USAP-DC

The ocean surrounding Antarctica is home to an extraordinary assemblage of fishes, dominated by a single group that are extremely well-suited to life in icy waters and which are of significant ecological importance there. Of great concern is the capacity of these fishes to withstand increases in temperature as the region of the Western Antarctic Peninsula warms at a rate faster than any other area in the Southern hemisphere. One particular group of Antarctic fishes, known as the icefishes, are particularly vulnerable to increases in temperature because unlike all other vertebrates on earth, icefishes are white-blooded due to their lack of the oxygen-binding protein hemoglobin. This greatly reduces their capacity to transport and deliver oxygen to tissues compared to red-blooded Antarctic fishes. Previous studies have shown that icefishes are indeed less tolerant to elevations in temperature but the underlying factors are completely unknown. Additionally, it is not understood if red- or white-blooded Antarctic fishes can adjust, or acclimate, to modest increases in temperature, similar to those changes in temperature the animals might experience as the earth warms. The investigators will determine if heart function and/or nervous system function limits thermal tolerance of Antarctic fishes, and will determine their capacity to acclimate to warmer temperatures. The project will further the NSF goal of training new generations of scientists by training graduate and undergraduate students. In addition, the project will collaborate with a high school biology teacher from a school which serves a largely minority student body. The students will learn about the marine environment, and will construct a camera to be used in the field to learn more about Antarctic fishes. Two students and the teacher will also attend a summer marine biology internship program.

Antarctic fishes within the suborder Notothenioidei (called "notothenioids") are among the organisms on earth least able to deal with changes in temperature. The hemoglobinless icefish are even less able to withstand temperature changes than are red-blooded notothenioids. While this is well documented, the underlying physiological and biochemical mechanisms responsible are unknown. The investigators will test the hypotheses that cardiac work is significantly greater in icefishes compared to red-blooded species, and that as temperature increases, the greater cardiac work of icefishes, coupled with reduced blood oxygen-carrying capacity, results in cardiac failure at a lower temperature compared to red-blooded species. They also hypothesize that neuronal function limits thermal tolerance of red-blooded notothenioids. These hypotheses will be tested using a wide variety of experiments. For example, the investigators will measure heart rate concurrently with critical thermal maximum. They will also characterize metabolic and gene-expression responses to elevated temperature and determine if mitochondrial function contributes to thermal tolerance using a variety of techniques. To determine if neuronal function limits thermal tolerance they will quantify behavioral responses to warming of whole animals and to warming of only the brain area. They will also determine if acclimation to warmer temperatures impacts heart function and they will measure activities of a variety of enzymes from central metabolic pathways.

Person	Role
Crockett, Elizabeth	Investigator
Joyce, William	Researcher
O'Brien, Kristin	Investigator and contact
Farrell, Anthony	Researcher
Egginton, Stuart	Researcher
Axelsson, Michael	Researcher
Biederman, Amanda	Researcher
Evans, Elizabeth	Researcher

Antarctic Organisms and Ecosystems	Award # 1341663
Antarctic Organisms and Ecosystems	Award # 1341602

USAP-1341602_1

Deployment	Type
Palmer Station, Antarctica	general deployment

None in the Database

Repository	Title (link)	Format(s)	Status
Dryad	Maximum cardiac performance of Antarctic fishes that lack haemoglobin and myoglobin: exploring the effect of warming on nature’s natural knockouts	None	exists
Dryad	Mitochondrial membranes in cardiac muscle from Antarctic notothenioid fishes vary in phospholipid composition and membrane fluidity	None	exists
Dryad	Physical, chemical, and functional properties of neuronal membranes vary between species of Antarctic notothenioids differing in thermal tolerance	None	exists
USAP-DC	Effects of acute warming on cardiovascular performance of Antarctic fishes	None	exists
USAP-DC	Cardiac metabolism in Antarctic fishes in response to an acute increase in temperature	None	exists
USAP-DC	Thermal sensitivity of membrane fluidity and integrity in hearts of Antarctic fishes that vary in expression of hemoglobin and myoglobin	None	exists
USAP-DC	Hypoxia response of hearts of Antarctic fishes	None	exists
GenBank	Chaenocephalus aceratus HIF-1A mRNA, complete cds	None	exists
GenBank	Notothenia coriiceps HIF-1A mRNA, complete cds	None	exists
GenBank	Eleginops maclovinus HIF-1A mRNA, partial cds	None	exists
GenBank	Parachaenichthys charcoti HIF-1A mRNA, partial cds	None	exists
GenBank	Gymnodraco acuticeps HIF-1A mRNA, partial cds	None	exists
GenBank	Chionodraco rastrospinosus HIF-1A mRNA, partial cds	None	exists
USAP-DC	Measurements of splenic contraction in Antarctic fishes	None	exists
USAP-DC	Acclimation of cardiovascular function in Notothenia coriiceps	None	exists
USAP-DC	Adrenergic and adenosinergic regulation of the cardiovascular system in the Antarctic icefish Chaenocephalus aceratus	None	exists

1. Biederman, D.E. Kuhn, K.M. O’Brien, and E.L. Crockett (2019). Mitochondrial membranes in cardiac muscle from Antarctic notothenioid fishes vary in phospholipid composition and membrane fluidity. Comparative Biochemistry and Physiology B 235: 46-53. (doi:10.1016/j.cbpb.2019.05.011)
2. Biederman, A.M., D.E. Kuhn, K.M. O’Brien, and E.L. Crockett. (2019). Physical, chemical, and functional properties of neuronal membranes vary between species of Antarctic notothenioids differing in thermal tolerance. Journal of Comparative Physiology B 189: 213-222. (doi:10.1007/s00360-019-01207-x)
3. Egginton, S., M. Axelsson, E.L. Crockett, K.M. O’Brien, and A.P. Farrell. (2019). Maximum cardiac performance of Antarctic fishes that lack hemoglobin and myoglobin: exploring the effects of warming on nature’s natural knockouts. Conservation Physiology 7 (doi:10.1093/conphys/coz049)
4. O’Brien, K.M., A.S. Rix, S. Egginton, A.P. Farrell, E.L. Crockett, K. Schlauch, R. Woolsey, M. Hoffman, and S. Merriman. (2018). Cardiac mitochondrial metabolism may contribute to differences in thermal tolerance of red- and white-blooded Antarctic notothenioid fishes. Journal of Experimental Biology 221. jeb 177816. (doi:10.1242/jeb.177816)
5. Joyce, W., S Egginton, A.P. Farrell, E.L. Crockett, K.M. O’Brien, and M. Axelsson (2018). Exploring nature’s natural knockouts: in vivo cardiorespiratory performance of Antarctic fishes during acute warming. Journal of Experimental Biology 221. jeb 183160. (doi:10.1242/jeb.183160)
6. Joyce, W., Axelsson, M., Egginton, S., Farrell, A. P., Crockett, E. L., & O’Brien, K. M. (2018). The effects of thermal acclimation on cardio-respiratory performance in an Antarctic fish (Notothenia coriiceps). Conservation Physiology, 6(1). (doi:10.1093/conphys/coy069)
7. O’Brien, K. M., Rix, A. S., Grove, T. J., Sarrimanolis, J., Brookings, A., Roberts, M., & Crockett, E. L. (2020). Characterization of the hypoxia-inducible factor-1 pathway in hearts of Antarctic notothenioid fishes. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 110505. (doi:10.1016/j.cbpb.2020.110505)
8. Rix, A.S., Grove, T.J., and K.M. O’Brien. (2017). Hypoxia-inducible factor-1a in Antarctic fishes contains a polyglutamine and glutamic acid insert that varies in length with phylogeny. Polar Biol. 40(12) 2537-2545. (doi:10.1007/s00300-017-2164-6)
9. Evans, E.E. , Farnoud, A., O’Brien, K.M., and E.L. Crockett (2020). Thermal profiles reveal stark contrasts in properties of biological membranes from heart among Antarctic notothenioid fishes which vary in expression of hemoglobin and myoglobin. (doi:10.1016/j.cbpb.2020.110539)
10. Joyce, W., and M. Axelsson (2020). Regulation of splenic contraction persists as a vestigial trait in white-blooded Antarctic fishes. J Fish Biol. 2020 (doi:10.1111/jfb.14579)
11. Joyce W, Egginton S, Farrell AP, Axelsson M. (2019). Adrenergic and adenosinergic regulation of the cardiovascular system in an Antarctic icefish: Insight into central and peripheral determinants of cardiac output. Comp Biochem Physiol A Mol Integr Physiol. 230:28-38 (doi:10.1016/j.cbpa.2018.12.012)
12. O’Brien, K. M., Joyce, W., Crockett, E. L., Axelsson, M., Egginton, S., & Farrell, A. P. (2021). Resilience of cardiac performance in Antarctic notothenioid fishes in a warming climate. Journal of Experimental Biology, 224(10). (doi:10.1242/jeb.220129)
13. Biederman, A. M., O’Brien, K. M., & Crockett, E. L. (2021). Homeoviscous adaptation occurs with thermal acclimation in biological membranes from heart and gill, but not the brain, in the Antarctic fish Notothenia coriiceps. Journal of Comparative Physiology B, 191(2), 289–300. (doi:10.1007/s00360-020-01339-5)
14. Ismailov, I. I., Scharping, J. B., Andreeva, I. E., & Friedlander, M. J. (2021). Antarctic teleosts with and without hemoglobin behaviorally mitigate deleterious effects of acute environmental warming. PLOS ONE, 16(11), e0252359. (doi:10.1371/journal.pone.0252359)
15. Ismailov, I. I., Scharping, J. B., Andreeva, I. E., & Friedlander, M. J. (2018). Behavioral Thermoregulation of Antarctic Teleosts With and Without Hemoglobin in Response to Acute Thermal Challenge. The FASEB Journal, 32(S1). (doi:10.1096/fasebj.2018.32.1_supplement.859.2)
16. O’Brien, K., Jasmin, A., Schilkey, F., Sena, J., & Lavelle, E. (2021). The Hypoxia Response Pathway is Functional Despite a Mutation in HIF‐1α in the Antarctic Notothenioid Fish Notothenia coriiceps. The FASEB Journal, 35(S1). (doi:10.1096/fasebj.2021.35.s1.05035)