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Parasitic mussels induce upstream movement in their fish hosts: early evidence of extended phenotype
Karlstad University, Faculty of Health, Science and Technology (starting 2013), Department of Environmental and Life Sciences (from 2013).ORCID iD: 0000-0002-6541-4795
Lund University, Sweden.
Karlstad University, Faculty of Health, Science and Technology (starting 2013), Department of Environmental and Life Sciences (from 2013).ORCID iD: 0000-0002-4417-6636
Karlstad University, Faculty of Health, Science and Technology (starting 2013), Department of Environmental and Life Sciences (from 2013).ORCID iD: 0000-0002-8738-8815
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2025 (English)In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 36, no 4, article id araf043Article in journal (Refereed) Published
Abstract [en]

Parasites often have a large impact on their hosts and can alter host phenotype to increase their own fitness, a phenomenon known as extended phenotype. Studies demonstrating extended phenotype for non-trophically transmitted parasites are scarce. Unionid mussels have a parasitic life stage adapted to parasitize fish which can affect host behavior, habitat use and growth rates, raising the question if parasitic freshwater mussels can also manipulate their host fish to compensate for downstream dispersal and to reach habitats favorable for newly excysted juvenile mussels. Wild-caught, parasite-na & iuml;ve juvenile brown trout (Salmo trutta) were PIT-tagged, and half of the individuals were infested with parasitic larvae from the freshwater pearl mussel (Margaritifera margaritifera), all individuals were then returned to their home stream. During the following year, trout were tracked to investigate movement and habitat use, and also periodically recaptured to measure growth and body condition factor. The infested trout showed significantly higher upstream movement than non-infested trout and were more often recaptured in stream sections with slow-moving shallow water, particularly during the parasite excystment period (270 d post infestation). These data suggest that the juvenile mussels were successfully transported an average of 170 m upstream from the host trout release points to stream sections favorable for adult mussels. Infested trout survived as well as the non-infested, but had a significantly lower specific growth rate than non-infested trout. These results indicate a first example of extended phenotype in unionid mussels and highlight the importance of understanding glochidia-induced changes to host fish behavioral ecology. Parasites often manipulate host behavior to increase their reproductive success, but studies on this phenomenon typically focus on parasites which lead to the eventual death of their host, an effect that parasitic freshwater mussels generally do not have. Here, we show that parasitic freshwater mussel larvae manipulate host fish into swimming further upriver to habitats well suited for the next stage of their lifecycle.

Place, publisher, year, edition, pages
Oxford University Press, 2025. Vol. 36, no 4, article id araf043
Keywords [en]
behavior, conservation, ecology, host manipulation, Margaritifera margaritifera, Salmo trutta, Salmonidae, unionida
National Category
Biological Sciences
Research subject
Biology
Identifiers
URN: urn:nbn:se:kau:diva-106391DOI: 10.1093/beheco/araf043ISI: 001522762000001PubMedID: 40621057Scopus ID: 2-s2.0-105010707850OAI: oai:DiVA.org:kau-106391DiVA, id: diva2:1986994
Available from: 2025-08-04 Created: 2025-08-04 Last updated: 2025-10-16Bibliographically approved
In thesis
1. Glochidiosis and behaviour
Open this publication in new window or tab >>Glochidiosis and behaviour
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Freshwater mussels in the order Unionida are a highly endangered and globally distributed taxon of parasitic bivalves. Consequently, many conservation and reintroduction projects have emerged to protect this valuable order. Adult mussels release parasitic larvae (glochidia) that affix themselves to their hosts, typically the gills of fish, where they become encysted in the tissue and metamorphose into juveniles; later, excysting as juveniles to develop into free-living adults in the sediment, completing the lifecycle. As Unionids are well-known ecosystem engineers, reintroduction efforts are generally met with support. However, members of the public unfamiliar with the scientific literature often have reservations when learning that the restoration project aims to introduce parasites to their local waterways. Little is known about the impacts of glochidiosis on host fishes; however, most effects are negative. With the growth of mussel conservation projects, more fish will be exposed to these negative impacts. 

In this dissertation, I explore the parasitic interactions of two of Europe’s most endangered mussels with some of their respective host fishes. I initially produced a general literature review to summarize all previous work on the topic and better understand which aspects needed the most attention (Paper I). From this, I surmised that the behavioural and molecular impacts of glochidiosis were the least studied and that there was a general over-representation of the interaction between the freshwater pearl mussel (Margaritifera margaritifera) and its salmonid hosts, a highly specialized interaction not well-suited for cross-species generalizations. I followed Paper I with an investigation into the impacts of infestation by the thick-shelled river mussel (Unio crassus) on the schooling behaviour of its host minnow (Phoxinus phoxinus; Paper II), and the impacts of both adult and larval life stages of U. crassus on the predator-prey interactions of its host bullhead (Cottus gobio) with a prey gammarid (Paper III). The results of Papers II and III suggested that unionid mussels may manipulate host behaviour; to test this hypothesis, a year-long field study was conducted on the movement patterns and habitat choice of brown trout (Salmo trutta) when infested with glochidia from M. margaritifera, the species most likely to express an extended phenotype (Paper IV), as speculated in Paper I. This investigation provided evidence in support of an expressed extended phenotype by a unionid mussel on its host fish.

Abstract [en]

Unionid mussels are a unique order of bivalves characterised by the presence of a parasitic larval life stage, known as a glochidium. In this dissertation, I explore the behavioural effects of glochidiosis (the condition of bearing glochidia) on common hosts of Europe’s most endangered unionids. The dissertation includes a general review of the effects of glochidiosis, two laboratory studies, and a year-long field study. The results presented here demonstrate that glochidia induce effects on their host fish similar to those caused by other parasites, including reduced growth, decreased swimming performance, and a general preference for calmer water and more structurally complex habitats. Together, the behavioural alterations induced by glochidiosis may benefit unionid recruitment, as infested host fish may transport excysting juvenile mussels to habitats favourable for later development. This provides evidence for the presence of an extended phenotype in unionids.

Place, publisher, year, edition, pages
Karlstad: Karlstads universitet, 2025. p. 93
Series
Karlstad University Studies, ISSN 1403-8099 ; 2025:19
Keywords
Unionida, Glochidia, Parasitology, Behavioural Ecology, Ecology, Host Manupilation
National Category
Ecology Behavioral Sciences Biology Other Biological Topics
Research subject
Biology
Identifiers
urn:nbn:se:kau:diva-103900 (URN)10.59217/ogie5789 (DOI)978-91-7867-570-8 (ISBN)978-91-7867-571-5 (ISBN)
Public defence
2025-05-23, 1B309, Sjöströmsalen, Karlstad, 10:00 (English)
Opponent
Supervisors
Note

Paper 4 part of thesis as manuscript, now published. 

Available from: 2025-04-30 Created: 2025-04-09 Last updated: 2025-10-16Bibliographically approved

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Rock, Sebastian L.Watz, JohanCalles, OlleÖsterling, Martin

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