Positive or negative? The shell alters the relationship among behavioral defense strategy, energy metabolic levels and antioxidant capacity in freshwater turtles

Zhang, Wenyi; Niu, Cuijuan; Liu, Yukun; Storey, Kenneth B.

doi:10.1186/s12983-019-0301-5

Cited by 7 publications

(9 citation statements)

References 60 publications

(57 reference statements)

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“…This result is similar to the adverse effects observed on a lizard (Eremias multiocellata; Han et al, 2020). However, heat waves did not induce significant oxidative damage in the Chinese soft-shell turtle (Pelodiscus sinensis; Zhang et al, 2019), or the yellow pond turtle (Mauremys mutica; Li et al, 2021). This discrepancy may be due to the population origin of the studied individuals.…”

Section: Higher Oxidative Damage By Heat Waves In Low-latitude Turtlesmentioning

confidence: 81%

“…This discrepancy may be due to the population origin of the studied individuals. Previous studies on P. sinensis (Hebei, 39°58′N) and M. mutica (Zhejiang, 30°46′N) have been conducted on turtles from high latitudes (Zhang et al, 2019;Li et al, 2021). As it may be that high-latitude reptiles live at temperatures lower than their physiological optimum (Hao et al, 2020;Liu et al, 2022), higher environmental temperatures would be beneficial for their functions (Huey et al, 2009), and heat waves may not lead to significant oxidative damage.…”

Section: Higher Oxidative Damage By Heat Waves In Low-latitude Turtlesmentioning

confidence: 99%

“…The Chinese three-keeled pond turtle (Mauremys reevesii) is an endangered and unique species that is widespread in mainland China (IUCN, 2022). The species biology has been widely investigated, including life-history cycle, sex determination, and thermal biological traits (Du et al, 2009;Ye et al, 2009;Zhang et al, 2019;Wu et al, 2022), making it an appropriate system to study physiological resistance to heat waves.…”

Section: Introductionmentioning

confidence: 99%

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Heat wave induces oxidative damage in the Chinese pond turtle (Mauremys reevesii) from low latitudes

Tao

Ou²,

Wu³

et al. 2022

Front. Ecol. Evol.

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IntroductionGlobal warming has led to frequent heat waves, causing global organisms to face severe survival challenges. However, the way in which heat waves threaten the fitness and survival of animals remains largely unclear. Oxidative damage and immunity are widely considered the link between heat waves and threats to animals.MethodsTo evaluate the oxidative damage caused by heat waves and to reveal the physiological resistance to heat waves by the antioxidant defense of animals from different latitudes, we exposed both high-latitude (Zhejiang) and low-latitude (Hainan) populations of Chinese pond turtle (Mauremys reevesii) to simulate heat waves and a moderate thermal environment for 1 week, respectively. Next, we compared the oxidative damage by malondialdehyde (MDA) and antioxidant capacity by superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), and total antioxidant capacity (T-AOC) in the liver tissues and evaluated the innate immunity by serum complement protein levels (C3, C4) and lysozyme activity in plasma of turtles.Results and discussionWe found that heat waves significantly increased the content of MDA and the activity of CAT, whereas it decreased the activity of SOD, T-AOC, and GSH/GSSG in turtles from low latitudes. Furthermore, heat waves increased CAT activity but decreased GSH/GSSG in turtles from high latitudes. Although the turtles from high latitudes had higher levels of innate immunity, the heat waves did not affect the innate immunity of C3, C4, or lysozyme in either population. These results indicate that the low-latitude population suffered higher oxidative damage with lower antioxidant capacities. Therefore, we predict that Chinese pond turtles from low latitudes may be more vulnerable to heat waves caused by climate warming. This study reveals the physiological and biochemical resistance to heat waves in Chinese pond turtles from different latitudes and highlights the importance of integrative determination of fitness-related responses in evaluating the vulnerability of ectotherms from different latitudes to climate warming.

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Section: Higher Oxidative Damage By Heat Waves In Low-latitude Turtlesmentioning

confidence: 81%

Section: Higher Oxidative Damage By Heat Waves In Low-latitude Turtlesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Heat wave induces oxidative damage in the Chinese pond turtle (Mauremys reevesii) from low latitudes

Tao

Ou²,

Wu³

et al. 2022

Front. Ecol. Evol.

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“…In the telomere dynamics, the invasive turtle T. scripta elegans showed a better capacity to maintain the expression of TERT under thermal stress than the two co‐occurring native turtles. Thermal stress did not result in telomere erosion in three turtle species and this may be partly due to the maintenance mechanism of TERT or a strong antioxidant capacity in these turtles (Willmore & Storey, 1997; Zhang et al, 2019). This may also suggest that telomere structure is more vulnerable to chronic environmental stress but not the acute stresses (Benowitz‐Fredericks et al, 2022; Houben et al, 2008).…”

Section: Discussionmentioning

confidence: 97%

Greater physiological resistance to heat may favour an invasive freshwater turtle, enabling it to outcompete native species in a changing climate

Zhang

Hua

et al. 2023

Freshwater Biology

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Climate warming and biological invasion can interact to affect ecosystems, and the results of such interactions depend on whether invaders show physiological advantages in their responses to warming environments as compared with native species after the establishment and local adaptation. However, it has rarely been evaluated. The present study compared the heat tolerance of a globally invasive turtle, the red‐eared slider Trachemys scripta elegans, and two co‐occurring native turtle species in China, the Chinese soft‐shelled turtle Pelodiscus sinensis and Chinese pond turtle Mauremys reevesii, after acclimation in the same thermal environment. The expression patterns of heat shock factor 1 (HSF1), multiple heat shock proteins (HSPs) and telomere reverse transcriptase (TERT), and changes in relative telomere length (RTL) were then evaluated in liver and muscle of turtles under thermal stress. The results showed that T. scripta elegans had greater physiological resistance to heat than the co‐occurring native turtle species, and that this higher tolerance was accompanied by a higher temperature induction of the peak expression of inducible HSPs in liver and a higher onset temperature for the main inducible HSPs in muscle. During thermal stress, T. scripta elegans showed a better ability to maintain the expression levels of TERT under extremely hot conditions, whereas high temperatures inhibited TERT in muscles of native turtle species. Meanwhile, thermal stress did not cause telomere erosion in any of the three turtle species and some treatments can lead to slightly longer telomeres in T. scripta elegans or M. reevesii. Overall, the invasive turtle species showed higher heat tolerance and physiological advantages in enduring hot weather in comparison to the co‐occurring native turtle species. This may favour these invaders in situations of climate warming. Our study highlights the role of physiological adaptations displayed by invaders in achieving advantages over native species under climate change.

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“…In terms of diet, tortoises are restricted mostly to the herbivorous end of the spectrum, while turtles span across from strictly herbivores to strictly carnivores, expanding their nutritional options (Rodrigues and Diniz-Filho, 2016) . Moreover, added energy investment into heavier shell morphology of tortoises is negatively associated with energy metabolism as well as its activity levels (Zhang et al, 2019) .…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial Genome Reveals Contrasting Pattern of Adaptive Selection in Turtles and Tortoises

Sahoo

Kumar

Rai

et al. 2021

Preprint

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Testudinoidea represents an evolutionarily unique taxon comprising both turtles and tortoises. The contrasting habitats that turtles and tortoises inhabit are associated with unique physio-ecological challenges hence enable distinct adaptive evolutionary strategies. To comparatively understand the pattern and strength of Darwinian selection and physicochemical evolution in turtle and tortoise mitogenomes, we employed adaptive divergence and selection analyses. We evaluated changes in structural and biochemical properties, and codon models on the mitochondrial protein-coding genes (PCGs) among three turtles and a tortoise lineage. We used mitochondrial PCGs that constitute the crucial oxidative phosphorylation (OXPHOS) respiratory system, a critical metabolic regulator which assumes key significance in energy regulation of ectotherms. We detected strong evidence of positive selection along the turtle lineages: Geoemydidae, Emydidae, and Platysternidae, but relatively weak signals in tortoises. The Platysternidae turtles revealed the highest gene and site-wise positive selection. In turtles, positively selected sites were prevalent in NAD2 and NAD4 genes in OXPHOS Complex I, and COB gene of Complex III, indicating convergent adaptive evolution. Besides, NAD3 was the only subunit that showed adaptive selection in both turtles and tortoises, expressing its relevance for all Testudinoidea. Structural and functional analysis revealed many sites and physiochemical changes in important conserved as well as biomedically significant regions, suggesting the influence of adaptive pressure on mitogenome functions. Hence, our study furnished novel evidence of contrasting evolutionary selective pressure acting on closely related groups such as turtles and tortoises with unique habitat preferences and associated eco-physiological challenges.

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Positive or negative? The shell alters the relationship among behavioral defense strategy, energy metabolic levels and antioxidant capacity in freshwater turtles

Cited by 7 publications

References 60 publications

Heat wave induces oxidative damage in the Chinese pond turtle (Mauremys reevesii) from low latitudes

Heat wave induces oxidative damage in the Chinese pond turtle (Mauremys reevesii) from low latitudes

Greater physiological resistance to heat may favour an invasive freshwater turtle, enabling it to outcompete native species in a changing climate

Mitochondrial Genome Reveals Contrasting Pattern of Adaptive Selection in Turtles and Tortoises

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