Thermal biology of the spotted snow skink, Niveoscincus ocellatus, in a warming world

Yuni, LPEK 2016 , 'Thermal biology of the spotted snow skink, Niveoscincus ocellatus, in a warming world', PhD thesis, University of Tasmania.

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Abstract

Thermal environment vary geographically and over time and they can have direct and indirect effects on natural populations, especially in ectotherms. Ectotherms rely on their thermal environment for thermoregulation, and the body temperatures they are able to maintain affect their physiological processes such as locomotor performance, developmental and growth rates, and energy expenditure. This thesis focusses on the thermal flexibility of a widely distributed ectothermic species, the spotted snow skink (Niveoscincus ocellatus) along an altitudinal gradient and across seasons to understand population-specific responses to different environmental conditions which may be important in allowing the species to occupy divergent thermal habitats. Further, I use this as a base to predict some of the potential effects of future climate change on this species (and ectotherms more generally).
I began by investigating the thermal biology (field active body temperature and thermal preference in the laboratory) across seasons in three populations of the spotted snow skink, Niveoscincus ocellatus, living along an altitudinal gradient in Tasmania. I demonstrated that the field active body temperature of N. ocellatus is dependent on its thermal environment but that the thermoregulation strategy might vary among populations of this species to respond to the variation in thermal environments at their localities. After establishing their thermal preferences in the laboratory that did not vary with site or season, I showed that N. ocellatus met their thermal preference along the altitudinal gradient and in all seasons, with an exception for the high altitude population in autumn. Their ability to meet their preferred body temperatures despite geographic and seasonal variation in thermal opportunities is important in allowing them to inhabit a wide range distribution area.
Since the field active body temperature in N. ocellatus depended on their thermal environments, I then focussed on other key physiological traits, namely on locomotor performance, energy expenditure, and date of birth that might be affected by the variation in the field active body temperatures in this species. I focused on the altitudinal and seasonal variation in the relationship between locomotor performance (sprint speed and endurance) and temperature in this species with particular focus on thermal optimum (T$$_{opt}$$) and performance breadth (B$$_{80}$$). Geographic variation was found in locomotor performance of N. ocellatus. The high altitude population had lower thermal optimum (T$$_{opt}$$) and a wider performance breadth (B$$_{80}$$) due to a lower limit of B$$_{80}$$ than populations at the lower altitudes. The higher limit of B$$_{80}$$, however, remained consistent among populations. These shifts toward lower T$$_{opt}$$ and lower limit of B$$_{80}$$ reflect the conditions they experience at the high altitude compared to the lower altitude sites. This reflects divergence in temperatures at which they are likely to be active at the lower sites when they emerge and prior to reaching their optimal temperatures. In contrast, higher temperatures can easily be avoided through thermoregulation and thus selection acts less strongly on this trait. There was also evidence of a seasonal shift in the relationship between temperature and locomotor performance which suggests a capacity for plastic responses in these traits – however this was only evident for B$$_{80}$$ of endurance. However, the strong site effect and the absence of widespread seasonal signals suggest local adaptation to local climatic conditions.
The third approach of this study was to examine the energy expenditure of the spotted snow skink (Niveoscincus ocellatus) living at two extremes of their distribution range (warm lowland versus cold alpine site) using the doubly labelled water method. Niveoscincus ocellatus expended more energy per gram per hour at the cold alpine site compared to their counterparts living at the warm lowland site. Lizards living at high altitude were active at lower temperatures compared with those at the low altitude site, which resulted in a longer activity time for the highland population. However, the differences in energy expenditure cannot be explained only by these differences in activity time. Lizards at the cold alpine site might compensate for the low temperatures by elevating their metabolism which subsequently increased their energy expenditure. An elevated metabolic rate combined with modified thermoregulatory behaviour is likely an important mechanism allowing N. ocellatus to cope with the cold environments at high altitude sites.
The final theme of my thesis focused on the relationship between date of birth and environmental temperature experienced by female N. ocellatus during the gestation period at the climatic extremes of the species distribution (warm lowland versus cold alpine populations) by using a long-term data set (14 years). In N. ocellatus, date of birth was strongly related to mean maximum air temperature during the gestation period in both populations. Geographic and annual variation in date of birth were observed in this species with earlier births between sites and among years within sites corresponding to warmer conditions experienced during gestation. Contrary to my predictions that there would be site-specific differences in the relationship between annual temperature variation and date of birth within populations, I found that the relationship was similar with each 1 °C shifting birth dates by between five and six days at each of the sites. This shift in birth date is despite the fact that the inter-annual variation in gestation temperature within site could be buffered via thermoregulatory behaviour. However, there was a similarity in the length of gestation between sites suggesting a combination of effective thermoregulation at the cold site, potentially combined with an adjustment of their physiological optima (for developmental rates) by the lizards at the cold alpine site. The implications of these results on temperature dependent phenological shifts are discussed in relation to potential impacts of future climate change.
Overall, this thesis demonstrated the influence of temperature on the physiological characteristics of the spotted snow skink, Niveoscincus ocellatus, across sites and seasons. Populations of N. ocellatus responded differently to the variation in their environment which appears to be determined by the level of temporal and spatial temperature variation they typically encounter. The combination of thermoregulatory behaviour and physiological adjustments, especially a downward shift in field active body temperature and physiological optima for locomotor performance, wider tolerance toward low temperatures, and elevated metabolic rate, acted as important potential buffer to allow N. ocellatus to overcome the challenges of the cold alpine areas in which their ranges extend. This study also indicates that N. ocellatus will potentially benefit from, at least modest, future predicted climate change. Firstly, the risks of fatalities of the extreme hot events can be avoided by a well-developed capacity for behavioural thermoregulation by this species. Secondly, warming will also allow for greater activity time (at or near their optimal temperatures for key physiological traits such as performance) which could facilitate range expansion into cold areas currently unsuitable for the species. Finally, the thermally-phenological shift in birth dates may initially enhance offspring fitness and even lead to greater demographic vigour. Thus, I concur with recent work that suggests that the effects of climate change on temperature dependent species is not necessarily all bad news and is different to the dire predictions made for other reptiles in tropical and desert areas.

Item Type: Thesis - PhD Yuni, LPEK Thermal flexibility, temperature, lizards, Niveoscincus, locomotor performance, energy expenditure, date of birth, thermoregulation Copyright 2016 the author Chapter 2 appears to be the equivalent of a pre-print version of an article published as: Yuni, L. P. E. K., Jones, S. M., Wapstra, E., 2019. Thermal biology of the spotted snow skink, Niveoscincus ocellatus, along an altitudinal gradient, Australian journal of zoology, 66(4), 235-246Chapter 4 appears to be the equivalent of a pre-print version of an article published as: Yuni, L. P. E. K., Jones, S. M., Wapstra, E., 2016. Energy expenditure of the spotted snow skink, Niveoscincus ocellatus, at two climatic extremes of its distribution range, Journal of thermal biology, 52, 205-216 View statistics for this item