Catching the parasite: three-spined sticklebacks eat trematode free-living stages

This blog post is provided by Ana Born-Torrijos and Miroslava Soldánová and tells the #StoryBehindThePaper for their article “Cercarial behaviour alters the consumer functional response of three-spined sticklebacks“, which was recently published in Journal of Animal Ecology.
Trematode free-living stages emerging from their snail host Radix balthica. Credit: Miroslava Soldánová.

When we see a small fish swimming about in a lake, we might assume they are searching for something to eat, perhaps some copepods, cladocerans or ostracods. What rarely springs to mind is that these small fish may in fact be feeding on parasites. Trematode parasites have free-living infectious stages called cercariae that swim in the water to infect their next hosts. During this brief life span of approximately 24-72 hours, these cercariae are vulnerable to predation from non-host predators, who simply regard them as an abundant, energy rich prey resource similar to zooplankton. Furthermore, some predators have the ability to act as biocontrol agents of parasite-induced diseases, which are particularly important in a context of future climate change scenarios.

How do we study parasite consumption by a fish predator?

Trematode infections often have a patchy distribution in their first intermediate snail hosts, from which the free-living cercariae are released. This causes the density of trematode cercariae to naturally vary within and among lake habitats. Consumer functional responses (hereafter ‘FRs’) describe the relationship between the consumption rate of a predator and the density of its prey, and are useful tool for understanding how predator-prey dynamics may change as prey densities vary.

Sampling of the first intermediate snail host Radix balthica, from which the free-living cercariae are released. Credit: Rune Knudsen.

Three main FR types are often used to describe predator-prey dynamics: Type I – when a predator consumes a constant proportion of the available prey; Type II – when the proportion of prey consumed decreases as the density of the prey increases; Type III – when the proportion of prey consumed initially increases, then decreases with increasing prey density. The main difference between Type II and Type III FRs is the proportion of prey that are consumed when the density of prey is low. Predators displaying a Type II FR are able to consume a high proportion of prey even when only few prey are present, which may have destabilising effects on prey populations.

The three types of functional responses to describe the relationships between prey density and prey consumption.
Functional responses in different predator-prey combinations

Our study investigated how the widely distributed freshwater fish, three-spined sticklebacks Gasterosteus aculeatus, consumed cercariae of two trematodes (Trichobilharzia, Plagiorchis) commonly found in lakes throughout Europe.

The beautiful study area, sub-Arctic lake Takvatn in Norway. Credit: Rachel Parterson.

Our FR experiments allowed three-spined sticklebacks to consume cercariae at a range of naturally occurring densities. We also considered how ecologically relevant factors may alter consumption rates, using (i) three-spined sticklebacks with different degrees of cestode parasitic infection, and (ii) two temperatures (6, 13ºC) representative of warmer and colder months in our sub-Arctic lake study system. Do not hesitate to check out our full paper if you are interested in the effects caused by predator’s infection status and water temperature. Three-spined sticklebacks displayed different FR types towards each trematode genera: Type II for Plagiorchis spp. and Type III for Trichobilharzia, with an overall higher consumption on Trichobilharzia.

A. Plagiorchis cercariae swimming in the water after emerging from their first intermediate snail host Radix balthica. B. Plagiorchis cercaria under the microscope (̴ 480 µm). Credit: Miroslava Soldánová.
A. Trichobilharzia cercariae swimming in the water after emerging from their first intermediate snail host Radix balthica. B. Trichobilharzia cercaria under the microscope (̴ 940 µm). Credit: Miroslava Soldánová.

Why do fish consume two tiny cercariae in a different manner?

            Imagine you are a fish searching for prey; you would be probably attracted to bigger and vigorous prey, right? Trichobilharzia is twice as big as Plagiorchis, and furthermore, they swim in dense clouds in a “rest-swim-rest” motion that could facilitate their predation. In contrast, Plagiorchis may go unnoticed by pelagic fish since this parasite swims continuously and slowly in benthic habitats. At the same time, this behaviour might make Plagiorchis cercariae easier to prey on when present at low densities, determining a Type II response, while Trichobilharzia may be more difficult to catch when swimming isolated from a cercariae cloud. The different swimming patterns have likely evolved to facilitate transmission to the next host, which are benthic invertebrates for Plagiorchis and birds for Trichobilharzia. It is then the traits inherent to parasite transmission and dispersal that likely determine the FR of three-spined sticklebacks towards these cercariae.

Video showing a three-spined stickleback actively consuming trematode free-living swimming cercarial stages during a functional response experimental trial.
Three-spined sticklebacks’ predatory impact on cercarial prey

Cercariae consumption by three-spined sticklebacks may have major impacts on trematode population dynamics, especially considering the wide distribution and high population densities three-spined sticklebacks can attain. This is where FRs become crucial in understanding the potential impact of a fish predator on parasite populations, by determining the rate at which parasites are consumed depending on their density in the environment. FRs could thus help to evaluate potential biocontrol agents to modulate problematic trematode infections. Although our study demonstrated that three-spined sticklebacks showed a Type III response to Trichobilharzia prey, the identification of a fish species displaying the destabilising effects of Type II responses would be highly beneficial in the suppression of this parasite, which is the main causative agent of human cercarial dermatitis (swimmer’s itch) in Europe. The right fish-trematode combination that might help reduce parasites of medical and veterinary importance is thus waiting to be discovered!

So, next time you see some small fish swimming about in your local lake, just imagine all the parasites that they are happily eating!

Ana Born Torrijos is a Postdoctoral Researcher at the Institute of Parasitology from the Biology Centre of the Czech Academy of Sciences (BC CAS). She is deeply interested in behavioral ecology of parasites, ecological parasitology and parasite transmission strategies. Her research includes in vivo and in vitro experiments in a parasitological and food ecology framework. Currently she leads a project focused on the infection and transmission strategies of a trematode present in marine aquaculture, involving transcriptomic and proteomic data to elucidate the physiological basis of infection-associated changes in host behaviour. You can follow Ana on Twitter @BornTorrijos. Researchgate: https://www.researchgate.net/profile/Ana_Born-Torrijos.

Miroslava Soldánová, Ph.D. is a freshwater ecologist with a broad interest in the role of digenean trematodes in aquatic ecosystems, their interactions with ecological communities, effects on food web dynamics and importance in the ecosystem structure and functioning. Miroslava’s research also focuses on elucidating ecological and environmental processes forming trematode populations and communities in freshwater molluscs at spatial and temporal scales in various freshwater ecosystems, uncovering hidden trematode diversity, and studying life-cycles, transmission strategies and use of trematode communities as indicators of environmental conditions and ecosystem stability.

Read the paper

Read the full paper here: Born‐Torrijos, A, Paterson, RA, van Beest, GS, et al. Cercarial behaviour alters the consumer functional response of three‐spined sticklebacks. J Anim Ecol. 2021; 00: 1– 11. https://doi.org/10.1111/1365-2656.13427

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