Integrative and Comparative Biology Integrative and Comparative Biology, volume 56, number 4, pp. 611–619 doi:10.1093/icb/icw036 Society for Integrative and Comparative Biology

SYMPOSIUM

The Distribution and Abundance of Parasites in Aquatic Ecosystems in a Changing Climate: More than Just Temperature David J. Marcogliese1 Aquatic Contaminants Research Division, Water Science and Technology Directorate, Science and Technology Branch, Environment and Climate Change Canada, St. Lawrence Centre, 105 McGill, 7th floor, Montreal, Quebec, Canada H2Y 2E7 From the symposium ‘‘Parasites and Pests in Motion: Biology, Biodiversity, and Climate Change’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2016 in Portland, Oregon. 1E-mail: [email protected]

Synopsis Evaluation of the potential response of parasites of aquatic organisms to climate change illustrates the complexity of host– parasite relationships and the difficulty of making accurate predictions for these biological systems. In recent years, trematodes have proven to be a useful model to evaluate potential effects of climate change on host–parasite systems. In the first part of this article, I review and summarize results from the recent use of trematodes and specifically their early life cycle stages in testing effects of temperature and other climate-driven variables on life history traits and host– parasite interactions. However, metazoan parasites in aquatic systems respond directly to changes in temperature and also to changes in other climate-driven abiotic parameters that are mediated directly on the parasite or indirectly through changes in the distribution and abundance of their hosts. In addition, though most research to date has focused on the effects of temperature, it is imperative to explore effects of precipitation, eutrophication, acidification, water levels and flow rates, habitat loss and fragmentation, extreme weather, and other forms of anthropogenic interference on the distribution of both hosts and parasites, as these biotic and abiotic factors and stressors do not operate independently of climate. In the second part of this article, the effects of some of these factors derived from our own field studies, as well as other investigations both in the laboratory and the field, on the distribution, abundance, and community structure of parasites in aquatic ecosystems will be reviewed and discussed.

Introduction particularly their cercariae have proven to be useful Since 2007, there has been an upsurge in studies experimental models to evaluate potential effects of exploring the linkages between infectious disease temperature and other climate-driven variables on and climate change (Altizer et al. 2013). In the nu- host–parasite systems. While the effects of climate merous reviews on the subject, several emphasize change on disease are usually framed primarily in aquatic ecosystems (Harvell et al. 1999, 2002; Hayes terms of increases in temperature and changes in et al. 2001; Marcogliese 2001, 2008; Marcos-Lo´pez precipitation, Marcogliese (2001) emphasized the in- et al. 2010; Lo˜hmus and Bjo¨rklund 2015). The ma- direct effects of climate change on eutrophication, jority of studies have focused on chytridiomycosis in stratification, ice cover, acidification, water levels, amphibians (Lips et al. 2008; Rohr et al. 2008, 2011; flow rates, oceanic currents, ultraviolet-light penetra- Blaustein et al. 2010; Rohr and Raffel 2010; Hof et al. tion, and extreme weather. Furthermore, other forms 2011) and infectious diseases in corals (Rosenberg of anthropogenic interference, such as habitat loss and Ben-Haim 2002; Bruno et al. 2007; Harvell et and fragmentation, pollution, species introductions, al. 2007; Sokolow 2009; Ruiz-Moreno et al. 2012), and hydrological modifications interact with climate both of which are the focus of conservation con- change (Marcogliese 2008). Herein, I follow up on cerns. However, in recent years trematodes and these general themes, with a focus on metazoan

Advanced Access publication June 1, 2016 ß Crown copyright 2016. 612 D. J. Marcogliese parasites in aquatic ecosystems, concentrating on de- ranges (20–25 8C) for mid- and low-latitude trema- velopments during the last 10 years. More specifi- tode species, but declined at higher temperatures cally, this article discusses first, the frequent and (Morley and Lewis 2013). These results contradict increasing use of freshwater and marine trematodes those of Poulin (2006), who did not account for as experimental systems to test effects of temperature acclimation of infected snails to experimental tem- increases due to climate change, emphasizing the peratures used in laboratory studies. Shedding also need to account for life cycle complexity, and varied differentially among sites, salinities, and second, recent studies from our laboratory and water levels, depending on the parasite species others on parasite populations and communities re- (Koprivnikar and Poulin 2009a, 2009b). In these lated to potential indirect effects of climate change. studies, however, snails were not acclimated and re- Trematodes of medical significance have been sults should be interpreted cautiously (Morley and studied in the laboratory for decades, and new Lewis 2013). host–parasite experimental systems appear on a reg- Cercarial survival and activity also were differen- ular basis as different host–parasite interactions tially affected by increasing temperature and salinity become the subject of study and manipulation. In among trematode species that infected the same spe- recent years, trematodes have been very popular cies of molluscan host (Koprivnikar et al. 2010). models for parasitological studies investigating cli- Given that climate change will impact salinity and mate change and its effects on host–parasite interac- water levels as well as temperature (Marcogliese tions. Typically, they have an obligate molluscan first 2001), and that different parasites respond differen- intermediate host, often a snail, in which the larval tially to various environmental parameters, it be- parasite asexually produces tens, hundreds, or even comes difficult to predict effects of a warmer thousands of cercariae. Molluscan first intermediate climate on parasite transmission based solely on tem- hosts release cercariae into the environment, where perature, even within the same host species or they infect the next host in the life cycle. This por- among host populations. To complicate climate tion of the life cycle has proven relatively amenable change scenarios even further, other studies have to experimentation and manipulation. The high suggested that cercarial production and activity can number of cercariae released, referred to as produc- vary with the strain or genotype of molluscan host tivity, permits sufficient sample sizes and replicability (Morley 2011; Morley and Lewis 2013; Berkhout et in experimental design. The effects of temperature al. 2014). have been, and continue to be, the primary focus However, physiological tolerances and thermal of studies on potential impacts of climate change optima vary not only among parasite species but on these parasites and others. among life stages within species (Marcogliese 2001; Barber et al. 2016). For trematode miracidia, which hatch from eggs and infect molluscs, a meta-analysis Empirical studies on temperature of published experimental results showed that all In recent years, numerous experimental studies have trematode species examined exhibited distinct zones examined the effects of temperature on cercarial re- of thermostability and temperature had only limited lease, survival and activity of different trematode spe- effect on survival and metabolism. Miracidia (which cies, often with unexpected results. Among infected hatch from eggs and infect snails) proved more ther- estuarine snails, cercarial shedding (productivity) in- mally resistant than cercariae, with climate change creased with increasing temperature in certain trem- apparently having limited impact on this segment atode species and decreased in others even though of a trematode’s life cycle (Morley 2012). some infected the same host species (Koprivnikar Furthermore, another meta-analysis on published ex- and Poulin 2009a, 2009b). In a meta-analyses of perimental data did not detect an effect of tempera- published experimental results, Poulin (2006) found ture on parasite development within the molluscan that cercarial emergence increased up to 200-fold host (Morley and Lewis 2013). following a 108C rise in temperature. The increases Thus, in order to better predict effects of climate in cercarial productivity were much higher than change, it is important to consider the net effect of would be predicted from those estimated from the temperature on a parasite’s entire life cycle. temperature sensitivity of most physiological pro- Logistically, this is a daunting task, but a few pio- cesses (Q10 of 2–3). In another meta-analysis, neering studies have examined the effects of temper- while accounting for a minimum emergence temper- ature on different life history traits and parasite–host ature threshold and acclimation, emergence was un- interactions at different stages of a life cycle in trem- affected by temperature over relatively wide optimal atodes. One series of studies was carried out on an Distribution and abundance of parasites 613 estuarine trematode (Maritrema novaezealandensis) the timing of infection at key and possibly vulnerable that infects snails, amphipods, and birds (Studer points in the hosts’ susceptibility to infection (Paull et al. 2010; Studer and Poulin 2013), and another and Johnson 2011; Paull et al. 2012; see also discus- examined a freshwater trematode (Ribeiroia onda- sion on host–parasite synchronicity in Marcogliese trae) that infects snails, frogs, and birds (Paull and 2001). Johnson 2011; Paull et al. 2012; Paull et al. 2015; Experiments repeated under conditions of vary- Altman et al. 2016). In these cases, the authors fo- ing temperatures, which better simulate natural cused on parasite–host interactions within ectother- conditions in wetlands and intertidal habitats, dif- mic hosts in which, presumably, temperature effects ferentially affected both trematode and host life his- should be most pronounced (Marcogliese 2008; but tory traits compared with those carried out under see Morley and Lewis 2014a). A summary of exper- constant temperature conditions (Studer and Poulin imental results is presented in Table 1 and Table 2 2013; Paull et al. 2015). Importantly, parasites and for the two different host–parasite systems. Productivity hosts responded differently to the same acclima- and rate processes of many life history traits (e.g., tion temperature (Altman et al. 2016). Thermal host growth and fecundity, parasite development acclimation led to different temperature effects and activity) simply increased with temperature on the resistance of the anuran host to infection (Paull and Johnson 2011; Paull et al. 2012), while by R. ondatrae cercariae and the clearance of es- others (e.g., parasite survival and infectivity) de- tablished metacercariae by the host. Thus, the host creased (Paull et al. 2012). A common pattern ob- appears to use separate immune mechanisms to served in different host–parasite systems was that combat different parasite stages of infection (cer- cercarial survival decreased with increasing temper- carial establishment vs. metacercarial persistence) ature (Studer et al. 2010; Morley 2011; Paull et al. that respond differently to temperature variability 2012; Studer and Poulin 2014). However, Morley’s (Altman et al. 2016). Furthermore, it is important (2011) meta-analysis of published laboratory stud- to consider the magnitude and the frequency of ies demonstrated that cercariae tended to display temperature variability in predicting parasite dy- zones of thermostability, resulting in minimal ef- namics under a changing climate (Paull et al. 2015). fects of climate change on survival under the pre- Taken as a whole, these studies on trematodes dem- dicted temperature-change scenarios on the order onstrate that temperature has differential effects on of 2–4 8C (Morley 2011). parasites, their hosts and host–parasite interactions Some parasite life history traits peaked then de- that vary among host and parasite species and the creased with increasing temperatures, again a pattern life history stages of the parasite itself. observed among many trematode species (Studer et al. 2010; Morley 2011; Studer and Poulin 2014; Empirical studies on other factors Morley and Lewis 2015). Life history traits of the first intermediate molluscan hosts and the second Extreme weather intermediate hosts also were affected differentially Extreme weather provides the opportunity to exam- by temperature and depended on whether they ine disease and parasite dynamics in novel conditions were infected or not, with effects also differing be- that may mimic future climate change (Studer and tween first and second intermediate hosts for the Poulin 2014). Prolonged heat waves can disrupt par- same parasite (Studer et al. 2010; Paull and asite transmission and increase parasite-induced Johnson 2011; Paull et al. 2012; Morley and Lewis mortality, a realistic possibility under proposed cli- 2015). Indeed, meta-analyses derived from published mate change scenarios (Studer et al. 2010; Studer and experimental studies of infectivity of trematode mi- Poulin 2013; see also Marcogliese 2001 for a review racidia, cercariae, and metacercariae demonstrated of effects of thermal effluents on host–parasite sys- that miracidial and cercarial infectivity increases to tems). Effects of interactions between and a plateau then decreases with higher temperature, temperature can extend beyond the host–parasite while that of metacercaria decreases (Studer and system in question to the entire community of Poulin 2014 for cercaria only; Morley and Lewis which they are a part. Parasite-induced mortality of 2015). the amphipod Corophium volutator, an important in- Pathology in some invertebrate intermediate hosts termediate host for microphallid trematodes and a increases with temperature while in other hosts it known ecosystem engineer, influences the structure may peak at intermediate temperatures (Studer of mud flat invertebrate communities in the Wadden et al. 2010; Paull and Johnson 2011; Paull et al. Sea (Poulin and Mouritsen 2006; Larsen and 2012). Warming due to climate change can alter Mouritsen 2014). A heatwave led to mass mortalities 614 D. J. Marcogliese

Table 1. Relative strength of temperature and temperature variability on different parasite and host traits in the life cycle of the intertidal trematode Maritrema novaezealandensis in its gastropod first intermediate host (Zeacumantus subcarinatus) and its amphipod second intermediate host (Paracalliope novizealandiae)

Trait Temperature (8C) 16 20 25 30 34 Cercarial productivity þ þþ þþþ þþ Cercarial survival þþþ þþ þþ þ þ Cercarial infection rate þ þþ þþþ þþ þ Amphipod susceptibility þþþþþ Amphipod survival þþþ þþ þþ –– Metacercarial development þ þþ þþþ –– Temperature variability (8C) 15 15 þ 515þ 10 15 þ 15 15 þ hw Cercarial productivity þþþþþþþþþþ Cercarial infection rate þþþþ þ þþ Amphipod survival þþþþþ Notes: Modified from Studer et al. (2010) with information from Studer and Poulin (2013). hw ¼ simulated heatwave. A þ sign indicates an increase in the measured parameter, with the number of þ signs indicating the relative strength of the effect. A – sign indicates a negative effect.

Table 2. Relative strength of temperature on different parasite 2006; Larsen and Mouritsen 2014). Removal of the and host traits in the life cycle of the freshwater trematode amphipod caused wholesale physical transformation Ribeiroia ondatrae in its gastropod first intermediate host of the mud flats, affecting primary productivity and (Planorbella trivolvis) and its anuran second intermediate host benthic community structure, and depleting the (Pseudacris regilla). major food resource for migrating shorebirds (re- Trait Temperature (8C) viewed in Marcogliese 2008). Subsequent laboratory 13 20 26 experiments (reviewed in Poulin and Mouritsen Parasite egg development – þþþ2006; Marcogliese 2008) and mesocosm studies Snail growth þ þþ þþþ (Larsen and Mouritsen 2014) supported the links between high temperature, cercarial productivity, Infected snail growth þþþþþþþ parasite-induced amphipod mortality and changes þ þþ þþþ Snail fecundity in benthic community structure. Infected snail fecundity þþþþ Other examples include studies of parasite com- Snail survival þ –– munities of the horn snail Cerithidea pliculosa,an Cercarial development ¼ þ þþþ important first intermediate host for a number of Cercarial survival þþþ þþ þ trematodes in the Yucantan before and after Cercarial penetration of frog þ þþ þþþ Hurricane Isidore in September 2001 (Aguirre- Cercarial establishment in frog þþþ þþ þ Macedo et al. 2011), fish parasite populations along Metacercarial numbers in frog þþ þþ þ the Mississippi coast following Hurricane Katrina in August 2005 (Overstreet 2007), and the impacts on Frog growth þ þþ þþþ infections of wild and domestic in terrestrial, Frog survival þþþ freshwater, and coastal marine ecosystems in the UK Frog malformations þþ þþþ þ of a major 16-month drought that occurred in 1976 Notes: Information from Paull and Johnson (2011) and Paull et al. (reviewed in Morley and Lewis 2014b). A general (2012). A þ sign indicates an increase in the measured parameter, result of the hurricanes mentioned above is that par- with the number of þ signs indicating the relative strength of the effect. A – sign indicates a negative effect. asite populations and communities crashed for a period of time ranging from months to years before becoming re-established (Overstreet 2007; of mud snails (Hydrobia ulvae) and amphipods Aguirre-Macedo et al. 2011). Given that most meta- (C. volutator), apparently caused by infection with zoan parasites have complex life cycles that include two microphallid trematodes (Microphallus clavifor- numerous hosts occurring at different trophic levels mis, Maritrema subdolum) (Poulin and Mouritsen and often rely on trophic interactions for Distribution and abundance of parasites 615 transmission, their presence suggests they are good per host fish) increased downstream of the effluent indicators of food web structure, ecosystem degrada- outflow (Marcogliese and Cone 2001; Marcogliese tion, and recovery (Marcogliese and Cone 1997; et al. 2009). The authors proposed that this was Marcogliese 2004, 2005; Overstreet 2007; Aguirre- not a toxicological, but rather an ecological effect Macedo et al. 2011; see also Okamura 2016). that results from the huge organic input from the effluent outflow into the St. Lawrence River, in Ocean acidification turn promoting oligochaete population growth in Despite ocean acidification and disease in corals and the riverine effluent waters, oligochaetes being obli- other organisms fueling increasing concerns in recent gate alternate hosts for numerous myxozoan species years, little information exists on potential effects on (Marcogliese and Cone 2001). They subsequently metazoan parasites, unlike studies on those in fresh- found oligochaete density to be higher downstream water fishes (reviewed in Marcogliese 2001, 2005). of Montreal than it was upstream, supporting the However, given that molluscs are sensitive to low hypothesis that the increase in infection was due to pH (Marcogliese 2001), it is reasonable to presume greater oligochaete densities in waters receiving efflu- that trematodes can be concomitantly affected. A ents (Marcogliese et al. 2009). Thus, the local distri- series of studies has examined the effects of pH on bution of myxozoan parasites in spottail shiners in different trematode and host life history characteris- the St. Lawrence River appeared to be affected by tics using different species of trematodes, some of eutrophication. which infect the same gastropod intermediate host Blanar et al. (2011) examined the helminth and (Hartland et al. 2015; MacLeod and Poulin 2015a). arthropod parasite fauna of mummichogs Cercariae of all trematode species displayed reduced (Fundulus heteroclitus) in the Miramichi and longevity under acidified conditions, as did metacer- Bouctouche rivers, New Brunswick as a follow-up cariae of one that encysts on the surface of inverte- to a prior series of ecotoxicological studies on effects brate transport hosts (MacLeod and Poulin 2015a). of pulp and paper mill effluents on the health of However effects of acidification and parasitism on these fish in the Miramichi. Analyses of parasite growth and length of the mud snail (Zeacumantus community structure incorporating water quality, subcarinatus) varied differentially with trematode contaminants in the fish, and host physiological species (MacLeod and Poulin 2015b). In a parallel data showed that the parasite community structure experiment, net transmission success of cercariae of was partially influenced by upstream–downstream M. novaezealandensis to its second intermediate host, differences in eutrophication as indicated by fecal the amphipod Paracalliope novizealandiae, was high- coliforms, and not chemical contaminants, from mu- est at the lowest pH tested through differential effects nicipal and pulp mill effluents (Blanar et al. 2011). on hosts and parasites (Hartland et al. 2015). Again, While this study and those above illustrate the effects the complexity of direct and indirect effects of cli- of eutrophication from anthropogenic sources, they mate change on hosts, parasites, and their interac- also demonstrate potential indirect consequences of tions renders predictions difficult. climate change on fish parasite populations and communities in a diverse array of parasites Eutrophication (Marcogliese 2001). Many freshwater systems are expected to experience Water levels and precipitation eutrophication as a result of climate change, thus affecting parasite populations and communities Under conditions of high water flow, parasite diversity (Marcogliese 2001). For example, outbreaks of sal- is seen to decrease (reviewed in Marcogliese 2001). monid proliferative kidney disease, caused by the Strong flow rates may transport small, motile, free- myxozoan bryosalmonae, known to living stages of parasites out of a system. Indeed, occur with increasing temperature, similarly may be high current flow reduced oligochaete abundance, promoted by eutrophication (Okamura et al. 2011; transmission to fish, and subsequent transmission to Okamura 2016). Both the parasite and its bryozoan oligochaetes in an experimental study on Myxobolus intermediate host proliferated at higher temperature cerebralis, the causative agent of whirling disease and nutrient levels (Okamura et al. 2011). In studies (Hallett and Bartholomew 2008). Faster currents also in the St. Lawrence River on effects of sewage efflu- reduced infections of Ceratomyxa shasta in ents on the myxozoan communities in spottail shi- invertebrate hosts (Manayunkia speciosa) and rainbow ners (Notropis hudsonius), prevalence and mean trout (Oncorhynchus mykiss) (Bjork and Bartholomew infracommunity richness (mean number of species 2009). 616 D. J. Marcogliese

Water levels in many rivers dictate water flow, communities discussed above, hydrology of the St. with high levels meaning high flow rates. Following Lawrence River, which is hugely impacted by climate up on the St. Lawrence River study above, when change, exerts a major influence on parasite commu- samples within the river were pooled by year over nity structure in fish at a large spatial scale. the entire 5-year sampling period, mean infracom- These studies provide examples illustrating fur- munity species richness of myxozoans in the spottail ther potential indirect consequences of climate shiner was negatively correlated with mean water change on parasites of aquatic organisms. It should levels measured during the month prior to fish sam- be noted that further anthropogenic regulation and pling (Marcogliese et al. 2009). Water levels in the intercession to mitigate effects of climate change St. Lawrence River are determined by precipitation may amplify other potential indirect consequences and snow melt. Thus, myxozoan diversity over the of climate change, with concomitant implications length of the river is driven by climate at a regional for flow rates, eutrophication, and other physico- scale, an effect which is superimposed over the eu- chemical parameters in aquatic ecosystems, thus fur- trophication effect discussed above, fueled by munic- ther affecting parasitism in aquatic ecosystems ipal pollution at a local scale (Marcogliese et al. (Marcogliese 2001). 2009). In a 2-year study on spottial shiners in the Salinity Richelieu River, a tributary of the St. Lawrence Sea level rise due to climate change will lead to salt River receiving municipal and agricultural effluents, water intrusion in coastal rivers, with consequences the helminth and arthropod parasite communities in for the parasite communities of fishes and other fish were drastically different between the years, aquatic organisms in coastal and low-lying areas annual variation being much greater than site varia- (Marcogliese 2008). Mummichogs are euryhaline tion within years (Marcogliese et al. 2016). Indeed, and extremely common along the eastern seaboard overall species richness at each site in 2003 was 15– of North America between the Gulf of Mexico and 18 species, declining to 9–13 species at the four sites the Gulf of St. Lawrence, Canada. In the Blanar et al. in 2004. In contrast, on the scale of an individual (2011) study discussed above, the downstream sites fish, total parasite abundance and the mean infra- in both the Miramichi and Bouctouche rivers were community richness were lower in 2003 at each brackish, while upstream sites were fresh, establishing site. These results could not be linked to any mea- a salinity gradient in both rivers. The most promi- surements of water quality or pollution. However, nent pattern in community structure was a distinct precipitation in the month prior to sampling was difference between upstream and downstream sites. 40% higher in 2003 compared with 2004, and was Mean infracommunity richness was significantly the only significant parameter consistently explaining lower at both downstream sites (Blanar et al. community structure (Marcogliese et al. 2016). The 2011). In their study, salinity appears to have a Richelieu River is artificially regulated in the section stronger effect on parasite community structure sampled, with water levels completely stable. Thus, than eutrophication (Blanar et al. 2011), even increased precipitation means higher flow rates. The though both are indirect effects of a changing cli- high flow rates in 2003 resulted in reduced diversity mate. As with the myxozoan study in spottail shi- and abundance of parasites in individual fish (see ners, large-scale patterns in water quality over large Marcogliese 2001), although the reasons for the higher overall species richness in 2003 remain sections of the rivers, in this case a salinity gradient, unclear. appear to superimpose their effects on parasite com- The St. Lawrence River downstream from munities in fishes over local effects such as eutrophi- Montreal consists of two water masses, one of high cation due to pollution. conductivity (green water) emanating from the Great Lakes to the west, and the other of low conductivity Landscape changes (brown water) draining from the Ottawa River to While habitat fragmentation typically is a indirect the north. The relative extent of the two water consequence of human actions, it likely will be exac- masses depends on the respective water volume erbated by a changing climate (Moore et al. 1997). from each drainage, which is a function of temper- Recent studies have demonstrated that parasite com- ature and precipitation. Conductivity, which differ- munity richness in frogs is linked to landscape struc- entiates the green and brown waters, was a major ture. Prevalence of the trematode parasite Alaria sp. determinant of helminth parasite community struc- in leopard frogs (Lithobates pipiens) was positively ture (Marcogliese et al. 2006). As with the myxozoan associated with surrounding forest cover surrounding Distribution and abundance of parasites 617 ponds in southern Ontario (Koprivnikar et al. 2006). Studer and Poulin 2013, 2014; Paull et al. 2015; Alaria sp. matures in mammals such as foxes, com- Altman et al. 2016). monly found in forested areas. Mean infracommu- The effects of climate change, however, are not nity richness was negatively correlated with urban limited to increasing temperature and changes in and agricultural area, also in leopard frogs, in south- precipitation. Indirect effects will impact numerous western Quebec (King et al. 2007). In bullfrogs biotic and abiotic variables in aquatic ecosystems. (Lithobates catesbeianus) from southwestern Quebec, Effects often are nonlinear due to species interac- the number of parasite species found at a locality was tions, confounding variables, temperature thresholds, negatively correlated with agricultural area, while the and context dependencies (Marcogliese 2008; Rohr et mean infracommunity richness was positively related al. 2011; Lo˜hmus and Bjo¨rklund 2015). Indeed, some to forest area surrounding ponds (King et al. 2010). environmental factors, especially those that are an- In these studies, parasites with avian and mammalian thropogenic, will overshadow or mask effects of cli- definitive hosts tended to be either lower in abun- mate change (Marcogliese 2008; Lafferty 2009). dance or absent in agricultural and urban landscapes. Studies of changes in parasite populations and com- King et al. (2007, 2010) suggested that habitat frag- munities in response to environmental change mentation due to anthropogenic landscape develop- should consider the broad picture at the ecosystem ment restricts access to wetlands by these hosts. In level, and also account for the scale of any observed another large-scale study, the abundance, richness, impacts. Indeed, there are increasing appeals for the and diversity of helminths in leopard frogs were as- interdisciplinary integration of community ecology, sociated with greater amounts of forested and woody biodiversity, and physiology into disease and climate wetland habitats, shorter distances between woody change research (Martin et al. 2010; Altizer et al. wetlands, and smaller-sized open water patches in 2013; Molna´r et al. 2013; Rohr et al. 2013). surrounding landscapes to anuran habitats (Schotthoefer et al. 2011). In terms of landscape Acknowledgments structure, local scale (1 km) was considered the I thank Chris Boyko and Jason Williams for organiz- most important for larval trematode abundances, ing the symposium ‘‘Parasites and Pests in Motion: whereas both local and regional (10 km) landscape Biology, Biodiversity and Climate Change’’ and ex- variables appeared most significant for adult hel- tending an invitation to participate as a guest minths (Schotthoefer et al. 2011). With habitat frag- speaker. Special thanks go to Drs Bruno Pernet, mentation, wetland food webs and aquatic–terrestrial Art Woods, Jane Cook, and one anonymous reviewer interactions become disrupted, followed by the re- whose comments substantially improved the article. duction or elimination of parasite species. Wetland Many of the studies mentioned in Canada and done area may also be compromised by human adaptation by the paper’s author have been supported via to climate change. Furthermore, the studies pre- Environment and Climate Change Canada’s St. sented above illustrate the importance of spatial Lawrence Action Plan. scale in determining effects of a changing climate on aquatic ecosystems. Funding Studies on the St. Lawrence and Richelieu rivers were Concluding remarks funded by Environment and Climate Change Canada’s Studies solely focusing on a single parasite species St. Lawrence Action Plan. and even single stages within parasite life cycles can lead to erroneous generalizations and predictions on References the effects of climate change on parasite transmis- Aguirre-Macedo ML, Vidal-Martı´nez VM, Lafferty KD. 2011. sion. Future research should attempt to encompass Trematode communities in snails can indicate impact and a variety of parasite species experimentally and in recovery from hurricanes in a tropical coastal lagoon. Int J situ to observe a range of potential effects. Parasitol 41:1403–8. Furthermore, transmission must be examined using Altizer S, Ostfeld RS, Johnson PTJ, Kutz S, Harvell CD. 2013. as many hosts as possible in a parasite’s life cycle to Climate change and infectious diseases: From evidence to a predictive framework. 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