Title: Recruitment is key to understanding amphibian’s different population-level responses to chytrid fungus infection

Abstract

Understanding why related species have differing population-level responses to threats can be key to identifying conservation options for declining populations. However, this is difficult when multiple threats are implicated. Chytrid fungus (Batrachochytrium dendrobatidis: Bd) is implicated in at least 500 amphibian population declines globally, although few tangible options exist to mitigate pathogen impacts. Other threatening processes also invariably operate on most amphibians. Non-native fish, for example, can contribute to amphibian declines and may exacerbate Bd impacts. We disentangled the impacts of Bd and non-native fish upon two stream breeding frog species with differing conservation statuses to reveal vital rates that are crucial for species persistence. Litoria spenceri are threatened and historically occurred at elevations between 300–1100 m asl in southeastern Australia. Litoria lesueurii are non-threatened and sympatric with L. spenceri at some sites. Using mark-recapture derived demographic rates known to correlate with climate and elevation, discrete-time deterministic population models were constructed for each species at high, moderate and low elevation sites, and multiple management scenarios. Our study reveals that age to maturation, clutch size and egg-year 1 survival influenced interspecific and intraspecific population-level responses of the two frogs to Bd impacts. Importantly, our results highlight that an amphibian population’s capacity to counteract Bd-mediated adult mortality is clearly constrained by other threats and environment interactions that moderate species recruitment. Furthermore, understanding limits to recruitment may help identify Bd mitigation strategies. In our study, disease mitigation may be best achieved at some sites by enhancing recruitment through non-native fish management.

Introduction

Understanding why amphibians have differing population-level responses to chytrid (Batrachochytrium dendrobatidis: Bd) infection is a key priority to identify conservation strategies for species threatened by the pathogen (Collins, 2010; James et al., 2015). Bd is implicated in at least 500 amphibian population declines globally (Scheele et al., 2019) and causes a disease known as chytridiomycosis in susceptible individuals (Berger et al., 1998). The response of individuals and populations to Bd can vary both between and within species (Blaustein et al., 2005; Briggs et al., 2005; Tobler and Schmidt, 2010). Crucially Bd can cause rapid population declines and extinctions of some species at some sites (e.g. Gillespie et al., 2015; Lips et al., 2006) but other species can experience slower rates of population decline or may persist despite Bd presence (Phillott et al., 2013; Scheele et al., 2015).

Variation in disease outcomes at the population-level can be influenced by numerous individual-level intrinsic and extrinsic factors, especially involving site-specific interactions between the host, environment, and pathogen (James et al., 2015). Notably, microclimate and microhabitat conditions, immune defenses and pathogen virulence can all influence an individual’s risk of infection and ability to survive or recover from infection (Daskin et al., 2014; Doddington et al., 2013; Gahl et al., 2012; Gervasi et al., 2014; Heard et al., 2014; Tobler and Schmidt, 2010). The same site-specific microclimatic conditions (particularly temperature) can influence pathogen growth and survival (Piotrowski et al., 2004), and amphibian demographic rates including age to maturation, clutch size and longevity (Morrison et al., 2004). Populations may persist despite Bd infection as long as sufficient adult frogs survive and successfully reproduce (Briggs et al., 2005). Several studies have hypothesized that an amphibian population’s extinction risk may be determined by their ability to compensate for Bd-induced mortality through recruitment (Muths et al., 2011; Phillott et al., 2013; Scheele et al., 2015; Tobler et al., 2012). These factors, and others, can all lead to differing outcomes for species exposed to Bd.

Bd infected populations may be at greater risk of extinction if impacted by other threats (Phillott et al., 2013) and most amphibians are invariably influenced by multiple threats (Bielby et al., 2008; Heard et al., 2011). The combined impacts of multiple threats on species can be complex (Blaustein and Kiesecker, 2002) but must be clarified to identify species management requirements. The implications for species are most serious if threats combine to have additive or synergistic effects (Brook et al., 2008; Wake, 2012) although management requirements may differ if threats combine to have antagonistic (opposing) effects (e.g. Gahl et al., 2011).

Introduced fish (such as trout species) can severely affect amphibians and are implicated in species declines (Gillespie, 2001; Knapp, 2005; Matthews et al., 2001; Vredenburg, 2004). The impacts of introduced fish could be particularly severe for species that are also influenced by Bd, as the threats may simultaneously affect different amphibian life stages. Introduced predatory fish can reduce amphibian larval survival (Gillespie, 2001; Hunter et al., 2011), whereas the impacts of Bd upon survival may be most severe following metamorphosis (Berger et al., 1999). The threats could therefore be additive and accelerate a species decline. Alternatively, the threats may have antagonistic effects; Bd impacts may be reduced if disease dynamics are influenced by population density (e.g. Rachowicz and Briggs, 2007), and fish predation may limit a species’ population density (e.g. Vredenburg, 2004). An understanding of these effects and interactions is therefore crucial to developing sound conservation strategies for amphibians where multiple threats are operating and potentially interacting.

Here, we examine the population-level responses of a threatened and a non-threatened frog species to two threats, Bd and introduced trout. Bd can reduce the apparent annual survival of both the Critically Endangered spotted tree frog (Litoria spenceri) (Hero et al., 2004) and non-threatened Lesueur's frog (Litoria lesueurii) at an individual-level (West, 2015). Although, whilst introduced trout (Salmo trutta and Oncorhynchus mykiss) can significantly reduce the survival of L. spenceri tadpoles they appear to have little effect on the survival of L lesueurii tadpoles (Gillespie, 2001). We suspected that differences in the species population-level outcomes to these threats may be due to different impacts of trout or different consequences of Bd infection due to demographic variation between sites correlated with temperature and elevation. Using recent demographic parameter estimates we developed a multistate matrix model to examine conditions that influence each frog species’ population viability in different environmental settings, to evaluate management options for threat mitigation.