Snake scales record environmental metal(loid) contamination.

Wetland snakes, as top predators, are becoming globally recognised as bioindicators of wetland contamination. Livers are the traditional test organ for contaminant exposure in organisms, but research is moving towards a preference for non-lethal tissue sampling. Snake scales can be used as an indicator of exposure, as many metals bind to the keratin. We used laser ablation with inductively coupled plasma-atomic emission spectroscopy and mass spectrometry (LA-ICP-MS) to quantify the concentrations of 19 metals and metalloids (collectively referred to 'metals' hereafter) in Western tiger snake (Notechis scutatus occidentalis) scales from four wetlands along an urban gradient, and compared them to concentrations measured in captive tiger snake scales. We conducted repeat measures to determine the concentration accuracy of each metal using LA-ICP-MS. Concentrations in wild Western tiger snake scales were significantly higher than in reference tiger snake scales for most metals analysed, suggesting accumulation from environmental exposure. We compared the scale concentrations to sediment concentrations of sampled wetlands, and found inter-site differences between mean concentrations of metals in scales parallel patterns recorded from sediment. Four metals (Mn, As, Se, Sb) had strong positive correlations with liver tissue contents suggesting scale concentrations can be used to infer internal concentrations. By screening for a larger suite of metals than we could using traditional digestive methods, we identified additional metals (Ti, V, Sr, Cs, Tl, Th, U) that may be accumulating to levels of concern in tiger snakes in Perth, Western Australia. This research has progressed the use of LA-ICP-MS for quantifying a suite of metals available in snake scales, and highlights the significance of using wetland snake scales as a non-lethal indicator of environmental contamination.

The Broad-Scale Analysis of Metals, Trace Elements, Organochlorine Pesticides and Polycyclic Aromatic Hydrocarbons in Wetlands Along an Urban Gradient, and the Use of a High Trophic Snake as a Bioindicator.

Wetlands and their biodiversity are constantly threatened by contaminant pollution from urbanisation. Despite evidence suggesting that snakes are good bioindicators of environmental health, the bioaccumulation of contaminants in reptiles is poorly researched in Australia. We conducted the first broad-scale analysis of 17 metals and trace elements, 21 organochlorine pesticides, and 14 polycyclic aromatic hydrocarbons in the sediments (4 samples per site, December 2018) from four wetlands along an urban gradient in Perth, Western Australia, and from the livers (5 livers per site, February-April 2019) of western tiger snakes Notechis scutatus occidentalis captured at those sites. All 17 metals and trace elements were detected in the sediments of wetlands as well as 16 in the livers of tiger snakes. Arsenic, Cu, Hg, Pb, Se, and Zn were at concentrations exceeding government trigger values in at least one sediment sample. Two organochlorine pesticides and six of seven polycyclic aromatic hydrocarbons were detected in the sediments of a single wetland, all exceeding government trigger values, but were not detected in tiger snakes. Metals and trace elements were generally in higher concentration in sediments and snake livers from more heavily urbanised wetlands. The least urbanised site had some higher concentrations of metals and trace elements, possibly due to agriculture contaminated groundwater. Concentrations of nine metals and trace elements in snake livers were statistically different between sites. Arsenic, Cd, Co, Hg, Mo, Sb, and Se near paralleled the pattern of contamination measured in the wetland sediments; this supports the use of high trophic wetland snakes, such as tiger snakes, as bioindicators of wetland contamination. Contamination sources and impacts on these wetland ecosystems and tiger snakes are discussed herein.

Island colonisation and the evolutionary rates of body size in insular neonate snakes.

Island colonisation by animal populations is often associated with dramatic shifts in body size. However, little is known about the rates at which these evolutionary shifts occur, under what precise selective pressures and the putative role played by adaptive plasticity on driving such changes. Isolation time played a significant role in the evolution of body size in island Tiger snake populations, where adaptive phenotypic plasticity followed by genetic assimilation fine-tuned neonate body and head size (hence swallowing performance) to prey size. Here I show that in long isolated islands (>6000 years old) and mainland populations, neonate body mass and snout-vent length are tightly correlated with the average prey body mass available at each site. Regression line equations were used to calculate body size values to match prey size in four recently isolated populations of Tiger snakes. Rates of evolution in body mass and snout-vent length, calculated for seven island snake populations, were significantly correlated with isolation time. Finally, rates of evolution in body mass per generation were significantly correlated with levels of plasticity in head growth rates. This study shows that body size evolution occurs at a faster pace in recently isolated populations and suggests that the level of adaptive plasticity for swallowing abilities may correlate with rates of body mass evolution. I hypothesise that, in the early stages of colonisation, adaptive plasticity and directional selection may combine and generate accelerated evolution towards an 'optimal' phenotype.

Fitness costs may explain the post-colonisation erosion of phenotypic plasticity.

Many organisms can adjust their phenotypes to match local environmental conditions via shifts in developmental trajectories, rather than relying on changes in gene frequencies wrought by natural selection. Adaptive developmental plasticity confers obvious benefits in terms of rapid response and higher mean fitness, so why is it not more common? Plausibly, adaptive plasticity also confers a cost; reshaping the phenotype takes time and energy, so that canalised control of trait values enhances fitness if the optimal phenotype remains the same from one generation to the next. Although this idea is central to interpreting the fitness consequences of adaptive plasticity, empirical data on costs of plasticity are scarce. In Australian tiger snakes, larger relative head size enhances maximal ingestible prey size on islands containing large prey. The trait arises via adaptive plasticity in snake populations on newly colonised islands but becomes genetically canalised on islands where snakes have been present for much longer periods. We experimentally manipulated relative head size in captive neonatal snakes to quantify the costs of adaptive plasticity. Although small-headed snakes were able to increase their head sizes when offered large prey, the delay in doing so, and their inability to consume large prey at the outset, significantly reduced their growth rates relative to conspecifics with larger heads at the beginning of the experiment. This study describes a proximate cause to the post-colonisation erosion of developmental plasticity recorded in tiger snake populations.

Thermal plasticity in young snakes: how will climate change affect the thermoregulatory tactics of ectotherms?

Climate change will result in some areas becoming warmer and others cooler, and will amplify the magnitude of year-to-year thermal variation in many areas. How will such changes affect animals that rely on ambient thermal heterogeneity to behaviourally regulate their body temperatures? To explore this question, we raised 43 captive-born tiger snakes Notechis scutatus in enclosures that provided cold (19-22 degrees C), intermediate (19-26 degrees C) or hot (19-37 degrees C) thermal gradients. The snakes adjusted their diel timing of thermoregulatory behaviour so effectively that when tested 14 months later, body temperatures (mean and maximum), locomotor speeds and anti-predator behaviours did not differ among treatment groups. Thus, the young snakes modified their behaviour to compensate for restricted thermal opportunities. Then, we suddenly shifted ambient conditions to mimic year-to-year variation. In contrast to the earlier plasticity, snakes failed to adjust to this change, e.g. snakes raised at cooler treatments but then shifted to hot conditions showed a higher mean body temperature for at least two months after the onset of the new thermal regime. Hence, thermal conditions experienced early in life influenced subsequent thermoregulatory tactics; the mean selected temperature of a snake depended more upon its prior raising conditions than upon its current thermoregulatory opportunities. Behavioural plasticity thus allows snakes to adjust to suboptimal thermal conditions but this plasticity is limited. The major thermoregulatory challenge from global climate change may not be the shift in mean values (to which our young snakes adjusted) but the increased year-to-year variation (with which our snakes proved less able to deal).