Host density and habitat structure influence host contact rates and Batrachochytrium salamandrivorans transmission

Abstract

Batrachochytrium salamandrivorans (Bsal) is an emerging invasive pathogen that is highly pathogenic to salamander species. Modeling infection dynamics in this system can facilitate proactive efforts to mitigate this pathogen's impact on north American species. Given its widespread distribution and high abundance, the eastern newt (Notophthalmus viridescens) has the potential to significantly influence Bsal epidemiology. We designed experiments to 1) estimate contact rates given different host densities and habitat structure and 2) estimate the probability of transmission from infected to susceptible individuals. Using parameter estimates from data generated during these experiments, we modeled infection and disease outcomes for a population of newts using a system of differential equations. We found that host contact rates were density-dependent, and that adding habitat structure reduced contacts. the probability of Bsal transmission given contact between newts was very high (>90%) even at early stages of infection. our simulations show rapid transmission of Bsal among individuals following pathogen introduction, with infection prevalence exceeding 90% within one month and >80% mortality of newts in three months. Estimates of basic reproductive rate (R 0) of Bsal for eastern newts were 1.9 and 3.2 for complex and simple habitats, respectively. Although reducing host density and increasing habitat complexity might decrease transmission, these management strategies may be ineffective at stopping Bsal invasion in eastern newt populations due to this species' hypersusceptibility. Across a variety of taxa, disease has been implicated as a major contributor to population-and species-level declines 1-6. Epidemiological modeling can facilitate disease response and management by elucidating host-pathogen interactions and identifying strategies that could reduce the severity of outbreaks in wild populations 7-9. Ideally, evaluating disease management strategies and modeling possible outcomes should occur prior to pathogen invasion, because the likelihood for disease control is greater and the cost of response is less 8,10-12. Conversely, reactive or delayed responses to disease outbreaks can result in significant biodiversity loss and economic impact, as demonstrated by the unexpected emergence of Batrachochytrium dendrobatids (Bd) 6,13,14 and Pseudogymnoascus destructans (the causative agent of White Nose syndrome) 13,15. The newly emergent fungal pathogen Batrachochytrium salamandrivorans (Bsal) provides a unique opportunity to evaluate possible management strategies, especially in areas where it has yet to emerge. Bsal is rapidly spreading in Europe, where it is believed to have been introduced from Asia via the pet trade 16,17. In areas where Bsal has emerged, populations of fire salamanders (Salamandra salamandra) have declined substantially 18. Preventing and mitigating Bsal outbreaks is described as one of the greatest current priorities for wildlife conservation 19. Bsal appears to have a high invasion probability ...

Putative resistance and tolerance mechanisms have little impact on disease progression for an emerging salamander pathogen

“…Moreover, N. meridionalis and N. perstriatus were also, on average, the least tolerant species, with a faster reduction in survival probability with increasing Bsal load compared to N. viridescens and T. granulosa . The lower resistance and tolerance of N. meridionalis and N. perstriatus to Bsal infection compared to T. granulosa and N. viridescens —two species that have previously been identified as significantly at risk from Bsal invasion (Malagon et al., 2020; Martel et al., 2014)—highlights that even among susceptible species there may be hyper‐sensitive species to prioritize for conservation. An important caveat, however, is that lower resistance and tolerance in N. meridionalis and N. perstriatus could be a consequence of these species coming from a captive assurance colony, where it is possible that genetic diversity was lower and microbiome less diverse than the wild populations of N. viridescens and T. granulosa —both which could affect susceptibility to Bsal infection.…”

“…We used the parameterized IPM to understand how perturbations in resistance and tolerance functions affected the mean survival time of an initially uninfected individual for different host species (Appendix S3). Because we did not have estimates for the relative contributions of direct and indirect transmission or the influence of host density on transmission (but see Malagon et al., 2020), we assumed that individuals persisted in an environment with a constant source of Bsal . This is not an unreasonable null assumption as the presence of a resistant Bsal spore stage that can transmit through the environment and the potential presence of other amphibian species that can maintain and shed infectious spores without succumbing to chytridiomycosis could largely decouple the force of infection from focal host density (Stegen et al., 2017).…”

Preparing for invasion: Assessing risk of infection by chytrid fungi in southeastern plethodontid salamanders

“…We expect a high likelihood of Bsal entering United States as the number of amphibians imported surpassed 26 million in 2006–2014 (Altmann & Kolby, 2017). In addition, recent studies showed that it only takes one second of contact to produce a successful infection in Eastern Newts (Malagon et al, 2020). In terms of biological invasions, our findings indicate that propagule pressure would be high if Bsal reaches a population of susceptible supershedder hosts like Eastern Newts (Longo et al, 2019; Malagon et al, 2020; McDonald et al, 2020), while plethodontid salamanders are more likely to provide some level of dilution if there is cross‐immunity between Bd and Bsal .…”

Host–multiparasite interactions in amphibians: a review

“…For example, eggs are the most sensitive to Saprolegnia [ 1 , 96 ], and tadpoles are less susceptible to Bd infection than metamorphosed individuals [ 110 ]. The behaviour of hosts can also influence bacterial disease outcomes: communal deposition of egg masses may enhance mortality due to Saprolegnia infection [ 114 ], and aggregation of hosts can facilitate parasite transmission in the case of amphibian chytrids [ 115 , 116 ]. How these factors affect the outcome of co-infections by multiple fungal agents has remained unknown and would require detailed investigations.…”