Mummichog

Mummichog
Scientific classification
Kingdom: Animalia
Phylum: Chordata
Class: Actinopterygii
Order: Cyprinodontiformes
Suborder: Cyprinodontoidei[2]
Family: Fundulidae
Genus: Fundulus
Species: F. heteroclitus
Binomial name
Fundulus heteroclitus
(Linnaeus, 1766)
Synonyms [3][4]
  • Cobitis heteroclita Linnaeus, 1766
  • Cobitis macrolepidota Walbaum, 1792
  • Esox pisciculus Mitchill, 1815
  • Esox pisculentus Mitchill, 1815
  • Fundulus antillarum Fowler, 1916
  • Fundulus badius Garman, 1895
  • Fundulus coenicolus (Bloch & Schneider, 1801)
  • Fundulus fasciatus (Bloch & Schneider, 1801)
  • Fundulus fonticola Valenciennes, 1846
  • Fundulus lozanoi (Gomez Caruana et al., 1984)
  • Fundulus nigrofaciatus (Lesueur, 1817)
  • Fundulus nisorius Cope, 1870
  • Fundulus ornatus (Lesueur, 1817)
  • Fundulus pisciculus (Mitchill, 1815)
  • Fundulus swampinus (Lacepède, 1803)
  • Fundulus vinctus Jordan & Gilbert, 1882
  • Fundulus viridescens DeKay, 1842
  • Fundulus zebra DeKay, 1842
  • Hydargira nigrofaciata Lesueur, 1817
  • Hydrargira ornata Lesueur, 1817
  • Hydrargira swampina Lacepède, 1803
  • Poecilia coenicola Bloch & Schneider, 1801
  • Poecilia fasciata Bloch & Schneider, 1801
  • Valencia lozanoi Gomez Caruana et al., 1984

The mummichog (Fundulus heteroclitus) is a small killifish found along the Atlantic coast of the United States and Canada. Also known as Atlantic killifish, mummies, gudgeons, and mud minnows, these fish inhabit brackish and coastal waters including estuaries and salt marshes. The species is noted for its hardiness and ability to tolerate highly variable salinity, temperature fluctuations from 6 to 35 °C (43 to 95 °F), very low oxygen levels (down to 1 mg/L), and heavily polluted ecosystems. As a result, the mummichog is a popular research subject in embryological, physiological, and toxicological studies. It is also the first fish ever sent to space, aboard Skylab in 1973.

Taxonomy

The genus name Fundulus comes from fundus, meaning bottom, from the fish's habit of swimming near muddy bottoms. The species name heteroclitus means irregular or unusual. The type specimen was first described by Carl Linnaeus in 1766, from near Charleston, South Carolina. Other scientific names now considered synonyms for this species include Cobitis heteroclita, Fundulus fasciatus, Fundulus pisculentus, and Fundulus nigrofasciatus.[5] The mummichog belongs to the order Cyprinodontiformes, and the family Fundulidae. There are two subspecies: F. h. heteroclitus (Linnaeus, 1766), in the south and F. h. macrolepidotus (Walbaum, 1792) in the north.

The name mummichog is derived from a Narragansett term which means "going in crowds", which reflects the mummichog's strong shoaling tendency.[6] Colloquial names include mummy, killie, salt water minnow, mud minnow, mud dabbler, marsh minnow, brackish water chub, gudgeon, and common killifish. Some of these terms may lead to confusion: the term minnow should be reserved for species of the Cyprinidae family, the mudminnows are members of the Umbridae family, and the name gudgeon is used for various bottom-dwelling species of cyprinid, eleotrid, and ptereleotrid fishes, none of which belongs to the same family as the fundulid mummichog.

Description

Mummichog at Saint Michaels, Chesapeake Bay, United States

The body of the mummichog is elongate but thick, with a deep caudal peduncle. Usual length is 7.5 to 9 cm (3.0 to 3.5 in) but maximum lengths of 13 to 15 cm (5.1 to 5.9 in) are possible. The mouth is upturned and the lower jaw protrudes when the mouth is closed. Pectoral and tail fins are round. Mummichogs have 10-13 dorsal fin rays, 9-12 anal fin rays, 16-20 pectoral fin rays. Males have larger dorsal and anal fins than females. There is no lateral line on the body, but lateral line pores are present on the head. The colour is variable (and may even change in shade within the same individual when placed near different backgrounds)[7][8] but is generally olive-brown or olive-green. There can be vertical bars on the sides that are thin, wavy, and silvery. Colors are more intense in males during the reproductive season, as they become dark olive-green on the back, steel-blue on the sides with about 15 silvery bars, and yellow or orange-yellow on the underside; the dorsal fin is mottled and a small eyespot may be present near the rear edge. Females tend to be paler, without bars or the intense yellow on the belly, and their dorsal fin is uniformly coloured.

Adults of the two subspecies can be distinguished based on slight morphological differences.[9] and genomic[10] Further, eggs of the northern subspecies have filaments (adhesive chorionic fibrils) that eggs of the southern subspecies lack. While the northern subspecies deposits eggs in the sand, the southern subspecies often deposits eggs inside empty mussel shells.[11][12]

The mummichog is very similar to the banded killifish, Fundulus diaphanus, and indeed the two species have been known to interbreed.[13] The two species may overlap in their choice of habitat, but in general the banded killifish is more commonly found in freshwater, which is not the case for the mummichog. The banded killifish tends to have thin dark bars on a light side, whereas in the mummichog the bars are thin and light on a dark side. Internally, the banded killifish has 4-7 gill rakers, as opposed to 8-12 in the mummichog.

Distribution and habitat

This species ranges along the Atlantic coast of North America, from Gaspé Peninsula, Anticosti Island and Port au Port Bay in the north to northeastern Florida in the south. It is present on Sable Island, 175 km (109 mi) southeast of the closest point of mainland Nova Scotia in the Atlantic Ocean.[14] The approximate geographical division between the two subspecies lies in New Jersey, Delaware and Virginia.

Introduced populations have become established on the Atlantic coast of Portugal and southwestern Spain, starting in the 1970s[15][16][17] and some have now reached the western Mediterranean basin.[18] There may also be introduced populations in Hawaii and the Philippines.[19] As bait fish, mummichogs are sometimes released in freshwater habitats, where they can survive, and there have been reports of individuals in New Hampshire ponds, as well as the upper Ohio River and Beaver River (Pennsylvania).[20]

The mummichog is a common fish in coastal habitats such as salt marshes, muddy creeks, tidal channels, brackish estuaries, eelgrass or cordgrass beds, and sheltered shorelines. It can be found within coastal rivers but seldom beyond the head of tide. A few landlocked populations may exist in freshwater lakes close to shore, for example on Digby Neck, Nova Scotia.[21]

Diet

Mummichogs are omnivorous. Analyses of their stomach contents have found diatoms, amphipods and other crustaceans, molluscs, fish eggs (including their own species), very small fish, insect larvae, and bits of eelgrass.

Physiology

This fish is well known for its ability to withstand a variety of environmental conditions.[22] They can survive temperatures between 6 and 35 °C (43–95 °F); even within the same tidal cycle they can tolerate rapid temperature changes from 15 to 30 °C (59–86 °F).[23] They are among fish species most tolerant of salinity changes (euryhaline).[24] Mummichog larvae can grow in salinities ranging from 0.4 to 100 parts per thousand, the latter being about three times the normal salinity of seawater. Adult mummichogs tolerate low oxygen levels down to 1 mg/L, at which they resort to aquatic surface respiration (breathing in the surface layer of water, richer in oxygen because of contact with air) to survive.[25][26] They can even survive for a few hours in moist air outside of water, breathing air directly.[27]

Populations have developed resistance to methylmercury, kepone, dioxins, polychlorinated biphenyl, and polyaromatic hydrocarbons.[28] One study[29] has looked at the genomic variation exhibited by mummichogs populations living in Newark Bay, New Bedford Harbor, and the Elizabeth River (Virginia) (in some areas heavily polluted with polychlorinated biphenyls and creosote, a complex mixture containing dioxin-like chemicals) and has found that about 20% of their genes were modified as compared to populations living in clean sites.

Behavior

Mummichogs live in dense shoals that can include several hundred individuals.

During cold winter months in the northern parts of their range, mummichogs move to upstream tidal pools, where they burrow into the mud at depths up to 20 cm (7.9 in) to overwinter.[30][31] They can also bury themselves in mud if they are caught in a drying tidal pool between spring tides. Alternatively, they can travel short distances on land to get back to the sea.[32]

In the laboratory, mummichogs have yielded clear examples of free-running circadian rhythms, in both body colour[33] and swimming activity.[34] For the latter, clear rhythms were obtained in single individuals as well as in groups of 5 or 25 individuals. Evidence of free-running semi-lunar rhythms have also been obtained in mummichogs: in constant laboratory conditions, egg production peaked every 14.8 days for up to 5 months.[35]

Reproduction

Spawning takes place from spring through fall. In the southern most populations, up to eight spawnings are possible in a season. Spawning takes place most often at high tide and when the moon is new or full. Maximal spawning occurs when high spring tides coincide with night,[36] though spawning during the day remains possible.

During courtship, males may pursue females, and females may attract males by turning on their sides near the bottom and flicking their tails. A male and female may swim together for a while, after which the male crowds the female against a rock or a plant and clasps her: the male's larger dorsal and anal fins curve around the female's body. Fingerlike projections that develop on the male's scales behind and below the dorsal fin may help the male maintain contact with the female. The pair quivers vigorously and eggs and sperm are released.[37]

The eggs are pale yellow, about 2 mm (0.08 in) in diameter, and strongly adhesive. During a spawning event, a female can deposit up to 740 eggs in separate clutches of 10 to 300 eggs at a time.[11] The eggs adhere to plants, algal mats, empty mussel shells, sand, or mud at sites that are reached by water only at high spring tides.[11] Eggs therefore develop while exposed to moist air, and they hatch when the next high spring tides reach them.[38][39][40] The eggs cannot hatch in air, nor can they do so in moving water; hatching is initiated by a lack of oxygen, something that can happen in the boundary layer of relatively still water surrounding the metabolically active egg at high tide, but not in air or in moving water.[41]

As opposed to their northern counterparts, the southern subspecies have eggs that lack filaments (adhesive chorionic fibrils)[42] and they often deposit those eggs inside empty mussel shells.[11][12] The two subspecies are also distinguished based on slight morphological[9] and genomic[10] differences.

Most mummichogs become sexually mature when two years old, around 3.8 cm (1.5 in) in length. Normal lifespan is four years.[11]

Parasites

Mummichogs are hosts to a parasitic fluke, Homalometron pallidum, which has a complex lifecycle involving the aquatic snail, Ecrobia truncata.[43] Other parasite species reported in mummichogs include 10 protozoans, eight trematodes, one nematode, two acanthocephalans, and two crustaceans.[44] A study in New Jersey found that mummichogs heavily infested with the digenean gill parasite Ascocotyle phagicola, spent more time near the surface and exhibited conspicuous behaviors such as jerking, an example of a parasite affecting the behavior of its host in a way beneficial to the parasite, as conspicuous behaviors near the surface make the fish more likely to be noticed by predatory wading birds, the next host in the parasite's life cycle.[45]

Interest to humans

Mummichogs are sold as bait in sport fisheries for marine species such as summer flounder and bluefish, or even sometimes for freshwater species.[23]

Mummichogs readily eat mosquito larvae and attempts have been made to use them as biocontrol agents of mosquito populations.[23]

Scientific Utility

Mummichogs are considered an important environmental model organism because of their ability to tolerate various extremes of chemical (pollution, etc.) and physical (temperature, salinity, oxygen, etc.) conditions. They are relatively abundant in nature and can be easily captured, transported and reared in laboratory facilities. They are commonly used in scientific studies of stress biology,[46] thermal physiology and toxicology, and have also been studied in the contexts of evolutionary biology, developmental biology, endocrinology, cancer biology, and chronobiology (study of circadian rhythms).[47][48] With the successful sequencing and assembly of the full killifish genome,[49] they serve as a premier scientific model for studying biochemical and physiological responses to varying environmental conditions.[50]

Their remarkable ability to tolerate various extremes of temperature and salinity has made them popular subjects in scientific studies of toxicology. For decades the killifish has been a useful laboratory model for toxicological studies that include exposures to single chemicals, chemical mixtures, and complex contaminated media. It is sometimes the only fish species found in severely polluted and oxygen-deprived waterways, such as the Elizabeth River in Virginia and, in New Jersey, the Hackensack River and the Arthur Kill. A 2008 Virginia Institute of Marine Science report stated that 38% of mummichogs from Elizabeth River had cancerous lesions, and "more than half had pre-cancerous lesions. That was largely due to high levels of polycyclic aromatic hydrocarbons".[51] Killifish eggs are used in developmental studies and when teaching embryology because the eyes, the beating heart, and the different stages of ontogenesis can be easily examined. Embryos are also extremely durable and easy to manipulate in the laboratory.

Mummichogs were the first fish sent to space.[52] In 1973 a couple of them were flown in a plastic bag aquarium aboard Skylab, during the Skylab 3 mission. In the absence of gravity the fish at first exhibited an unusual swimming behavior: they constantly pitched forward and therefore described tight circles. However, by day 22 of the mission they swam normally. Fifty eggs at an advanced stage of development had also been taken on board, and 48 of them hatched during the flight. The hatchlings swam normally.[53] More experiments with mummichogs in space followed as part of the Apollo-Soyuz Test Project[54] and as part of a biological package aboard the Bion 3 satellite.

References

  1. ↑ NatureServe (2013). "Fundulus heteroclitus". IUCN Red List of Threatened Species. Version 2014.3. International Union for Conservation of Nature. Retrieved March 12, 2015.
  2. ↑ http://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&search_value=165647
  3. ↑ Nicolas Bailly (2014). Nicolas Bailly, eds. "Fundulus heteroclitus heteroclitus (Linnaeus, 1766)". FishBase. World Register of Marine Species. Retrieved March 12, 2015.
  4. ↑ Nicolas Bailly (2014). Nicolas Bailly, eds. "Fundulus heteroclitus macrolepidotus (Walbaum, 1792)". FishBase. World Register of Marine Species. Retrieved March 12, 2015.
  5. ↑ Scott, W.B., and Crossman, E.J. 1973. Freshwater fishes of Canada. Bulletin 184 of the Fisheries Research Board of Canada, Ottawa.
  6. ↑ "Mummichog." Merriam-Webster.com. Merriam-Webster, n.d. Web. 6 February 2014. <http://www.merriam-webster.com/dictionary/mummichog>
  7. ↑ Connolly, C.J. 1925. Adaptive changes in shades and color of Fundulus. Biological Bulletin (Woods Hole) 48: 56-77.
  8. ↑ Bagnara, J.T., and Hadley, M.E. 1973. Chromatophores and color change. Prentice-Hall, New Jersey.
  9. 1 2 Able, K.W.; Felley, J.D. (1986). "Geographical variation in Fundulus heteroclitus: tests for concordance between egg and adult morphologies". American Zoologist. 26: 145–157. doi:10.1093/icb/26.1.145.
  10. 1 2 Brown, B.L.; Chapman, R.W. (1991). "Gene flow and mitochondrial DNA variation in the killifish, Fundulus heteroclitus". Evolution. 45: 1147–1161. doi:10.2307/2409722.
  11. 1 2 3 4 5 Coad, B.W. 1995. Encyclopedia of Canadian Fishes. Canadian Museum of Nature, Ottawa, 928p.
  12. 1 2 Taylor, M.H. (1986). "Environmental and endocrine influences on reproduction of Fundulus heteroclitus". American Zoologist. 26: 159–171. doi:10.1093/icb/26.1.159.
  13. ↑ Hubbs, C.L., Walker, B.W., and Johnson, R.E. 1943. Hybridization in nature between species of American cyprinodont fishes. Contributions to the Laboratory of Vertebrate Biology of the University of Michigan 23: 21 p.
  14. ↑ Garside, E.T. (1969). "Distribution of insular fishes of Sable Island, Nova Scotia". Journal of the Fisheries Research Board of Canada. 26: 1390–1392. doi:10.1139/f69-126.
  15. ↑ Hernando, J.A., 1975. Nuevas localidades de Valencia hispanica (Pisces: Ciprinodontidae) en el Suroeste de España. Doñana Acta Vertebrata 2: 265-267.
  16. ↑ Coelho, M.; Gomes, J.; Ré, P.B. (1976). "Valencia hispanica, a new fish to Portugal". Arquivos do Museu Bocage. 6: 1–3.
  17. ↑ Gutiérrez-Estrada, J.C.; Prenda, J.; Oliva, F; Fernandez-Delgado, C. (1998). "Distribution and habitat preferences of the introduced mummichog Fundulus heteroclitus (Linneaus) [sic] in South-western Spain". Estuarine Coastal and Shelf Science. 46: 827–835. doi:10.1006/ecss.1997.0318.
  18. ↑ Gisbert, E.; Lopez, M.A. (2007). "First record of a population of the exotic mummichog, Fundulus heteroclitus (L., 1766) in the Mediterranean Sea basin (Ebro River delta)". Journal of Fish Biology. 71: 1220–1224. doi:10.1111/j.1095-8649.2007.01579.x.
  19. ↑ Fish Base Mummichog distribution
  20. ↑ USGS Nonindigenous aquatic species database Mummichog occurrences
  21. ↑ Klawe, W.L. (1957). "Common mummichog and newt in a lake on Digby Neck, Nova Scotia". Canadian Field-Naturalist. 71: 154–155.
  22. ↑ Burnett, K.G.; Bain, L.J.; Baldwin, D.S.; et al. (2007). "Fundulus as the premier teleost model in environmental biology: Opportunities for new insights using genomics". Comparative Biochemistry and Physiology D. 2: 257–266. doi:10.1016/j.cbd.2007.09.001.
  23. 1 2 3 Abraham, B.J. 1985. Species Profiles: Life histories and environmental requirements of coastal fishes and invertebrates (Mid-Atlantic)--mummichog and striped killifish. U.S. Fish and Wildlife Service Biological Reports 82 (11.40): 23 p. http://www.nwrc.usgs.gov/wdb/pub/species_profiles/82_11-040.pdf
  24. ↑ Whitehead, A (2010). "The evolutionary radiation of diverse osmotolerant physiologies in killifish (Fundulus sp.)". Evolution. 64: 2070–2085. PMID 20100216. doi:10.1111/j.1558-5646.2010.00957.x.
  25. ↑ Wannamaker, C.M.; Rice, J.A. (2000). "Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States". Journal of Experimental Marine Biology and Ecology. 249: 145–163. doi:10.1016/s0022-0981(00)00160-x.
  26. ↑ Stierhoff, K.L.; Targett, T.E.; Grecay, P.A. (2003). "Hypoxia tolerance of the mummichog: the role of access to the water surface". Journal of Fish Biology. 63: 580–592. doi:10.1046/j.1095-8649.2003.00172.x.
  27. ↑ Halpin, P.M.; Martin, K.L.M. (1999). "Aerial respiration in the salt marsh fish Fundulus heteroclitus (Fundulidae)". Copeia. 1999: 743–748. doi:10.2307/1447607.
  28. ↑ Weis, J (2002). "Tolerance to environmental contaminants in the mummichog, Fundulus heteroclitus". Human and Ecological Risk Assessment. 8: 933–953. doi:10.1080/1080-700291905756.
  29. ↑ Whitehead, A.; Galvez, F.; Zhang, S.; Williams, L.M.; Oleksiak, M.F. (2011). "Functional genomics of physiological plasticity and local adaptation in killifish". Journal of Heredity. 102 (5): 499–511. PMC 3156563 Freely accessible. PMID 20581107. doi:10.1093/jhered/esq077.
  30. ↑ Chidester, F.E. (1920). "The behavior of Fundulus heteroclitus in the salt marshes of New Jersey". American Naturalist. 54: 244–245. doi:10.1086/279787.
  31. ↑ Raposa, K (2003). "Overwintering habitat selection by the mummichog, Fundulus heteroclitus, in a Cape Cod (USA) salt marsh". Wetlands Ecology and Management. 11: 175–182.
  32. ↑ Mast, S. O. (1915). "The behavior of Fundulus, with especial reference to overland escape from tide-pools and locomotion on land". Journal of Animal Behavior. 5: 341–350. doi:10.1037/h0075747.
  33. ↑ Kavaliers, M.; Abbott, F.S. (1977). "Rhythmic colour change of the killifish, Fundulus heteroclitus". Canadian Journal of Zoology. 55: 553–561. doi:10.1139/z77-070.
  34. ↑ Kavaliers, M. (1980). "Social groupings and circadian activity of the killifish, Fundulus heteroclitus". Biological Bulletin. 158: 69–76. doi:10.2307/1540759.
  35. ↑ Hsiao, S.-M.; Meier, A.H. (1989). "Comparison of semilunar cycles of spawning activity in Fundulus grandis and F. heteroclitus held under constant laboratory conditions". Journal of Experimental Zoology. 252: 213–218. doi:10.1002/jez.1402520302.
  36. ↑ Taylor, M.H.; Leach, G.J.; DiMichele, L.; Levithan, W.H.; Jacob, W.F. (1979). "Lunar spawning cycle in the mummichog, Fundulus Heteroclitus (Pisces: Cyprinodontidae)". Copeia. 1979: 291–297. doi:10.2307/1443417.
  37. ↑ Newman, H.H. (1907). "Spawning behavior and sexual dimorphism in Fundulus heteroclitus and allied fish". Biological Bulletin (Woods Hole). 12: 314–345. doi:10.2307/1535681.
  38. ↑ Taylor, M.H., DiMichele, L., and Leach, G.J. 1977. Egg stranding in the life cycle of the mummichog Fundulus heteroclitus. Copeia: 1977: 397-399.
  39. ↑ Taylor, M.H.; DiMichele, L. (1983). "Spawning site utilization in a Delaware population of Fundulus heteroclitus (Pisces: Cyprinodontidae)". Copeia. 1983: 719–725. doi:10.2307/1444338.
  40. ↑ Taylor, M.H. (1999). "A suite of adaptations for intertidal spawning". American Zoologist. 39: 313–320. doi:10.1093/icb/39.2.313.
  41. ↑ DiMichele, L.; Powers, D.A. (1984). "The relationship between oxygen consumption rate and hatching in Fundulus heteroclitus". Physiological Zoology. 57: 46–51. doi:10.1086/physzool.57.1.30155966.
  42. ↑ Morin, R.P.; Able, K.W. (1983). "Patterns of geographic variation in the egg morphology of the fundulid fish, Fundulus heteroclitus". Copeia. 1983: 726–740. doi:10.2307/1444339.
  43. ↑ Stunkard, Horace W. (1964). "The morphology, life history and systematics of the digenetic trematode Homalometron pallidum Stafford 1904" (PDF). The Biological Bulletin. 126 (1): 163–173. doi:10.2307/1539426.
  44. ↑ Hoffman, G.L. 1967. Parasites of North American freshwater fishes. University of California Press, Berkeley, 486 pp.
  45. ↑ Santiago Bass, C.; Weis, J.S. (2009). "Conspicuous behaviour of Fundulus heteroclitus associated with high digenean metacercariae gill abundances". Journal of Fish Biology. 74: 763–772. doi:10.1111/j.1095-8649.2008.02148.x.
  46. ↑ Schulte, Patricia M (2014). "What is environmental stress? Insights from fish living in a variable environment". Journal of Experimental Biology. 217: 23–34. PMID 24353201. doi:10.1242/jeb.089722.
  47. ↑ Kavaliers, M (1980). "Social groupings and circadian activity of the killifish, Fundulus heteroclitus". Biological Bulletin. 158: 69–76. doi:10.2307/1540759.
  48. ↑ Kavaliers, M.; Abbott, F.S. (1977). "Rhythmic colour change of the killifish, Fundulus heteroclitus". Canadian Journal of Zoology. 55: 553–561. doi:10.1139/z77-070.
  49. ↑ http://www.ncbi.nlm.nih.gov/genome/
  50. ↑ Lister, AL; Van Der Kraak, GJ; Rutherford, R; MacLatchy, D (2011). "Fundulus heteroclitus: ovarian reproductive physiology and the impact of environmental contaminants". Comparative Biochemistry and Physiology C. 154 (4): 278–287. doi:10.1016/j.cbpc.2011.07.004.
  51. ↑ Rona Kobell Elizabeth River rises from the depths.Dedicated group is slowly bringing one of nation's most polluted rivers back to life. Bay Journal, July 01, 2011
  52. ↑ Reebs, S.G. (2009) Fish in space Retrieved 12 December 2014.
  53. ↑ Von Baumgarten, R.J.; Simmonds, R.C.; Boyd, J.F.; Garriott, O.K. (1975). "Effects of prolonged weightlessness on the swimming pattern of fish aboard Skylab 3". Aviation, Space, and Environmental Medicine. 46: 902–906.
  54. ↑ Hoffman, R.B.; Salinas, G.A.; Baky, A.A. (1977). "Behavioral analyses of killifish exposed to weightlessness in the Apollo-Soyuz test project". Aviation, Space, and Environmental Medicine. 48: 712–717.
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