Cercarial behaviour alters the consumer functional response of three-spined sticklebacks

This is the peer reviewed version of the following article: Born-Torrijos, A., Paterson, R., van Beest, G., Vyhlídalová, T., Henriksen, E.H., Knudsen, R., Kristoffersen, R., Amundsen, P.-A. & Soldánová, M. (2021). Cercarial behaviour alters the consumer functional response of three-spined sticklebacks. Journal of Animal Ecology, 90, 978-988, which has been published in final form at https://doi.org/10.1111/1365-2656.13427. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. This article may not be enhanced, enriched or otherwise transformed into a derivative work, without express permission from Wiley or by statutory rights under applicable legislation. Copyright notices must not be removed, obscured or modified. The article must be linked to Wiley’s version of record on Wiley Online Library and any embedding, framing or otherwise making available the article or pages thereof by third parties from platforms, services and websites other than Wiley Online Library must be prohibited. Free-living parasite life stages may contribute substantially to ecosystem biomass and thus represent a significant source of energy flow when consumed by non-host organisms. However, ambient temperature and the predator's own infection status may modulate consumption rates towards parasite prey. We investigated the combined effects of temperature and predator infection status on the consumer functional response of three-spined sticklebacks towards the free-living cercariae stages of two common freshwater trematode parasites (Plagiorchis spp., Trichobilharzia franki). Our results revealed genera-specific functional responses and consumption rates towards each parasite prey: Type II for Plagiorchis spp. and Type III for T. franki, with an overall higher consumption rate on T. franki. Elevated temperature (13°C) increased the consumption rate on Plagiorchis spp. prey for sticklebacks with mild cestode infections ( High consumption of cercarial prey by sticklebacks may impact parasite population dynamics by severely reducing or even functionally eliminating free-living parasite life stages from the environment. This supports the potential role of fish as biocontrol agents for cercariae with similar dispersion strategies, in instances where functional response relationships have been established. Our study demonstrates how parasite consumption by non-host organisms may be shaped by traits inherent to parasite transmission and dispersal, and emphasises the need to consider free-living parasite life stages as integral energy resources in aquatic food webs. </ol

Production and periodicity in the emergence of cercariae of \kur{Diplostomum} spp. (Digenea) from snails \kur{Radix lagotis} (Lymnaeidae)

The cercarial emergence patterns of three species of Diplostomum (D. mergi, D. spathaceum and D. pariventosum) parasitising freshwater first intermediate host Radix lagotis were studied under various experimental conditions, i.e., field, laboratory and incubator, and seasons, i.e., spring, summer and autumn. This study provided novel data on the production and periodicity in cercarial emergence and revealed both interspecific and intraspecific variaons related to the species-specific adaptive nature of cercariae to facilitate transmission to second intermediate fish hosts

Small but diverse: larval trematode communities in the small freshwater planorbids Gyraulus albus and Segmentina nitida (Gastropoda: Pulmonata) from the Ruhr River, Germany

This study reveals the importance of small planorbid snails, in particular Gyraulus albus, as first intermediate hosts for a species-rich trematode fauna in European freshwater systems, and highlights the parasite contribution to the ecosystem biodiversity

Složení společenstev larválních stádií motolic (Digenea) u vybraných zástupců plicnatých plžů čeledi Planorbidae

In the present study the species diversity, seasonal dynamics, composition of larval trematode communities and factors influencing their structure were studied in two species of planorbid gastropods (Gyraulus albus and Segmentina nitida) in typical eutrophic fishponds in South Bohemia, Czech Republic. The study significantly contributed to the present knowledge about the fauna of trematodes in small planorbids, provided evidence for validity of general rules affecting trematode community composition and structure and demonstrated the underestimated role of both snail species as first intermediate hosts for trematodes in the past

Temperature does not influence functional response of amphipods consuming different trematode prey

This is a post-peer-review, pre-copyedit version of an article published in Parasitology Research. The final authenticated version is available online at: http://dx.doi.org/https://doi.org/10.1007/s00436-020-06859-1.Direct consumption on free-living cercariae stages of trematodes by non-host organisms interferes with trematode transmission and leads to reduced infections in the next suitable hosts. Consumer functional responses provide a useful tool to examine relationships between consumption rates and ecologically relevant prey densities, whilst also accounting for abiotic factors that likely influence consumption rates. We investigated how temperature influences the consumer functional response of the amphipod Gammarus lacustris towards the cercariae of three freshwater trematodes (Diplostomum, Apatemon and Trichobilharzia). Amphipods displayed different functional responses towards the parasites, with Type II responses for Diplostomum and Type I responses for Apatemon prey. Temperature did not alter the consumption rate of the amphipod predator. Trichobilharzia was likely consumed at similar proportions as Diplostomum; however, this could not be fully evaluated due to low replication. Whilst Type II responses of invertebrate predators are common to various invertebrate prey types, this is the first time a non-filter feeding predator has been shown to exhibit Type I response towards cercarial prey. The prey-specific consumption patterns of amphipods were related to cercarial distribution in the water column rather than to the size of cercariae or temperature influence. The substantial energy flow into food webs by non-host consumer organisms highlights the importance of understanding the mechanisms that modulate functional responses and direct predation in the context of parasitic organisms

Taxa-specific activity loss and mortality patterns in freshwater trematode cercariae under subarctic conditions

Cercarial activity and survival are crucial traits for the transmission of trematodes. Temperature is particularly important, as faster depletion of limited cercarial energy reserves occurs at high temperatures. Seasonal climate conditions in high latitude regions may be challenging to complete trematode life cycle during the 6-month ice-free period, but temperature effects on the activity and survival of freshwater cercariae have not been previously identified. After experimentally simulating natural subarctic conditions during warmer and colder months (13 and 6°C), a statistical approach identifying changes in the tendency of cercarial activity loss and mortality data was used to detect differences in three trematode genera, represented by four taxa (Diplostomum spp., Apatemon spp., small- and large-sized Plagiorchis spp.). A strong temperature-dependent response was identified in both activity loss and mortality in all taxa, with Diplostomum spp. cercariae showing the most gradual changes compared to other taxa. Furthermore, whilst activity loss and mortality dynamics could not be divided into ‘fish- vs invertebrate-infecting cercariae’ groups, the detected taxa-specific responses in relation to life-history traits indicate the swimming behaviour of cercariae and energy allocation among larvae individuals as the main drivers. Cercariae exploit the short transmission window that allows a stable continuance of trematodes’ life cycles in high-latitude freshwater ecosystems