Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Comparative larval development of three amphidromous Rhinogobius species, making reference to their habitat preferences and migration biology

Masashi Kondo A E , Ken Maeda B , Kentarou Hirashima C and Katsunori Tachihara D
+ Author Affiliations
- Author Affiliations

A Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan.

B Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna, Okinawa 904-0495, Japan.

C Wakayama Prefectural Museum of Natural History, 370-1 Funao, Kainan, Wakayama 642-0001, Japan.

D Laboratory of Fisheries Biology and Coral Reef Studies, Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan.

E Corresponding author. Email: mimizu5b@yahoo.co.jp

Marine and Freshwater Research 64(3) 249-266 https://doi.org/10.1071/MF12234
Submitted: 28 August 2012  Accepted: 3 December 2012   Published: 18 March 2013

Abstract

Eggs and larvae of three amphidromous species of Rhinogobius goby (Rhinogobius brunneus, Rhinogobius sp. MO and Rhinogobius sp. CB) from Okinawa Island, Japan, were reared under uniform conditions to describe and compare their larval development. Although the larval morphologies of the three species were very similar, some differences were observed in the timing of ontogenetic events among them. R. brunneus had the largest yolk and saved it for a longer period of time, whereas Rhinogobius sp. MO had the smallest yolk, which was exhausted earlier. The period until yolk exhaustion is thought to restrict the distance that migrating larvae can drift, which determines the specific adult distribution. Each of these two amphidromous species are close relatives of different fluvial resident species. Evolution of the fluvial residents could be explained by different scenarios based on the larval traits of R. brunneus and Rhinogobius sp. MO. Rhinogobius sp. CB hatched at a smaller size and grew slower than the other two species. No fluvial species have derived from Rhinogobius sp. CB. One possible explanation is that the smaller and slower-growing larvae of Rhinogobius sp. CB find it more difficult to remain within streams.

Additional keywords: egg size, Gobiidae, Gobioidei, insular stream, pool, Ryukyu Archipelago, speciation, waterfall.


References

Akihito, S. K., Ikeda, Y., and Sugiyama, K. (2002). Rhinogobius. In ‘Fishes of Japan with Pictorial Keys to the Species’. English edn. (Ed. T. Nakabo.) pp. 1251–1255. (Tokai University Press: Tokyo.)

Benzie, V. (1968). Some ecological aspects of the spawning behaviour and early development of the common whitebait, Galaxias maculatus attenuatus (Jenyns). Proceedings of the New Zealand Ecological Society 15, 31–39.

Goto, A. (1986). Movement and population size of the river sculpin Cottus hangiongensis in the Daitobetsu River of southern Hokkaido. Japanese Journal of Ichthyology 32, 421–430.

Goto, A. (1988). Reproductive behavior and homing after downstream spawning migration in the river sculpin, Cottus hangiongensis. Japanese Journal of Ichthyology 34, 488–496.

Ha, P. Y., and Kinzie, R. A. (1996). Reproductive biology of Awaous guamensis, an amphidromous Hawaiian goby. Environmental Biology of Fishes 45, 383–396.
Reproductive biology of Awaous guamensis, an amphidromous Hawaiian goby.CrossRef |

Hirashima, K., and Tachihara, K. (2000). Embryonic development and morphological changes in larvae and juveniles of two land-locked gobies, Rhinogobius spp. (Gobiidae), on Okinawa Island. Japanese Journal of Ichthyology 47, 29–41..

Hirashima, K., and Tachihara, K. (2006). Longitudinal distribution and dietary habits of the genus Rhinogobius in the Genka River of northern Okinawa Island, Japan. Japanese Journal of Ichthyology 53, 71–76..

Iguchi, K., and Mizuno, N. (1999). Early starvation limits survival in amphidromous fishes. Journal of Fish Biology 54, 705–712.
Early starvation limits survival in amphidromous fishes.CrossRef |

Iguchi, K., Ito, F., Yamaguchi, M., and Matsubara, N. (1998). Spawning downstream migration of ayu in the Chikuma River. Bulletin of the National Research Institute of Fisheries Science 11, 75–84..

Inui, R., Onikura, N., Kawagishi, M., Nakatani, M., Tomiyama, Y., and Oikawa, S. (2010). Selection of spawning habitat by several gobiid fishes in the subtidal zone of a small temperate estuary. Fisheries Science 76, 83–91.
Selection of spawning habitat by several gobiid fishes in the subtidal zone of a small temperate estuary.CrossRef | 1:CAS:528:DC%2BC3cXis1eqsg%3D%3D&md5=7fa274e66e3002f308ecb15a2a78561dCAS |

Katoh, M., and Nishida, M. (1994). Biochemical and egg size evolution of freshwater fishes in the Rhinogobius brunneus complex (Pisces, Gobiidae) in Okinawa, Japan. Biological Journal of the Linnean Society 51, 325–335.
Biochemical and egg size evolution of freshwater fishes in the Rhinogobius brunneus complex (Pisces, Gobiidae) in Okinawa, Japan.CrossRef |

Kondo, M., Maeda, K., Yamasaki, N., and Tachihara, K. (2012). Spawning habitat and early development of Luciogobius ryukyuensis (Gobiidae). Environmental Biology of Fishes 95, 291–300.
Spawning habitat and early development of Luciogobius ryukyuensis (Gobiidae).CrossRef |

Leis, J. M., and Carson-Ewart, B. M. (2000). ‘The Larvae of Indo-Pacific Coastal Fishes: an Identification Guide to Marine Fish Larvae.’ (Brill: Leiden, The Netherlands.)

Maeda, K., and Tachihara, K. (2010). Diel and seasonal occurrence patterns of drifting fish larvae in the Teima Stream, Okinawa Island. Pacific Science 64, 161–176.
Diel and seasonal occurrence patterns of drifting fish larvae in the Teima Stream, Okinawa Island.CrossRef |

Maeda, K., Yamasaki, N., Kondo, M., and Tachihara, K. (2008). Reproductive biology and early development of two species of sleeper, Eleotris acanthopoma and Eleotris fusca (Teleostei: Eleotridae). Pacific Science 62, 327–340.
Reproductive biology and early development of two species of sleeper, Eleotris acanthopoma and Eleotris fusca (Teleostei: Eleotridae).CrossRef |

McDowall, R. M. (1997). Is there such a thing as amphidromy? Micronesica 30, 3–14.

McDowall, R. M. (2009). Early hatch: a strategy for safe downstream larval transport in amphidromous gobies. Reviews in Fish Biology and Fisheries 19, 1–8.
Early hatch: a strategy for safe downstream larval transport in amphidromous gobies.CrossRef |

Miller, P. J. (1984). The tokology of gobioid fishes. In ‘Fish Reproduction: Strategies and Tactics’. (Eds G. W. Potts and R. J. Wooton.) pp. 119–153. (Academic Press: London.)

Mizuno, N. (1960). Study on a freshwater goby, Rhinogobius similis Gill, with a proposition on the relationship between land-locking and speciation of some freshwater gobies in Japan. Memoirs of the College of Science, University of Kyoto, Series B 27, 97–115.

Mizuno, N. (1961). Study on the gobioid fish, ‘Yoshinobori’ Rhinogobius similis Gill – I. Comparison of life histories of three ecological types. Bulletin of Japanese Society of Scientific Fisheries 27, 6–11.
Study on the gobioid fish, ‘Yoshinobori’ Rhinogobius similis Gill – I. Comparison of life histories of three ecological types.CrossRef |

Moriyama, A., Yanagisawa, Y., Mizuno, N., and Omori, K. (1998). Starvation of drifting goby larvae due to retention of free embryos in upstream reaches. Environmental Biology of Fishes 52, 321–329.
Starvation of drifting goby larvae due to retention of free embryos in upstream reaches.CrossRef |

Myers, G. S. (1949). Usage of anadromous, catadromous and allied terms for migratory fishes. Copeia 1949, 89–97.
Usage of anadromous, catadromous and allied terms for migratory fishes.CrossRef |

Nishida, M. (1994). Life-history variation and speciation in Yoshinobori fishes. In ‘Migrating Freshwater Fishes Between Rivers and the Sea: Life History and Evolution’. (Eds A. Goto, K. Tsukamoto and K. Maekawa.) pp. 154–169. (Tokai University Press: Tokyo.) [In Japanese]

Nishida, M. (2001). Evolutionary process toward larger egg: Rhinogobius species. In ‘Evolutionary Biology of Egg Size in Aquatic Animals’. (Eds A. Goto and K. Iguchi.) pp. 149–170. (Kaiyusya: Tokyo.) [In Japanese]

Oijen, M. J. P., Suzuki, T., and Chen, I.-S. (2011). On the earliest published species of Rhinogobius. With a redescription of Gobius brunneus Temminck and Schlegel, 1845. Journal of the National Taiwan Museum 64, 1–17.

Oshiro, N., and Nishizima, S. (1978). An observation on the juveniles of ‘Yoshinobori’ (Gobiidae) in the sea-waters. Biological Magazine Okinawa 16, 17–22..

R Development Core Team (2011). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (last accessed 18 February 2013).

Sakai, H., and Yasuda, F. (1978). Development of eggs and larvae of the freshwater goby, Rhinogobius brunneus. Japanese Journal of Ichthyology 25, 92–100.

Suzuki, T., and Chen, I.-S. (2011). Redescriptions of three species of genus Rhinogobius (Perciformes, Gobiidae) described by Dr. Shigeho Tanaka. Bulletin of the Osaka Museum of Natural History 65, 9–24..

Suzuki, T., and Sakamoto, K. (2005). Record of a gobiid fish, Rhinogobius sp. TO (Perciformes, Gobiidae) from the Noubi and Okazaki plains, Japan. Bulletin of Biogeographical Society of Japan 60, 13–20..

Suzuki, T., Chen, I.-S., and Senou, H. (2011). A new species of Rhinogobius Gill, 1859 (Teleostei: Gobiidae) from the Bonin Islands, Japan. Journal of Marine Science and Technology 19, 693–701.

Tachihara, K. (2009). Two landlocked Rhinogobius species in the Ryukyu Archipelago: conservation and the future of gobies endemic to isolated rivers. Japanese Journal of Ichthyology 56, 70–74..

Takahashi, S., and Okazaki, T. (2002). A new lentic form of the ‘yoshinobori’ species complex, Rhinogobius spp. from Lake Biwa, Japan, compared with lake-river migrating Rhinogobius sp. OR. Ichthyological Research 49, 333–339.
A new lentic form of the ‘yoshinobori’ species complex, Rhinogobius spp. from Lake Biwa, Japan, compared with lake-river migrating Rhinogobius sp. OR.CrossRef |

Tamada, K. (2009). Variations in clutch and egg sizes in the amphidromous goby Rhinogobius sp. CB along a river course and within a spawning season. Ichthyological Research 56, 69–75.
Variations in clutch and egg sizes in the amphidromous goby Rhinogobius sp. CB along a river course and within a spawning season.CrossRef |

Tsunagawa, T., and Arai, T. (2008). Flexible migration of Japanese freshwater gobies Rhinogobius spp. as revealed by otolith Sr : Ca ratios. Journal of Fish Biology 73, 2421–2433.
Flexible migration of Japanese freshwater gobies Rhinogobius spp. as revealed by otolith Sr : Ca ratios.CrossRef |

Tsunagawa, T., and Arai, T. (2011). Migratory history of the freshwater goby Rhinogobius sp. CB in Japan. Ecology of Freshwater Fish 20, 33–41.
Migratory history of the freshwater goby Rhinogobius sp. CB in Japan.CrossRef |

Tsunagawa, T., Suzuki, T., and Arai, T. (2010). Otolith Sr : Ca ratios of freshwater goby Rhinogobius sp. TO indicating absence of sea migrating traits. Ichthyological Research 57, 319–322.
Otolith Sr : Ca ratios of freshwater goby Rhinogobius sp. TO indicating absence of sea migrating traits.CrossRef |

Yamasaki, N., Kondo, M., Maeda, K., and Tachihara, K. (2011). Reproductive biology of three amphidromous gobies, Sicyopterus japonicus, Awaous melanocephalus, and Stenogobius sp., on Okinawa Island. Cybium 35, 345–359.

Yokoi, K., and Hosoya, K. (2006). Early development of the endangered freshwater goby, Rhinogobius sp. BI (Gobiidae). Ichthyological Research 53, 160–165.
Early development of the endangered freshwater goby, Rhinogobius sp. BI (Gobiidae).CrossRef |


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