Regional Distribution of a Brain-Encysting Parasite Provides Insight on Parasite-Induced Host Behavioral Manipulation

Helland-Riise, Siri Helene; Nadler, Lauren E.; Vindas, Marco A.; Bengston, Erik; Turner, Andrew; Johansen, Ida Beitnes; Weinersmith, Kelly L.; Hechinger, Ryan F.; Øverli, Øyvind

doi:10.1645/19-86

Cited by 8 publications

(14 citation statements)

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“…This study was part of a larger project examining the influence of E. californiensis on killifish physiology, neurobiology and behaviour throughout development, and involved laboratory rearing of fish from wild‐caught gametes (Helland‐Riise et al., 2020). These fish were exposed for 13 months post‐hatch under different ‘long‐term treatments’ (repeatedly exposed or sham exposed to parasites).…”

Section: Methodsmentioning

confidence: 99%

“…cercaria) that seeks out and infects its next host, the California killifish Fundulus parvipinnis (Martin, 1950). After encounter, the parasite burrows through the fish's epithelium and makes its way to the brain's meningeal surface, where it encysts as a metacercaria (Helland‐Riise et al., 2020; Martin, 1950; Shaw et al., 2009). Fish with established parasites on the brain may exhibit more conspicuous behaviours than uninfected conspecifics (e.g.…”

Section: Introductionmentioning

confidence: 99%

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A brain‐infecting parasite impacts host metabolism both during exposure and after infection is established

et al. 2020

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1. Metabolic costs associated with parasites should not be limited to established infections. Even during initial exposure to questing and attacking parasites, hosts can enact behavioural and physiological responses that could also incur metabolic costs. However, few studies have measured these costs directly. Hence, little is known about metabolic costs arising from parasite exposure. 2. Furthermore, no one has yet measured whether and how previous infection history modulates metabolic responses to parasite exposure. 3. Here, using the California killifish Fundulus parvipinnis and its brain-infecting parasite Euhaplorchis californiensis, we quantified how killifish metabolism, behaviour and osmoregulatory phenotype changed upon acute exposure to parasite infectious stages (i.e. cercariae), and with long-term infection. 4. Exposure to cercariae caused both naïve and long-term infected killifish to acutely increase their metabolic rate and activity, indicating detection and response to parasite infectious stages. Additionally, these metabolic and behavioural effects were moderately stronger in long-term infected hosts than naïve killifish, suggesting that hosts may develop learned behavioural responses, nociceptor sensitization and/or acute immune mechanisms to limit new infections. 5. Although established infection altered the metabolic response to parasite exposure, established infection did not alter standard metabolic rate, routine metabolic rate, maximum metabolic rate, aerobic scope or citrate synthase enzyme activity. 6. Unexpectedly, established infection reduced lactate dehydrogenase enzyme activity in killifish brains and relative Na + /K +-ATPase abundance in gills, suggesting novel mechanisms by which E. californiensis may alter its hosts' behaviour and osmoregulation. 7. Thus, we provide empirical evidence that parasites can disrupt the metabolism of their host both during parasite exposure and after infection is established. This response may be modulated by previous infection history, with probable knock-on effects for host performance, brain energy metabolism, osmoregulation and ecology. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A brain‐infecting parasite impacts host metabolism both during exposure and after infection is established

et al. 2020

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“…However, in nature, killifish achieve high parasite intensities through the slow accumulation of parasites throughout their lifetimes. We used a long-term, repeated infection method to more accurately mimic natural exposure patterns (more fully described in Helland-Riise et al, 2020 ). In short, experimental infections were carried out continuously from when fish were approximately 8 weeks post-hatch, throughout the life of the fish (approximately a 9-month infection period, September 2016 – June 2017).…”

Section: Methodsmentioning

confidence: 99%

“…Thereafter, high-resolution images (10× magnification) of the stained sections of the infected fish were acquired using an automated slide scanner system (Axio Scan Z1, Carl Zeiss Microscopy, Munich, Germany). Images were analysed visually, and parasites were quantified by counting metacercariae on the diencephalon/mesencephalon only, because the number of parasites found in this area is highly correlated to total parasite numbers (Helland-Riise et al, 2020). Note that microdissections did not dislocate metacercariae, as the parasites are located on the brain surface (see Fig.…”

Section: Tissue Processing Microdissection and Parasite Quantificationmentioning

confidence: 99%

“…This is the first time that serotonergic neurochemistry has been studied in killifish subjected to repeated experimental infections, mimicking natural infections and yielding parasite densities observed in wild adult fish. To achieve this, we used a recently developed laboratory protocol yielding parasite intensities comparable to those in wild fish (Helland-Riise et al, 2020). To study serotonergic responses, we used a series of sequential stressors: transport stress combined with exposure to a novel environment, a simulated predator attack, and acute confinement in a small volume of water.…”

Section: Introductionmentioning

confidence: 99%

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Brain-encysting trematodes (Euhaplorchis californiensis) decrease raphe serotonergic activity in California killifish (Fundulus parvipinnis)

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Modulation of brain serotonin (5-HT) signalling is associated with parasite-induced changes in host behaviour, potentially increasing parasite transmission to predatory final hosts. Such alterations could have substantial impact on host physiology and behaviour, as 5-HT serves multiple roles in neuroendocrine regulation. These effects, however, remain insufficiently understood, as parasites have been associated with both increased and decreased serotonergic activity. Here, we investigated effects of trematode Euhaplorchis californiensis metacercariae on post-stress serotonergic activity in the intermediate host California killifish (Fundulus parvipinnis). This parasite is associated with conspicuous behaviour and increased predation of killifish by avian end-hosts, as well as inhibition of post-stress raphe 5-HT activity. Until now, laboratory studies have only been able to achieve parasite densities (parasites/unit host body mass) well below those occurring in nature. Using laboratory infections yielding ecologically relevant parasite loads, we show that serotonergic activity indeed decreased with increasing parasite density, an association likely indicating changes in 5-HT neurotransmission while available transmitter stores remain constant. Contrary to most observations in the literature, 5-HT activity increased with body mass in infected fish, indicating that relationships between parasite load and body mass may in many cases be a real underlying factor for physiological correlates of body size. Our results suggest that parasites are capable of influencing brain serotonergic activity, which could have farreaching effects beyond the neurophysiological parameters investigated here.

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Survival of metazoan parasites in fish: Putting into context the protective immune responses of teleost fish

Dezfuli

Giari

Bosi

2021

Advances in Parasitology

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Regional Distribution of a Brain-Encysting Parasite Provides Insight on Parasite-Induced Host Behavioral Manipulation

Abstract: BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.

Cited by 8 publications

References 48 publications

A brain‐infecting parasite impacts host metabolism both during exposure and after infection is established

A brain‐infecting parasite impacts host metabolism both during exposure and after infection is established

Brain-encysting trematodes (Euhaplorchis californiensis) decrease raphe serotonergic activity in California killifish (Fundulus parvipinnis)

Survival of metazoan parasites in fish: Putting into context the protective immune responses of teleost fish

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