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6. Using decision analysis to support proactive management of emerging infectious wildlife diseases

Author

Grant, Evan H Campbell, Muths, Erin, Katz, Rachel A, Canessa, Stefano, Adams, Michael J, Ballard, Jennifer R, Berger, Lee, Briggs, Cheryl J, Coleman, Jeremy TH, Gray, Matthew J, Harris, M Camille, Harris, Reid N, Hossack, Blake, Huyvaert, Kathryn P, Kolby, Jonathan, Lips, Karen R, Lovich, Robert E, McCallum, Hamish I, Mendelson, Joseph R, Nanjappa, Priya, Olson, Deanna H, Powers, Jenny G, Richgels, Katherine LD, Russell, Robin E, Schmidt, Benedikt R, Spitzen-van der Sluijs, Annemarieke, Watry, Mary Kay, Woodhams, Douglas C, and White, C LeAnn

Published
2017

7. Divergent population responses following salamander mass mortalities and declines driven by the emerging pathogen Batrachochytrium salamandrivorans

Author

Erens, Jesse, primary, Preissler, Kathleen, additional, Speybroeck, Jeroen, additional, Beukema, Wouter, additional, Spitzen-van der Sluijs, Annemarieke, additional, Stark, Tariq, additional, Laudelout, Arnaud, additional, Kinet, Thierry, additional, Schmidt, Benedikt R., additional, Martel, An, additional, Steinfartz, Sebastian, additional, and Pasmans, Frank, additional

Published
2023
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8. FIRST RECORD OF BATRACHOCHYTRIUM DENDROBATIDIS IN THE NORTHERN NETHERLANDS.

Author

Mantzana-Oikonomaki, Vasiliki, Desreveaux, Anne, Preißler, Kathleen, Maan, Martine E., Spitzen-van der Sluijs, Annemarieke, and Sabino-Pinto, Joana

Subjects
BATRACHOCHYTRIUM dendrobatidis, AMPHIBIANS, CHYTRIDIOMYCOSIS
Abstract

Batrachochytrium dendrobatidis (Bd) infects amphibians and has been linked to the decline of hundreds of anuran amphibians all over the world. In the province of Groningen in the Netherlands, this fungal pathogen was not detected before this study. To determine whether Groningen was Bd-free, we surveyed 12 locations in this province in 2020 and 2021. Samples were then used to quantify the presence of Bd with a qPCR assay. In total, 2 out of 110 (∼0.02%) collected in 2020 and 11 out of 249 samples collected in 2021 tested positive for Bd. Infected amphibians were found in 4 out of the 12 sites, and the prevalence of Bd was estimated at 4% for both years combined. Our study provides the first record of Bd in Groningen, and we hypothesize that Bd is present throughout the Netherlands in regions currently considered "Bd-free." Furthermore, we warn scientists and policymakers to be apprehensive when calling a site free from Bd when sampling is limited or not recent. [ABSTRACT FROM AUTHOR]

Published
2024
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9. Sand lizards (Lacerta agilis) decrease nymphal infection prevalence for tick-borne pathogens Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in a coastal dune ecosystem

Author

Köhler, Clara Florentine, Sprong, Hein, Fonville, Manoj, Esser, Helen, de Boer, Willem Frederik, van der Spek, Vincent, Spitzen-van der Sluijs, Annemarieke, Köhler, Clara Florentine, Sprong, Hein, Fonville, Manoj, Esser, Helen, de Boer, Willem Frederik, van der Spek, Vincent, and Spitzen-van der Sluijs, Annemarieke

Abstract

Understanding which factors determine tick-borne disease hazard can contribute to effective disease control. In Europe, the hazard of the pathogens Borrelia burgdorferi s.l. and Anaplasma phagocytophilum is determined by local tick densities (mainly Ixodes ricinus) and the reservoir competence of the host species community. Sand lizards (Lacerta agilis) are common hosts for larvae and nymphs of I. ricinus and non-competent reservoirs for both pathogens. Consequently, high relative abundance of L. agilis is hypothesized to be associated with lower infection prevalence in nymphs. Here, we aimed to test whether this effectively occurs in natural settings. We sampled different habitat types within a heterogenous dune landscape at the Dutch coast and estimated (1) L. agilis densities, (2) host community competence, (3) the density and infection prevalence of questing I. ricinus ticks and (4) the number and infection prevalence of ticks feeding on L. agilis. Captured L. agilis had high tick burdens and contributed substantially to feeding I. ricinus larvae in their natural habitat. B. burgdorferi s.l. and A. phagocytophilum were virtually absent from feeding larvae and nymphs. The nymphal infection prevalence of both pathogens in questing ticks was lower in habitat types where L. agilis was more abundant. Hence, L. agilis strongly reduced community competence. The density of questing nymphs was higher in habitat types with denser vegetation and also varied more between habitat types than infection prevalence. As a result, nymphal density had a stronger effect on the density of infected ticks than did nymphal infection prevalence. Synthesis and applications. Coastal dune habitats favourable for L. agilis have lower densities of questing nymphs and a lower human infection hazard. These results might be applicable to similar ecosystems where L. agilis is present. From a public health perspective, this underlines the importance of preserving early successional habitat, as enc

Published
2023

12. Compensatory recruitment allows amphibian population persistence in anthropogenic habitats

Author

Cayuela, Hugo, primary, Monod-Broca, Benjamin, additional, Lemaître, Jean-François, additional, Besnard, Aurélien, additional, Gippet, Jérôme M. W., additional, Schmidt, Benedikt R., additional, Romano, Antonio, additional, Hertach, Thomas, additional, Angelini, Claudio, additional, Canessa, Stefano, additional, Rosa, Giacomo, additional, Vignoli, Leonardo, additional, Venchi, Alberto, additional, Carafa, Marco, additional, Giachi, Filippo, additional, Tiberi, Andrea, additional, Hantzschmann, Alena M., additional, Sinsch, Ulrich, additional, Tournier, Emilie, additional, Bonnaire, Eric, additional, Gollmann, Günter, additional, Gollmann, Birgit, additional, Spitzen-van der Sluijs, Annemarieke, additional, Buschmann, Holger, additional, Kinet, Thierry, additional, Laudelout, Arnaud, additional, Fonters, Remi, additional, Bunz, Yoann, additional, Corail, Marc, additional, Biancardi, Carlo, additional, Di Cerbo, Anna R., additional, Langlois, Dominique, additional, Thirion, Jean-Marc, additional, Bernard, Laurent, additional, Boussiquault, Elodie, additional, Doré, Florian, additional, Leclerc, Titouan, additional, Enderlin, Nadine, additional, Laurenceau, Florian, additional, Morin, Lucy, additional, Skrzyniarz, Mégane, additional, Barrioz, Mickael, additional, Morizet, Yohan, additional, Cruickshank, Sam S., additional, Pichenot, Julian, additional, Maletzky, Andreas, additional, Delsinne, Thibaut, additional, Henseler, Dominik, additional, Aumaître, Damien, additional, Gailledrat, Miguel, additional, Moquet, Julien, additional, Veen, Robert, additional, Krijnen, Peter, additional, Rivière, Laurent, additional, Trenti, Matteo, additional, Endrizzi, Sonia, additional, Pedrini, Paolo, additional, Biaggini, Marta, additional, Vanni, Stefano, additional, Dudgeon, David, additional, Gaillard, Jean-Michel, additional, and Léna, Jean-Paul, additional

Published
2022
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14. Expanding distribution of lethal amphibian fungus Batrachochytrium salamandrivorans in Europe

Author

Spitzen-van der Sluijs, Annemarieke, Martel, An, Asselberghs, Johan, Bales, Emma K., Beukema, Wouter, Bletz, Molly C., Dalbeck, Lutz, Goverse, Edo, Kerres, Alexander, Kinet, Thierry, Kirst, Kai, Laudelout, Arnaud, Fonte, Luis F. Marin da, Nollert, Andreas, Ohlhoff, Dagmar, Sabino-Pinto, Joana, Schmidt, Benedikt R., Speybroeck, Jeroen, Spikmans, Frank, Steinfartz, Sebastian, Veith, Michael, Vences, Miguel, Wagner, Norman, Pasmans, Frank, and Lotters, Stefan

Subjects
Amphibians -- Health aspects, Disease transmission -- Forecasts and trends, Market trend/market analysis, Health
Abstract

Amphibians provide an iconic example of diseasedriven global loss in biodiversity. The recently described chytrid fungus Batrachochytrium salamandrivorans (Bsal) is an emerging pathogen that is driving amphibian populations to local [...]

Published
2016
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16. EAZA Amphibian Taxon Advisory Group Best Practice Guidelines (striped) fire salamander, Salamandra salamandra (terrestris)

Author

Bogaerts, Sergé, Lötters, Stefan, Spitzen-van der Sluijs, Annemarieke, Preißler, Kathleen, Caspers, Barbara, Oswald, Pia, Michaels, Christopher, ter Meulen, Tjerk, Reinhardt, Timm, Martel, An, Pasmans, Frank, Marcia, Gerardo, Tapley, Ben, and Marquis, Oliver

Abstract

EAZA Best Practice Guidelines (Striped) fire salamander, Salamandra salamandra (terrestris) is the first version of the EAZA Best Practice Guidelines for this species. This guideline has evolved out of the growing concern for extinction of local fire salamander populations due to the introduction of the invasive chytrid fungus Batrachochytrium salamandrivorans (Bsal) into Europe. Multiple populations of Salamandra salamandra terrestris have collapsed in north-western Europe. Upon the discovery of Bsal, and associated mass mortalities, a captive assurance colony was established in the Netherlands at GAIA Zoo and later also in Rotterdam Zoo. A studbook is managed in ZIMS by GAIA Zoo. In the face of continuous spreading of Bsal into new areas within Belgium and Germany, both countries aim to develop similar ex-situ programs. To ensure collaboration, shared goals and to effectively share knowledge and resources, the multidisciplinary ’Ex-situ Salamandra Group’ (ESG) was initiated by scientists, NGOs and zoos from the three bordering Bsal affected countries. Close collaboration and mutual commitment between all partners involved is the strength of this group. For this ex-situ program, it is necessary to collect available scientific knowledge on genetics, ecology and behaviour, and translate them into practical ways to keep and possibly in a later stage also breed the species. The development of a scientifically based and EAZA (European Association of Zoos and Aquaria) approved husbandry protocol for S. s. terrestris, as lies in front of you, is a first product. The complete literature list can be found at the end of this document. This document consists of two sections: • Section 1. Biology and field data: this part reflects the taxonomic information and information about the subspecies Salamandra salamandra terrestris as this subspecies has been the best studied of all subspecies and it is the focus subspecies for the ESG. It includes data on natural habitat, ecology, behaviour, diet and reproduction; • Section 2. Zoo management: this part includes suggestions about the enclosures, feeding, social structure, breeding, handling, transportation, veterinary problems of the fire salamander and recommended research to extent and improve this guideline. These Best Practice Guidelines are for current keepers who wish to expand their knowledge about this species to take care of the animals in the best possible way, but also for future keepers need for basic information. It is recommended to consult the guidelines and to contact the TAG-members for any questions or problems.

Published
2021

17. Does Chytridiomycosis Affect Tree Frog Attachment?

Author

Nieuwboer, L., van Leeuwen, J.L., Martel, An, Pasmans, Frank, Spitzen-Van Der Sluijs, Annemarieke, Langowski, J.K.A., Nieuwboer, L., van Leeuwen, J.L., Martel, An, Pasmans, Frank, Spitzen-Van Der Sluijs, Annemarieke, and Langowski, J.K.A.

Abstract

The pandemic disease chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), is a major threat to amphibian biodiversity. For most species, the exact mechanisms of chytridiomycosis that lead to negative population dynamics remain uncertain, though mounting evidence suggests that sublethal effects could be an important driver. In this review, we propose that tree frog attachment is a promising case to study the sublethal effects of a Bd infection on amphibians. A synthesis of the current knowledge on the functional morphology of the adhesive toe pads of tree frogs, on the underlying mechanisms of tree frog attachment, and on the epidermal pathology of chytridiomycosis substantiates the hypothesis that Bd-induced epidermal alterations have the potential to disrupt tree frog attachment. We highlight a series of (biomechanical) experiments to test this hypothesis and to shed some light on the sublethal disease mechanisms of chytridiomycosis. The knowledge generated from such an approach could contribute to future research on Bd epidemiology and ultimately to the conservation of the biodiversity of arboreal anurans.

Published
2021

20. Using environmental DNA for detection of Batrachochytrium salamandrivorans in natural water

Author

Spitzen ‐ van der Sluijs, Annemarieke, Stark, Tariq, DeJean, Tony, Verbrugghe, Elin, Herder, Jelger, Gilbert, Maarten, Janse, Jöran, Martel, An, Pasmans, Frank, Valentini, Alice, dI&I I&I-4, dI&I I&I-4, and Bernatchez, Louis

Subjects
lcsh:GE1-350, amphibians, Ecology, Natural water, Batrachochytrium salamandrivorans, Outbreak, Early detection, Zoology, Biology and Life Sciences, Biology, environmental DNA, lcsh:Microbial ecology, emerging infectious diseases, medicine.drug_formulation_ingredient, Genetics, medicine, lcsh:QR100-130, Environmental DNA, Garden pond, early detection, lcsh:Environmental sciences, Ecology, Evolution, Behavior and Systematics, Volume concentration
Abstract

Rapid, early, and reliable detection of invasive pathogenic microorganisms is essential in order to either predict or delineate an outbreak, and monitor appropriate mitigation measures. The chytrid fungus Batrachochytrium salamandrivorans is expanding in Europe, and infection with this fungus may cause massive mortality in urodelans (salamanders and newts). In this study, we designed and validated species‐specific primers and a probe for detection of B. salamandrivorans in water. In a garden pond in close proximity to the B. salamandrivorans index site in the Netherlands, B. salamandrivorans‐infected newts had been detected in 2015 and have been monitored since. In 2016 and 2017, no B. salamandrivorans was detected at this site, but in 2018 B. salamandrivorans flared up in this isolated pond which allowed validation of the technique in situ. We here present the development of an environmental DNA technique that successfully detects B. salamandrivorans DNA in natural waterbodies even at low concentrations. This technique may be further validated to play a role in B. salamandrivorans range delineation and surveillance in both natural waterbodies and in captive collections.

Published
2020

21. Using environmental DNA for detection of Batrachochytrium salamandrivorans in natural water

Author

dI&I I&I-4, Spitzen ‐ van der Sluijs, Annemarieke, Stark, Tariq, DeJean, Tony, Verbrugghe, Elin, Herder, Jelger, Gilbert, Maarten, Janse, Jöran, Martel, An, Pasmans, Frank, Valentini, Alice, dI&I I&I-4, Spitzen ‐ van der Sluijs, Annemarieke, Stark, Tariq, DeJean, Tony, Verbrugghe, Elin, Herder, Jelger, Gilbert, Maarten, Janse, Jöran, Martel, An, Pasmans, Frank, and Valentini, Alice

Published
2020

23. Mitigating Batrachochytrium salamandrivorans in Europe

Author

Thomas, Valarie, Wang, Yu, Van Rooij, Pascale, Verbrugghe, Elin, Baláž, Vojtech, Bosch, Jaime, Cunningham, Andrew A, Fisher, Matthew C, Garner, Trenton W J, Gilbert, Maarten J, Grasselli, Elena, Kinet, Thierry, Laudelout, Arnaud, Lötters, Stefan, Loyau, Adeline, Miaud, Claude, Salvidio, Sebastiano, Schmeller, Dirk S, Schmidt, B R; https://orcid.org/0000-0002-4023-1001, Spitzen-van der Sluijs, Annemarieke, Steinfartz, Sebastian, Veith, Michael, Vences, Miguel, Wagner, Norman, Canessa, Stefano, Martel, An, Pasmans, Frank, Thomas, Valarie, Wang, Yu, Van Rooij, Pascale, Verbrugghe, Elin, Baláž, Vojtech, Bosch, Jaime, Cunningham, Andrew A, Fisher, Matthew C, Garner, Trenton W J, Gilbert, Maarten J, Grasselli, Elena, Kinet, Thierry, Laudelout, Arnaud, Lötters, Stefan, Loyau, Adeline, Miaud, Claude, Salvidio, Sebastiano, Schmeller, Dirk S, Schmidt, B R; https://orcid.org/0000-0002-4023-1001, Spitzen-van der Sluijs, Annemarieke, Steinfartz, Sebastian, Veith, Michael, Vences, Miguel, Wagner, Norman, Canessa, Stefano, Martel, An, and Pasmans, Frank

Abstract

The infectious chytrid fungus Batrachochytrium salamandrivorans (Bsal) has been responsible for severe population declines of salamander populations in Europe. Serious population declines and loss of urodelan diversity may occur if appropriate action is not taken to mitigate against the further spread and impact of Bsal. We provide an overview of several potential mitigation methods, and describe their possible advantages and limitations. We conclude that long-term, context-dependent, multi-faceted approaches are needed to successfully mitigate adverse effects of Bsal, and that these approaches should be initiated pre-arrival of the pathogen. The establishment of ex situ assurance colonies, or management units, for species threatened with extinction, should be considered as soon as possible. While ex situ conservation and preventive measures aimed at improving biosecurity by limiting amphibian trade may be implemented quickly, major challenges that lie ahead are in designing in situ disease containment and mitigation post-arrival and in increasing public awareness.

Published
2019

24. Conservation decisions under pressure: Lessons from an exercise in rapid response to wildlife disease

Author

Canessa, Stefano, primary, Spitzen‐van der Sluijs, Annemarieke, additional, Stark, Tariq, additional, Allen, Bryony E., additional, Bishop, Phillip J., additional, Bletz, Molly, additional, Briggs, Cheryl J., additional, Daversa, David R., additional, Gray, Matthew J., additional, Griffiths, Richard A., additional, Harris, Reid N., additional, Harrison, Xavier A., additional, Hoverman, Jason T., additional, Jervis, Phillip, additional, Muths, Erin, additional, Olson, Deanna H., additional, Price, Stephen J., additional, Richards‐Zawacki, Corinne L., additional, Robert, Jacques, additional, Rosa, Gonçalo M., additional, Scheele, Ben C., additional, Schmidt, Benedikt R., additional, and Garner, Trenton W. J., additional

Published
2019
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26. Mitigating Batrachochytrium salamandrivorans in Europe

Author

Thomas, Valarie, primary, Wang, Yu, additional, Van Rooij, Pascale, additional, Verbrugghe, Elin, additional, Baláž, Vojtech, additional, Bosch, Jaime, additional, Cunningham, Andrew A., additional, Fisher, Matthew C., additional, Garner, Trenton W.J., additional, Gilbert, Maarten J., additional, Grasselli, Elena, additional, Kinet, Thierry, additional, Laudelout, Arnaud, additional, Lötters, Stefan, additional, Loyau, Adeline, additional, Miaud, Claude, additional, Salvidio, Sebastiano, additional, Schmeller, Dirk S., additional, Schmidt, Benedikt R., additional, Spitzen-van der Sluijs, Annemarieke, additional, Steinfartz, Sebastian, additional, Veith, Michael, additional, Vences, Miguel, additional, Wagner, Norman, additional, Canessa, Stefano, additional, Martel, An, additional, and Pasmans, Frank, additional

Published
2019
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27. Role of sand lizards in the ecology of Lyme and other tick-borne diseases in the Netherlands

Author

Spitzen - van der Sluijs Annemarieke, Reimerink Johan HJ, Fonville Manoj, Tijsse-Klasen Ellen, and Sprong Hein

Subjects
Infectious and parasitic diseases, RC109-216
Abstract

Abstract Background Lizards are considered zooprophylactic for almost all Borrelia burgdorferi species, and act as dilution hosts in parts of North America. Whether European lizards significantly reduce the ability of B. burgdorferi to maintain itself in enzootic cycles, and consequently decrease the infection rate of Ixodes ricinus ticks for B. burgdorferi and other tick-borne pathogens in Western Europe is not clear. Results Ticks were collected from sand lizards, their habitat (heath) and from the adjacent forest. DNA of tick-borne pathogens was detected by PCR followed by reverse line blotting. Tick densities were measured at all four locations by blanket dragging. Nymphs and adult ticks collected from lizards had a significantly lower (1.4%) prevalence of B. burgdorferi sensu lato, compared to questing ticks in heath (24%) or forest (19%). The prevalence of Rickettsia helvetica was significantly higher in ticks from lizards (19%) than those from woodland (10%) whereas neither was significantly different from the prevalence in ticks from heather (15%). The prevalence of Anaplasma and Ehrlichia spp in heather (12%) and forest (14%) were comparable, but significantly lower in ticks from sand lizards (5.4%). The prevalence of Babesia spp in ticks varied between 0 and 5.3%. Tick load of lizards ranged from 1 - 16. Tick densities were ~ 5-fold lower in the heather areas than in woodlands at all four sites. Conclusions Despite their apparent low reservoir competence, the presence of sand lizards had insignificant impact on the B. burgdorferi s.l. infection rate of questing ticks. In contrast, sand lizards might act as reservoir hosts for R. helvetica. Remarkably, the public health risk from tick-borne diseases is approximately five times lower in heather than in woodland, due to the low tick densities in heather.

Published
2010
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28. Ranavirus genotypes in the Netherlands and their potential association with virulence in water frogs (Pelophylax spp.)

Author

dPB I&I, Veterinair Pathologisch Diagnostisch Cnt, dFAH AVR, LS Theoretische Epidemiologie, LS Klinisch Onderzoek Wagenaar, dI&I I&I-4, dPB CR, LS Pathologie, Saucedo, Bernardo, Hughes, Joseph, Spitzen-van der Sluijs, Annemarieke, Kruithof, Natasja, Schills, Marc, Rijks, Jolianne M, Jacinto-Maldonado, Mónica, Suarez, Nicolás, Haenen, Olga L M, Voorbergen-Laarman, Michal A, van den Broek, Jan, Gilbert, Maarten, Gröne, Andrea, van Beurden, Steven J, Verheije, M Hélène, dPB I&I, Veterinair Pathologisch Diagnostisch Cnt, dFAH AVR, LS Theoretische Epidemiologie, LS Klinisch Onderzoek Wagenaar, dI&I I&I-4, dPB CR, LS Pathologie, Saucedo, Bernardo, Hughes, Joseph, Spitzen-van der Sluijs, Annemarieke, Kruithof, Natasja, Schills, Marc, Rijks, Jolianne M, Jacinto-Maldonado, Mónica, Suarez, Nicolás, Haenen, Olga L M, Voorbergen-Laarman, Michal A, van den Broek, Jan, Gilbert, Maarten, Gröne, Andrea, van Beurden, Steven J, and Verheije, M Hélène

Published
2018

29. Ranavirus genotypes in Netherlands and their potential association with virulence in water frogs (Pelophylax spp.)

Author

Saucedo, Bernardo, Hughes, Joseph, Spitzen-Van Der Sluijs, Annemarieke, Kruithof, Natasja, Schills, Marc, Rijks, Jolianne M., Jacinto-Maldonado, Mónica, Suarez, Nicolás, Haenen, Olga L.M., Voorbergen-Laarman, Michal, Van Den Broek, Jan, Gilbert, Maarten, Gröne, Andrea, van Beurden, Steven J., Verheije, M.H., Saucedo, Bernardo, Hughes, Joseph, Spitzen-Van Der Sluijs, Annemarieke, Kruithof, Natasja, Schills, Marc, Rijks, Jolianne M., Jacinto-Maldonado, Mónica, Suarez, Nicolás, Haenen, Olga L.M., Voorbergen-Laarman, Michal, Van Den Broek, Jan, Gilbert, Maarten, Gröne, Andrea, van Beurden, Steven J., and Verheije, M.H.

Abstract

Ranaviruses are pathogenic viruses for poikilothermic vertebrates worldwide. The identification of a common midwife toad virus (CMTV) associated with massive die-offs in water frogs (Pelophylax spp.) in Netherlands has increased awareness for emerging viruses in amphibians in the country. Complete genome sequencing of 13 ranavirus isolates collected from ten different sites in the period 2011-2016 revealed three CMTV groups present in distinct geographical areas in Netherlands. Phylogenetic analysis showed that emerging viruses from the northern part of Netherlands belonged to CMTV-NL group I. Group II and III viruses were derived from the animals located in the center-east and south of the country, and shared a more recent common ancestor to CMTV-amphibian associated ranaviruses reported in China, Italy, Denmark, and Switzerland. Field monitoring revealed differences in water frog host abundance at sites where distinct ranavirus groups occur; with ranavirus-associated deaths, host counts decreasing progressively, and few juveniles found in the north where CMTV-NL group I occurs but not in the south with CMTV-NL group III. Investigation of tandem repeats of coding genes gave no conclusive information about phylo-geographical clustering, while genetic analysis of the genomes revealed truncations in 17 genes across CMTV-NL groups II and III compared to group I. Further studies are needed to elucidate the contribution of these genes as well as environmental variables to explain the observed differences in host abundance.

Published
2018

31. Investigation of Amphibian Mortality Events in Wildlife Reveals an On-Going Ranavirus Epidemic in the North of the Netherlands

Author

Rijks, Jolianne M, Saucedo, Bernardo, Spitzen-van der Sluijs, Annemarieke, Wilkie, Gavin S, van Asten, Alphons J A M, van den Broek, Jan, Boonyarittichaikij, Roschong, Stege, Marisca, van der Sterren, Fleur, Martel, An, Pasmans, Frank, Hughes, Joseph, Gröne, Andrea, van Beurden, Steven J, Kik, Marja J L, Veterinair Pathologisch Diagnostisch Cnt, LS Pathologie, dPB I&I, Infection & Immunity, dFAH AVR, Applied Veterinary Research, Veterinair Pathologisch Diagnostisch Cnt, LS Pathologie, dPB I&I, Infection & Immunity, dFAH AVR, and Applied Veterinary Research

Subjects
0301 basic medicine, Pelobates fuscus, Ranavirus, MAJOR CAPSID PROTEIN, Animal Phylogenetics, Pathology and Laboratory Medicine, DISEASE, Geographical Locations, 0403 veterinary science, Larvae, MOLECULAR, Medicine and Health Sciences, IRIDOVIRUS, Phylogeny, Netherlands, Data Management, Multidisciplinary, biology, Ecology, Spadefoot toad, 04 agricultural and veterinary sciences, DNA Virus Infections, 3. Good health, Europe, Phylogenetics, Vertebrates, Medicine, Sequence Analysis, Research Article, PELOPHYLAX KL. ESCULENTUS, Amphibian, Computer and Information Sciences, food.ingredient, 040301 veterinary sciences, Iridovirus, Science, MODELS, Animals, Wild, Research and Analysis Methods, Toads, Amphibians, Necrosis, 03 medical and health sciences, Signs and Symptoms, food, Midwife toad, FISH, Diagnostic Medicine, biology.animal, Animals, Evolutionary Systematics, Veterinary Sciences, Molecular Biology Techniques, Sequencing Techniques, Epidemics, Molecular Biology, Taxonomy, Evolutionary Biology, Metamorphosis, Organisms, Outbreak, Biology and Life Sciences, biology.organism_classification, 030104 developmental biology, People and Places, Threatened species, CHARACTERIZATION, Zoology, Sequence Alignment, Developmental Biology
Abstract

In the four years following the first detection of ranavirus (genus Ranavirus, family Iridoviridae) infection in Dutch wildlife in 2010, amphibian mortality events were investigated nationwide to detect, characterize and map ranaviruses in amphibians over time, and to establish the affected host species and the clinico-pathological presentation of the disease in these hosts. The ultimate goal was to obtain more insight into ranavirus disease emergence and ecological risk. In total 155 dead amphibians from 52 sites were submitted between 2011 and 2014, and examined using histopathology, immunohistochemistry, virus isolation and molecular genetic characterization. Ranavirus-associated amphibian mortality events occurred at 18 sites (35%), initially only in proximity of the 2010 index site. Specimens belonging to approximately half of the native amphibian species were infected, including the threatened Pelobates fuscus (spadefoot toad). Clustered massive outbreaks involving dead adult specimens and ranavirus genomic identity indicated that one common midwife toad virus (CMTV)-like ranavirus strain is emerging in provinces in the north of the Netherlands. Modelling based on the spatiotemporal pattern of spread showed a high probability that this emerging virus will continue to be detected at new sites (the discrete reproductive power of this outbreak is 0.35). Phylogenetically distinct CMTV-like ranaviruses were found in the south of the Netherlands more recently. In addition to showing that CMTV-like ranaviruses threaten wild amphibian populations not only in Spain but also in the Netherlands, the current spread and risk of establishment reiterate that understanding the underlying causes of CMTV-like ranavirus emergence requires international attention.

Published
2016

33. Course of an Isolated Ranavirus Outbreak in a Pelobates fuscus Population in The Netherlands

Author

Spitzen-van der Sluijs, Annemarieke, Pasmans, Frank, Struijk, Richard P.J.H., Schils, Marc, Doorbos, Pieter, van der Sterren, Fleur, Rijks, J.M., Kik, M.J.L., Saucedo, Bernardo, Bosman, Willem, Martel, An, Spitzen-van der Sluijs, Annemarieke, Pasmans, Frank, Struijk, Richard P.J.H., Schils, Marc, Doorbos, Pieter, van der Sterren, Fleur, Rijks, J.M., Kik, M.J.L., Saucedo, Bernardo, Bosman, Willem, and Martel, An

Abstract

Viruses in the genus Ranavirus (family Iridoviridae) are known to have the potential to adversely affect fish, amphibians, and reptiles. Ranaviruses are associated with large-scale die-offs and rapid population declines in amphibians. The development and progression of an outbreak, however, vary greatly depending on the host species and geographic location. We describe the recurrent course of an outbreak of common midwife toad virus in an isolated population (Staphorst) of common spadefoot toads (Pelobates fuscus) in The Netherlands from 2012 to 2015. After initial mass mortality of toad larvae in 2012, no mass mortality was recorded in 2013 and 2014. In 2015, however, a recurrent outbreak of the virus is believed to have caused high mortality rates among this species in the Staphorst population.

Published
2016

34. Course of an Isolated Ranavirus Outbreak in a Pelobates fuscus Population in The Netherlands

Author

Veterinair Pathologisch Diagnostisch Cnt, Dutch Wildlife Health Centre (DWHC), dPB I&I, Spitzen-van der Sluijs, Annemarieke, Pasmans, Frank, Struijk, Richard P.J.H., Schils, Marc, Doorbos, Pieter, van der Sterren, Fleur, Rijks, J.M., Kik, M.J.L., Saucedo, Bernardo, Bosman, Willem, Martel, An, Veterinair Pathologisch Diagnostisch Cnt, Dutch Wildlife Health Centre (DWHC), dPB I&I, Spitzen-van der Sluijs, Annemarieke, Pasmans, Frank, Struijk, Richard P.J.H., Schils, Marc, Doorbos, Pieter, van der Sterren, Fleur, Rijks, J.M., Kik, M.J.L., Saucedo, Bernardo, Bosman, Willem, and Martel, An

Published
2016

35. Investigation of Amphibian Mortality Events in Wildlife Reveals an On-Going Ranavirus Epidemic in the North of the Netherlands

Author

Veterinair Pathologisch Diagnostisch Cnt, LS Pathologie, dPB I&I, Infection & Immunity, dFAH AVR, Applied Veterinary Research, Rijks, Jolianne M, Saucedo, Bernardo, Spitzen-van der Sluijs, Annemarieke, Wilkie, Gavin S, van Asten, Alphons J A M, van den Broek, Jan, Boonyarittichaikij, Roschong, Stege, Marisca, van der Sterren, Fleur, Martel, An, Pasmans, Frank, Hughes, Joseph, Gröne, Andrea, van Beurden, Steven J, Kik, Marja J L, Veterinair Pathologisch Diagnostisch Cnt, LS Pathologie, dPB I&I, Infection & Immunity, dFAH AVR, Applied Veterinary Research, Rijks, Jolianne M, Saucedo, Bernardo, Spitzen-van der Sluijs, Annemarieke, Wilkie, Gavin S, van Asten, Alphons J A M, van den Broek, Jan, Boonyarittichaikij, Roschong, Stege, Marisca, van der Sterren, Fleur, Martel, An, Pasmans, Frank, Hughes, Joseph, Gröne, Andrea, van Beurden, Steven J, and Kik, Marja J L

Published
2016

38. Expanding Distribution of Lethal Amphibian FungusBatrachochytrium salamandrivoransin Europe

Author

Spitzen-van der Sluijs, Annemarieke, primary, Martel, An, additional, Asselberghs, Johan, additional, Bales, Emma K., additional, Beukema, Wouter, additional, Bletz, Molly C., additional, Dalbeck, Lutz, additional, Goverse, Edo, additional, Kerres, Alexander, additional, Kinet, Thierry, additional, Kirst, Kai, additional, Laudelout, Arnaud, additional, Marin da Fonte, Luis F., additional, Nöllert, Andreas, additional, Ohlhoff, Dagmar, additional, Sabino-Pinto, Joana, additional, Schmidt, Benedikt R., additional, Speybroeck, Jeroen, additional, Spikmans, Frank, additional, Steinfartz, Sebastian, additional, Veith, Michael, additional, Vences, Miguel, additional, Wagner, Norman, additional, Pasmans, Frank, additional, and Lötters, Stefan, additional

Published
2016
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39. Salamander chytrid fungus (Batrachochytrium salamandrivorans) in the United States—Developing research, monitoring, and management strategies

Author

Campbell Grant, Evan H., primary, Muths, Erin L., additional, Katz, Rachel A., additional, Canessa, Stefano, additional, Adams, M.J., additional, Ballard, Jennifer R., additional, Berger, Lee, additional, Briggs, Cheryl J., additional, Coleman, Jeremy, additional, Gray, Matthew J., additional, Harris, M. Camille, additional, Harris, Reid N., additional, Hossack, Blake R., additional, Huyvaert, Kathryn P., additional, Kolby, Jonathan E., additional, Lips, Karen R., additional, Lovich, Robert E., additional, McCallum, Hamish I., additional, Mendelson, Joseph R., additional, Nanjappa, Priya, additional, Olson, Deanna H., additional, Powers, Jenny G., additional, Richgels, Katherine L. D., additional, Russell, Robin E., additional, Schmidt, Benedikt R., additional, Spitzen-van der Sluijs, Annemarieke, additional, Watry, Mary Kay, additional, Woodhams, Douglas C., additional, and White, C. LeAnn, additional

Published
2016
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41. The novel ‘CandidatusAmphibiichlamydia ranarum’ is highly prevalent in invasive exotic bullfrogs (Lithobates catesbeianus)

Author

Martel, An, primary, Adriaensen, Connie, additional, Sharifian‐Fard, Mojdeh, additional, Vandewoestyne, Mado, additional, Deforce, Dieter, additional, Favoreel, Herman, additional, Bergen, Karolien, additional, Spitzen‐van der Sluijs, Annemarieke, additional, Devisscher, Sander, additional, Adriaens, Tim, additional, Louette, Gerald, additional, Baert, Kristof, additional, Hyatt, Alex, additional, Crameri, Sandra, additional, Haesebrouck, Freddy, additional, and Pasmans, Frank, additional

Published
2012
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43. Death in the clouds: ranavirus associated mortality in assemblage of cloud forest amphibians in Nicaragua.

Author

STARK, TARIQ, LAURIJSSENS, CARLIJN, WETERINGS, MARTIJN, SPITZEN-VAN DER SLUIJS, ANNEMARIEKE, MARTEL, AN, and PASMANS, FRANK

Subjects
AMPHIBIANS, CHYTRIDIOMYCOSIS, LITHOBATES, AGALYCHNIS, TADPOLES
Abstract

Amphibian diseases are acknowledged as significant contributors to the decline and extinction of amphibian species. The main culprits currently considered are chytridiomycosis and Ranavirus. In Central America, highly endemic and geographical restricted terrestrial species may be at risk from these diseases. We collected 49 Agalychnis callidryas larvae, one Lithobates forrei and five unidentified larvae on the Nicaraguan Island Ometepe, all deceased, and skin samples were taken. The presence of Ranavirus was determined using PCR. Ranavirus was found involved in 41 of 55 tadpoles. Forty-one Agalychnis callidryas, one Lithobates forrei and another five unidentified anuran tadpoles. [ABSTRACT FROM AUTHOR]

Published
2014
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44. Conservation decisions under pressure: Lessons from an exercise in rapid response to wildlife disease.

Author

Canessa, Stefano, Spitzen‐van der Sluijs, Annemarieke, Stark, Tariq, Allen, Bryony E., Bishop, Phillip J., Bletz, Molly, Briggs, Cheryl J., Daversa, David R., Gray, Matthew J., Griffiths, Richard A., Harris, Reid N., Harrison, Xavier A., Hoverman, Jason T., Jervis, Phillip, Muths, Erin, Olson, Deanna H., Price, Stephen J., Richards‐Zawacki, Corinne L., Robert, Jacques, and Rosa, Gonçalo M.

Abstract

Novel outbreaks of emerging pathogens require rapid responses to enable successful mitigation. We simulated a 1‐day emergency meeting where experts were engaged to recommend mitigation strategies for a new outbreak of the amphibian fungal pathogen Batrachochytrium salamandrivorans. Despite the inevitable uncertainty, experts suggested and discussed several possible strategies. However, their recommendations were undermined by imperfect initial definitions of the objectives and scope of management. This problem is likely to arise in most real‐world emergency situations. The exercise thus highlighted the importance of clearly defining the context, objectives, and spatial–temporal scale of mitigation decisions. Managers are commonly under pressure to act immediately. However, an iterative process in which experts and managers cooperate to clarify objectives and uncertainties, while collecting more information and devising mitigation strategies, may be slightly more time consuming but ultimately lead to better outcomes. [ABSTRACT FROM AUTHOR]

Published
2020
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45. Ranavirus-associated mass mortality in wild amphibians, The Netherlands, 2010: A first report.

Author

Kik, Marja, Martel, An, Spitzen-van der Sluijs, Annemarieke, Pasmans, Frank, Wohlsein, Peter, Gröne, Andrea, and Rijks, Jolianne M.

Subjects
*VETERINARY medicine, *PELOPHYLAX, *NEWTS, *VETERINARY virology, *HEMORRHAGIC diseases, *ANIMAL mortality
Abstract

In 2010, a mass die-off of over 1000 wild water frogs (Pelophylax spp.) and at least 10 common newts (Lissotriton vulgaris) occurred in a pond in The Netherlands. Haemorrhagic disease with hepatomegaly and splenomegaly was evident. Microscopically, multiple organs presented cells with multifocal intracytoplasmic inclusion bodies, in which ranavirus-like particles were demonstrated ultrastructurally. All specimens examined tested positive for ranavirus by PCR. The sequence obtained showed a 100% identity with the one deposited for common midwife toad virus (CMTV). This is the first report of ranavirus-associated mortality in wild amphibian populations in The Netherlands. It is also the first time CMTV or a CMTV-like virus has been reported in these two species in the adult stage and outside of Spain. [ABSTRACT FROM AUTHOR]

Published
2011
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46. Divergent population responses following salamander mass mortalities and declines driven by the emerging pathogen Batrachochytrium salamandrivorans .

Author

Erens J, Preissler K, Speybroeck J, Beukema W, Spitzen-van der Sluijs A, Stark T, Laudelout A, Kinet T, Schmidt BR, Martel A, Steinfartz S, and Pasmans F

Subjects
Animals, Batrachochytrium, Amphibians, Urodela, Chytridiomycota physiology
Abstract

Understanding wildlife responses to novel threats is vital in counteracting biodiversity loss. The emerging pathogen Batrachochytrium salamandrivorans ( Bsal ) causes dramatic declines in European salamander populations, and is considered an imminent threat to global amphibian biodiversity. However, real-life disease outcomes remain largely uncharacterized. We performed a multidisciplinary assessment of the longer-term impacts of Bsal on highly susceptible fire salamander ( Salamandra salamandra ) populations, by comparing four of the earliest known outbreak sites to uninfected sites. Based on large-scale monitoring efforts, we found population persistence in strongly reduced abundances to over a decade after Bsal invasion, but also the extinction of an initially small-sized population. In turn, we found that host responses varied, and Bsal detection remained low, within surviving populations. Demographic analyses indicated an ongoing scarcity of large reproductive adults with potential for recruitment failure, while spatial comparisons indicated a population remnant persisting within aberrant habitat. Additionally, we detected no early signs of severe genetic deterioration, yet nor of increased host resistance. Beyond offering additional context to Bsal -driven salamander declines, results highlight how the impacts of emerging hypervirulent pathogens can be unpredictable and vary across different levels of biological complexity, and how limited pathogen detectability after population declines may complicate surveillance efforts.

Published
2023
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