© 2003 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Material properties of North Atlantic cod eggs and early-stage larvae and their influence on acoustic scattering
a Woods Hole Oceanographic Institution Woods Hole, MA 02543, USA
b Ocean Sciences Centre, Memorial University of Newfoundland St John's, NewFoundland, Canada A1C 5S7
*Correspondence to D. Chu; tel: +1-508-289-3318; fax: +1-508-457-2194. e-mail: dchu{at}whoi.edu.
To study the acoustic signatures of Atlantic cod (Gadus morhua) at different biological stages from eggs to early-stage larvae (<37 days post-hatch), we conducted a series of experiments to estimate their sound-speed and density contrasts. A laboratory version of the "Acoustic Properties of Zooplankton" system was used. Sound speed was estimated by means of travel time between two transducers using a broadband acoustic signal (
300–600 kHz). Density was estimated using a dual-density method in which two fluids of different densities were employed. It was found that the density contrasts of cod eggs and early-stage larvae were nearly all slightly less than unity (0.969–0.998), while the effective sound-speed contrasts were only slightly greater than unity (1.017–1.024) for eggs and yolk-sac stage larvae (<5 days post-hatch), and increased significantly (>1.130) for larvae older than 16 days. This change in sound-speed contrast reflected the transition of the swimbladder from an uninflated state to an inflated state. The regression relation between estimated target strength at 500 kHz and larval length in centimetres was found to be TS = 176.1 log10L – 82.4(dB). The inflation ratio of the swimbladder for early-stage larvae was an exponential function of time. The predicted period of time until full swimbladder inflation was 43.3 days.
Keywords: acoustic scattering, cod eggs, cod larvae, swimbladder inflation
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Introduction |
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 Top Introduction MethodsResults and data analysisConclusionsReferences |
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Historically, the Atlantic cod (Gadus morhua) has been a commercially important, demersal gadoid species in the North Atlantic. However, stocks have declined severely in most of the western North Atlantic mainly because of commercial overfishing (Murawski et al., 1997), and in the past decade studies on cod have increased significantly (Anon., 1992; Lough and Potter, 1993; Ottersen and Sundby, 1995; Rose et al., 2000; Hansen et al., 2001; Nielsen et al., 2001). Larval cod was chosen as one of the target species by the GLOBal ocean ECosystem dynamics (US GLOBEC), Georges Bank program (Anon., 1991). Many studies have focused on the biological aspects of cod larvae, i.e. feeding, growth, and behaviour (Lough and Potter, 1993; Ottersen and Sundby, 1995; Lough and Mountain, 1996; Lough et al., 1996; Puvanendran and Brown, 1999; Steinarsson and Bjoernsson, 1999).
In order to determine the distribution and abundance of cod stocks, acoustic techniques have been used successfully as a sampling tool in a number of surveys (Godø and Ona, 1999; Lawson and Rose, 2000; Rose et al., 2000; Anderson and Rose, 2001). While acoustic signatures such as the target strength (TS) of adult cod and other fish species have been investigated intensively (Foote, 1985; Rose and Porter, 1996; Barange et al., 1996; Nainggolan and Pasaribu, 1997; Horne et al., 2000), the acoustic signatures of the early life stages and the change in these properties as the larvae grow have largely been ignored.
For fish with swimbladders, such as adult cod, it is well known that backscattering is dominated by the contribution from that organ. At or near the swimbladder, resonance frequency, the acoustic backscattering at full inflation is omnidirectional and the TS is several hundred times higher than that of a rigid target of the same size (Clay and Medwin, 1977). At higher frequencies, the backscattering can be described by the Kirchhoff approximation, i.e. an integration over the surface of the swimbladder (Foote, 1985). During their early life stages, from egg to 30–40 days post-hatch as body size increases from 3–5 mm to about 10 mm, cod undergo three stages of development: pre-swimbladder, swimbladder formation, and swimbladder inflation (Morrison, 1993). Simply scaling down the acoustic properties of adult fish to larval fish will not work, since the scattering mechanism is not clear, i.e. regardless of whether the swimbladder is fully or fractionally filled. In addition, before the swimbladder is fully developed, the volume ratio of the swimbladder to the whole body could be much smaller than that of adult fish and hence the scattering contribution from fish flesh may be significant. To model the scattering by this type of larval fish, the body material properties, such as density and sound-speed contrasts, are needed. However, these material properties of cod larvae have not been reported.
In this paper, we present estimations of the density and sound-speed contrasts of cod at early life stages, ranging from eggs to larvae (up to 36 days post-hatch). Based on the results, the estimated TS of individual larvae at different early life stages can be obtained. In the next section, methods of measuring density and sound-speed contrasts are briefly described. Details of the actual experiment are given in the third section. Data analysis and result discussions are then presented and finally some conclusions are drawn.
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Methods |
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TopIntroductionMethodsResults and data analysisConclusionsReferences |
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The estimation of sound-speed contrast
Sound speed is determined by measuring the direct travel time between the two broadband transducers of the Acoustic Properties Of zooPlankton (APOP system) (Chu et al., 2000a). Two transducers are placed facing each other—one as a transmitter and the other as a receiver (Figure 1). A sound speed can be estimated by measuring the differences in travel time with and without animals present. Since acoustic scattering depends, among other factors, on the ratio of the sound speed of the target to that of the surrounding medium—the sound-speed contrast, h—rather than on the sound speed of the scattering target itself, it is more important to know h in describing the acoustic scattering by marine organisms. The sound-speed contrast has been estimated using several different methods (Greenlaw, 1977; Køgeler et al., 1987; Foote, 1990; Chu et al., 2000a). For fluid-like, weakly scattering targets such as cod eggs, the sound-speed contrast can be approximately estimated with both time-average and "Distorted Wave Born Approximation" (DWBA) scattering models (Chu et al., 2000a):
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| (1) |
tm is the time difference between the travel time with and without the presence of animals, 
V is the volume fraction of the animals in the animal compartment, and tD=D/c is the time for an acoustic wave travelling over a distance of D (the thickness of the animal layer; Figure 1).
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For gas-bearing animals such as cod larvae with swimbladders, the sound-speed contrast determined by Equation (1) only represents the effective sound-speed contrast because of scattering by the swimbladder and the larval flesh and does not provide the direct link between the physical properties of the organisms and the estimated h. To understand the estimated h better we use the well-known dispersion relation (Lax, 1951; Ishimaru, 1978):
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| (2) |
is the forward-scattering amplitude of an individual animal. The real and imaginary parts of km can be used to infer the sound speed and the attenuation coefficient of the organisms, respectively. For weakly scattering objects, can be determined using the DWBA and is proportional to the volume of the target (Chu and Ye, 1999). For swimbladders, however, the DWBA is no longer valid and different solutions to compute have to be sought. Equation (2) assumes all scatterers have the same size, but it can be generalized to
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| (3) |
ß is the number density (no. m–3) for animal class ß. Approximate solutions widely used in studying the backscattering by fish with swimbladders are those for spherical bubbles (Clay and Medwin, 1977; Love, 1978). Deformation of the swimbladder from spheres to prolate spheroids leads to a slight deviation of resonance frequency (Strasberg, 1953) and can be easily included in a simplified form (Weston, 1967; Love, 1978). Corrections to the quality factor Q and the overall scattering level require a more complicated solution (Ye, 1997).
Estimation of density contrast
A dual-density method was used to estimate the density of cod eggs and larvae (Chu et al., 2000b). This method, involving two fluids with different densities (fluid 1 and fluid 2), does not require the animals to be motionless as do the methods of sinking rate (Knutsen et al., 2001), density bottle (Foote, 1990), and density gradient (Køgeler et al., 1987). Another advantage of the current dual-density method is that it can avoid the uncertainty introduced by water unavoidably adhering to the animals, that occurs with the traditional method involving displacement volume and weight measurements (Lowndes, 1942). The dual-density method requires a set of density and weight measurements that can be described by the following equations:
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| (4) |
1, 2, f, and m. Note that the density m is the density of the mixture of fluids 1 and 2 only and excludes the animals. Of all the variables in Equation (4), there are four unknowns, v1, v2, vf, and f; the others are either known (vT is obtained through calibration), or directly measurable during the experiment (w1, w2, 1, 2, m). Since there are four unknowns and four equations, we can solve the equation for density f. Although Equation (4) is non-linear, it is straightforward to obtain the solution:
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| (5) |
Experiment
The experiments were conducted from April 2001 to July 2001 at the Ocean Sciences' Centre (OSC), Memorial University of Newfoundland, where a large number of larval cod were reared. It was the spawning and production season for cod and so there were enough live cod eggs and larvae surplus to the on-going projects at the OSC to conduct reliable experiments.
Since the sound speed in seawater as well as in the animal's body is very sensitive to temperature, the acoustic chamber of the APOP was kept in an experimental tank (about 2x2x0.7 m) to keep it equilibrated with the surrounding seawater. The seawater in the tank was continuously pumped directly from the ocean. A drain on the tank bottom allowed the water to circulate. This kept the water temperature as close as possible to the temperature in the incubator, where the cod eggs and larvae were kept. Although the water depth in the tank was only about 0.7 m, to avoid any stratification that might affect the quality of the experiments a pump was used to mix the seawater in the tank. The temperature was mostly between 6 and 12°C. The animals were held in a mesh container, which was then placed in the tank for at least 20 min so that they would acclimatize to the seawater before each sound-speed measurement. The temperature difference was usually less than 2–3°C before acclimation. To prevent the possibility of bubbles becoming attached to the wall inside the acoustic chamber a small, hand-held water pump was used to push water through the chamber and release any that formed.
The acoustic chamber of the APOP is a cylindrical tube (21 cm long and 2.5 cm in diameter) made of Acetal plastic (Delrin) (Figure 1). The animal compartment (D) is 2 cm in length. A guide tube about 10 cm long is attached to the animal compartment. During the experiment, live animals were fed into the guide tube with a pipette and were gently pushed into the animal compartment with the plunger (Figure 1). The animals were confined in the compartment by two thin rubber sheets, natural latex sheeting with a thickness of 0.04 mm (Chu et al., 2000a). Several pipette loads were usually needed to fill the compartment sufficiently. A pair of broadband transducers (350–650 kHz) were mounted at the two ends of the chamber. Acoustic pulses were transmitted and the waveforms with and without animals present were recorded at a sampling rate of 10 MHz. Each time-series was averaged coherently over 200 pings.
After the acoustic measurements had been made and while the chamber was still submerged, the animal compartment was examined to make sure that there were no visible bubbles attached to the latex sheet. The animals were then transferred to a beaker (500 ml) for density measurements and were inspected visually to make sure that there was no apparent body damage after the sound-speed estimation. In the density experiment, natural seawater and distilled water were used as fluids 1 and 2, respectively. The volume of the container was 28.895 ml. To reduce the uncertainty of the measurement, the volume ratio of fluid 1 to fluid 2 was kept at close to 1:1. After adding fluid 2 to the mixture of fluid 1 plus the animals, the resulting solution was then mixed slowly by sucking and injecting with a needle syringe to avoid introducing bubbles into the chamber. The weights were measured with a digital, electric-balance scale (Ohaus, AP210, with a precision of ±0.1 mg). The densities were measured with a density meter (Anton Paar, DMA4500, with a precision of ±0.00003 g m–3).
In addition to the analyses of sound-speed and density contrasts, we also measured the lipid content of the cod eggs and larvae. Live larval cod were collected for lipid analysis using the technique described by Parrish (1999). Thin-layer chromatography (TLC) on silica gel-coated Chromarods was used in conjunction with an Iatroscan flame-ionization detector to separate samples into 13 lipid classes. The total lipids were determined by summing the lipid classes. This lipid extraction method has a detection limit of about 50 ng. Between 15 and 200 larvae, depending on their size, were pooled to obtain enough sample volume to analyze. These groups were always from the same cohort and hatch day, that was used for the acoustic and density measurements. The water from the experimental tank was used as a blank.
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Results and data analysis |
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TopIntroductionMethodsResults and data analysisConclusionsReferences |
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The density contrast of cod eggs was always less than unity, consistent with the fact that the eggs always floated on the water surface. Similarly, the density contrasts of early-stage larvae were mostly less than unity (Table 1). In general, the density contrasts were almost constant and slightly less than unity (mean g=0.9875, s.d.=0.0142), indicating that they were lighter than seawater. On the other hand, the corresponding sound-speed contrasts were generally larger than unity and increased with the age of the larvae, reflecting the influence of swimbladders in larvae older than 5 days post-hatch. The sizes of the eggs, larvae, and swimbladder (Table 1) were estimated from amplified images taken under a microscope (Figure 2). The mean length and volume of swimbladders of 5 days post-hatch larvae were not actually measured. They were inferred from the prolate-spheroid model described in the following paragraph. The size of larvae 30 days post-hatch was smaller than that of 22 days because the larvae were from different groups and the former group grew more slowly. The total lipid-per-unit dry weight of larval cod increased as the age of larvae increased, but there was no obvious relation between the total lipid content and either the density contrast or the sound-speed contrast, except that larval cod have a higher total lipid content than eggs.
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Typically, swimbladders in cod larvae start to develop about 5 days post-hatch and are initially spherical in shape. Later they become elongated and the elongation accelerates after 30 days post-hatch (Morrison, 1993) (Figure 2). The effective sound-speed contrast heff of larvae with swimbladders listed in Table 1 was computed using Equation (1), since this represents the apparent sound-speed contrast per-unit-total-fish volume despite the fact that the scatterers are treated as weakly scattering objects. A more rigorous approach is to use Equation (3) with two types of scatterers, weakly scattering objects (body flesh) and gas bubbles (swimbladder). For eggs and 1-day post-hatch larvae, there are no swimbladders, while for cod larvae older than 5 days post-hatch, both body tissue and swimbladder contribute to the scattering and will affect the estimated effective sound-speed contrast. Sound-speed contrast and the scattering-induced attenuation coefficient plotted as a function of the number of days post-hatch reveal that the sound-speed contrast generally increases with time and the attenuation generally decreases with time (Figure 3). The theoretical predictions were based on the best fit obtained by adjusting the size of the swimbladders, modelled as prolate spheroids, to reflect the percentage of the gas volume in swimbladders, or the ratio of swimbladder inflation. The theoretical model used in obtaining Figure 3 is a hybrid scattering model. The overall scattering is the incoherent sum of the scattering from swimbladder and tissue:
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| (6) |
swim and tissue are the differential-scattering cross-sections in the forward direction of swimbladder and fish tissue, respectively. For the swimbladder, the scattering model combines the solutions given by Love (1978) and Ye (1997), which take into account its geometric elongation and physical properties. For the tissue, the scattering model was based on the DWBA solution for a prolate spheroid of the same volume (Chu and Ye, 1999). The inverted inflation ratio can be described approximately by an exponential function: Rinf = 
eßt, where and ß are coefficients, 0.0173 and 0.2002, respectively, determined by linear regression (Figure 4), and t is the number of days post-hatch. The extrapolation to Rinf=100% predicts that 43.3 days are needed for the swimbladder to be fully inflated. With the estimated sound-speed and density contrasts and the sizes of swimbladders determined by the best fit, thus taking into account the inflation ratio, the model could be used to estimate the average TS in decibels of individual cod larvae at 500 kHz (Figure 5). The regression line was found to be
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| (7) |
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On the same basis we computed the TS at 120 kHz, to compare our results with previously published data for juvenile and adult cod (Nakken and Olsen, 1977; Rose and Porter, 1996). The comparison is shown in Figure 6. Note that the regression line based on Nakken and Olsen (1977) has a slope coefficient greater than 20 (24.6), while the slope from Rose and Porter (1996) is less than 20 (17.9). The regression lines for juvenile and adult cod intercept that for larval cod based on our experiments. By allowing a 2% variation in the fitted parameters of all three regressions, the intercepting points fall in a box bounded by L = 1.19 – 1.43 cm and TS = –67.1 to – 57.5 dB. This box is shown as a shaded rectangle in Figure 6. On the other hand, the length corresponding to 43.3 days post-hatch, the time when the swimbladder is fully inflated (Figure 4), can be estimated independently from the regression of the data listed in Table 1 (inset in Figure 6). This length is estimated to be 1.17 cm. Given the uncertainties associated with both the measurements and the scattering model, this estimate is reasonably close to the length range of the intercept box (1.19–1.43 cm) which defines the transition region as the swimbladders become fully inflated. Around this biological and physiological change of state, the acoustic scattering has very different characteristics, particularly in the slope of the TS–L function.
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In all of our computations, higher-order (two-way), multiple scattering corrections were not considered. Although the number of animals in the experiments was as high as 17 000 for larval cod of 5 days post-hatch, the volume fraction of gas of the swimbladders, or void fraction was only on the order of 10–6. Consequently, the correction due to higher-order multiple scattering, according to Ye (1995) and Kargl (2002), was negligible and could be ignored.
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Conclusions |
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TopIntroductionMethodsResults and data analysisConclusionsReferences |
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Experimental analyses of the sound-speed and density contrasts of the eggs and larvae of Atlantic cod up to 36 days post-hatch have been made. The density contrasts for almost all measured early larval stages were less than unity, while the corresponding sound-speed contrasts were mostly greater than unity. By fitting the sound-speed contrast and attenuation acoustic data, a regression relation between the TS and the larval length was derived.
In addition, based on the estimated dimensions of the swimbladders, an exponential relation between the age of larvae and the swimbladder-inflation ratio was found. Based on this relation, the time required for the swimbladder to be fully inflated was estimated to be 43.3 post-hatch days. The length of the cod larvae at that age is estimated to be 1.2–1.4 cm. For cod larger than 1.5 cm, the previously determined TS functions for juvenile and adult cod should be applicable (e.g., Nakken and Olsen, 1977).
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Acknowledgements |
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We thank a number of people at the Ocean Sciences Centre, Memorial University of Newfoundland: Dr J. Brown for providing laboratory space and experimental facilities, D. Boyce, L. Thorne, and D. Green for providing cod eggs and larvae, J. Wells for the lipid analysis, and Dr P. Davis for protein analysis. The work is supported by the Comer Science and Education Foundation, Grant No. 250471 and the National Science Foundation, Grant No. OCE-9730680. This is Woods Hole Oceanographic Institution contribution number 10666.
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References |
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