Physiological plasticity v. inter-population variability: understanding drivers of hypoxia tolerance in a tropical estuarine fish
Geoffrey Mark Collins A B D , Timothy Darren Clark B C and Alexander Guy Carton A
+ Author Affiliations
- Author Affiliations
A Centre for Sustainable Tropical Fisheries and Aquaculture, College of Marine and Environmental Science, James Cook University, Townsville, Qld 4810, Australia.
B AIMS@JCU Collaborative Research Program, Townsville, Qld 4810, Australia.
C University of Tasmania and CSIRO Agriculture Flagship, Hobart, Tas. 7000, Australia.
D Corresponding author. Email: geoffreymcollins@gmail.com
Marine and Freshwater Research 67(10) 1575-1582 https://doi.org/10.1071/MF15046
Submitted: 5 February 2015 Accepted: 13 August 2015 Published: 13 October 2015
Abstract
Physiological plasticity and inter-population variability (e.g. local adaptation) are two key drivers in determining the capacity for species to cope with environmental change, yet the relative contribution of each parameter has received little attention. Here, we investigate the acclimation potential of two geographically distinct populations of the barramundi (Lates calcarifer) to diel hypoxia. Fish were exposed to a daily hypoxia challenge of 6 h below 62% saturation, down to a minimum of 10 ± 5% saturation, followed by a return to normoxia. Respiratory and haematological variables were assessed after 8 and 16 days of daily hypoxia exposure. Hypoxia tolerance (measured as the critical oxygen tension; [O2]crit) was not different between populations and not different from control fish after 8 days ([O2]crit = 20.7 ± 2.8% saturation), but improved similarly in both populations after 16 days ([O2]crit = 16.5 ± 3.1% saturation). This improvement corresponded with increases in haematocrit and haemoglobin, but not an increase in the mean cell haemoglobin concentration. Given the similarity of the response between these two geographically distinct populations, we conclude that hypoxia tolerance for barramundi may be more dependent on physiological plasticity than inherent variability between populations.
Additional keywords: barramundi, Lates calcarifer, local adaptation, oxygen.
References
AIMS (2012). AIMS Data Centre. 2012. (Australian Institute of Marine Science: Townsville, Qld, Australia.) Available at http://maps.aims.gov.au/index.html?intro=false&z=4&ll=142.91883,-17.51872&l0=aims_aims:AIMS%20-%20Temperature%20Loggers,ea_World_NE2-coast-cities-reefs_Baselayer [Verified 19 August 2012].Almeida‐Val, V. M. F., Chippari Gomes, A. R., and Lopes, N. P. (2005). Metabolic and physiological adjustments to low oxygen and high temperature in fishes of the Amazon. In ‘Fish Physiology. Vol. 21’. (Eds L. V. Adalberto, V. M. F. de Almeida-Val and D. J. Randall.) pp. 443–500. (Academic Press: San Diego, CA.)
BOM (2012). Daily Weather Observations. (Bureau of Meteorology: Canberra, ACT, Australia.) Available at http://www.bom.gov.au/climate/dwo/index.shtml [Verified 25 August 2012].
Borowiec, B. G., Darcy, K. L., Gillette, D. M., and Scott, G. R. (2015). Distinct physiological strategies are used to cope with constant hypoxia and intermittent hypoxia in killifish (Fundulus heteroclitus). The Journal of Experimental Biology 218, 1198–1211.
| Distinct physiological strategies are used to cope with constant hypoxia and intermittent hypoxia in killifish (Fundulus heteroclitus).Crossref | GoogleScholarGoogle Scholar | 25722002PubMed |
Brady, D. C., Targett, T. E., and Tuzzolino, D. M. (2009). Behavioral responses of juvenile weakfish (Cynoscion regalis) to diel-cycling hypoxia: swimming speed, angular correlation, expected displacement, and effects of hypoxia acclimation. Canadian Journal of Fisheries and Aquatic Sciences 66, 415–424.
| Behavioral responses of juvenile weakfish (Cynoscion regalis) to diel-cycling hypoxia: swimming speed, angular correlation, expected displacement, and effects of hypoxia acclimation.Crossref | GoogleScholarGoogle Scholar |
Brauner, C. J., and Val, A. L. (2005). Oxygen transfer. In ‘Fish Physiology. Vol. 21’. (Eds L. V. Adalberto, V. M. F. de Almeida-Val and D. J. Randall.) pp. 277–306. (Academic Press: San Diego, CA.)
Burford, M. A., Revill, A. T., Palmer, D. W., Clementson, L., Robson, B. J., and Webster, I. T. (2011). River regulation alters drivers of primary productivity along a tropical river-estuary system. Marine and Freshwater Research 62, 141–151.
| 1:CAS:528:DC%2BC3MXitlejt7w%3D&md5=eea3e7c331a67ecb63b48bf771dbb7b2CAS |
Burleson, M. L., Wilhelm, D. R., and Smatresk, N. J. (2001). The influence of fish size on the avoidance of hypoxia and oxygen selection by largemouth bass. Journal of Fish Biology 59, 1336–1349.
Bushnell, P. G., Steffensen, J. F., and Johansen, K. (1984). Oxygen consumption and swimming performance in hypoxia-acclimated rainbow trout Salmo gairdneri. The Journal of Experimental Biology 113, 225–235.
Butler, B. (2008). ‘Report 5: Water Quality.’ (National Centre for Tropical Wetland Research: Townsville, Qld, Australia.)
Butler, B., and Burrows, D. (2007). Dissolved oxygen guidelines for freshwater habitats of northern Australia. ACTFR Report number 07/32. (Australian Centre for Tropical Freshwater Research, James Cook University: Townsville, Qld, Australia.)
Butler, B., Burrows, D., and Pearson, R. G. (2007). ‘Testing the Hypoxia Tolerance of Tropical Freshwater Fishes.’ (Australian Centre for Tropical Freshwater Research, James Cook University: Townsville, Qld, Australia.)
Chapman, L. G., Galis, F., and Shinn, J. (2000). Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in the morphological traits of an African cichlid. Ecology Letters 3, 387–393.
| Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in the morphological traits of an African cichlid.Crossref | GoogleScholarGoogle Scholar |
Chenoweth, S. F., Hughes, J. M., Keenan, C. P., and Lavery, S. (1998). When oceans meet: a teleost shows secondary intergradation at an Indian–Pacific interface. Proceedings of the Royal Society of London. Series B, Biological Sciences 265, 415–420.
| When oceans meet: a teleost shows secondary intergradation at an Indian–Pacific interface.Crossref | GoogleScholarGoogle Scholar |
Clark, T. D., Eliason, E. J., Sandblom, E., Hinch, S. G., and Farrell, A. P. (2008). Calibration of a hand-held haemoglobin analyser for use on fish blood. Journal of Fish Biology 73, 2587–2595.
| Calibration of a hand-held haemoglobin analyser for use on fish blood.Crossref | GoogleScholarGoogle Scholar |
Clark, T. D., Donaldson, M. R., Drenner, S. M., Hinch, S. G., Patterson, D. A., Hills, J., Ives, V., Carter, J. J., Cooke, S. J., and Farrell, A. P. (2011). The efficacy of field techniques for obtaining and storing blood samples from fishes. Journal of Fish Biology 79, 1322–1333.
| The efficacy of field techniques for obtaining and storing blood samples from fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Glt7jJ&md5=4b7139beed9376d954f3613bb50c910cCAS | 22026608PubMed |
Clark, T. D., Sandblom, E., and Jutfelt, F. (2013). Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. The Journal of Experimental Biology 216, 2771–2782.
| Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations.Crossref | GoogleScholarGoogle Scholar | 23842625PubMed |
Collins, G. M., Clark, T. D., Rummer, J. L., and Carton, A. G. (2013). Hypoxia tolerance is conserved across genetically distinct sub-populations of an iconic, tropical Australian teleost (Lates calcarifer). Conservation Physiology 1, cot029.
| Hypoxia tolerance is conserved across genetically distinct sub-populations of an iconic, tropical Australian teleost (Lates calcarifer).Crossref | GoogleScholarGoogle Scholar |
Cook, D. G., Iftikar, F. I., Baker, D. W., Hickey, A. J. R., and Herbert, N. A. (2013). Low-O2 acclimation shifts the hypoxia avoidance behaviour of snapper (Pagrus auratus) with only subtle changes in aerobic and anaerobic function. The Journal of Experimental Biology 216, 369–378.
| Low-O2 acclimation shifts the hypoxia avoidance behaviour of snapper (Pagrus auratus) with only subtle changes in aerobic and anaerobic function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltVagt70%3D&md5=b622da4b597e0e50ebb329eb668b39e1CAS | 23038727PubMed |
Crispo, E., and Chapman, L. J. (2008). Population genetic structure across dissolved oxygen regimes in an African cichlid fish. Molecular Ecology 17, 2134–2148.
| Population genetic structure across dissolved oxygen regimes in an African cichlid fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVeksbc%3D&md5=27c44ec35416f05ec3be47947c6b6198CAS | 18410294PubMed |
Crispo, E., and Chapman, L. J. (2010). Geographic variation in phenotypic plasticity in response to dissolved oxygen in an African cichlid fish. Journal of Evolutionary Biology 23, 2091–2103.
| Geographic variation in phenotypic plasticity in response to dissolved oxygen in an African cichlid fish.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfisVSlsQ%3D%3D&md5=1cbdf1e400bf833b91550467bc0710feCAS | 20722894PubMed |
Dan, X.-M., Yan, G.-J., Zhang, A.-J., Cao, Z.-D., and Fu, S.-J. (2014). Effects of stable and diel-cycling hypoxia on hypoxia tolerance, postprandial metabolic response, and growth performance in juvenile qingbo (Spinibarbus sinensis). Aquaculture 428–429, 21–28.
| Effects of stable and diel-cycling hypoxia on hypoxia tolerance, postprandial metabolic response, and growth performance in juvenile qingbo (Spinibarbus sinensis).Crossref | GoogleScholarGoogle Scholar |
Davis, J. C. (1975). Minimal dissolved oxygen requirements of aquatic life with emphasis on Canadian species: a review. Journal of the Fisheries Research Board of Canada 32, 2295–2332.
| Minimal dissolved oxygen requirements of aquatic life with emphasis on Canadian species: a review.Crossref | GoogleScholarGoogle Scholar |
Diaz, R. J., and Breitburg, D. L. (2009). Chapter 1 The hypoxic environment. In ‘Fish Physiology. Vol. 27.’ (Eds A. P. F. Jeffrey, G. Richards and J. B. Colin.) pp. 1–23. (Academic Press: San Diego, CA.)
Edmunds, R. C., van Herwerden, L., and Fulton, C. J. (2010). Population-specific locomotor phenotypes are displayed by barramundi, Lates calcarifer, in response to thermal stress. Canadian Journal of Fisheries and Aquatic Sciences 67, 1068–1074.
| Population-specific locomotor phenotypes are displayed by barramundi, Lates calcarifer, in response to thermal stress.Crossref | GoogleScholarGoogle Scholar |
Edmunds, R. C., Smith-Keune, C., Van Herwerden, L., Fulton, C. J., and Jerry, D. R. (2012). Exposing local adaptation: synergistic stressors elicit population-specific lactate dehydrogenase-B (ldh-b) expression profiles in Australian barramundi, Lates calcarifer. Aquatic Sciences 74, 171–178.
| Exposing local adaptation: synergistic stressors elicit population-specific lactate dehydrogenase-B (ldh-b) expression profiles in Australian barramundi, Lates calcarifer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksVKjsg%3D%3D&md5=a0cf6b5a6efed3fbf599fd9fa863bee9CAS |
Farrell, A. P., and Richards, J. G. (2009). Chapter 11 Defining hypoxia: an integrative synthesis of the responses of fish to hypoxia. In ‘Fish Physiology. Vol. 27.’ (Eds A. P. F. Jeffrey, G. Richards and J. B. Colin.) pp. 487–503. (Academic Press: San Diego, CA.)
Flint, N., Crossland, M. R., and Pearson, R. G. (2015). Sublethal effects of fluctuating hypoxia on juvenile tropical Australian freshwater fish. Marine and Freshwater Research 66, 293–304.
| Sublethal effects of fluctuating hypoxia on juvenile tropical Australian freshwater fish.Crossref | GoogleScholarGoogle Scholar |
Froese, R. (2006). Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. Journal of Applied Ichthyology 22, 241–253.
| Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations.Crossref | GoogleScholarGoogle Scholar |
Fu, S.-J., Brauner, C. J., Cao, Z.-D., Richards, J. G., Peng, J.-L., Dhillon, R., and Wang, Y.-X. (2011). The effect of acclimation to hypoxia and sustained exercise on subsequent hypoxia tolerance and swimming performance in goldfish (Carassius auratus). The Journal of Experimental Biology 214, 2080–2088.
| The effect of acclimation to hypoxia and sustained exercise on subsequent hypoxia tolerance and swimming performance in goldfish (Carassius auratus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOntrfL&md5=8e8f81ec6812610ccb39b5d282c07796CAS | 21613525PubMed |
Gamble, S., Carton, A. G., and Pirozzi, I. (2014). Open-top static respirometry is a reliable method to determine the routine metabolic rate of barramundi, Lates calcarifer. Marine and Freshwater Behaviour and Physiology 47, 19–28.
| Open-top static respirometry is a reliable method to determine the routine metabolic rate of barramundi, Lates calcarifer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisVCrsLk%3D&md5=a0ea0dbc19614f31dea1994e6270db80CAS |
Gillanders, B. M., Elsdon, T. S., Halliday, I. A., Jenkins, G. P., Robins, J. B., and Valesini, F. J. (2011). Potential effects of climate change on Australian estuaries and fish utilising estuaries: a review. Marine and Freshwater Research 62, 1115–1131.
| Potential effects of climate change on Australian estuaries and fish utilising estuaries: a review.Crossref | GoogleScholarGoogle Scholar |
Jerry, D. R., Smith-Keune, C., Hodgsone, L., Pirozzi, I., Carton, A. G., Hutson, K. S., Brazenor, A. K., Gonzalez, A. T., Gamble, S., Collins, G. M., and VanderWal, J. (2013). ‘Vulnerability of an iconic Australian finfish (barramundi – Lates calcarifer) and aligned industries to climate change across tropical Australia.’ (Fisheries Research and Development Corporation and James Cook University: Townsville, Qld, Australia.)
Kay, W. R., Smith, M. J., Pinder, A. M., McRae, J. M., Davis, J. A., and Halse, S. A. (1999). Patterns of distribution of macroinvertebrate families in rivers of north-western Australia. Freshwater Biology 41, 299–316.
| Patterns of distribution of macroinvertebrate families in rivers of north-western Australia.Crossref | GoogleScholarGoogle Scholar |
Kind, P. K., Grigg, G. C., and Booth, D. T. (2002). Physiological responses to prolonged aquatic hypoxia in the Queensland lungfish, Neoceratodus forsteri. Respiratory Physiology & Neurobiology 132, 179–190.
| Physiological responses to prolonged aquatic hypoxia in the Queensland lungfish, Neoceratodus forsteri.Crossref | GoogleScholarGoogle Scholar |
Kramer, D. L. (1987). Dissolved oxygen and fish behavior. Environmental Biology of Fishes 18, 81–92.
| Dissolved oxygen and fish behavior.Crossref | GoogleScholarGoogle Scholar |
McNeil, D. G., and Closs, G. P. (2007). Behavioural responses of a south-east Australian floodplain fish community to gradual hypoxia. Freshwater Biology 52, 412–420.
| Behavioural responses of a south-east Australian floodplain fish community to gradual hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFSit74%3D&md5=8015077d9a37d9c9146a91c6d6e98578CAS |
Moore, R., and Reynolds, L. (1982). Migration patterns of barramundi, Lates calcarifer (Bloch), in Papua New Guinea. Marine and Freshwater Research 33, 671–682.
| Migration patterns of barramundi, Lates calcarifer (Bloch), in Papua New Guinea.Crossref | GoogleScholarGoogle Scholar |
Newton, J. R., Smith-Keune, C., and Jerry, D. R. (2010). Thermal tolerance varies in tropical and sub-tropical populations of barramundi (Lates calcarifer) consistent with local adaptation. Aquaculture 308, S128–S132.
| Thermal tolerance varies in tropical and sub-tropical populations of barramundi (Lates calcarifer) consistent with local adaptation.Crossref | GoogleScholarGoogle Scholar |
Nilsson, G. E., and Ostlund-Nilsson, S. (2004). Hypoxia in paradise: widespread hypoxia tolerance in coral reef fishes. Proceedings. Biological Sciences 271, S30–S33.
| Hypoxia in paradise: widespread hypoxia tolerance in coral reef fishes.Crossref | GoogleScholarGoogle Scholar |
Nilsson, G. E., Östlund-Nilsson, S., and Munday, P. L. (2010). Effects of elevated temperature on coral reef fishes: loss of hypoxia tolerance and inability to acclimate. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 156, 389–393.
| Effects of elevated temperature on coral reef fishes: loss of hypoxia tolerance and inability to acclimate.Crossref | GoogleScholarGoogle Scholar |
Norin, T., Malte, H., and Clark, T. D. (2014). Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. The Journal of Experimental Biology 217, 244–251.
| Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures.Crossref | GoogleScholarGoogle Scholar | 24115064PubMed |
Pearson, R. G., Godfrey, P. C., Arthington, A. H., Wallace, J., Karim, F., and Ellison, M. (2013). Biophysical status of remnant freshwater floodplain lagoons in the Great Barrier Reef catchment: a challenge for assessment and monitoring. Marine and Freshwater Research 64, 208–222.
| Biophysical status of remnant freshwater floodplain lagoons in the Great Barrier Reef catchment: a challenge for assessment and monitoring.Crossref | GoogleScholarGoogle Scholar |
Petersen, L. H., and Gamperl, A. K. (2011). Cod (Gadus morhua) cardiorespiratory physiology and hypoxia tolerance following acclimation to low-oxygen conditions. Physiological and Biochemical Zoology 84, 18–31.
| Cod (Gadus morhua) cardiorespiratory physiology and hypoxia tolerance following acclimation to low-oxygen conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFKkurk%3D&md5=97ef3352705582d54ad8a09306011994CAS | 21050128PubMed |
Pollock, M. S., Clarke, L. M. J., and Dubé, M. G. (2007). The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environmental Reviews 15, 1–14.
| The effects of hypoxia on fishes: from ecological relevance to physiological effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlyitLg%3D&md5=4c12a3bcfb2e14d1195b370959170434CAS |
Pusey, B. J., Kennard, M. J., and Arthington, A. H. (2004). ‘Freshwater Fishes of North-Eastern Australia.’ (CSIRO Publishing: Melbourne, Vic., Australia.)
Righton, D. A., Andersen, K. H., Neat, F., Thorsteinsson, V., Steingrund, P., Svedäng, H., Michalsen, K., Hinrichsen, H. H., Bendall, V., Neuenfeldt, S., Wright, P., Jonsson, P., Huse, G., van der Kooij, J., Mosegaard, H., Hüssy, K., and Metcalfe, J. D. (2010). Thermal niche of Atlantic cod Gadus morhua: limits, tolerance and optima. Marine Ecology Progress Series 420, 1–13.
| Thermal niche of Atlantic cod Gadus morhua: limits, tolerance and optima.Crossref | GoogleScholarGoogle Scholar |
Routley, M. H., Nilsson, G. E., and Renshaw, G. M. C. (2002). Exposure to hypoxia primes the respiratory and metabolic responses of the epaulette shark to progressive hypoxia. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 131, 313–321.
| Exposure to hypoxia primes the respiratory and metabolic responses of the epaulette shark to progressive hypoxia.Crossref | GoogleScholarGoogle Scholar |
Russell, D. J., and Garrett, R. N. (1988). Movements of juvenile barramundi, Lates calcarifer (Bloch), in north-eastern Queensland. Marine and Freshwater Research 39, 117–123.
| Movements of juvenile barramundi, Lates calcarifer (Bloch), in north-eastern Queensland.Crossref | GoogleScholarGoogle Scholar |
Seebacher, F., White, C. R., and Franklin, C. E. (2015). Physiological plasticity increases resilience of ectothermic animals to climate change. Nature Climate Change 5, 61–66.
| Physiological plasticity increases resilience of ectothermic animals to climate change.Crossref | GoogleScholarGoogle Scholar |
Stierhoff, K. L., Tyler, R. M., and Targett, T. E. (2009). Hypoxia tolerance of juvenile weakfish (Cynoscion regalis): laboratory assessment of growth and behavioral avoidance responses. Journal of Experimental Marine Biology and Ecology 381, S173–S179.
| Hypoxia tolerance of juvenile weakfish (Cynoscion regalis): laboratory assessment of growth and behavioral avoidance responses.Crossref | GoogleScholarGoogle Scholar |
Stuart, I. G., and Berghuis, A. P. (2002). Upstream passage of fish through a vertical-slot fishway in an Australian subtropical river. Fisheries Management and Ecology 9, 111–122.
| Upstream passage of fish through a vertical-slot fishway in an Australian subtropical river.Crossref | GoogleScholarGoogle Scholar |
Tetens, V., and Lykkeboe, G. (1981). Blood respiratory properties of rainbow trout, Salmo gairdneri: responses to hypoxia acclimation and anoxic incubation of blood in vitro. Journal of Comparative Physiology 145, 117–125.
| Blood respiratory properties of rainbow trout, Salmo gairdneri: responses to hypoxia acclimation and anoxic incubation of blood in vitro.Crossref | GoogleScholarGoogle Scholar |
Tewksbury, J. J., Huey, R. B., and Deutsch, C. A. (2008). Putting the heat on tropical animals. Science 320, 1296–1297.
| Putting the heat on tropical animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1yrsrw%3D&md5=ec9bec60ea7ecbf97f9fe9787fabbd3bCAS | 18535231PubMed |
Tyler, R. M., and Targett, T. E. (2007). Juvenile weakfish Cynoscion regalis distribution in relation to diel-cycling dissolved oxygen in an estuarine tributary. Marine Ecology Progress Series 333, 257–269.
| Juvenile weakfish Cynoscion regalis distribution in relation to diel-cycling dissolved oxygen in an estuarine tributary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFemtLo%3D&md5=3d9f59a81d4516c00419232e477eba9cCAS |
Val, A. L., de Almeida‐Val, V. M. F., and Randall, D. J. (2005). Tropical environment. In ‘Fish Physiology’, Vol. 21. (Eds V. M. F. de Almeida‐Val, A. L. Val and D. J. Randall.) pp. 1–45. (Academic Press: San Diego, CA.)
Vaquer-Sunyer, R., and Duarte, C. M. (2008). Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences of the United States of America 105, 15 452–15 457.
| Thresholds of hypoxia for marine biodiversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Gnt7zI&md5=c454861f956cdc1d1a800598fbc662c1CAS |
Via, S., Gomulkiewicz, R., De Jong, G., Scheiner, S. M., Schlichting, C. D., and Van Tienderen, P. H. (1995). Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology & Evolution 10, 212–217.
| Adaptive phenotypic plasticity: consensus and controversy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFagtQ%3D%3D&md5=df5b014d126d2fd9b4b5b05df119f9deCAS |
Waltham, N. J., Burrows, D., Butler, B., Wallace, J., Thomas, C., James, C., and Brodie, J. (2013). ‘A Technical Report to the Australian Government from the CSIRO Flinders and Gilbert Agricultural Resource Assessment, Part of the North Queensland Irrigated Agriculture Strategy.’ (James Cook University and CSIRO: Townsville, Qld, Australia.)
Wells, R. M. G. (2009). Blood‐gas transport and hemoglobin function: adaptations for functional and environmental hypoxia. In ‘Fish Physiology. Vol. 27.’ (Eds A. P. F. Jeffrey, G. Richards and J. B. Colin.) pp. 255–299. (Academic Press: San Diego, CA.)
Wells, R. M. G., and Pankhurst, N. W. (1999). Evaluation of simple instruments for the measurement of blood glucose and lactate, and plasma protein as stress indicators in fish. Journal of the World Aquaculture Society 30, 276–284.
| Evaluation of simple instruments for the measurement of blood glucose and lactate, and plasma protein as stress indicators in fish.Crossref | GoogleScholarGoogle Scholar |
West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences of the United States of America 102, 6543–6549.
| Developmental plasticity and the origin of species differences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlais7g%3D&md5=8cf36c6822f3ee0a150bb71ae8bb68d9CAS | 15851679PubMed |
Wood, S. C., and Johansen, K. (1972). Adaptation to hypoxia by increased HbO2 affinity and decreased red cell ATP concentration. Nature: New Biology 237, 278–279.
| Adaptation to hypoxia by increased HbO2 affinity and decreased red cell ATP concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XkvVGqtbg%3D&md5=f0fd995b20abafd1472c1629765005a5CAS |
Yang, H., Cao, Z.-D., and Fu, S.-J. (2013). The effects of diel-cycling hypoxia acclimation on the hypoxia tolerance, swimming capacity and growth performance of southern catfish (Silurus meridionalis). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 165, 131–138.
| The effects of diel-cycling hypoxia acclimation on the hypoxia tolerance, swimming capacity and growth performance of southern catfish (Silurus meridionalis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmt12hsb4%3D&md5=d67424cbdec0d815e320976062230284CAS |
