Anuran larval developmental plasticity and survival in response to variable salinity of ecologically relevant timing and magnitude

Abstract

Salinity in affected freshwater ecosystems fluctuates with seasonal rainfall, tidal flux, rates of evaporation, chemical runoff and the influence of secondary salinization. Environmental stressors such as salinity can have lasting effects on anuran development, yet little is known about the effects of fluctuating salinity on tadpole ontogeny or the effects of differing magnitudes of salinity exposure, as would occur in natural wetland systems. We examined how salinity fluctuations affected survival, growth and development of Litoria ewingii by exposing tadpoles to a range of salinity concentrations (5.6-10.85 ppt) at three different stages of development (hind limb-bud formation; toe differentiation and forearm development). We also investigated the plasticity of tadpole growth rates in response to non-lethal, transient salinity influxes, specifically examining the capacity for compensatory growth and its relationship to the timing, magnitude or frequency of salinity exposure. Our results show that later-stage tadpoles are more tolerant to elevated salinity than those exposed at a younger age, and that exposure to high salinity later in life suppresses the potential for compensatory growth. Tadpoles exposed to transient low salinity lost less mass during metamorphosis than animals in constant salinity treatments, indicating a possible alternate to compensatory growth. Exposure to near-lethal salinities early in development did not alter tadpole responses to subsequent salinity stress. Our results provide some of the first evidence that both the timing and magnitude of transient environmental stressors can have an effect on anuran development and developmental trade-offs in a stressful environment.

Occurrence of Amphibians in Saline Habitats: A Review and Evolutionary Perspective

“…Although these selection pressures may be common in some environments, amphibians in many other environments may experience much-more unpredictable, dramatic salinity selection events. Indeed, it has been argued that dramatically fluctuating salinity levels are the norm, rather than the exception, in most environments (Wu et al 2012;Kearney et al 2014).…”

“…Road deicing events also result in extreme, transient spikes of salinity in roadside aquatic habitats, not unlike a coastal storm event Wade 1992, 1996), and habitat degradation and the changing of agricultural practices are also leading to extreme and unpredictable fluctuations of salinity in many inland habitats (Kearney et al 2014). Unpredictable episodes of selection therefore probably play some of the most important roles in amphibian adaption to salt in both inland and coastal natural and anthropogenically altered environments.…”

“…Our understanding of how amphibians adapt to these fluctuating environments is still, however, mostly unexplored. Kearney et al (2014) provide a much-needed first look at this subject, and their results suggest that animals experiencing transient salinity react very differently than do those experiencing constant salinity. Much more work is needed on this subject, as understanding the frequency, predictability, and nature of selection events clearly is key to our understanding of adaptation in these environments (Parsons 2005;Bell 2013).…”

“…Acclimation may increase tolerance in these and other species (e.g., Licht et al 1975;Wu et al 2014) through physiological means such as increased Na + /K + -ATPase expression, allowing larvae to more-efficiently maintain osmotic homeostasis (Bernabò et al 2013;Wu et al 2014). The effects of acclimation do not appear to be universal, however, and in some cases may have either no effect (Kearney et al 2014) or even inhibit adaptation (e.g., Hua and Pierce 2013). Acclimation to gradually increasing salinities may be a realistic ecological scenario in some habitats, such as saline desert ponds, where evaporation leads to increasing salinity over time (Gomez-Mestre and Tejedo 2003), but may be less ecologically realistic in other habitats where salinity may be governed more by dramatic unpredictable events such as storms and road deicing salt application (see above; Hopkins et al 2014).…”

Full compensation of growth in salt‐tolerant tadpoles after release from salinity stress

“…Compensatory growth of animals has mostly been studied in response to biotic stressors, such as food deprivation, density and predation risk (Metcalfe & Monaghan, ; Räsänen, Laurila & Merilä, ; Ali et al ., ; Vonesh & Bolker, ; Capellan & Nicieza, ; Jasienski, ; Hector et al ., ). Except for temperature (Mortensen & Damsgård, ; Nicieza & Metcalfe, ; Maclean & Metcalfe, ; Metcalfe & Monaghan, ; Ali et al ., ), few studies have addressed compensatory growth in response to abiotic stressors, and this is especially true for salinity (Squires et al ., ; Wu, Gomez‐Mestre & Kam, ; Kearney et al ., ). However, this is an ecologically and evolutionarily relevant question for animals inhabiting brackish water because the salinity of such habitats may fluctuate frequently and widely either from natural events, such as tidal flux and rainfall (Wu et al ., ), or anthropogenic sources, such as road deicing salt runoff (Karraker, ).…”