Wildlife is increasingly threatened by drops in number of individuals and populations, and eventually by extinction. Besides loss of habitat, persecution, pet trade,… a decrease in individual health status is an important factor to consider. In this article, Ballouard et al (2021)  perform a thorough analysis on the prevalence of two pathogens (herpes virus and mycoplasma) in (mainly) Western Hermann’s tortoises in south-east France. This endangered species was suspected to suffer from infections obtained through released/escaped pet tortoises. By incorporating samples of captive as well as wild tortoises, they convincingly confirm this and identify some possible ‘pet’ vectors. 

In February this year, a review paper on health assessments in wildlife was published (Kophamel et al 2021). Amongst others, it shows reptilia/chelonia are relatively well-represented among publications. It also contains a useful conceptual framework, in order to improve the quality of the assessments to better facilitate conservation planning. The recommended manuscript (Ballouard et al 2021) adheres to many aspects of this framework (e.g. minimum sample size, risk status, …) while others might need more (future) attention. For example, climate/environmental changes are likely to increase stress levels, which could lead to more disease symptoms. So, follow-up studies should consider conducting endocrinological investigations to estimate/monitor stress levels. Kophamel et al (2021) also stress the importance of strategic international collaboration, which may allow more testing of Eastern Hermann’s Tortoise, as these were shown to be infected by mycoplasma.

The genetic health of individuals/populations shouldn’t be forgotten in health/stress assessments. As noted by Ballouard et al (2021), threatened species often have low genetic diversity which makes them more vulnerable to diseases. So, it would be interesting to link the infection data with (individual) genetic characteristics. In future research, the samples collected for this paper could fit that purpose.

Finally, it is expected that this paper will contribute to the conservation management strategy of the Hermann’s tortoises. As such,  it will be interesting to see how the results of the current paper will be implemented in the ‘field’. As the infections are likely caused by releases/escaped pets and as treating the wild animals is difficult, preventing them from getting infected through pets seems a priority.  Awareness building among pet holders and monitoring/treating pets should be highly effective.

References

Ballouard J-M, Bonnet X, Jourdan J, Martinez-Silvestre A, Gagno S, Fertard B, Caron S (2021) First detection of herpesvirus and mycoplasma in free-ranging Hermann’s tortoises (Testudo hermanni), and in potential pet vectors. bioRxiv, 2021.01.22.427726, ver. 4 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.01.22.427726

Kophamel S, Illing B, Ariel E, Difalco M, Skerratt LF, Hamann M, Ward LC, Méndez D, Munns SL (2021), Importance of health assessments for conservation in noncaptive wildlife. Conservation Biology. https://doi.org/10.1111/cobi.13724

Host-parasitoid interactions have been the focus of extensive ecological research for decades. One the of the major reasons is the importance host-parasitoid interactions play for the biological control of crop pests. Parasitoids are the main natural regulators for a large number of economically important pest insects, and in many cases they could be the only viable crop protection strategy. Parasitoids are also integral part of complex food webs whose structure and diversity display large spatio-temporal variations [1-3]. With the increasing globalization of human activities, the generalized spread and establishment of invasive species is a major cause of disruption in local community and food web spatio-temporal dynamics. In particular, the deliberate introduction of non-native parasitoids as part of biological control programs, aiming the suppression of established, and also highly invasive crop pests, is a common practice with potentially significant, yet poorly understood effects on local food web dynamics (e.g. [4]).
In their study, Muru et al. [5] took advantage of an existing biological control program focusing on the Asian chestnut gall wasp Dryocosmus kuriphilus, an invasive (and highly damaging) pest of chestnut trees. The species is currently a successful invader in many geographic regions, including southern France, where local parasitoid communities failed to provide an adequate control since its widespread establishment in 2010 [6]. In response, the non-native parasitoid species Torymus sinensis, which is highly-specific to the Asian chestnut gall wasp, was massively released in commercial chestnut orchards across several regions in France and the island of Corsica. The pest population outbreak was successfully contained, and thanks to the vast amount of host-parasitoid interaction data collected as part of the program, the authors were able to explore the effects of the large fluctuations in Asian chestnut gall wasp natural abundances on native parasitoid communities, immediately before, and up to five years following the introduction of its natural enemy T. sinensis.
Using co-occurrence and clustering analyses, Muru et al. [5] demonstrate that the invasion and the consecutive (efficient) control of the Asian chestnut gall wasp by the parasitoid T. sinensis have a significant impact on the structure of local parasitoid food webs. In particular, following decline in the Asian chestnut gall wasp’s populations, native parasitoids markedly switched to alternative hosts, most likely due to their respectively higher relative abundances. This pattern seemed to be driven by the degree of generalism in native parasitoid species. Indeed, when its abundances were still relatively high, the Asian chestnut gall wasp was primarily attacked by species capable of exploiting a broad range of hosts, while at low population densities only specialist parasitoids such as Mesolobus sericeus were able to persist and compete with the non-native T. sinensis.
The current study is important for two major reasons. First, it underscores the value of long-term species interaction data in order to understand the dynamic nature of food webs, namely their structural flexibility in response to changes in the environment or, as in this case, large fluctuation in abundances of a major pest species. In this context, biological control programs could be a great source of data for exploring long-term, large-scale dynamics of species interactions, and their use in ecological studies deserves to be further emphasized. Second, the study adds to the increasing empirical evidence that mobile generalist foragers can display adaptive, frequency-dependent switching behaviour ([1], [7]), which has been suggested to act as a key stabilizing mechanism in food webs by buffering fluctuating population dynamics at larger spatial scales ([8- 10]).
However, the timing of such buffering seems important, especially in systems such as commercial chestnut orchards. Despite their capacity to adaptively switch their foraging behaviour, the response of the native parasitoid communities to the new, unfamiliar resource was not fast enough in order to contain the primary outbreak under an appropriate damage threshold, thus requiring the introduction of the more specialized parasitoid T. sinensis. Nevertheless, based on current ecological theory, results presented by Muru et al. [5] suggest that the response of native parasitoid community to fluctuating host dynamics – i.e. shifts in parasitoid foraging behaviour based on their traits – could be predictable. This is encouraging considering the growing impact of biological invasions and insect pest outbreaks, but also the need to implement efficient, yet sustainable strategies for crop protection. Future studies would show at what extent observations by Muru et al. [5] are generalizable over longer time periods or other model systems. Noticeably, better understanding about population dynamics and interactions with the broader community of hosts available across habitats should allow to fine-tune predictions about parasitoids’ response to fluctuating resources.

References

[1] Eveleigh ES, McCann KS, McCarthy PC, Pollock SJ, Lucarotti CJ, Morin B, McDougall GA, Strongman DB, Huber JT, Umbanhowar J, Faria LDB (2007). Fluctuations in density of an outbreak species drive diversity cascades in food webs. Proc. Natl. Acad. Sci. USA 104, 16976-16981. doi: 10.1073/pnas.0704301104
[2] Tylianakis JM, Tscharntke T, Lewis OT (2007). Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445, 202-205. doi: 10.1038/nature05429
[3] Murakami M, Hirao T, Kasei A (2008). Effects of habitat configuration on host–parasitoid food web structure. Ecol. Res. 23, 1039-1049. doi: 10.1007/s11284-008-0478-0
[4] Geslin B, Gauzens B, Baude M, Dajoz I, Fontaine C, Henry M, Ropars L, Rollin O, Thébault E, Vereecken NJ (2016). Massively introduced managed species and their consequences for plant–pollinator interactions. Adv. Ecol. Res. 57, 147-199. doi: 10.1016/bs.aecr.2016.10.007
[5] Muru D, Borowiec N, Thaon M, Ris N, Viciriuc M I, Warot S, Vercken E (2020) The open bar is closed: restructuration of a native parasitoid community following successful control of an invasive pest. bioRxiv, 2019.12.20.884908, ver. 6 peer-reviewed and recommended by PCI Zoology. doi: 10.1101/2019.12.20.884908
[6] Borowiec N, Thaon M, Brancaccio L, Warot S, Vercken E, Fauvergue X, Ris N, Malausa J-C (2014). Classical biological control against the chestnut gall wasp 'Dryocosmus kuriphilus' (Hymenoptera, Cynipidae) in France. Plant Prot. Q. 29, 7-10.
[7] Bartley TJ, McCann KS, Bieg C, Cazelles K, Granados M, Guzzo MM, MacDougall AS, Tunney TD, McMeans BC (2019). Food web rewiring in a changing world. Nat. Ecol. Evol. 3, 345–354. doi: 10.1038/s41559-018-0772-3
[8] Kondoh M (2003). Foraging adaptation and the relationship between food-web complexity and stability. Science. 299, 1388-1391. doi: 10.1126/science.1079154
[9] McCann KS, Rooney N (2009). The more food webs change, the more they stay the same. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1789-801. doi: 10.1098/rstb.2008.0273
[10] Valdovinos FS, Ramos-Jiliberto R, garay-Narváez L, Urbani P, Dunne JA (2010). Consequences of adaptive behaviour for the structure and dynamics of food webs. Ecol. Lett. 13, 1546-1559. doi: 10.1111/j.1461-0248.2010.01535.x

The intricate relationships between parasites and their hosts often involve a choreography of behavioral changes, with parasites manipulating their hosts in a way that enhances - or seemingly enhances – their transmission (Hughes et al., 2012; Moore, 2002; Poulin, 2010). Host manipulation is increasingly acknowledged as a pervasive adaptive transmission strategy employed by parasites, and as such is one of the most remarkable manifestations of the extended phenotype (Dawkins, 1982).

In this laboratory study, Rigaud et al. (2023) delved into the time course of antipredator behavioral modifications induced by the acanthocephalan Pomphorhynchus laevis in its amphipod intermediate host Gammarus pulex. This system has a good foundation of prior knowledge (Bakker et al., 2017; Fayard et al., 2020; Perrot-Minnot et al., 2023), nicely drawn upon for the present work. This parasite orchestrates a switch from predation suppression, during the noninfective phase, to predation enhancement upon maturation. Specifically, G. pulex infected with the non-infective acanthella stage of the parasite can exhibit increased refuge use and reduced activity compared to uninfected individuals (Dianne et al., 2011, 2014), leading to decreased predation by trout (Dianne et al., 2011). In contrast, upon reaching the infective cystacanth stage, the parasite can enhance the susceptibility of its host to trout predation (Dianne et al., 2011).

The present work aimed to understand the temporal sequence of these behavioral changes across the entire ontogeny of the parasite. The results confirmed the protective role of P. laevis during the acanthella stage, wherein infected amphipods exhibited heightened refuge use. This protective manipulation, however, became significant only later in the parasite's ontogeny, suggesting a delayed investment strategy, possibly influenced by the extended developmental time of P. laevis. The protective component wanes upon reaching the cystacanth stage, transitioning into an exposure strategy, aligning with theoretical predictions and previous empirical work (Dianne et al., 2011; Parker et al., 2009). The switch was behavior-specific. Unlike the protective behavior, a decline in the amphipod activity rate manifested early in the acanthella stage and persisted throughout development, suggesting potential benefits of reduced activity for the parasite across multiple stages. Furthermore, the findings challenge previous assumptions regarding the condition-dependency of manipulation, revealing that the parasite-induced behavioral changes predominantly occurred in the presence of cues signaling potential predators. Finally, while amphipods infected with acanthella stages displayed survival rates comparable to their uninfected counterparts, increased mortality was observed in those infected with cystacanth stages.

Understanding the temporal sequence of host behavioral changes is crucial for deciphering whether it is adaptive to the parasite or not. This study stands out for its meticulous examination of multiple behaviors over the entire ontogeny of the parasite highlighting the complexity and condition-dependent nature of manipulation. The protective-then-expose strategy emerges as a dynamic process, finely tuned to the developmental stages of the parasite and the ecological challenges faced by the host. The delayed emergence of protective behaviors suggests a strategic investment by the parasite, with implications for the host's survival and the parasite's transmission success. The differential impact of infection on refuge use and activity rate further emphasizes the need for a multidimensional approach in studying parasitic manipulation (Fayard et al., 2020). This complexity demands further exploration, particularly in deciphering how trophically-transmitted parasites shape the behavioral landscape of their intermediate hosts and its temporal dynamic (Herbison, 2017; Perrot-Minnot & Cézilly, 2013).  As we discover the many subtleties of these parasitic manipulations, new avenues of research are unfolding, promising a deeper understanding of the ecology and evolution of host-parasite interactions.

References

Bakker, T. C. M., Frommen, J. G., & Thünken, T. (2017). Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology, 123(11), 779–784. https://doi.org/10.1111/eth.12660

Dawkins, R. (1982). The extended phenotype: The long reach of the gene (Reprinted). Oxford University Press.

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Gaillard, M., Léger, E., & Rigaud, T. (2011). Protection first then facilitation: A manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution, 65(9), 2692–2698. https://doi.org/10.1111/j.1558-5646.2011.01330.x

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Guvenatam, A., & Rigaud, T. (2014). Parasite-induced alteration of plastic response to predation threat: Increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. International Journal for Parasitology, 44(3–4), 211–216. https://doi.org/10.1016/j.ijpara.2013.11.001

Fayard, M., Dechaume‐Moncharmont, F., Wattier, R., & Perrot‐Minnot, M. (2020). Magnitude and direction of parasite‐induced phenotypic alterations: A meta‐analysis in acanthocephalans. Biological Reviews, 95(5), 1233–1251. https://doi.org/10.1111/brv.12606

Herbison, R. E. H. (2017). Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation. Frontiers in Ecology and Evolution, 5, 102. https://doi.org/10.3389/fevo.2017.00102

Hughes, D. P., Brodeur, J., & Thomas, F. (2012). Host manipulation by parasites. Oxford university press.

Moore, J. (2002). Parasites and the behavior of animals. Oxford University Press.

Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K., & Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution, 63(2), 448–458. https://doi.org/10.1111/j.1558-5646.2008.00565.x

Perrot-Minnot, M.-J., & Cézilly, F. (2013). Investigating candidate neuromodulatory systems underlying parasitic manipulation: Concepts, limitations and prospects. Journal of Experimental Biology, 216(1), 134–141. https://doi.org/10.1242/jeb.074146

Perrot-Minnot, M.-J., Cozzarolo, C.-S., Amin, O., Barčák, D., Bauer, A., Filipović Marijić, V., García-Varela, M., Servando Hernández-Orts, J., Yen Le, T. T., Nachev, M., Orosová, M., Rigaud, T., Šariri, S., Wattier, R., Reyda, F., & Sures, B. (2023). Hooking the scientific community on thorny-headed worms: Interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite, 30, 23. https://doi.org/10.1051/parasite/2023026

Poulin, R. (2010). Parasite Manipulation of Host Behavior. In Advances in the Study of Behavior (Vol. 41, pp. 151–186). Elsevier. https://doi.org/10.1016/S0065-3454(10)41005-0

Rigaud, T., Balourdet, A., & Bauer, A. (2023). Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: The switch in manipulation according to parasite developmental stage differs between behaviors. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2023.04.25.538244