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Embryonic development and larval behavior of the kissing loach (Parabotia curta): adaptations to an ephemeral, hypoxic environment

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Abstract

Many teleost fishes in lowland fresh waters spawn in ephemeral flooded areas, the bottoms of which are prone to hypoxia. Little is known about how embryos and larvae deal with these potentially hostile environments. This study examines the functional and behavioral ontogeny of one such species, the kissing loach (Parabotia curta). Kissing loach eggs are demersal and adhesive. Hatching occurs at 24.8 ± 0.1 h post-fertilization at 25°C, much earlier than most fish species. The newly hatched larvae are precocious with no functional mouth, fins or eye pigmentation. Swimbladder inflation normally occurs at about 4 days posthatch, even before which the hatched larvae moved immediately toward the water surface to hang from water moss. Experiments with larvae 20 h after hatching showed that they spent significantly less time on the bottom in hypoxic water (2 mg/l) than in normoxic water, and suggest that hypoxia is a major directive factor in eliciting surfacing behavior. For the kissing loach, we have previously reported short-term spawning after the formation of flood areas as well as wide scattering of the spawned eggs in the temporal flooded areas. These traits with the present results of hatching at an early stage and the immediate upward movement of larvae are considered to be effective strategies for using ephemeral, hypoxic flooded areas for reproduction.

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References

  • Abe T, Iwata A (2007) Ayumodoki (Leptobotia curta), conservation of reproductive areas as the crux of their existence. Jpn J Ichthyol 54:234–238

    Google Scholar 

  • Abe T, Kobayashi I, Kon M, Sakamoto T (2007a) Spawning behavior of the kissing loach (Leptobotia curta) in temporary waters. Zool Sci 24:850–853

    Article  PubMed  Google Scholar 

  • Abe T, Kobayashi I, Kon M, Sakamoto T (2007b) Spawning of the kissing loach (Leptobotia curta) is limited to periods following the formation of temporary waters. Zool Sci 24:922–926

    Article  PubMed  Google Scholar 

  • Ali AB (1993) Aspects of the fecundity of the feral catfish, Clarias macrocephalus (Gunther), population obtained from the rice fields used for rice-fish farming, in Malaysia. Hydrobiologia 254:81–89

    Article  Google Scholar 

  • Anjos MB, De Oliveira RR, Zuanon J (2008) Hypoxic environments as refuge against predatory fish in the Amazonian floodplains. Braz J Biol 68:45–50

    Article  PubMed  CAS  Google Scholar 

  • Balon EK (1975) Reproductive guilds of fishes: a proposal and definition. J Fish Res Board Can 32:821–864

    Article  Google Scholar 

  • Bhimachar BS, David A (1945) On the occurence of ‘external’ gills in the loach—Lepidocephalus thermalis (C.V.). Curr Sci 14:74

    Google Scholar 

  • Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145–170

    Article  PubMed  CAS  Google Scholar 

  • Bohlen J (2003) Temperature and oxygen requirements of the endangered spined loach, Cobitis taenia L. (Teleostei, Cobitidae) and implications for the management of natural populations. Arch Hydrobiol 157:195–212

    Article  Google Scholar 

  • Brunelli E, Perrotta E, Tripepi S (2004) Ultrastructure and development of the gills in Rana dalmatina (Amphibia, Anura). Zoomorphology 123:203–211

    Article  Google Scholar 

  • Carlson AR, Siefert RE, Herman LJ (1974) Effects of lower dissolved oxygen concentration on channel catfish (Ictalurus punctatus) embryos and larvae. Trans Am Fish Soc 103:623–626

    Article  Google Scholar 

  • Fontenot QC, Rutherford DA, Kelso WE (2001) Effects of Environmental hypoxia associated with the annual flood pulse on the distribution of larval sunfish and shad in the Atchafalaya River Basin, Louisiana. Trans Am Fish Soc 130:107–116

    Article  Google Scholar 

  • Gracey AY, Troll JV, Somero GN (2001) Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci USA 98:1993–1998

    Article  PubMed  CAS  Google Scholar 

  • Hassell HL, Coutin PC, Nugegoda D (2008) Hypoxia impairs embryo development and survival in black bream (Acanthopagrus butcheri). Mar Pollut Bull 57:302–306

    Article  PubMed  CAS  Google Scholar 

  • Hosoya K (2000) Cobitis sp. 2 subsp. 1. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, 2nd edn. Tokai University Press, Tokyo, p 275

    Google Scholar 

  • Humphries P, King AJ, Koehn JD (1999) Fish, flows and floodplains: links between freshwater fishes and their environment in the Murray-Darling River system, Australia. Environ Biol Fish 56:129–151

    Article  Google Scholar 

  • Iwamatsu T (2004) Stages of normal development in the medaka Oryzias latipes. Mech Dev 121:605–618

    Article  PubMed  CAS  Google Scholar 

  • Junk WJ, Soares MGM, Carvalho FM (1983) Distribution on fish species in a lake of Amazon River floodplain near Manaus (Lago Camaleão), with special reference to extreme oxygen conditions. Amazoniana 7:397–431

    Google Scholar 

  • Kamler E (1992) Early life history of fishes: an energetics approach. Chapman & Hall, London

    Google Scholar 

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310

    Article  PubMed  CAS  Google Scholar 

  • King AJ, Humphries P, Lake PS (2003) Fish recruitment on floodplains: the roles of patterns of flooding and life history characteristics. Can J Fish Aquat Sci 60:773–786

    Article  Google Scholar 

  • Lelek A (1987) Misgurnus fossilis (Linnaeus, 1758). In: European Committee for the Conservation of Nature and Natural Resources (ed) The freshwater fishes of Europe, vol 9. Threatened fishes of Europe. Aula-Verlag, Wiesbaden, pp 253–255

  • Lucas MC, Baras E (2001) Migration of freshwater fishes. Blackwell Science, Oxford

    Book  Google Scholar 

  • Maehata M (2001) Hemigrammocypris rasborella. In: Kawanabe H, Mizuno N, Hosoya K (eds) Freshwater fishes of Japan. YAMA-KEI Publishers, Tokyo, pp 256–257

    Google Scholar 

  • Maehata M (2003) Leptobotia curta. In: Ministry of the Environment (ed) Threatened wildlife of Japan, red data book 2nd edn. Vol 4, Pisces—brackish and fresh water fishes. Japan Wildlife Research Center, Tokyo, pp 48–49

  • Maehata M (2007) Reproductive ecology of the Far Eastern catfish, Silurus asotus (Siluridae), with a comparison to its two congeners in Lake Biwa, Japan. Environ Biol Fish 78:135–146

    Article  Google Scholar 

  • Matsuda S (1971) Artificial breeding and care of ayumodoki (Leptobotia curta) at the aquarium in Shiga Prefectural Biwako Cultural Hall. J Jpn Assoc Zool Aqua 13:42–44

    Google Scholar 

  • McNeil DG, Closs GP (2007) Behavioural responses of a south-east Australian floodplain fish community to gradual hypoxia. Freshw Biol 52:412–420

    Article  CAS  Google Scholar 

  • Nakamura M (1969) Cyprinid fishes of Japan. Studies on the life history of cyprinid fishes of Japan. Research Institute for Natural Resources, Tokyo

    Google Scholar 

  • Nakamura M, Motonobu T (1971) Life history of the cobitid fish Leptobotia curta (Temminck et Schlegel). Misc Rep Res Inst Nat Resour 75:8–15

    Google Scholar 

  • Paugy D (2002) Reproductive strategies of fishes in a tropical temporary stream of the Upper Senegal basin: Baoulé River in Mali. Aquat Living Resour 15:25–35

    Article  Google Scholar 

  • Rombough PJ (1988) Respiratory gas exchange, aerobic metabolism and effects of hypoxia during early life. In: Hoar WS, Randall DJ (eds) Fish physiology, vol volume 11. Academic Press, New York, pp 59–161

    Google Scholar 

  • Sado T, Kimura S (2005) Developmental morphology of the cyprinid fish Chela dadiburjori. Ichthyol Res 52:20–26

    Article  Google Scholar 

  • Shimizu T, Sakai H, Mizuno N (1998) Embryonic and larval development of a Japanese spinous loach, Cobitis takatsuensis. Ichthyol Res 45:377–384

    Article  Google Scholar 

  • Soares MGM, Menezes NA, Junk WJ (2006) Adaptations of fish species to oxygen depletion in a central Amazonian floodplain lake. Hydrobiologia 568:353–367

    Article  Google Scholar 

  • Suguro N (2002) Early rearing conditions of Hotoke loach, Lefua echigonia. Suisanzoshoku 50:55–62

    Google Scholar 

  • Turner TF, Trexler JC, Miller GL, Toyer KE (1994) Temporal and spatial dynamics of larval and juvenile fish abundance in a temperate floodplain river. Copeia 1994:174–183

    Article  Google Scholar 

  • Warkentin KM (2000) Environmental and developmental effects on external gill loss in red-eyed tree frog, Agalychnis callidryas. Physiol Biochem Zool 73:557–565

    Article  PubMed  CAS  Google Scholar 

  • Warkentin KM (2007) Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching. Comp Biochem Physiol A 148:720–731

    Article  Google Scholar 

  • Watanabe M, Kobori N, Matsumoto A (1948) On the development of the Japanese loach. Collect Breed 10:72–75

    Google Scholar 

  • Watanabe K, Abe T, Iwata A (2009) Phylogenetic position and generic status of the Japanese botiid loach. Ichthyol Res 56:421–425

    Article  Google Scholar 

  • Williams DD, Coad BW (1979) The ecology of temporary streams III. Temporary stream fishes in Southern Ontario, Canada. Int Revue ges Hydrobiol 64:501–515

    Article  Google Scholar 

  • Wolf NG, Kramer DL (1987) Use of cover and the need to breath: the effects of hypoxia on vulnerability of dwarf gouramis to predatory snakeheads. Oecologia 73:127–132

    Article  Google Scholar 

  • Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45

    Article  PubMed  CAS  Google Scholar 

  • Yuma M, Hosoya K, Nagata Y (1998) Distribution of the freshwater fishes of Japan: an historical overview. Environ Biol Fish 52:97–124

    Article  Google Scholar 

Download references

Acknowledgments

We are especially grateful to Dr. Masayoshi Maehata, Lake Biwa Museum, for his guidance on the artificial breeding of kissing loach. We thank Mr. Ichiro Kobayashi, Mr. Yoshiaki Okamoto, Mr. Yusuke Kashiwa, Mr. Yoshio Kanou, Ms. Maria Abe and the members of Okayama Freshwater Fish Society for their assistance during the course of this study. We also thank Dr. Takaaki Shimizu, Ehime Prefectural Chuyo Fisheries Experimental Station, and Mr. Ryota Kawanishi, Graduate School of Science and Engineering, Ehime University, for their helpful information on the loaches. I am grateful to Dr. Katsutoshi Watanabe, Division of Biological Science, Graduate School of Science, Kyoto University, for helpful suggestions for this study. This study was supported by the Japan Society for the Promotion of Science: Grant nos. 204924 (T.A.), 19570057 and 22570065 (T.S.), the municipal offices of Seto and Okayama, and Kirin Brewery Co. Ltd. (Okayama Brewery). T.A. was supported by research fellowships from the Japan Society for the Promotion of Science for young scientists.

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  1. Tsukasa Abe

    Present address: LAGO Co., Ltd, 396-2 Taga, Omihachiman, 523-0821, Japan

Authors and Affiliations

  1. Ushimado Marine Laboratory, Graduate School of Natural Science and Technology, Okayama University, 130-17 Kashino, Ushimado, Setouchi, 701-4303, Japan

    Tsukasa Abe & Tatsuya Sakamoto

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  1. Tsukasa Abe
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  2. Tatsuya Sakamoto
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Correspondence to Tsukasa Abe.

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Abe, T., Sakamoto, T. Embryonic development and larval behavior of the kissing loach (Parabotia curta): adaptations to an ephemeral, hypoxic environment. Ichthyol Res 58, 238–244 (2011). https://doi.org/10.1007/s10228-011-0217-3

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  • DOI: https://doi.org/10.1007/s10228-011-0217-3

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