Channichthyidae

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Icefish
Icefish Chionodraco hamatus.jpg
Chionodraco hamatus
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Actinopterygii
Order: Perciformes
Suborder: Notothenioidei
Family: Channichthyidae
T. N. Gill, 1861 [1]
Genera

see text

The crocodile icefish or white-blooded fish comprise a family (Channichthyidae) of notothenioid fish found in the Southern Ocean around Antarctica. They are the only known vertebrates to lack hemoglobin in their blood as adults. [2] Icefish populations are known to reside in the Atlantic and Indian sectors of the Southern Ocean, as well as the continental shelf waters surrounding Antarctica. [3] Water temperatures in these regions remain relatively stable, generally ranging from −1.8 to 2 °C (28.8 to 35.6 °F). [4] One icefish, Champsocephalus esox, is distributed north of the Antarctic Polar Frontal Zone. [3] At least 16 species of crocodile icefish are currently recognized, [2] although eight additional species have been proposed for the icefish genus Channichthys. [5]

Contents

In February 2021, scientists discovered and documented a breeding colony of Neopagetopsis ionah icefish estimated to have 60 million active nests across an area of approximately 92 square miles at the bottom of the Weddell Sea in Antarctica. [6] The majority of nests were occupied by one adult fish guarding an approximated estimate of 1,735 eggs in each nest. [7]

Genera

The following genera have been classified within the family Channichthyidae: [8] [9]

Diet and body size

All icefish are believed to be piscivorous, but can also feed on krill. [10] Icefish are typically ambush predators; thus, they can survive long periods between feeding, and often consume fish up to 50% of their own body length. Maximum body lengths of 25–50 cm (9.8–19.7 in) have been recorded in these species. [11]

Respiratory and circulatory system

Champsocephalus gunnari on a 1978 Soviet postage stamp 1978 CPA 4849.jpg
Champsocephalus gunnari on a 1978 Soviet postage stamp

Icefish blood is colorless because it lacks hemoglobin, the oxygen-binding protein in blood. [2] [12] Channichthyidae are the only known vertebrates to lack hemoglobin as adults. Although they do not manufacture hemoglobin, remnants of hemoglobin genes can be found in their genome. The hemoglobin protein is made of two subunits (alpha and beta). In 15 of the 16 icefish species, the beta subunit gene has been completely deleted and the alpha subunit gene has been partially deleted. [13] One icefish species, Neopagetopsis ionah, has a more complete, but still nonfunctional, hemoglobin gene. [14]

Red blood cells (RBCs) are usually absent, and if present, are rare and defunct. [15] Oxygen is dissolved in the plasma and transported throughout the body without the hemoglobin protein. The fish can live without hemoglobin via low metabolic rates and the high solubility of oxygen in water at the low temperatures of their environment (the solubility of a gas tends to increase as temperature decreases). [2] However, the oxygen-carrying capacity of icefish blood is less than 10% that of their relatives with hemoglobin. [16]

Myoglobin, the oxygen-binding protein used in muscles, is absent from all icefish skeletal muscles. In 10 species, myoglobin is found in the heart muscle, specifically ventricles. [17] Loss of myoglobin gene expression in icefish heart ventricles has occurred at least four separate times. [2] [18]

To compensate for the absence of hemoglobin, icefish have larger blood vessels (including capillaries), greater blood volumes (four-fold those of other fish), larger hearts, and greater cardiac outputs (five-fold greater) compared to other fish. [2] Their hearts lack coronary arteries, and the ventricle muscles are very spongy, enabling them to absorb oxygen directly from the blood they pump. [19] Their hearts, large blood vessels and low-viscosity (RBC-free) blood are specialized to carry out very high flow rates at low pressures. [20] This helps to reduce the problems caused by the lack of hemoglobin. In the past, their scaleless skin had been widely thought to help absorb oxygen. However, current analysis has shown that the amount of oxygen absorbed by the skin is much less than that absorbed through the gills. [19] The little extra oxygen absorbed by the skin may play a part in supplementing the oxygen supply to the heart, [19] which receives venous blood from the skin and body before pumping it to the gills. Additionally, icefish have larger cardiac mitochondria and increased mitochondrial biogenesis in comparison to red-blooded notothenioids. [21] [22] This adaptation facilitates enhanced oxygen delivery by increasing mitochondrial surface area, and reducing distance between the extracellular area and the mitochondria.

Evolution

Chaenocephalus aceratus Chaenocephalus aceratus.jpg
Chaenocephalus aceratus
Chaenodraco wilsoni Chaenodraco wilsoni.jpg
Chaenodraco wilsoni

The icefish are considered a monophyletic group and likely descended from a sluggish demersal ancestor. [3] The cold, well-mixed, oxygen-rich waters of the Southern Ocean provided an environment where a fish with a low metabolic rate could survive even without hemoglobin, albeit less efficiently.

When the icefish evolved is unknown; two main competing hypotheses have been postulated. The first is that they are only about 6 million years old, appearing after the Southern Ocean cooled significantly. The second suggests that they are much older, 15-20 million years. [3]

Although the evolution of icefish is still disputed, the formation of the Antarctic Polar Frontal Zone (APFZ) and the Antarctic Circumpolar Current (ACC) is widely believed to mark the beginning of the evolution of Antarctic fish. [23] The ACC moves in a clockwise northeast direction, and can be up to 10,000 km (6,200 mi) wide. This current formed 25-22 million years ago, and thermally isolated the Southern Ocean by separating it from the warm subtropical gyres to the north.

During the mid-Tertiary period, a species crash in the Southern Ocean opened up wide range of empty niches to colonize. Despite the hemoglobin-less mutants being less fit, the lack of competition allowed even the mutants to leave descendants that colonized empty habitats and evolved compensations for their mutations. Later, the periodic openings of fjords created habitats that were colonized by a few individuals. These conditions may have also allowed for the loss of myoglobin. [2]

Loss of hemoglobin

The loss of hemoglobin was initially believed to be an adaptation to the extreme cold, as the lack of hemoglobin and red blood cells decreases blood viscosity, which is an adaptation that has been seen in species adapted to cold climates. In refuting this original hypothesis, previous analysis has proposed that the lack of hemoglobin, while not lethal, is not adaptive. [2] Any adaptive advantages incurred by reduced blood viscosity are outweighed by the fact that icefish must pump much more blood per unit of time to make up for the reduced oxygen carrying capacity of their blood. [2] The high blood volume of icefish is itself evidence that the loss of hemoglobin and myoglobin was not advantageous for the ancestor of the icefish. Their unusual cardiovascular physiology, including large heart, high blood volume, increased mitochondrial density, and extensive microvasculature, suggests that icefish have had to evolve ways of coping with the impairment of their oxygen binding and transport systems.

Recent research by Corliss et al. (2019) claims that the loss of hemoglobin has adaptive value. [24] Iron is a limiting nutrient in the environments inhabited by the icefish. [25] By no longer synthesizing hemoglobin, they claim that icefish are minimizing endogenous iron use. To demonstrate this, they obtained retinal samples of Champsocephalus gunnari and stained them to detect hemoglobin alpha 3'f. They found expression of hemoglobin alpha 3'f within the retinal vasculature of Champsocephalus gunnari , demonstrating for the first time that there is limited transcription and translation of a hemoglobin gene fragment within an icefish. Because this fragment of hemoglobin does not contain any iron binding sites, the finding suggests that hemoglobin was selected against to conserve iron.

Loss of myoglobin

Phylogenetic relationships indicate that the nonexpression of myoglobin in cardiac tissue has evolved at least four discrete times. [17] This repeated loss suggests that cardiac myoglobin may be vestigial or even detrimental to icefish. Sidell and O'Brien (2006) investigated this possibility. First, they performed a test using stopped flow spectrometry. They found that across all temperatures, oxygen binds and dissociates faster from icefish than it does from mammalian myoglobin. However, when they repeated the test with each organism at a temperature that accurately reflected its native environment, the myoglobin performance was roughly equivalent between icefish and mammals. So, they concluded that icefish myoglobin is neither more nor less functional than the myoglobin in other clades. [2] This means that myoglobin is unlikely to have been selected against. The same researchers then performed a test in which they selectively inhibited cardiac myoglobin in icefish with natural myoglobin expression. They found that icefish species that naturally lack cardiac myoglobin performed better without myoglobin than did fish that naturally express cardiac myoglobin. [2] This finding suggests that fish without cardiac myoglobin have undergone compensatory adaptation.

Reason for trait fix

The Southern Ocean is an atypical environment. To begin with, the Southern Ocean has been characterized by extremely cold but stable temperatures for the past 10-14 million years. [26] These cold temperatures, which allow for higher water oxygen content, combined with a high degree of vertical mixing in these waters, means oxygen availability in Antarctic waters is unusually high. The loss of hemoglobin and myoglobin would have negative consequences in warmer environments. [12] The stability in temperature is also "lucky", as strong fluctuations in temperature would create a more stressful environment that would likely weed out individuals with deleterious mutations. Although most research suggests that the loss of hemoglobin in icefish was a neutral or maladaptive trait that arose due to a random evolutionary event, [27] some researchers have also suggested that the loss of hemoglobin might be tied to a necessary adaptation for the icefish. [27] Most animals require iron for hemoglobin production, and iron is often limited in ocean environments. [28] Through hemoglobin loss, icefish may minimize their iron requirements. This minimization could have aided the icefish survival 8.5 million years ago when Arctic diversity plummeted dramatically. [27]

Cardiovascular physiology

Pagetopsis macropterus Pamac u0.gif
Pagetopsis macropterus

The key to solving this conundrum is to consider the other functions that both hemoglobin and myoglobin perform. While emphasis is often placed and understandably so on the importance of hemoglobin and myoglobin in oxygen delivery and use, recent studies have found that both proteins are actually also involved in the process of breaking down nitric oxide. [29] This means that when icefish lost hemoglobin and myoglobin, it did not just mean a decreased ability to transport oxygen, but it also meant that total nitric oxide levels were elevated. [2] Nitric oxide plays a role in regulating various cardiovascular processes in icefish, such as the dilation of branchial vasculature, cardiac stroke volume, and power output. [30] The presence of nitric oxide also can increase angiogenesis, mitochondrial biogenesis, and cause muscle hypertrophy; all of these traits are characteristics of icefish. The similarity between nitric oxide-mediated trait expression and the unusual cardiovascular traits of icefish suggests that while these abnormal traits have evolved over time, much of these traits were simply an immediate physiological response to heightened levels of nitric oxide, which may in turn have led to a process of homeostatic evolution. [2] In addition, the heightened levels of nitric oxide that followed as an inevitable consequence of the loss of hemoglobin and myoglobin may have actually provided an automatic compensation, allowing for the fish to make up for the hit to their oxygen transport system and thereby providing a grace period of the fixation of these less than desirable traits.

Related Research Articles

<span class="mw-page-title-main">Hemoglobin</span> Metalloprotein that binds with oxygen

Hemoglobin is a protein containing iron that facilitates the transport of oxygen in red blood cells. Almost all vertebrates contain hemoglobin, with the exception of the fish family Channichthyidae and the tissues of some invertebrate animals. Hemoglobin in the blood carries oxygen from the respiratory organs to the other tissues of the body, where it releases the oxygen to enable aerobic respiration which powers the animal's metabolism. A healthy human has 12 to 20 grams of hemoglobin in every 100 mL of blood. Hemoglobin is a metalloprotein, a chromoprotein, and globulin.

<span class="mw-page-title-main">Myoglobin</span> Iron and oxygen-binding protein

Myoglobin is an iron- and oxygen-binding protein found in the cardiac and skeletal muscle tissue of vertebrates in general and in almost all mammals. Myoglobin is distantly related to hemoglobin. Compared to hemoglobin, myoglobin has a higher affinity for oxygen and does not have cooperative binding with oxygen like hemoglobin does. Myoglobin consists of non-polar amino acids at the core of the globulin, where the heme group is non-covalently bounded with the surrounding polypeptide of myoglobin. In humans, myoglobin is only found in the bloodstream after muscle injury.

<span class="mw-page-title-main">Hemoprotein</span> Protein containing a heme prosthetic group

A hemeprotein, or heme protein, is a protein that contains a heme prosthetic group. They are a very large class of metalloproteins. The heme group confers functionality, which can include oxygen carrying, oxygen reduction, electron transfer, and other processes. Heme is bound to the protein either covalently or noncovalently or both.

<span class="mw-page-title-main">Nototheniidae</span> Family of fishes

Nototheniidae, the notothens or cod icefishes, is a family of ray-finned fishes, part of the suborder Notothenioidei which is traditionally placed within the order Perciformes. They are largely found in the Southern Ocean.

<span class="mw-page-title-main">Notothenioidei</span> Suborder of fishes

Notothenioidei is one of 19 suborders of the order Perciformes. The group is found mainly in Antarctic and Subantarctic waters, with some species ranging north to southern Australia and southern South America. Notothenioids constitute approximately 90% of the fish biomass in the continental shelf waters surrounding Antarctica.

Icefish may mean:

<span class="mw-page-title-main">Iron in biology</span> Use of Iron by organisms

Iron is an important biological element. It is used in both the ubiquitous iron-sulfur proteins and in vertebrates it is used in hemoglobin which is essential for blood and oxygen transport.

<span class="mw-page-title-main">Nitric oxide dioxygenase</span>

Nitric oxide dioxygenase (EC 1.14.12.17) is an enzyme that catalyzes the conversion of nitric oxide (NO) to nitrate (NO−
3) . The net reaction for the reaction catalyzed by nitric oxide dioxygenase is shown below:

Champsocephalus esox, the pike icefish or northern icefish, is a species of marine ray-finned fish belonging to the family Channichthyidae, the crocodile icefishes.

<i>Chionodraco hamatus</i> Species of fish

Chionodraco hamatus is a species of marine ray-finned fish belonging to the family Channichthyidae, the crocodile icefishes. It is found in the Southern Ocean.

<span class="mw-page-title-main">Blackfin icefish</span> Species of fish

The blackfin icefish, also known as the Scotia Sea icefish, is a species of crocodile icefish belonging to the family Channichthyidae. The blackfin icefish belongs to Notothenioidei, a suborder of fishes that accounts for 90% of the fish fauna on the Antarctic continental shelf. Icefishes, also called white-blooded fishes, are a unique family in that they are the only known vertebrates to lack haemoglobin, making their blood oxygen carrying capacity just 10% that of other teleosts. Icefishes have translucent blood and creamy white gills.

<i>Channichthys</i> Genus of fishes

Channichthys is a genus of marine ray-finned fish belonging to the family Channichthyidae, the crocodile icefishes. They are native to the Southern Ocean.

<i>Chionodraco</i> Genus of fishes

Chionodraco is a genus of marine ray-finned fish belonging to the family Channichthyidae, the crocodile icefishes. They are found in the Southern Ocean.

<span class="mw-page-title-main">Jonah's icefish</span> Species of fish

Jonah's icefish is a benthopelagic species of marine ray-finned fish belonging to the family Channichthyidae, the crocodile icefishes. It is the only member of the monotypic genus Neopagetopsis. It is found in the Southern Ocean at depths of from 20 to 900 metres. It has a circum-Antarctic distribution on the continental slope and continental shelf, with the northernmost records from the South Shetland and the South Orkney Islands.

<i>Chionodraco rastrospinosus</i> Species of fish

The ocellated icefish is a fish of the family Channichthyidae. It lives in the cold waters off Antarctica and is known for having transparent haemoglobin-free blood.

Antarctic fish is a common name for a variety of fish that inhabit the Southern Ocean. There are relatively few families in this region, the most species-rich being the Liparidae (snailfishes), followed by Nototheniidae. The latter is one of eight different families that belong to the suborder Notothenioidei of the order Perciformes. They are also called notothenioids, but this name is also used to describe the other three, non-Antarctic families and some of the non-Antarctic genera in the mainly Antarctic families belonging to the suborder.

<i>Notothenia coriiceps</i> Species of fish

Notothenia coriiceps, also known as the black rockcod, Antarctic yellowbelly rockcod, or Antarctic bullhead notothen, is a species of marine ray-finned fish, belonging to the family Nototheniidae, the notothens or cod icefishes. It is widely spread around the Antarctic continent. Like other Antarctic notothenioid fishes, N. coriiceps evolved in the stable, ice-cold environment of the Southern Ocean. It is not currently targeted by commercial fisheries.

<i>Cryodraco antarcticus</i> Species of fish

Cryodraco antarcticus, the long-fingered icefish, is a demersal species of marine ray-finned fish belonging to the family Channichthyidae, the crocodile icefishes. It occurs only in deep waters of the Southern Ocean.

<i>Channichthys rhinoceratus</i> Species of fish

Channichthys rhinoceratus, the unicorn icefish, is a species of marine ray-finned fish belonging to the family Channichthyidae, the crocodile icefishes. It is endemic to the Kerguelen-Heard Plateau in the Southern Ocean. It is a demersal species living from surface waters to depths up to 750 m (2,460 ft). It is considered by some researchers as the only species in the genus Channichthys.

<i>Chionodraco myersi</i> Species of fish

Chionodraco myersi, the Myers's icefish, is a species of marine ray-finned fish belonging to the family Channichthyidae, the crocodile icefishes. It is found in the Southern Ocean.

References

  1. ↑ Richard van der Laan; William N. Eschmeyer & Ronald Fricke (2014). "Family-group names of Recent fishes". Zootaxa. 3882 (2): 001–230. doi: 10.11646/zootaxa.3882.1.1 . PMID   25543675.
  2. 1 2 3 4 5 6 7 8 9 10 11 12 13 Sidell, Bruce D; Kristin M O'Brien (2006-05-15). "When Bad Things Happen to Good Fish: The Loss of Hemoglobin and Myoglobin Expression in Antarctic Icefishes". Journal of Experimental Biology. 209 (10): 1791–1802. doi: 10.1242/jeb.02091 . ISSN   0022-0949. PMID   16651546.
  3. 1 2 3 4 Kock, KH (2005). "Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part I". Polar Biology. 28 (11): 862–895. doi:10.1007/s00300-005-0019-z. S2CID   12382710.
  4. ↑ Clarke, A (1990). Kerry, K. R; Hempel, G (eds.). Temperature and evolution: Southern Ocean cooling and the Antarctic marine fauna. pp. 9–22. doi:10.1007/978-3-642-84074-6. ISBN   978-3-642-84076-0. S2CID   32563062.{{cite book}}: |journal= ignored (help)
  5. ↑ Voskoboinikova, Olga (2002). "Early life history of two Channichthys species from the Kerguelen Islands, Antarctica (Pisces: Notothenioidei: Channichthyidae)". Zoosystematica Rossica. 10 (2): 407–412. doi:10.31610/zsr/2001.10.2.407. S2CID   252225313.
  6. ↑ Imbler, Sabrina (13 January 2022). "'Major Discovery' Beneath Antarctic Seas: A Giant Icefish Breeding Colony". The New York Times.
  7. ↑ Purser, Autun; Hehemann, Laura; Boehringer, Lilian; Tippenhauer, Sandra; Wege, Mia; Bornemann, Horst; Pineda-Metz, Santiago E.A.; Flintrop, Clara M.; Koch, Florian; Hellmer, Hartmut H.; Burkhardt-Holm, Patricia; Janout, Markus; Werner, Ellen; Glemser, Barbara; Balaguer, Jenna; Rogge, Andreas; Holtappels, Moritz; Wenzhoefer, Frank (2022). "A vast icefish breeding colony discovered in the Antarctic". Current Biology. 32 (4): 842–850.e4. doi: 10.1016/j.cub.2021.12.022 . hdl: 2263/90796 . PMID   35030328. S2CID   245936769.
  8. ↑ Froese, Rainer, and Daniel Pauly, eds. (2021). "Channichthyidae" in FishBase . June 2021 version.
  9. ↑ Eschmeyer, William N.; Fricke, Ron & van der Laan, Richard (eds.). "Genera in the family Channichthyidae". Catalog of Fishes . California Academy of Sciences . Retrieved 12 October 2021.
  10. ↑ LaMesa, Mario (2004). "The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review". Polar Biology. 27 (6): 321–338. doi:10.1007/s00300-004-0599-z. S2CID   36398753.
  11. ↑ Artigues, Bernat (2003). "Fish length-weight relationships in the Weddell Sea and Bransfield Strait". Polar Biology. 26 (7): 463–467. doi:10.1007/s00300-003-0505-0. S2CID   25224018.
  12. 1 2 Ruud, Johan T. (1954-05-08). "Vertebrates without Erythrocytes and Blood Pigment". Nature. 173 (4410): 848–850. Bibcode:1954Natur.173..848R. doi:10.1038/173848a0. PMID   13165664. S2CID   3261779.
  13. ↑ Cocca, E (1997). "Do the hemoglobinless icefishes have globin genes?". Comp. Biochem. Physiol. A. 118 (4): 1027–1030. doi:10.1016/s0300-9629(97)00010-8.
  14. ↑ Near, T. J.; Parker, S. K.; Detrich, H. W. (2006). "A genomic fossil reveals key steps in hemoglobin loss by the antarctic icefishes". Molecular Biology and Evolution. 23 (11): 2008–2016. doi: 10.1093/molbev/msl071 . PMID   16870682.
  15. ↑ Barber, D. L; J. E Mills Westermann; M. G White (1981-07-01). "The blood cells of the Antarctic icefish Chaenocephalus aceratus Lönnberg: light and electron microscopic observations". Journal of Fish Biology. 19 (1): 11–28. doi:10.1111/j.1095-8649.1981.tb05807.x. ISSN   1095-8649.
  16. ↑ Holeton, George (2015-10-15). "Oxygen uptake and circulation by a hemoglobinless Antarctic fish (Chaenocephalus aceratus Lonnberg) compared with three red-blooded Antarctic fish". Comparative Biochemistry and Physiology. 34 (2): 457–471. doi:10.1016/0010-406x(70)90185-4. PMID   5426570.
  17. 1 2 Sidell, B. D.; Vayda, M. E.; Small, D. J.; Moylan, T. J.; Londraville, R. L.; Yuan, M. L.; Rodnick, K. J.; Eppley, Z. A.; Costello, L.; et al. (1997). "Variable expression of myoglobin among the hemoglobinless antarctic icefishes". Proceedings of the National Academy of Sciences of the United States of America. 94 (7): 3420–3424. Bibcode:1997PNAS...94.3420S. doi: 10.1073/pnas.94.7.3420 . PMC   20385 . PMID   9096409.
  18. ↑ Grove, Theresa (2004). "Two species of Antarctic icefishes (Genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression". Polar Biology. 27 (10): 579–585. doi:10.1007/s00300-004-0634-0. S2CID   6394817.
  19. 1 2 3 Rankin, J.C; H Tuurala (January 1998). "Gills of Antarctic Fish". Comparative Biochemistry and Physiology A. 119 (1): 149–163. doi:10.1016/S1095-6433(97)00396-6. ISSN   1095-6433. PMID   11253779.
  20. ↑ Tota, Bruno; Raffaele Acierno; Claudio Agnisola; Bruno Tota; Raffaele Acierno; Claudio Agnisola (1991-06-29). "Mechanical Performance of the Isolated and Perfused Heart of the Haemoglobinless Antarctic Icefish Chionodraco Hamatus (Lonnberg): Effects of Loading Conditions and Temperature". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 332 (1264): 191–198. Bibcode:1991RSPTB.332..191T. doi:10.1098/rstb.1991.0049. ISSN   0962-8436.
  21. ↑ Urschel, M. R.; O'Brien, K. M. (2008-08-15). "High mitochondrial densities in the hearts of Antarctic icefishes are maintained by an increase in mitochondrial size rather than mitochondrial biogenesis". Journal of Experimental Biology. 211 (16): 2638–2646. doi: 10.1242/jeb.018598 . ISSN   0022-0949. PMID   18689417.
  22. ↑ Bargelloni, Luca; Babbucci, Massimiliano; Ferraresso, Serena; Papetti, Chiara; Vitulo, Nicola; Carraro, Roberta; Pauletto, Marianna; Santovito, Gianfranco; Lucassen, Magnus; Mark, Felix Christopher; Zane, Lorenzo (December 2019). "Draft genome assembly and transcriptome data of the icefish Chionodraco myersi reveal the key role of mitochondria for a life without hemoglobin at subzero temperatures". Communications Biology. 2 (1): 443. doi:10.1038/s42003-019-0685-y. ISSN   2399-3642. PMC   6884616 . PMID   31815198.
  23. ↑ Eastman, Joseph (1993). Antarctic Fish Biology: Evolution in a Unique Environment. San Diego, California: Academic Press, Inc.
  24. ↑ Corliss, Bruce A.; Delalio, Leon J.; Stevenson Keller, T. C.; Keller, Alexander S.; Keller, Douglas A.; Corliss, Bruce H.; Beers, Jody M.; Peirce, Shayn M.; Isakson, Brant E. (2019-11-12). "Vascular Expression of Hemoglobin Alpha in Antarctic Icefish Supports Iron Limitation as Novel Evolutionary Driver". Frontiers in Physiology. 10: 1389. doi: 10.3389/fphys.2019.01389 . ISSN   1664-042X. PMC   6861181 . PMID   31780954.
  25. ↑ Sedwick, P. N.; Marsay, C. M.; Sohst, B. M.; Aguilar-Islas, A. M.; Lohan, M. C.; Long, M. C.; Arrigo, K. R.; Dunbar, R. B.; Saito, M. A.; Smith, W. O.; DiTullio, G. R. (2011-12-15). "Early season depletion of dissolved iron in the Ross Sea polynya: Implications for iron dynamics on the Antarctic continental shelf". Journal of Geophysical Research. 116 (C12): C12019. Bibcode:2011JGRC..11612019S. doi: 10.1029/2010JC006553 . hdl: 1912/4994 . ISSN   0148-0227.
  26. ↑ Kennett, J. P. (1977). "Cenozoic evolution of Antarctic glaciation, the circus-Antarctic Ocean and their impact on global paleooceanography". Journal of Geophysical Research. 82 (27): 3843–3860. Bibcode:1977JGR....82.3843K. doi:10.1029/jc082i027p03843.
  27. 1 2 3 Corliss, Bruce A.; Delalio, Leon J.; Stevenson Keller, T. C.; Keller, Alexander S.; Keller, Douglas A.; Corliss, Bruce H.; Beers, Jody M.; Peirce, Shayn M.; Isakson, Brant E. (2019-11-12). "Vascular Expression of Hemoglobin Alpha in Antarctic Icefish Supports Iron Limitation as Novel Evolutionary Driver". Frontiers in Physiology. 10: 1389. doi: 10.3389/fphys.2019.01389 . ISSN   1664-042X. PMC   6861181 . PMID   31780954.
  28. ↑ Galbraith, Eric D.; Le Mézo, Priscilla; Solanes Hernandez, Gerard; Bianchi, Daniele; Kroodsma, David (2019). "Growth Limitation of Marine Fish by Low Iron Availability in the Open Ocean". Frontiers in Marine Science. 6. doi: 10.3389/fmars.2019.00509 . ISSN   2296-7745.
  29. ↑ Gardner, P. R. (2004). "Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin, and their associated reductases". Journal of Inorganic Biochemistry. 99 (1): 247–266. doi:10.1016/j.jinorgbio.2004.10.003. PMID   15598505.
  30. ↑ Pellegrino, D.; R. Acierno & B. Tota (2003). "Control of cardiovascular function in the icefish Chionodraco hamatus: involvement of serotonin and nitric oxide". Computational Biochemical Physiology. 134A (2): 471–480. doi:10.1016/s1095-6433(02)00324-0. PMID   12547277.
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