Indirect effects of parasitism include increased profitability of prey to optimal foragers
Parasites make hosts more profitable but less available to predators
Recommendation: posted 10 July 2023, validated 13 July 2023
Schiesari, L. (2023) Indirect effects of parasitism include increased profitability of prey to optimal foragers. Peer Community in Ecology, 100423. 10.24072/pci.ecology.100423
Even though all living organisms are, at the same time, involved in host-parasite interactions and embedded in complex food webs, the indirect effects of parasitism are only beginning to be unveiled.
Prosnier et al. investigated the direct and indirect effects of parasitism making use of a very interesting biological system comprising the freshwater zooplankton Daphnia magna and its highly specific parasite, the iridovirus DIV-1 (Daphnia-iridescent virus 1). Daphnia are typically semitransparent, but once infected develop a white phenotype with a characteristic iridescent shine due to the enlargement of white fat cells.
In a combination of infection trials and comparison of white and non-white phenotypes collected in natural ponds, the authors demonstrated increased mortality and reduced lifetime fitness in infected Daphnia. Furthermore, white phenotypes had lower mobility, increased reflectance, larger body sizes and higher protein content than non-white phenotypes. As a consequence, total energy content was effectively doubled in white Daphnia when compared to non-white broodless Daphnia.
Next the authors conducted foraging trials with Daphnia predators Notonecta (the backswimmer) and Phoxinus (the European minnow). Focusing on Notonecta, unchanged search time and increased handling time were more than compensated by the increased energy content of white Daphnia. White Daphnia were 24% more profitable and consistently preferred by Notonecta, as the optimal foraging theory would predict. The authors argue that menu decisions of optimal foragers in the field might be different, however, as the prevalence – and therefore availability - of white phenotypes in natural populations is very low.
The study therefore contributes to our understanding of the trophic context of parasitism. One shortcoming of the study is that the authors rely exclusively on phenotypic signs for determining infection. On their side, DIV-1 is currently known to be highly specific to Daphnia, their study site is well within DIV-1 distributional range, and the symptoms of infection are very conspicuous. Furthermore, the infection trial – in which non-white Daphnia were exposed to white Daphnia homogenates - effectively caused several lethal and sublethal effects associated with DIV-1 infection, including iridescence. However, the infection trial also demonstrated that part of the exposed individuals developed intermediate traits while still keeping the non-white, non-iridescent phenotype. Thus, there may be more subtleties to the association of DIV-1 infection of Daphnia with ecological and evolutionary consequences, such as costs to resistance or covert infection, that the authors acknowledge, and that would be benefitted by coupling experimental and observational studies with the determination of actual infection and viral loads.
Prosnier L., N. Loeuille, F.D. Hulot, D. Renault, C. Piscart, B. Bicocchi, M, Deparis, M. Lam, & V. Médoc. (2023). Parasites make hosts more profitable but less available to predators. BioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.02.08.479552
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
This work was supported by the French national program EC2CO-Biohefect/Ecodyn//Dril/MicrobiEen (Influence du parasitisme sur la distribution des flux d’énergie dans les réseaux trophiques)
Evaluation round #2
DOI or URL of the preprint: https://doi.org/10.1101/2022.02.08.479552
Version of the preprint: 3
Author's Reply, 23 Jun 2023
Decision by Luis Schiesari, posted 29 Mar 2023, validated 30 Mar 2023
Dear Dr Prosnier
Thank you for your revised version of ´Parasites make hosts more profitable but less available to predators´.
Both reviewers and myself consider that your manuscript is now improved, in particular with respect to (i) the clarification of the Methods (Table 1, for example, is helpful) and (ii) the reorganization of the material presented in the Results and Appendices, which (iii) increased the emphasis on the joint analysis (MFA) of results of the experimental infection.
However, there are still several points made by the referees and myself that have to be considered prior to recommendation of your manuscript by PCI Ecology.
From my side, I am still concerned about the reliance on phenotypic analysis for determination of infection status, and I do not think the rebuttal letter did a sufficiently thorough job in addressing my concerns.
The rebuttal letter is clear in explaining that Daphnia were never actually tested for infection status.
But I also asked whether the authors could instead provide reflectance data for Daphnia that were exposed to presumably infected Daphnia cadavers (i.e., because had the white phenotype) versus Daphnia that were exposed to presumably uninfected Daphnia cadavers (i.e. because had the non-white phenotype). This would be easier for the readers to accept than presenting reflectance data from wild individuals, as the experimental results were indeed consistent with infection of at least part of the individuals.
I then asked whether Daphnia from Bercy and La Villette had previously been subject to DIV-1 testing. If a previous study did demonstrate that Daphnia and DIV-1 actually coexist in these two ponds, the readers would feel more comfortable about your studies based on wild caught Daphnia. If no one ever tested Daphnia in these two ponds for DIV-1, the readers would feel a little more comfortable if the authors were able to say ´DIV-1 infection of Daphnia magna is common in ponds surrounding Paris´ (with the appropriate references) or ´DIV-1 is a virus parasite of Daphnia magna that is widespread in ponds in Central Europe, and iridescence in D. magna cannot be attributed to any other parasite or physiological change to date´ (with the appropriate references).
I did not receive any clear response to these two queries.
On the same line, the authors need to carefully go through the manuscript and adjust the text regarding the infection status of wild caught Daphnia. For example, lines 340-342 read ´Concerning D. magna coloration (Measure 6), we found three peaks in the spectrum that were compared between healthy and infected individuals using Wilcoxon signed-rank tests, because data were not normally distributed´. Likewise, the legend in Figure reads ´Effects of DIV-1 on reflectance between 280 and 850 nm. Blue (dashed) lines are healthy D. magna and red (solid) lines are infected D. magna.´
In no case you can say that wild Daphnia are infected or uninfected, or healthy or infected. Perhaps you could say ´presumably infected´ and ´presumably uninfected´, or ´white phenotype´ and ´non-white phenotype´ in every case that you refer to wild Daphnia. Of course it does not read as nice, but this is really all you can say.
I am looking forward a revised version of your manuscript, as well as a rebuttal letter to the comments raised by the two referees and myself.
Sincerely, Luis Schiesari
Reviewed by Thierry DE MEEUS, 06 Mar 2023
Reviewed by Eglantine Mathieu-Bégné, 20 Mar 2023
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.02.08.479552
Version of the preprint: 2
Author's Reply, 28 Feb 2023
Decision by Luis Schiesari, posted 24 Jul 2022
Dear Dr Prosnier,
I have now received feedback from two reviewers regarding your manuscript, ´Parasites make hosts more profitable but less available to predators´.
Both reviewers and myself agree that your manuscript deals with a very interesting general question in ecology, namely, the direct and indirect effects of parasites in a food web context; that the coupling of experimental and observational approaches is a positive aspect of your research; and that there is a combination of relevant response variables being measured.
At the same time, both reviewers and myself understand that your manuscript requires revisions before it can be recommended by PCI. Please see the reviewers´ comments below.
In additipn to the comments raised by the referees, I am concerned that infection was never actually measured. The authors argue that the phenotypic consequence of infection (=iridescence) is well known, and this may be acceptable for part of the response variables (in particular for those that were derived from experimental infection). However, at least in one case the association between phenotype and the assumption of infection is problematic – this is the measure of reflectance (measure 8). That is, measuring reflection as a response to infection when infected versus non-infected individuals were classified based on reflectance is... a circular reasoning. These were wild Daphnia and there was no test for DIV-1. Can you provide reflectance of the experimentally infected Daphnia? Furthermore, the reader would be less concerned if you were able to mention that Daphnia in these particular water bodies were previously tested for DIV-1.
Overall, then, the manuscript is of interest but the authors should undertake a major review, and provide a detailed response letter, in light of the comments given by the referees and myself before it can be Recommended by PCI.
Best regards, Luis Schiesari
Additional minor comments by the Recommender
Line 53. ´concurrently in addition´ is redundant.
Lines 200-202. Body size was measured in naturally infected individuals, but also in naturally non-infected individuals. So it would be best to use a different term (maybe ´wild Daphnia´?) in this as well as elsewhere in the manuscript (e.g. line 210)
Lines 261, 265. ´proposed´ reads odd. Maybe ´offered´?
Line 279. Lower case i, instead of capital I
Lines 438-440. This hypothesis was not formulated before, nor there is a citation for such a hypothesis being proposed in the literature. Or, alternatively, frame it in a way that it makes clear that this is your interpretation, a posteriori.
Lines 444-446. Unclear. Are you proposing lower speed is a cause for larger size?
In the Figures, Legends for the colors (i.e. colored box-plots and lines) are usually missing, and in the Results please reinforce the nature of the results (that is, make sure that the reader follows whether this or that effect is based on experimental or observational evidence).
Figure 1. Not clear how survival was measured and analyzed. If all newborns were exposed at the same time, why to break down the mortality of those that died before brooding and those that died after brooding? Should we assume that the blue continuous line and the red intermittent line in Figure 1A are cumulative, i.e., they comprise all individuals entering the experiment?