Increased temperature has no consequence for behavioral manipulation despite effects on both partners in the interaction between a crustacean host and a manipulative parasite

Abstract

Parasites alter many traits of their hosts. In particular, parasites known as "manipulative" may increase their probability of transmission by inducing phenotypic alterations in their intermediate hosts. Although parasitic-induced alterations can modify species' ecological roles, the proximate factors modulating this phenomenon remain poorly known. As temperature is known to affect host-parasite associations, understanding its precise impact has become a major challenge in a context of global warming. Gammarids are ecologically important freshwater crustaceans and serve as intermediate hosts for several acanthocephalan species. These parasites induce multiple effects on gammarids, including alterations of their behavior, ultimately leading to modifications in their functional role. Here, experimental infections were used to assess the effect of two temperatures on several traits of the association between Gammarus pulex and its acanthocephalan parasite Pomphorhynchus laevis. Elevated temperature affected hosts and parasites in multiple ways (decreased host survival, increased gammarids activity, faster parasites development and proboscis eversion). However, behavioral manipulation was unaffected by temperature. These results suggest that predicted change in temperature may have little consequences on the trophic transmission of parasites through changes in manipulation, although it may modify it through increased infection success and faster parasites development. Abiotic conditions can strongly influence interspecific interactions and, ultimately, the dynamics of ecological communities. In direct connection with climate change, the understanding of such effect has become a major challenge in recent years 1-3. Abiotic conditions, including temperature, can, for instance, affect predator-prey interactions and food-web dynamics 4-6 or competition between species 7-11. They can also directly or indirectly affect host-parasite interactions 12-14 , with cascading effects for trophic interactions and ecosystem stability 15-17. This is all the more relevant in the case of parasite species that infest and modify the phenotype of host species known as 'ecosystem engineers' , i.e. species that can affect the physical properties of ecosystems 18-20. For instance, some recent evidence suggests that changes in temperature can modulate the influence of parasitic infection on both the functional role and the coexistence of crustacean amphipod species 17,21-23. Crustacean amphipods are widespread throughout a large range of freshwater habitats 24,25 , in which they play a key ecological role. They represent an important food resource for many species 26,27 and are themselves a major predator 24,28 , capable of modulating the composition of freshwater macroinvertebrates communities 28,29. Some species can also directly influence water quality and the recycling of organic matter through their shredder role on dead leaves 25,30-32. Crustacean amphipods serve as intermediate host for a large variety of helminths with complex

Effects of temperature and a manipulative parasite on the swimming behaviour of Gammarus pulex in flowing water

“…These results highlight that temperature is a factor influencing the movements of gammarids but that it does not influence the manipulation effects of P. laevis on G. pulex. In accordance with the study of Labaude et al (2020) in static water, we did not found an amplification of P. laevis manipulation under warmer conditions in flowing water. According to Marcogliese (2008), acanthocephalan parasites could be affected by variations in water temperature: if water temperature increases, metabolic changes induce a shorter lifespan and faster growth, with a modification in their transmission capacities.…”

“…These results demonstrate that acanthocephalan extended phenotype can be modulated according to their host aquatic environment. However, Labaude et al (2020) found no effect of temperature on the manipulation behaviour of P. laevis in static water. Therefore, the way that acanthocephalan manipulate their hosts depending on such environmental constraints still requires further investigation to better understand how trophic transmission and ecosystem functioning could be affected by climate change (Marcogliese, 2001).…”

“…For example, a faster development of acanthocephalans induced by warmer temperature reduced the time to reach the infective cystacanth stage in their intermediate host. It could be interesting to compare the capacity of transmission with more extreme hotter and colder water temperature than tested in this study and in Labaude et al (2020), to see if parasite metabolic changes induced by warmer temperature could have an effect on their manipulation ability.…”

“…Pomphorhynchus laevis still induce the same intensity of manipulation when the water temperature is warmer in order to potentially increase the predation rate by definitive host on its intermediate host and therefore its transmission rate. However, elevated temperature could affect the behavioural manipulation indirectly through effects on many parameters of the metabolism of acanthocephalans (Labaude et al, 2020). For example, a faster development of acanthocephalans induced by warmer temperature reduced the time to reach the infective cystacanth stage in their intermediate host.…”

Effect of urbanization on zoonotic gastrointestinal parasite prevalence in endemic toque macaque (Macaca sinica) from different climatic zones in Sri Lanka

“…Among the three sub species inhabiting different climatic zones of the island, M. s. sinica found in the dry zone harbour a higher prevalence of GI parasites compared to the other two subspecies. This may be due to increase infection success and faster development in parasites in the high temperature than in relatively low temperature ranges ( Labaude et al, 2020 ). Maximum temperature is an important variable in determining soil-transmitted helminth distribution owing to effect of heat and low humidity of the soil on the embryonation, development and survival of free-living infective stages ( Brooker et al, 2003 ).…”