Swimming ability of eels (Anguilla rostrata, Conger oceanicus) at estuarine ingress: contrasting patterns of cross-shelf transport?

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1 Mar Biol (2008) 154: DOI /s ORIGINAL PAPER Swimming ability of eels (Anguilla rostrata, Conger oceanicus) at estuarine ingress: contrasting patterns of cross-shelf transport? M. J. Wuenschel Æ K. W. Able Received: 1 June 2007 / Accepted: 27 March 2008 / Published online: 8 April 2008 Ó Springer-Verlag 2008 Abstract The transport of eel early life stages may be critical to their population dynamics. This transport from ocean spawning to freshwater, estuarine and coastal nursery areas is a combination of physical and biological processes (including swimming behavior). In New Jersey, USA, the American eel (Anguilla rostrata) enters estuaries as glass eels ( mm TL) in contrast to the Conger eel (Conger oceanicus) that enters as larger (metamorphosing) leptocephali ( mm TL). To begin to understand the mechanisms of cross-shelf transport for these species, we measured the potential swimming capability (critical swimming speed, U crit ) under ambient conditions throughout the ingress season. A. rostrata glass eels were collected over many months (January June) at a range of temperatures (4 21 C), with relative condition declining over the course of the ingress period as temperatures warmed. C. oceanicus occurred later in the season (April June) and at warmer temperatures ( C). Mean U crit values for A. rostrata ( cm s -1 ) and C. oceanicus ( cm s -1 ) were comparable, but variable, with portions of the variability explained by water temperature, relative condition, ontogenetic stage, and fish length. Travel times to Little Egg Inlet, New Jersey, estimated using 50% U crit values, indicate it would take Communicated by H.O. Pörtner. M. J. Wuenschel K. W. Able Marine Field Station, Institute of Marine and Coastal Sciences, Rutgers University, 800 c/o 132 Great Bay Blvd, Tuckerton, NJ 08087, USA M. J. Wuenschel (&) NOAA NMFS NEFSC, Woods Hole Laboratory, 166 Water Street, Woods Hole, MA 02543, USA mark.wuenschel@noaa.gov A. rostrata *30 and *60 days to swim from the shelf edge and Gulf Stream, respectively. Travel times for C. oceanicus were shorter, *20 days from the shelf edge, and *45 days from the Gulf Stream. Despite differences in life stage, our results indicate both species are competent swimmers, and suggest they are capable of swimming from the Gulf Stream and/or edge of the continental shelf to estuarine inlets. Introduction The transport of larvae and juvenile fish from offshore spawning areas to estuarine nursery habitats is critical to the population dynamics of many marine fishes. Larval transport is a combination of passive (currents, drift, hydrodynamics) and active (fish swimming behavior) processes (Pineda et al. 2007). Many catadromous eels throughout the world utilize estuarine and freshwater nursery habitats that are many hundreds to thousands of kilometers from their oceanic spawning sites. Similarly, complex life histories occur in several eel species such as Anguilla rostrata and Conger oceanicus on the east coast of the US. The recent decline in many eel species that are found in estuaries worldwide and in the North Atlantic (Castonguay et al. 1994a; Haro et al. 2000; Wirth and Bernatchez 2003; Friedland et al. 2007) has brought increased attention to the complex life histories of eels, and our limited understanding of the factors and mechanisms that influence their population dynamics. An effect of the ocean environment on early life history stages has been suggested for North Atlantic eels (A. rostrata and A. anguilla; Castonguay et al. 1994b; Wirth and Bernatchez 2003; Friedland et al. 2007), however, significant gaps

2 776 Mar Biol (2008) 154: exist in our understanding of ocean life stages, including the cross-shelf transport mechanisms for these species. Common features of A. rostrata and C. oceanicus life history are that they (1) spawn in the Sargasso Sea, (2) have leptocephalus larvae that disperse and are ultimately transported by the Gulf Stream in the western Atlantic Ocean, and (3) eventually detrain from the Gulf Stream and migrate to estuarine waters (McCleave 1993; McCleave and Miller 1994; Able and Fahay 1998). Early leptocephalus stages of the two species are similar and thought to drift with prevailing currents, developing the ability to undergo diel vertical migrations as they grow (A. rostrata and A. anguilla [20 mm found at m during day and m at night, C. oceanicus found at m at night with none collected during the day; Castonguay and McCleave 1987). Beyond the leptocephalous stage, however, the life histories of these two species differ. In A. rostrata, metamorphosis presumably occurs outside the continental shelf, and early stage glass eels complete the migration to coastal and inland waters (Tesch 2003). Stage 1 A. rostrata glass eels (Haro and Krueger 1988) do not feed, cross the continental shelf (Kleckner and McCleave 1982; McCleave 1993), and ingress to (i.e. enter) estuaries where they develop pigmentation (stages 2 7; Haro and Krueger 1988), begin feeding, and continue their migration to estuarine and freshwater habitats. Over the course of time (age) and development of A. rostrata glass eels, they decrease in size (TL and weight), even for a period after they begin feeding (Jessop 1998). In contrast, C. oceanicus exit the Gulf Stream and cross the continental shelf as leptocephali, colonizing juvenile estuarine habitats where metamorphosis occurs (McCleave and Miller 1994; Bell et al. 2003; Correia et al. 2004). C. oceanicus decrease in size as they develop into late stage leptocephali and through metamorphosis into the glass eel/juvenile stage, however, they likely continue to feed throughout the pre-metamorphic leptocephalous stage (Mochioka 2003), during cross shelf transport. The conger eel remains in these estuarine waters, without further upstream migration into freshwater habitats. Several studies have indicated that leptocephali and glass eels are good swimmers (Miller and Tsukamoto 2004; Ross et al. 2007), possibly explaining the rarity of A. rostrata and C. oceanicus in ichthyoplankton surveys on the continental shelf (Able and Fahay 1998). Recent discoveries on the swimming ability of the pelagic juvenile stage of reef fishes (Fisher 2005; Fisher et al. 2005; Leis and Fisher 2006; and references therein) have dramatically transformed our understanding of the dispersal and transport of reef fishes; however, at present the swimming ability of early life stages of temperate, estuarine-dependent fishes, including eels, remains unknown. The swimming abilities and energetic costs associated with swimming across the continental shelf may limit the distances/durations that active swimming can operate as a viable transport mechanism, thus defining the potential estuarine ingress locations for progeny spawned at a given location and date. Further, within this range of possible recruitment locations, the energetic cost of swimming may be sufficient to cause a significant decline in condition, and in turn affect subsequent survival (Hoey and McCormick 2004). For many estuarine-dependent marine fishes that spawn offshore (e.g. bluefish), larvae and/or juveniles enter estuarine habitats (ingress) over a protracted period (Hare and Cowen 1993; Able 2005; Taylor et al. 2007) with individuals and/or cohorts arriving at different sizes and levels of condition. Temperate catadromous eels are an extreme case in that they spawn at great distances from ingress locations, have prolonged larval duration, and in the case of A. rostrata do not feed during ingress. Since condition of larval fish may vary in response to environmental variables (McCormick and Molony 1995; Suthers 2000), and correlate with later growth and survival (Hoey and McCormick 2004; Gagliano and McCormick 2007), processes occurring in the ocean stage of eel early life history may affect subsequent survival in estuarine and freshwater habitats, and ultimate recruitment to the adult population. Due to the long larval period and great distance from spawning sites, arrival of ingress stage A. rostrata to estuaries on the east coast of the US occurs over many months with significant variation in size, age, and condition (Haro and Krueger 1988; Jessop 1998; Sullivan et al. 2006). A decrease in mean total length of ingressing A. rostrata glass eels was reported over the course of the ingress season in New Jersey from a 16-year time series of weekly plankton samples (Sullivan et al. 2006), with significantly smaller eels collected later in the *6-month ingress season. The ingress of C. oceanicus to east coast estuaries is generally less protracted (Able and Fahay 1998; Bell et al. 2003); however, like A. rostrata, variations in size at ingress have been observed (Witting et al. 1999; Bell et al. 2003). Therefore, for many species that ingress over many months such as A. rostrata and C. oceanicus and exhibit variable size and condition at ingress, condition indices may provide insights into understanding variations in recruitment when assuming that condition and survival probability are correlated (Anderson 1988; Suthers et al. 1992). Further, migratory behavior and the selection of settlement and juvenile habitats may be influenced by physiological condition, as has been documented in the European eel A. anguilla that change from freshwater to saltwater preference as body condition decreases (Edeline et al. 2004, 2006). To help elucidate potential mechanisms for cross-shelf transport and ingress of A. rostrata and C. oceanicus, which differ in the timing of estuarine ingress and

3 Mar Biol (2008) 154: developmental stage at ingress, we studied the critical swimming speed (U crit ) and relative condition of ingress stage leptocephali and glass eels of these species throughout their season of ingress. U crit is a special case of prolonged swimming where velocity is gradually increased at set intervals until the point of complete fatigue, when both aerobic and anaerobic resources are exhausted (Brett 1964; Beamish 1978; Lurman et al. 2007). U crit provides a maximum performance measure of the speed fish can swim and is useful for comparison to swimming capability of other species (especially reef fishes) that also travel long distances. Further, U crit has been found to be highly correlated with both sustained (24 h) swimming ability in a flume (Fisher and Wilson 2004) and in situ swimming speed of settlement stage reef fish larvae in the field (Leis and Fisher 2006), and can therefore be used to estimate longer-term swimming ability. In this study, we measured swimming ability and relative condition of A. rostrata and C. oceanicus upon ingress to Little Egg Inlet, New Jersey throughout the ingress season. These data provide the first estimates of swimming speeds for ingress stages of these species, and are used to evaluate possible transport pathways and mechanisms. Methods Specimen collection at ingress Ingressing A. rostrata and C. oceanicus were collected with a 1 m diameter plankton net (1 mm mesh) deployed from a bridge over Little Sheepshead Creek just inside Little Egg Inlet (Fig. 1). The net was fished at the surface (0 1 m) during night-time flood tides for 30 min per set. The physical and biological characteristics of this sampling location have been previously described (Witting et al. 1999; Bell et al. 2003; Sullivan et al. 2006). Additional C. oceanicus (n = 28) were collected using artificial habitat collectors constructed of polyethylene rope fibers (Silberschneider et al. 2001). The collectors were deployed in an embayment of Schooner Creek, a portion of which serves as the Rutgers University Marine Field Station (RUMFS) boat basin (Fig. 1). These collectors were retrieved periodically (twice weekly) during morning daylight hours to remove eels. All eels were immediately transported to the laboratory (RUMFS) and held in aquaria at ambient temperature and salinity until introduction into the swimming flume (within 3 h of capture). Swimming experiments were carried out in a multichannel experimental swimming flume similar in design to that of Stobutzki and Bellwood (1997), supplied with ambient seawater (temperature and salinity approximately equal to that of the capture location). The apparatus Fig. 1 Map of the study area in southern New Jersey, USA, indicating locations of ichthyoplankton sampling at Little Sheepshead Creek (filled circle) and the Rutgers University Marine Field Station on Schooner Creek (filled square) where artificial habitat collectors were deployed and experiments were conducted consisted of multiple lanes ( mm), with flow straighteners at the mouth of each channel to reduce turbulence. The swimming lanes were large enough to allow eels to swim unencumbered, as the tail tip amplitude for eels has been estimated to be 10% of total length (Hess and Videler 1984). A pump circulated water through the system and a calibrated gate valve controlled the volume of water passing through the flume. Individual A. rostrata glass eels and C. oceanicus leptocephali were swum in the flume at low light levels (3 10 lux), and monitored continuously with the aid of an infrared video system to record swimming behavior and time at exhaustion. Additional C. oceanicus were swum in the flume under lighted ( lux) conditions. Flow rate, and therefore swimming speed, were calculated as the flow volume per unit time (ml s -1 ) divided by the cross-sectional area (cm 2 )ofthe flume channels. Flow rates in the flume were calibrated weekly. Swimming ability The maximum swimming speed of ingress stage A. rostrata and C. oceanicus was determined in a method similar to that for larval reef fish (Bellwood and Fisher 2001). Eels were placed in the swimming flume and allowed to acclimate for 10 min at flow rates of *2.2 cm s -1 prior to the start of the experiment. Water speed was incrementally increased by *4.0cms -1 every 3 min until the fish no longer maintained position in the swimming channel and became impinged on the rear screen. The speed and the time spent in the last flow rate interval were recorded, and

4 778 Mar Biol (2008) 154: critical swimming speed (U crit ) was calculated as: U crit = U + (t/t i 9 U i ), where U is the penultimate speed, U i is the velocity increment (*4 cms -1 ), t is the time swum in the final velocity increment, and t i is the set time interval for each velocity increment (3 min) (Bellwood and Fisher 2001; Green and Fisher 2004). After exhaustion, individuals were removed from the flume, immobilized in MS-222, and their total length (TL) measured (±0.1 mm) with calipers. A. rostrata glass eels were staged based on pigment patterns following Haro and Krueger (1988). C. oceanicus were staged following Bell et al. (2003) based on the percentage preanal length, dentition and pigment patterns. Subsequently, individual eels were placed in pre-weighed aluminum pans; their wet weight (WW, ± g) recorded, and placed in an oven (70 C) for 48 h before final dry weight (DW, ± g) was determined. The dry weight percentage (%DW, unitless) was calculated as DW/WW. An index of relative condition was constructed using the residuals from the regression fit of log-transformed lengths and dry weights (DW) for each species and life stage: Relative conditionðrc; unitlessþ ¼ ðactual DW predicted DWÞ= ðpredicted DWÞ Thus, positive condition index values indicate greater weight than predicted by the regression, and negative values indicate lesser weight than predicted (Limburg and Ross 1995; Jessop 2003). Measures of relative condition were used to describe the seasonal patterns of condition and to evaluate if higher condition individuals were better swimmers (i.e. higher RC & higher U crit ). We estimated sustained swimming speeds as 50% of U crit following Fisher and Wilson (2004) and Leis and Fisher (2006). The sustained swimming speeds were then used to calculate potential distances traveled over 10, 30, and 60 days assuming constant swimming. These distances were plotted in relation to the capture location, shelf bathymetry, and average location of the northern wall of the Gulf Stream (data obtained from pubs/abs/jc/1999jc900133/1999jc html). Statistical analysis Observations were made at ambient conditions; temperatures and relative condition levels both varied over the course of the ingress season (see below) limiting direct partitioning of the effects of these factors. To evaluate the effects of temperature, total length and relative condition of eels on critical swimming speed we used multiple regression to determine the significance of temperature, relative condition and total length on U crit. The following model was used for each species (and stage): U crit ¼ a þ b T þ c TL þ d RC where U crit (cm s -1 ) is modeled as a linear response to temperature (T; C), relative condition (RC; unitless) and total length (TL; mm). The model constant a, and parameters b, c, and d were estimated in SAS. The magnitude of the temperature effect on U crit within species and life stages was evaluated by calculating the Q 10 : Q 10 ¼ R 10 T 2 ð 2 T 1 Þ R 1 where, R 1 and R 2 are U crit (cm s -1 ) at temperatures T 1 and T 2. Results Patterns at ingress Anguilla rostrata and Conger oceanicus differed in several ways at ingress. The majority of A. rostrata collected and used in the U crit experiments were stage 1 glass eels. Despite being a uniform developmental stage, there was a wide range in length ( mm) and wet weight ( mg) of stage 1 A. rostrata at ingress (Table 1), with some individuals being three times heavier than others. Very few (4.3%) were stage 2, and these were slightly smaller than stage 1 glass eels with a large overlap in size. C. oceanicus were collected later in the season (April June), and at warmer temperatures ( C) than A. rostrata (January June; C). Fewer C. oceanicus were collected, and these were pooled into two groups; stages ER M1 (66.1%), and stages M2 M3 (33.9%). There was also a large range in size ( mm) and wet weight ( mg) for ingress stage (ER M1) C. oceanicus, and their mean weight (1003 mg ± ) was more than five times the mean weight of stage 1 A. rostrata (180 mg ± 35.46). The dry weight percentage of C. oceanicus was much lower than that for A. rostrata, with earlier life stages (C. oceanicus stage ER M1) having higher water content, indicated by lower percentage dry weight than later life stages (C. oceanicus stage M2 M3; Fig. 2). The percentage dry weight of C. oceanicus increased through development as they decreased in total length during their metamorphosis to the glass eel stage, approaching levels similar to A. rostrata glass eels. The relative condition of stage 1 A. rostrata declined throughout the ingress season, as water temperatures increased (Fig. 3). The majority of A. rostrata collected later in the season, when temperatures were warmer, had lower relative condition. The C. oceanicus were collected over a shorter time period, and there was no trend in condition

5 Mar Biol (2008) 154: over the course of ingress or in relation to temperature (Fig. 3). Swimming ability Most of the eels voluntarily swam in the flume against the water current; however, a low percentage (17% overall) failed to swim/orient against the current at the acclimation and lowest flow rates and were excluded from further analyses (Table 1). A. rostrata U crit were cm s -1 for stage 1 and cm s -1 for stage 2 glass eels whereas C. oceanicus U crit ranged from 12.0 to 26.8 cm s -1 for ER M1 stage transforming leptocephalii and cm s -1 for M2 M3 stage individuals. Within species and life stage, temperature was the most significant factor in the multiple regression models for U crit (Table 2; Figs. 4, 5); however, species and stage specific models explained only small portions of individual variability in U crit (r 2 = ; Table 2). The relative condition was significant in the model for stage 1 A. rostrata, but not significant for stage ER M1 C. oceanicus. The total length did not have a significant effect on U crit for any of the species/life stages (Table 2; Figs. 4, 5). In C. oceanicus, later stages (M2 M3) showed greater variability in U crit with respect to temperature, length and relative condition as compared to earlier stages (ER M1). Within species, mean U crit was generally higher for earlier life stages (13.3 cm s -1 stage 1 A. rostrata; 18.6 cm s -1 stage ER M1 for C. oceanicus) than later stages (11.7 cm s -1 for stage 2 A. rostrata; 14.7 cm s -1 for stage M2 M3 C. oceanicus); however, differences in temperature ranges and sample sizes precluded detailed analyses between life stages. The predicted rate of increase in U crit with temperature, quantified as Q 10, varied by species and Fig. 3 Relative condition of a Anguilla rostrata (stage 1, open circle; stage 2, filled circle) and b Conger oceanicus (stage ER M1, open square; stage M2 M3, filled square), and c weekly temperature during the period of ingress. Data markers are offset so that error bars can be seen clearly Fig. 2 Dry weight percentage in relation to total length for Anguilla rostrata (stage 1, open circle; stage 2, filled circle), and Conger oceanicus (stage ER M1, open square; stage M2 M3, filled square). See text for stage descriptions life stage (Table 3) and ranged from 1.06 (calculated over the range C) for stage 2 A. rostrata to 2.16 (calculated over the range C) for stage M2 M3 C. oceanicus. Sustained swimming ability was estimated as 50% mean U crit values for each species and life stage (Table 3) to calculate cross-shelf transport times. Plots of the estimated straight line swimming times to Little Egg Inlet, NJ calculated for stage 1 A. rostrata were *30 days from the shelf edge and 60 days from the average position of the Gulf Stream for the line perpendicular to the shore (Fig. 6). If transport occurs more parallel to the coast from the south, swimming times to Little Egg Inlet, NJ for A. rostrata would be *60 days from the shelf and *80 days from the Gulf Stream. In contrast, estimates for

6 780 Mar Biol (2008) 154: Table 1 Summary of eel sizes (total length, wet weight, dry weight, and dry weight percentage), temperatures, and numbers of eels that were used in experiments (both those that swam and those that did not and were removed from subsequent analyses) for each species Collection period Anguilla rostrata Conger oceanicus Stage 1 Stage 2 Stage ER M1 Stage M2 M3 1 March 2006 to 6 June January 2007 to 12 April April 2006 to 25 April April 2006 to 23 June May 2006 to 23 June 2006 TL (mm) 59.1 ± 2.84 ( ) 54.8 ± 3.57 ( ) ± 9.97 ( ) 76.5 ± 5.65 ( ) Temperature 12.5 ± 3.28 ( ) 13.7 ± 2.42 ( ) 19.2 ± 2.97 ( ) 22.0 ± 2.34 ( ) ( C) Wet weight (g) ± ( ) Dry weight (g) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) Dry weight (%) 21.0 ± 0.94 ( ) 19.9 ± 1.02 ( ) 9.5 ± 1.65 ( ) 15.1 ± 2.09 ( ) n (did not swim) n (swam) a 15 b Swam (%) Values reported are mean ± SD (minimum maximum). Stages based on Haro and Krueger (1988) for Anguilla rostrata and Bell et al. (2003) for Conger oceanicus a Twenty-six individuals collected from plankton net and swam in the dark; six individuals collected in eel collectors and swam in lighted conditions b Two individuals collected in ichtyoplankton net and swam in the dark; thirteen individuals collected in eel collectors and swam under lighted conditions C. oceanicus were less; *20 days from the shelf edge, and *45 days from the Gulf Stream along a track perpendicular to the coast, and *30 days from the shelf edge and *60 days from the Gulf Stream along the more southerly track parallel to the coast. Discussion Patterns at ingress The timing of ingress for eels utilized in this study is consistent with previous studies at this location (Witting et al. 1999; Able and Fahay 1998; Sullivan et al. 2006). In a 16-year study of A. rostrata ingress at Little Inlet, NJ, Sullivan et al. (2006) found low water temperatures delayed arrival and decreased the abundance of stage 1 and 2 glass eels, and additionally that there was a significant decline in size at ingress during the *6-month ingress season. Jessop (1998) reported declines in length, mass and condition of A. rostrata over the course of the ingress season to the Bay of Fundy and Atlantic coast of Nova Scotia, with a concurrent increase in pigmentation; however, he sampled the upper estuary and included more pigmentation stages (stage 1 7) than the current study (stage 1 2) making it difficult to interpret declines in length and mass due to development versus individual condition. We limited our analyses to ingress stages for A. rostrata and C. oceanicus, and determined stage specific relative condition of individuals for both species to reduce potential changes during development. Further, ingressing individuals used in this study were collected throughout the previously documented periods of ingress at this location in order to encompass the broad ranges in environmental conditions and individual size and relative condition observed for these species at this location. The seasonal patterns in temperature and condition (higher condition eels were collected earlier in the season at lower temperatures, and lower condition eels were collected later in the season at higher temperatures) limited analysis of their direct effects on U crit. The decline in condition of A. rostrata over the study period, as temperature increased, resulted in few individuals with positive relative condition being tested at higher temperatures which may have reduced our estimates for U crit at higher temperatures and masked even more significant effects of temperature and relative condition. However, the lower condition of later cohorts of A. rostrata ingressing glass eels may be due to one or more of the following: (1) later cohorts are older with a longer postmetamorphic period thus depleting more stored energy reserves; (2) higher metabolic costs at higher temperatures use up more of the stored energy reserves during the cross-shelf (non-feeding) period; and (3) anguilliform locomotion typical of these

7 Mar Biol (2008) 154: Fig. 4 Critical swimming speeds (U crit ) for Anguilla rostrata glass eels as a function of a temperature, b total length, and c relative condition. Lines depict predicted relations from the significant multiple linear regression for stage 1 glass eels, calculated for the range of data for each variable plotted on the x-axis, at the average value for the other parameters in the model. Stages of glass eels denoted by (stage 1, open circle; stage 2, filled circle) Fig. 5 Critical swimming speeds (U crit ) for Conger oceanicus leptocephali as a function of a temperature, b total length, and c relative condition. Lines depict predicted relations from the significant multiple linear regression for stage ER M1 leptocephali, calculated for the range of data for each variable plotted on the x-axis, at the average value for the other parameters in the model. Stages of eels denoted by (stage ER M1, open square; stage M2 M3, filled square) species is more efficient in viscous fluid regimes (Blaxter 1986; Webb and Weihs 1986). Water viscosity decreases as temperature increases, therefore swimming efficiency is likely lower for later cohorts swimming in warmer waters. Alternatively, the earliest cohorts of A. rostrata may experience warmer waters (Fig. 5) before temperatures reach minimum values on the northeast continental shelf of the US in late February early March (Mountain and Holzwarth 1989), enabling them to be more active and cross the shelf in less time than later cohorts with reduced activity at lower temperatures. Clearly, future studies need to consider seasonal and temperature effects on ingress of A. rostrata throughout their broad range. Ingress of C. oceanicus leptocephali occurred over a shorter period at warmer temperatures, and there was no trend in condition over the ingress period, nor was relative condition significant in either of the multivariate models describing U crit for C. oceanicus. Swimming ability Swimming performance is considered to be an important factor in the survival of fishes (Plaut 2001), especially early life stages that travel great distances and experience high mortality, and this may be especially important for species that spawn in the ocean but must reach estuarine nurseries. We chose to use critical swimming speed (U crit ) to assess swimming ability for the following reasons: (1) U crit has proven useful in understanding dispersal, recruitment, ingress and connectivity of reef fishes (Stobutzki 1997; Stobutzki and Bellwood 1997; Bellwood and Fisher 2001; Green and Fisher 2004; Leis and Fisher 2006; Grorud-

8 782 Mar Biol (2008) 154: Table 2 Parameter estimates from multivariate linear regression models for U crit of eel species and life stages as a function of temperature, total length, and relative condition Model parameter Species Anguilla rostrata Conger oceanicus Stage 1 Stage 2 Stage ER M1 Stage M2 M3 Intercept (a) Temperature (b; C) *** ** Total length (c; mm) Relative condition (d) * Model r *** *** n Stages determined as in Table 1. Models were of the form U crit = a + b 9 temperature + c 9 total length + d 9 relative condition. Significance of the model parameters is noted as: *P \ 0.05; **P \ 0.01; ***P \ Table 3 Mean critical swimming speed (U crit ) and Q 10 for eel species and life stages ingressing into Little Egg Inlet, New Jersey predicted from multiple regression models Species Stage U crit [±95% CI] (cm s -1 ) Q 10 Estimated sustained swimming distance (km day -1 ) Anguilla rostrata [0.675] 1.58 (5 15 C) [1.695] 1.06 (10 15 C) 5.00 Conger oceanicus ER M [1.365] 1.73 ( C) 7.99 M2 M [3.488] 2.16 (16 25 C) 6.31 Sustained swimming distance per day was estimated as 50% U crit (see text for further explanation), where constant swimming at 28 cm s -1 = km h -1. Temperature range used for Q 10 calculation is indicated in parentheses. Stages determined as in Table 1 Colvert and Sponaugle 2006); (2) it has been shown to be highly related to sustained and in situ swimming ability in early life stages of fishes (Fisher and Wilson 2004; Leis and Fisher 2006); and (3) a recent review (Plaut 2001) concluded that U crit is the best ecophysiological measure of swimming performance in fishes because it can be correlated to other more ecologically relevant traits. Although prolonged swimming ability of individuals (and total distance possible) may be underestimated, since fish are not allowed to rest or feed during the trials (although stage 1 A. rostrata do not feed) U crit is a useful measure of the ability of fishes to modify their spatial distribution in their natural environments. Temperature had a significant effect on U crit for stage 1 A. rostrata and stage ER M1 C. oceanicus with Q 10 values calculated from the predictive models of 1.58 and 1.72, respectively (Table 3). A Q 10 of *2 is common for many physiological processes, which indicates a doubling (of in this case U crit ) with each 10 C increase in temperature. For A. rostrata, the increase in the maximum U crit values from 5 to 15 C showed a steeper increase with temperature, before leveling off, therefore the Q 10 may be closer to two at lower temperatures. At higher temperatures (15 20 C), U crit of A. rostrata increases more slowly with temperature, possibly due to decreased efficiency or stress. The U crit of C. oceanicus, from 15 to 25 C, did not appear to level off at higher temperatures indicating they may be better adapted to swimming at these temperatures. The swimming ability of eels from this study is consistent with other observations of glass eel swimming ability; however, since prior studies did not employ U crit methodology direct comparisons are difficult. More advanced A. anguilla (later developmental/pigment stage glass eels, stage VI A i VI A iv, equivalent to stage 2 6 for A. rostrata) were able to swim at 30 cm s -1 for 3 min (McCleave 1980). Therefore, under the U crit protocol employed in the current study we would not expect U crit values greater than 30 cm s -1 (given the *3 min incremental increases in velocity), which is slightly higher than the maximum values of U crit we found for A. rostrata. Barbin and Krueger (1994) studied the swimming ability of A. rostrata elvers (glass eels; unknown stage, mm TL), indicating they were able to travel against the flow in a substrate-less chamber at water speeds up to about 40 cm s -1. The chamber they used had turbulent flows designed to simulate stream conditions, with a significant boundary layer present, allowing eels to find refuge in boundary layers, and exploit burst speeds of short duration. Langdon and Collins (2000) studied the swimming ability of Australasian glass eels (A. australis and A. reinhardtii),

9 Mar Biol (2008) 154: Fig. 6 Estimated straight line distance traveled to Little Egg Inlet, New Jersey (open triangle) in 10, 30, and 60 days for Anguilla rostrata glass eels (stage 1; dashed circles) and Conger oceanicus leptocephali (stage ER M1; solid circles). The shelf edge is indicated by the 200 m isobath, and the average position of the northern wall of the Gulf Stream (filled circles). Lines represent pathways perpendicular (a) and parallel (b) to the coast. See text for further explanation finding these species able to maintain swimming speeds of 29 and 32 cm s -1, respectively for 30 min period. Although the methodologies differed between studies, our results for A. rostrata seem comparable and thus reasonable. To our knowledge there are no laboratory estimates of swimming ability for C. oceanicus or the leptocepahlus stage of other eels available for comparison. However, in a recent review, Leis and Fisher (2006) compiled U crit for settlement stage reef fishes from 11 families (not including eels) ranging from 11.3 to 61.5 cm s -1. Mean U crit determined for the species and life stages of eels in this study ( cm s -1 ) are within the range, but below the overall mean for reef fishes (36 cm s -1 ). This is not surprising considering the lower temperatures used in the present study ( C) compared to the studies on reef fishes (20 30 C), the significant effect of temperature on U crit demonstrated in this study and others (Green and Fisher 2004), and the differences in swimming modes between eels and reef fishes. U crit values for both A. rostrata and C. oceanicus were variable, with only a portion of the variability explained by water temperature, relative condition, and fish length for each species/life-stage (Table 2). Some of this variability may have been due to the fact that eels were collected with an ichthyoplankton net and artificial habitat collectors (as opposed to light traps for many reef fishes), which may have caused some degree of stress. However, A. rostrata glass eels and metamorphosing C. oceanicus are relatively hardy at these ontogenetic stages, indicated by the high percentages that swam in the flume, and based on previous experience holding specimens in the laboratory that fed, grew and metamorphosed (Bell et al. 2003). Other sources of variation in individual performance may include previous history. Since collections were generally limited to night-time incoming tides, fish were collected at various tide stages and hours of darkness. Some individuals may have been active for longer periods prior to measurement of U crit and therefore more fatigued than others. Circatidal activity patterns in A. rostrata have been reported; however, they break down over time when eels are held in the laboratory (Wippelhauser and McCleave 1988). Given these limitations, we chose to run experiments as soon as possible after collection to reduce alteration of behavior in captivity. Therefore, the mean critical swimming speeds reported here should be considered conservative estimates, since the maximum values observed were much greater than the mean. Studies on swimming ability of early life stages of fishes (mostly reef fishes) have not considered the relative condition of individuals, and generally encompass narrower ranges in temperatures than the present study. Temperature increased significantly during the ingress season and condition declined for A. rostrata (Fig. 3), and we found relative condition had significant effect on U crit for stage 1 A. rostrata, despite the following qualifiers. U crit is a short term measure of swimming ability, and individuals in relatively poor condition may be able to perform at similar levels to higher condition individuals for short periods of time. We might expect that relative condition would have a greater effect on sustained swimming abilities (long-term, 24 h and greater) of stage 1 A. rostrata since they do not feed during this ontogenetic stage. In contrast, relative condition did not have a significant effect on U crit of stage ER M1 C. oceanicus. This may be a reflection of several factors, including lower sample sizes and variation in condition for C. oceanicus, and the more limited time and temperature ranges of ingress. In addition, since C. oceanicus ingress as leptocephali, presumably continue to feed, and have reduced glass eel stage duration (Bell et al. 2003) relative condition may be less of a factor as compared to A. rostrata. Swimming ability of later stage C. oceanicus was generally lower and more variable than for early stage C. oceanicus. Reduced swimming ability of transitional stage C. oceanicus may be due to the dramatic changes in size and body composition (indicated by dry weight percentage, Fig. 2) that accompanies metamorphosis from leptocephali to glass eel stages.

10 784 Mar Biol (2008) 154: Implications for cross-shelf transport Both C. oceanicus leptocephali and A. rostrata glass eels demonstrated competent swimming ability. Their mean U crit values (12 19 cm s -1 ) are greater than the average along-shelf current of the Middle Atlantic Bight (SW at 5 10 cm s -1, Hare and Cowen 1993), and about equal to average along shelf speeds in the slope region of the northeast continental shelf of the US (15.4 ± 4.9 cm s -1, Hare et al. 2002), but less than the average speed of the Gulf Stream (N NE at ± 38.2 cm s -1, Hare et al. 2002). Since fishes are unlikely to maintain U crit in the wild, these two species appear unable to overcome Gulf Stream and slope currents; however, the life stage that crosses the shelf has the ability to swim at speeds greater than the mean prevailing shelf current and thus alter their spatial distribution. Due to the complex, distant, and enigmatic properties of eel early life history, an experimental ecology approach such as this provides a means to study factors affecting eels in the ocean where they are sparse and difficult to sample (Suquet et al. 2005). A strong relationship between U crit and sustained swimming ability (speed fish can maintain for 24 h) has been demonstrated for nine species of tropical fishes recruiting to reefs, with sustained swimming ability being approximately 50% of U crit (Fisher and Wilson 2004). In those instances, U crit explained 64% of the variation in sustained swimming speed, whereas total length only explained 33% of the variation in sustained swimming. Similarly, Leis and Fisher (2006) found a strong relationship between U crit and in situ swimming speeds of released settlement stage larvae recruiting to reefs. Their data, across 11 families of reef fishes, indicated that in situ speeds were *50% of U crit, demonstrating the applicability of laboratory derived U crit to fishes in the wild. If we assume A. rostrata glass eels and C. oceanicus leptocephali sustained and/or in situ swimming speeds are *50% of U crit (13 19 cm s -1 ), resulting estimates of sustained swimming speeds for these species are ( cm s -1 ) enabling them to potentially travel distances of 6 8 km day -1. During a preliminary trial in which water velocity was held constant, we observed a stage 1 A. rostrata at 12 C swim for [1 hat*20 cm s -1. Therefore, we believe our estimates of sustained swimming ability based on 50% of the mean U crit provide useful first approximations of endurance swimming for these species and life stages. The potential travel distance estimates (above) assume eels can maintain a bearing, with any variability in orientation decreasing the realized distance traveled. Directional swimming has been demonstrated in young reef fish larvae (Leis et al. 2007); however, the orientation ability of eels remains unknown. Larval behaviors (including swimming) act in concert with oceanographic processes to determine the transport of pelagic early life stages (Pineda et al. 2007). The temperature threshold for swimming behavior of glass eels (A. anguilla and A. rostrata) held in aquaria was estimated to be between 4 and 7 C (Linton et al. 2007). Further, Williamson (1987) observed three transparent A. rostrata glass eels drifting vertically in the nearshore waters off Newfoundland at a temperature of 7 C, therefore temperature plays a role in the behavioral aspect of eel transport. In the present study, A. rostrata swam against the current at low temperatures (4 7 C) in the flume, but their swimming ability was greatly reduced at these temperatures (Fig. 4). Higher temperature thresholds have been reported for freshwater migration of A. rostrata; 11 C in Georgia (Helfman et al. 1984) and 12 C in New Brunswick (Smith 1955). We attribute low catch rates of A. rostrata at temperatures below a threshold of *7 C in the present and other studies (Sullivan et al. 2006; M.C. Sullivan and K.W. Able, unpublished data) to reductions in activity and occurrence in the water column, possibly limiting transport at low temperatures. In addition to playing a role in the behavioral component of eel transport, temperature affects metabolic rate and therefore the energetic costs of transport. Assuming A. rostrata metamorphose outside the shelf, before beginning their journey to coastal waters (Tesch 2003), otolith based estimates of age (from the metamorphic band to ingress) can be used to determine the duration of the cross-shelf transport. Powles and Warlen (2002) aged ingressing A. rostrata glass eels captured from three estuaries on the east coast of the US and CA. They reported the glass eel (post-metamorphic) period for fish entering the same New Jersey estuary to be 62.3 days (±8.8 days), which agrees with our estimates from Fig. 5, thus indicating it would take glass eels *60 days to swim to Little Egg Inlet from the Gulf Stream (from the southeast). Similar estimates of time between metamorphosis and estuarine arrival were reported for A. rostrata collected in Rhode Island (62.2 ± days; Wang and Tzeng 1998). Lower estimates of post-metamorphic age, *31 days (18 41 days), were reported for A. rostrata recruits to Maine (Arai et al. 2000), which is located farther from both the Gulf Stream and shelf edge, therefore shorter transit times may be possible. Since C. oceanicus ingress as letocephali stages, their transit time cannot be estimated by postmetamorphic age. Travel times for glass eels recruiting to east coast estuaries is undoubtedly influenced by ocean currents as well as swimming ability, and the potential travel distances and times we estimated (Table 3; Fig. 6) do not include ocean currents or diel vertical migrations. Mechanisms of cross-shelf transport of A. rostrata and C. oceanicus are

11 Mar Biol (2008) 154: likely complex and are a function of their ability to both swim and utilize onshore currents to locate suitable nearshore and estuarine habitats. The olfactory abilities of eels are well documented (Tosi et al. 1990; Sola 1995) and significant correlations between precipitation and the abundance of ingressing glass eels suggest increased river discharge may improve the ability of eels to locate and actively migrate to estuaries (Sullivan et al. 2006). Models of transport and ingress will need to consider active swimming ability of ingress stages. Despite differences in life stage traversing the shelf, our results demonstrate the swimming ability of these species, and suggest both species may be able to actively swim great distances in the ocean, from the edge of the continental shelf and the Gulf Stream to east coast estuaries. A better understanding of crossshelf transport mechanisms in eels will be necessary to evaluate eel recruitment and the potential effects of climate induced changes in temperature, precipitation and the position of the Gulf Stream. Acknowledgments The authors appreciate the assistance of staff at the Rutgers University Marine Field Station, especially R. Hagan and S. Zeck in the collection of eels. This paper benefited from discussions with M. Sullivan. Authors thank Jon Hare and anonymous reviewers for comments on earlier drafts of this manuscript. These experiments complied with current laws in the United States and were conducted in accordance with the regulations of the Rutgers University Institutional Animal Care and Use Committee (IACUC). This study was supported in part by New Jersey Sea Grant. This paper is contribution No from the Institute of Marine and Coastal Sciences, Rutgers University. 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