Climate change is a prevalent and continuous issue, driving a significant increase of 0.85°C in global average surface temperature[1], rising to 1.5°C in certain regions during particular seasons[2], resulting in observable changes to the environment globally, its ecosystems, habitats and the species which it holds. This is no exception for the Squamata order, classifying Reptiles and Lizards[3] - poikilothermic species that possess ectothermic temperature regulation. Ectotherms rely on absorption of external, environmental heat sources, generated by the sun, to maintain a constant body temperature, due to the inability of the organism to produce its own body heat in contrast to endotherms. Environmental temperatures also influence nesting and incubation of eggs for oviparous females. The question thus posed is: if such species are temperature-sensitive in various aspects of living, what possible changes may occur due to climate change? The answer may be reflected in species’ ability of phenotypic plasticity or changes behaviourally. However, in this article we will be focusing on temperature and climate change impacts on neurological development in young reptiles, specifically Bassiana duperreyi.
Figure 1: Photograph of Bassiana duperreyi, also known as the Eastern three lined skink[16] .
Bassiana duperreyi, also known as the Eastern three lined skink, is a reptile located in Australia (Fig. 1) [3]. A large number of the population is found within the MurrayDarling Basin (Fig. 2)[3]. This basin contains dry Mallee woodland and shrubland in the North, with areas of greater rainfall found in regions of woods in the South and East[4]. Mallee woodlands indicate the main form of foliage that grows within the region; the Eucalyptus plant[4]. Originating from swollen roots known as a lignotuber, it then grows upward and outward via several branches on the ground surface[4]. The understories consist of various species of sclerophyllous shrubs, such as Xanthorrhoea tussocks which are large grass-like trees[4]. It is in this habitat under rocks, logs or open areas that Bassiana duperreyi lay their eggs, via digging, in shared nests[5] .
Figure 2: Map of Australia highlighting the area of the Murray- Darling Basin[17] .
Figure 3: A scatter graph demonstrating the increase in mean air temperature over ten years, leading to a shift in nesting eggs. Early years’ groups 1,2, 3, 4, and 5 years and Later years’ groups 6, 7, 8, 9 and 10 years[18].
A warming trend was indicated, with nesting temperatures increasing by 1.5°C[6]. This has resulted in premature spring thermal progression, leading to alterations in nesting patterns and behaviours of female Bassiana duperreyi. (Fig. 3)[6] .
Figure 4: Scatter graphs representing (a) mean air temperature in a year, (b) nest temperature and (c) nest depth changes over a ten year period[19] .
Reptiles have been found to react to such ecological changes via three methods: adapt in situ, if temperatures remain within the optimal range[7] keep up with changes in the environment[8], or produce plastic responses[9], such as phenotypic plasticity. These methods that female Bassiana duperreyi may adopt significantly influence nesting sites and the eggs that they hold, which rely on the environment for thermoregulation during development as they are unable to move themselves[10] . Physiologically, increasing temperatures have resulted in oviposition in female individuals occurring earlier within the season, shifting months from November to December/January[6]. Behaviour has also altered, where nests are dug deeper into the soil to reach cooler temperatures (Fig. 4), producing a more constant internal nesting temperature for a week after the eggs are first deposited[6]. However, this effect is only temporary and throughout the course of the eggs developing, incubation temperatures continue to increase, demonstrating a mean change from 22°C to 30°C[6] leading to overall incubation time length halving[5] and eggs to hatch earlier.
Figure 5: Main areas of the reptilian brain. The region of the Medial Cortex is circled in red. Rostral (front) to Caudal (back) is from left to right of the diagram.[20]
Temperature fluctuations not only speed up the rate at which hatchlings are produced but alter how they develop within the egg before they hatch. Embryogenesis is affected by rising temperatures and thus has a considerable impact on a key process that occurs during this stage - brain development[11]. Nests with temperatures of 24°C (±5°C) deemed ‘hot’ compared to ‘cold’ nests with a temperature of 18°C (±5°C) produce individuals with varying brain networks and different neurone densities[11]. This has been established in two regions of the brain, the Telencephalon and the Medial Cortex (Figure 5)[11]. In ‘cold’ nests the Telencephalon grew larger compared to ‘hot’ nests. This was also reflected in the Medial Cortex including its subregions known as the Medial, Dorsal and Lateral Cortex[11]. Yet the Medial Cortex developing under ‘hot’ conditions contained a greater number and density of neurones[11]. These differences are particularly relevant in the overall brain function and abilities of hatchlings, as the Telencephalon is related to motor function and the Medial Cortex is key for learning and memory [11] . Thus, greater neurone density providing well-connected neural pathways could correlate to greater learning capacity within the Medial Cortex of reptiles incubated in ‘hot’ nests.
Figure 6: Graph showing different learning scores between hot- incubated hatchlings, 24°C (±5°C), and coldincubated hatchlings 18°C (±5°C)[21]
The discrepancy of neural function of hatchlings incubated in hot or cold nests is exhibited in various abilities. Avoiding predators is a phenotypic plastic characteristic that individuals incubated in hot nests demonstrate greater capabilities in[12]. In one study, Bassiana duperreyi hatchlings were placed in a hide in which they had to escape. Hot-incubated Bassiana duperreyi produced better learning results (Fig. 6), where errors were corrected more frequently compared to their cold-incubated counterparts[12] . This learning mechanism may allow individuals to develop an understanding of the advantages and disadvantages of different methods of evasion, increasing their response and alertness for predators and thus increasing the probability of survival.
Figure 7: Distribution graphs between hot (solid line) and cold (dashed line) incubated lizards, showing differences in learning rate, where positive numbers demonstrate learning and 0 shows no learning.[22]
In a different experiment, the ability to locate food displays the same trend between hot- and cold-incubated eggs, with learning success rates being higher in hot-incubated lizards, whilst also being able to learn faster when completing maze tasks[13]. Over 15 trials to locate food within a maze, the rate at which Bassiana duperreyi completed the challenge increased (Fig. 7), suggesting that the lizards were learning the correct path to acquire food[13]. Utilising this skill in the wild may allow the reptiles to establish several pathways leading to areas providing a range of food sources and therefore decreasing competition.
Figure 8: Bar graph showing the mean number of trials taken for hot hatchlings to successfully complete a task. [23]
Associative learning between colours and objects has been demonstrated via various instrumental learning tasks in young Bassiana duperreyi[14]. Four different challenges were created to test colour association, spatial discrimination and choice reversal[14] . Before these tasks were completed, the young lizards had to successfully complete two trial stages[14] . Interestingly, only the hot-incubated lizards passed this stage, whereas all the cold-incubated lizards failed[14] . The four challenges that proceeded after the trial runs were placed in a series, where some aspects of one task were repeated in another, yet also containing new elements of difficulty[14]. Although success rates fluctuated, the hot-incubated reptiles were able to complete some, if not all the tests (Fig. 8), demonstrating the ability to use information learnt from previous experience and apply it to novel challenges[14]. This skill of application may serve advantages in developing strategies for several situations such as identifying potential nesting grounds, competing for mates or defending and attacking in fights.
Such thermosensitivity possessed by Bassiana duperreyi during embryogenesis and consequently thermal developmental plasticity[15] that occurs has shown to have a substantial impact on the evolutionary fitness of the species as a whole[14] . Embryos developing in hotter nest temperatures, within the optimum range of 20°C to 35°C has increased chances of neurologically developing successfully[15] with a wider network of neural pathways resulting in advantageous learning potential. Thus, the lizards that are laid in hotter incubated nests may have a greater tolerance to environmental change, with beneficial traits such as identifying food faster, establishing pathways and avoiding predators. However, this gap between hotincubated and cold-incubated lizards may narrow as the reptiles mature, with cold-incubated individuals improving their skills via learning over time[12] .
Although ostensibly climate change within the ecological habitat of Bassiana duperreyi benefits the survival of this species, it must be noted that they have certain environmental tolerance limits. As mentioned earlier, female lizards when nesting have tried to defer the effect of increasing temperatures by digging deeper nests and shifting the period for oviposition. These tactics are effective but concerningly only temporary.[6] Even if Bassiana duperreyi are able to respond to such changes, the overall ecosystem in which they are placed and the intertwined food chains and food webs may not be able to remain constant, resulting in further environmental pressures, possibly generating directional or disruptive selection. This may favour individuals with advantageous phenotypes, thus potentially reducing the range of allele frequencies in the Bassiana duperreyi gene pool.
It is apparent that we must remain vigilant in observing the many effects of climate change; not only highlighting the physical environmental changes, but also understanding how they alter biological mechanisms, including reproductive and neurological systems, within species. The Bassiana duperreyi is only one of many examples.
KEY WORDS & DEFINITIONS
Basin- a geographical formation found in large areas across the world where the ground is lower compared to the rest of the surface, can be described as a dip in the Earth’s surface. Directional Natural Selection- the species’ phenotype favours one extreme rather than the mean phenotype or the opposite extreme phenotype. Disruptive Natural Selection- the species’ mean phenotype is not favoured compared to the two extremes of the phenotype. Ectothermic regulation- an organism relies on general environmental temperatures and heat generated by the sun to maintain a constant body temperature, due to the inability of the organism to control it itself. Embryogenesis- development of an embryo. In situ- in the original location. Lignotuber- woody swollen root of the Mallee eucalypts. Oviparous- offspring are produced in eggs that hatch outside of the mother’s body. Oviposition- when female reptiles deposit their eggs. Phenotypic Plasticity- when an organism can change physiologically, morphologically, behaviourally, or a mix of either, to counter change in environment or stimuli. Poikilothermic- an organism with a body temperature that alters with environmental temperature. Squamata- the Order for Bassiana duperreyi, part of the hierarchical classification of species.
REFERENCES
Article written and submitted by Zainab Khan, First year Neuroscience student, Queen Mary University of London.
Issue 5 Editorial Team
Editor Jake Weeks AMRSB, FLS, FISAP (Herp Edu), MIACE Researchers & Authors Asia Hoile Connor Tyler, AMRSB Connor Whelan Gary Weeks Shane Gausden Invited & Submitting Authors Dr. Sonya Miles BVSc CertAVP (ZM) MRCVS (UK) Chris Mortelmans (Be) Jonathan Rheins (US) Moritz von Zeddelmann (Ger) Zainab Khan (UK) For information contact by email magazine@reptileacademy.co.uk Always seek professional veterinary advice from a qualified exotics specialist with regards to the health of your animal. Copyright © 2021 The Reptile Academy Ltd. All rights reserved. KDP ISBN: 9798478300845 United Kingdom Company Number: 11421088 The Reptile Academy Ltd holds a Licence under the Animal Welfare Act (2006) The Animal Welfare (Licensing of Activities Involving Animals) (England) Regulations 2018 Animal Activities Licence Number: 80/19 Issued by Southampton City Council, UK
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