Energy balance and metabolic changes in an overwintering wolf spider, Schizocosa stridulans

Potts, Leslie J.; Košťál, Vladimı́r; Šimek, Petr; Teets, Nicholas M.

doi:10.1016/j.jinsphys.2020.104112

Cited by 12 publications

(5 citation statements)

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“…This approach enables global assessment of low molecular mass metabolites within cells and tissues and allows analysis of their biological significance as responses to environmental stressors [ 27 , 28 ]. Metabolomic analysis provides good prospects in the search for new biomarkers of winter hardiness, that can enhance our understanding of energy balance, metabolic changes, and biological functions of endogenous metabolites [ 29 – 31 ]. A metabolomics approach has been used previously to analyze metabolic changes that support overwintering in several species including thirteen-lined ground squirrels ( Ictidomys tridecemlineatus ) [ 32 – 34 ], Syrian hamsters ( Mesocricetus auratus ) [ 35 ], common cutworms ( Spodoptera litura ) [ 30 ], and wolf spiders ( Schizocosa stridulans ) [ 31 ] but, to date, has not been applied to overwintering by amphibians or reptiles.…”

Section: Introductionmentioning

confidence: 99%

“…Metabolomic analysis provides good prospects in the search for new biomarkers of winter hardiness, that can enhance our understanding of energy balance, metabolic changes, and biological functions of endogenous metabolites [ 29 – 31 ]. A metabolomics approach has been used previously to analyze metabolic changes that support overwintering in several species including thirteen-lined ground squirrels ( Ictidomys tridecemlineatus ) [ 32 – 34 ], Syrian hamsters ( Mesocricetus auratus ) [ 35 ], common cutworms ( Spodoptera litura ) [ 30 ], and wolf spiders ( Schizocosa stridulans ) [ 31 ] but, to date, has not been applied to overwintering by amphibians or reptiles. The present study provides the first metabolomics analysis of a frog species, the Xizang plateau frog, Nanorana parkeri (Anura, Dicroglossidae), that lives in one of the most extreme environments on Earth, the Qinghai-Tibet Plateau.…”

Section: Introductionmentioning

confidence: 99%

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Metabolic responses of plasma to extreme environments in overwintering Tibetan frogs Nanorana parkeri: a metabolome integrated analysis

Niu

Zhang

et al. 2021

Front Zool

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Many animals lower their metabolic rate in response to low temperatures and scarcity of food in the winter in phenomena called hibernation or overwintering. Living at high altitude on the Tibetan Plateau where winters are very cold, the frog Nanorana parkeri, survives in one of the most hostile environments on Earth but, to date, relatively little is known about the biochemical and physiological adjustments for overwintering by this species. The present study profiled changes in plasma metabolites of N. parkeri between winter and summer using UHPLC-QE-MS non-target metabolomics in order to explore metabolic adaptations that support winter survival. The analysis showed that, in total, 11 metabolites accumulated and 95 were reduced in overwintering frogs compared with summer-active animals. Metabolites that increased included some that may have antioxidant functions (canthaxanthin, galactinol), act as a metabolic inhibitor (mono-ethylhexylphthalate), or accumulate as a product of anaerobic metabolism (lactate). Most other metabolites in plasma showed reduced levels in winter and were generally involved in energy metabolism including 11 amino acids (proline, isoleucine, leucine, valine, phenylalanine, tyrosine, arginine, tryptophan, methionine, threonine and histidine) and 4 carbohydrates (glucose, citrate, succinate, and malate). Pathway analysis indicated that aminoacyl-tRNA biosynthesis, phenylalanine, tyrosine and tryptophan biosynthesis, and nitrogen metabolism were potentially the most prominently altered pathways in overwintering frogs. Changes to these pathways are likely due to fasting and global metabolic depression in overwintering frogs. Concentrations of glucose and urea, commonly used as cryoprotectants by amphibians that winter on land, were significantly reduced during underwater hibernation in N. parkeri. In conclusion, winter survival of the high-altitude frog, N. parkeri was accompanied by substantial changes in metabolomic profiles and this study provides valuable information towards understanding the special adaptive mechanisms of N. parkeri to winter stresses.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Metabolic responses of plasma to extreme environments in overwintering Tibetan frogs Nanorana parkeri: a metabolome integrated analysis

Niu

Zhang

et al. 2021

Front Zool

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“…As a result, energy drain is a significant risk associated with winter warming (Williams et al 2015). Indeed, some insects have lower survival and energy reserves during warmer winters (Williams et al 2015, Potts et al 2020, Devlin et al 2022, González-Tokman et al 2020). For D. suzukii, the impact of warm winters is complicated, because while days above 10 °C are necessary for foraging, as indicated by increased trap catches (Leach et al 2019a), in lab conditions, when the average temperature is above 5 °C, frequent warming periods are detrimental to survival (Stockton and Loeb 2021).…”

Section: Discussionmentioning

confidence: 99%

Survival and nutritional requirements for overwintering Drosophila suzukii (Diptera: Drosophilidae) in Kentucky

McCabe,

Unfried,

Teets

2023

Environmental Entomology

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The ability to cope with novel climates is a key determinant of an invasive species’ success. Drosophila suzukii (Matsumura, 1931) is an invasive fruit pest, and its seasonality varies across its range. Current evidence suggests that D. suzukii occurs year-round in warmer climates but has low overwintering survival in colder climates and relies on refuges or reinvades each spring. Here, we assessed the capacity of D. suzukii ability to overwinter in Kentucky, a temperate mid-latitude state with relatively mild but variable winters. We tracked year-round population changes for 3 yr and observed the highest populations in early winter months. Following an annual population crash in winter, small numbers of flies remained through the late winter and spring. We also conducted outdoor cage studies to determine the extent to which food resources and microhabitat impact survival and postwinter fecundity under natural conditions. Flies with no food had poor survival during the warmest periods of winter, and flies in all treatments had lower survival in the coldest month. Provisioning flies with either artificial diet or wild berries improved survival. As a follow-up, we determined whether D. suzukii could survive and reproduce after long-term exposure to a typical winter temperature on various wild berries. Drosophila suzukii had the highest survival on privet (Ligustrum sp.), but all berry types yielded higher survival than flies without food. Our results suggest that noncrop berries play an important role for overwintering D. suzukii, and as winters warm the availability of wild berries could influence early-season populations.

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“…Moreover, UHPLC-QE Orbitrap/MS analysis showed that freezing exposure induced a substantial change in the metabolomic profiles of the Xizang plateau frog, Nanorana parkeri [ 13 ]. Metabolomic analysis provides opportunities to assess regulatory mechanisms of energy metabolism and to discover new biomarkers in animals responding to environmental stress [ 14 – 16 ]. To date, studies using metabolomics to unravel the mechanisms of ectotherm adaptation to high-altitude environments remain scarce.…”

Section: Introductionmentioning

confidence: 99%

Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii

Zhang,

Men,

Jia

et al. 2023

Front Zool

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Extreme environmental conditions at high altitude, such as hypobaric hypoxia, low temperature, and strong UV radiation, pose a great challenge to the survival of animals. Although the mechanisms of adaptation to high-altitude environments have attracted much attention for native plateau species, the underlying metabolic regulation remains unclear. Here, we used a multi-platform metabolomic analysis to compare metabolic profiles of liver between high- and low-altitude populations of toad-headed lizards, Phrynocephalus vlangalii, from the Qinghai–Tibet Plateau. A total of 191 differential metabolites were identified, consisting of 108 up-regulated and 83 down-regulated metabolites in high-altitude lizards as compared with values for low-altitude lizards. Pathway analysis revealed that the significantly different metabolites were associated with carbohydrate metabolism, amino acid metabolism, purine metabolism, and glycerolipid metabolism. Most intermediary metabolites of glycolysis and the tricarboxylic acid cycle were not significantly altered between the two altitudes, but most free fatty acids as well as β-hydroxybutyric acid were significantly lower in the high-altitude population. This may suggest that high-altitude lizards rely more on carbohydrates as their main energy fuel rather than lipids. Higher levels of phospholipids occurred in the liver of high-altitude populations, suggesting that membrane lipids may undergo adaptive remodeling in response to low-temperature stress at high altitude. In summary, this study demonstrates that metabolic profiles differ substantially between high- and low-altitude lizard populations, and that these differential metabolites and metabolic pathways can provide new insights to reveal mechanisms of adaptation to extreme environments at high altitude.

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Energy balance and metabolic changes in an overwintering wolf spider, Schizocosa stridulans

Cited by 12 publications

References 51 publications

Metabolic responses of plasma to extreme environments in overwintering Tibetan frogs Nanorana parkeri: a metabolome integrated analysis

Metabolic responses of plasma to extreme environments in overwintering Tibetan frogs Nanorana parkeri: a metabolome integrated analysis

Survival and nutritional requirements for overwintering Drosophila suzukii (Diptera: Drosophilidae) in Kentucky

Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii

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