Cockle infection by Himasthla quissetensis - II. The theoretical effects of climate change

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Cockle infection by Himasthla quissetensis — II. The theoretical effects of climate change

Xavier de Montaudouin

^a,

⁎ , Hugues Blanchet

^a

, Céline Desclaux-Marchand

^a

, Hocein Bazairi

^b

, Nazik Alfeddy

^b

, Guy Bachelet

^a

aUMR EPOC 5805, Université de Bordeaux-CNRS, Station Marine d'Arcachon, 2 rue du Professeur Jolyet, 33120 Arcachon, France

bUniversity Mohammed V-Agdal, Faculty of Sciences, 4 Av. Ibn Battota, Rabat, Morocco

a b s t r a c t a r t i c l e i n f o

Article history:

Received 29 September 2014

Received in revised form 19 December 2014 Accepted 22 December 2014

Available online xxxx

Keywords:

Parasitism Trematodes Cockles Climate change Temperature

Numerous marine populations experience parasite pressure. This is the case of the cockles

Cerastoderma edule

which are often highly infected by trematode macroparasites. These parasites display a complex life cycle, with a succession of free-living and parasitic stages. Climate, and in particular temperature, is an important modulator of the transmission dynamics of parasites. Consequently, global change is thought to have implications for the epidemiology of infectious diseases. Using

Himasthla quissetensis, a dominant parasite of cockles as 2nd intermedi-

ate host in Arcachon Bay (France), we used mathematical models of parasite emergence (cercariae) and parasite infection (metacercariae) in cockles as a function of water temperature, in order to study different scenarios of temperature increases. Globally, with a +0.5 °C to +6.0 °C simulation, cumulated emergence of cercariae and accumulation of metacercariae tended to decrease or stagnate, respectively. This is the consequence of a trade-off between sooner (spring) and later (autumn) cercariae emergence/infestation on one hand, and a longer inhibition period of cercariae emergence/infestation during the hottest days in summer. Using sea water temperature in Oualidia (Morocco) where mean annual sea temperature is 3 °C higher than in Arcachon Bay, our model predicted infestation all year long (no seasonality). The model gave a correct estimation of the total number of parasites that was expected in cockles. Conversely, observed infestation in Oualidia followed a seasonal pattern like in Arcachon Bay. These results suggest that, if temperature is a strong driver of parasite transmission, extrapolation in the frame- work of climate change should be performed with caution.

© 2015 Elsevier B.V. All rights reserved.

1. Introduction

Many marine invertebrate populations experience a parasite pressure that may, in some circumstances, play a major role in their dynamics.

Under extreme conditions, parasite-related population collapse has been observed which had a strong impact on the local economy (Bushek et al., 2012). Molluscs, in particular, commonly host trematodes (Lauckner, 1980, 1983). These macroparasites have a complex life cycle with a succession of hosts and free-living stages. There is today a general consensus to admit that a large part of these trematode life-cycles is strongly dependent on temperature, even though there is also a large in- terspeci ﬁ c variability among trematode species (Poulin, 2006). Besides, the relation between parasite processes (sporocyst/rediae maturation, cercariae emergence, metacercariae infection) and temperature can display different forms (linear, dome-shaped, logistic). Morley and Lewis (2013), in their meta-analysis on thermodynamics of cercarial development in freshwater systems, showed that temperature does not exert only substantial disproportionate effect, but that many trematode

species can demonstrate zone of thermostability over optimal tempera- ture of cercariae emergence. Beyond the fact that temperature affects directly the distribution of potential hosts and consequently the occur- rence of related trematode species (Harvell et al., 1999), it is one of the important factors driving the phenology of parasites themselves. The most studied stage is certainly the one between the fi rst and the second intermediate host. In the fi rst intermediate host (always a Mollusc), the parasite is asexually multiplying and developing cercariae larvae, without obvious effect of temperature, at least in freshwater systems (Morley and Lewis, 2013). However, cercariae emergence is related to the develop- ment rates within the molluscan host which depends on the temperature that should rise above a minimum value ( “ minimum development temperature threshold ” (Morley and Lewis, 2013)). Conversely, emer- gence of cercariae follows a seasonal pattern (de Montaudouin et al., submitted for publication; Meißner, 2001) and is dependent on tempera- ture (Mouritsen and Jensen, 1997; Poulin, 2006) but also on other abiotic factors such as salinity or light (Koprivnikar and Poulin, 2009; Koprivnikar et al., 2014; Morley et al., 2010; Shostak and Esch, 1990). Cercariae lifespan in the water is short (a few hours), and cercariae survival as well as infection ef fi ciency (in the second intermediate host) decrease with temperature increase (Evans, 1985; Fried and Ponder, 2003; Lo

Journal of Sea Research xxx (2015) xxx–xxx

⁎ Corresponding author. Tel.: +33 5 56 22 39 04; fax: +33 5 56 83 86 51.

E-mail address:x.de-montaudouin@epoc.u-bordeaux1.fr(X. de Montaudouin).

Contents lists available at ScienceDirect

Journal of Sea Research

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / s e a r e s

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2013b). In both cases, the collapse of amphipod populations was pre- dicted, with a delay of several years when temperature increase was ca. +1 °C but within a year if the increase was ca. +4 – 5 °C. Modifying the average temperature in a model has an impact on the period of infection if one considers that parasite transmission success follows a dome-shaped relation with temperature (i.e. there is an optimal tem- perature but both too low and too high temperatures have inhibiting effect). It has also possible outputs if light is another driver of infesta- tion, even assuming that light levels will remain unaffected by global change. Shortened winter periods might increase the growth potential of many parasite populations with the occurrence of more generations within a year or longer parasite release during the favourable season (Hakalahti et al., 2006). However, a modi ﬁ cation of the “ infestation window ” may also decrease the overlap of presence between parasites and their host and result in less infection and less host mortality (Paull and Johnson, 2014). Finally, another important process can also perturb any prediction: the potential adaptation of parasites and host to increasing temperature, from phenotypic plasticity to evolutionary genotypic adaptation. The variability of results obtained when challeng- ing cercariae emergence, survival and infectivity (i.e. variance compared to the mean) suggests that parasites can adapt through adaptative evolu- tion (Studer and Poulin, 2014). Another argument in favour of parasite/

host adaptation capacity consists in comparing similar parasite/host systems at different latitudes and/or in observing the similarity of infec- tion loads between sites with contrasted average temperatures (Studer et al., 2013c).

In a previous study, we evaluated the effect of temperature on emer- gence of Himasthla quissetensis (Miller & Northup, 1926) Stunkard, 1938, cercariae from dog whelks Nassarius reticulatus (Linnaeus) ( ﬁ rst interme- diate host) and monitored the infection of the second intermediate host, the cockle Cerastoderma edule (Linnaeus) in a semi-sheltered sand ﬂ at of Arcachon Bay (France) (de Montaudouin et al., submitted for publication). In the present paper, our aim was to consider the cercariae emergence model (de Montaudouin et al., submitted for publication), to perform a similar type of model for cockle infection and to explore differ- ent scenarios of temperature increase on both cercariae emergence and metacercariae accumulation rates. Then, the obtained result will be com- pared to a site in Morocco (Oualidia), where dog whelks, cockles and H. quissetensis are present and where annual temperature is currently higher than in Arcachon Bay.

2. Materials and methods

2.1. Study site

The study was conducted in Arcachon Bay (44°40 ′ N, 1°10 ′ W), a 180-km

²

macrotidal lagoon on the south-western Atlantic coast of France. The monitoring site was a sheltered sand ﬂ at in the inner part of the bay (La Canelette), where salinity range was 22 – 32. Water

ature for emergence (M = 20.8 at night and 20.3 at light), and s is the standard deviation of the optimal temperature (s = 1.74 at night and 2.71 at light).

These parameters were obtained by non-linear ﬁ tting procedure (Bates and Watts, 1988) which was performed using function nls() in R platform (R, 2014).

From this function and the water temperature values at La Canelette during 5 years, it was possible to simulate the emergence of cercariae (de Montaudouin et al., submitted for publication). In the present work, we performed additional simulations corresponding to an increase of temperature with different scenarios (i.e. different levels of temperature increase).

These additional simulations were performed to evaluate the possible consequences of temperature increase on the seasonal pattern of emer- gence and on the intensity of cercariae emergence by one ﬁ rst interme- diate host during one year. The tested range of water temperature increase was between +0.5 and +6 °C, in accordance with the different scenarios proposed by the last Intergovernmental Panel on Climate Change report (IPCC, 2013).

2.3. Model of H. quissetensis infection in cockles

Five one-year cockle transplant experiments were performed in Arcachon Bay from 1998 to 2002, from a site where cockles were free of H. quissetensis ( “ Arguin ” ) to a site where infection was reported ( “ La Canelette ” ). The number of H. quissetensis metacercariae per cockle was determined each month (de Montaudouin et al., submitted for publication). The 5-years survey of both temperature and metacercariae accumulation was used to ﬁ t a mathematical model simulating the number of metacercariae infecting an average cockle as a function of water temperature.

This model allowed us to simulate the effect of a water temperature increase (climate change) on cockle infection. The range of tested temperature was similar to the one previously mentioned for cercariae emergence (+0.5 to +6 °C). The simulation was based on an average water temperature pro fi le corresponding to the mean of the fi ve water temperature pro fi les measured during the fi ve consecutive years of survey.

A similar non linear curve ﬁ tting method was used than those de- scribed in § 2.2 (Eq. (1)) to ﬁ t a Lorentz function to these experimental data.

While this equation only considers cercariae emergence according to water temperature, the sister paper also considers cercariae longevity and infectivity (de Montaudouin et al., submitted for publication).

2.4. Cockle infection in warmer waters: the case of Oualidia (Morocco)

Oualidia is an Atlantic lagoon (32°44 ′ N, 9°01 ′ W) which also

harbours cockles (C. edule), dog whelks (N. reticulatus) and the trematode

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H. quissetensis. We utilized an unpublished database (2010 sampling) containing: 1) monthly water temperatures, and 2) infection patterns of 20-mm shell length C. edule by the trematode H. quissetensis; the monthly accumulation of metacercariae per cockle was deduced from these data and compared (order of magnitude) to infection pattern predicted by our model when using sea water temperatures recorded in Oualidia.

3. Results

3.1. Simulation of cercariae emergence under increasing temperature scenarios

The simulation of cercariae emergence based upon the sea water temperatures recorded at La Canelette during a ‘ standard ’ year (mean across 1998 – 2002 periods) (Fig. 1a) displayed two peaks of emergence when water temperature was ca. 19 – 20 °C (beginning of May to mid- July and beginning of September to beginning of October) (Fig. 1b). Be- tween these peaks, a 50% drop of emergence was observed for water temperature N 22 °C during the middle of the summer period, and no

emergence occurred from beginning of November to beginning of May when water temperature was b 15 °C. When applying an increase to the averaged sea water temperature pro ﬁ le, the general trend was a decrease of cercariae emergence by dog whelks that remained b 5%

at + 2 °C, but would reach − 10% at + 3 °C and − 18% at 6 °C (Fig. 2).

This trend is mostly related to the fact that a temperature increase inhibits cercariae emergence during summer when temperature is getting too high, and that the decrease is not compensated by an earlier emergence in spring and a later emergence in autumn (Fig. 1b).

3.2. Model of H. quissetensis infection in cockles

The function that best ﬁ tted the daily rate of metacercariae infection in a cockle (I) according to temperature (T, in °C) was (Fig. 3):

I ¼ 0 : 573 e

⁻¹²

T−19:6

ð Þ²

3:06²

: ð 2 Þ

Fig. 1.Figure 1: (a) Mean sea water temperature from 1998 to 2002 at La Canelette, with the possible“window”of infection (grey rectangle, 15 °CbT °b25 °C). Two scenarios of temperature increase, + 3 °C and +6 °C are drawn. (b) Corresponding theoretical emergence ofHimasthla quissetensiscercariae per day and per dog whelkNassarius reticulatus, calculated from Eq.(1)(see text), with mean sea temperature at La Canelette and two temperature increase scenarios (+3 °C and +6 °C). The possible total amount of cercariae emerging per year and per dog whelk is mentioned.

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3.3. Simulation of temperature increase effects

From Eq. (2) and temperature recorded at La Canelette between 1998 and 2002 (Fig. 1a), the theoretical infection of cockles by metacercariae was estimated (Fig. 4).

When averaging all ﬁ ve years, a bi-modal pattern of infection was obtained. Infection theoretically started in March, reached a maximum between June and mid-July, dropped until the end of August, reached again a maximum at the beginning of October to de ﬁ nitively drop by the end of November. The average number of cumulated metacercariae per cockle during an average year was 86.

Then, a simulation of temperature increase was performed by + 0.5 °C steps until + 6 °C which corresponds to the upper estima- tion of IPCC (2013). When applying a temperature increase to the averaged sea water temperature pro ﬁ le (Fig. 1a), there was only a very small variation of the infection by cockles (Fig. 5). This trend is mostly related to the fact that inhibition of infection during summer, when temperature is getting too high, is equally balanced by infection possibility during spring and autumn, and even during winter (Fig. 4).

3.4. Cockle infection at Oualidia (Morocco)

In Oualidia lagoon, the mean sea water temperature ﬂ uctuated from 16.1 °C in December to 22.1 °C in August, which represented in average a +3 °C increase compared to Arcachon Bay temperature. However, the pattern was different because Oualidia temperature was 1.7 °C cooler than in Arcachon Bay in August and 9.5 °C warmer in December (Fig. 6a). The general result was that, according to our model, infection of cockles by H. quissetensis was potentially possible all year long in Oualidia (Fig. 6b) with a total of 178 metacercariae accumulated per cockle and per year. Observed results showed a different pattern with no infection during winter and some series of infection pulses between April and December leading to a total of 79 metacercariae cumulated per cockle in the course of one year.

4. Discussion

As already observed for cercariae emergence and temperature (de Montaudouin et al., submitted for publication), the relation between H. quissetensis metacercariae accumulation rate in C. edule and water temperature ﬁ ts a dome-shaped curve. This major result explains that our model predicts a decrease of cercariae emergence and a relative stability of metacercariae accumulation in cockles in relation with a pu- tative increase of average yearly sea surface temperature. A maximum increase of + 6 °C in water temperature was tested, corresponding to one of the worst scenarios predicted for 2100 (IPCC, 2013). Concerning cercariae, the drop of emergence is predicted beyond + 1 °C and reaches − 10% for +3 °C and − 18% for +6 °C. This predicted decrease is directly due to the mathematical form of the function and to the fact that, even today, sea water temperature during summer is close to cercarial emergence inhibition ( N 22 °C). Therefore, if sea water temper- ature increases all year long, cercarial emergence will start earlier and stop later in the year (this prediction does not take into account a possible but unknown time of restoration for rediae to develop new cercariae, a time which could also depend on temperature). This dis- placement of infestation period ranks among the expected conse- quences of climate change (Hakalahti et al., 2006; Marcogliese, 2001; Paull and Johnson, 2014; Pickles et al., 2013). However, this net increase of cercariae shed in the water will not compensate the lon- ger period of inhibition during warmer summers. The same pattern was observed concerning metacercariae accumulation in cockles, except that in this case the shorter (spring) and later infection (autumn) in a year was compensated by the longer summer inhibition period. Then,

Fig. 3.Number ofHimasthla quissetensismetacercariae per cockleCerastoderma eduleand

per day (+1 standard deviation) according to water temperature, at La Canelette, from transplant experiment (Observed, black line) andﬁtted by the model (Model, grey curve, Eq.(2)) (see text).

Fig. 2.Theoretical number ofHimasthla quissetensiscercariae emerged per year and per dog whelkNassarius reticulatus(+/- 1 standard error) according to possible sea temperature increase scenarios at La Canelette. The theoretical number of cercariae was obtained from the model.

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the expected result was that water temperature increase would not im- pact cockle infection. One of the uncertainties about this scenario is that it does not take into account the effect of temperature on the physiology of the cockle. For example, clearance rate of cockles is also affected when temperature is b 8 °C or N 20 °C (Brock and Kofoed, 1987). One other major uncertainty about this scenario concerns the homogeneity of the temperature increase during the year. We hypothesized that tem- perature would increase evenly along the year but it is possible that this increase would be uneven among seasons. For example, if temperature does not increase in summer months, the inhibitory period would not compensate anymore and an increase of infection might be noticed.

However, the lack of a signi ﬁ cant increase of infestation with tempera- ture enhancement is not in disagreement with some previous studies.

Morley and Lewis (2008) proposed that short-term ﬂ uctuations in hel- minth prevalence in intermediate hosts could be compensated by the stability in ﬁ nal host, allowing recovery to occur rapidly following ex- treme climate events. Studer and Poulin (2014), with a more large- scale analysis, proposed that the variability of phenotypes (and related genotypes) observed in parasites could contribute to an adaptation in a case of global change. As an illustration, Studer et al. (2013c) demon- strated that there was no latitudinal or temperature related pattern

that could be identi fi ed for metacercariae abundance in a large scale ep- idemiological study in New-Zealand (10° latitude gradient, ca. 6 °C an- nual temperature range (12 to 18 °C)). These authors identi fi ed the infection level of the fi rst intermediate host as the main predictor, but this latter might be itself temperature dependent. Besides, the relatively long generation time of trematodes (compared to e.g. microparasites) should provide a longer response time to environmental change (Mas-Coma et al., 2009). Other studies with amphipod models as sec- ond intermediate hosts assume that if the temperature increase re- mains moderate (+ 1 °C), no effect on second intermediate host will be noticed (Shim et al., 2013), or the effect would be at a long-term scale (Studer et al., 2013b). It is also salient to emphasize that most pre- dictions, including our model, do not take into account all other parasite stages. Indeed, trematodes infectivity can vary between all different eggs and larval stages under the in fl uence of similar temperature re- gimes (Morley and Lewis, In Press). Finally, authors agree in pointing out that many other factors may intervene due to the complexity of the parasite life-cycle with the succession of free-living and parasitic stages (Thieltges et al., 2008): a temperature increase may disadvan- tage host competitors (Larsen et al. 2011), compromise host resistance (Harvell et al., 1999), modulate population dynamics of decoy organ- isms (Studer et al., 2013a), etc.

The discrepancy between our model prediction and observed infes- tation dynamics of cockle in Oualidia (Morocco) argues in favour of the mismatch between simple models of infestation according to tempera- ture and ﬁ eld reality in terms of parasite-host dynamics. Of course, the model is simplistic in the way that it only considers differences of tem- peratures between both sites. It is evident that Oualidia and La Canelette also differ by several other factors, such as salinity, Chla concentration, tidal range, etc. (Gam et al., 2010). The model gives a rather good esti- mate of the total number of metacercariae that are infecting cockles:

79 observed vs. 178 predicted. The order of magnitude is correct although the model overestimates. Conversely, the model is poor to de- scribe the host-parasite dynamics. It predicts all year-long infestation (no seasonality) because temperature is always in the range of infesta- tion (15 – 22 °C), while no infestation was noticed in Oualidia between December and April (seasonality). This result suggests that either other key-factors than temperature drive cockle infection (light, hydro- dynamics, dynamics of other hosts) and/or hosts adapt to climate, by simply modulating their optima according to the environment. For ex- ample, in the study-case of H. quissetensis, optimal cercariae emergence temperature is 25 °C in warm waters of South Carolina (Craig, 1975), vs.

20 °C in the temperate waters of Arcachon Bay (de Montaudouin et al.,

Fig. 4.Theoretical infection byHimasthla quissetensismetacercariae per day and per cockleCerastoderma edule, calculated from Eq.(2)(see text), with mean sea water temperature at La Canelette and two temperature increase scenarios (+3 °C and + 6 °C).

Fig. 5.Simulated theoretical number ofHimasthla quissetensismetacercariae per day and per cockleCerastoderma edule(+/- 1 standard error) according to possible sea water temperature increase at La Canelette.

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submitted for publication). The question of how likely and how long is necessary for parasites and their hosts to adapt to global change remains to be determined.

Acknowledgements

Many thanks to the staff of the National Reserve of Banc d'Arguin (33-France) and to Pascal Lebleu for his help. This work was partly ﬁ nanced by PNEC French programme (Programme National Environnement Côtier, University/Ifremer/CNRS-UMR-5805 n°2003/

1140739). CDM PhD scholarship was provided by the French Ministry of Research. Many thanks to both referees for their accurate and exhaus- tive comments on this paper (and its sister paper!).

References

Bates, D.M., Watts, D.G., 1988.Nonlinear regression analysis and its applications. Wiley and Sons, New York.

Berkhout, B.W., Lloyd, M.M., Poulin, R., Studer, A., 2014.Variation among genotypes in re- sponses to increasing temperature in a marine parasite: evolutionary potential in the face of global warming. Int. J. Parasitol. 44, 1019–1027.

Brock, V., Kofoed, L.H., 1987.Species speciﬁc irrigatory efﬁciency inCardium(Cerastoderma) edule(L.) andC. lamarcki(Reeve) resonding to different environmental temperatures.

Biol. Oceanogr. 4, 211–226.

Bushek, D., Ford, S.E., Burt, I., 2012.Long-term patterns of an estuarine pathogen along a salinity gradient. J. Mar. Res. 70, 225–251.

Craig, L.H., 1975.Himasthla quissetensisandLepocreadium setiferoides: emergence patterns from their molluscan host,Nassarius obsoletus. Exp. Parasitol. 38, 56–63.

de Montaudouin, X., Blanchet, H., Lavesque, N., Desclaux-Marchand, C., Bachelet, G., 2015.

Cockle infection by Himasthla quissetensis — I. From cercariae emission to metacercariae infection. J. Sea Res. (submitted for publication).

Evans, N.A., 1985.The inﬂuence of environmental temperature upon transmission of the cercariae ofEchinostoma liei(Digenea: Echinostomatidae). Parasitology 90, 269–275.

Fried, B., Ponder, E.L., 2003.Effects of temperature on survival, infectivity andin vitro encystment of the cercariae ofEchinostoma caproni. J. Helminthol. 77, 235–238.

Gam, M., de Montaudouin, X., Bazaïri, H., 2010.Population dynamics and secondary produc- tion of the cockleCerastoderma edule: comparison between Merja Zerga (Moroccan Atlantic Coast) and Arcachon (French Atlantic coast). J. Sea Res. 63, 191–201.

Hakalahti, T., Karvonen, A., Valtonen, E.T., 2006.Climate warming and disease risks in temperate regions—Argulus coegoniandDiplostomum spathaceumas case studies.

J. Helminthol. 80, 93–98.

Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W., Vasta, G.R., 1999.Emerging marine diseases-climate links and anthropogenic factors.

Science 285, 1505–1510.

Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S., Samuel, M.D., 2002.Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.

IPCC, 2013.Summary for policymakers. In: Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, V., Midgley, P.M. (Eds.), Climate Change 2013: The Physical Science Basis. Contribution of the Working Group I of the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.

Cambridge University Press, Cambridge (UK), New York (USA), p. 31.

Fig. 6.(a) Mean observed sea water temperature at La Canelette (Arcachon Bay, France) (full line) and at Oualidia (Morocco) (dotted line). (b) Simulated theoretical infection byHimasthla quissetensismetacercariae per day and per cockleCerastoderma edule, calculated from Eq.(2)(see text), with mean sea temperature at La Canelette (Canelette sim) and Oualidia (Oualidia sim) and observed infection at Oualidia (Oualidia obs). The scenario of La Canelette +3 °C (Canelette sim T ° + 3) is also plotted for comparison with Oualidia (Oualidia obs).

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Koprivnikar, J., Poulin, R., 2009.Effects of temperature, salinity, and water level on the emergence of marine cercariae. Parasitol. Res. 10, 957–965.

Koprivnikar, J., Ellis, D., Shim, K.C., Forbes, M.R., 2014.Effects of temperature and salinity on emergence ofGynaecotyla aduncacercariae from the intertidal gastropodIlyanassa obsoleta. J. Parasit. 100, 242–245.

Larsen, M.H., Jensen, K.T., Mouritsen, K.N., 2011.Climate inﬂuences parasite-mediated competitive release. Parasitology 138, 1436–1441.

Lauckner, G., 1980.Diseases of Mollusca: Gastropoda. In: Kinne, O. (Ed.), Diseases of Marine Animals. Wiley, Chichester, pp. 311–424.

Lauckner, G., 1983.Diseases of Mollusca: Bivalvia. In: Kinne, O. (Ed.), Diseases of Marine Animals. Biologische Anstalt Helgoland, Hamburg, pp. 477–961.

Lo, C.T., Lee, K.M., 1996.Pattern of emergence and the effects of temperature and light on the emergence and survival of Heterophyid cercariae (Centrocestus formosanusand Haplorchis pumilio). J. Parasit. 82, 347–350.

Marcogliese, D.J., 2001.Implications of climate change for parasitism of animals in the aquatic environment. Can. J. Zool. 79, 1331–1352.

Mas-Coma, S., Valero, M.A., Bargues, M.D., 2009.Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistomiasis. Vet. Parasitol. 163, 264–280.

Meißner, K., 2001.Infestation pattern of microphallid trematodes inCorophium volutator (Amphipoda). J. Sea Res. 45, 141–151.

Meißner, K., Bick, A., 1999.Laboratory studies of parasite transmission aspects between Hydrobiaspp. (Gastropoda) andCorophium volutator(Amphipoda). Int. Rev.

Hydrobiol. 84, 61–72.

Morley, N.J., Lewis, J.W., 2008.The inﬂuence of climatic conditions on long-term changes in the helminth fauna of terrestrial molluscs and the implications for parasite transmission in southern England. J. Helminthol. 82, 325–335.

Morley, N.J., Lewis, J.W., 2013.Thermodynamics of cercarial development and emergence in trematodes. Parasitology 140, 1211–1224.

Morley, N.J., Lewis, J.W., 2015. Thermodynamics of trematode infectivity. Parasitology http://dx.doi.org/10.1017/S0031182014001632(in press).

Morley, N.J., Adam, M.E., Lewis, J.W., 2010.The effects of host size and temperature on the emergence ofEchinoparyphium recurvatumcercariae fromLymnaea peregraunder natural light conditions. J. Helminthol. 84, 317–326.

Mouritsen, K.N., 2002.TheHydrobia ulvae–Maritrema subdolumassociation: cercarial emergence controlled by host activity. J. Helminthol. 76, 349–353.

Mouritsen, K.N., Jensen, K.T., 1997.Parasite transmission between soft-bottom inverte- brates: temperature mediated infection rates and mortality inCorophium volutator.

Mar. Ecol. Prog. Ser. 151, 123–134.

Mouritsen, K.N., Tompkins, D.M., Poulin, R., 2005.Climate warming may cause a parasite- induced collapse in coastal amphipod populations. Oecologia 146, 476–483.

Paull, S.H., Johnson, P.T.J., 2014.Experimental warming drives a seasonal shift in the timing of host-parasite dynamics with consequences for disease risk. Ecol. Lett. 17, 445–453.

Pechenik, J.A., Fried, B., 1995.Effect of temperature on survival and infectivity of Echinostoma trivolviscercariae: a test of the energy limitation hypothesis. Parasitolo- gy 111, 373–378.

Pickles, R.S.A., Thornton, D., Feldman, R., Marques, A., Murray, D.L., 2013.Predicting shifts in parasite distribution with climate change: a multitrophic level approach. Glob.

Chang. Biol. 19, 2645–2654.

Poulin, R., 2006.Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.

R, 2014.A language and environment for statistical computing. R Foundation for statistical computing, Vienna.

Shim, K.C., Koprivnika, J., Forbes, M.R., 2013.Variable effects of increased temperature on a trematode parasite and its intertidal hosts. J. Exp. Mar. Biol. Ecol. 439, 61–68.

Shostak, A.W., Esch, G.W., 1990.Photocycle-dependent emergence by cercariae of Halopegus occidualisfromHelisoma anceps, with special reference to cercarial emergence patterns as adaptations for transmission. J. Parasit. 76, 790–795.

Studer, A., Poulin, R., 2014.Analysis of trait mean and variability versus temperature in trematode cercariae: is there scope for adaptation to global warming? Int. J. Parasitol. 44, 403–413.

Studer, A., Thieltges, D.W., Poulin, R., 2010.Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Mar. Ecol. Prog. Ser. 415, 11–22.

Studer, A., Kremer, L., Nelles, J., Poulin, R., Thieltges, D.W., 2013a.Biotic interference in parasite transmission: can the feeding of anemones counteract an increased risk of parasitism in amphipods at higher temperature? J. Exp. Mar. Biol. Ecol. 445, 116–119.

Studer, A., Poulin, R., Tompkins, D.M., 2013b.Local effects of a global problem: modelling the risk of parasite-induced mortality in an intertidal trematode-amphipod system.

Oecologia 172, 1213–1222.

Studer, A., Widmann, M., Poulin, R., Krkošek, M., 2013c.Large scale patterns of trematode parasitism in bivalve host: no evidence for a latitudinal gradient in infection levels.

Mar. Ecol. Prog. Ser. 491, 125–135.

Thieltges, D.W., Jensen, K.T., Poulin, R., 2008.The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407–426.