New Perspectives on the Early Life History of Tropical Anguillid Eels: Implications for Resource Management

American Fisheries Society Symposium 58:71–84, 2009 © 2009 by the American Fisheries Society New Perspectives on the Early Life History of Tropical Anguillid Eels: Implications for Resource Management MICHAEL J. MILLER 1, JUN AOYA M A , AND KATSU M I TSU K A M OTO Ocean Research Institute, The University of Tokyo 1-15-1 Minamidai, Nakano, Tokyo 164-8639 Japan Abstract.—Recent studies on leptocephali and glass eels of anguillid species in the western North Pacific and Indonesian Seas suggest that tropical eels have very different life history characteristics than temperate species, which may have important implications for their conservation and management. Some species in the Indonesian Seas region, such as the Indonesian mottled eel Anguilla celebesensis and the Indo- nesian longfinned eel A. borneensis, appear to have short spawning migrations and larval durations compared with temperate species. Species such as the Indonesian mottled eel A. celebesensis likely have multiple populations that spawn locally and recruit back to the same area. However, the giant mottled eel A. marmorata appears to have several separate populations in various regions of the Indian Ocean and western North and South Pacific oceans. The northern population of this species probably spawns in the North Equatorial Current region of the western North Pacific and has a long spawning migration more characteristic of temperate species. These findings suggest that the population structures of various tropical and temperate eel species may be quite different. Therefore some tropical anguillid species may require management at regional levels rather than as single panmictic species, as generally has been the case for temperate species. Introduction where all adults throughout their range return to spawn and then die. Their larvae, called lep- Eels of the genus Anguilla are well known tocephali, are then transported by currents back for their long migrations from freshwater or toward their juvenile growth habitats. coastal growth habitats to spawning areas far The question about whether spawning and out in the open ocean. Because of this type of recruitment patterns shown by northern tem- offshore spawning and the apparently random perate anguillid eels have resulted in single return of their larvae throughout their ranges, panmictic populations has been the focus of anguillid eel species in temperate regions such considerable research using various genetic as North America, Europe, East Asia, and Aus- methods. Although most initial studies of the tralia and New Zealand have been historically two species of Atlantic eels found no spatial viewed as probably having large single panmic- heterogeneity within either species (see Avise tic spawning populations. Each of these species 2003), some recent studies using allozymes has been considered to have one spawning area (Maes and Volckaert 2002) and the newly de- veloped genetic markers of microsatellite DNA 1 Corresponding author: [email protected] 71 72 Miller et al. (Daemen et al. 2001; Wirth and Bernatchez from various areas also have suggested that dif- 2001) have detected some genetic structure in ferent spawning areas exist for tropical eels in the European eel, Anguilla anguilla. In con- the Indonesia and Philippines region (Arai et trast, more recent microsatellite studies have al. 2001a, 2003). In addition, the most wide- found no evidence of genetic structure in the spread anguillid, the giant mottled eel has been European eel or the American eel, A. rostrata found to have at least five genetically distinct (Wirth and Bernatchez 2003; Dannewitz et al. populations in various regions of the Indian and 2005). Similar studies on the Japanese eel, A. western Pacific oceans (Ishikawa et al. 2004). japonica, in East Asia have produced evidence Therefore, if some tropical anguillid species both for and against the presence of genetic have multiple spawning areas or genetically structure (Sang et al. 1994; Chan et al. 1997; isolated populations, they cannot be viewed by Ishikawa et al. 2001; Tseng et al. 2009, this fisheries managers in the same way as temper- volume). ate eels. Any eel species that is nonpanmictic However, even if there is some spatial will require a site-specific, rather than a spe- heterogeneity within these species, the level cies-wide, management approach. of genetic divergence is very small compared This paper examines recent findings on the with that found within most species of widely early life history of tropical eels and discusses distributed marine organisms (Avise 2000) and their implications for population structure. Im- may represent only minor levels of reproductive proved understanding of the population struc- segregation or differential recruitment patterns ture of tropical eels is urgently needed to guide throughout the species’ range. Whether or not effective conservation efforts for these species catadromous eels have panmictic population that are found in many parts of the world. structures has important management implications, because if a species is largely or entirely Species Ranges of Tropical Anguillids panmictic, then it can be managed as one population throughout its range. This means that the Tropical eels are widely distributed on effects of continental habitat loss or overfishing both sides of the equator in the Indian and Pa- in one part of the range of a species should not cific oceans and in the Indonesian Seas region, significantly affect future recruitment back to with about four species or subspecies found in that particular area if the population is stable the Indian Ocean, five in the Indonesian Seas in other areas. For example, even if a particu- region, five or six in the New Guinea and Solo- lar region of the species’ range has very low mon Islands region, and four across the south survival and spawner escapement, recruitment Pacific from eastern Australia to Tahiti (Table back to that region may remain constant if 1; Ege 1939; Watanabe 2003). The giant mot- there is still enough spawner escapement from tled eel, African longfin eel A. mossambica, other regions. and African mottled eel A. bengalensis labiata This model for catadromous eels may not (A. nebulosa labiata) are present in east Africa be useful for all species, because new informa- along the western Indian Ocean, and the Indi- tion suggests that panmixia may not be typi- an mottled eel A. bengalensis bengalensis (A. cal of tropical anguillids. Recent studies on the nebulosa nebulosa) is present along the Bay of distribution of leptocephali of tropical anguil- Bengal in the northern Indian Ocean. The rang- lids have found evidence of short spawning es of the latter two species also extend south- migrations and the presence of more than one ward to the Indian Ocean side of Sumatra and spawning area for the same species (Aoyama et Java Islands of southern Indonesia where the al. 1999, 2003; Arai et al. 2001a; Kuroki et al. giant mottled eel is also present. In the Indone- 2006a). Data on larval durations of glass eels sian Seas region (Figure 1), the giant mottled Tropical Eel Life History and Management 73 Table 1. Tropical species and subspecies of anguillid eels of the western Pacific and Indian oceans, listing the relative sizes of their ranges and early life history (ELH) studies on their leptocephali and on the inshore migration or otolith microstructure of their glass eels. See Figure 1 for the ranges of the species in the Indonesia region and Watanabe et al. (2003) for the ranges of all species. Size of species ELH Size of species ELH Region/Species range studies Region/Species range studies Indonesia region Western South Pacific A. borneensis Very small 3,17 A. reinhardtii Medium 2 A. interioris Small 3,18 A. bicolor pacifica Large 2,7 A celebesensis Small 3,4,5,8,10,11,12,17 A. megastoma Large 2 * A. bicolor pacifica Large 1 ,3,2,4,5,7,8,11,12,17 A. obscura Large 2 * A. marmorata Very large 1 ,3,4,5,7,8,9,11,12,14,16,17 A. marmorata Very large 2,7 N. Eastern Indian Ocean Western Indian Ocean A. bengalensis bengalensis Medium A. bengalensis labiat a Medium A. bicolor bicolor Large 1,6,13,19 A. mosambica Medium 1,15 * A. marmorata Very large 1 A. bicolor bicolor Large 1,15 A. marmorata Very large 1,15 Jespersen 19421, Aoyama et al. 19992, 20033, Arai et al. 1999a 4,b5,c6, 2001a7, b8, 20029, 200310, and Marui et al. 200111, Sugeha et al. 2001a12, Setiawan et al. 200113, Miller et al. 200214, Robinet et al. 200315, Kuroki et al. 200516, 2006a17b18*, 200719 ; Leptocephali could not be clearly identified, but may have included these species. 40ºN 30ºN A. marmorata A. celebesensis 20ºN A. bicolor pacifica A. interioris ? 10ºN A. borneensis 0º 10ºS 100ºE 110ºE 120ºE 130ºE 140ºE Figure 1. Map showing the estimated species ranges of the five species of tropical anguillid eels that inhabit the western North Pacific and Indonesian Seas regions, according to Ege (1939) and other recent reports or observations of various life history stages of these species. 74 Miller et al. eel is widely distributed and the Indonesian Recent Advances in Early Life History shortfin eel A. bicolor pacifica reaches as far Studies as Taiwan, with a few glass eels being found as far north as southern Japan (Yamamoto et al. Studies on Tropical Eel Leptocephali 2001). The Indian shortfin eel A. bicolor bicolor is also widely distributed and is found on The discovery of small anguillid lepto- both sides of the Indian Ocean. In contrast, the cephali in the Indian Ocean off the west coast Indonesian mottled eel A. celebesensis is more of Sumatra in 1929 (Jespersen 1942; see restricted to Indonesia and the Philippines. Miller 2003) suggested that tropical eels may The Indonesian longfinned eel A. borneensis not migrate as far to spawn as do temperate (A.

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