623:. 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. 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. 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. 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.
589:
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. 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. This finding suggests that fish without cardiac myoglobin have undergone compensatory adaptation.
598:
these waters, means oxygen availability in
Antarctic waters is unusually high. The loss of hemoglobin and myoglobin would have negative consequences in warmer environments. 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, some researchers have also suggested that the loss of hemoglobin might be tied to a necessary adaptation for the icefish. Most animals require iron for hemoglobin production, and iron is often limited in ocean environments. 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.
564:
proposed that the lack of hemoglobin, while not lethal, is not adaptive. 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. 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.
53:
31:
501:
513:
409:
607:
543:(ACC) is widely believed to mark the beginning of the evolution of Antarctic fish. 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.
483:, and the ventricle muscles are very spongy, enabling them to absorb oxygen directly from the blood they pump. Their hearts, large blood vessels and low-viscosity (RBC-free) blood are specialized to carry out very high flow rates at low pressures. This helps to reduce the problems caused by the lack of hemoglobin. In the past, their
487:
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. The little extra oxygen absorbed by the skin may play a part in supplementing the oxygen supply to the heart, which
453:
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
588:
Phylogenetic relationships indicate that the nonexpression of myoglobin in cardiac tissue has evolved at least four discrete times. 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
597:
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. These cold temperatures, which allow for higher water oxygen content, combined with a high degree of vertical mixing in
563:
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
618:
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
554:
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
896:
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;
567:
Recent research by
Corliss et al. (2019) claims that the loss of hemoglobin has adaptive value. Iron is a limiting nutrient in the environments inhabited by the icefish. By no longer synthesizing hemoglobin, they claim that icefish are minimizing endogenous iron use. To demonstrate this, they
1422:
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".
580:, 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.
531:
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.
196:
sectors of the
Southern Ocean, as well as the continental shelf waters surrounding Antarctica. Water temperatures in these regions remain relatively stable, generally ranging from −1.8 to 2 °C (28.8 to 35.6 °F). One icefish,
1515:
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).
436:. 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. One icefish species,
400:; 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.
528:
ancestor. 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.
488:
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
1744:
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).
1586:
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).
1207:
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".
1645:
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).
1242:
Holeton, George (2015-10-15). "Oxygen uptake and circulation by a hemoglobinless
Antarctic fish (Chaenocephalus aceratus Lonnberg) compared with three red-blooded Antarctic fish".
492:. This adaptation facilitates enhanced oxygen delivery by increasing mitochondrial surface area, and reducing distance between the extracellular area and the mitochondria.
293:
1518:"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"
1879:
Pellegrino, D.; R. Acierno & B. Tota (2003). "Control of cardiovascular function in the icefish Chionodraco hamatus: involvement of serotonin and nitric oxide".
479:), greater blood volumes (four-fold those of other fish), larger hearts, and greater cardiac outputs (five-fold greater) compared to other fish. Their hearts lack
1339:
Grove, Theresa (2004). "Two species of Antarctic icefishes (Genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression".
1468:"High mitochondrial densities in the hearts of Antarctic icefishes are maintained by an increase in mitochondrial size rather than mitochondrial biogenesis"
1280:
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).
984:
1844:
Gardner, P. R. (2004). "Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin, and their associated reductases".
2058:
345:
1917:
1704:
Kennett, J. P. (1977). "Cenozoic evolution of Antarctic glaciation, the circus-Antarctic Ocean and their impact on global paleooceanography".
208:
At least 16 species of crocodile icefish are currently recognized, although eight additional species have been proposed for the icefish genus
2084:
797:
Clarke, A. (1990). "Temperature and evolution: Southern Ocean cooling and the Antarctic marine fauna". In Kerry, K. R; Hempel, G (eds.).
1647:"Early season depletion of dissolved iron in the Ross Sea polynya: Implications for iron dynamics on the Antarctic continental shelf"
460:, the oxygen-binding protein used in muscles, is absent from all icefish skeletal muscles. In 10 species, myoglobin is found in the
2032:
225:
in Antarctica. The majority of nests were occupied by one adult fish guarding an approximated estimate of 1,735 eggs in each nest.
2071:
840:"Early life history of two Channichthys species from the Kerguelen Islands, Antarctica (Pisces: Notothenioidei: Channichthyidae)"
574:
and stained them to detect hemoglobin alpha 3'f. They found expression of hemoglobin alpha 3'f within the retinal vasculature of
432:
to lack hemoglobin as adults. Although they do not manufacture hemoglobin, remnants of hemoglobin genes can be found in their
814:
454:
decreases). However, the oxygen-carrying capacity of icefish blood is less than 10% that of their relatives with hemoglobin.
2076:
620:
418:
221:
icefish estimated to have 60 million active nests across an area of approximately 92 square miles at the bottom of the
1746:"Vascular Expression of Hemoglobin Alpha in Antarctic Icefish Supports Iron Limitation as Novel Evolutionary Driver"
1588:"Vascular Expression of Hemoglobin Alpha in Antarctic Icefish Supports Iron Limitation as Novel Evolutionary Driver"
2123:
2089:
428:
is colorless because it lacks hemoglobin, the oxygen-binding protein in blood. Channichthyidae are the only known
878:
994:
1015:
LaMesa, Mario (2004). "The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review".
1803:
Galbraith, Eric D.; Le Mézo, Priscilla; Solanes Hernandez, Gerard; Bianchi, Daniele; Kroodsma, David (2019).
708:"When Bad Things Happen to Good Fish: The Loss of Hemoglobin and Myoglobin Expression in Antarctic Icefishes"
540:
52:
960:
536:
243:
1922:
1993:
1980:
1998:
762:
Kock, KH (2005). "Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part I".
1050:
Artigues, Bernat (2003). "Fish length-weight relationships in the Weddell Sea and Bransfield Strait".
2128:
1971:
2151:
505:
413:
2115:
1933:
611:
375:
332:
129:
2110:
2063:
205:
2102:
2019:
1713:
1658:
1432:
1293:
1097:
980:
199:
475:
To compensate for the absence of hemoglobin, icefish have larger blood vessels (including
8:
517:
438:
289:
39:
1717:
1662:
1436:
1425:
Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences
1297:
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1985:
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47:
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2006:
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1189:
1113:
989:
942:
930:
863:
839:
810:
737:
729:
663:
641:
639:
524:
The icefish are considered a monophyletic group and likely descended from a sluggish
480:
465:
1857:
1071:
1036:
824:
783:
306:
1888:
1853:
1816:
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1388:
1360:
1348:
1311:
1301:
1251:
1216:
1179:
1148:
1125:
1105:
1088:
Ruud, Johan T. (1954-05-08). "Vertebrates without Erythrocytes and Blood Pigment".
1059:
1024:
920:
910:
851:
802:
771:
719:
653:
576:
570:
551:
350:
162:
1923:
HHMI video about the discovery and natural history of the icefish (requires FLASH)
1168:"A genomic fossil reveals key steps in hemoglobin loss by the antarctic icefishes"
2011:
855:
469:
397:
284:
264:
1956:
1286:
Proceedings of the National Academy of Sciences of the United States of America
1282:"Variable expression of myoglobin among the hemoglobinless antarctic icefishes"
555:
individuals. These conditions may have also allowed for the loss of myoglobin.
489:
446:
238:
189:
177:
114:
94:
1533:
1421:
1352:
1063:
1028:
915:
898:
806:
775:
658:
30:
2145:
1830:
1821:
1805:"Growth Limitation of Marine Fish by Low Iron Availability in the Open Ocean"
1804:
1771:
1762:
1690:
1613:
1604:
1541:
1493:
1452:
1400:
1228:
956:
733:
340:
233:
The following genera have been classified within the family Channichthyidae:
1725:
1184:
1167:
550:
period, a species crash in the Southern Ocean opened up wide range of empty
217:
In February 2021, scientists discovered and documented a breeding colony of
1900:
1865:
1789:
1631:
1559:
1501:
1444:
1408:
1306:
1193:
1117:
934:
879:"'Major Discovery' Beneath Antarctic Seas: A Giant Icefish Breeding Colony"
741:
667:
461:
274:
210:
193:
170:
1325:
1263:
535:
Although the evolution of icefish is still disputed, the formation of the
500:
2045:
1965:
1671:
1646:
476:
389:
319:
301:
251:
222:
188:
in their blood as adults. Icefish populations are known to reside in the
104:
1802:
1484:
1467:
1139:
Cocca, E (1997). "Do the hemoglobinless icefishes have globin genes?".
640:
Richard van der Laan; William N. Eschmeyer & Ronald Fricke (2014).
484:
472:
in icefish heart ventricles has occurred at least four separate times.
429:
360:
185:
181:
925:
724:
707:
512:
2050:
1681:
1206:
1109:
457:
327:
314:
64:
2037:
1927:
1743:
1585:
1950:
1918:
A story about the use of the crocodile icefish for medical research
1514:
965:
895:
547:
525:
84:
1379:
Rankin, J.C; H Tuurala (January 1998). "Gills of Antarctic Fish".
449:(RBCs) are usually absent, and if present, are rare and defunct.
408:
1878:
1644:
450:
443:
has a more complete, but still nonfunctional, hemoglobin gene.
433:
173:
74:
2024:
425:
393:
899:"A vast icefish breeding colony discovered in the Antarctic"
705:
606:
1574:
Antarctic Fish Biology: Evolution in a Unique Environment
979:
1279:
403:
1166:Near, T. J.; Parker, S. K.; Detrich, H. W. (2006).
1465:
983:; Fricke, Ron & van der Laan, Richard (eds.).
1165:
706:Sidell, Bruce D; Kristin M O'Brien (2006-05-15).
2143:
1378:
1843:
1703:
897:Holtappels, Moritz; Wenzhoefer, Frank (2022).
837:
619:also involved in the process of breaking down
184:. They are the only known vertebrates to lack
1576:. San Diego, California: Academic Press, Inc.
1466:Urschel, M. R.; O'Brien, K. M. (2008-08-15).
1374:
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697:
1043:
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1235:
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29:
1820:
1779:
1761:
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1670:
1621:
1603:
1549:
1483:
1381:Comparative Biochemistry and Physiology A
1332:
1315:
1305:
1183:
1132:
924:
914:
790:
723:
674:
657:
1415:
1078:
1049:
605:
511:
499:
407:
1244:Comparative Biochemistry and Physiology
1241:
955:
949:
592:
2144:
1014:
985:"Genera in the family Channichthyidae"
876:
796:
1932:
1931:
1739:
1737:
1735:
1338:
1275:
1273:
1138:
642:"Family-group names of Recent fishes"
558:
383:
1881:Computational Biochemical Physiology
1087:
761:
757:
755:
753:
751:
633:
583:
973:
877:Imbler, Sabrina (13 January 2022).
13:
1732:
1270:
1221:10.1111/j.1095-8649.1981.tb05807.x
404:Respiratory and circulatory system
14:
2163:
1911:
1846:Journal of Inorganic Biochemistry
748:
51:
1872:
1858:10.1016/j.jinorgbio.2004.10.003
1837:
1796:
1706:Journal of Geophysical Research
1697:
1651:Journal of Geophysical Research
1638:
1579:
1566:
1508:
1472:Journal of Experimental Biology
1459:
1172:Molecular Biology and Evolution
1159:
712:Journal of Experimental Biology
388:All icefish are believed to be
995:California Academy of Sciences
889:
870:
831:
1:
1893:10.1016/s1095-6433(02)00324-0
1393:10.1016/S1095-6433(97)00396-6
1153:10.1016/s0300-9629(97)00010-8
838:Voskoboinikova, Olga (2002).
626:
541:Antarctic Circumpolar Current
206:Antarctic Polar Frontal Zone.
1256:10.1016/0010-406x(70)90185-4
568:obtained retinal samples of
537:Antarctic Polar Frontal Zone
495:
204:is distributed north of the
7:
1809:Frontiers in Marine Science
144:
10:
2168:
856:10.31610/zsr/2001.10.2.407
1940:
1534:10.1038/s42003-019-0685-y
1353:10.1007/s00300-004-0634-0
1141:Comp. Biochem. Physiol. A
1064:10.1007/s00300-003-0505-0
1029:10.1007/s00300-004-0599-z
916:10.1016/j.cub.2021.12.022
807:10.1007/978-3-642-84074-6
776:10.1007/s00300-005-0019-z
659:10.11646/zootaxa.3882.1.1
602:Cardiovascular physiology
228:
142:
137:
48:Scientific classification
46:
37:
28:
23:
1822:10.3389/fmars.2019.00509
1763:10.3389/fphys.2019.01389
1605:10.3389/fphys.2019.01389
1572:Eastman, Joseph (1993).
961:"Family Channichthyidae"
959:; Pauly, Daniel (eds.).
396:. Icefish are typically
1750:Frontiers in Physiology
1726:10.1029/jc082i027p03843
1592:Frontiers in Physiology
1209:Journal of Fish Biology
577:Champsocephalus gunnari
571:Champsocephalus gunnari
506:Chaenocephalus aceratus
414:Champsocephalus gunnari
392:, but can also feed on
1522:Communications Biology
1445:10.1098/rstb.1991.0049
1307:10.1073/pnas.94.7.3420
844:Zoosystematica Rossica
615:
612:Pagetopsis macropterus
521:
509:
421:
2111:Paleobiology Database
1185:10.1093/molbev/msl071
981:Eschmeyer, William N.
609:
515:
503:
411:
1672:10.1029/2010JC006553
969:. June 2021 version.
799:Antarctic Ecosystems
593:Reason for trait fix
468:. Loss of myoglobin
419:Soviet postage stamp
200:Champsocephalus esox
1718:1977JGR....82.3843K
1663:2011JGRC..11612019S
1437:1991RSPTB.332..191T
1298:1997PNAS...94.3420S
1102:1954Natur.173..848R
518:Chaenodraco wilsoni
439:Neopagetopsis ionah
219:Neopagetopsis ionah
40:Chionodraco hamatus
1485:10.1242/jeb.018598
883:The New York Times
616:
559:Loss of hemoglobin
522:
510:
422:
384:Diet and body size
371:Pseudochaenichthys
159:white-blooded fish
2139:
2138:
2098:Open Tree of Life
1934:Taxon identifiers
1712:(27): 3843–3860.
1478:(16): 2638–2646.
1431:(1264): 191–198.
1178:(11): 2008–2016.
1096:(4410): 848–850.
990:Catalog of Fishes
909:(4): 842–850.e4.
816:978-3-642-84076-0
801:. pp. 9–22.
725:10.1242/jeb.02091
718:(10): 1791–1802.
584:Loss of myoglobin
481:coronary arteries
379:
366:
356:
336:
323:
310:
297:
280:
270:
260:
247:
155:crocodile icefish
151:
150:
133:
2159:
2132:
2131:
2119:
2118:
2106:
2105:
2093:
2092:
2080:
2079:
2067:
2066:
2054:
2053:
2041:
2040:
2028:
2027:
2015:
2014:
2002:
2001:
1989:
1988:
1976:
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1961:
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1929:
1928:
1905:
1904:
1876:
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1869:
1841:
1835:
1834:
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1794:
1793:
1783:
1765:
1741:
1730:
1729:
1701:
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1694:
1684:
1674:
1642:
1636:
1635:
1625:
1607:
1583:
1577:
1570:
1564:
1563:
1553:
1512:
1506:
1505:
1487:
1463:
1457:
1456:
1419:
1413:
1412:
1376:
1365:
1364:
1336:
1330:
1329:
1319:
1309:
1292:(7): 3420–3424.
1277:
1268:
1267:
1239:
1233:
1232:
1204:
1198:
1197:
1187:
1163:
1157:
1156:
1147:(4): 1027–1030.
1136:
1130:
1129:
1110:10.1038/173848a0
1085:
1076:
1075:
1047:
1041:
1040:
1012:
1006:
1005:
1003:
1001:
977:
971:
970:
953:
947:
946:
928:
918:
893:
887:
886:
874:
868:
867:
835:
829:
828:
794:
788:
787:
759:
746:
745:
727:
703:
672:
671:
661:
637:
398:ambush predators
374:
364:
354:
344:
331:
318:
305:
288:
279:Richardson, 1844
278:
268:
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16:Family of fishes
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1986:Channichthyidae
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1942:Channichthyidae
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1347:(10): 579–585.
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903:Current Biology
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638:
634:
629:
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595:
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546:During the mid-
539:(APFZ) and the
498:
470:gene expression
464:, specifically
447:Red blood cells
406:
386:
348:
285:Chionobathyscus
265:Champsocephalus
231:
167:Channichthyidae
127:
125:Channichthyidae
50:
17:
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1912:External links
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341:Neopagetopsis
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176:found in the
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1384:
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1344:
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1289:
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1247:
1243:
1237:
1215:(1): 11–28.
1212:
1208:
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1134:
1093:
1089:
1055:
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998:. Retrieved
988:
975:
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767:
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649:
645:
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621:nitric oxide
617:
610:
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587:
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569:
566:
562:
545:
534:
530:
523:
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504:
474:
462:heart muscle
456:
445:
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423:
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387:
369:
359:
339:
326:
313:
300:
283:
275:Channichthys
273:
263:
250:
237:
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218:
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211:Channichthys
209:
198:
171:notothenioid
166:
158:
154:
152:
143:
124:
38:
18:
2046:iNaturalist
1966:Wikispecies
477:capillaries
430:vertebrates
390:piscivorous
365:Regan, 1913
349: [
302:Chionodraco
252:Chaenodraco
223:Weddell Sea
161:comprise a
105:Perciformes
1528:(1): 443.
1000:12 October
926:2263/90796
627:References
466:ventricles
417:on a 1978
361:Pagetopsis
290:Andriashev
269:Gill, 1861
244:Richardson
186:hemoglobin
182:Antarctica
130:T. N. Gill
111:Suborder:
1831:2296-7745
1772:1664-042X
1691:0148-0227
1682:1912/4994
1614:1664-042X
1542:2399-3642
1494:0022-0949
1453:0962-8436
1401:1095-6433
1229:1095-8649
943:245936769
864:252225313
734:0022-0949
496:Evolution
485:scaleless
458:Myoglobin
328:Dacodraco
315:Cryodraco
71:Kingdom:
65:Eukaryota
2146:Category
1957:Q1412616
1951:Wikidata
1901:12547277
1866:15598505
1790:31780954
1756:: 1389.
1632:31780954
1598:: 1389.
1560:31815198
1502:18689417
1409:11253779
1194:16870682
1118:13165664
1072:25224018
1037:36398753
966:FishBase
935:35030328
825:32563062
784:12382710
742:16651546
668:25543675
548:Tertiary
526:demersal
424:Icefish
307:Lönnberg
190:Atlantic
145:see text
121:Family:
85:Chordata
81:Phylum:
75:Animalia
61:Domain:
24:Icefish
1781:6861181
1714:Bibcode
1659:Bibcode
1623:6861181
1551:6884616
1433:Bibcode
1361:6394817
1326:9096409
1294:Bibcode
1264:5426570
1126:3261779
1098:Bibcode
646:Zootaxa
346:Nybelin
294:Neyelov
180:around
138:Genera
101:Order:
91:Class:
2129:234518
2116:266365
2103:668238
2077:171119
2064:111258
1899:
1864:
1829:
1788:
1778:
1770:
1689:
1630:
1620:
1612:
1558:
1548:
1540:
1500:
1492:
1451:
1407:
1399:
1359:
1324:
1314:
1262:
1227:
1192:
1124:
1116:
1090:Nature
1070:
1035:
941:
933:
862:
823:
813:
782:
740:
732:
666:
552:niches
451:Oxygen
434:genome
378:, 1937
376:Norman
355:, 1947
335:, 1916
322:, 1900
309:, 1905
296:, 1978
292:&
259:, 1914
246:, 1844
229:Genera
194:Indian
163:family
132:, 1861
2124:WoRMS
2090:30806
2059:IRMNG
2051:51478
1999:59323
1357:S2CID
1317:20385
1122:S2CID
1068:S2CID
1033:S2CID
939:S2CID
860:S2CID
821:S2CID
780:S2CID
426:blood
394:krill
353:]
333:Waite
320:Dollo
257:Regan
169:) of
2085:NCBI
2072:ITIS
2038:4258
2033:GBIF
2025:5350
1994:BOLD
1897:PMID
1885:134A
1862:PMID
1827:ISSN
1786:PMID
1768:ISSN
1687:ISSN
1628:PMID
1610:ISSN
1556:PMID
1538:ISSN
1498:PMID
1490:ISSN
1449:ISSN
1405:PMID
1397:ISSN
1322:PMID
1260:PMID
1225:ISSN
1190:PMID
1114:PMID
1002:2021
931:PMID
811:ISBN
738:PMID
730:ISSN
664:PMID
650:3882
192:and
174:fish
153:The
2020:EoL
2012:7ZR
2007:CoL
1981:AFD
1889:doi
1854:doi
1817:doi
1776:PMC
1758:doi
1722:doi
1677:hdl
1667:doi
1655:116
1618:PMC
1600:doi
1546:PMC
1530:doi
1480:doi
1476:211
1441:doi
1429:332
1389:doi
1385:119
1349:doi
1312:PMC
1302:doi
1252:doi
1217:doi
1180:doi
1149:doi
1145:118
1106:doi
1094:173
1060:doi
1025:doi
921:hdl
911:doi
852:doi
803:doi
772:doi
720:doi
716:209
654:doi
157:or
2148::
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1996::
1983::
1968::
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165:(
Text is available under the Creative Commons Attribution-ShareAlike License. Additional terms may apply.