An emerging viral pathogen truncates population age structure in a European amphibian and may reduce population viability
- Published
- Accepted
- Subject Areas
- Conservation Biology, Ecology, Zoology, Freshwater Biology, Population Biology
- Keywords
- Demography, Environmental Stochasticity, Disease, Amphibians, Ranavirus
- Copyright
- © 2018 Campbell et al.
- Licence
- This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ Preprints) and either DOI or URL of the article must be cited.
- Cite this article
- 2018. An emerging viral pathogen truncates population age structure in a European amphibian and may reduce population viability. PeerJ Preprints 6:e27056v1 https://doi.org/10.7287/peerj.preprints.27056v1
Abstract
Infectious diseases can alter the demography of their host populations, reducing their viability even in the absence of mass mortality. Amphibians are the most threatened group of vertebrates globally, and emerging infectious diseases play a large role in their continued population declines. Viruses belonging to the genus Ranavirus are responsible for one of the deadliest and most widespread of these diseases. To date, no work has used individual level data to investigate how ranaviruses affect population demographic structure. We used skeletochronology and morphology to evaluate the impact of ranaviruses on the age structure of populations of the European common frog (Rana temporaria) in the United Kingdom. We compared ecologically similar populations that differed only in their historical presence or absence of ranavirosis (the acute syndrome caused by ranavirus infection). Our results suggest that ranavirosis may truncate the age structure of R. temporaria populations. One potential explanation for such a shift might be increased adult mortality and subsequent shifts in the life history of younger age classes that increase reproductive output earlier in life. Additionally we constructed population projection models which indicated that such increased adult mortality could heighten the vulnerability of frog populations to stochastic environmental challenges.
Author Comment
This is a submission to PeerJ for review.
Supplemental Information
Supplementary Methods - Population Projection Modelling
A comprehensive overview of the rationale and methodologies behind our populations projection matrix modelling analyses.
The number of frogs sampled per each population
The number of R. temporaria sampled at each individual population.
Snout to vent length by age
The relationship between snout to vent length (SVL) and age in R. temporaria from ranavirosis-positive and disease-free populations. We found no significant effect of disease history on the SVL of frogs. Our data does however show clear evidence of continued growth throughout life regardless of disease history.
The age at which R. temporaria reached sexual maturity by sex and population disease history
The proportion of individuals that reached sexual maturity at each possible age within the summed male and female populations of each disease history. Age at sexual maturity was calculated via skeletochronology.
Projected populations under different combinations of starting population vectors and transition matrices
Projected population dynamics of R. temporaria populations modelled under different scenarios. Starting population vectors were created by weighted random sampling of 150 animals based on the proportions of each age class observed in populations of each disease history in our data. D-f = disease free and R-p = ranavirosis-positive. Our R-p matrix incorporated decreasing annual adult survival and our R-p starting population vector was age structure truncated.
Survival elasticities of our population matrices
Computed elasticities of each survival element of our population projection matrices. Elasticities of our matrix which incorporated increasing adult mortality and therefore represented a population subjected to ongoing ranavirosis are shown in red, whilst those of our matrix which represented a disease-free population are shown in blue. For reference the elasticities of an extended matrix created using the unadjusted viral rates published by Biek et al. 2002 are shown in white.
Fecundity elasticities of our population matrices
Computed elasticities of each fecundity element of our population projection matrices. Elasticities of our matrix which incorporated increasing adult mortality and therefore represented a population subjected to ongoing ranavirosis are shown in red, whilst those of our matrix which represented a disease-free population are shown in blue. For reference the elasticities of an extended matrix created using the unadjusted viral rates published by Biek et al. 2002 are shown in white.
Basal population matrix
Basal population matrix. Row one represents the fecundity of all life stages on the horizontal into the egg life stage, the number is equivalent to females produced per female. All other rows represent the proportional survival of each age class on the horizontal to the relevant age class on the vertical aspect of the matrix.
Population projections under varying decreases in per annual survival rates of adult R. temporaria
Population dynamics of theoretical disease-free populations and theoretical ranavirosis-positive populations modelled with an increasingly large annual percentage increase in adult mortality due disease. We found no significant difference between the population estimates through time based on varying this survival parameter alone (ANOVA; df = 6, F=0.889, p=0.505). In the absence of an empirically proven value for this parameter, we selected a value of 5% annual increase in mortality to represent the probabilistic increase of succumbing to ranavirosis with an increasing number of years returning to breed within the same infected population.
Matrix representing spawning failure in a ranavirosis-positive population
Population matrix representing complete spawning failure in ranavirosis-positive populations (5% reduced survival per year for adults). Row one represents the fecundity of all life stages on the horizontal into the egg life stage, the number is equivalent to females produced per female. All other rows represent the proportional survival of each age class on the horizontal to the relevant age class on the vertical aspect of the matrix.
Matrix representing spawning failure in a disease-free population
Population matrix representing complete spawning failure in disease-free populations. Row one represents the fecundity of all life stages on the horizontal into the egg life stage, the number is equivalent to females produced per female. All other rows represent the proportional survival of each age class on the horizontal to the relevant age class on the vertical aspect of the matrix.
Matrix representing mass mortality in ranavirosis-positive populations
Population matrix representing a year with a mass mortality event in ranavirosis-positive populations. Row one represents the fecundity of all life stages on the horizontal into the egg life stage, the number is equivalent to females produced per female. All other rows represent the proportional survival of each age class on the horizontal to the relevant age class on the vertical aspect of the matrix.
Matrix representing a mass mortality and spawning failure in a ranavirosis-positive population
Population matrix representing a year with a mass mortality event and total reproductive failure in ranavirosis-positive populations. Row one represents the fecundity of all life stages on the horizontal into the egg life stage, the number is equivalent to females produced per female. All other rows represent the proportional survival of each age class on the horizontal to the relevant age class on the vertical aspect of the matrix.