From a local observation to a European-wide phenomenon: Amphibian deformities at Serra da Estrela Natural Park, Portugal

Laurentino, Telma G.; Pais, Miguel Pessanha; Rosa, Gonçalo M.

doi:10.11160/bah.15003

Cited by 14 publications

(18 citation statements)

References 31 publications

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“…Water quality analyses were not indicative of environmental contamination 66 . To reduce the risk of spreading pathogens across sites, we used disposable vinyl gloves to handle animals and disinfected field equipment and hiking boots in a 1% solution of Virkon ® (Antec International ltd., Sudbury, Suffolk, UK) between sites 67 .…”

Section: Methodsmentioning

confidence: 95%

Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages

Rosa

Sabino‐Pinto

Laurentino

et al. 2017

Sci Rep

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Emerging diseases have been increasingly associated with population declines, with co-infections exhibiting many types of interactions. The chytrid fungus (Batrachochytrium dendrobatidis) and ranaviruses have extraordinarily broad host ranges, however co-infection dynamics have been largely overlooked. We investigated the pattern of co-occurrence of these two pathogens in an amphibian assemblage in Serra da Estrela (Portugal). The detection of chytridiomycosis in Portugal was linked to population declines of midwife-toads (Alytes obstetricans). The asynchronous and subsequent emergence of a second pathogen - ranavirus - caused episodes of lethal ranavirosis. Chytrid effects were limited to high altitudes and a single host, while ranavirus was highly pathogenic across multiple hosts, life-stages and altitudinal range. This new strain (Portuguese newt and toad ranavirus – member of the CMTV clade) caused annual mass die-offs, similar in host range and rapidity of declines to other locations in Iberia affected by CMTV-like ranaviruses. However, ranavirus was not always associated with disease, mortality and declines, contrasting with previous reports on Iberian CMTV-like ranavirosis. We found little evidence that pre-existing chytrid emergence was associated with ranavirus and the emergence of ranavirosis. Despite the lack of cumulative or amplified effects, ranavirus drove declines of host assemblages and changed host community composition and structure, posing a grave threat to all amphibian populations.

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Section: Methodsmentioning

confidence: 95%

Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages

Rosa

Sabino‐Pinto

Laurentino

et al. 2017

Sci Rep

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“…We monitored another spring water artificial pond at a similar elevation where Ranavirus outbreaks have never been recorded but where infection occasionally occurs: the 50 m 2 artificial pond in the Sazes area (40°20'39.70”N, 7°42'52.63”W; 985 m a.s.l.). The two ponds are about 23 km apart, both approximately 1.2–1.7 m deep, located in mountain slopes with the same orientation (facing west), and have the same amphibian assemblage composition breeding regularly (Laurentino, Pais & Rosa, ; Rosa et al ., ).…”

Section: Methodsmentioning

confidence: 99%

“…Schematic phenology of the host species, Bosca's newt Lissotriton boscai in Serra da Estrela (Portugal) in ponds located at about 800-1100 m above sea level showing a representation of expected relative proportion of males and females in the water throughout the year. Arrow indicates time of the first outbreak of ranavirosis(2011)and dashed line illustrates the expected relative abundance of females in the absence of outbreak (based on relative data from previous years and other similar ponds, collected as part of ongoing amphibian monitoring studies;Rosa et al, 2013Rosa et al, , 2017Laurentino et al, 2016). Top bar represents the temperature throughout the year from cool (dark) to warm(light).…”

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confidence: 99%

Sex‐biased disease dynamics increase extinction risk by impairing population recovery

Rosa

Bosch

Martel

et al. 2019

Animal Conservation

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The periodicity of life‐cycle events (phenology) modulates host availability to pathogens in a repeatable pattern. The effects of sexual differences in host phenology have been little explored in wildlife epidemiological studies. A recent series of ranavirosis outbreaks led to serious declines of Boscas’ newt populations at Serra da Estrela (Portugal). The peculiar phenology of this species, in which a large number of females remain in the aquatic habitat after the breeding season, turns it into a suitable model to test how sex‐biased mortality can affect host population persistence in the context of infectious diseases. We investigated how the phenology of Bosca's newt (i.e. biased number of females) mediated the impact of Ranavirus. We then evaluated the risk of extinction of the population under different scenarios of sex‐biased mortality using a population viability analysis. Two newt populations (one subject to yearly outbreaks and a comparative site where outbreaks have not been recorded) were tracked for trends over time following emergence of ranaviral disease, allowing us to assess the differential impact of the disease on both sexes. In addition to a significant decline in abundance of adult newts, our data suggest that phenology can affect disease dynamics indirectly, leading to reduction in females and a reversal of the sex ratio of the breeding population. Our models suggest that female‐biased mortality does not exacerbate Ranavirus‐driven population declines in the short‐term, but is likely to have a deleterious impact during the recovery process once the lethal effect of disease is removed from the system.

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“…The most frequently reported abnormalities involve the hind limbs, including partially missing limbs, completely missing limbs, extra limbs, and misshapen limbs (Johnson, Reeves, et al., ; Reeves et al., ). Most recent reports involve North American amphibians, although mass malformations have also been observed in other countries (Bacon, Linzey, Rogers, & Fort, ; Flyaks & Borkin, ; Gurushankara, Krishnamurthy, & Vasudev, ; Laurentino, Pais, & Rosa, ; Ouellet, ). Several retrospective studies based on museum samples and historical resurveys further indicate that limb malformations have increased over time (Hoppe, ; Johnson & Lunde, ; McCallum & Trauth, ), highlighting the importance of investigating environmental changes associated with morphological abnormalities through space and time.…”

Section: Introductionmentioning

confidence: 96%

Continental‐extent patterns in amphibian malformations linked to parasites, chemical contaminants, and their interactions

Haas

Reeves

Pinkney

et al. 2017

Global Change Biology

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Widespread observations of malformed amphibians across North America have generated both concern and controversy. Debates over the causes of such malformationswhich can affect >50% of animals in a population-have continued, likely due to involvement of multiple causal factors. Here, we used a 13-year dataset encompassing 53,880 frogs and toads from 422 wetlands and 42 states in the conterminous USA to test hypotheses relating abnormalities and four categories of potential drivers: (i) chemical contaminants, (ii) land use practices, (iii) parasite infection, and (iv) targeted interactions between parasites and pesticides. Using a hierarchically nested, competing-model approach, we further examined how these associations varied spatially among geographic regions. Although malformations were rare overall (average = 1.6%), we identified 96 hotspot sites with 5%-25% abnormal individuals. Using the full dataset of 934 collections (without data on parasite infection), malformation frequency was best predicted by the presence of oil and gas wells within the watershed. Among collections also examined for parasite infection (n = 154), average parasite load and its interaction with pesticide application positively predicted malformations: wetlands with a greater abundance of the trematode Ribeiroia ondatrae were more likely to have malformed amphibians, but these effects were strongest when pesticide application was also high, consistent with prior experimental research.Importantly, however, the influence of these factors also varied regionally, helping explain divergent results from previous studies at local scales; parasite infection was more influential in the West and Northeast, whereas pesticide application and oil/gas wells correlated with abnormalities in the Northeast, Southeast, and western regions of the USA. These results, based on the largest systematic sampling of amphibian malformations, suggest that increased observations of abnormal amphibians are associated with both parasite infection and chemical contaminants, but that their relative importance and interaction strength varied with the spatial extent of the analysis.

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From a local observation to a European-wide phenomenon: Amphibian deformities at Serra da Estrela Natural Park, Portugal

Cited by 14 publications

References 31 publications

Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages

Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages

Sex‐biased disease dynamics increase extinction risk by impairing population recovery

Continental‐extent patterns in amphibian malformations linked to parasites, chemical contaminants, and their interactions

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