Distribution patterns, inter-and intra-host dynamics of an emerging salmonid parasite T. bryosalmonae across temporal and spatial scales
dc.contributor.advisor | Vasemägi, Anti | |
dc.contributor.advisor | Päkk, Priit | |
dc.contributor.author | Lauringson, Magnus | |
dc.contributor.department | Institute of Veterinary Medicine and Animal Sciences | |
dc.contributor.other | Ros, Albert (opponent) | |
dc.date.accessioned | 2024-05-02T19:09:11Z | |
dc.date.available | 2024-05-02T19:09:11Z | |
dc.date.defensed | 2024-05-30 | |
dc.date.issued | 2024 | |
dc.description | A Thesis for applying for the degree of Doctor of Philosophy in Agricultural Sciences. | eng |
dc.description | Väitekiri filosoofiadoktori kraadi taotlemiseks põllumajandusteaduste erialal. | est |
dc.description.abstract | Global climate change is shifting the physical and chemical properties of freshwater ecosystems, involving increased water temperature, altered hydrological regime and nutrient concentrations. These changes influence particularly cold-water macro vertebrates, such as salmonids, resulting in loss of habitat and population declines. The physiochemical alternations caused by climate change also have an effect on the biotic environment, including changes in virulence, pathogenicity, distribution and prevalence of pathogens and diseases. One emerging widespread illness is salmonid specific proliferative kidney disease (PKD), caused by myxozoan parasite Tetracapsuloides bryosalmonae, which is primarily affecting juvenile fish during their first growth summer. PKD causes hyperplasia in kidney and spleen tissue, anemia and external clinical signs include abdominal swelling and pale gills. Myxozoans are endoparasites, who have evolved from free-living cnidarians and typically possess a complex two-host life-cycle, involving an invertebrate and vertebrate host. For myxozoan T. bryosalmonae, cycling occurs between freshwater bryozoans and salmonid hosts. In Europe, native brown trout (Salmo trutta), Atlantic salmon (Salmo salar), European grayling (Thymallus thymallus), Arctic charr (Salvelinus alpinus) and European whitefish (Coregonus lavaretus), as well as non-native rainbow trout (Oncorhynchus mykiss) are susceptible to T. bryosalmonae (for review see Ros et al., 2022). While the severity of PKD is strongly dependent on water temperature, with disease symptoms progressing with rising temperature, only a few studies have found T. bryosalmonae in northern regions. Moreover, detailed knowledge on the parasite distribution and prevalence is not available in northernmost regions of Europe. Earlier PKD related research has also primarily been centered around juvenile salmonids, with the main focus on farmed rainbow trout (Oncorhynchus mykiss) and wild brown trout (Salmo trutta) in single host systems. Investigation of T. bryosalmonae resistance and tolerance patterns in sympatric wild salmonid populations is therefore expected to improve our understanding on parasite dynamics and host defence mechanisms. It has been speculated that migrating fish could act as parasite vectors, however it is unclear, if and how anadromous salmonid species contribute to the parasite’s life-cycle during their later life-stages. The specific foci of the current thesis was to cover the abovementioned knowledge gaps by investigation of T. bryosalmonae distribution, prevalence and infection dynamics at different spatial and temporal scales with an addition of intra-host and inter-host dimensions. The thesis revealed how T. bryosalmonae is widely distributed within rivers flowing into the Barents and Norwegian Sea in Northernmost Europe, which indicates that T. bryosalmonae is already present in the region and future climate change and heat waves may likely cause new disease outbreaks in northern latitudes. T. bryosalmonae infection typically occurs during the first growth summer of salmonid fish. However in northernmost Europe, it was found that almost exclusively all young-of-the-year fish were uninfected with the parasite and infections primarily occur among yearlings. It was also apparent that the average summer water temperature was remarkably higher in rivers to host the parasite. Inter-species comparison revealed that brown trout (Salmo trutta) is more frequently infected with the parasite than Atlantic salmon (Salmo salar) in sympatric populations of northernmost Europe. The second study shed light onto inter-specific PKD susceptibility through investigating changes in T. bryosalmonae load and the severity of disease signs (renal hyperplasia, haematocrit) in wild sympatric brown trout and Atlantic salmon populations. Parasite burden and clinical progression of PKD demonstrated highly distinct patterns between sympatric Atlantic salmon and brown trout. While both species initially showed low levels of parasite load, the rate of parasite multiplication was much faster in brown trout compared with Atlantic salmon. However, despite this slower build-up, the amount of parasite DNA reached similar levels in both species by the end of September. This indicates that the speed of parasite multiplication, rather than the absolute number of parasites in the host kidney, may be an important factor causing between-species variation in the disease susceptibility. Comparing parasite load with disease symptoms demonstrated a strong difference in disease tolerance between Atlantic salmon and brown trout. In the beginning of August, renal hyperplasia slightly increased for both species. However, despite the homogeneous build-up of parasite burden between the host species, kidneys of Atlantic salmon recovered by the end of the season. On the other hand, brown trout developed a severe kidney hyperplasia by the end of September with a considerable inter-individual variation. The results demostrate that Atlantic salmon is more resistant than brown trout against T. bryosalmonae. T. bryosalmonae is often found within juvenile salmonids in rivers hosting anadromous salmonid populations, however we knew very little on parasite presence within anadromous adult fish, who have exploited marine environment for several years. Wide-scale T. bryosalmonae sampling among adult sea trout caught from the marine environment within the Estonian coastal area indicated that more than one third of Estonia’s sea trout are infected with the parasite during their marine feeding phase. Spatial analysis revealed an increasing infection trend among the adult fish from south to north and west to east along the coast of Estonia, which mirrored T. bryosalmonae prevalence patterns in nearby rivers and streams. Based on age determination within the sampled sea trout via otoliths, it was observed that the parasite can even be detected in up to six-year-old sea trout and probability of infection increases with age, demonstrating that infections or re-infections can occur in later life stages of the anadromous fish. In all, the current thesis has advanced our understanding on T. bryosalmonae prevalence in different spatial, inter-host and intra-host scales, contributing towards a better understanding on the host-pathogen interactions and parasite distribution in wild salmonid populations. | eng |
dc.description.abstract | Erinevaid parasiidi ehk nugiliste liike on maailmas hinnanguliselt rohkem kui vabalt elavaid organisme ning parasitismi peetakse levinumaks eluvormiks kui kisklust. Samas on parasiitide mõju peremeesorganismidele, liikide vahelistele suhetele ning ökosüsteemi toimimisele sageli alahinnatud, kuna enamik nugilisi on raskesti märgatavad või palja silmaga nähtamatud. Kuigi parasiitide otsene mõju peremehele võib varieeruda letaalsest positiivseni, põhjustab parasitism sageli peremehele füsioloogilist stressi, vähendab ellujäämust ning võib tuua kaasa muutusi populatsioonidünaamikas. Üheks selliseks võrdlemisi väheuuritud nugiliseks on nii Euroopas kui Põhja-Ameerikas laialt levinud lõhe-neerueoslik (T. bryosalmonae), kes kuulub limaeosloomade (Myxozoa) klassi ning kotteoslaste (Saccosporidae) sugukonda. Limaeosloomad on välja arenenud vabalt elavatest kõrveraksetest ning enamasti vajab nugiline paljunemiseks nii selgrootut kui selgroogset peremeest. 20. sajandi lõpus kirjeldatigi uut limaeoslaste klassi Malakosporiidid (Malacosporea), kuhu kuulub ka lõhe-neerueoslik ning sai selgeks, et nugilise lõpp-peremeheks on magevee sammalloomad. Lõhe-neerueosliku poolt põhjustatud lõhilaste vohandilise neeruhaiguse sümptomeid (Proliferative kidney disease – PKD), nagu näiteks neerukoe rakkude kontrollimatu paljunemine ning kehvveresus, kirjeldati juba 100 aastat tagasi. Siiski jõuti haiguse põhjuste väljaselgitamiseni alles sajandivahetusel. Uuringud näitasid, et PKD ägenemine kaladel on seotud veetemperatuuri tõusuga ning veetemperatuuri alandamine on kalakasvandustes haiguse tekitatud kahju vähendamisel võtmetähtsusega. Kuna haiguse kulg on sõltuvuses veetemperatuurist, arenevad haigustunnused välja tavaliselt suve teises pooles või sügise alguses. Seejuures on kõige rohkem mõjutatud kevadel koorunud noorkalad ning soojadel suvedel võib haigus põhjustada looduslikes lõhilaste asurkondades kõrget suremust. Euroopas on lõhe-neerueosliku suhtes vastuvõtlikud jõe- ja meriforell (Salmo trutta), lõhe (Salmo salar), harjus (Thymallus thymallus), arktika paalia (Salvelinus alpinus) ja siig (Coregonus lavaretus) ning sisse toodud lõhilastest vikerforell (Ochoryncus mykiss). Kuigi lõhe-neerueosliku elutsüklit ning haigustunnuseid on võrdlemisi põhjalikult kirjeldatud, on varasemad uuringuid läbi viidud peamiselt vikerforellil ning jõeforellil labori tingimustes. Vähem on teada, kui laialt on nugiline levinud looduslikes veekogudes, seda eriti kõrgematel laiuskraadidel ja vanemate kalade hulgas ning kas esineb liikide vahelisi erinevusi haigustundlikkuse osas. Käesolevas väitekirjas läbiviidud uuringute põhjal sai selgeks, et lõhe-neerueoslik on laialt levinud Põhja-Euroopas, asustades Barentsi ja Norra merre suubuvaid jõgesid üle kogu Põhja-Norra ranniku. Võttes arvesse vohandilise neeruhaiguse tugevat seost veetemperatuuriga võib eeldada, et kliima soojenedes sagenevad uuritud regioonis ka vohandilise neeruhaiguse puhangud. Ühtlasi selgus, et neerueoslikuga tabandumine toimub Põhja-Euroopa lõhilastel peamiselt teisel elusuvel. Hilisemat nakatumist põhjustab tõenäoliselt regiooni jahe kliima, mille tulemusel on samasuviste lõhilaste kasvuperiood väga lühike (marjast koorumine võib toimuda alles juuni lõpus), see vähendab ühtlasi parasiidiga tabandumise tõenäosust. Samuti joonistus Põhja-Norra uuringust selgelt välja, et parasiidiga jõed olid suvel märgatavalt soojemad jõgedest, kus neerueoslikku ei olnud ning nugilist esines forellil sagedamini kui lõhel. Põhjalik forelli ja lõhe vahelist parasiidi vastuvõtlikkust selgitav uuring viidi läbi Eesti põhjaranniku jõgedes, kus võrreldi lõhe ja forelli noorjärkude vahel haigustunnuste avaldumise ning suhtelise parasiidi arvukuse dünaamika erinevusi esimese elusuve jooksul. Selgus, et neerueoslik paljuneb kiiremini forelli neerukoes, mille tulemusel on suve keskpaigas parasiidi arvukus forellide hulgas oluliselt kõrgem kui lõhede seas kuid kasvuperioodi lõpuks polnud parasiidi arvukuses olulist erinevust. Suve keskpaigas ägenesid mõõdetud haigustunnused sarnaselt mõlemal liigil, kuid suve lõpus avaldusid liikide vahel olulised erinevused. Nimelt augustis hakkasid lõhel haigustunnused taanduma kuid forellil muutusid haiguse sümptomid järjest ägedamaks. Seega näitab läbiviidud uuring ilmekalt forelli suuremat tundlikkust vohandilise neeruhaiguse suhtes. Kolmas läbiviidud uuring hõlmas neerueosliku esinemise hindamist täiskasvanud meriforellide seas, et selgitada välja millisel määral on vanemad, riimvees toituvad forellid nugilisega tabandunud. Kui Liivi lahest, Väinamerest ning suursaarte ümbrusest püütud meriforellide seas neeruparasiiti peaaegu ei leidunud, siis Soome lahe põhjarannikul oli märkimisväärne osa meriforellidest lõhe-neerueoslikuga nakatunud. Ühtlasi peegeldas uuritud parasiidi levikumuster neerueosliku esinemise sagedust Eesti rannikujõgedes. Samuti selgus, et nugilisega nakatumise tõenäosus suureneb koos vanusega ning uuritud valimi hulgas leidus neerueoslikku ka kuue aasta vanustel meriforellidel. Kokkuvõtvalt võib öelda, et käesolev väitekiri lisab uusi olulisi teadmisi lõhe-neerueosliku geograafilise leviku, esinemissageduse ja vohandilise neeruhaiguse haigusdünaamika kohta lõhilastel ning identifitseerib veel siiani lahendamata küsimusi parasiidi ökoloogias. | est |
dc.description.abstract | Publication of this thesis is supported by Estonian University of Life Sciences. | eng |
dc.description.sponsorship | Publication of this thesis is supported by Estonian University of Life Sciences. | eng |
dc.identifier.isbn | 978-9916-719-75-6 | |
dc.identifier.issn | 2382-7076 | |
dc.identifier.uri | http://hdl.handle.net/10492/8899 | |
dc.identifier.uri | https://doi.org/10.15159/emu.135 | |
dc.publisher | Estonian University of Life Sciences | eng |
dc.relation.ispartofseries | Doctoral Theses of the Estonian University of Life Sciences | eng |
dc.relation.ispartofseries | Eesti Maaülikooli doktoritööd | est |
dc.rights | © Magnus Lauringson, 2024 | |
dc.rights | info:eu-repo/semantics/openAccess | eng |
dc.rights.uri | https://www.riigiteataja.ee/en/eli/ee/Riigikogu/act/519062017005/consolide | est |
dc.subject | dissertations | enh |
dc.subject | dissertatsioonid | est |
dc.subject | Roheline Ülikool (töö toetab EMÜ Rohelise Ülikooli põhimõtteid) | est |
dc.subject | Green University (thesis is related to EMÜ Green University iniciative’s aims) | eng |
dc.subject | parasiidid | est |
dc.subject | lõhe-neerueoslik | est |
dc.subject | Tetracapsuloides bryosalmonae | lat |
dc.subject | levik (bioloogia) | est |
dc.subject | lõhilased | est |
dc.subject | parasites | eng |
dc.subject | distribution (biology) | eng |
dc.subject | salmonids | eng |
dc.title | Distribution patterns, inter-and intra-host dynamics of an emerging salmonid parasite T. bryosalmonae across temporal and spatial scales | eng |
dc.title.alternative | Lõhe-neerueosliku (T. bryosalmonae) levikumustrid, peremeesliikide sisene ja vaheline esinemis- ja haigusdünaamika lõhilastel | est |
dc.type | info:eu-repo/semantics/doctoralThesis | eng |
dc.type.qualificationname | PhD |
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