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Sinking rates of late-stage fish larvae: Implications for larval ingress into estuarine nursery habitats
Journal of Experimental Marine Biology and Ecology 330 (2006) 493 – 504 www.elsevier.com/locate/jembe
Sinking rates of late-stage fish larvae: Implications for larval ingress into estuarine nursery habitats Jonathan A. Hare *,1, Harvey J. Walsh, Mark J. Wuenschel 2 NOAA NOS NCCOS, Center for Coastal Fisheries and Habitat Research, 101 Pivers Island Road, Beaufort, North Carolina 28516, USA Received 15 June 2005; received in revised form 1 September 2005; accepted 16 September 2005
Abstract Many species spawn in oceanic waters yet their juvenile stages use nearshore and estuarine habits and the bio-physical mechanisms by which late-larvae enter these juvenile habitats may be an important bottleneck in the population dynamics of these species. To provide parameters for the development of larval ingress models, sinking rates were measured of the late-stage larvae of six fish species: Atlantic croaker (Micropogonias undulatus), spot (Leiostomus xanthurus), Atlantic menhaden (Brevoortia tyrannus), summer flounder (Paralichthys dentatus), southern flounder (P. lethostigma), and gulf flounder (P. albigutta). Species-specific differences were found in sinking rates; Atlantic croaker had the slowest sinking rates and Atlantic menhaden and the three flounder species had the fastest sinking rates. Additionally, sinking rates increased for all species as length increased. The total amount of variability explained in sinking rates was low (20–50%), indicating a large amount of variability at the level of the individual. The observed patterns in sinking rates were then combined with previous studies on the mechanisms of larval ingress to present species-specific conceptual models of ingress. Published by Elsevier B.V. Keywords: Atlantic croaker; Atlantic menhaden; Buoyancy; Gulf flounder; Larval ingress; Sinking rate; Southern flounder; Spot; Summer flounder
1. Introduction Many species of marine fish have oceanic larval stages and nearshore and estuarine juvenile stages. For these species, the entrance of late-larvae into juvenile habitats may act as a bottleneck in the dynamics of the population (Quinlan and Crowder, 1999). A dominant mechanism of larval ingress is selective tidal * Corresponding author. Tel.: +1 401 782 3295; fax: +1 401 782 3201. E-mail address: [email protected] (J.A. Hare). 1 Current address: NOAA NMFS NEFSC, Narragansett Laboratory, 28 Tarzwell Drive, Narrgansett, Rhode Island 02882, USA. 2 Current address: Rutgers University Marine Field Station, Institute of Marine and Coastal Sciences, 800 Great Bay Blvd, c/o 132 Great Bay Blvd., Tuckerton, New Jersey 08087-2004, USA. 0022-0981/$ - see front matter. Published by Elsevier B.V. doi:10.1016/j.jembe.2005.09.011
stream transport, whereby larvae are higher in the water column on flood tides and near the bottom on ebb tides, thus effecting up-estuary transport (Forward and Tankersley, 2001). Other, more passive mechanisms also result in larvae entering estuaries including bottom residual inflow in the gravitational circulation of estuaries (Weinstein et al., 1980; Schultz et al., 2003) and physical events that result in the net transport of water into estuaries (e.g., wind, Shaw et al., 1985). Recent studies have indicated that some species enter estuaries via multiple mechanisms and that the importance of specific ingress mechanisms differ among ontogenetic stages and species (Joyeux, 1998; Churchill et al., 1999a,b; Hare et al., in press). Circulation modeling offers one approach to further examine the mechanisms by which oceanic larvae
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enter estuarine nursery areas. Models can be relatively simple (e.g., one-dimensional sediment-like transport models, Pringle and Franks, 2001) or complex (e.g., three-dimensional circulation models with Lagrangian particle tracking, Xie and Eggleston, 1999; Brown et al., 2004). A number of studies have shown that vertical distribution of larvae in the nearshore and estuarine water column has a large effect on larval transport (Rowe and Epifanio, 1994; Forward and Tankersley, 2001; Hare et al., in press), and thus larval vertical distribution models need to be coupled with physical models to accurately examine the mechanisms of larval ingress. One component of larval vertical distribution is buoyancy of larvae (Sundby, 1983; Aadlandsvik et al., 2001). Most fish larvae are negatively buoyant, causing them to sink (Hoss et al., 1989; Kitajima et al., 1993, 1994a,b, 1998). Energy is needed to keep larvae in the water column: either physical energy in the form of mixing (Sundby, 1983), biological energy in the form of swimming (Leis and Carson-Ewart, 2001; Trnski, 2002) or buoyancy compensation using the swimbladder (Hoss et al., 1989; Govoni and Hoss, 2001). A number of studies have documented diel and ontogenetic patterns in larval density and/or sinking rate (Hoss et al., 1989; Kitajima et al., 1994a,b, 1998; Forward et al., 1994), and individual variability in buoyancy has been linked to condition (Sclafani et al., 1997). For most transport model applications, sinking rate is the needed parameter for developing larval vertical distribution models (e.g., Hare et al., 1999; Aadlandsvik et al., 2001). Sinking rate is function of fish density, ambient water density, and fish drag (Sundby, 1983; Power, 1989). Fish density and ambient density are easily estimated, but drag is complex. Models have been developed to estimate sinking rates of spheres and columns of given densities (Sundby, 1983, 1991; Power, 1989; Aadlandsvik et al., 2001), but these shapes only approximate the body shape of fishes. Thus, measures of fish density are difficult to convert to sinking rate because of the differences in drag resulting from different fish shapes and orientation in the water column. Sinking rate of larvae can also be measured directly (Hoss et al., 1989), and is positively related to larval density (Kitajima et al., 1994a). With such measurements, care must be taken that the ambient water density and experimental water density are known, since larval density can vary with ambient water density (Kitajima et al., 1994a,b). Further, experimental temperature needs to approximate ambient temperature to maintain swimbladder volume, since gas
volume is affected by temperature and changes in swimbladder volume alter buoyancy and therefore sinking rate (Govoni and Hoss, 2001). Our goal was to measure sinking rate of several species of fish that enter estuaries as late-stage larvae: Atlantic croaker (Micropogonias undulatus, Sciaenidae), spot (Leiostomus xanthurus, Sciaenidae), Atlantic menhaden (Breevortia tyrannus, Clupeidae), gulf flounder (Paralichthys albigutta, Paralichthyidae), southern flounder (Paralichthys lethostigma, Paralichthyidae), and summer flounder (Paralichthys dentatus, Paralichthyidae). Late-stage larvae of these species typically ingress through Beaufort Inlet during winter, while moving from oceanic spawning areas to estuarine nursery habitats and while transforming from larvae to juveniles (Hettler and Chester, 1990; Warlen and Burke, 1990). We captured ingressing larvae weekly through the fall and winter of 2004–2005. After capture, we immediately returned to the laboratory and measured sinking rate. Using multiple linear regression, we examined the effects of ambient water density and ontogeny on sinking rate. We were also concerned with the effect of time to measurement of sinking rate in the laboratory. Fish larvae influence buoyancy in part through inflation or deflation of a gas bladder (Hoss et al., 1989; Forward et al., 1993). The buoyancy of fish held in the laboratory for longer periods prior to sinking rate measurements may change as a result of the potential deflation of the swimbladder through diffusion. It is our hope that the resulting estimates of sinking rate prove useful in future studies that use models to investigate larval ingress into nearshore and estuarine habitats. 2. Materials and methods 2.1. Experimental apparatus Sinking rate was measured by releasing anesthetized larvae at the top of columns filled with seawater in the laboratory and measuring the time required for larvae to sink a known distance. Four columns were used, each with water of a different salinity: 15, 20, 25, and 30. Tap water was mixed with Instant Ocean Synthetic Sea SaltsR to achieve target salinities. Columns were placed in a water bath to maintain experimental temperatures near the ambient temperature. Temperature in the water bath was maintained using a temperature controller (1 / 2 hp, 10–18 8C, Aqua Logic, Inc.) and water in the bath was thoroughly mixed using a utility pump. The experimental glass columns were 25 cm high and 22 cm in diameter, and were filled with 23 cm of water. A 10 cm
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measurement zone (from 8 cm below the water’s surface to 5 cm above the bottom) was marked on both the front and the back of each column. 2.2. Measurement of field and experimental water temperature, salinity, and density Approximately 12 h prior to fish collection, ambient water temperature was measured with a hand-held thermometer, and a temperature-controlled water bath was set to this temperature. About 30 min prior to sampling, ambient water temperature was measured again with a hand-held thermometer and the water bath temperature controller was adjusted if necessary. During the collection of fish larvae, ambient temperature and salinity were measured with a CTD (Model 6600-D, YSI, Inc., temperature accuracy F 0.15 8C, salinity accuracy F0.35). The temperature and salinity of water in each experimental column (see below) were also measured using the CTD. Ambient and experimental water density was estimated from ambient and experimental temperature and salinity based on Fofonoff (1985). Depth was estimated as 0.5 m for ambient conditions and 0.05 m for experimental conditions. 2.3. Collection of late-stage larvae Late-stage fish larvae were collected weekly using a 2 m2 plankton net with 947 Am mesh deployed in a channel approximately 1 km inside of Beaufort Inlet, North Carolina (Warlen, 1994). Eleven collections were made from 8 December 2004 to 16 February 2005. Each week, the net was deployed for approximately 20 min during nighttime flood tides following the collection of weekly larval ingress monitoring samples. A 5 L plastic cod-end bucket was attached at the end of the net to assist in keeping fish larvae alive during capture and return to the laboratory. Once the net was retrieved, the cod end was placed in a bucket of ambient seawater. Live fish larvae were picked from the sample and placed in a petri dish containing ambient seawater. Larvae were then anesthetized with tricaine methanesulfonate (MS-222) just prior to sinking rate measurements. Species examined included Atlantic croaker, spot, Atlantic menhaden, southern flounder, gulf flounder, and summer flounder. 2.4. Sinking rate measurements Sinking rate was measured by timing the decent of anesthetized larvae through the marked 10 cm measurement zone in the columns. Standard length of each larva
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was measured to the nearest millimeter and then the larva was placed just below the water’s surface in the middle of the column. A stopwatch was started when larvae crossed the top mark of the measurement zone and was stopped when larvae crossed the bottom mark of the measurement zone. We were concerned that the handling and anesthetizing fish could influence their density, and thus their sinking rate. Either gas could be lost from the swimbladder (e.g., through diffusion) or biochemical reactions could take place that result in a density change. All sinking rate measurements were completed within 1 h of larval fish collection. Also, the order that sinking rate measurements were made was noted (measurement sequence), allowing an estimate of time of anesthesia to be used in data analysis. The number of larvae for which sinking rates were measured depended on the field collections, so weekly sample sizes varied. If many individuals were collected in a given week (approximately N 10), larvae were placed in randomly assigned columns (salinities) with water densities less than ambient conditions. For example, when ambient water densities were low, only columns with salinities of 15 and 20 were used; when ambient water densities were high, columns with salinities of 15, 20, 25 and 30 were used. If only a few individuals were collected in a given week (approximately b10), larvae were placed in a single column (salinity) with water density less than ambient conditions. The number and length of larvae used in sinking rate measurements and the columns used are provided in Table 1. 2.5. Data analysis Multiple regression was used to determine if four variables significantly affected sinking rate. The model used was SR ¼ a þ bd rtAmb rtExp þ cdrtAmb þ ddSL þ edMS where sinking rate (SR cm s 1) is modeled as a linear response to the difference between ambient water density and experimental water density (r tAmb r tExp), ambient water density (r tAmb), length (SL, mm), and measurement sequence (MS, starting at 1 and increasing by 1 for each larva measured each week). The parameter a is the model constant. Linear responses were estimated by parameters b, c, d, and e. Significance of the model parameters was determined based on the a = 0.05 and the r 2 of the model fit also was calculated. Since it would have been very difficult to match ambient conditions in the laboratory owing to changes in temperature and
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Species
Atlantic croaker
Spot
Atlantic menhaden
Gulf flounder
Southern flounder
Summer flounder
Parameter
n Mean SL SD SL Cols n Mean SL SD SL Cols n Mean SL SD SL Cols n Mean SL SD SL Cols n Mean SL SD SL Cols n Mean SL SD SL Cols
Sampling date (December 2004–March 2005) 8-Dec
16-Dec
22-Dec
29-Dec
5-Jan
12-Jan
19-Jan
26-Jan
2-Feb
9-Feb
16-Feb
23-Feb
35 12.17 1.32 1, 2, 3, 4
8 12.00 1.00 1, 2, 3
17 11.88 1.45 1, 2, 3 24 15.21 1.32 1, 2, 3 10 22.50 1.43 1, 3
21 11.48 1.26 1, 2 2 15.00 0.00 2
6 15.50 2.22 3
13 10.46 1.01 1, 2 15 13.73 1.24 1, 2, 3
12 11.25 0.72 1, 2 12 15.92 2.10 1, 2 12 24.00 2.20 1, 2
20 10.45 1.12 1, 2 20 15.75 1.37 1, 2 23 23.96 2.42 1, 2, 3 1 14.00 0.00 2 12 11.75 1.23 1, 2
19 11.84 1.66 1, 2, 3
8 9.50 1.22 3
9 11.33 0.82 2 25 15.24 2.29 1, 2 17 24.29 1.84 2 3 9.33 0.47 2 17 11.47 0.78 1, 2 1 11.00 0.00 1
13 11.46 0.63 1, 2
12 21.58 1.19 1, 2, 3, 4 1 8.00 0.00 3
28 11.14 1.73 1, 2, 3 3 14.33 2.05 3 8 21.00 0.00 3 9 10.00 0.00 3 3 13.00 0.00 3
5 23.00 1.41 3 2 12.00 1.00 2 14 11.57 0.82 1, 2 5 13.60 1.02 2
15 25.20 2.14 1, 2, 3 1 10.00 0.00 2 5 12.40 0.49 1, 2, 3 7 13.43 0.90 1, 2, 3
9 11.44 1.34 1, 2, 3 35 10.23 1.07 1, 2, 3
1 15.00 0.00 3
The experimental columns used (fourth row) contained salinities of 20 (col 1), 25 (col 2), 30 (col 3) and 35 (col 4).
9 11.22 0.63 1, 2 3 14.67 1.25 2
2-Mar
9-Mar
15 27.07 1.88 1, 2
10 11.50 0.81 1, 2, 3 7 16.00 1.20 2, 3 9 25.89 0.99 3
2 12.50 0.50 3 4 13.75 0.43 3
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Table 1 Number (first row), mean length (second row), and standard deviation in length (third row) of late-stage larvae used in sinking rate measurements on 11 dates
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1). Temperature varied from 6.3 to 15.2 8C. Salinity varied from 28.1 to 33.2. The variability in temperature and salinity lead to a broad range of ambient water densities from 21.9 to 25.6 r t. 3.2. Factors affecting larval sinking rate
Fig. 1. Ambient water density (r t), temperature (8C), and salinity during weekly collection of ingressing larval fish. Sampling was conducted from a bridge spanning a channel ~1 km inside of Beaufort Inlet, North Carolina. Samples were collected during nighttime flood tides approximately 2 h before high tide.
salinity during the tidal cycle (see Churchill et al., 1999a), different experimental water densities were used when possible to the allow the effect of ambient density on sinking rates to be quantified. Parameters from the above model then were used to calculate sinking rates at ambient water densities (r tAmb r tExp = 0) and the beginning of the weekly measurements (MS = 1).
The dominant factor in the multiple regression models was the difference between ambient and experimental water densities. All species, except summer flounder, exhibited a significant increase in sinking rate with increasing difference between ambient and experimental water density (Table 2, Figs. 2–7). The increase in sinking rate with increased difference between ambient and experimental water density was greater for Atlantic croaker, spot, and Atlantic menhaden (0.087, 0.106, 0.068 cm s 1 rt 1) than for southern, gulf and summer flounder (0.026, 0.027, 0.003 cm s 1 rt 1). Ambient water density and length also influenced sinking rate. As ambient water density increased, sinking rate decreased for Atlantic croaker and gulf flounder (Table 2, Figs. 2–7). The sinking rates of Atlantic croaker, Atlantic menhaden, and southern flounder increased significantly with larval length (Table 2, Figs. 2–7). Measurement sequence significantly affected sinking rate as well, indicating a change in larval buoyancy following anesthesia. Atlantic croaker, spot, Atlantic menhaden and gulf flounder sank significantly faster as measurement sequence increased (Table 2, Figs. 2–7). 3.3. Sinking rate estimates
3. Results 3.1. Environmental variability Ambient water temperature, salinity, and density varied during the 11 weeks of the experiments (Fig.
Estimates of sinking rates for specific values of the independent variables were derived from the multiple regression models. Of particular interest are sinking rates when there is no difference between ambient and experimental water density (r tAmb r tExp = 0) and
Table 2 Parameter estimates from multivariate linear regression models for the sinking rate of late-stage larvae of six species as a function of the difference between ambient and experimental water density, ambient water density, fish length, and measurement sequence Model parameter
Species Atlantic croaker
Constant (a) 0.526 Density difference (b) 0.087*** Ambient density (c) 0.037* Length (d) 0.031** Measurement sequence (e) 0.015*** Model r 2 0.534
Spot
Atlantic menhaden
Gulf flounder
Southern flounder
Summer flounder
0.481 0.106*** 0.025 0.014 0.011* 0.356
1.480 0.068** 0.017 0.074** 0.016*** 0.195
3.171*** 0.026* 0.091*** 0.019 0.007** 0.429
0.247 0.027* 0.005 0.079** 0.001 0.240
2.356 0.003 0.046 0.011 0.003 0.307
Significance of the model parameters is noted as: *p b 0.05; **p b 0.01, ***p b 0.001.
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4. Discussion 4.1. Experimental artifacts The experiments conducted here reveal two potential artifacts that require consideration: the effect of measurement sequence on sinking rate and potential biological cycles in sinking rate. The significant effects of measurement sequence on the sinking rates of Atlantic croaker, spot, Atlantic menhaden and gulf flounder indicate that the density of larvae changed during the course of a night’s experiment. The likely mechanism is escape of gas from the swimbladder, which would
Fig. 2. Sinking rate of late-stage larval Atlantic croaker (Micropogonias undulatus) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
no time between anesthesia and sinking rate measurements (MS = 1). For these values and at an ambient density of 23.5 r t and average length-at-ingress, Atlantic croaker had the lowest sinking rate, spot had an intermediate rate, and Atlantic menhaden, gulf flounder, southern flounder, and summer flounder had higher sinking rates (Table 3). These sinking rate estimates imply that the body density of larval Atlantic croaker is closest to seawater and that the body density of larval Atlantic menhaden, gulf flounder, southern flounder, and summer flounder is greater than seawater.
Fig. 3. Sinking rate of late-stage larval spot (Leiostomus xanthurus) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
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larval density owing to the experimental methods, either independent to gulf flounder or shared between gulf flounder, spot, Atlantic croaker, and Atlantic menhaden. The effect of measurement sequence in gulf flounder was lower than in the other species, hinting at an unknown mechanism affecting all species and then the loss of gas from the swimbladder as an added mechanism affecting spot, Atlantic croaker, and Atlantic menhaden. Osmoregulatory failure of the anesthetized larvae in our experiments may explain part the gradual increase in sinking rates over time for all species (including those without swimbladders); loss of osmotic control by Gadus morhua larvae was
Fig. 4. Sinking rate of late-stage larval Atlantic menhaden (Brevoortia tyrannus) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
result in larvae becoming heavier. In a preliminary examination, the swimbladders of anesthetized Atlantic croaker, Atlantic menhaden, and spot were smaller after one hour (H. Walsh, unpublished data). The anesthesia (MS-222) may have caused relaxation of the muscular valves that regulate blood flow to the gas removal (oval) region of the swimbladder, increasing resorption of gas from the swimbladder into the blood. Larvae of species in the genus Paralichthys either have vestigial, non-functional swimbladders (Bisbal and Bengtson, 1995) or no swimbladder (J. Govoni, pers comm., NOAA Beaufort Laboratory), so there must be another mechanism that results in increasing
Fig. 5. Sinking rate of late-stage larval gulf flounder (Paralichthys albigutta) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
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specifically examine sinking rates over diel, tidal, or lunar cycles. The experiment was conducted over 11 weeks and encompassed more than three lunar cycles and six spring–neap cycles. However, sampling was passive and was conducted on maximum, nighttime flood tides. Hettler et al. (1997) discussed the inherent confounding of time of sampling in the diel cycle and in the spring–neap cycle when using these collection methods; in our study the circular correlation between time of sampling and time in the spring–neap cycle was 0.843 ( p b 0.001). A number of studies have indicated diel cycles in sinking rate (Hoss et al., 1989; Kitajima et al., 1993, 1994a,b, 1998; Forward et al., 1994).
Fig. 6. Sinking rate of late-stage larval southern flounder (Paralichthys lethostigma) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
shown to increase larval density and influence vertical position, but the causes of bosmotic breachQ were unclear (Sclafani et al., 1997). By including the measurement sequence in the multivariate model of sinking rates, we were able to estimate sinking rates at a comparable measurement sequence for all larvae (Table 3). However, the impact of collection and transport to the lab on sinking rate was not quantified, potentially introducing an unknown error into the estimates presented here. Diel and longer-term cycles also may have influenced the results of this study, but we were unable to
Fig. 7. Sinking rate of late-stage larval summer flounder (Paralichthys dentatus) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
J.A. Hare et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 493–504 Table 3 Estimated sinking rate of six fish species ingressing into Beaufort Inlet as late-larvae Species
Est. sinking rate [F95% CI] (cm s 1)
Atlantic croaker Spot Atlantic menhaden Gulf flounder Southern flounder Summer flounder
0.022 0.121 0.734 0.846 1.253 1.126
[F0.089] [F0.343] [F0.313] [F0.202] [F0.214] [F0.268]
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are comparable with different experimental procedures and generally reflect larval density (Kitajima et al., 1994a). 4.3. General patterns in sinking rate of ingressing larvae
Sinking rate estimates were made from multiple linear regression models (Table 2) with the difference between ambient and experimental water density set at 0, ambient water density set at 23.5 r t. Length set at the average length examined here (see Table 1), and measurement sequence set at 1. 95% confidence intervals (CI) are also provided for the estimates.
Whether there are longer-scale patterns in sinking rates remains a question, but there are certainly spring–neap and lunar patterns in larval ingress and settlement (Tanaka et al., 1989; Sponaugle and Cowen, 1997; Tzeng et al., 2003). Cycles in sinking rate could contribute to the settlement and ingress of larvae owing to the interaction of sinking rate and larval ingress mechanisms. 4.2. Comparison with other studies The estimates of sinking rates derived here compare favorably with other estimates for these and related species. For Atlantic menhaden in the length range of 20–22 mm, Hoss et al. (1989) found sinking rates of approximately 1.2–1.4 cm s 1 compared to 0.734 cm s 1 found here. For lab-reared metamorphic stage summer flounder, estimated sinking rates of 1.1–1.3 cm s 1 (pers. comm. Chaoshu Zeng, James Cook University), compared to 1.126 cm s 1 found here. Hoss et al. (1989) used field caught larvae and made measurements at sea. Zeng (pers. comm.) used lab-reared larvae and made measurements in the laboratory. Owing to the agreement of sinking rate measures, we have confidence that the sinking rate estimates developed here
Several general patterns in sinking rates were evident when comparing the results of the multiple regression models among species (Table 4). For all species except summer flounder, sinking rates increased as the difference between ambient and experimental water density increased. Sinking rate is a function of fish density, water density, and drag and as the experimental water density decreased, sinking rates increased. However, the rate of increase in sinking rates with density difference varied among species. The rate of increase ranged from 0.068 to 0.106 cm s 1 Drt 1 difference for Atlantic croaker, spot, and Atlantic menhaden, whereas the rate of increase was about 0.027 for gulf and southern flounder and 0.003 for summer flounder. These differences in rate are likely caused by differences in drag among the different species. Qualitatively, Atlantic croaker and spot sank headfirst and both Atlantic menhaden and the flounders sank horizontally. The flattened ellipsoid shape of the flounder likely lead to increased drag to the point that drag influenced sinking rate on the same magnitude as the difference between larval density and water density. In hindsight, if we had quantified sinking orientation, perhaps more of the variability in sinking rate could have been explained. The influence of drag on the sinking rate of metamorphic stage flounder leads to the hypothesis that flounder could possibly control their vertical position in a flowing water column by swimming into the flow and changing their aspect ratio. The asymmetrical flattened ellipsoid shape of flounder may act as a foil, with changes in aspect relative to the flow creating an upward or downward force, thereby allowing flounder to easily change position in a flowing water column without adjusting their buoyancy. The non-vertical angle of
Table 4 Summary of the effect of different factors on sinking rates based on the significant terms from the multiple linear regression Species
Inc. r tAmb r tExp
Inc. r tAmb
Inc. length
Measurement sequence
Atlantic croaker Spot Atlantic menhaden Gulf flounder Southern flounder Summer flounder
Inc. Inc. Inc. Inc. Inc.
Dec. SR
Inc. SR
Inc. Inc. Inc. Inc.
SR SR SR SR SR
Inc. SR Dec. SR Inc. SR
SR SR SR SR
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descent for anesthetized flounder larvae in the static columns observed in the present study supports the hypothesis that in the presence of flow, these larvae are able to move up or down in the water column with minimal swimming activity. Activity patterns have been linked to light and salinity in late-larval Japanese flounder, Paralichthys olivaceus (Burke et al., 1995), but the role of lift and drag in keeping flounder in the water column has not been investigated. Ambient density of the water also influenced the sinking rate of larvae (Table 4), but the effect of ambient density was smaller than the effect of the difference between ambient and experimental density. Kitajima et al. (1994a,b) found that larval density decreased with decreases in ambient water density in Japanese flounder and black sea bream, but in relative terms the difference between larval and ambient density increased. The result would be an increasing sinking rate as ambient density decreased, which was the general pattern found here. The implications of this relationship to larval ingress would seem to facilitate retention of larvae within estuaries. Sinking rates increased as larval length increased for all species except summer flounder (Table 4). Many studies have documented ontogenetic patterns in both larval density (Kitajima et al., 1993, 1994a,b, 1998) and sinking rate (Hoss et al., 1989). The implications of increased density and sinking rate are that more energy is needed to keep larvae in the water column as larvae develop. In contrast, it is easier for benthic species to remain near the bottom even in the face of strong vertical mixing, which again would seem to facilitate retention of later-stage larvae within estuaries. Even though sea water density and larval length had significant effects on sinking rate, there still was a large amount of unexplained variability. Regression r 2’s ranged from 0.195 to 0.534, so 50–80% of the variability in sinking rate remained unexplained. Some of this unexplained variability may be related to variability in larval condition. Sclafani et al. (1997) indicated that fish with lower condition were heavier and thus would have a higher sinking rate. The relationship between condition and sinking rate was not examined in this study, but future use of the parameters developed here should include both the means and variance of sinking rate to more accurately capture the dynamics of larval ingress. 4.4. Sinking rates and larval transport Hare et al. (in press) examined three mechanisms of estuarine ingress: bottom layer residual inflow, event-
scale inflow (e.g., wind-driven), and selective tidal stream transport. They concluded that summer flounder use primarily selective-tidal stream transport, Atlantic croaker used a mixture of ingress mechanisms, and Atlantic menhaden used primarily residual bottom inflow and event-driven processes. The sinking rates derived here can be used to further develop the hypotheses regarding larval ingress mechanisms of the different species. Gulf, southern, and summer flounder have relatively high sinking rates and are on the bottom during ebb and slack tides. During flood tides they actively move into the water column, not by adjusting their buoyancy (since they do not have a functional swimbladder), but by swimming up into the water column. On ebb tides, their high sinking rate keeps them on or very near the bottom despite increased vertical mixing resulting from increased flow rates. Thus, these species of flounder use predominantly selective tidal stream transport to enter estuaries. Atlantic croaker have relatively slow sinking rates and their vertical distribution is affected by vertical turbulence more so than Paralichthys flounder, spot, and Atlantic menhaden. During flood and ebb tides, Atlantic croaker move back and forth in the estuary, but by spending most of their time in the lower part of the water column, they move up estuary in the residual bottom inflow. Density discontinuities in the estuarine water column would limit mixing into the upper portions of the water column. During wind events, when vertical mixing is increased, Atlantic croaker are mixed into the water column and move with the water; during the study of Hare et al. (1999), most of the event-scale transport was up-estuary so Atlantic croaker moved upestuary. With some buoyancy control or active swimming that is linked to tidal cycles (12.5 h), Atlantic croaker exhibit up-estuary selective tidal stream transport, but because Atlantic croaker do not go to the bottom (like flounder) nor are they heavy enough to resist vertical mixing, their ability to utilize selective tidal stream transport is compromised by some downestuary movement on ebb tides. Yet, with development Atlantic croaker become heavier and are better able to use selective tidal stream transport to enter estuaries (Hare et al., in press). Spot are similar to Atlantic croaker, but have a greater capacity to utilize selective-tidal stream transport because they have greater sinking rates and are better able to resist mixing into the water column on ebb tides. Hare et al. (in press) did not examine ingress of spot, but Churchill et al. (1999a) concluded that spot were better at utilizing selective-tidal
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stream transport than Atlantic croaker and the sinking rate measurements derived here support their findings. However, like Atlantic croaker, we hypothesize that a combination of ingress mechanisms is important for spot entering estuarine habitats and that the importance of these mechanisms likely changes with development. Atlantic menhaden have a moderately high sinking rate, yet Hare et al. (in press) found that ingress occurred primarily through residual bottom in-flow and event-driven flows. The interpretation is that the high sinking rates keep larvae primarily in the lower part of the water column, but owing to the need to fill the swimbladder at the surface near dusk (Forward et al., 1993), larvae are distributed throughout the water column at specific times of the day and are susceptible to event-driven flows and ebb tides. Batty (1987) studied the swimming behavior of larvae of another clupeid, Clupea harengus, in the laboratory and found that larvae were inactive in the dark except for periodic vertical swimming bouts, which were replaced by horizontal swimming as light intensity increased. During the day, menhaden larvae maintain position in the water column through active swimming, with energetic cost of activity compensated for by the increased search volume and/or prey encounter rates. At light levels below the feeding threshold, menhaden offset their negative buoyancy by inflating their swimbladder, allowing reduced swimming activity costs (which may also reduce interactions with potential predators). The net result for transport is that Atlantic menhaden rely on eventscale processes to enter estuaries more so than the other species examined here. The results of this study and others demonstrate that species use multiple mechanisms to enter estuarine habitats and that ontogeny plays a role (see Joyeux, 1998; Churchill et al., 1999a,b; Hare et al., in press). The energetic costs of ingress will depend, in part, on the sinking rate of larvae. Larvae adjust their position in the water column by regulating their buoyancy (via swimbladder), active swimming, or a combination of these depending on species. Although not investigated in the present study, factors and behaviors related to activity, feeding and predator avoidance likely play important roles in influencing the vertical distribution of larvae in the wild. Thus, the biological characteristics of each species interact with the physical environment to effect movement in the marine environment. The sinking rates determined in this study provide some of the necessary parameters to develop larval vertical distribution models
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to couple with 3-D numerical circulation models (e.g., Hare et al., 1999), which would result in a powerful tool to further examine larval ingress as a potential bottleneck in the population dynamics of species that spawn on the shelf but use estuaries as juvenile nurseries. Acknowledgements We thank Katey Marancik, Gretchen Bath Martin, and Jacqueline Jenkins for helping collect fish larvae and measure sinking rates. Christian Reiss and Michael Greene raised important questions about sinking rate that largely formed the motivation for this study. Chaoshu Zeng provided us with his data on sinking rate for lab-reared summer flounder for comparison. This study was supported in part by a National Science Foundation Grant (OCE 9876565) to C. Jones, S. Thorrold, A. Valle-Levinson, and J. Hare. Jeff Govoni, Christian Reiss, and John Burke reviewed earlier versions of this manuscript. [SS] References Aadlandsvik, B., Coombs, S., Sundby, S., Temple, G., 2001. Buoyancy and vertical distribution of eggs and larvae of blue whiting (Micromesistius poutassou): observations and modelling. Fish. Res. 50 (1–2), 59 – 72. Batty, R.S., 1987. Effect of light intensity on activity and foodsearching of larval herring Clupea harengus: a laboratory study. Mar. Biol. 95, 323 – 327. Bisbal, G.A., Bengtson, D.A., 1995. Development of the digestive tract in larval summer flounder. J. Fish Biol. 47, 277 – 291. Brown, C.A., Holt, S.A., Jackson, G.A., Brooks, D.A., Holt, G.J., 2004. Simulating larval supply to estuarine nursery areas: how important are physical processes to the supply of larvae to the Aransas Pass Inlet? Fish. Oceanogr. Transl. 13, 181 – 196. Burke, J.S., Tanaka, M., Seikai, T., 1995. Influence of light and salinity on behaviour of larval Japanese flounder (Paralichthys olivaceus) and implications for inshore migration. J. Sea Res. 34, 59 – 69. Churchill, J.H., Forward, R.B., Luettich, R.J., Hench, J.L., Hettler, W.F., Crowder, L.B., Blanton, J.O., 1999a. Circulation and larval fish transport within a tidally dominated estuary. Fish. Oceanogr. Transl. 8 (suppl. 2), 173 – 189. Churchill, J.H., Hench, J.L., Luettich, R.J., Blanton, J.O., Werner, F.E., 1999b. Flood tide circulation near Beaufort Inlet North Carolina: implications for larval recruitment. Estuaries 22, 1057 – 1070. Fofonoff, N.P., 1985. Physical properties of seawater: a new salinity scale and equation of state for seawater. J. Geophys. Res. 90, 3332 – 3342. Forward, R.J., Tankersley, R.A., 2001. Selective tidal-stream transport of marine animals. Oceanogr. Mar. Biol. Ann. Rev. 39, 305 – 353. Forward, R.J., McKelvey, L.M., Hettler, W.F., Hoss, D.E., 1993. Swimbladder inflation of the Atlantic menhaden Brevoortia tyrannus. Fish. Bull. 91, 254 – 259.
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Forward, R.J., Hettler, W.F., Hoss, D.E., 1994. Swimbladder deflation in the Atlantic menhaden Brevoortia tyrannus. Fish. Bull. 92, 641 – 646. Govoni, J.J., Hoss, D.E., 2001. Comparison of the development and function of the swimbladder of Brevoortia tyrannus (Clupeidae) and Leiostomus xanthurus (Sciaenidae). Copeia 2001, 430 – 442. Hare, J.A., Quinlan, J.A., Werner, F.E., Blanton, B.O., Govoni, J.J., Forward, R.B., Settle, L.R., Hoss, D.E., 1999. Larval transport during winter in the SABRE study area: results of a coupled vertical larval behaviour — three-dimensional circulation model. Fish. Oceanogr. Transl. 8 (suppl. 2), 57 – 76. Hare, J.A., Thorrold, S.R., Walsh, H.J., Reiss, C., Valle-Levinson, A., Jones, C.M., in press. Bio-physical mechanisms of larval fish ingress into Chesapeake Bay. Mar. Ecol. Prog. Ser. Hettler, W.F., Chester, A.J., 1990. Temporal distribution of ichthyoplankton near Beaufort Inlet North Carolina. Mar. Ecol. Prog. Ser. 68, 157 – 168. Hettler Jr., W.F., Peters, D.S., Colby, D.R., Laban, E.H., 1997. Daily variability in abundance of larval fishes inside Beaufort Inlet. Fish. Bull. 95, 477 – 493. Hoss, D.E., Checkley, D.M., Settle, L.R., 1989. Diurnal buoyancy changes in larval Atlantic menhaden (Breevortia tyrranus). Rapp. P.-v. Reun. -Cons. Int. Explor. Mer. 191, 105 – 111. Joyeux, J.-C., 1998. Spatial and temporal entry patterns of fish larvae into North Carolina estuaries: comparisons among one pelagic and two demersal species. Estuar. Coast. Shelf Sci. 47, 731 – 752. Kitajima, C., Yamane, Y., Matsui, S., Kihara, Y., Furuichi, M., 1993. Ontogenetic change in buoyancy in the early stage of red sea bream. Nippon Suisan Gakkaishi /Bull. Jpn. Soc. Sci. Fish. 59, 209 – 216. Kitajima, C., Yamane, Y., Matsui, S., 1994a. Developmental changes in specific gravity in the early stages of the Japanese flounder Paralichthys olivaceus. Nippon Suisan Gakkaishi 60, 617 – 623. Kitajima, C., Yamane, Y., Matsui, S., 1994b. Ontogenetic changes in specific gravity during early development of black sea bream. Nippon Suisan Gakkaishi 60, 755 – 762. Kitajima, C., Yamane, Y., Matsui, S., Yoshimatsu, T., 1998. Ontogenetic change in specific gravity in the early stages of the ayu Plecoglossus altivelis. Bull. Jpn. Soc. Sci. Fish. 64, 822 – 829. Leis, J.M., Carson-Ewart, B.M., 2001. Behaviour of pelagic larvae of four coral-reef fish species in the ocean and an atoll lagoon. Coral Reefs 19, 247 – 257. Power, J.H., 1989. Sink or swim: growth dynamics and zooplankton hydrodynamics. Am. Nat. 133, 706 – 721. Pringle, J.M., Franks, P.J.S., 2001. Asymmetric mixing transport: a horizontal transport mechanism for sinking plankton and sediment in tidal flows. Limnol. Oceanogr. 46, 381 – 391. Quinlan, J.A., Crowder, L.B., 1999. Searching for sensitivity in the life history of Atlantic menhaden: inferences from a matrix model. Fish. Oceanogr. Transl. 8 (Suppl. 2), 124 – 133.
Rowe, P.M., Epifanio, C.E., 1994. Flux and transport of larval weakfish in Delaware Bay USA. Mar. Ecol. Prog. Ser. 110, 115 – 120. Schultz, E.T., Lwiza, K.M.M., Fencil, M.C., Martin, J.M., 2003. Mechanisms promoting upriver transport of larvae of two fish species in the Hudson River estuary. Mar. Ecol. Prog. Ser. 251, 263 – 277. Sclafani, M., Stirling, G., Leggett, W.C., 1997. Osmoregulation, nutritional effects and buoyancy of marine fish larvae: a bioassay for assessing density changes during the earliest life history stages. Mar. Biol. 129, 1 – 9. Shaw, R.F., Wiseman, W.J., Turner, R.E., Rouse, L.J., Condrey, R.E., 1985. Transport of larval Gulf menhaden Brevoortia patronus in continental shelf waters of western Louisiana: a hypothesis. Trans. Am. Fish. Soc. 114, 452 – 460. Sponaugle, S., Cowen, R.K., 1997. Early life history traits and recruitment patterns of Caribbean wrasses (Labridae). Ecol. Monogr. 67, 177 – 202. Sundby, S., 1983. A one-dimensional model for the vertical distribution of pelagic fish eggs in the mixed layer. Deep-Sea Res. 30, 645 – 661. Sundby, S., 1991. Factors affecting the vertical distribution of eggs. ICES Mar. Sci. Symp. 192, 33 – 38. Tanaka, M., Goto, T., Tomiyama, M., Sudo, H., Azuma, M., 1989. Lunar-phased immigration and settlement of metamorphosing Japanese flounder larvae into the nearshore nursery ground. Rapp. P.-v. Reun. -Cons. Int. Explor. Mer. 191, 303 – 310. Trnski, T., 2002. Behaviour of settlement-stage larvae of fishes with an estuarine juvenile phase: in situ observations in a warm-temperate estuary. Mar. Ecol. Prog. Ser. 242, 205 – 214. Tzeng, M.W., Hare, J.A., Lindquist, D.G., 2003. Ingress of transformation stage gray snapper, Lutjanus griseus (Pisces: Lutjanidae) through Beaufort Inlet North Carolina. Bull. Mar. Sci. 72, 891 – 908. Warlen, S.M., 1994. Spawning time and recruitment dynamics of larval Atlantic menhaden, Breevortia tyrannus, into a North Carolina estuary. Fish. Bull. 92, 420 – 433. Warlen, S.M., Burke, J.S., 1990. Immigration of larvae of fall/winter spawning marine fishes into a North Carolina estuary. Estuaries 13, 453 – 461. Weinstein, M.P., Weiss, S.L., Hodson, R.G., Gerry, L.R., 1980. Retention of three taxa of postlarval fishes in an intensively flushed tidal estuary Cape Fear River, North Carolina. Fish. Bull. 78, 419 – 436. Xie, L., Eggleston, D.B., 1999. Computer simulations of wind-induced estuarine circulation patterns and estuary–shelf exchange processes: the potential role of wind forcing on larval transport. Estuar. Coast. Shelf Sci. 49, 221 – 234.
Sinking rates of late-stage fish larvae: Implications for larval ingress into estuarine nursery habitats Jonathan A. Hare *,1, Harvey J. Walsh, Mark J. Wuenschel 2 NOAA NOS NCCOS, Center for Coastal Fisheries and Habitat Research, 101 Pivers Island Road, Beaufort, North Carolina 28516, USA Received 15 June 2005; received in revised form 1 September 2005; accepted 16 September 2005
Abstract Many species spawn in oceanic waters yet their juvenile stages use nearshore and estuarine habits and the bio-physical mechanisms by which late-larvae enter these juvenile habitats may be an important bottleneck in the population dynamics of these species. To provide parameters for the development of larval ingress models, sinking rates were measured of the late-stage larvae of six fish species: Atlantic croaker (Micropogonias undulatus), spot (Leiostomus xanthurus), Atlantic menhaden (Brevoortia tyrannus), summer flounder (Paralichthys dentatus), southern flounder (P. lethostigma), and gulf flounder (P. albigutta). Species-specific differences were found in sinking rates; Atlantic croaker had the slowest sinking rates and Atlantic menhaden and the three flounder species had the fastest sinking rates. Additionally, sinking rates increased for all species as length increased. The total amount of variability explained in sinking rates was low (20–50%), indicating a large amount of variability at the level of the individual. The observed patterns in sinking rates were then combined with previous studies on the mechanisms of larval ingress to present species-specific conceptual models of ingress. Published by Elsevier B.V. Keywords: Atlantic croaker; Atlantic menhaden; Buoyancy; Gulf flounder; Larval ingress; Sinking rate; Southern flounder; Spot; Summer flounder
1. Introduction Many species of marine fish have oceanic larval stages and nearshore and estuarine juvenile stages. For these species, the entrance of late-larvae into juvenile habitats may act as a bottleneck in the dynamics of the population (Quinlan and Crowder, 1999). A dominant mechanism of larval ingress is selective tidal * Corresponding author. Tel.: +1 401 782 3295; fax: +1 401 782 3201. E-mail address: [email protected] (J.A. Hare). 1 Current address: NOAA NMFS NEFSC, Narragansett Laboratory, 28 Tarzwell Drive, Narrgansett, Rhode Island 02882, USA. 2 Current address: Rutgers University Marine Field Station, Institute of Marine and Coastal Sciences, 800 Great Bay Blvd, c/o 132 Great Bay Blvd., Tuckerton, New Jersey 08087-2004, USA. 0022-0981/$ - see front matter. Published by Elsevier B.V. doi:10.1016/j.jembe.2005.09.011
stream transport, whereby larvae are higher in the water column on flood tides and near the bottom on ebb tides, thus effecting up-estuary transport (Forward and Tankersley, 2001). Other, more passive mechanisms also result in larvae entering estuaries including bottom residual inflow in the gravitational circulation of estuaries (Weinstein et al., 1980; Schultz et al., 2003) and physical events that result in the net transport of water into estuaries (e.g., wind, Shaw et al., 1985). Recent studies have indicated that some species enter estuaries via multiple mechanisms and that the importance of specific ingress mechanisms differ among ontogenetic stages and species (Joyeux, 1998; Churchill et al., 1999a,b; Hare et al., in press). Circulation modeling offers one approach to further examine the mechanisms by which oceanic larvae
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enter estuarine nursery areas. Models can be relatively simple (e.g., one-dimensional sediment-like transport models, Pringle and Franks, 2001) or complex (e.g., three-dimensional circulation models with Lagrangian particle tracking, Xie and Eggleston, 1999; Brown et al., 2004). A number of studies have shown that vertical distribution of larvae in the nearshore and estuarine water column has a large effect on larval transport (Rowe and Epifanio, 1994; Forward and Tankersley, 2001; Hare et al., in press), and thus larval vertical distribution models need to be coupled with physical models to accurately examine the mechanisms of larval ingress. One component of larval vertical distribution is buoyancy of larvae (Sundby, 1983; Aadlandsvik et al., 2001). Most fish larvae are negatively buoyant, causing them to sink (Hoss et al., 1989; Kitajima et al., 1993, 1994a,b, 1998). Energy is needed to keep larvae in the water column: either physical energy in the form of mixing (Sundby, 1983), biological energy in the form of swimming (Leis and Carson-Ewart, 2001; Trnski, 2002) or buoyancy compensation using the swimbladder (Hoss et al., 1989; Govoni and Hoss, 2001). A number of studies have documented diel and ontogenetic patterns in larval density and/or sinking rate (Hoss et al., 1989; Kitajima et al., 1994a,b, 1998; Forward et al., 1994), and individual variability in buoyancy has been linked to condition (Sclafani et al., 1997). For most transport model applications, sinking rate is the needed parameter for developing larval vertical distribution models (e.g., Hare et al., 1999; Aadlandsvik et al., 2001). Sinking rate is function of fish density, ambient water density, and fish drag (Sundby, 1983; Power, 1989). Fish density and ambient density are easily estimated, but drag is complex. Models have been developed to estimate sinking rates of spheres and columns of given densities (Sundby, 1983, 1991; Power, 1989; Aadlandsvik et al., 2001), but these shapes only approximate the body shape of fishes. Thus, measures of fish density are difficult to convert to sinking rate because of the differences in drag resulting from different fish shapes and orientation in the water column. Sinking rate of larvae can also be measured directly (Hoss et al., 1989), and is positively related to larval density (Kitajima et al., 1994a). With such measurements, care must be taken that the ambient water density and experimental water density are known, since larval density can vary with ambient water density (Kitajima et al., 1994a,b). Further, experimental temperature needs to approximate ambient temperature to maintain swimbladder volume, since gas
volume is affected by temperature and changes in swimbladder volume alter buoyancy and therefore sinking rate (Govoni and Hoss, 2001). Our goal was to measure sinking rate of several species of fish that enter estuaries as late-stage larvae: Atlantic croaker (Micropogonias undulatus, Sciaenidae), spot (Leiostomus xanthurus, Sciaenidae), Atlantic menhaden (Breevortia tyrannus, Clupeidae), gulf flounder (Paralichthys albigutta, Paralichthyidae), southern flounder (Paralichthys lethostigma, Paralichthyidae), and summer flounder (Paralichthys dentatus, Paralichthyidae). Late-stage larvae of these species typically ingress through Beaufort Inlet during winter, while moving from oceanic spawning areas to estuarine nursery habitats and while transforming from larvae to juveniles (Hettler and Chester, 1990; Warlen and Burke, 1990). We captured ingressing larvae weekly through the fall and winter of 2004–2005. After capture, we immediately returned to the laboratory and measured sinking rate. Using multiple linear regression, we examined the effects of ambient water density and ontogeny on sinking rate. We were also concerned with the effect of time to measurement of sinking rate in the laboratory. Fish larvae influence buoyancy in part through inflation or deflation of a gas bladder (Hoss et al., 1989; Forward et al., 1993). The buoyancy of fish held in the laboratory for longer periods prior to sinking rate measurements may change as a result of the potential deflation of the swimbladder through diffusion. It is our hope that the resulting estimates of sinking rate prove useful in future studies that use models to investigate larval ingress into nearshore and estuarine habitats. 2. Materials and methods 2.1. Experimental apparatus Sinking rate was measured by releasing anesthetized larvae at the top of columns filled with seawater in the laboratory and measuring the time required for larvae to sink a known distance. Four columns were used, each with water of a different salinity: 15, 20, 25, and 30. Tap water was mixed with Instant Ocean Synthetic Sea SaltsR to achieve target salinities. Columns were placed in a water bath to maintain experimental temperatures near the ambient temperature. Temperature in the water bath was maintained using a temperature controller (1 / 2 hp, 10–18 8C, Aqua Logic, Inc.) and water in the bath was thoroughly mixed using a utility pump. The experimental glass columns were 25 cm high and 22 cm in diameter, and were filled with 23 cm of water. A 10 cm
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measurement zone (from 8 cm below the water’s surface to 5 cm above the bottom) was marked on both the front and the back of each column. 2.2. Measurement of field and experimental water temperature, salinity, and density Approximately 12 h prior to fish collection, ambient water temperature was measured with a hand-held thermometer, and a temperature-controlled water bath was set to this temperature. About 30 min prior to sampling, ambient water temperature was measured again with a hand-held thermometer and the water bath temperature controller was adjusted if necessary. During the collection of fish larvae, ambient temperature and salinity were measured with a CTD (Model 6600-D, YSI, Inc., temperature accuracy F 0.15 8C, salinity accuracy F0.35). The temperature and salinity of water in each experimental column (see below) were also measured using the CTD. Ambient and experimental water density was estimated from ambient and experimental temperature and salinity based on Fofonoff (1985). Depth was estimated as 0.5 m for ambient conditions and 0.05 m for experimental conditions. 2.3. Collection of late-stage larvae Late-stage fish larvae were collected weekly using a 2 m2 plankton net with 947 Am mesh deployed in a channel approximately 1 km inside of Beaufort Inlet, North Carolina (Warlen, 1994). Eleven collections were made from 8 December 2004 to 16 February 2005. Each week, the net was deployed for approximately 20 min during nighttime flood tides following the collection of weekly larval ingress monitoring samples. A 5 L plastic cod-end bucket was attached at the end of the net to assist in keeping fish larvae alive during capture and return to the laboratory. Once the net was retrieved, the cod end was placed in a bucket of ambient seawater. Live fish larvae were picked from the sample and placed in a petri dish containing ambient seawater. Larvae were then anesthetized with tricaine methanesulfonate (MS-222) just prior to sinking rate measurements. Species examined included Atlantic croaker, spot, Atlantic menhaden, southern flounder, gulf flounder, and summer flounder. 2.4. Sinking rate measurements Sinking rate was measured by timing the decent of anesthetized larvae through the marked 10 cm measurement zone in the columns. Standard length of each larva
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was measured to the nearest millimeter and then the larva was placed just below the water’s surface in the middle of the column. A stopwatch was started when larvae crossed the top mark of the measurement zone and was stopped when larvae crossed the bottom mark of the measurement zone. We were concerned that the handling and anesthetizing fish could influence their density, and thus their sinking rate. Either gas could be lost from the swimbladder (e.g., through diffusion) or biochemical reactions could take place that result in a density change. All sinking rate measurements were completed within 1 h of larval fish collection. Also, the order that sinking rate measurements were made was noted (measurement sequence), allowing an estimate of time of anesthesia to be used in data analysis. The number of larvae for which sinking rates were measured depended on the field collections, so weekly sample sizes varied. If many individuals were collected in a given week (approximately N 10), larvae were placed in randomly assigned columns (salinities) with water densities less than ambient conditions. For example, when ambient water densities were low, only columns with salinities of 15 and 20 were used; when ambient water densities were high, columns with salinities of 15, 20, 25 and 30 were used. If only a few individuals were collected in a given week (approximately b10), larvae were placed in a single column (salinity) with water density less than ambient conditions. The number and length of larvae used in sinking rate measurements and the columns used are provided in Table 1. 2.5. Data analysis Multiple regression was used to determine if four variables significantly affected sinking rate. The model used was SR ¼ a þ bd rtAmb rtExp þ cdrtAmb þ ddSL þ edMS where sinking rate (SR cm s 1) is modeled as a linear response to the difference between ambient water density and experimental water density (r tAmb r tExp), ambient water density (r tAmb), length (SL, mm), and measurement sequence (MS, starting at 1 and increasing by 1 for each larva measured each week). The parameter a is the model constant. Linear responses were estimated by parameters b, c, d, and e. Significance of the model parameters was determined based on the a = 0.05 and the r 2 of the model fit also was calculated. Since it would have been very difficult to match ambient conditions in the laboratory owing to changes in temperature and
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Species
Atlantic croaker
Spot
Atlantic menhaden
Gulf flounder
Southern flounder
Summer flounder
Parameter
n Mean SL SD SL Cols n Mean SL SD SL Cols n Mean SL SD SL Cols n Mean SL SD SL Cols n Mean SL SD SL Cols n Mean SL SD SL Cols
Sampling date (December 2004–March 2005) 8-Dec
16-Dec
22-Dec
29-Dec
5-Jan
12-Jan
19-Jan
26-Jan
2-Feb
9-Feb
16-Feb
23-Feb
35 12.17 1.32 1, 2, 3, 4
8 12.00 1.00 1, 2, 3
17 11.88 1.45 1, 2, 3 24 15.21 1.32 1, 2, 3 10 22.50 1.43 1, 3
21 11.48 1.26 1, 2 2 15.00 0.00 2
6 15.50 2.22 3
13 10.46 1.01 1, 2 15 13.73 1.24 1, 2, 3
12 11.25 0.72 1, 2 12 15.92 2.10 1, 2 12 24.00 2.20 1, 2
20 10.45 1.12 1, 2 20 15.75 1.37 1, 2 23 23.96 2.42 1, 2, 3 1 14.00 0.00 2 12 11.75 1.23 1, 2
19 11.84 1.66 1, 2, 3
8 9.50 1.22 3
9 11.33 0.82 2 25 15.24 2.29 1, 2 17 24.29 1.84 2 3 9.33 0.47 2 17 11.47 0.78 1, 2 1 11.00 0.00 1
13 11.46 0.63 1, 2
12 21.58 1.19 1, 2, 3, 4 1 8.00 0.00 3
28 11.14 1.73 1, 2, 3 3 14.33 2.05 3 8 21.00 0.00 3 9 10.00 0.00 3 3 13.00 0.00 3
5 23.00 1.41 3 2 12.00 1.00 2 14 11.57 0.82 1, 2 5 13.60 1.02 2
15 25.20 2.14 1, 2, 3 1 10.00 0.00 2 5 12.40 0.49 1, 2, 3 7 13.43 0.90 1, 2, 3
9 11.44 1.34 1, 2, 3 35 10.23 1.07 1, 2, 3
1 15.00 0.00 3
The experimental columns used (fourth row) contained salinities of 20 (col 1), 25 (col 2), 30 (col 3) and 35 (col 4).
9 11.22 0.63 1, 2 3 14.67 1.25 2
2-Mar
9-Mar
15 27.07 1.88 1, 2
10 11.50 0.81 1, 2, 3 7 16.00 1.20 2, 3 9 25.89 0.99 3
2 12.50 0.50 3 4 13.75 0.43 3
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Table 1 Number (first row), mean length (second row), and standard deviation in length (third row) of late-stage larvae used in sinking rate measurements on 11 dates
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1). Temperature varied from 6.3 to 15.2 8C. Salinity varied from 28.1 to 33.2. The variability in temperature and salinity lead to a broad range of ambient water densities from 21.9 to 25.6 r t. 3.2. Factors affecting larval sinking rate
Fig. 1. Ambient water density (r t), temperature (8C), and salinity during weekly collection of ingressing larval fish. Sampling was conducted from a bridge spanning a channel ~1 km inside of Beaufort Inlet, North Carolina. Samples were collected during nighttime flood tides approximately 2 h before high tide.
salinity during the tidal cycle (see Churchill et al., 1999a), different experimental water densities were used when possible to the allow the effect of ambient density on sinking rates to be quantified. Parameters from the above model then were used to calculate sinking rates at ambient water densities (r tAmb r tExp = 0) and the beginning of the weekly measurements (MS = 1).
The dominant factor in the multiple regression models was the difference between ambient and experimental water densities. All species, except summer flounder, exhibited a significant increase in sinking rate with increasing difference between ambient and experimental water density (Table 2, Figs. 2–7). The increase in sinking rate with increased difference between ambient and experimental water density was greater for Atlantic croaker, spot, and Atlantic menhaden (0.087, 0.106, 0.068 cm s 1 rt 1) than for southern, gulf and summer flounder (0.026, 0.027, 0.003 cm s 1 rt 1). Ambient water density and length also influenced sinking rate. As ambient water density increased, sinking rate decreased for Atlantic croaker and gulf flounder (Table 2, Figs. 2–7). The sinking rates of Atlantic croaker, Atlantic menhaden, and southern flounder increased significantly with larval length (Table 2, Figs. 2–7). Measurement sequence significantly affected sinking rate as well, indicating a change in larval buoyancy following anesthesia. Atlantic croaker, spot, Atlantic menhaden and gulf flounder sank significantly faster as measurement sequence increased (Table 2, Figs. 2–7). 3.3. Sinking rate estimates
3. Results 3.1. Environmental variability Ambient water temperature, salinity, and density varied during the 11 weeks of the experiments (Fig.
Estimates of sinking rates for specific values of the independent variables were derived from the multiple regression models. Of particular interest are sinking rates when there is no difference between ambient and experimental water density (r tAmb r tExp = 0) and
Table 2 Parameter estimates from multivariate linear regression models for the sinking rate of late-stage larvae of six species as a function of the difference between ambient and experimental water density, ambient water density, fish length, and measurement sequence Model parameter
Species Atlantic croaker
Constant (a) 0.526 Density difference (b) 0.087*** Ambient density (c) 0.037* Length (d) 0.031** Measurement sequence (e) 0.015*** Model r 2 0.534
Spot
Atlantic menhaden
Gulf flounder
Southern flounder
Summer flounder
0.481 0.106*** 0.025 0.014 0.011* 0.356
1.480 0.068** 0.017 0.074** 0.016*** 0.195
3.171*** 0.026* 0.091*** 0.019 0.007** 0.429
0.247 0.027* 0.005 0.079** 0.001 0.240
2.356 0.003 0.046 0.011 0.003 0.307
Significance of the model parameters is noted as: *p b 0.05; **p b 0.01, ***p b 0.001.
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4. Discussion 4.1. Experimental artifacts The experiments conducted here reveal two potential artifacts that require consideration: the effect of measurement sequence on sinking rate and potential biological cycles in sinking rate. The significant effects of measurement sequence on the sinking rates of Atlantic croaker, spot, Atlantic menhaden and gulf flounder indicate that the density of larvae changed during the course of a night’s experiment. The likely mechanism is escape of gas from the swimbladder, which would
Fig. 2. Sinking rate of late-stage larval Atlantic croaker (Micropogonias undulatus) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
no time between anesthesia and sinking rate measurements (MS = 1). For these values and at an ambient density of 23.5 r t and average length-at-ingress, Atlantic croaker had the lowest sinking rate, spot had an intermediate rate, and Atlantic menhaden, gulf flounder, southern flounder, and summer flounder had higher sinking rates (Table 3). These sinking rate estimates imply that the body density of larval Atlantic croaker is closest to seawater and that the body density of larval Atlantic menhaden, gulf flounder, southern flounder, and summer flounder is greater than seawater.
Fig. 3. Sinking rate of late-stage larval spot (Leiostomus xanthurus) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
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larval density owing to the experimental methods, either independent to gulf flounder or shared between gulf flounder, spot, Atlantic croaker, and Atlantic menhaden. The effect of measurement sequence in gulf flounder was lower than in the other species, hinting at an unknown mechanism affecting all species and then the loss of gas from the swimbladder as an added mechanism affecting spot, Atlantic croaker, and Atlantic menhaden. Osmoregulatory failure of the anesthetized larvae in our experiments may explain part the gradual increase in sinking rates over time for all species (including those without swimbladders); loss of osmotic control by Gadus morhua larvae was
Fig. 4. Sinking rate of late-stage larval Atlantic menhaden (Brevoortia tyrannus) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
result in larvae becoming heavier. In a preliminary examination, the swimbladders of anesthetized Atlantic croaker, Atlantic menhaden, and spot were smaller after one hour (H. Walsh, unpublished data). The anesthesia (MS-222) may have caused relaxation of the muscular valves that regulate blood flow to the gas removal (oval) region of the swimbladder, increasing resorption of gas from the swimbladder into the blood. Larvae of species in the genus Paralichthys either have vestigial, non-functional swimbladders (Bisbal and Bengtson, 1995) or no swimbladder (J. Govoni, pers comm., NOAA Beaufort Laboratory), so there must be another mechanism that results in increasing
Fig. 5. Sinking rate of late-stage larval gulf flounder (Paralichthys albigutta) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
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specifically examine sinking rates over diel, tidal, or lunar cycles. The experiment was conducted over 11 weeks and encompassed more than three lunar cycles and six spring–neap cycles. However, sampling was passive and was conducted on maximum, nighttime flood tides. Hettler et al. (1997) discussed the inherent confounding of time of sampling in the diel cycle and in the spring–neap cycle when using these collection methods; in our study the circular correlation between time of sampling and time in the spring–neap cycle was 0.843 ( p b 0.001). A number of studies have indicated diel cycles in sinking rate (Hoss et al., 1989; Kitajima et al., 1993, 1994a,b, 1998; Forward et al., 1994).
Fig. 6. Sinking rate of late-stage larval southern flounder (Paralichthys lethostigma) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
shown to increase larval density and influence vertical position, but the causes of bosmotic breachQ were unclear (Sclafani et al., 1997). By including the measurement sequence in the multivariate model of sinking rates, we were able to estimate sinking rates at a comparable measurement sequence for all larvae (Table 3). However, the impact of collection and transport to the lab on sinking rate was not quantified, potentially introducing an unknown error into the estimates presented here. Diel and longer-term cycles also may have influenced the results of this study, but we were unable to
Fig. 7. Sinking rate of late-stage larval summer flounder (Paralichthys dentatus) as a function of A) the difference between experimental and ambient water density, B) ambient water density itself, C) larval length, and D) measurement sequence. Individual measurements are denoted (D). Multiple linear regressions are also shown (–); regressions were calculated for the range of data for the given variable (e.g., ambient water density) at the average value for the other parameters in the model (e.g., difference between experimental and ambient water density, larval length, and measurement sequence).
J.A. Hare et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 493–504 Table 3 Estimated sinking rate of six fish species ingressing into Beaufort Inlet as late-larvae Species
Est. sinking rate [F95% CI] (cm s 1)
Atlantic croaker Spot Atlantic menhaden Gulf flounder Southern flounder Summer flounder
0.022 0.121 0.734 0.846 1.253 1.126
[F0.089] [F0.343] [F0.313] [F0.202] [F0.214] [F0.268]
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are comparable with different experimental procedures and generally reflect larval density (Kitajima et al., 1994a). 4.3. General patterns in sinking rate of ingressing larvae
Sinking rate estimates were made from multiple linear regression models (Table 2) with the difference between ambient and experimental water density set at 0, ambient water density set at 23.5 r t. Length set at the average length examined here (see Table 1), and measurement sequence set at 1. 95% confidence intervals (CI) are also provided for the estimates.
Whether there are longer-scale patterns in sinking rates remains a question, but there are certainly spring–neap and lunar patterns in larval ingress and settlement (Tanaka et al., 1989; Sponaugle and Cowen, 1997; Tzeng et al., 2003). Cycles in sinking rate could contribute to the settlement and ingress of larvae owing to the interaction of sinking rate and larval ingress mechanisms. 4.2. Comparison with other studies The estimates of sinking rates derived here compare favorably with other estimates for these and related species. For Atlantic menhaden in the length range of 20–22 mm, Hoss et al. (1989) found sinking rates of approximately 1.2–1.4 cm s 1 compared to 0.734 cm s 1 found here. For lab-reared metamorphic stage summer flounder, estimated sinking rates of 1.1–1.3 cm s 1 (pers. comm. Chaoshu Zeng, James Cook University), compared to 1.126 cm s 1 found here. Hoss et al. (1989) used field caught larvae and made measurements at sea. Zeng (pers. comm.) used lab-reared larvae and made measurements in the laboratory. Owing to the agreement of sinking rate measures, we have confidence that the sinking rate estimates developed here
Several general patterns in sinking rates were evident when comparing the results of the multiple regression models among species (Table 4). For all species except summer flounder, sinking rates increased as the difference between ambient and experimental water density increased. Sinking rate is a function of fish density, water density, and drag and as the experimental water density decreased, sinking rates increased. However, the rate of increase in sinking rates with density difference varied among species. The rate of increase ranged from 0.068 to 0.106 cm s 1 Drt 1 difference for Atlantic croaker, spot, and Atlantic menhaden, whereas the rate of increase was about 0.027 for gulf and southern flounder and 0.003 for summer flounder. These differences in rate are likely caused by differences in drag among the different species. Qualitatively, Atlantic croaker and spot sank headfirst and both Atlantic menhaden and the flounders sank horizontally. The flattened ellipsoid shape of the flounder likely lead to increased drag to the point that drag influenced sinking rate on the same magnitude as the difference between larval density and water density. In hindsight, if we had quantified sinking orientation, perhaps more of the variability in sinking rate could have been explained. The influence of drag on the sinking rate of metamorphic stage flounder leads to the hypothesis that flounder could possibly control their vertical position in a flowing water column by swimming into the flow and changing their aspect ratio. The asymmetrical flattened ellipsoid shape of flounder may act as a foil, with changes in aspect relative to the flow creating an upward or downward force, thereby allowing flounder to easily change position in a flowing water column without adjusting their buoyancy. The non-vertical angle of
Table 4 Summary of the effect of different factors on sinking rates based on the significant terms from the multiple linear regression Species
Inc. r tAmb r tExp
Inc. r tAmb
Inc. length
Measurement sequence
Atlantic croaker Spot Atlantic menhaden Gulf flounder Southern flounder Summer flounder
Inc. Inc. Inc. Inc. Inc.
Dec. SR
Inc. SR
Inc. Inc. Inc. Inc.
SR SR SR SR SR
Inc. SR Dec. SR Inc. SR
SR SR SR SR
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descent for anesthetized flounder larvae in the static columns observed in the present study supports the hypothesis that in the presence of flow, these larvae are able to move up or down in the water column with minimal swimming activity. Activity patterns have been linked to light and salinity in late-larval Japanese flounder, Paralichthys olivaceus (Burke et al., 1995), but the role of lift and drag in keeping flounder in the water column has not been investigated. Ambient density of the water also influenced the sinking rate of larvae (Table 4), but the effect of ambient density was smaller than the effect of the difference between ambient and experimental density. Kitajima et al. (1994a,b) found that larval density decreased with decreases in ambient water density in Japanese flounder and black sea bream, but in relative terms the difference between larval and ambient density increased. The result would be an increasing sinking rate as ambient density decreased, which was the general pattern found here. The implications of this relationship to larval ingress would seem to facilitate retention of larvae within estuaries. Sinking rates increased as larval length increased for all species except summer flounder (Table 4). Many studies have documented ontogenetic patterns in both larval density (Kitajima et al., 1993, 1994a,b, 1998) and sinking rate (Hoss et al., 1989). The implications of increased density and sinking rate are that more energy is needed to keep larvae in the water column as larvae develop. In contrast, it is easier for benthic species to remain near the bottom even in the face of strong vertical mixing, which again would seem to facilitate retention of later-stage larvae within estuaries. Even though sea water density and larval length had significant effects on sinking rate, there still was a large amount of unexplained variability. Regression r 2’s ranged from 0.195 to 0.534, so 50–80% of the variability in sinking rate remained unexplained. Some of this unexplained variability may be related to variability in larval condition. Sclafani et al. (1997) indicated that fish with lower condition were heavier and thus would have a higher sinking rate. The relationship between condition and sinking rate was not examined in this study, but future use of the parameters developed here should include both the means and variance of sinking rate to more accurately capture the dynamics of larval ingress. 4.4. Sinking rates and larval transport Hare et al. (in press) examined three mechanisms of estuarine ingress: bottom layer residual inflow, event-
scale inflow (e.g., wind-driven), and selective tidal stream transport. They concluded that summer flounder use primarily selective-tidal stream transport, Atlantic croaker used a mixture of ingress mechanisms, and Atlantic menhaden used primarily residual bottom inflow and event-driven processes. The sinking rates derived here can be used to further develop the hypotheses regarding larval ingress mechanisms of the different species. Gulf, southern, and summer flounder have relatively high sinking rates and are on the bottom during ebb and slack tides. During flood tides they actively move into the water column, not by adjusting their buoyancy (since they do not have a functional swimbladder), but by swimming up into the water column. On ebb tides, their high sinking rate keeps them on or very near the bottom despite increased vertical mixing resulting from increased flow rates. Thus, these species of flounder use predominantly selective tidal stream transport to enter estuaries. Atlantic croaker have relatively slow sinking rates and their vertical distribution is affected by vertical turbulence more so than Paralichthys flounder, spot, and Atlantic menhaden. During flood and ebb tides, Atlantic croaker move back and forth in the estuary, but by spending most of their time in the lower part of the water column, they move up estuary in the residual bottom inflow. Density discontinuities in the estuarine water column would limit mixing into the upper portions of the water column. During wind events, when vertical mixing is increased, Atlantic croaker are mixed into the water column and move with the water; during the study of Hare et al. (1999), most of the event-scale transport was up-estuary so Atlantic croaker moved upestuary. With some buoyancy control or active swimming that is linked to tidal cycles (12.5 h), Atlantic croaker exhibit up-estuary selective tidal stream transport, but because Atlantic croaker do not go to the bottom (like flounder) nor are they heavy enough to resist vertical mixing, their ability to utilize selective tidal stream transport is compromised by some downestuary movement on ebb tides. Yet, with development Atlantic croaker become heavier and are better able to use selective tidal stream transport to enter estuaries (Hare et al., in press). Spot are similar to Atlantic croaker, but have a greater capacity to utilize selective-tidal stream transport because they have greater sinking rates and are better able to resist mixing into the water column on ebb tides. Hare et al. (in press) did not examine ingress of spot, but Churchill et al. (1999a) concluded that spot were better at utilizing selective-tidal
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stream transport than Atlantic croaker and the sinking rate measurements derived here support their findings. However, like Atlantic croaker, we hypothesize that a combination of ingress mechanisms is important for spot entering estuarine habitats and that the importance of these mechanisms likely changes with development. Atlantic menhaden have a moderately high sinking rate, yet Hare et al. (in press) found that ingress occurred primarily through residual bottom in-flow and event-driven flows. The interpretation is that the high sinking rates keep larvae primarily in the lower part of the water column, but owing to the need to fill the swimbladder at the surface near dusk (Forward et al., 1993), larvae are distributed throughout the water column at specific times of the day and are susceptible to event-driven flows and ebb tides. Batty (1987) studied the swimming behavior of larvae of another clupeid, Clupea harengus, in the laboratory and found that larvae were inactive in the dark except for periodic vertical swimming bouts, which were replaced by horizontal swimming as light intensity increased. During the day, menhaden larvae maintain position in the water column through active swimming, with energetic cost of activity compensated for by the increased search volume and/or prey encounter rates. At light levels below the feeding threshold, menhaden offset their negative buoyancy by inflating their swimbladder, allowing reduced swimming activity costs (which may also reduce interactions with potential predators). The net result for transport is that Atlantic menhaden rely on eventscale processes to enter estuaries more so than the other species examined here. The results of this study and others demonstrate that species use multiple mechanisms to enter estuarine habitats and that ontogeny plays a role (see Joyeux, 1998; Churchill et al., 1999a,b; Hare et al., in press). The energetic costs of ingress will depend, in part, on the sinking rate of larvae. Larvae adjust their position in the water column by regulating their buoyancy (via swimbladder), active swimming, or a combination of these depending on species. Although not investigated in the present study, factors and behaviors related to activity, feeding and predator avoidance likely play important roles in influencing the vertical distribution of larvae in the wild. Thus, the biological characteristics of each species interact with the physical environment to effect movement in the marine environment. The sinking rates determined in this study provide some of the necessary parameters to develop larval vertical distribution models
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to couple with 3-D numerical circulation models (e.g., Hare et al., 1999), which would result in a powerful tool to further examine larval ingress as a potential bottleneck in the population dynamics of species that spawn on the shelf but use estuaries as juvenile nurseries. Acknowledgements We thank Katey Marancik, Gretchen Bath Martin, and Jacqueline Jenkins for helping collect fish larvae and measure sinking rates. Christian Reiss and Michael Greene raised important questions about sinking rate that largely formed the motivation for this study. Chaoshu Zeng provided us with his data on sinking rate for lab-reared summer flounder for comparison. This study was supported in part by a National Science Foundation Grant (OCE 9876565) to C. Jones, S. Thorrold, A. Valle-Levinson, and J. Hare. Jeff Govoni, Christian Reiss, and John Burke reviewed earlier versions of this manuscript. [SS] References Aadlandsvik, B., Coombs, S., Sundby, S., Temple, G., 2001. Buoyancy and vertical distribution of eggs and larvae of blue whiting (Micromesistius poutassou): observations and modelling. Fish. Res. 50 (1–2), 59 – 72. Batty, R.S., 1987. Effect of light intensity on activity and foodsearching of larval herring Clupea harengus: a laboratory study. Mar. Biol. 95, 323 – 327. Bisbal, G.A., Bengtson, D.A., 1995. Development of the digestive tract in larval summer flounder. J. Fish Biol. 47, 277 – 291. Brown, C.A., Holt, S.A., Jackson, G.A., Brooks, D.A., Holt, G.J., 2004. Simulating larval supply to estuarine nursery areas: how important are physical processes to the supply of larvae to the Aransas Pass Inlet? Fish. Oceanogr. Transl. 13, 181 – 196. Burke, J.S., Tanaka, M., Seikai, T., 1995. Influence of light and salinity on behaviour of larval Japanese flounder (Paralichthys olivaceus) and implications for inshore migration. J. Sea Res. 34, 59 – 69. Churchill, J.H., Forward, R.B., Luettich, R.J., Hench, J.L., Hettler, W.F., Crowder, L.B., Blanton, J.O., 1999a. Circulation and larval fish transport within a tidally dominated estuary. Fish. Oceanogr. Transl. 8 (suppl. 2), 173 – 189. Churchill, J.H., Hench, J.L., Luettich, R.J., Blanton, J.O., Werner, F.E., 1999b. Flood tide circulation near Beaufort Inlet North Carolina: implications for larval recruitment. Estuaries 22, 1057 – 1070. Fofonoff, N.P., 1985. Physical properties of seawater: a new salinity scale and equation of state for seawater. J. Geophys. Res. 90, 3332 – 3342. Forward, R.J., Tankersley, R.A., 2001. Selective tidal-stream transport of marine animals. Oceanogr. Mar. Biol. Ann. Rev. 39, 305 – 353. Forward, R.J., McKelvey, L.M., Hettler, W.F., Hoss, D.E., 1993. Swimbladder inflation of the Atlantic menhaden Brevoortia tyrannus. Fish. Bull. 91, 254 – 259.
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