Rev Fish Biol Fisheries DOI 10.1007/s11160-013-9316-8 REVIEWS Tropical and temperate freshwater amphidromy: a comparison between life history characteristics of Sicydiinae, ayu, sculpins and galaxiids Shun Watanabe • Midori Iida • Clara Lord • Philippe Keith • Katsumi Tsukamoto Received: 30 August 2012 / Accepted: 19 June 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Amphidromy is a distinctive form of the evolution of their life histories. It is likely that the diadromy, but differences in the life histories of evolutionary direction of the larval stage of tropical tropical and temperate amphidromous fishes suggest amphidromy is to remain in the sea and that of that there are two types of freshwater amphidromy. temperate amphidromy is towards having the ability to The life histories of Sicydiinae gobies, ayu (Plecog- remain in freshwater if needed. Tropical and temper- lossus altivelis), Japanese sculpins (Cottus) and gal- ate amphidromy appear to be biologically informative axiids (Galaxiidae), suggest that the Sicydiinae are categories and evaluations of this hypothesis will representatives of tropical freshwater amphidromy, facilitate better understanding of the various forms of whereas ayu, sculpins and galaxiids are representa- amphidromy in the future. tives of temperate freshwater amphidromy. The Sic- ydiine larval stage may be required to occur in the Keywords Amphidromous species Á Sicydiine ocean for all species, but ayu, sculpins and galaxiids species Á Landlocked form Á Fluvial form Á have landlocked or fluvial forms with larvae that do Oceanic dependency not need to enter the ocean for larval feeding and growth. This suggests that Sicydiine larvae have a high oceanic dependency whereas ayu, sculpins and galax- Introduction iid larvae have a low oceanic dependency. Freshwater amphidromous fish in tropical and temperate zones Myers (1949) defined three categories of diadromy, appear to have developed two different strategies in which are anadromy, catadromy and amphidromy. He introduced the new term, ‘amphidromy’, from the Greek words meaning ‘running’ and ‘around’, or ‘on S. Watanabe (&) Á K. Tsukamoto both sides’. McDowall (1988) also proposed that College of Bioresource Sciences, Nihon University, amphidromy occurs in two distinct forms: freshwater 1866 Kameino, Fujisawa-shi, Kanagawa 252-0880, Japan amphidromy (Fig. 1a), in which spawning is in e-mail: [email protected] freshwater and the larvae are temporarily marine M. Iida before returning to freshwater to grow and mature, and Faculty of Science, University of the Ryukyus, 1 Senbaru, marine amphidromy (Fig. 1b), in which spawning is Nishihara, Okinawa 903-0213, Japan marine and the larvae/juveniles are temporarily in freshwater before returning to the sea to grow to C. Lord Á P. Keith Muse´um National d’Histoire Naturelle, DMPA, UMR, maturity. However, there has been considerable con- 7208, 57 rue Cuvier CP026, 75231 Paris Cedex 05, France fusion about the nature of amphidromy and the 123 Rev Fish Biol Fisheries distinctiveness of freshwater amphidromy compared anadromy in which large mature adults return to to anadromy (McDowall 2007a). The term amphidr- freshwater for reproduction, but not for feeding. In omy has sometimes been ignored by North American amphidromous species, migrations to and from the sea and European biologists and ichthyologists, whereas do not involve reproduction and are rather ‘trophic’ anadromy and catadromy have long been used migrations (Myers 1949; McDowall 2007a, 2009), so (McDowall 2007a). Some researchers do not distin- simply considering amphidromous life histories as a guish between anadromous and amphidromous fishes special category of anadromy seems to be an over- and simply describe them as diadromous. On the other simplification that is not particularly scientifically hand, this term has become well-established by the useful. majority of researchers who work on temperate and McDowall (1987) reported that amphidromous cool temperate islands such as Japan and New Zealand fishes are present in both northern and southern and tropical and subtropical Indo-Pacific insular temperate regions from analysis of data on the systems such as Re´union Island, the Hawaiian Islands geographic distribution of diadromy. In the temperate and French Polynesia, because their studies refer to the regions, there are many freshwater amphidromous species inhabiting these environments as being species such as galaxiid fishes of the genera Aplochi- amphidromous. ton, Galaxias and Neochanna (McDowall 1988, There are major differences between anadromous 1990), retropinnids of the genus Prototroctes (McDo- and freshwater amphidromous species that are bio- wall 1988, 1990), some fishes in the family Cottidae logically significant. McDowall (2009) simply and (Goto 1990; Yokoyama and Goto 2002), the pinguip- clearly explained the difference in both as follows. In edid Cheimarrichthys fosteri (McDowall 1990, 2000), anadromy, reproduction and most somatic growth take the ayu, Plecoglossus altivelis, of the family Pleco- place in the different biomes of freshwater and the sea glossidae (Azuma 1981; Tsujimura and Taniguchi and the return migration to the spawning biome of 1995; Iguchi et al. 1999; Iguchi and Nishida 2000), freshwater is undertaken by mature, adult fish. They some species in the Eleotridae (McDowall 1990) and do little or no feeding and growing after initiating the in the Gobioidei of the genus Rhinogobius (Akihito return migration, which can therefore be described as a and Yoshino 1984). Numerous research efforts have reproductive migration. In contrast, most somatic been made to study the taxonomy, biology and growth and reproduction in freshwater amphidromous ecology of these diverse fishes. fishes is in freshwater, and the return migration to the McDowall (1987) was dubious about the geo- spawning biome is undertaken by small juveniles. graphic distribution of amphidromy being mostly in They return to freshwater to feed and grow for many the temperate regions and suspected that a different months or sometimes years before maturation and picture of its latitudinal occurrence would emerge, reproduction occurs in freshwater. This life cycle is particularly when gobioid taxonomy and life histories also functionally and strategically different from in the tropical zone would be elucidated. Over the past Freshwater Sea Hatched pre-larvae emigrate immediately to sea by the flow of the river A Birth Freshwater Feeding and growth Feeding Amphidromy Reproduction and growth Post-larvae or small juveniles return to Freshwater B Birth Feeding and growth Marine Amphidromy Feeding and Reproduction growth Fig. 1 The different types of amphidromy that are freshwater amphidromy (A) and marine amphidromy (B) as classified by McDowall (1988) 123 Rev Fish Biol Fisheries few decades a considerable number of studies have been Life history characteristics of the Sicydiinae made on gobioid taxonomy and life histories, especially for the subfamily Sicydiinae (Gobioidei). This subfam- All Sicydiine species mainly inhabit tropical and ily comprises nine described genera and nearly 120 subtropical islands. However, among sicydiine spe- species (Froese and Pauly 2013, FishBase, World Wide cies only S. japonicus lives at temperate latitudes (Iida Web electronic publication. www.fishbase.org, version et al. 2013), and various studies have been made on the 04/2013), which include the genera Akihito, Cotylopus, ecology of this species recently. The juveniles and Lentipes, Sicydium, Sicyopterus, Sicyopus, Smilosicy- adults of Sicydiinae gobies grow, feed and reproduce opus, Stiphodon and Parasicydium (Keith and Lord in rivers after their larvae grow in the marine 2011; Keith et al. 2011). The species in these genera environment. They have high fecundity (50,000 to mostly occur on tropical and subtropical islands in the 70,000 ova in S. lagocephalus, Delacroix 1987; Keith Indo-Pacific, West Africa, Central America and the et al. 1999, 225,000 in S. japonicus,Doˆtu and Mito Caribbean region (McDowall 2007a; Keith and Lord 1955, 1,000 to 10,000 in Stiphodon percnopterygi- 2011) although Sicyopterus japonicus is distributed onus, Yamasaki and Tachihara, 2006), small eggs from Taiwan to Fukushima, Japan and has the north- (0.49 to 0.58 mm in S. percnopterygionus, Yamasaki ernmost geographic distribution among the Sicydiinae and Tachihara 2006), and their newly hatched larvae (Iida et al. 2009, 2013). Myers (1949) stated that the are small in size (1.1 mm in S. lagocephalus to amphidromous prototype is the goby genus Sicydium 1.8 mm in S. stimpsoni and Lentipes concolor, Man- and its close allies, which are common in tropical acop 1953; Lindstrom 1999). After hatching the larvae freshwaters around the world. McDowall has recently drift downstream towards the sea where they spend a published six review papers (McDowall 2003, 2004, variable amount of time feeding and growing, ranging 2007a, b, 2009, 2010) about freshwater amphidromy from 2 to 9 months (63 to 106 days in Lentipes that were especially focused on Sicydiine species rather concolor, Radtke et al. 2001, 66 to 164 days in than other freshwater amphidromous species. He sug- Cotylopus acutipinnis, Teichert et al. 2012, 133 to gested that if any tropical and subtropical freshwater 256 days in S. lagocephalus, Hoareau et al. 2007b). fish group could be regarded as ‘iconic’, it would be They have among the longest marine larval phases of these gobies (McDowall 2007a). Over the past few any tropical fish species