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The Hidden Effects of Parasites in a Changing Ocean.

Trematode parasites are a fascinating group of species which occur in almost all types of marine habitat and infect many ecologically and commercially important marine organisms. They possess complex life histories that involve multiple host species, often radically change morphology as they move between hosts, and can dramatically alter the performance of infected organisms. (1) Trematode infection can regulate host population density by sterilising hosts, altering host foraging behaviour, and/or by increasing the likelihood of infected individuals being consumed by the next host in the parasite's life cycle. (2) This plethora of biological interactions means that trematode parasites are an extremely important component of all marine ecosystems and are embedded in these systems to a greater degree than most species.

As with all marine organisms, trematodes are affected by human-mediated changes to the global oceans--for example, warmer temperatures, less available oxygen, increased seawater acidity. Of course, given the complex nature of host-parasite interactions, the effects of such changes to the marine environment could have equally complex consequences for disease dynamics. The potential for such substantial change to the role of trematode parasites caused by a changing marine environment can best be understood by following a single parasite species through a complete life cycle.

Adult trematodes live within the definitive host, the site of sexual reproduction. These hosts are often large fish, marine mammals or shore birds, and as such are often not directly affected by climate change--they have sufficient physiological ability to tolerate changes in seawater temperature, pH or oxygen content. However, the adult parasites often reside in the gut of the definitive host, absorbing nutrients that the host consumes. Consequently, if the food supply of the definitive host is reduced by climate change, through lower abundance of prey species, there could be a knock-on effect on the performance of the parasite--for example, reduced reproductive output caused by starvation. Sexual reproduction produces parasite eggs which invariably exit the definitive host via faeces, which then hatch into miracidia (small mobile larvae) when the eggs contact seawater. Miracidia seek out and infect the first intermediate host, almost always a marine snail. Eggs and miracidia are the first life-stages of the parasite to come into direct contact with seawater, and are therefore a potential weak link in the parasite's life cycle if climate change causes seawater to become too warm, hypoxic and/or acidic for these organisms. If climate change negatively affects these life stages, the overall performance of the parasite may suffer--fewer eggs will hatch and fewer miracidia will survive long enough to find and infect a snail.

Once within the snail, successful miracidia transform into a sporocyst, a sac-like structure that generates genetically identical cercariae (another small, swimming larvae--see Figure 1), which emerge periodically from infected snails to seek out the next host in the parasite's life cycle. Of all the hosts in the parasite's life cycle, the first intermediate host is potentially the most vulnerable to climate change; snails are relatively primitive organisms that do not possess sophisticated physiological mechanisms to deal with elevated temperature or reduced seawater pH. Consequently, they exhibit higher levels of mortality in these conditions than definitive hosts. In addition, trematode infection sterilises host snails, and is often associated with greater mortality in infected individuals. The stress of infection plus the stress of climate change has the potential to interact synergistically in host snails, compounding the effects of each single stressor.

Cercariae, much like the miracidia, are vulnerable to changing environmental conditions as they are also directly exposed to seawater upon emergence from their host. Cercariae are, however, more numerous than miracidia, as each sporocyst can produce thousands of cercariae per day. Cercariae are produced in such large numbers to compensate for the low chance of success in finding the next host in the life cycle. Much research has gone into exploring the response of cercariae to simulated climate change, (3) although it appears that cercariae belonging to different species of trematode exhibit significantly different tolerances to many climate change-related stressors. (4) Interestingly, cercariae also represent a significant food resource for non-host organisms, especially as they are produced in such large numbers. (5) If cercariae survival is reduced by climate change, then these non-host organisms will have less food to eat.

To complete their stage of the transmission process, cercariae must find and infect the second intermediate host, often a bivalve, crustacean or small fish. Cercariae penetrate the second intermediate host and form a resting cyst (also known as a metacercariae --Figure 2) in the host's muscle tissue, where they await a predation event that will transfer the parasite from the second intermediate host to the definitive host--the definitive host eats the second intermediate host, thus completing the parasite's life cycle. In the same way that sporocysts can increase mortality in infected snails, too many cysts and the second intermediate host may also die; here again, we see the potential for stress caused by parasites to interact with or compound stress caused by climate change.

We can clearly see that at every stage of the parasite's life cycle, both parasite and host are vulnerable to the stressors associated with climate change. It is a surprise, therefore, that the combined effects of parasitism and climate change are not studied more often. This may in part be due to the underestimation of the effect of parasites in natural systems. Almost all stages of the trematode life cycle are too small to see with the naked eye, and some researchers equate this small size with a small potential effect. (6) This neglect may also be due to the equilibrium that is often reached between parasite and host. While parasites take energy from hosts by definition, the death of the host does not really benefit the parasite--ultimately, that's where their food comes from. From an evolutionary perspective, this has led to the development of many host-parasite relationships that do not end in the death of the host, but rather a kind of equilibrium where hosts are negatively affected by parasites, but are not killed by them.

However, in a rapidly changing marine environment, we must remain vigilant to note previously stable relationships that become unbalanced. Significant, mass die-offs have been recorded that were a direct result of trematode infection combined with extreme environmental events (such as heatwaves (7)). It seems wise to begin evaluating all components of the host-parasite life cycle for evidence of potentially dramatic synergisms that could result in equally dramatic shifts in our marine ecosystems.

Colin MacLeod is a postdoctoral fellow in the Biodiversity Research Centre, University of British Columbia. While completing PhD at Otago, he was a member of the NZ Ocean Acidification Community. 1 2 3 4

(1.) KV Galaktionov and AA Dobrovolskij, The Biology of Trematodes (Dordrecht: Kluwer, 2003).

(2.) R Poulin, "Global Warming and Temperature-mediated Increases in Cercarial Emergence in Trematode Parasites," Parasitology, 132:1 (2006), 143, https://doi. org/10.1017/S0031182005008693.

(3.) A Studer and R Poulin, "Cercarial Survival in an Intertidal Trematode: A Multifactorial Experiment with Temperature, Salinity and Ultraviolet Radiation," Parasitology Research, 112:1 (2013), 243-49, https://doi.org/10.1007/ s00436-012-3131-3.

(4.) CD MacLeod and R Poulin, "Differential Tolerances to Ocean Acidification by Parasites that Share the Same Host," International Journal for Parasitology, 47:5 (2015), https://doi.org/10.1016/j.ijpara.2015.02.007.

(5.) DW Thieltges, P-A Amundsen, RF Hechinger, PTJ Johnson, KD Lafferty, KN Mouritsen, ... R Poulin, "Parasites as Prey in Aquatic Food Webs: Implications for Predator Infection and Parasite Transmission," Oikos, 122 (2013), 1473-82, https://doi.org/10.1111/j.1600-0706.2013.00243.x.

(6.) AM Kuris, RF Hechinger, JC Shaw, KL Whitney, L Aguirre-Macedo, CA Boch, ... KD Lafferty, "Ecosystem Energetic Implications of Parasite and Free-living Biomass in Three Estuaries," Nature, 454:7203 (2008), 515-18, https:// doi.org/10.1038/nature06970.

(7.) KN Mouritsen and KT Jensen, "Parasite Transmission Between Soft-bottom Invertebrates: Temperature Mediated Infection Rates and Mortality in Corophium volutator," Marine Ecology Progress Series, 151:1 (1997), 123-34.

Caption: Figure 1. A trematode cercaria.

Caption: Figure 2. A trematode metacercaria.
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Title Annotation:trematodes
Author:Macleod, Colin
Publication:Junctures: The Journal for Thematic Dialogue
Article Type:Essay
Date:Dec 1, 2018
Words:1339
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