Physiological and biochemical responses to elevated temperature in a threatened freshwater crayfish, Euastacus sulcatus (Decapoda: Parastacidae)
James W. P. Bone A C , Gillian M. C. Renshaw B and Clyde H. Wild A
+ Author Affiliations
- Author Affiliations
A Environmental Futures Research Institute, Griffith School of Environment, Gold Coast Campus, Griffith University, Qld 4222, Australia.
B Hypoxia and Ischemia Research Unit, School of Allied Health Sciences, Gold Coast Campus, Griffith University, Qld 4222, Australia.
C Corresponding author. Email: j.bone@griffith.edu.au
Marine and Freshwater Research 68(10) 1845-1854 https://doi.org/10.1071/MF16232
Submitted: 28 June 2016 Accepted: 17 December 2016 Published: 8 March 2017
Abstract
Projected elevations in environmental temperature are expected to have a detrimental effect on organisms with distributions that are already restricted to high-altitude refugia, especially where dispersal is compromised due to population isolation by unsuitable intervening habitats. The present study was carried out on such an organism, namely Euastacus sulcatus, to determine: (1) the temperature at which thermal stress occurs under laboratory conditions; and (2) whether thermal stress is already occurring naturally in contemporary field-acclimatised individuals. The laboratory data provided evidence that biochemical and physiological stress occurred in E. sulcatus at 22.5°C or higher. In the field, oxidative stress was characterised by an increase in the oxidised redox state of glutathione within a low-altitude population accompanied by significantly elevated protein carbonyls and lipid peroxidation. The data confirmed that potential thermal stress was present in E. sulcatus residing at the lower end of its altitudinal distribution, indicating that this threatened species is already challenged within localised populations in their natural environment. Together, these results reveal that future increases in environmental temperature are not only likely to result in increased baseline levels of stress in E. sulcatus, but also forecast further restriction in the altitudinal distribution of the species in a warming climate.
References
Angilletta, M. J., Niewiarowski, P. H., and Navas, C. A. (2002). The evolution of thermal physiology in ectotherms. Journal of Thermal Biology 27, 249–268.| The evolution of thermal physiology in ectotherms.Crossref | GoogleScholarGoogle Scholar |
Baker, M. A., Cerniglia, G. J., and Zaman, A. (1990). Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Analytical Biochemistry 190, 360–365.
| Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmt1Ons70%3D&md5=7dca8f8965fab9f95b74e45fc5114392CAS |
Berlett, B. S., and Stadtman, E. R. (1997). Protein oxidation in aging, disease, and oxidative stress. The Journal of Biological Chemistry 272, 20313–20316.
| Protein oxidation in aging, disease, and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsFKhsbw%3D&md5=6c05c20fdd6fbfb4bb53a2cecd68063dCAS |
Bone, J. W. P., Wild, C. H., and Furse, J. M. (2014). Thermal limit of Euastacus sulcatus (Decapoda: Parastacidae), a freshwater crayfish from the highlands of central eastern Australia. Marine and Freshwater Research 65, 645–651.
| Thermal limit of Euastacus sulcatus (Decapoda: Parastacidae), a freshwater crayfish from the highlands of central eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Bone, J. W. P., Renshaw, G. M. C., Furse, J. M., and Wild, C. H. (2015). Using biochemical markers to assess the effects of imposed temperature stress on freshwater decapod crustaceans: Cherax quadricarinatus as a test case. Comparative Physiology – B. Biochemical, Systemic, and Environmental Physiology 185, 291–301.
| Using biochemical markers to assess the effects of imposed temperature stress on freshwater decapod crustaceans: Cherax quadricarinatus as a test case.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFOgurfL&md5=398a09610539b3ab55482d20cb91f88fCAS |
Dalle-Donne, I., Rossi, R., Giustarini, D., Milzani, A., and Colombo, R. (2003). Protein carbonyl groups as biomarkers of oxidative stress. Clinica Chimica Acta 329, 23–38.
| Protein carbonyl groups as biomarkers of oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVCktr8%3D&md5=43ff364b6f30871e809aa438b982e92eCAS |
Furse, J., and Coughran, J. (2010). Euastacus sulcatus. In ‘The IUCN Red List of Threatened Species’, ver 3.1. (International Union for Conservation of Nature and Natural Resources.) Available at http://dx.doi.org/10.2305/IUCN.UK.2010-3.RLTS.T153638A4524232.en [Verified 2 March 2017].
Furse, J. M., and Wild, C. H. (2004). Laboratory moult increment, frequency, and growth in Euastacus sulcatus, the Lamington Spiny Crayfish. Freshwater Crayfish 14, 205–211.
Furse, J. M., Dawkins, K. L., and Coughran, J. (2013). Two new species of Euastacus (Decapoda: Parastacidae) from the Gondwana Rainforests of Central Eastern Australia. Freshwater Crayfish 19, 103–112.
| Two new species of Euastacus (Decapoda: Parastacidae) from the Gondwana Rainforests of Central Eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Gutteridge, J. M. C., and Halliwell, B. (1990). The measurement and mechanism of lipid peroxidation in biological systems. Trends in Biochemical Sciences 15, 129–135.
| The measurement and mechanism of lipid peroxidation in biological systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXksFCgu7w%3D&md5=08d12349344080746b3ee1b5a586a61aCAS |
Hara, A., and Radin, N. S. (1978). Lipid extraction of tissues with a low-toxicity solvent. Analytical Biochemistry 90, 420–426.
| Lipid extraction of tissues with a low-toxicity solvent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXmtFWmsL0%3D&md5=a14c91b002708c1aea0607dbc04605c9CAS |
Heise, K., Puntarulo, S., Nikinmaa, M., Abele, D., and Poertner, H. O. (2006). Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout Zoarces viviparus L. The Journal of Experimental Biology 209, 353–363.
| Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout Zoarces viviparus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitFSgsLY%3D&md5=407dc6528f2d723916e05c863b312367CAS |
Horwitz, P. (1995). The conservation status of Australian freshwater crayfish: review and update. Freshwater Crayfish 10, 70–80.
Jones, C. M. (1990). General biology of Cherax quadricarinatus. Aquaculture Branch, Northern Territory Department of Primary Industries, Darwin, NT, Australia.
King, C. R. (1994). Growth and survival of redclaw crayfish hatchlings (Cherax quadricarinatus von Martens) in relation to temperature, with comments on the relative suitability of Cherax quadricarinatus and Cherax destructor for culture in Queensland. Aquaculture 122, 75–80.
| Growth and survival of redclaw crayfish hatchlings (Cherax quadricarinatus von Martens) in relation to temperature, with comments on the relative suitability of Cherax quadricarinatus and Cherax destructor for culture in Queensland.Crossref | GoogleScholarGoogle Scholar |
Le Moullac, G., and Haffner, P. (2000). Environmental factors affecting immune responses in Crustacea. Aquaculture 191, 121–131.
| Environmental factors affecting immune responses in Crustacea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtlOmtb0%3D&md5=59d50556a3238174e4e2cb4e39d52c6dCAS |
Levine, R. L., Williams, J. A., Stadtman, E. P., and Shacter, E. (1994). Carbonyl assays for determination of oxidatively modified proteins. In ‘Methods in Enzymology’. (Ed. P. Lester.) Vol. 233, pp. 346–357. (Academic Press: Waltham, MA, USA.)
Lowe, K., FitzGibbon, S., Seebacher, F., and Wilson, R. (2010). Physiological and behavioural responses to seasonal changes in environmental temperature in the Australian spiny crayfish Euastacus sulcatus. Comparative Physiology – B. Biochemical, Systemic, and Environmental Physiology 180, 653–660.
| Physiological and behavioural responses to seasonal changes in environmental temperature in the Australian spiny crayfish Euastacus sulcatus.Crossref | GoogleScholarGoogle Scholar |
Matozzo, V., Gallo, C., and Marin, M. G. (2011). Effects of temperature on cellular and biochemical parameters in the crab Carcinus aestuarii (Crustacea, Decapoda). Marine Environmental Research 71, 351–356.
| Effects of temperature on cellular and biochemical parameters in the crab Carcinus aestuarii (Crustacea, Decapoda).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFWhsL0%3D&md5=17224e216b8de1a7d862974591300987CAS |
Mihaljević, B., Katušin-Ražem, B., and Ražem, D. (1996). The reevaluation of the ferric thiocyanate assay for lipid hydroperoxides with special considerations of the mechanistic aspects of the response. Free Radical Biology & Medicine 21, 53–63.
| The reevaluation of the ferric thiocyanate assay for lipid hydroperoxides with special considerations of the mechanistic aspects of the response.Crossref | GoogleScholarGoogle Scholar |
Parihar, M. S., Dubey, A. K., Javeri, T., and Prakash, P. (1996). Changes in lipid peroxidation, superoxide dismutase activity, ascorbic acid and phospholipid content in liver of freshwater catfish Heteropneustes fossilis exposed to elevated temperature. Journal of Thermal Biology 21, 323–330.
| Changes in lipid peroxidation, superoxide dismutase activity, ascorbic acid and phospholipid content in liver of freshwater catfish Heteropneustes fossilis exposed to elevated temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXks12isw%3D%3D&md5=c7e7d6634c5dee01d5479407db1613d1CAS |
Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecology Evolution and Systematics 37, 637–669.
| Ecological and evolutionary responses to recent climate change.Crossref | GoogleScholarGoogle Scholar |
Pascual, C., Sánchez, A., Sánchez, A., Vargas-Albores, F., LeMoullac, G., and Rosas, C. (2003). Haemolymph metabolic variables and immune response in Litopenaeus setiferus adult males: the effect of an extreme temperature. Aquaculture 218, 637–650.
| Haemolymph metabolic variables and immune response in Litopenaeus setiferus adult males: the effect of an extreme temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1Ggsrs%3D&md5=76c63894849e8eb2f2b42293edc7e535CAS |
Ponniah, M., and Hughes, J. (2004). The evolution of Queensland spiny mountain crayfish of the genus Euastacus. I. Testing vicariance and dispersal with interspecific mitochondrial DNA. Evolution 58, 1073–1085.
| The evolution of Queensland spiny mountain crayfish of the genus Euastacus. I. Testing vicariance and dispersal with interspecific mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |
Pörtner, H. O. (2002). Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 132, 739–761.
| Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals.Crossref | GoogleScholarGoogle Scholar |
Renshaw, G. M. C., Kutek, A. K., Grant, G. D., and Anoopkumar-Dukie, S. (2012). Forecasting elasmobranch survival following exposure to severe stressors. Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 162, 101–112.
| Forecasting elasmobranch survival following exposure to severe stressors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFajtrg%3D&md5=2e7a7dbb13d6616d87f791fe50413acbCAS |
Sánchez, A., Pascual, C., Sánchez, A., Vargas-Albores, F., Le Moullac, G., and Rosas, C. (2001). Hemolymph metabolic variables and immune response in Litopenaeus setiferus adult males: the effect of acclimation. Aquaculture 198, 13–28.
| Hemolymph metabolic variables and immune response in Litopenaeus setiferus adult males: the effect of acclimation.Crossref | GoogleScholarGoogle Scholar |
Schafer, F. Q., and Buettner, G. R. (2001). Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biology & Medicine 30, 1191–1212.
| Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFegt78%3D&md5=46894096528a83080c213d98ef8803b6CAS |
Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985). Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150, 76–85.
| Measurement of protein using bicinchoninic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlsFKksL0%3D&md5=b39b5cd77527706e458fb36189ccb884CAS |
Somero, G. N., and Hochachka, P. W. (1971). Biochemical adaptation to the environment. American Zoologist 11, 159–167.
| Biochemical adaptation to the environment.Crossref | GoogleScholarGoogle Scholar |
Stadtman, E. (1992). Protein oxidation and aging. Science 257, 1220–1224.
| Protein oxidation and aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xls1yitrk%3D&md5=ec5dd1f8a8e7c2a58fa93ccf0a709ad6CAS |
Turrens, J. F. (2003). Mitochondrial formation of reactive oxygen species. The Journal of Physiology 552, 335–344.
| Mitochondrial formation of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1ehtLc%3D&md5=65d30c8e9275123ee0eb1eb04c36706bCAS |
Verlecar, X. N., Jena, K. B., and Chainy, G. B. N. (2007). Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature. Chemico-Biological Interactions 167, 219–226.
| Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFehtrw%3D&md5=2b03d42847e6c507b2f7f291f99764daCAS |
Wheeler, R. E. (1963). Studies on the total haemocyte count and haemolymph volume in Periplaneta americana (L.) with special reference to the last moulting cycle. Journal of Insect Physiology 9, 223–235.
| Studies on the total haemocyte count and haemolymph volume in Periplaneta americana (L.) with special reference to the last moulting cycle.Crossref | GoogleScholarGoogle Scholar |
Williams, S. E., Bolitho, E. E., and Fox, S. (2003). Climate change in Australian tropical rainforests: an impending environmental catastrophe. Proceedings of the Royal Society of London – B. Biological Sciences 270, 1887–1892.
| Climate change in Australian tropical rainforests: an impending environmental catastrophe.Crossref | GoogleScholarGoogle Scholar |
Winston, G. W., and Di Giulio, R. T. (1991). Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology 19, 137–161.
| Prooxidant and antioxidant mechanisms in aquatic organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1Kgsrc%3D&md5=9905f6e38c7e66acabb3a4826794eaecCAS |
