Coastal ecosystems on a tipping point: Global warming and parasitism combine to alter community structure and function

Abstract

Mounting evidence suggests that the transmission of certain parasites is facilitated by increasing temperatures, causing their host population to decline. However, no study has yet addressed how temperature and parasitism may combine to shape the functional structure of a whole host community in the face of global warming. Here, we apply an outdoor mesocosm approach supported by field surveys to elucidate this question in a diverse intertidal community of amphipods infected by the pathogenic microphallid trematode, Maritrema novaezealandensis. Under present temperature (17°C) and level of parasitism, the parasite had little impact on the host community. However, elevating the temperature to 21°C in the presence of parasites induced massive structural changes: amphipod abundances decreased species-specifically, affecting epibenthic species but leaving infaunal species largely untouched. In effect, species diversity dropped significantly. In contrast, four degree higher temperatures in the absence of parasitism had limited influence on the amphipod community. Further elevating temperatures (19-25°C) and parasitism, simulating a prolonged heat-wave scenario, resulted in an almost complete parasite-induced extermination of the amphipod community at 25°C. In addition, at 19°C, just two degrees above the present average, a similar temperature-parasite synergistic impact on community structure emerged as seen at 21°C under lower parasite pressure. The heat-wave temperature of 25°C per se affected the amphipod community in a comparable way: species diversity declined and the infaunal species were favoured at the expense of epibenthic species. Our experimental findings are corroborated by field data demonstrating a strong negative relationship between current amphipod species richness and the level of Maritrema parasitism across 12 sites. Hence, owing to the synergistic impact of temperature and parasitism, our study predicts that coastal amphipod communities will deteriorate in terms of abundance and diversity in face of anticipated global warming, functionally changing them to be dominated by infaunal species.

The Ecological Importance of Amphipod–Parasite Associations for Aquatic Ecosystems

“…Birds that prey on infected amphipods are the final hosts. Several studies on the trematodes of amphipods include results on the ecological effects of the host-parasite relationship (e.g., [63,[135][136][137]).…”

“…An additive effect of temperature and parasitism has been reported in intertidal trematode-amphipod systems [136,161,163,175]. Under the conditions of increasing temperature due to global warming, trematodes could cause increased parasite-induced mortality and a substantial reduction in amphipod populations, with ecosystem-wide consequences [63,136].…”

“…The positive influence of a temperature between 20 and 25 • C on the transmission rate and the development of the parasite accounts for the predicted massive infection and mortality of the host and the possible collapse of the P. novizealandiae population due to global warming [161,162]. Mouritsen et al [136] showed in a mesocosm experiment that temperature alone was not sufficient to cause population effects, while the combination of increased temperature and parasitism (M. novaezelandensis) led to a decline of the amphipod community richness in the system. In contrast, temperature did not enhance infection or impact of another trematode (Gynaecotyla adunca) in C. volutator [176] and this suggests that not all the amphipod/parasite systems react in the same way to the same perturbing factor.…”

Environmental stressors induced strong small-scale phenotypic differentiation in a wide-dispersing marine snail

“…The transitional nature of the intertidal habitat from marine to terrestrial conditions strongly influences the physiology and the ecology of intertidal organisms due to the increase in environmental harshness (e.g. desiccation, extremes in temperature and salinity) along the vertical zonation of the intertidal area (Denny & Paine, 1998; Mouritsen, Sørensen, Poulin, & Fredensborg, 2018; Vermeij, 1972). From this perspective, intertidal organisms, such as aquatic gastropods, are likely to exhibit increased phenotypic plasticity in response to such environmental selective pressures (Berrigan & Scheiner, 2004).…”

“…Some plastic trait responses, usually those imposed by the biochemistry and physiology of the organism, can be reversed over short time scales, which is not the case for developmental plasticity as it tends to be irreversible or takes longer to be reversed (Pigliucci et al, 2006). Parasites, for instance, can induce morphological, behavioral, and physiological change of individual snail hosts thereby influencing several aspects of host life history that can significantly alter size-structure, demography, resource-use, and intra and interspecific interactions of host population (Fredensborg, Mouritsen, & Poulin, 2005; Miura, Kuris, Torchin, Hechinger, & Chiba, 2006; Mouritsen et al, 2018). They have been also reported to induce changes in microhabitat choice (Curtis, 1987) and in body size in snails (Alda, Bonel, Cazzaniga, & Martorelli, 2010; Levri, Dillard, & Martin, 2005; Miura et al, 2006; Mouritsen & Jensen, 1994; Probst & Kube, 1999).…”