Freshening rather than warming drives trematode transmission from periwinkles to mussels

In the Western Baltic Sea, climate change is happening at much faster rate than in most other seas and organisms are additionally exposed to a steep and variable salinity gradient. Climate change has previously been shown to affect parasite transmission in other marine ecosystems, yet little is known about potential effects of warming and desalination on parasite–host interactions. In laboratory experiments, we determined the combined effects of projected seawater warming and freshening on the emergence, activity, survival, and infectivity of cercariae (free-swimming infectious stage) of the trematode Himasthla elongata (Mehlis 1831), shed from its first intermediate host, the periwinkle Littorina littorea (Linnaeus 1758), in the Baltic Sea. We also assessed the susceptibility of the second intermediate host, the mussel Mytilus edulis Linnaeus, 1758, to cercarial infections. Generally, salinity was the main driver, particularly of cercarial activity, infectivity, and mussel susceptibility to infection. At the lowest salinity (13), cercariae were 50% less active compared to the highest salinity (19). Infection success and host susceptibility followed a similar pattern, with 47% and 43% less metacercariae (encysted stage) present at salinity 13 than at salinity 19, respectively. In contrast, effects of simulated warming were found only for cercarial survival, with cercarial longevity being higher at 19 than at 23 °C. No significant interactions between temperature and salinity were found. In contrast to the literature, the results suggest that a climate change-driven freshening (partly also warming) may lead to a general decline of marine trematodes, with possible beneficial effects for the involved hosts

Effects of first intermediate host density, host size and salinity on trematode infections in mussels of the south-western Baltic Sea

Trematode prevalence and abundance in hosts are known to be affected by biotic drivers as well as by abiotic drivers. In this study, we used the unique salinity gradient found in the south-western Baltic Sea to: (i) investigate patterns of trematode infections in the first intermediate host, the periwinkle Littorina littorea and in the downstream host, the mussel Mytilus edulis, along a regional salinity gradient (from 13 to 22) and (ii) evaluate the effects of first intermediate host (periwinkle) density, host size and salinity on trematode infections in mussels. Two species dominated the trematode community, Renicola roscovita and Himasthla elongata. Salinity, mussel size and density of infected periwinkles were significantly correlated with R. roscovita, and salinity and density correlated with H. elongata abundance. These results suggest that salinity, first intermediate host density and host size play an important role in determining infection levels in mussels, with salinity being the main major driver. Under expected global change scenarios, the predicted freshening of the Baltic Sea might lead to reduced trematode transmission, which may be further enhanced by a potential decrease in periwinkle density and mussel size

Heat sensitivity of first host and cercariae may restrict parasite transmission in a warming sea

To predict global warming impacts on parasitism, we should describe the thermal tolerance of all players in host–parasite systems. Complex life-cycle parasites such as trematodes are of particular interest since they can drive complex ecological changes. This study evaluates the net response to temperature of the infective larval stage of Himasthla elongata, a parasite inhabiting the southwestern Baltic Sea. The thermal sensitivity of (i) the infected and uninfected first intermediate host (Littorina littorea) and (ii) the cercarial emergence, survival, self-propelling, encystment, and infection capacity to the second intermediate host (Mytilus edulis sensu lato) were examined. We found that infection by the trematode rendered the gastropod more susceptible to elevated temperatures representing warm summer events in the region. At 22 °C, cercarial emergence and infectivity were at their optimum while cercarial survival was shortened, narrowing the time window for successful mussel infection. Faster out-of-host encystment occurred at increasing temperatures. After correcting the cercarial emergence and infectivity for the temperature-specific gastropod survival, we found that warming induces net adverse effects on the trematode transmission to the bivalve host. The findings suggest that gastropod and cercariae mortality, as a tradeoff for the emergence and infectivity, will hamper the possibility for trematodes to flourish in a warming ocean

Biotic and abiotic drivers affect parasite richness, prevalence and abundance in Mytilus galloprovincialis along the Northern Adriatic Sea

Although it is generally known that a combination of abiotic and biotic drivers shapes the distribution and abundance of parasites, our understanding of the interplay of these factors remains to be assessed for most marine host species. The present field survey investigated spatial patterns of richness, prevalence and abundance of parasites in Mytilus galloprovincialis along the coast of the northern Adriatic Sea. Herein, the relationships between biotic (host size, density and local parasite richness of mussel population) and abiotic (eutrophication and salinity) drivers and parasite richness of mussel individuals, prevalence and abundance were analysed. Local parasite richness was the most relevant factor driving parasite species richness in mussel individuals. Prevalence was mainly driven by eutrophication levels in 3 out of 4 parasite species analysed. Similarly, abundance was driven mainly by eutrophication in two parasite species. Mussel size, density and salinity had only minor contributions to the best fitting models. This study highlights that the influence of abiotic and biotic drivers on parasite infections in mussels can be differentially conveyed, depending on the infection measure applied, i.e., parasite richness, prevalence or abundance. Furthermore, it stresses the importance of eutrophication as a major factor influencing parasite prevalence and abundance in mussels in the Adriatic Se

Experiments on the life cycle of the trematode Himasthla elongata

In this experiment, we assessed the different transmission steps from the first to the second intermediate host: i) cercarial emergence from periwinkles, ii) cercarial activity and survival after emergence, iii) cercarial infectivity in mussels, and iv) susceptibility of mussels to cercarial infection. For iii) cercariae were treated but not the mussels, whereas for iv) mussels were treated but not the cercariae. The experiment was run in August-September 2017 in the climate chambers of GEOMAR in Kiel. All experiments were conducted using temperature and salinity (fully crossed) as well as time (only for cercarial output) as fixed factors, and periwinkle/mussel identity nested within water bath as random factor. Temperature levels applied were 19 and 23°C. Salinity levels applied were 13, 16 and 19

Exp. II: cercarial activity and survival

For cercarial activity and survival infected periwinkles were acclimated for three weeks under the different treatments (n=10 individuals per treatment) and incubated to allow for cercarial release. At the start of the experiment, approximately 45 cercariae per treatment were added individually to wells of three 96-well plates The 96-well plates were then exposed to the different temperature treatments placing them in the six thermobaths (three 96-well plates per treatment combination). Activity and survival were then assessed under a stereomicroscope after 4, 6, 9, 18, 27, and 45 hours. Cercariae were considered fully active when they were constantly swirling around (category: fully active). When laying at the bottom and not reacting, these were considered dead (category: dead), when still reacting, even if slowly, these were still considered alive (category: alive). This last category included "fully active"

Exp. I: cercarial emergence from periwinkles

Cercarial emergence was assessed by counting all cercariae that emerged from single periwinkles exposed to the different treatments. Periwinkles were collected in Årøsund, Denmark and screened in the laboratory to verify the infection status. To measure cercarial emergence, periwinkles were individually transferred from the jars into 50 mL Plexiglas beakers, one day after the 7-days acclimation (sampling 1), one week after the start of exposure to the treatments (sampling 2), and two weeks after the start of exposure to the treatments (sampling 3). Each incubation lasted eight hours. At the end of the incubation period, the water from each beaker was transferred into 50 mL Falcon tubes. In addition, the beakers were immediately washed with 5 mL ethanol (99%), and the solution was also added to the Falcon tube to ensure the collection of all cercariae and their preservation for later counting