Acoustic scattering characteristics of several zooplankton groups
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1 ICES Journal of Marine Science, 53: Acoustic scattering characteristics of several zooplankton groups Timothy K. Stanton, Dezhang Chu, and Peter H. Wiebe Stanton, T. K., Chu, D., and Wiebe, P. H Acoustic scattering characteristics of several zooplankton groups. ICES Journal of Marine Science, 53: The acoustic echo levels from zooplankton are strongly dependent upon the acoustic frequency and size, shape, orientation, and material properties of the animals. Because of the great number of species of zooplankton, it is practical to study the acoustic properties of species grouped by their gross anatomical similarity. Zooplankton from several major groups are discussed: fluid-like (decapod shrimp, euphausiid, salp), hard elastic shelled (gastropod), and gas-bearing (siphonophore). The results from laboratory tests show that the plots of (single ping) target strength versus acoustic frequency have a distinct pattern for each animal type. For example, the plot for euphausiids when ensonified at broadside incidence contained a series of broadly spaced deep nulls; the plot for gastropods either had more tightly spaced nulls or a flat spectrum; the plot for siphonophores either had a less consistent pattern of nulls or a flat spectrum. The nulls from the euphausiid data were sometimes as deep as 30 db below surrounding levels. The patterns are linked to the physics of the scattering process and modeled mathematically. In addition, key results on these animals from Stanton et al. (1994a, ICES J. Mar. Sci., 51: ) are summarized to further illustrate the variability in scattering characteristics of the animal groups (for example, data from 2-mm-long gastropods show that they produce a level of echo energy per unit biomass approximately (i.e., 43 db) times greater than that of 30-mm-long salps). The impact of these observations on design and interpretation of acoustic surveys is discussed. Very importantly, drawing a simple relationship between echo energy and biomass for regions containing a complex assemblage of zooplankton would be greatly flawed International Council for the Exploration of the Sea Key words: acoustics, biomass, scattering, zooplankton. T. K. Stanton and D. Chu: Department of Applied Ocean Physics and Engineering, Woods Hole Oceanographic Institution, 98 Water Street, Woods Hole, Massachusetts , USA. P. H. Wiebe: Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA. Correspondence to Stanton [tel: , fax: ]. Introduction In order for acoustic surveys of zooplankton to be accurate, the acoustic scattering properties of the animals must be known. This requirement poses severe practical problems because of the wide variety of zooplankton present in the ocean. The scattering of sound by the animals depends upon their size, shape, orientation, and material properties as well as the frequency of the echosounder. With the many species of zooplankton spanning a wide range of these morphological parameters, the scattering properties will, in turn, vary widely. Approaching the problem of acoustically characterizing the animals on a species-by-species basis is generally not practical, except in some special circumstances where only one or several species will consistently dominate the scattering. Hence, other systematic approaches must be used. In our studies, we group zooplankton according to gross anatomical class. The three major classes studied to date are: fluid-like (e.g. shrimp-like animals and salps), gas-bearing (e.g. siphonophores), and elasticshelled (e.g. gastropods) (Fig. 1). Because of the distinctly different boundary conditions of each class, the scattering models will vary accordingly. By studying animals in each class, the results can provide insight into the scattering properties of other animals within the same class. In this paper, we present new results from recent laboratory-style measurements, conducted at sea, of acoustic scattering by animals from the abovementioned three classes. Data and associated scattering /96/ $18.00/ International Council for the Exploration of the Sea
2 290 T. K. Stanton et al. (a) (b) f FI f BI "Winged" foot Opercular opening Hard elastic shell models illustrating differences in acoustic signatures of the animals due to their differences in morphologies are presented. Also given are key results from Stanton et al. (1994a) which demonstrate variability in overall scattering levels due to the various types of animals. Impact of the variability in scattering properties on echo-sounder surveys of complex (i.e. multispecies) zooplankton assemblages is discussed. Basic equations Incident field (c) Gas inclusion Incident field Tissue (nectophores, gastrozooids, etc) The following analysis relies on the basic quantities, scattering amplitude, f, backscattering cross-section, σ bs, and target strength, TS, which are defined below. The scattering amplitude is defined in terms of the amplitude of the incident sound pressure P 0 and scattered pressure p s as: where r is the distance between the target and echosounder, k is the acoustic wavenumber (=2π/λ, where λ f TISSUE Incident field Figure 1. Zooplankton from three anatomical groups: (a) fluid-like (euphausiid), (b) hard elastic-shelled (gastropod), and (c) gas-bearing (siphonophore). Near each animal is a diagram illustrating dominant scattering mechanisms. f FI f L f GAS is the acoustic wavelength), and i= 1. The target strength can be defined in terms of the square of the magnitude of the scattering amplitude for the backscattering direction: TS=10 log f bs 2 =10 log σ bs =10 log (σ/4π) (2) Expressions are also given in this equation relating target strength to the two different forms of backscattering cross-section, σ bs and σ. The average target strength is averaged first on a linear scale before the logarithm operation is performed: Experiments θ L We have recently completed a series of acoustic scattering experiments involving individual live zooplankton in a laboratory-style tank both on land and at sea. The land experiments were performed at the Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA and the Naval Undersea Warfare and Engineering
3 Acoustic scattering characteristics of zooplankton 291 Center, Newport, Rhode Island, USA over the period with live decapod shrimp that were caught locally. For animals living further offshore, the tank experiments were performed on the deck of two ships, RV Oceanus (1993) and RV Endeavor (1994), with live, freshly caught animals near the sites at which the animals were caught. The sites were over or near Georges Bank, which is approximately 100 km from Cape Cod, Massachusetts. At these sites, a wide variety of animals were captured with a 1-m-diameter ring net equipped with a 335-μm mesh and a 32-cmdiameter 46-cm-tall codend bucket similar to that described by Reeve (1981). The net was hauled slowly from m depths to the surface and the experiments performed as soon as possible after capture of the animals. The scattering measurements focused on the three categories discussed above: salps and euphausiids (fluid-like), gastropods (elastic-shelled), and siphonophores (gas-bearing). In all experiments, the animals were suspended in the beams of acoustic transducers with thin monofilament or human hair tethers and ensonified at some or all of the frequencies 50 khz, 70 khz, 120 khz, 165 khz, 200 khz, and 250 khz 1.2 MHz. The lower frequency range ( 200 khz) involved powerful single-frequency transducers transmitting a gated sine wave, while the upper range ( 250 khz) involved a combination of powerful single-frequency transducers and three sets of less sensitive broadband transducers that were used to transmit chirp signals (i.e. linearly frequency modulated signals). The broadband transducers had center frequencies of approximately 250 khz, 500 khz, and 1 MHz with about a one octave bandwidth. Owing to the lower sensitivity of the broadband transducers and reverberation due to temperature and salinity microstructure at the lower frequencies, many measurements involved only a subset of frequencies. Time constraints also limited how many frequencies were used. Furthermore, great care was exercised (1) making sure that the animals were free of bubbles that may have become attached to them during handling and (2) ensuring that the data kept for analysis were free from contamination due to possible echoes from the tether. Hundreds of pings per frequency were typically recorded so that the statistical behavior of the echoes could be studied. Details of the experimental setup and calibration procedures can be found in Stanton et al. (1994a), Chu et al. (1992), and Stanton (1990). Target-strength results and modeling In this section, broadband single-ping echoes from various individual zooplankton are examined euphausiid (Meganyctiphanes norvegica (Sars)), gastropod (Limacina retroversa (Fleming)) and siphonophore (Agalma okeni (Eschscholtz) or A. elegans (Sars)). Average target-strength values and associated simplified modeling for frequencies as low as 50 khz and as high as 1.4 MHz are reported for the various animals in Stanton et al. (1994a). Broadband measurements of target strength of the various individual animals showed some marked differences in pattern of (single-ping) target strength versus frequency (Fig. 2). The patterns derived from the euphausiid echoes were typically characterized by a series of peaks and deep dips or nulls. In contrast, a substantial fraction of the data from the siphonophores and gastropods contained much less structure. The TS versus frequency pattern of the echoes from these latter two animals ranged from sometimes nearly flat to other times exhibiting a strong structure. Although the patterns of the echoes from the two animals both spanned the same extremes, the patterns from all three animals were significantly different on a statistical basis when many echoes from each animal were studied (Martin et al., 1996). It is apparent from these plots that the differences in morphology give rise to differences in acoustic scattering signatures. Structures in the TS versus frequency plots indicate an interference pattern due to echoes from the same transmitted signal arriving at different times from the same animal (Fig. 1). Depending upon the acoustic frequency, the echoes can add constructively and produce a peak, add destructively resulting in a null, or produce some intermediate result. Because the ping is much longer than the dimensions of any animal under investigation, it is impossible to distinguish between any multiple echoes from the raw chirp echoes. However, because of the high bandwidth of the chirp signals (roughly one octave), we were able to compress the echoes with a commonly used matched filter process. The duration of the compressed echo is approximately equal to the inverse of the bandwidth of the signal. Applying the matched filter to each (total) echo from each animal typically resulted in a main return along with at least one secondary arrival (unpublished). The time difference between the two arrivals of the matched filter output was different for each animal. The time difference for broadside incidence with the euphausiids correspond to the time it would take for the acoustic signal to travel from one side of the animal to the other, and back again. This observation indicates that one arrival is due to the front interface and the other from the back interface (Fig. 1a). The general formula to describe this phenomenon is given by: f bs f FI +f BI (near broadside incidence) (4) where the summation of scattering amplitudes from the front interface ( FI ) and back interface ( BI ) produces the total scattering amplitude. This formulation has been presented in earlier work for decapod shrimp (Stanton et al., 1993a) and evaluated in detail,
4 292 T. K. Stanton et al. Euphausiid Gastropod 40 Target strength (db) Siphonophore but is now further verified with the use of both a different species within the same anatomical group and matched filter processing. For angles off broadside, one can either expand the above summation to take into account discrete contributions from other body parts (Stanton et al., 1994b) or use a standard volume integral (Distorted Wave Born Approximation or DWBA) approach (Chu et al., 1993; Stanton et al., 1993b). The time difference between the two main arrivals of the matched filter output for the gastropods did not correspond to the round trip between any parts of the body. In fact, the time difference corresponded to the round trip between two points separated by a distance much larger than any dimension of the animal. Since this is not physically possible, it was apparent that a different physical mechanism was dominating the scattering. In contrast to the fluid-like euphausiid, where the sound wave can easily penetrate the body, the gastropod has a hard elastic shell that has the potential for supporting Lamb waves that circumnavigate the shell (Fig. 1b). These surface elastic waves (SEW) can sometimes be subsonic (especially in the near unity ka range Frequency (khz) Figure 2. Target strength versus frequency for single echoes off individual zooplankton. Two pings per species are given to illustrate the range of scattering properties of the animals. Theoretical curve (when plotted) is given by thin line. Experimental data given by thick line. in which we are dealing) which can give rise to secondary echoes returning at a time much after the initial echo from the front interface. The secondary echoes we have observed correspond to a subsonic speed approximately 1/8 that of the surrounding water. The corresponding general model is given as: f bs f FI +f L (5) where the summation of returns due to the front interface and Lamb ( L ) wave are given. This is a greatly modified form of the exact solution for the scattering of sound by fluid-filled spherical elastic shells. Only the dominant (subsonic) Lamb wave is given and implicit in the equation are terms to account for roughness of the shell (giving rise to random paths around the shell) and complete extinction of the Lamb wave due to geometries when it encounters the opercular opening of the shell. The time differences between the two main arrivals of the matched-filter output of the echoes from the siphonophores corresponded to lengths comparable to and smaller than the total length of the animal. This observation indicates that one echo is most likely to be
5 Acoustic scattering characteristics of zooplankton 293 due to the gas inclusion while the other echo is from some other part of the body tissue (Fig. 1c). This hypothesis is supported by an independent measurement of the scattering by a siphonophore with and without the gas inclusion. The echo from the animal without the gas was due only to tissue and about 5 db less than that from the animal with the gas. The formula for the scattering amplitude can therefore be written as: f bs f GAS +f TISSUE (6) where the scattering amplitudes from gas and tissue are added to form the total scattering amplitude. The scattering amplitude from the gas inclusion can be calculated using the exact modal series solution for fluid spheres (since fluid in this acoustics context applies to gas in that it does not support shear waves). The scattering by the tissue can be modeled using either a simple ray formula as in Equation (4) or a more precise formula involving the DWBA. Application of the above formulae using their more explicit forms shows reasonable agreement under some conditions between theory and single-ping echoes (Fig. 2). The two-ray weakly scattering theory fits some euphausiid data (left plot). However, the patterns from other echoes are more erratic and the two-ray model is not appropriate (right plot). In fact, it is shown in another analysis that in this more chaotic type of pattern a six-ray model is more appropriate (Stanton et al., 1994b). It is hypothesized that in that case there are echoes from many parts of the body, such as off broadside incidence (that is in contrast to broadside incidence where it is expected that only two rays dominate the scattering). The two extreme cases for the gastropod were readily described by the same theory. In the case in which the pattern of target strength versus frequency was oscillatory, the theory included echo contributions from both the front interface and Lamb wave (left plot). In the case in which the pattern of data was relatively flat, the Lamb wave was suppressed in the model which led to the flat theoretical curve (right plot). It is hypothesized for the experiment producing the oscillatory data for the gastropod that the opercular opening was oriented such that the Lamb wave could propagate freely on the surface with enough energy so that it could re-radiate and interfere significantly with the echo from the front interface. Similarly, it is hypothesized that, in the experiment producing the flat pattern, the Lamb wave was attenuated severely due to the opercular opening. Hence, the echo from the front interface suffered no interference. Finally, for the flat patterns associated with the siphonophore, it is assumed that the gas bubble dominated the scattering free from significant interferences. The exact solution to the gas sphere predicts the observed flat pattern (left plot). However, in the cases in which the patterns from the siphonophore contained a series of peaks and deep nulls, a more complex theory is required. It is hypothesized that for some orientations the echoes from the various parts of the tissue may add up strongly enough to interfere substantially with the echo from the bubble. Modeling of the tissue contribution would involve evaluation of the second term in Equation (6), most likely in a stochastic manner. Once the echoes are averaged over many pings (according to Equation (3)) as the animal changes orientation, the structure in the TS versus frequency plots tends to become washed out, except in the case of euphausiids where some of the structure remains (not shown). This residual structure is due to the fact that the structure occurs near broadside incidence where the echoes are the strongest. Although the structure off broadside incidence varies substantially, the echo is much weaker and cannot fully offset the null values in the averaging process (Stanton et al., 1993b). Impact on acoustic surveys of zooplankton The differences in scattering properties illustrated above have a profound impact on the manner in which one should interpret echo survey data. As a result of the different scattering mechanisms of the animals, each type of animal scatters sound with a different degree of efficiency. For example, at 200 khz, the 2-mm-long gastropods scatter sound approximately times more efficiently (on an echo energy per unit biomass scale) than the 30-mm-long salps (Table 1). As a result of this difference in scattering efficiency, it only takes about 14 m 3 of these small gastropods to produce a level of volume scattering strength of 70 db at 200 khz, while it would take about 190 salps to produce that same level (Table 2). This difference changes dramatically at 38 khz, where the 2-mm-long gastropods are in the Rayleigh scattering region and 6250 are required to produce the 70 db volume scattering strength. (Note that the values for the shrimp and salp do not decrease monotonically with frequency because nulls in the backscattering versus frequency plots (not shown) do not wash out completely when averaging over angle of orientation (averaging was performed over all angles, 0 2 π).) These differences in scattering efficiency must be taken into account when estimating biomass from values of echo energy. The importance of taking into account the differences in scattering efficiencies was illustrated in a recent study by Wiebe and colleagues (Wiebe et al., in press), where the distribution of zooplankton and their associated volume scattering strengths were studied over Georges Bank near Cape Cod, Massachusetts, USA. In that study it was observed that the volume-scattering
6 294 T. K. Stanton et al. Table 1. Relative echo energy per unit biomass for animals as measured from several major classes of gross anatomical features. Acoustic frequency: 200 khz. The results are similar at other higher frequencies. (From Stanton et al., 1994a). Relative (echo energy)/(biomass) Linear scale Decibel (db) scale Physical information Average length (mm) Average wet wt. (mg) Gastropod (elastic shelled) Siphonophore (gas-inclusion) Decapod shrimp (fluid-like) Yellowtail fish (swimbladder-bearing) Salp (fluid-like) Table 2. Number of animals per cubic meter it would require to produce a volume scattering strength of 70 db. Sizes of animals used in calculations are given in Table 1. Frequency (khz) Gastropod Siphonophore coefficient (a linear form of the volume-scattering strength) was 4 7 times greater in the stratified region, where there was a strong consistent thermocline, than that observed in the well-mixed region, where the temperature was essentially constant throughout the entire water column. However, the biomass in both regions was essentially the same. The difference between the two values of volume-scattering coefficient was largely explained by the presence of gastropods. There were many more gastropods in the stratified region than in the well-mixed region (enough to account for the factor of 4 7). However, the gastropods contributed to less than 25% of the total biomass in each region. Thus, it was the change in species composition of the population, not the biomass, that appeared to cause the change in acoustic echo levels. Summary and conclusions Decapod shrimp Salp As a result of a series of laboratory-style experiments both on land and at sea, major differences in scattering mechanisms of various zooplankton groups have been observed and mathematically modeled. In particular, the fluid-like, elastic-shelled, and gas-bearing animals have distinct patterns of target strength versus frequency as well as sometimes dramatically different scattering efficiencies. The difference in patterns and scattering efficiencies, as well as compressed (matched filter) time series, has helped guide the development of the scattering models. This new set of models is helping to make possible the accurate interpretation of acoustic surveys of zooplankton in the ocean. The potential of these models was realized in their application to volume reverberation data where a wide variety of zooplankton were involved. While the results are very promising, it is clear that other anatomical groups must be studied as well as other species within the above-mentioned groups. With a broader set of data and scattering models, areas with other animal types can be accurately surveyed as well. In conclusion, great differences in morphologies of various zooplankton groups can lead to great differences in their scattering signatures. Understanding the physical scattering mechanisms will help form the basis of accurate scattering models and improved interpretation of acoustic survey data. Acknowledgements The authors are grateful to the following people from the Woods Hole Oceanographic Institution, Woods Hole, Massachusetts: Paul Boutin, Shirley Bowman, Nancy Copley, Charles Corwin, Bob Eastwood, Al Gordon, Steve Murphy, Ed Verry, and the Captains and Crews of the RVs Oceanus and Endeavor. This work was supported by the National Science Foundation Grant No. OCE and the US Office of Naval Research Grant Nos. N J-1729 and N This is Woods Hole Oceanographic Institution Contribution No References Chu, D., Stanton, T. K., and Wiebe, P. H On the frequency dependence of sound backscattering from live zooplankton. ICES Journal of Marine Science, 49: Chu, D., Foote, K. G., and Stanton, T. K Further analysis of target strength measurements of Antarctic krill at
7 Acoustic scattering characteristics of zooplankton khz and 120 khz: comparison with deformed cylinder model and inference of orientation distribution. Journal of the Acoustical Society of America, 93: (L). Martin, L. V., Stanton, T. K., Lynch, J. F., and Wiebe, P. H Acoustic classification of zooplankton based on singleping broadband insonifications. ICES Journal of Marine Science, 53: Reeve, M. R Large cod-end reservoirs as an aid to the live collection of delicate zooplankton. Limnology and Oceanography, 26: Stanton, T. K Sound scattering by spherical and elongated shelled bodies. Journal of the Acoustical Society of America, 88: Stanton, T. K., Clay, C. S., and Chu, D. 1993a. Ray representation of sound scattering by weakly scattering deformed fluid cylinders: simple physics and application to zooplankton. Journal of the Acoustical Society of America, 94: Stanton, T. K., Chu, D., Wiebe, P. H., and Clay, C. S. 1993b. Average echoes from randomly-oriented random-length finite cylinders: zooplankton models. Journal of the Acoustical Society of America, 94: Stanton, T. K., Wiebe, P. H., Chu, D., Benfield, M., Scanlon, L., Martin L., and Eastwood, R. L. 1994a. On acoustic estimates of zooplankton biomass. ICES Journal of Marine Science, 51: Stanton, T. K., Wiebe, P. H., Chu, D., and Goodman, L. 1994b. Acoustic characterization and discrimination of marine zooplankton and turbulence. ICES Journal of Marine Science, 51: Wiebe, P. H., Mountain, D., Stanton, T. K., Greene, C., Lough, G., Kaartvedt, S., Manning, J., Dawson, J., and Copley, N. In press. Acoustical study of the spatial distribution of plankton on Georges Bank and the relationship between volume backscattering strength and the taxonomic composition of the plankton. Deep-Sea Research.
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