Review of Ocean-Atmospheric Factors in the Atlantic and Pacific Oceans Influencing Spawning and Recruitment of Anguillid Eels

American Fisheries Society Symposium 69:231 249, 2009 2009 by the American Fisheries Society Review of Ocean-Atmospheric Factors in the Atlantic and Pacific Oceans Influencing Spawning and Recruitment of Anguillid Eels Mi c h a e l J. Miller* a n d Sh i n g o Ki m u r a Ocean Research Institute, The University of Tokyo,, Minamidai, Nakano, Tokyo 164-8639, Japan Kevin D. Friedland National Marine Fisheries Service, 28 Tarzwell Drive, Narragansett, Rhode Island 02882, USA Br i a n Kn i g h t s 1 University of Westminster, 115 New Cavendish Street, London W1W 6UW, UK Heeyong Kim 2 Ocean Research Institute, The University of Tokyo, Minamidai, Nakano, Tokyo 164-8639, Japan Do n a l d J. Je l ly m a n National Institute of Water and Atmosphere, Post Office Box 8602, Christchurch, New Zealand Katsumi Tsukamoto Ocean Research Institute, The University of Tokyo, Minamidai, Nakano, Tokyo 164-8639, Japan Abstract. Declines in recruitment of temperate anguillid eels have occurred in the past 30 years in many areas of their species ranges. The cumulative effects of anthropogenic changes to their freshwater growth habitats are likely contributors to reductions in population sizes, but changes in ocean-atmospheric conditions in the ocean also appear to be contributing to the declines. This paper reviews how changes in the ocean may contribute to recruitment declines by affecting the spawning location of silver eels, larval feeding success, or the transport of their leptocephalus larvae by ocean currents. Recruitment of European eels Anguilla anguillla has shown correlations with the North Atlantic Oscillation and specific changes in ocean conditions in the Sargasso Sea where spawning and development occurs. The American eel A. rostrata spawns in an area that overlaps with the European eel and so could also be affected by these types of changes. Recruitment of Japanese eels A. japonica appears to be correlated to the El Niño Southern Oscillation index and latitudinal changes in salinity fronts in the western North Pacific. The general spawning and recruitment patterns of the temperate Australasian shortfin eels A. australis and New Zealand longfin eels A. dieffenbachii in the western South Pacific are similar to those of the northern temperate anguillids and also may be affected by El Niño-related factors. The changes in ocean conditions associated with atmospheric forcing or a warming of the ocean could alter the biological characteristics of the surface layer where leptocephali feed, due to changes in productivity or community structure, in addition to having possible effects on larval * Corresponding author: miller@ori.u-tokyo.ac.jp 1 Current address: King s College London, Norfolk Building, Surrey Street, London WC2R 2LS, UK 2 Current address: National Fisheries Research and Development Institute, 408-1 Sirang-ri, Gijang-eup, Gjiang-kunm Busan, 619-705, Korea 231

232 miller et al. transport and location of the spawning areas by silver eels. Changes in ocean-atmospheric conditions could result in lower feeding success and survival of leptocephali, or increased retention in offshore areas due to changes in the location of spawning areas, resulting in reductions in recruitment. Introduction The most important fisheries species of anguillid eels are those found at the higher latitudes of the North Atlantic and western Pacific, and major declines in recruitment particularly at the margins of the species ranges have raised serious concerns among scientists (Dekker et al. 2003). These temperate species include the European eel Anguilla anguilla and American eel A. rostrata in the North Atlantic, the Japanese eel A. japonica in the western North Pacific, and the Australasian shortfin eel A. australis and the New Zealand longfin eel A. dieffenbachii in the western South Pacific. Concern about these species has increased recently because recruitment of the northern temperate species has declined markedly from the most recent peak levels in the late 1970s to early 1980s (Figure 1; Dekker 1998; Haro et al. 2000; McCleave 2001; Casselman 2003; Tatsukawa Index (% of 1979-1994 mean) 600 400 200 American eel European eel Japanese eel 0 1970 1975 1980 1985 1990 1995 2000 Year Figure 1. Trends in recruitment indices of northern temperate anguillid species (% of 1979 1994 means, 3-year running averages) for the American eel in the St. Laurence River in Canada (Moses-Saunders Dam trap, assuming age of 6+ of yellow eels at time of trapping in the 1970 1980s), the European eel in the Netherlands (Den Oever glass eel fishery-independent surveys), and the Japanese eel in Japan (total commercial catches of glass eels). Data are from Casselman (2003), ICES (2006, 2007), and Kimura (2003). 2003). There also are some indications that the two southern temperate anguillid species that recruit to New Zealand may be showing signs of declines (Jellyman 2007, 2009; Jellyman et al. 2000). However, because the catadromous life histories of anguillid eels are so complex and difficult to monitor during their oceanic stages, the specific causes of these declines have been difficult to determine. The amount of freshwater and estuarine growth habitats available for the production of silver eels has been reduced on decadal scales by anthropogenic factors such as land reclamation, construction of dams, and pollution throughout much of their ranges (Haro et al. 2000; Feunteun 2002; Knights 2003; Dekker 2004). Other anthropogenic factors in addition to fishing mortality that have been proposed as influencing recruitment include parasite introductions and toxins in the body of silver eels that could cause physiological disruptions during their migration or spawning (e.g., Robinet and Feunteun 2002; Kirk 2003; Palstra et al. 2007). Recent research also has suggested that virus infections may reduce the ability of silver eels to reach their spawning areas (van Ginneken et al. 2005). The effects of such impacts on entire populations have not been determined, but scientists and management agencies have expressed concerns (e.g., ICES 2001, 2006, 2007; Dekker et al. 2003). In addition to the effects of anthropogenic factors, it has been hypothesized that changes in ocean-climate conditions could have had important impacts on the northern temperate species (Castonguay et al. 1994; Kimura et al. 2001; Knights 2003; Friedland et al. 2007; Bonhommeau et al. 2008a, 2008b; Kettle et al. 2008). Even for the European eels though, only a few studies have clarified exactly how oceanic factors might affect larval migrations or their feeding success (Friedland et al. 2007; Bonhommeau et al. 2008a, 2008b). Because silver eels have never been seen in their spawning areas, it is not known if the factors leading to reduced recruitment are due to fewer silver eels migrating to spawn each year, a reduced survival of these migrants, changes in oceanic con-

ocean-atmospheric factors influencing spawning and recruitment of anguillid eels 233 ditions affecting spawning success, or poor larval feeding, transport, or survival. In this paper, we review the possible ways that changes in ocean-atmospheric conditions could affect the recruitment of temperate anguillid eels. To help evaluate these potential factors, the literature on the spawning areas and larval distributions of temperate anguillid eels and their relationship to patterns of ocean-atmospheric conditions in the western Pacific and North Atlantic oceans are overviewed. There is increasing understanding of how climatic changes and ocean regime shifts are affecting physical and biological conditions in regions of the world s oceans (Weijerman et al. 2005; Drinkwater 2006; Lehodey et al. 2006; Beamish et al. 2009, this volume), so the objective of this review is to examine the possible relationships between specific life history events of anguillid eels and changes in ocean conditions. In the North Atlantic, changes in oceanatmospheric factors have been found to occur in association with the North Atlantic Oscillation (NAO; Hurrell 1995; Hurrell and Dickson 2004) that have been linked to changes in physical (Curry and McCartney 2001) and biological (Hays et al. 2005; Lehodey et al. 2006; Stige et al. 2006) conditions. In the Pacific, the El Niño Southern Oscillation (ENSO) is known to affect sea surface temperatures and ocean current patterns in the eastern Pacific and for having major influences on climatic conditions worldwide (McPhaden 1999). These effects of ENSO have major effects on the equatorial Pacific and the biological characteristics of the eastern Pacific (Sugimoto et al. 2001; Lehodey et al. 2006). Another longer-term regime shift in oceanatmospheric factors in the Pacific Ocean has been termed the Pacific Decadal Oscillation (PDO), which has major affects on the ecosystem of the northeastern Pacific (Hare and Mantua 2000; Lehodey et al. 2006; Beamish et al. 2009). In addition to these types of regime shifts, there is also evidence that there has been a gradual warming of the world s oceans (Levitus et al. 2000) that may be affecting productivity in the surface layer (Behrenfeld et al. 2006) where leptocephali feed. One obvious way that various types of changes in oceanic conditions could be affecting anguillid eels is by reducing their feeding success during their long larval migrations from their offshore spawning areas to their freshwater and estuarine growth habitats where they recruit. However, evaluating the possible effects of oceanic factors on the feeding of leptocephali is particularly complicated because their morphology and physiology are very different from other fish larvae. Leptocephali appear to feed on marine snow or other particulate organic matter such as discarded larvacean houses or even dissolved organic matter (Otake et al. 1993; Mochioka and Iwamizu 1996), which are not easily measured. The availability of marine snow and other types of particulate matter in the surface layer where leptocephali live is thought to depend on primary and secondary production and is coupled to phytoplankton blooms (Turner 2002). In the open ocean, primary production is controlled by, among other factors, nutrient availability and surface mixing dynamics (Palter et al. 2005), thus providing possible linkages between ocean-atmospheric changes and the feeding success of leptocephali. In the North Atlantic, the possibility that ocean-atmospheric changes could affect anguillid eels led to hypotheses that changes associated with the NAO may be affecting the recruitment of the European eel and possibly the American eel (Castonguay et al. 1994; ICES 2001; Knights 2003; Friedland et al. 2007; Kettle et al. 2008). Both species spawn at the southern edge of the Gulf Stream recirculation gyre in the Sargasso Sea (Figure 2), but the American eel only needs to move west and across the Gulf Stream, whereas the European eel must move eastward all the way across the North Atlantic basin. The possibility that the long migration of the European eel could be influenced by ocean-atmospheric changes has been supported by correlations between glass eel recruitment data and the NAO index and other ocean-atmospheric parameters in the Sargasso Sea (Knights 2003; Friedland et al. 2007; Bonhommeau et al. 2008b). The Japanese eel spawns in a similar westward flowing current in the western North Pacific (Tsukamoto 1992, 2006), and ocean-atmospheric changes also have been hypothesized to affect its recruitment (Kimura et al. 2001). This species is distributed in East Asia from Taiwan to Japan and spawning occurs in the North Equatorial Current, which bifurcates into both a northward flow that transports larvae to their recruitment areas, and a southward flow to areas outside of its range (Kimura et al. 1994). This transport situation is also complicated by north south movements of the salinity

234 miller et al. 60ºN A 90ºW 60ºW 30ºW 0º 30ºE 60ºN 45ºN 30ºN North America FC Gulf Stream N. Atlantic Drift Europe Africa 45ºN 30ºN 45ºN B Asia Japan C S. Equatorial Current 0º 30ºN Kuroshio 15ºS 15ºN NEC Australia E. Australian Current 30ºS 0º MC Tasman Front New Zealand 45ºS 120ºE 135ºE 150ºE 150ºE 165ºE 180º 165ºW Figure 2. The spawning areas of the northern temperate species of anguillid eels in the subtropical gyres of the western North Atlantic showing the Florida Current (FC), Gulf Stream, and North Atlantic Drift in panel (A) and in the western North Pacific showing the North Equatorial Current (NEC), Mindanao Current (MC), and Kuroshio Current in panel (B). The region where spawning likely occurs by the southern temperate anguillid species in the western South Pacific is also shown along with the South Equatorial Current and the East Australian Current in panel (C). front typically present at the northern margin of the spawning area. A southward movement of the front during El Niño could contribute to larvae entering the southward flow (Kimura and Tsukamoto 2006), and correlations between the El Niño Southern Oscillation index (SOI) and recruitment to southern Japan have been found (Kimura et al. 2001). Changes in the equatorial Pacific from ENSO also could have an effect on the anguillid spawning and larval development areas in the western South Pacific where there are two species of temperate anguillid eels that recruit to eastern Australia and throughout New Zealand (Jellyman 2003). Based on the presence of their leptocephali in the region (Jellyman 1987, 2003; Aoyama et al. 1999), it is probable that Australasian shortfin eels spawn somewhere in the westward flowing South Equatorial Current. Their leptocephali presumably move westward and then southward in the East Australian Current where some move westward and recruit to eastern Australia. Other larvae recruit to New Zealand, although the actual migration route has not been determined. Another species, the New Zealand longfin eel, also recruits to New Zealand, but its leptocephali have never been distinguished so its spawning area remains a mystery (Jellyman and Tsukamoto 2002). Teleconnections of ENSO reach into the western South Pacific (Gouriou and Delcroix 2002), so the spawning area and larval transport of these South Pacific temperate eels could be affected by ocean-atmospheric factors.

ocean-atmospheric factors influencing spawning and recruitment of anguillid eels 235 In the following sections, each species of temperate anguillid eel and their relationship to patterns of ocean-atmospheric conditions in the three subtropical gyres of the western Pacific and North Atlantic oceans are examined. The objective of this review is to provide a general perspective on how temperate eel populations may be responding to ocean-atmospheric changes that can help to facilitate future research and efforts to manage and conserve these important catadromous fishes. Atlantic Eels Spawning Area and Oceanic Conditions The spawning area of the anguillid eels in the Sargasso Sea was discovered by the Danish fisheries scientist Johannes Schmidt in the early part of the 20th century after collections of leptocephali were made in many regions of the Atlantic and Mediterranean Sea (Schmidt 1922). The smallest leptocephali of both species were found in the southern Sargasso Sea, and larvae smaller than 10 mm were later shown to be widely distributed in overlapping areas south of about 308N (Figure 2), with the European eel appearing to spawn slightly to the east of the American eel (McCleave et al. 1987). The Sargasso Sea is the western part of the North Atlantic subtropical gyre that has the northward flowing Florida Current to the west and its continuation as the Gulf Stream to the north (Schmitz and McCartney 1993). The anguillid eels spawn in the southern Sargasso Sea, where there is westward current flow that transports their leptocephali towards the Florida Current. The general location of the main spawning area of the Atlantic eels has been determined from small recently hatched leptocephali 4 7 mm total length (TL) that were collected in several surveys over a wide region (Schoth and Tesch 1982; Boëtius and Harding 1985; McCleave et al. 1987; Kleckner and McCleave 1988). It has been shown that spawning was occurring south of distinct temperature fronts that are consistently present during the spawning season in late winter and early spring (Kleckner and McCleave 1988). These fronts were also found to cause discontinuities in the assemblages of leptocephali of various families, and the associated frontal jets likely transport some leptocephali eastward (Miller and McCleave 1994). After the spawning season, the leptocephali of both anguillid species appear to become widely distributed as they are transported by the currents and eddies in the region (Boëtius and Harding 1985; Kleckner and McCleave 1985; McCleave and Kleckner 1987; Kettle and Haines 2006). Various sizes were present in the summer and early fall across the southern Sargasso, and leptocephali of both species have been documented in the Florida Current (Kleckner and McCleave 1982; McCleave and Kleckner 1987). One of the more direct transport pathways out of the southern Sargasso Sea may be the flow of the Antilles Current off the northeastern edge of the northern Bahamas. American eel leptocephali must cross the Florida Current and Gulf Stream to recruit to the east coast of North America, but those of the European eel must continue being transported to the east by the Gulf Stream and North Atlantic Drift. The actual pathway and transport time of European eel leptocephali remains poorly understood, however, due to the limited spatial and temporal coverage of sampling surveys across the eastern part of the basin (McCleave et al. 1998). Studies of leptocephalus distribution and modeling of drift patterns suggest that most European eel leptocephali probably use the Gulf Stream North Atlantic Drift system and, possibly, the Azores Current after moving west through the southern Sargasso (McCleave and Kleckner 1987; Kettle and Haines 2006). However, direct eastward or northeastward movement of some leptocephali appears to be a possible second route due to flows associated with the frontal jets that form in the subtropical convergence zone each year (Miller and McCleave 1994; Ullman et al. 2007). Regardless of how they achieve it or how long it takes, the migration of the European eel is probably the longest of any anguillid species, making its recruitment especially vulnerable to oceanic changes. Possible Oceanic Factors Affecting Recruitment Oceanic changes associated with shifts in the NAO in the North Atlantic have been hypothesized to contribute to changes in Atlantic eel recruitment due the variety of physical and biological factors affected by this atmospheric phenomenon. The NAO winter index (Hurrell 1995) is defined as the differ-

236 miller et al. ence in sea level pressure between Iceland and Portugal in the North Atlantic. Correlations between the NAO and the index of catches of glass eels at Den Oever in the Netherlands (DOI), which is based on standardized fishery-independent sampling (Dekker 1998, 2002), led to the hypothesis that changes in the ocean related to the NAO may be influencing recruitment fluctuations (ICES 2001; Knights 2003). Westerberg (ICES 2001), Knights (2003), and Friedland et al. (2007) have demonstrated significant inverse correlations between the NAO and DOI. However, the strength of these correlations has been questioned by Dekker (2004) because trends since the 1990s in the NAO towards zero have not resulted in clear increases in the DOI. It appears that the effects of global warming that have occurred since the 1980s, reflected in a steep and continual increase in the northern hemisphere temperature and Sargasso Sea surface temperature anomalies, have overridden the effects of the NAO (B. Knights and S. Bonhommeau, Agrocampus Rennes, Rennes, France, unpublished analysis). However, another more recent study has also found correlations between the NAO and catch data of both glass eels and adults of the European eel from many different parts of its range (see Kettle et al. 2008). To clarify possible cause effect relationships between oceanic changes and European eel recruitment, Friedland et al. (2007) examined the correlations between several specific ocean-climate parameters in the Sargasso Sea with the DOI. Because temperature changes have occurred in the surface layer of the North Atlantic and southern Sargasso Sea spawning area (Grey et al. 2000; Polyakov et al. 2005), an isotherm-latitude analysis was performed. This showed that the latitude of the 22.58C isotherm in January and February has moved from as far south as 26 278N in the 1950s to as far north as 28 298N in recent years (Figure 3). Peak negative correlations with the DOI were found in January and February in an area centered at 608W, which is the longitude of the eastern region of the European eel spawning area (Friedland et al. 2007). The 22.58C isotherm was used because it is linked to the northernmost temperature front that appears to form at the northern boundary of anguillid spawning in the Sargasso Sea (Kleckner and McCleave 1988). This front has been observed to form at the same water density in all previous studies in the region prior to 1994 (Kleckner and McCleave 1988; Miller and Figure 3. Changes in the latitude of the 22.58C isotherm in the Sargasso Sea in the 4 months just before and during the early spawning season of the Atlantic eels (adapted from Friedland et al. 2007). This isotherm is associated with the temperature front that forms the northern boundary of the spawning area of both the American and European eels. McCleave 1994), and migrating silver eels may use this front to identify the spawning area. Changes in the latitude of these fronts could affect both the spawning location and early larval transport towards the Florida Current because currents in this region are likely complex (Reverdin et al. 2003). Length frequency data for American eel leptocephali in the summer and fall suggest that some leptocephali are retained offshore to the east of the Florida Current (McCleave and Kleckner 1987). Therefore, a northward movement of the spawning area could affect the larval transport out of the Sargasso Sea if the strongest westward flow is in the southern areas, such as off the northeast edge of the northern Bahamas where leptocephali of both species were abundant (McCleave and Kleckner 1987). Friedland et al. (2007) also identified potentially important changes in wind-driven factors and mixed layer depth (MLD) in the Sargasso Sea that could affect larval transport or feeding success. Spring wind speeds and southward Ekman transports between 1949 and 2003 were found to have decreased in the northern Sargasso Sea region, possibly contributing to increased larval retention in the Sargasso gyre.

ocean-atmospheric factors influencing spawning and recruitment of anguillid eels 237 Mixed layer depth (m) Ekman depths were about 30 50 m during the first three decades of the time series but have shallowed to 10 20 m in recent years. Spring MLD in the northern Sargasso Sea has also shallowed during February to May since 1985 and for the spring months of March, April, and May during the peak spawning season. This decrease in MLD was observed to have been about 50 100 m, using two different methods of calculation (Figure 4). Because wind stress, eddies, and MLD can affect nutrient levels and primary productivity in the surface layer (Palter et al. 2005), the changes observed could affect the feeding success of both species of Atlantic anguillid leptocephali, as hypothesized by Knights (2003). The hypothesis that recruitment fluctuations of the European eel may be related to feeding success was supported recently by negative correlations between ocean surface layer temperature (0 100 m) in the northern Sargasso Sea and recruitment to Europe (Bonhommeau et al. 2008b). The ocean temperature in the northern Sargasso Sea has increased since about 1970, and an apparent regime shift in sea surface temperature corresponded to sharp decreases in recruitment at seven different sites in Europe from Spain to Germany (Bonhommeau et al. 2008b). Increases in temperature cause lower 0 50 100 150 200 -criterion Pre-1985 1985 onwards h mix -criterion 250 Jan Feb Mar Apr May Jan Feb Mar Apr May Month Figure 4. Changes in the mixed layer depth (MLD) in the northern Sargasso Sea near Bermuda in the 4 months during the spawning season measured using two calculation techniques (adapted from Friedland et al. 2007). productivity (Behrenfeld et al. 2006), so correlations between recruitment and ocean temperature may be reflecting reduced feeding success of leptocephali. Direct measurements of primary productivity in the northern Sargasso Sea were also found to be correlated with a 3-year lag to the Loire River recruitment time series in France (Figure 5), but not those at the other locations (Bonhommeau et al. 2008b). A similar, but more recent study has also found correlations between primary productivity in the northern Sargasso Sea and recruitment of both European and American eels over short periods of 11 or 13 years, at time lags of 2.5 and 1.5 years, for the European and American eels, respectively (see Bonhommeau et al. 2008a). Changes in ocean productivity may also be associated with changes in the length and condition of glass eels recruiting to Europe (Désaunay and Guérault 1997; Dekker 1998, 2004). Changes in the North Atlantic gyres could also affect recruitment success. For example, fluctuations in the strength or location of the Gulf Stream have been proposed as possible factors affecting larval transport (Castonguay et al. 1994). Curry and Mc- Cartney (2001) showed that Gulf Stream transport increased during the positive phase of the NAO in recent decades compared to the negative phase that ended in the early 1970s. This resulted in a strength- Recruitment index 280 2.8 PP 260 2.7 240 2.6 220 2.5 200 2.4 RI 180 2.3 1994 1996 1998 2000 2002 2004 Primary productivity Figure 5. Time-series of a log-transformed recruitment index (RI) of glass eels of the European eel in the Loire River, France, from the 1994 to 2004 recruitment seasons (solid line with circles), and 3-years lagged integrated primary production (PP) in the upper 140 m (mg C/m 2 ; dashed line with squares) in the northern Sargasso Sea near Bermuda from 1991 to 2001 (adapted from Bonhommeau et al. 2008b).

238 miller et al. ening of the subtropical gyre with increased transport, a weakening of the subpolar gyre, and a slight northward shift in the location of the Gulf Stream. Although no correlation was detected between the transport index of Curry and McCartney (2001) and recruitment of glass eels to Europe (Bonhommeau et al. 2008b), this type of change could affect the proportional transport of leptocephali into the northern and southern branches of the Gulf Stream flow or the rates of transport towards Europe. The NAO also appears to be associated with changes in patterns of the northern branch of the Gulf Stream that enters the subpolar gyre, the North Atlantic Drift, as it reaches the northeast Atlantic (Bersch 2002). This could affect leptocephalus transport to the northern part of the range of the European eel. Alternatively, the southern branch flows into the Azores Current, which also has shown apparent changes related to the NAO, such as a slight southward shift and apparent increased recirculation south or west back into the Gulf Stream (Reverdin et al. 2003; Siedler et al. 2005). Therefore, although strengthening of the Gulf Stream might be expected to facilitate successful recruitment to Europe, this increased flow may have caused a strengthening and expansion of Gulf Stream recirculation in recent decades (Curry and McCartney 2001). This could have resulted in increased retention of leptocephali in the western half of the gyre. The various trends mentioned above may reflect changes acting not only in the Sargasso Sea, but also later in the larval migration phase. Significant regime shifts in the physical and biological structure of the northeast Atlantic and North Sea have been observed, affecting a wide range of marine organisms from zooplankton to fishes (Richardson and Schoeman 2004; Hays et al. 2005; Weijerman et al. 2005; Lehodey et al. 2006; Stige et al. 2006). More local factors could be acting on nonfeeding eels as they cross the continental shelf after metamorphosis from the leptocephalus stage. For example, although Atlantic inflow to the North Sea may have increased in association with changes in the NAO, wind-driven currents in the North Sea and inflows of seawater through the Skagerrak-Kattegat straits could have been less favorable for transporting glass and yellow eel into the Baltic Sea (Westerberg 1998; Knights 2003 and unpublished results). The Japanese Eel Spawning Area and Oceanic Conditions The Japanese eel spawns in the westward flowing North Equatorial Current region of the western North Pacific (Tsukamoto 1992), so this species has a general spawning and larval recruitment pattern very similar to that of the American eel in the Atlantic. The North Pacific is also a large subtropical gyre, with the powerful Kuroshio Current being the western boundary current and recirculation occurring in the western part of the gyre. It differs in that the southern border of the Philippine Sea is much further south of the spawning area than it is in the Sargasso Sea, which has the Bahamas and the Greater Antilles along its southern margin (Figure 2). This is important because although the westward flow of the North Equatorial Current is much stronger (Reverdin et al. 1994) than the flow in the southern Sargasso Sea, the North Equatorial Current bifurcates into northward and southward flows at a latitude that can change both seasonally and annually (Kim et al. 2004). The spawning area in the North Equatorial Current may typically be located from about 13 158N to the west of seamounts of the West Mariana Ridge at about 1438E because no leptocephali have been collected further east (Tsukamoto et al. 2003; Tsukamoto 2006). Small 4 5-mm larvae have been collected recently in an area just west of one of these seamounts. All larval records in the past 15 years indicate a limited spawning area (Tsukamoto 2006) just south of a salinity front in the region (Tsukamoto 1992; Kimura and Tsukamoto 2006). To the north of this front, there are many eddies and alternating east and west flows with several countercurrents apparently present (Kaneko et al. 1998; Kobashi and Kawamura 2001), so that region is not good for the transport of leptocephali. Because of the poor transport conditions to the north and the bifurcation of the North Equatorial Current at the western margin of the North Pacific, it appears that the Japanese eel spawning area has ended up being located in a much more precise area than the spawning area of the Atlantic eels (Tsukamoto 2006). Japanese eel leptocephali must avoid becoming trapped in eddies and avoid being entrained from the North Equatorial Current

SOI ocean-atmospheric factors influencing spawning and recruitment of anguillid eels 239 bifurcation zone into the southward transport of the Mindanao Current (Figure 2). This would carry their leptocephali into the Celebes Sea or into the North Equatorial Countercurrent that flows back to the east (Kimura et al. 1994, 2001). The Japanese eel is not distributed in northern Indonesia or the southern Philippines, although there are several other tropical anguillid species living there. Behavioral mechanisms used by leptocephali, such as diel vertical migration into the Ekman layer, have been proposed as possibly facilitating entrainment into the northward flowing branch of the North Equatorial Current that enters the Kuroshio (Kimura et al. 1994). Once in the northward flow, some larvae may be transported into the South China Sea to the south of Taiwan to recruit to the southern parts of their species range, and others are transported north into the Kuroshio in the East China Sea for eventual recruitment to Korea and Japan at the northern extent of their range (Kimura et al. 1999). Possible Oceanic Factors Affecting Recruitment Lat. of salin. front ( N) 20 18 16 14 12 10 81 SOI SF 86 91 96 01 Year Figure 6. Plots of the latitude of the salinity front (SF) along 1378E in the western North Pacific and of the Southern Oscillation index (SOI) from 1981 to 2001. Although the basic geography of spawning and recruitment of the Japanese eel is similar to that of the American eel in the western North Atlantic, there are several different factors that also appear to make the Japanese eel vulnerable to ocean-atmospheric changes. The Japanese eel has a much narrower pathway leading to successful recruitment because entrainment into the southward flow of the Mindanao Current or into a large persistent eddy east of Taiwan near the beginning of the Kuroshio are two possible factors that could reduce recruitment (Figure 2). Kimura et al. (2001) presented evidence that changes in the location of the salinity front typically found at the northern margin of the spawning area could influence the effect of these factors. One possibility is that a steady northward movement of this front in recent decades could have caused more leptocephali to be retained offshore in the large eddy east of Taiwan (Kimura et al. 2001), and consequently contributed to a decline in recruitment since the 1970s. Interannual recruitment fluctuations, however, may be more related to the southward movement of the salinity front in some years, which appeared to correlate to fluctuations of glass eel catches in southern Japan (Kimura et al. 2001). The movement of the front occurs primarily in association with El Niño events (Kimura et al. 2001; Figure 6), which affects the amount of rainfall in the region and therefore the location of the salinity front. The southward movement of the salinity front and presumably its associated eastward countercurrent could contribute to lower recruitment success in several ways. If salinity is an important cue used by silver eels to locate the spawning area, this could result in spawning further south than normal (Kimura et al. 2001; Kimura and Tsukamoto 2006). This would likely result in more leptocephali drifting southward in the Mindanao Current. Alternatively, it could disrupt the westward flow at the appropriate latitude for spawning and reduce the success of entrainment into the Kuroshio due to increased entrainment into eddies or countercurrents. Recent modeling research indicates that a southward displacement of the spawning area from 158N (Figure 7, top panels) during El Niño events to 13.88N and 12.48N (Figure 7, bottom panels) may cause a much higher percentage of leptocephali to enter the Mindanao Current (see Kim et al. 2007). Support for the hypothesis that a southward movement of the salinity front could affect the location of the Japanese eel spawning area was seen in 2002. The salinity front was further south than usual at about 128N in 2002 (Kimura and Tsukamoto 2006), which was a mild El Niño year (Lagerloef et al. 2003) compared to the 1997 1998 El Niño (McPhaden 1999). The 1997 1998 El Niño appeared to cause disruptions in the westward flow in the spawn- 2 1 0-1 -2

240 miller et al. El Niño Jul 1982 15 N spawning No-El Niño Jul 1999 15 N spawning 50 N 40 N 30 N 20 N 10 N El Niño Jul 1982 13.8 N spawning El Niño Jul 1997 12.4 N spawning 0 50 N 40 N 30 N Nov 2002 20 N 10 N 120 E 135 E 150 E 165 E 120 E 135 E 150 E 165 E 0 Figure 7. Plots of modeled trajectories of particles/leptocephali of the Japanese eel in the western North Pacific after being released/spawned at different spawning locations (white circles) in July of various years and latitudes, which show abnormal larval transport resulting from spawning at the more southern locations. Top panels show trajectories when spawning occurs near the northern margin of the spawning area (i.e., salinity front at normal location) during El Niño and normal years. Bottom panels show trajectories when the spawning area was shifted to the south (i.e., salinity front further south than usual) during El Niño conditions (see Kim et al. 2007 for details about modeling procedures). The location where a 42-mm Japanese eel leptocephalus was collected in November in the Celebes Sea outside of the normal species range during the mild El Niño year of 2002 is shown with the white square in the bottom left. ing area in 1998 (Tsukamoto et al. 2003), but the southward movement of the salinity front in 2002 may have caused an increase in entrainment of leptocephali into the Mindanao Current. Direct evidence of entrainment into the southward flow of the Mindanao Current came later in 2002, when a 42.8-mm Japanese eel leptocephalus was collected at 4.98N, 120.98E in the Celebes Sea on November 19 (Figure 7). The specimen was identified genetically, and its otolith microstructure indicated it had likely hatched on about July 22, 2002 (A. Shinoda, Ocean Research Institute, University of Tokyo, personal communication). The collection of 8 11-mm leptocephali just south of the front in 2002 at a lower latitude than in non-el Niño years (Kimura and Tsukamoto 2006), and the observation that drifters released at that time at 128N and 108N moved south into the Mindanao Current, suggested that the leptocephali located south of the front had a high probability of being entrained into the Mindanao Current (Kimura and Tsukamoto 2006). At least part of the flow of this

ocean-atmospheric factors influencing spawning and recruitment of anguillid eels 241 current typically enters the Celebes Sea (Lukas et al. 1991), so leptocephali were likely transported from the southern region of the North Equatorial Current (NEC) into the Mindanao Current and then into the Celebes Sea. The collection of a Japanese eel leptocephalus at this location was the first confirmation of the transport of a larva outside of the range of this species and represents clear evidence of the potential for the southward movement of the salinity front to disrupt larval transport of this species. In addition, it is also possible that changes in the productivity or community structure of the surface layer of the western North Pacific have occurred that affect the survival or growth of Japanese eel leptocephali, as has been hypothesized for the Atlantic eels. Major physical and biological changes have occurred in the northwestern and northeastern Pacific after the PDO shifted state in 1977 (Hare and Mantua 2000; Sugimoto et al. 2001; Lehodey et al. 2006). However, fluctuating but decreasing trends in MLD, nutrients, chlorophyll a, and net community production concentrations also have been detected in the region just to the west of the spawning area along 1378E between 1971 and 2000 (Sugimoto and Tadokoro 1998; Watanabe et al. 2005). Bonhommeau et al. (2008a) also showed evidence of increasing sea surface temperatures in this region, and found a correlation with temperature fluctuations and glass eel recruitment to Japan (Tatsukawa 2003) using a 0.5-year tag. These changes occurred when the Japanese eel showed decreasing recruitment and at latitudes where leptocephali are located, so their early larval migration feeding success may have been affected. In comparison to the changes in the more northern areas of the North Pacific, the impact of the PDO on the conditions in the NEC spawning and larval development areas of the Japanese eel appear to be much less. However, the frequency of El Niño events appear to have increased since the PDO regime shift in the mid-1970s (Kimura and Tsukamoto 2006), which may have had a substantial influence on interannual recruitment fluctuation in the Japanese eel in the past three decades. The effects of regime shifts can interact differently with diadromous species with contrasting life histories, however, because catches of pink salmon Oncorhynchus gorbuscha and chum salmon O. keta in the North Pacific have increased since the late 1970s (Beamish et al. 2009). South Pacific Eels Spawning Area and Oceanic Conditions The spawning areas of the two species of temperate anguillid eels in the western South Pacific have not been determined as clearly as the northern hemisphere species, but they have been presumed to be in the westward-flowing South Equatorial Current (Figures 2 and 8) (Jellyman 1987, 2003). The genetic identification of Australasian shortfin eel leptocephali (22 32 mm TL) in the South Equatorial Current region (Figure 8) to the south of the Solomon Islands supports this hypothesis (Aoyama et al. 1999), as do other recent catches of anguillid leptocephali in the region (Kuroki et al. 2008). Other smaller anguillids were collected just to the northwest of Fiji in the Equatorial Pacific Fresh Pool, a distinct lens of low salinity water in the upper 100 m (Delcroix and Picaut 1998; Hénin et al. 1998) that was present at about 10 178S in August of 1995 (Miller et al. 2006). This hydrographic feature may provide salinity fronts to act as landmarks of the spawning area, as fronts seem to in the northern hemisphere anguillid spawning areas. Spawning by the Australasian shortfin eel in this region would represent a typical location compared to the northern temperate anguillid species because the South Equatorial Current would transport leptocephali westward, and the western boundary current of the western South Pacific subtropical gyre, the East Australian Current, would transport them southward (Jellyman 1987, 2003; Arai et al. 1999; Shiao et al. 2001). The spawning area is likely in the southern part of the South Equatorial Current, which usually has a two-core structure with westward flow in the upper 300 400 m from the equator to about 188S (Delcroix et al. 1987; Kessler and Taft 1987; Roden 1998). Between the two branches of westward flow, there is often a narrow band of eastward flow of the South Equatorial Countercurrent, which is typically between 58S and 108S (Delcroix et al. 1987; Kessler and Taft 1987; Qiu and Chen 2004). The strength of the South Equatorial Countercurrent appears to be greatest in March and weakest in August (Chen and Qiu 2004; Qiu and Chen 2004). At the western margin of the western South Pacific, the South Equatorial Current bifurcates at about

242 miller et al. 5ºN 0 5ºS 10ºS 15ºS 20ºS 25ºS Australia 30ºS 35ºS Coral Sea Western Pacific Ocean EAC SI LH NC SECC Vanuatu NF Tasman Front Fiji New Zealand 150ºE 160ºE 170ºE 180º 170ºW Figure 8. Map of the western South Pacific showing the location where genetically identified Australasian shortfin eel leptocephali (large black circle) were collected on September 4, 1995 (N = 7; 22 32 mm) and where other anguillid leptocephali (large white circles) were collected in August and September 1995 during the KH-95-2 survey for leptocephali based on Aoyama et al. (1999) and Miller et al. (2006). The small white circles show the locations of other stations during the survey where no anguillid leptocephali were collected. The average location of the low salinity fresh pool (salinity < 35.0) is on the northwest side of the dotted line based on Delcroix and Picaut (1998). The major branches of eastward flow originating from the East Australian Current (EAC) are shown based on Ridgway and Dunn (2003). The South Equatorial Current (SEC), South Equatorial Countercurrent (SECC), and the Solomon Islands (SI), are shown. New Caledonia (NC), Norfolk Island (NF), and Lord Howe Island (LH) where Australasian shortfin eels also recruit, in addition to Australia and New Zealand, are labeled. SEC SEC 188S, with the southward branch becoming the East Australian Current (Qu and Lindstrom 2002; Ridgway and Dunn 2003). Such oceanographic features would suggest that that the spawning area of Australasian shortfin eels is located to the south of the typical latitude of the South Equatorial Countercurrent and north of the southern edge of the South Equatorial Current. Spawning in this location would maximize the chance of entering the East Australian Current, which would transport leptocephali southward to where they recruit. However, recent larval dispersal modeling indicates that likely spawning areas of Australasian shortfin eels and New Zealand longfin eels may extend further south than the southern boundary of the South Equatorial Current (Jellyman and Bowen 2009, this volume). Once in the East Australian Current, those leptocephali that recruit to Australia must detrain from the current and move westward. It has previously been suggested that larvae that will recruit to New Zealand must stay in the flow of the East Australian Current that turns eastward and moves across the Tasman Sea (Aoyama et al. 1999). The recent modeling effort by Jellyman and Bowen (2009) indicates that this route is questionable, as the ages at arrival in New Zealand may be too young to accommodate a trans-tasman migration. However, because the geostrophic flow to the north of New Zealand and up to 158S near Fiji is typically to the east (Morris et al. 1996; Qiu and Chen 2004), the leptocephali recruiting to New Zealand may have to move along the flow of the Tasman Front (Tilburg et al. 2001) after being transported southward from the South Equatorial Current by the East Australian Current. The flow of the East Australian Current has been recently shown to have several branches of eastward flow

ocean-atmospheric factors influencing spawning and recruitment of anguillid eels 243 (Ridgway and Dunn 2003), which would explain how this species can recruit to regions ranging from New Caledonia to New Zealand (Figure 8). These possibilities and the results of the recent modeling should be considered in future surveys to find the spawning areas of these eels. The spawning area of the other New Zealand species, the New Zealand longfin eel, is unknown because no leptocephali have ever been identified. Larval duration estimated from otolithometry in glass eels showed that New Zealand longfin eels have a longer leptocephalus stage than Australasian shortfin eels and most other anguillids (Marui et al. 2001; Jellyman 2003). However, females of this species appear to leave their freshwater growth habitats at a more advanced state of reproductive maturation, suggesting that the spawning migration is shorter (Jellyman 1987, 2003). The recent use of satellite pop-up tagging techniques with migrating silver eels has shown potential to assist in understanding their migrations and identifying potential spawning sites (Jellyman and Tsukamoto 2002). Possible Oceanic Factors Affecting Recruitment Because the precise location of the spawning area of Australasian shortfin eels in the South Equatorial Current region is unknown, it is difficult to determine how spawning behavior or early larval development may be affected by changes in oceanatmospheric conditions in the western South Pacific. However, the collection of small anguillid leptocephali in a narrow band of latitude just to the northwest of Fiji and to the south of the Solomon Islands suggests that alterations to the physical environment of the region of the South Equatorial Current on either side of Fiji could affect the spawning area and early larval development or transport of Australasian shortfin eels. Analyses of the effects of ENSO forcing on the upper ocean conditions in the western Pacific have focused primarily on the equatorial region (i.e., Johnson and McPhaden 2000), but the likely spawning area in the southern branch of the South Equatorial Current also appears to be affected by these events. The western South Equatorial Current region is likely the part of the western South Pacific most affected by ENSO events, based on the changes documented in association with the 1997 1998 El Niño. The 1997 ENSO had major effects on the salinity, temperature and current structure of the equatorial Pacific (Delcroix and Picaut 1998; Hénin et al. 1998; Johnson and McPhaden 2000). The surface salinity of this region increased drastically during the 1997 1998 El Niño and the longitudinal fluctuations in the extent of the low salinity fresh pool appear to correspond to changes in the SOI (Gouriou and Delcroix 2002). These effects extended into the northwestern South Pacific, primarily as changes to the fresh pool region to the north and northeast of Fiji. The changes in 1997 1998 were also observed in measures of sea surface height variations in this area, with a lower sea surface height being present as a result of an increase in salinity (Bowen et al. 2006; Qiu and Chen 2006). A smaller reduction of sea surface height also appears to have occurred in association with the 2002 El Niño event (Lagerloef et al. 2003). Variations in the salinity and temperature structure between 108S and 208S also have been seen in earlier multiyear data sets, along with apparent variations in the strength or latitudinal location of the South Equatorial Current (Kessler and Taft 1987; Delcroix and Picaut 1998; Hénin et al. 1998). A change in the surface salinity in this area could be important if the salinity front that likely forms along the edges of the fresh pool plays a role in defining the spawning area in the western South Pacific, as fronts appear to do in the western North Pacific and in the Sargasso Sea (Kleckner and Mc- Cleave 1988; Kimura and Tsukamoto 2006). Apparent salinity fronts were present at the southern edge of the fresh pool north or northwest of Fiji in August of 1993 (Roden 1998) and in August 1995 when anguillid leptocephali were collected in the low-salinity water (Figure 8; Miller et al. 2006). In contrast to the Sargasso Sea where primarily temperature varies across the fronts and the western North South Pacific where salinity varies, in the western South Pacific, both temperature and salinity vary at this latitude and a distinct density front was observed north of Fiji in August by Roden (1998). A westward or northwestward shift in the location of this front in association with ENSO events (Gouriou and Delcroix 2002) could result in a corresponding shift in the location of the spawning area or disruptions in locating the spawning area. A shift in the location of spawn-