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The response in native wildlife to an invading pathogen: Swedish amphibians and Batrachochytrium dendrobatidis
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Emerging infectious diseases are causing mortality and declines in wildlife populations globally. My thesis aims to get as clear a picture as possible of the effect the invasive chytrid fungus Batrachochytrium dendrobatidis has on the Swedish amphibian community.

In Paper I I performed a large-scale survey testing for the presence of Bd in three regions in Sweden (Southern, Central and Northern). I sampled 1917 amphibians from 101 localities and found that Bd was widespread in southern and central Sweden, occurring in all nine investigated species and in 45.5 % of the sampled sites with an overall prevalence of 13.8%. I found a positive correlation between the temperature at spawning for each species and species prevalence. Species that require higher temperatures for egg-laying are distributed in the southern parts of the country, which led to a higher prevalence in the southern region.

In Paper II, I investigated which local environmental factors in breeding habitats, landscape structure and amphibian community affect the occurrence and prevalence of Bd among breeding sites in southern Sweden. Bd prevalence in the four species with the highest prevalence (Bombina bombina, Bufotes variabilis, Epidalea calamita and Rana arvalis) was higher in ponds surrounded by less mature forest, few wetlands, and higher pH.

In Papers III and IV, I looked at species and population differences in responses to Bd infection. I performed an infection experiment described in Paper III, where I exposed individuals from two common Swedish species (moor frog R. arvalis and common toad Bufo bufo) originating from two regions (north and south) with two different strains of Bd (from Sweden and the UK). I found that infection led to lower survival and growth in both species, more so in B. bufo than in R. arvalis. Small size proved to be a strong determinant of survival. As individuals from the northern population were significantly smaller than the southern ones, this may have led to the northern populations being more affected by Bd infection. In Paper IV, I studied variation in MHC Class IIB loci in B. bufo along a latitudinal gradient across Sweden. Variation in MCH genes decreased from south to north. Also, differences in survival from the experiment in Paper III could be explained by MHC haplotypes. I found that survival in the southern region was dependent on both Bd-strain and MHC haplotype.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. , p. 44
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1879
Keywords [en]
Emerging diseases, chytrid, amphibians, wildlife
National Category
Ecology
Research subject
Biology with specialization in Animal Conservation
Identifiers
URN: urn:nbn:se:uu:diva-396987ISBN: 978-91-513-0812-8 (print)OAI: oai:DiVA.org:uu-396987DiVA, id: diva2:1369696
Public defence
2019-12-13, Ekmansalen, EBC, Norbyvägen 14, Uppsala, 10:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council FormasAvailable from: 2019-11-15 Created: 2019-11-12 Last updated: 2019-11-18
List of papers
1. Occurrence of Batrachochytrium dendrobatidis in Sweden: higher infection prevalence in southern species
Open this publication in new window or tab >>Occurrence of Batrachochytrium dendrobatidis in Sweden: higher infection prevalence in southern species
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The chytrid fungus Batrachochytrium dendrobatidis (Bd) has caused worldwide declines in amphibian populations. While Bd is widespread in southern and central Europe, its occurrence and distribution in northernmost Europe is mostly unknown. We surveyed for Bd in breeding anurans in Sweden by sampling 1917 amphibians from 101 localities and three regions in Sweden (Southern, Northern and Central). We found that Bd was widespread in southern and central Sweden, occurring in all nine investigated species and in 45.5 % of the 101 localities with an overall prevalence of 13.8%. No infected individuals were found in the four northern sites sampled. The records from central Sweden represent the northernmost records of Bd in Europe. While the proportion of sites positive for Bd was similar between the southern and central areas, prevalence was much higher in the southern area. This was due to southern species with a distribution mainly restricted to southernmost Sweden having higher prevalence than widespread generalist species. The nationally red-listed green toad Bufotes variabilis and fire bellied toad Bombina bombina had the highest prevalence (61.4% and 48.9% respectively). Across species, Bd prevalence was strongly positively correlated with water temperature at the start of egg-laying. However, no individuals showing visual signs of chytridiomycosis were found in the field. These results indicate that Bd is widespread and common in southern and central Sweden with southern species breeding in higher temperatures and with longer breeding periods having higher prevalence. However, the impact of Bd on amphibian populations in northernmost Europe remains unknown.

Keywords
chytrid, emerging diseases, amphibian
National Category
Ecology
Research subject
Biology with specialization in Animal Conservation
Identifiers
urn:nbn:se:uu:diva-396761 (URN)
Funder
Swedish Research Council Formas
Available from: 2019-11-08 Created: 2019-11-08 Last updated: 2019-11-12
2. Effects of host species and environmental factors on the prevalence of Batrachochytrium dendrobatidis in northern Europe
Open this publication in new window or tab >>Effects of host species and environmental factors on the prevalence of Batrachochytrium dendrobatidis in northern Europe
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2018 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 13, no 10, article id e0199852Article in journal (Refereed) Published
Abstract [en]

The fungal pathogen Batrachochytrium dendrobatidis (Bd) poses a major threat to amphibian populations. To assist efforts to address such threats, we examined differences in Bd host infection prevalence among amphibian species and its relations to both local environmental factors in breeding habitats and landscape variables measured at three scales (500, 2000 and 5000 m radii) around breeding sites in southernmost Sweden. We sampled 947 anurans of six species in 31 ponds and assessed their infection status. We then examined correlations of infection prevalence with canopy cover, pond perimeter and pH (treated as local-scale pond characteristics), and the number of ponds, area of arable land, area of mature forest, number of resident people and presence of sea within the three radii (treated as landscape variables). The Bd infection prevalence was very low, 0.5-1.0%, in two of the six anuran species (Bufo bufo and Rana temporaria), and substantially higher (13-64%) in the other four (Bombina bombina, Bufotes variabilis, Epidalea calamita, Rana arvalis). In the latter four species Bd infection prevalence was positively associated with ponds' pH (site range: 5.3-8.1), and negatively associated with areas of mature forest and/or wetlands in the surroundings. Our results show that the infection dynamics of Bd are complex and associated with host species, local pond characteristics and several landscape variables at larger spatial scales. Knowledge of environmental factors associated with Bd infections and differences in species' susceptibility may help to counter further spread of the disease and guide conservation action plans, especially for the most threatened species.

Place, publisher, year, edition, pages
PUBLIC LIBRARY SCIENCE, 2018
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-369896 (URN)10.1371/journal.pone.0199852 (DOI)000448438400003 ()30359384 (PubMedID)
Funder
Swedish Research Council Formas, 215-2014-594Carl Tryggers foundation , 15:220, KF17:14
Available from: 2018-12-19 Created: 2018-12-19 Last updated: 2019-11-12Bibliographically approved
3. Body size mediates latitudinal population differences in response to Bd infection in two amphibian species
Open this publication in new window or tab >>Body size mediates latitudinal population differences in response to Bd infection in two amphibian species
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The chytrid fungus Batrachochytrium dendrobatidis (Bd), is a generalist pathogen which has caused amphibian population declines worldwide. In many species Bd infection causes the disease chytridiomycosis, leading to high mortality. However, infection may cause sub-lethal fitness effects even in species that are resistant or tolerant to Bd. Moreover, populations of the same species may differ in their sensitivity to Bd, but the factors behind this variation are poorly understood. Here we exposed two common North European amphibians (moor frog Rana arvalis, common toad Bufo bufo) from two latitudinally divergent regions to two different BdGPL strains in a laboratory experiment. We found that Bd exposure lowered survival in both species, but this effect was much stronger in B. bufo.  Moreover, survival was lower in the northern region in both species, this difference again being much stronger in B. bufo. Northern individuals were smaller in both species and the survival difference between regions was size mediated with smaller individuals being more sensitive to Bd. We discuss potential additional factors contributing to this result. Bd exposure also led to sub-lethal effects in terms of reduced growth in both species suggesting that even individuals surviving the infection may have reduced fitness mediated by reduction if body size. However, we did not detect any differences in amphibian responses to the two Bd strains.

Keywords
chytrid, latitudinal gradient, amphibians, regional differences
National Category
Ecology
Research subject
Biology with specialization in Animal Conservation
Identifiers
urn:nbn:se:uu:diva-396762 (URN)
Funder
Swedish Research Council Formas
Available from: 2019-11-08 Created: 2019-11-08 Last updated: 2019-11-12
4. Latitudinal MHC variation and haplotype associated differential survival in response to experimental infection of two strains of Bd-GPL in common toads
Open this publication in new window or tab >>Latitudinal MHC variation and haplotype associated differential survival in response to experimental infection of two strains of Bd-GPL in common toads
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-382090 (URN)10.1101/597559 (DOI)
Available from: 2019-04-20 Created: 2019-04-20 Last updated: 2019-11-12

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