ICES Journal of Marine Science, 53: 289–295. 1996
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. 1996. Acoustic scattering characteristics of
several zooplankton groups. – ICES Journal of Marine Science, 53: 289–295.
? 1996 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
02543-1053, USA. P. H. Wiebe: Department of Biology, Woods Hole Oceanographic
Institution, Woods Hole, Massachusetts 02543, USA. Correspondence to Stanton [tel:
+1 508 289 2757, fax: +1 508 457 2194].
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
1054–3139/96/020289+07 $18.00/0
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
? 1996 International Council for the Exploration of the Sea
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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: 505–512) 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 19 000 (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.
290
T. K. Stanton et al.
(a)
(b)
"Winged"
foot
Opercular
opening
Hard elastic
shell
fFI
fBI
θL
fFI
fL
(c)
Gas inclusion
fGAS
Incident field
fTISSUE
Tissue
(nectophores,
gastrozooids, etc)
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.
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
The following analysis relies on the basic quantities,
scattering amplitude, f, backscattering cross-section, óbs,
and target strength, TS, which are defined below. The
scattering amplitude is defined in terms of the amplitude
of the incident sound pressure P0 and scattered pressure
ps as:
where r is the distance between the target and echosounder, k is the acoustic wavenumber (=2ð/ë, where ë
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 logPfbsP2 =10 log óbs =10 log (ó/4ð)
(2)
Expressions are also given in this equation relating
target strength to the two different forms of backscattering cross-section, óbs and ó. The average target strength
is averaged first on a linear scale before the logarithm
operation is performed:
Experiments
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
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Incident field
Incident field
Acoustic scattering characteristics of zooplankton
291
age 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:
Target-strength results and modeling
fbszfFI +fBI
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)). Aver-
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,
(near broadside incidence)
(4)
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Center, Newport, Rhode Island, USA over the period
1990–1992 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-ìm mesh and a 32-cmdiameter#46-cm-tall codend bucket similar to that
described by Reeve (1981). The net was hauled slowly
from 50–500 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).
292
T. K. Stanton et al.
–40
Euphausiid
–60
–80
–100
Gastropod
–60
–80
–100
–40
Siphonophore
–60
–80
–100
400
500
600
700
800
400
Frequency (kHz)
500
600
700
800
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.
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
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:
fbszfFI +fL
(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
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Target strength (dB)
–40
Acoustic scattering characteristics of zooplankton
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:
fbszfGAS +fTISSUE
(6)
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 19 000 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 ð).)
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
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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
293
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)
Decibel
(dB)
scale
19 000
260
270
140
1
43
24
24
21
0
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)
38
120
200
420
Gastropod
(m "3)
6250
83
14
3.8
Siphonophore
(m "3)
Decapod
shrimp
(m "3)
Salp
(m "3)
0.20
0.38
0.59
1.5
67
2.9
1.6
2.9
110
230
190
190
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
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
Average
length
(mm)
1.9
37
16
450
26
Average
wet wt.
(mg)
3.6
1400
38
1 700 000
620
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-9201264 and the US Office of
Naval Research Grant Nos. N00014-89-J-1729 and
N00014-95-1-0287. This is Woods Hole Oceanographic
Institution Contribution No. 9181.
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