A complete Holocene record of trematode–bivalve infection and implications for the response of parasitism to climate change

Abstract

Increasing global temperature and sea-level rise have led to concern about expansions in the distribution and prevalence of complex-lifecycle parasites (CLPs). Indeed, numerous environmental variables can influence the infectivity and reproductive output of many pathogens. Digenean trematodes are CLPs with intermediate invertebrate and definitive vertebrate hosts. Global warming and sea level rise may affect these hosts to varying degrees, and the effect of increasing temperature on parasite prevalence has proven to be nonlinear and difficult to predict. Projecting the response of parasites to anthropogenic climate change is vital for human health, and a longer term perspective (10 4 y) offered by the subfossil record is necessary to complement the experimental and historical approaches of shorter temporal duration (10 −1 to 10 3 y). We demonstrate, using a high-resolution 9,600-y record of trematode parasite traces in bivalve hosts from the Holocene Pearl River Delta, that prevalence was significantly higher during the earliest stages of sea level rise, significantly lower during the maximum transgression, and statistically indistinguishable in the other stages of sea-level rise and delta progradation. This stratigraphic paleobiological pattern represents the only long-term high-resolution record of pathogen response to global change, is consistent with fossil and recent data from other marine basins, and is instructive regarding the future of disease. We predict an increase in trematode prevalence concurrent with anthropogenic warming and marine transgression, with negative implications for estuarine macrobenthos, marine fisheries, and human health.parasites | disease | global warming | paleoecology | mollusks P redictions for the increase of global temperature and concomitant sea-level rise in the coming decades and centuries have led to concerns about the range expansion or shift of parasites and pathogens to higher latitudes, resulting in an increase in prevalence and severity of diseases. Indeed, environmental factors such as temperature, humidity, and precipitation can strongly influence the infectivity and reproductive output of many pathogens (1, 2); however, the life cycles of parasites can be quite complex, and accurately predicting how their prevalence will be influenced by these factors can be difficult. For example, digenean trematodes are complex-lifecycle parasites (CLPs) with multiple intermediate invertebrate hosts and a definitive vertebrate host. Environmental change may affect each of these hosts to varying degrees, such that a modest increase in temperature could result in an increase of parasite reproductive output and infectivity. However, a more severe increase in temperature could be beyond the thermal tolerance of one of the hosts, thus ultimately resulting in a decrease in prevalence (3)(4)(5). Still other studies have produced quantitative models and compared spatial and temporal (seasonal-to historical-scale) aspects of climatic and other environmental variables with outbreak data i...

Development of quantitative PCR assay for detection of the trematode parasite Proctoeces maculatus in the blue mussel Mytilus edulis

“…Due to the effects of climate change, northward range expansions have already occurred in other trematode species, and as global temperatures rise, even greater range expansions are expected (MasComa et al 2008, 2009, Huntley et al 2014. For some parasites, climate change is also predicted to lead to greater disease impact due to an increase in local prevalence (Mas-Coma et al 2008, Huntley et al 2014, Williams & Boyko 2016.…”

“…For some parasites, climate change is also predicted to lead to greater disease impact due to an increase in local prevalence (Mas-Coma et al 2008, Huntley et al 2014, Williams & Boyko 2016. This is likely related to higher transmission rates caused by an increase in cercarial production response to warming water temperatures (Poulin 2006).…”

“…A re cent modeling study showed that sea surface temperatures (SSTs) in the Northeast Atlantic are increasing almost 3 times faster than the global average (Saba et al 2016). Furthermore, SSTs in the Gulf of Maine are rising faster than 99% of the world's ocean waters (Pershing et al 2015).Due to the effects of climate change, northward range expansions have already occurred in other trematode species, and as global temperatures rise, even greater range expansions are expected (MasComa et al 2008, 2009, Huntley et al 2014. For some parasites, climate change is also predicted to lead to greater disease impact due to an increase in local prevalence (Mas-Coma et al 2008, Huntley et al 2014, Williams & Boyko 2016.…”

Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence

“…Fossil evidence for parasitic flatworms can be derived from (1) rare exceptionally preserved body fossils, which can be isolated (Poinar and Boucot, 2006;Dentzien-Dias et al, 2013) or remain associated with their hosts (Upeniece, 2001(Upeniece, , 2011 or (2) more commonly occur as characteristic traces or skeletal pathologies in their (intermediate) hosts, which have the potential to be traced back in the fossil record (Ruiz and Lindberg, 1989;Ruiz, 1991;Ituarte et al, 2001Ituarte et al, , 2005Huntley, 2007;Todd and Harper, 2011;Huntley and Scarponi, 2012;Huntley et al, 2014;Huntley and Scarponi, 2015;Huntley and De Baets, 2015). Parasite body fossils are scarce due to their small size, lack of hard parts and the residence within the host and/or isolation from their hosts (Conway Morris, 1981;Littlewood and Donovan, 2003;De Baets et al, 2011).…”

“…This is not straightforward since it has been demonstrated that the remains of soft-bodied helminths can be destroyed during the pearl formation process (Lauckner, 1983). However, other pathologies are believed to be more characteristic for particular lineages of parasitic flatworms such as Gymnophallidae including shell pits (Ruiz and Lindberg, 1989;Ruiz, 1991;Huntley, 2007;Todd and Harper, 2011, Figure 1(e); Huntley and Scarponi, 2012;Huntley et al, 2014;Huntley and Scarponi, 2015;Huntley and De Baets, 2015) and volcano-to igloo-shaped calcareous concretions (Campbell, 1985;Ituarte et al, 2001Ituarte et al, , 2005; Figure 2(aec); Huntley and De Baets, 2015). Ituarte et al (2001Ituarte et al ( , 2005) demonstrated a link between igloo-shaped concretions and gymnophallid digenean flatworms, which these authors traced back to 6400 years in the Holocene.…”