandemic yearning for a collaborative project, a group of 2 undergrads, 4 masters, 5 Ph.D. students and 1 P.I. from 4 different labs sat down (online) together asking to what extent do researchers account for parasites in their studies. Thus began the long journey of our systematic review. Our goal was to quantify if and how parasites are considered in studies on behavioral and physiological performance of animals captured in the wild. For over a year, we assembled online, on Gather, to filter, read and analyze papers published in 8 journals in recent years on wild animal physiological and behavioural performance. The beginning of the COVID-19 pandemic was a tough time for all. This was our way to reconnect, work together and grab a coffee in our virtual “office” space (Figure 2).

 
Figure 2.  Our lab virtual office space  (Shown in the screenshot are J. De Bonville, S.A. Binning, A. Kack and E. Chrétien)

Following PRISMA guidelines for meta-analyses and literature reviews, we searched Web of Science with a specific search key in select journals and collected papers published from January 2016 to December 2020 . Following multiple filtering sessions to respect our list of criteria, we started with 3000 papers and ended up with 680 papers across 8 journals. We only kept research articles that studied behavioural or physiological performance of wild vertebrates, at the whole organism level. From the final 680 papers, we proceeded to screen for traces of parasite consideration.

  • First, did the authors mention parasites or infection at any point in their manuscript.
  • Second, was there any control done to account for the presence of parasites in animals sampled in the field, such as a treatment or exclusion of highly infected individuals.
  • Third, were parasites considered while analysing the performance traits, either as a confounding effect or as the main effect of the study, as done in a study where they tested the hypothesis that naturally present parasites would affect metabolic rates and escape response of fish5.       

We were not surprised to find that parasites were often overlooked or ignored by researchers. However, there was an overwhelmingly low number of papers that either controlled or analysed parasites at some point in their studies: only 58 studies representing about 8% from our total screening number of 680 (Figure 3).

Figure 3.  Overview of our study results. Number of analysed articles showing the percentage including parasites in their text and those who took action regarding parasites, by either controlling, including them in their analyses or both. 
 

We also noticed that parasite control and analysis was higher for studies in more controlled environments (such as experimental studies or lab setting vs observational or field studies). This could be explained by the level of handling of animals during research. We do realize, however, that certain researchers could be aware of parasites influencing the measured performance trait or treated animals prior to experimentation, but decided to omit it while writing their manuscript. To increase transparency and repeatability, we highly encourage researchers to mention any control or preliminary analyses they could have done regarding parasites.

In our manuscript, we proceed to give a series of guidelines to help researchers better account for infection status. For instance, if animals are euthanized following trait measurements, we encourage researchers to screen for internal parasites that could target organs related to the studied performance trait. If cognition is being studied, an inspection of the brain for signs of infection could improve the explanation of certain results.

 Some final notes for our readers: it is understandable that not everyone wants to work with parasites (these grotesque, yet stunning organisms), but we strongly incite researchers to mention any treatment or exclusion of naturally infected individuals and even better, to consider them as confounding factors in experiments. Parasites are not going anywhere. We should embrace them as a feature of study systems, not as a bug.

About the Authors

The 4 authors met at the Université de Montréal where they all did some part of their grad studies. Today, Jeremy De Bonville is a Ph.D. candidate there, working on the influence of infection on fish ecophysiology. Emmanuelle Chrétien is starting an assistant professor position at Université du Québec à Rimouski (UQAR), where Joëlle Guitard is also doing a Ph.D. Marie Barou Dagues is currently a postdoc at the Centre for Biological Studies of Chizé (CNRS) in France. order of the authors on the image is : Jeremy De Bonville (top left), Emmanuelle Chrétien (top right), Joëlle J. Guitard (bottom left) and Marie Barou Dagues (bottom right).

References

  1. Chretien, E., De Bonville, J., Guitard, J., Binning, S. A., Melis, E., Kack, A., Cote, 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. Journal of Animal Ecology. https://doi.org/10.1111/1365-2656.13864
  2. 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
  3. 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
  4. 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
  5. 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

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