- Email: [email protected]
Acoustic discrimination of two zooplankton species (mysid) at 38 and 120 kHz
Deep-Sea Research I 46 (1999) 319—333
Acoustic discrimination of two zooplankton species (mysid) at 38 and 120 kHz P.M. David*, O. Guerin-Ancey, J.P. Van Cuyck Centre d+Oce&anologie de Marseille, Univ. d+Aix-Marseille 2, UMR 6540 CNRS/Dimar, Campus de Luminy, Case 901, 13288 Marseille Cedex 9, France Received 20 March 1997; received in revised form 17 November 1997; accepted 9 March 1998
Abstract Using bifrequency sonar (38 kHz, 120 kHz) directed towards the open sea from the inside of a submarine cave, two species of Mysidacea (Crustacea), similar in shape but not in size, and with different patterns of behaviour, were observed simultaneously and discriminated, and their biomass was estimated during their migration. The first species, Hemimysis speluncola ((1 cm length), lives in the submarine cave, forming a distinct community that migrates horizontally. The second species, Siriella jaltensis ('1 cm length), lives in the open sea and migrates vertically. These species are both detected clearly at 120 kHz, but only the larger one, Siriella jaltensis, is detected at 38 kHz. This distinction allows one to determine the size limits of planktonic objects detected at these frequencies, i.e. 3 mm at 120 kHz and 10 mm at 38 kHz, corresponding to one quarter of the wavelength. The target strength (TS) of each species was calculated from the field data and compared to results calculated from three models. As the volume of the cave occupied by the Hemimysis population is about 300 m, and the density of the swarm is 36,000 individuals/m, the number of individuals in the cave is estimated to be around 10 million (or 24 kg). The density of the open-water population of Siriella is estimated to be 13 individuals/m. 1999 Elsevier Science Ltd. All rights reserved.
1. Introduction Underwater acoustics is used to calculate the biomass and determine the distribution of plankton and fish (Beamish, 1971; Mitson and Wood, 1961). The calculation requires knowledge of the target strength (TS) of the organisms (Beamish, 1971). This varies according to the type of organism, as it depends on shape, size, and contrasts of both density and speed of sound (Samovol’kin, 1974; Kristensen and Dalen, 1986).
* Corresponding author. Fax: 0033 49 18 29 194; e-mail: [email protected] 0967-0637/99/$—see front matter 1999 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 3 7 ( 9 8 ) 0 0 0 6 4 - 8
320
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
Experiments can provide TS values for single organisms, but problems arise from the use of very high frequencies and limitations on the size of tank. Theoretical TS can be calculated by the use of models (Anderson, 1950; Machlup, 1952; Stanton, 1988) whether or not experiments to find TS for individual organisms are carried out. Methods and models have therefore been developed in order to determine zooplankton distribution and biomass acoustically, using single or multiple frequencies (Holliday et al., 1989; Greenlaw and Johnson, 1983; Pieper et al., 1990; Guerin-Ancey and David, 1993). All acoustic techniques require adequate validation by net sampling. Although the acoustic data can then be compared with data from zooplankton samples, uncertainties still arise due to the mode of sampling, the selectivity of the net, net avoidance, sampling variability, different time scales (Wiebe, 1972) and because a natural plankton community is generally a mixture of organisms (Artemov, 1983). Doubt therefore remains as to the actual population of the insonified water column; it is impossible to know the minimum size of the plankton that is detected, and whether the echoes really are due to the species found in the samples. It is therefore a great advantage to undertake measurements in populations where there are a few easily identified species, so reducing problems of validation. The submarine caves near Marseilles in southern France provide such an opportunity, where it is possible to study the acoustic response of a natural population of small zooplankters in detail. In order to obtain acoustic data attributable to a known population, we carried out a series of field experiments, in June 1990, inside a submarine cave containing a monospecific mysid population and outside, where there is a population of another mysid, and a series of laboratory experiments with specimens from these two populations. The aims were to determine the backscattering at two frequencies (38 and 120 kHz), the physical-acoustic parameters of the two species, their acoustic discrimination, and the limits of detection of the echo-sounder in terms of size class. 1.1. The natural populations The submarine caves in the neighbourhood of Marseilles were formed by underground rivers and became submerged 100,000 years ago. They open to the sea at about 20 m depth, are narrow and run horizontally into the land, to a distance of more than 200 m. The cave on Jarre Island, southeast of Marseilles, was chosen because of its depth (15 m) and easy accessibility by scuba diving, and because it has been well studied (Laborel and Vacelet 1958, 1959; Ledoyer 1989; Bourdillon and Castelbon, 1983; Bourdillon et al., 1986; Macquart-Moulin and Patriti, 1966; Macquart-Moulin and Passelaigue, 1982). The cave is inhabited by a largely monospecific community of the mysid crustacean, Hemimysis speluncola. During the day the animals live in the dark parts of the cave (70 m inside, at 10\ lux) in crevices in the walls and form dense swarms that are easy to capture by pump or net. When light decreases in the evening, the swarms gradually move out into the cave itself and leave the cave in the middle of the night. Before sunrise, the animals return to the dark parts of the cave. Because this behaviour is well known and involves a single species (Passelaigue 1989, 1991), echoes obtained within the cave can be attributed to the Hemimysis speluncola swarm with certainty.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
321
Another mysid, Siriella jaltensis, which is a little larger in size ('1 cm), lives outside the cave. During the day it occurs under stones on the sea bed. In the middle of the night it migrates vertically to the sea surface. During this migration animals pass the cave entrance and can be observed from the cave.
2. Material and methods A Biosonics sonar system with frequencies of 38 and 120 kHz was used for the field study. The transducers were fixed inside the cave at a distance of 7.5 m from the cave entrance facing outwards (Fig. 1). In this way the echo-sounder beam could ‘‘observe’’ movements near the axis of the beam inside and outside the cave. The transducers were connected by an electrical cable to the echo-sounder itself on board the N.O ANTEDON, moored nearby. Acoustic data were obtained on echograms and on a DAT casio magnetic recorder. These were then analysed in order to discriminate between the two species, to observe their migrating behaviour, to measure their respective volume scattering (Sv), to calculate the in situ target strength (TS) of individuals, and to estimate the biomass inside the cave. Sampling was carried out by divers using a small net inside the cave to catch specimens from the dense swarms in the crevices, and with a plankton net slowly hauled vertically outside the cave. Living organisms used in the laboratory measurements were carefully kept immersed in sea-water prior to the acoustic studies.
Fig. 1. Schematic representation of the acoustic experiment in the cave.
322
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
After the in-vitro experiments, the animals were fixed in formalin for counting and measuring. The allometric measurements of the bodies of 100 individuals of each species (length, radius) were used to calculate the additional parameters such as spherical radius of the equivalent volume and equivalent cylinder, incorporated in the theoretical models. The simple scattering hypothesis assumes that the total acoustic scattering energy is the sum of the components of each target excited by the ultrasonic wave (Gerard, 1991). Multiple scattering assumes that the global energy is the sum of these components, plus the multiple reflection of the wave from the particles (Arzelies, 1979). The choice of the simple or multiple scattering fields can be made empirically by comparing the wavelength j to the mean distance d between organisms. If d/j;1, the simple scattering hypothesis may be assumed. Passelaigue (1991) has estimated that the Hemimysis swarm contains 36,000 individuals/m, homogeneously distributed. The mean living space for each organism is therefore 28 cm, equivalent to a mean distance between two individuals of 3 cm. This is greater than the wavelength at 120 kHz, which is 1.25 cm, so one can assume the simple scattering hypothesis in the case of Hemimysis. Outside the cave, the living space for Siriella is less restricted (Macquart-Moulin and Passelaigue, 1982), so one may assume simple scattering to be true in this case too. The volume backscattering (Sv) is therefore calculated as the sum of the individual scattering, expressed as Sv"TS#10 log N .
(1)
where N is the number of individuals insonified by the ultrasonic beam. Schematically, the target strength can be calculated as TS"10 log (p/4n) and p/na"[4((1!gh)/(3gh)#(1!g)/(1#2g))] [2(ka)/(2#3(ka))] , where a is the radius of the equivalent spherical volume of the animal, g is the ratio of the density of the sphere to the density of the surrounding medium (i.e. density contrast), h is the ratio of the speed of sound inside the sphere to that in the surrounding medium (i.e. sound-speed contrast), and k is the wave number obtained from the expression k"2nf /c, where f is the frequency and c the speed of sound in the medium. Since the body size of Hemimysis is too small for its TS to be measured directly in the laboratory, the density contrast g was measured using calibrated baths of glycerine, and the sound-speed contrast h was measured using a velocimeter, according to Greenlaw (1977). Since the body size of Siriella is large enough for its TS to be measured directly in the laboratory, four preserved individuals of similar sizes (14 to 16 mm) were used to determine the TS between 300 kHz and 1.2 MHz in a tank. Using the simplex inversion method (Caceci and Cacheris, 1984) we obtained g and h values for Siriella.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
323
Then, these values were introduced in theoretical scattering models involving simple shaped targets, namely fluid sphere, spherical shell, and fluid cylinder (Anderson, 1950; Machlup, 1952; Stanton, 1988; Van Cuyck et al., 1992) to estimate the TS at 38 and 120 kHz for both species (Tables 1—3). Table 1 Target strength (TS) at 38 and 120 kHz of 4 Hemimysis speluncola size classes, calculated using fluid sphere, spherical shell and fluid cylinder models. The experimentally measured density and sound speed contrasts are g"1.067 and h"1.01 Fluid sphere
Spherical shell
Fluid cylinder
Classes Hemimysis
TS 38
TS 120
TS 38
TS 120
TS 38
TS 120
1: 2: 3: 4:
!152 !137 !123 !120
!132 !117 !104 !101
!146 !130 !117 !113
!126 !110 !98 !95
!144 !130 !116 !117
!124 !111 !97 !98
Larvae Juvenile Male Female
Table 2 Size classes of the Hemimysis speluncula population in the cave. N is the number of individuals in each size class calculated from the percentages of the total population. TS was calculated using the spherical shell model. Scattering volume (Sv) was calculated using N and TS of the mean population
Classes Hemimysis
Mean size (mm)
Population (%)
N Number m!3
TS Spherical Shell
Sv (dB)
1: Larvae 2: Juvenile 3: Male 4: Female Total
1.5 3.5 5.4 6.4 4.8
5 40 40 15 100
1 800 14,400 14,400 5 400 36,000
!126 !110 !98 !95 !98.6
!93 !68 !56 !58 !53
Table 3 Target strength (TS) at 38 and 120 kHz of four specimens of Siriella jaltensis, calculated using fluid sphere, spherical shell and fluid cylinder models, from TS experimentally measured between 300 kHz and 1.2 MHz. The density and sound-speed contrasts extracted with the simplex method are g"1.085 and h"1.013 Fluid sphere
Spherical shell
Fluid cylinder
Classes Siriella
TS 38
TS 120
TS 38
TS 120
TS 38
TS 120
14.3 mm 16 mm 15.5 mm 16 mm mean
!96 !93 !94 !95 !95
!80 !78 !81 !81 !80
!107 !87 !94 !89 !94
!76 !83 !77 !79 !79
!116 !115 !116 !118 !116
!97 !96 !101 !105 !100
324
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
3. Results The hydrographic measurements show that there is no density change along the cave at the mouth that might affect animals migrating horizontally or the passage of sound. There is also no fresh water coming from the cave. Light is the only factor showing a gradient that could determine and orientate migrations (Bourdillon and Castelbon, 1983; Macquart-Moulin and Passelaigue, 1982), although it may be noted that a chlorophyll maximum has been observed outside, near the cave entrance. The population of Hemimysis (Fig. 2) sampled inside the cave, was composed of larvae (class 1, mean length 1.5 mm), juveniles (class 2, mean length 3 mm), males (class 3, mean length 5.4 mm) and females (class 4, mean length 6.4 mm). The population of Siriella (Fig. 2) found outside the cave was composed of juveniles (class 1, mean length 13 mm), young adults (class 2, mean length 18 mm) and females (class 3, mean length 21 mm). The acoustic survey of the cave area shows three periods in the movement of plankton. Moments from each of these periods are illustrated in Figs. 3 and 4: (1) Before sunset, which occurred at 21.20 h, no echo was detected at 120 kHz (Fig. 3) or 38 kHz (Fig. 4) and the cave seemed to be empty, as it appeared to be outside the cave entrance. (2) Some two and a half hours after the sun had gone down, echoes were received from close to the receiver at 120 kHz; these were attributed to Hemimysis. The signal spread gradually throughout the cave in front of the receiver as the Hemimysis swarm appeared to move towards the cave mouth. The swarm filled the cave (Fig. 3) but stayed inside, at least 2—3 m from the mouth, until
Fig. 2. Size distributions of Hemimysis speluncola living inside the cave and Siriella jaltensis living outside.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
325
Fig. 3. Acoustic backscattering at 120 kHz, showing the population distribution at 21.20, 01.00 and 02.30 h, inside (0—8 m) and outside (8—16 m) the cave. Sv is the average of 10 successive values.
the moon disappeared. Virtually no echo was detected at 38 kHz before this time (Fig. 4). (3) An hour later Hemimysis was still detected at 120 kHz throughout the cave (Fig. 3), and Siriella was detected outside at both 38 and 120 kHz (Figs. 3 and 4). The echograms show that small zooplankters like Hemimysis can be detected at 120 kHz but not at 38 kHz, whereas the larger Siriella can be detected at both frequencies.
326
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
Fig. 4. Acoustic backscattering at 38 kHz, showing the population distribution at 21.20, 01.00 and 02.30 h, inside (0—8 m) and outside (8—16 m) the cave. Sv is the average of 10 successive values.
In the cave, scattering levels varied in space and time. For example, at 120 kHz at 01.00 h (Fig. 3), the Sv values of the Hemimysis swarm ranged between !53 dB and !75 dB. This variation could be due to a change in the number of organisms, but as Passelaigue and Bourdillon (1986) observed that they are numerically homogeneously distributed, this is unlikely; it could instead be due to changes in orientation or stage composition.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
327
Knowing the density of Hemimysis and the Sv measured in the cave, we estimated the TS of Hemimysis using Eq. (1). Since Passelaigue (1991) estimated the mean density of the swarm at 36,000 individuals m\ in June, from 1986 to 1989, and never indicated any change in this estimation, we assume that it would be the same density during this experiment. Given this number and considering that the population consists of only one size class (mean 4.8 mm), and that the maximum Sv was !53 dB, measured at 01.00 h, the mean in situ target strength of Hemimysis at 120 kHz is calculated to be !98.6 dB. This result is close to the value (!98 dB) that van Cuyck et al. (1992) obtained with the spherical shell model (Table 1) for the males. However, as shown in Fig. 2, the population of Hemimysis contains different quantities of four size classes (larvae, juveniles, males and females). In this case, the total signal is the sum of the scattering of each class. This was calculated for each class (Table 2) and compared with the total backscattering. The sum of the adult signals (classes 3 and 4) is !54 dB, while the sum for classes 2—3—4 is !53.84 dB and for all classes is also !53.84 dB. This indicates that the juveniles contribute little, although they are numerous, to the total backscattering signal, and the larvae do not contribute at all. The lower limit for detection therefore seems to be around 3 mm, corresponding to one-quarter of the wavelength at 120 kHz. During migration the density of the population varied, resulting in changes to the backscattering signal. During the day the organisms were concentrated in crevices in the cave. At 01.00 h the density of Hemimysis at 3 m inside the cave had reached a maximum, and the observed backscattering (Sv) was !53 dB. By 02.30 h the swarm had spread throughout the cave and begun to go outside, and the backscattering signal had fallen to !55 dB. Since the backscattering signal represents only the adults, i.e. 55% of the total population, we estimate the density of organisms in the swarm, using the spherical shell TS of classes 3 and 4 (Table 2), to have been 46,000 individuals/m at 01.00 h and 28,000 individuals/m at 02.30 h. The mean value, 37,000 individuals/m, is very close to Passelaigue’s data. Given an average density of 37,000 Hemimysis/m, with a total weight of 86 g, and a TS of !98.6 dB, we calculated the volume backscattering for 1 kg of organic matter representing 418,000 Hemimysis, to be !42 dB/m. As the total Hemimysis population in the cave is estimated by this author at 10 million individuals, we estimate that it contains about 24 kg of organic matter or 1.44 kg of carbon (see Cushing et al., 1958). Outside the cave, the organisms were also observed at 120 kHz (Fig. 3). At 01.00 h the population was still in the cave. At 02.30 h there was a response from inside and outside the cave, which appeared to come from Hemimysis in the cave and from Siriella outside on its vertical migration. The maximum backscattering, measured outside, near the mouth of the cave, was !68.69 dB. The TS values calculated at 120 kHz for preserved specimen of Siriella are shown in the Table 3 from the three models. In calculating the density of Siriella in front of the cave, we used a TS value of !79 dB in order to be consistent with the Hemimysis estimates using the spherical shell model. Since the 120 kHz frequency can detect Hemimysis at a length of 2—4 mm, this frequency will detect the total adult and juvenile Siriella population whose shortest length is 11.5 mm.
328
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
From Eq. (1) and the maximum recorded backscattering (!68.69 dB), we calculated the population density of Siriella to be 13 individuals m\. This is three orders of magnitude less than Hemimysis density, but is in accord with the plankton samples taken in the evening and at night, which gave the following results between the surface and 15 m depth: Hour Individuals m\
21.20 0
01.00 0.25
02.30 4
The 38 kHz echograms (Fig. 4) show that none of the Hemimysis, not even the largest organisms (8 mm), were detected. Signals came only from outside the cave, from the Siriella population with a minimum length of 11.5 mm. Outside the cave, the maximum backscattering (Fig. 4) observed at 38 kHz was !82 dB. The TS of Siriella (Table 3), calculated using inverse methods, provide an estimate of the population density. Using the TS at 38 kHz, obtained with the spherical shell model in order to be consistent with the Hemimysis estimate and Eq. (1), we calculated a density of 16 animals m\. This is very close to the density calculated from the 120 kHz data and indicates that even the smallest individuals could be detected at 38 kHz. We therefore conclude that the minimum size of mysids that can be detected at 38 kHz is between 8 and 11.5 mm, i.e. approximatively one quarter of the wavelength. The TS values calculated at 120 and 38 kHz from the spherical shell model provide an estimate of the number of Hemimysis and Siriella. This model could be tried for other crustaceans. 4. Discussion The TS of mysids depends on the acoustic characteristics of the target, such as size, shape, speed of sound and density contrasts, and on the frequency of detection. The values of g and h measured for living crustaceans Hemimysis, according to the Greenlaw (1977) method, give g"1.067 and h"1.01, for a size range of 4 to 8 mm. The range of density contrast (g) reported in the literature for planktonic marine crustaceans, essentially euphausiids, varies from 1.016 to 1.12, while the values of sound speed contrast (h) range from 1.007 to 1.033 (Greenlaw, 1977; Holliday and Pieper, 1980; Kogeler et al., 1987; Chu et al., 1993). In addition, we observe, as did Kogeler et al. (1987) and Kristensen and Dalen (1986), that the density increases when the body length decreases, which can explain the high contrast values found here. Using the simplex method, the mean values g"1.085 and h"1.013 were calculated for four preserved Siriella. The preservation, but also the death, produces changes in the body composition leading to effects on the physical parameters. Flagg and Smith (1989) considered that the preserved non gelatinous plankter composition is relatively unchanged, but Greenlaw et al. (1977) noticed a 1.9% decrease. Nevertheless, g and h values for the studied crustaceans are very close to those quoted in the literature. Differences are also due to the very diverse experimental conditions, such as temperature, fresh or sea water, species, size, shape, preserved or living organism.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
329
All the TS values given for Hemimysis (Table 1) with the spherical shell and the fluid cylinder models are similar and close to the TS found in the literature for crustaceans of the same size range (Holliday and Pieper, 1980). The fluid sphere model always gives the lower TS. The difference between the TS at 38 and 120 kHz is about 19 dB. At 38 kHz the TS are less than !100 dB (Table 1), so this species is too small to be detected at this frequency. For Siriella, (Table 3) the fluid sphere and the spherical shell models give similar results, and the fluid cylinder gives lower TS (20 dB difference). Between 38 and 120 kHz the difference is 15 dB. From all these results, it appears that the spherical shell model is convenient for both species and gives TS close to the literature values. The range of TS reported in the literature for 30—40 mm length euphausiids varies from !89 to !84 dB at 38 kHz and from !74 to !80 dB at 120 kHz (Foote et al., 1990; Greene et al., 1991; Chu et al., 1993) and for 7 to 31 mm length mysids from !95 to !67 dB at 1.2 MHz and 420 kHz (Richter, 1985; Wiebe et al., 1990). As noted above, the relation between the length of the crustacean and the wavelength is particularly important for TS and biomass determination. The best estimate of TS of a population is obtained when the size of the individuals equals the wavelength. If the individuals of a population are similar in size, the backscattering signal can provide an estimate of biomass such that Sv is a linear function of the number of individuals. The biomass of the Hemimysis swarm calculated using a mean TS of !98.6 dB at 120 kHz is !42 dB kg\, for a mean length of 4.8 mm and a mean weight of 2.39 mg. At the same frequency, Macaulay et al. (1995) found !38 dB kg\ for 25—30 mm length, assuming an average weight of 200 mg/individual of the euphausiid Meganyctiphanes and using a TS of !75 dB. Brierley and Watkins (1996) found !38.77 dB kg\ for 25—55 mm length Antarctic krill at 120 kHz. The value of the biomass of Hemimysis (!42 dB kg\) seems to be weak compared with the results above, but in an actual study we measured a Meganyctiphanes mean weight of 400 mg for the same lengths, giving a biomass of !41 dB kg\ at 120 kHz and for a TS"!75 dB. It is therefore not recommended that a single TS value be used to calculate the biomass of a population with a wide size distribution and hence to establish a linear relationship between Sv and the biomass of a zooplankton population that is not uniform in size. Theoretical curves for backscattering as a function of individual size were calculated for Hemimysis using the Machlup diffusion model, at 120 kHz (Fig. 5). Two minima may be observed: the first one applies to the smaller individuals at the beginning of the Rayleigh zone (Rayleigh, 1896) and the second one at the end of the first resonance in the case of larger individuals. So, for a population, the measured Sv is essentially represented by the size class that is equal to the wavelength, whose TS is at the top of the curve. The energetic contribution of other classes, smaller and larger than the preponderant class, will be negligible, because of their lower TS. Estimates of biomass using the TS from the average size of all Hemimysis are therefore incorrect, because the average TS of the population is not that which is calculated from the average size of the population.
330
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
Fig. 5. Theoretical curves of volume scattering (Sv) at 120 kHz, using the spherical shell diffusion model, as a function of size for different numbers of particles, ranging from 1 to 100, 000. The bold line represents the volume scattering of Hemimysis speluncola, calculated from the theoretical TS of each size class in the real population.
The theoretical total backscattering of a wide size-range plankton population is Sv"10 log
i"1 2 N
N p /4n
where N is the number of individuals of size class i and p is the backscattering cross-section where TS"10 log (p /4n). However, if the size of the individuals in the population ranges widely between one-quarter and one wavelength, the TS of the largest animals will dominate the signal; the larvae and juveniles of Hemimysis, for example, will contribute weakly to the backscattering. Theoretical curves (Fig. 5) of volume scattering at 120 kHz as a function of individual size have been calculated for Hemimysis using the spherical shell diffusion theoretical model (Machlup, 1952). This shows that 1000 individuals of 1.4 mm give the same signal as a single individual at 6 mm if the threshold of the echo-sounder is !100 dB, and that only one organism greater than 5 mm will be detected. However, the volume backscattering of Hemimysis evaluated from the theoretical TS of each size class of the real population (Fig. 5, bold line) shows that individuals smaller than 3 mm could reflect enough energy at 120 kHz to be detectable. In practice, the measured Sv (Fig. 3) includes the signal of the population of juveniles
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
331
whose size is between 3 and 5 mm, but not the larvae whose size is smaller than 3 mm. In other words, small plankton, which may be big enough to be seen on their own, would not be detected if some individuals, close in size to the wavelength, were present. Though 120 kHz is a good frequency for detecting Hemimysis adults, it does not seem to be a good frequency for detecting Siriella. Indeed, the largest individuals are longer than the wavelength and are near the first resonance where TS changes rapidly. At this point, longer individuals can have a weaker TS than smaller ones. Conversely, 38 kHz is a good frequency to detect this species, as its response lies in the Rayleigh zone.
Acknowledgements This research was supported by the French National Centre of Scientific Research (CNRS). We thank Prof. Jack Matthews for critically reading the manuscript and for his valuable help in the preparation of the English manuscript.
References Anderson, V.C., 1950. Sound scattering from a fluid sphere. Journal of the Acoustical Society of America 22, 426—443. Artemov, A.T., 1983. Determination of acoustic backscatter cross section of small pelagic organisms in aggregation. Oceanology. URSS 23 (2), 52—61. Arzelies, P., 1979. Propagation des ondes dans un milieu peuple´ de diffuseurs isotropes. Revue du CETHEDEC, 16° anne´e, 3° trim. N°60, 3—8. Beamish, P., 1971. Quantitative measurement of acoustic scattering from zooplanktonic organisms. Deep-Sea Research 19, 811—822. Bourdillon, A., Castelbon, C., 1983. La re´partition spatio-temporelle des Mysidace´s. Socie´te´ Franiaise pour l’Etude du Comportement Animal. bulletin international 5, 105—117. Bourdillon, A., Harmelin, J.G., Passelaigue, F., Vacelet, J., 1986. Le peuplement des grottes sous-marines obscures. Bulletin de la Socie´te´ de Biospe´le´ologie 8, 4—7. Brierley, A.S., Watkins, J.L., 1996. Acoustic targets at South Georgia and the South Orkney Islands during a season of krill scarcity. Marine Ecology Progress Series 138, 51—61. Caceci, M.S., Cacheris, W.P., 1984. Fitting curves to data. The simplex algorithm is the answer. BYTE, May 84, 340—362. Chu, D., Foote, K.G., Stanton, T.K., 1993. Further analysis of target strength measurements of Antarctic krill at 38 and 120 kHz: Comparison with deformed cylinder model and inference of orientation distribution. Journal of the Acoustical Society of America 93(5), 2985—2988. Cushing D.H., Humphrey, G.F., Banse, K., Laevastu, T., 1958. Report of the committee on terms and equivalents. International Council for the Exploration of the Sea 144, 15—16. Flagg, C.N., Smith, S.L., 1989. On the use of the acoustic Doppler current profiler to measure zooplankton abundance. Deep-Sea Research 36(3), 455—474. Foote, K.G., Everson, I., Watkins, J.L., Bone, D.G., 1990. Target strengths of Antarctic krill (Euphausia superba) at 38 and 120 kHz. Journal of the Acoustical Society of America 87(1), 16—24. Gerard, O., 1991. Propagation acoustique dans un milieu diphasique: Eau-bulle d’air. Facteur (de re´flexion et de transmission d’un rideau de bulles. The`se de l’Universite´ Aix-Marseille II, 175pp.
332
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
Greene, C.H., Stanton, T.K., Wiebe, P.H., McClatchie, S., 1991. Acoustic estimates of Antarctic krill. Nature 349, 110. Greenlaw, C.F., 1977. Backscattering spectra of preserved zooplankton. Journal of the Acoustical Society of America 62, 44—52. Greenlaw, C.F., Johnson, R.K., 1983. Multiple frequency acoustical estimation. Biological Oceanography 2, 227—252. Guerin-Ancey, O., David, P.M., 1993. Use of a multibeam-multifrequency sounder to study the distribution of small zooplankton. Deep-Sea Research-I 40(1), 119—128. Holliday, D.V., Pieper, R.E., 1980. Volume scattering strength and zooplankton distribution at acoustic frequencies between 0.5—3.0 Mhz. Journal of the Acoustical Society of America 67, 135—146. Holliday, D.V., Pieper, R.E., Kleppel, G.S., 1989. Determination of plankton size distribution from multifrequency acoustic technology. International Council for the Exploration of the Sea 46, 52—61. Kogeler, J.W., Falk-Petersen, S., Kristensen, A., Pettersen, F., Dalen, J., 1987. Density- and sound speed contrasts in sub-Arctic zooplankton. Polar Biology 7, 231—235. Kristensen, A., Dalen, J., 1986. Acoustic estimation of size distribution and abundance of zooplankton. Journal of the Acoustical Society of America 80(2), 601—611. Laborel, J., Vacelet, J., 1958. Etude des peuplements d’une grotte sous-marine du golfe de Marseille. Bulletin de l’Institut Oce´anographique de Monaco, 1120, 1—20. Laborel, J., Vacelet, J., 1959. Les grottes sous-marines obscures en Me´diterrane´e. Comptes-Rendus de l’Acade´mie des Sciences Paris, Serie D 248, 2619—2612. Ledoyer, M., 1989. Les Mysidace´s (Crustacea) des grottes sous-marines obscures de Me´diterrane´e nordoccidentale et du proche Atlantique (Portugal et Made`re). Marine Nature 2(1), 39—62. Macaulay, M.C., Wishner, K.F., Daly, K.L., 1995. Acoustic scattering from zooplankton and micronekton in relation to a whale feeding site near Georges Bank and Cape Cod. Continental Shelf Research 15 (4—5), 509—537. Machlup, S., 1952. A theoretical model for sound scattering by marine crustaceans. Journal of the Acoustical Society of America 24(3), 290—293. Macquart-Moulin, C., Passelaigue, F., 1982. Mouvements nycthe´me´raux d’Hemimysis speluncola Ledoyer, espe`ce cavernicole, et de Leptomysis lingvura G.O. Sars, espe`ce non cavernicole (Crustacea, Mysidacea). Tethys 10(3), 221—228. Macquart-Moulin, C. Patriti, G., 1966. Remarque sur la biologie d’Hemimysis speluncola Ledoyer, Mysidace´ sciaphile des grottes sous-marines obscures de la re´gion de Marseille. Recueil des Travaux de la Station Marine d’Endoume 40(56), 253—258. Mitson, R.B., Wood, R.J., 1961. An automatic method of counting fish echoes. International Council for the Exploration of the Sea 26(3), 281—291. Passelaigue, F., 1989. Determinisme des migrations du Mysidace´ marin cavernicole Hemimysis speluncola Ledoyer. Oceanis 15(2), 131—132. Passelaigue, F., 1991. Les migrations journalie`res d’un Mysidace´ marin cavernicole Hemimysis speluncola Comparaison avec les migrations verticales du plancton. The`se d’Etat, Universite´ d’Aix-Marseille II, 209 pp. Passelaigue, F., Bourdillon, A., 1986. Distribution and Circadian Migrations of the Cavernicolous Mysid Hemimysis speluncola Ledoyer. In: Brill, E.J. (Ed.), Bermuda Marine Cave Symposium Stygologia. Vol. 2 (1/2), Leiden, 113—118. Pieper, R.E., Holliday, D.V., Kleppel, G.S., 1990. Quantitative zooplankton distributions from multifrequency acoustics. Journal of Plankton Research 22, 433—441. Rayleigh (Lord Strutt), J.W., 1896. The Theory of Sound, MacMillan, New York; Dover, New York Publ., 1945, 2, 149—154. Richter, K.E., 1985. Acoustic scattering at 1.2 Mhz from individual zooplankters and copepod populations. Deep-Sea Research 32(2), 149—161. Samovol’kin V.G., 1974. Acoustic backscattering cross section of small fish, Crustaceans and Medusae as function of their foreshortening. Oceanoloy URSS 14 (5), 660—665. Stanton, T.K., 1988. Sound scattering by cylinders of finite lengths. I. Fluid cylinders. Journal of the Acoustical Society of America 83(1) 55—63.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
333
Van Cuyck, J.P., Sessarego, J.P., David, P.M., Guerin-Ancey, O., 1992. Study of acoustical reflexion coefficient of a monospecific planktonic layer. In: Weydert, M. (Ed.), 1rst European Conference on Underwater Acoustic. Luxembourg, September 14—17. Wiebe, P.H., 1972. A field investigation of the relationship between length of tow, size of net and sampling error. International Council for the Exploration of the Sea 34, 268—275. Wiebe, P.H., Greene, C.H., Stanton, T.K., Burczynski, J., 1990. Sound scattering by live zooplankton and micronekton: Empirical studies with a dual-beam acoustical system. Journal of the Acoustical Society of America 85(1), 2346—2360.
Acoustic discrimination of two zooplankton species (mysid) at 38 and 120 kHz P.M. David*, O. Guerin-Ancey, J.P. Van Cuyck Centre d+Oce&anologie de Marseille, Univ. d+Aix-Marseille 2, UMR 6540 CNRS/Dimar, Campus de Luminy, Case 901, 13288 Marseille Cedex 9, France Received 20 March 1997; received in revised form 17 November 1997; accepted 9 March 1998
Abstract Using bifrequency sonar (38 kHz, 120 kHz) directed towards the open sea from the inside of a submarine cave, two species of Mysidacea (Crustacea), similar in shape but not in size, and with different patterns of behaviour, were observed simultaneously and discriminated, and their biomass was estimated during their migration. The first species, Hemimysis speluncola ((1 cm length), lives in the submarine cave, forming a distinct community that migrates horizontally. The second species, Siriella jaltensis ('1 cm length), lives in the open sea and migrates vertically. These species are both detected clearly at 120 kHz, but only the larger one, Siriella jaltensis, is detected at 38 kHz. This distinction allows one to determine the size limits of planktonic objects detected at these frequencies, i.e. 3 mm at 120 kHz and 10 mm at 38 kHz, corresponding to one quarter of the wavelength. The target strength (TS) of each species was calculated from the field data and compared to results calculated from three models. As the volume of the cave occupied by the Hemimysis population is about 300 m, and the density of the swarm is 36,000 individuals/m, the number of individuals in the cave is estimated to be around 10 million (or 24 kg). The density of the open-water population of Siriella is estimated to be 13 individuals/m. 1999 Elsevier Science Ltd. All rights reserved.
1. Introduction Underwater acoustics is used to calculate the biomass and determine the distribution of plankton and fish (Beamish, 1971; Mitson and Wood, 1961). The calculation requires knowledge of the target strength (TS) of the organisms (Beamish, 1971). This varies according to the type of organism, as it depends on shape, size, and contrasts of both density and speed of sound (Samovol’kin, 1974; Kristensen and Dalen, 1986).
* Corresponding author. Fax: 0033 49 18 29 194; e-mail: [email protected] 0967-0637/99/$—see front matter 1999 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 3 7 ( 9 8 ) 0 0 0 6 4 - 8
320
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
Experiments can provide TS values for single organisms, but problems arise from the use of very high frequencies and limitations on the size of tank. Theoretical TS can be calculated by the use of models (Anderson, 1950; Machlup, 1952; Stanton, 1988) whether or not experiments to find TS for individual organisms are carried out. Methods and models have therefore been developed in order to determine zooplankton distribution and biomass acoustically, using single or multiple frequencies (Holliday et al., 1989; Greenlaw and Johnson, 1983; Pieper et al., 1990; Guerin-Ancey and David, 1993). All acoustic techniques require adequate validation by net sampling. Although the acoustic data can then be compared with data from zooplankton samples, uncertainties still arise due to the mode of sampling, the selectivity of the net, net avoidance, sampling variability, different time scales (Wiebe, 1972) and because a natural plankton community is generally a mixture of organisms (Artemov, 1983). Doubt therefore remains as to the actual population of the insonified water column; it is impossible to know the minimum size of the plankton that is detected, and whether the echoes really are due to the species found in the samples. It is therefore a great advantage to undertake measurements in populations where there are a few easily identified species, so reducing problems of validation. The submarine caves near Marseilles in southern France provide such an opportunity, where it is possible to study the acoustic response of a natural population of small zooplankters in detail. In order to obtain acoustic data attributable to a known population, we carried out a series of field experiments, in June 1990, inside a submarine cave containing a monospecific mysid population and outside, where there is a population of another mysid, and a series of laboratory experiments with specimens from these two populations. The aims were to determine the backscattering at two frequencies (38 and 120 kHz), the physical-acoustic parameters of the two species, their acoustic discrimination, and the limits of detection of the echo-sounder in terms of size class. 1.1. The natural populations The submarine caves in the neighbourhood of Marseilles were formed by underground rivers and became submerged 100,000 years ago. They open to the sea at about 20 m depth, are narrow and run horizontally into the land, to a distance of more than 200 m. The cave on Jarre Island, southeast of Marseilles, was chosen because of its depth (15 m) and easy accessibility by scuba diving, and because it has been well studied (Laborel and Vacelet 1958, 1959; Ledoyer 1989; Bourdillon and Castelbon, 1983; Bourdillon et al., 1986; Macquart-Moulin and Patriti, 1966; Macquart-Moulin and Passelaigue, 1982). The cave is inhabited by a largely monospecific community of the mysid crustacean, Hemimysis speluncola. During the day the animals live in the dark parts of the cave (70 m inside, at 10\ lux) in crevices in the walls and form dense swarms that are easy to capture by pump or net. When light decreases in the evening, the swarms gradually move out into the cave itself and leave the cave in the middle of the night. Before sunrise, the animals return to the dark parts of the cave. Because this behaviour is well known and involves a single species (Passelaigue 1989, 1991), echoes obtained within the cave can be attributed to the Hemimysis speluncola swarm with certainty.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
321
Another mysid, Siriella jaltensis, which is a little larger in size ('1 cm), lives outside the cave. During the day it occurs under stones on the sea bed. In the middle of the night it migrates vertically to the sea surface. During this migration animals pass the cave entrance and can be observed from the cave.
2. Material and methods A Biosonics sonar system with frequencies of 38 and 120 kHz was used for the field study. The transducers were fixed inside the cave at a distance of 7.5 m from the cave entrance facing outwards (Fig. 1). In this way the echo-sounder beam could ‘‘observe’’ movements near the axis of the beam inside and outside the cave. The transducers were connected by an electrical cable to the echo-sounder itself on board the N.O ANTEDON, moored nearby. Acoustic data were obtained on echograms and on a DAT casio magnetic recorder. These were then analysed in order to discriminate between the two species, to observe their migrating behaviour, to measure their respective volume scattering (Sv), to calculate the in situ target strength (TS) of individuals, and to estimate the biomass inside the cave. Sampling was carried out by divers using a small net inside the cave to catch specimens from the dense swarms in the crevices, and with a plankton net slowly hauled vertically outside the cave. Living organisms used in the laboratory measurements were carefully kept immersed in sea-water prior to the acoustic studies.
Fig. 1. Schematic representation of the acoustic experiment in the cave.
322
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
After the in-vitro experiments, the animals were fixed in formalin for counting and measuring. The allometric measurements of the bodies of 100 individuals of each species (length, radius) were used to calculate the additional parameters such as spherical radius of the equivalent volume and equivalent cylinder, incorporated in the theoretical models. The simple scattering hypothesis assumes that the total acoustic scattering energy is the sum of the components of each target excited by the ultrasonic wave (Gerard, 1991). Multiple scattering assumes that the global energy is the sum of these components, plus the multiple reflection of the wave from the particles (Arzelies, 1979). The choice of the simple or multiple scattering fields can be made empirically by comparing the wavelength j to the mean distance d between organisms. If d/j;1, the simple scattering hypothesis may be assumed. Passelaigue (1991) has estimated that the Hemimysis swarm contains 36,000 individuals/m, homogeneously distributed. The mean living space for each organism is therefore 28 cm, equivalent to a mean distance between two individuals of 3 cm. This is greater than the wavelength at 120 kHz, which is 1.25 cm, so one can assume the simple scattering hypothesis in the case of Hemimysis. Outside the cave, the living space for Siriella is less restricted (Macquart-Moulin and Passelaigue, 1982), so one may assume simple scattering to be true in this case too. The volume backscattering (Sv) is therefore calculated as the sum of the individual scattering, expressed as Sv"TS#10 log N .
(1)
where N is the number of individuals insonified by the ultrasonic beam. Schematically, the target strength can be calculated as TS"10 log (p/4n) and p/na"[4((1!gh)/(3gh)#(1!g)/(1#2g))] [2(ka)/(2#3(ka))] , where a is the radius of the equivalent spherical volume of the animal, g is the ratio of the density of the sphere to the density of the surrounding medium (i.e. density contrast), h is the ratio of the speed of sound inside the sphere to that in the surrounding medium (i.e. sound-speed contrast), and k is the wave number obtained from the expression k"2nf /c, where f is the frequency and c the speed of sound in the medium. Since the body size of Hemimysis is too small for its TS to be measured directly in the laboratory, the density contrast g was measured using calibrated baths of glycerine, and the sound-speed contrast h was measured using a velocimeter, according to Greenlaw (1977). Since the body size of Siriella is large enough for its TS to be measured directly in the laboratory, four preserved individuals of similar sizes (14 to 16 mm) were used to determine the TS between 300 kHz and 1.2 MHz in a tank. Using the simplex inversion method (Caceci and Cacheris, 1984) we obtained g and h values for Siriella.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
323
Then, these values were introduced in theoretical scattering models involving simple shaped targets, namely fluid sphere, spherical shell, and fluid cylinder (Anderson, 1950; Machlup, 1952; Stanton, 1988; Van Cuyck et al., 1992) to estimate the TS at 38 and 120 kHz for both species (Tables 1—3). Table 1 Target strength (TS) at 38 and 120 kHz of 4 Hemimysis speluncola size classes, calculated using fluid sphere, spherical shell and fluid cylinder models. The experimentally measured density and sound speed contrasts are g"1.067 and h"1.01 Fluid sphere
Spherical shell
Fluid cylinder
Classes Hemimysis
TS 38
TS 120
TS 38
TS 120
TS 38
TS 120
1: 2: 3: 4:
!152 !137 !123 !120
!132 !117 !104 !101
!146 !130 !117 !113
!126 !110 !98 !95
!144 !130 !116 !117
!124 !111 !97 !98
Larvae Juvenile Male Female
Table 2 Size classes of the Hemimysis speluncula population in the cave. N is the number of individuals in each size class calculated from the percentages of the total population. TS was calculated using the spherical shell model. Scattering volume (Sv) was calculated using N and TS of the mean population
Classes Hemimysis
Mean size (mm)
Population (%)
N Number m!3
TS Spherical Shell
Sv (dB)
1: Larvae 2: Juvenile 3: Male 4: Female Total
1.5 3.5 5.4 6.4 4.8
5 40 40 15 100
1 800 14,400 14,400 5 400 36,000
!126 !110 !98 !95 !98.6
!93 !68 !56 !58 !53
Table 3 Target strength (TS) at 38 and 120 kHz of four specimens of Siriella jaltensis, calculated using fluid sphere, spherical shell and fluid cylinder models, from TS experimentally measured between 300 kHz and 1.2 MHz. The density and sound-speed contrasts extracted with the simplex method are g"1.085 and h"1.013 Fluid sphere
Spherical shell
Fluid cylinder
Classes Siriella
TS 38
TS 120
TS 38
TS 120
TS 38
TS 120
14.3 mm 16 mm 15.5 mm 16 mm mean
!96 !93 !94 !95 !95
!80 !78 !81 !81 !80
!107 !87 !94 !89 !94
!76 !83 !77 !79 !79
!116 !115 !116 !118 !116
!97 !96 !101 !105 !100
324
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
3. Results The hydrographic measurements show that there is no density change along the cave at the mouth that might affect animals migrating horizontally or the passage of sound. There is also no fresh water coming from the cave. Light is the only factor showing a gradient that could determine and orientate migrations (Bourdillon and Castelbon, 1983; Macquart-Moulin and Passelaigue, 1982), although it may be noted that a chlorophyll maximum has been observed outside, near the cave entrance. The population of Hemimysis (Fig. 2) sampled inside the cave, was composed of larvae (class 1, mean length 1.5 mm), juveniles (class 2, mean length 3 mm), males (class 3, mean length 5.4 mm) and females (class 4, mean length 6.4 mm). The population of Siriella (Fig. 2) found outside the cave was composed of juveniles (class 1, mean length 13 mm), young adults (class 2, mean length 18 mm) and females (class 3, mean length 21 mm). The acoustic survey of the cave area shows three periods in the movement of plankton. Moments from each of these periods are illustrated in Figs. 3 and 4: (1) Before sunset, which occurred at 21.20 h, no echo was detected at 120 kHz (Fig. 3) or 38 kHz (Fig. 4) and the cave seemed to be empty, as it appeared to be outside the cave entrance. (2) Some two and a half hours after the sun had gone down, echoes were received from close to the receiver at 120 kHz; these were attributed to Hemimysis. The signal spread gradually throughout the cave in front of the receiver as the Hemimysis swarm appeared to move towards the cave mouth. The swarm filled the cave (Fig. 3) but stayed inside, at least 2—3 m from the mouth, until
Fig. 2. Size distributions of Hemimysis speluncola living inside the cave and Siriella jaltensis living outside.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
325
Fig. 3. Acoustic backscattering at 120 kHz, showing the population distribution at 21.20, 01.00 and 02.30 h, inside (0—8 m) and outside (8—16 m) the cave. Sv is the average of 10 successive values.
the moon disappeared. Virtually no echo was detected at 38 kHz before this time (Fig. 4). (3) An hour later Hemimysis was still detected at 120 kHz throughout the cave (Fig. 3), and Siriella was detected outside at both 38 and 120 kHz (Figs. 3 and 4). The echograms show that small zooplankters like Hemimysis can be detected at 120 kHz but not at 38 kHz, whereas the larger Siriella can be detected at both frequencies.
326
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
Fig. 4. Acoustic backscattering at 38 kHz, showing the population distribution at 21.20, 01.00 and 02.30 h, inside (0—8 m) and outside (8—16 m) the cave. Sv is the average of 10 successive values.
In the cave, scattering levels varied in space and time. For example, at 120 kHz at 01.00 h (Fig. 3), the Sv values of the Hemimysis swarm ranged between !53 dB and !75 dB. This variation could be due to a change in the number of organisms, but as Passelaigue and Bourdillon (1986) observed that they are numerically homogeneously distributed, this is unlikely; it could instead be due to changes in orientation or stage composition.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
327
Knowing the density of Hemimysis and the Sv measured in the cave, we estimated the TS of Hemimysis using Eq. (1). Since Passelaigue (1991) estimated the mean density of the swarm at 36,000 individuals m\ in June, from 1986 to 1989, and never indicated any change in this estimation, we assume that it would be the same density during this experiment. Given this number and considering that the population consists of only one size class (mean 4.8 mm), and that the maximum Sv was !53 dB, measured at 01.00 h, the mean in situ target strength of Hemimysis at 120 kHz is calculated to be !98.6 dB. This result is close to the value (!98 dB) that van Cuyck et al. (1992) obtained with the spherical shell model (Table 1) for the males. However, as shown in Fig. 2, the population of Hemimysis contains different quantities of four size classes (larvae, juveniles, males and females). In this case, the total signal is the sum of the scattering of each class. This was calculated for each class (Table 2) and compared with the total backscattering. The sum of the adult signals (classes 3 and 4) is !54 dB, while the sum for classes 2—3—4 is !53.84 dB and for all classes is also !53.84 dB. This indicates that the juveniles contribute little, although they are numerous, to the total backscattering signal, and the larvae do not contribute at all. The lower limit for detection therefore seems to be around 3 mm, corresponding to one-quarter of the wavelength at 120 kHz. During migration the density of the population varied, resulting in changes to the backscattering signal. During the day the organisms were concentrated in crevices in the cave. At 01.00 h the density of Hemimysis at 3 m inside the cave had reached a maximum, and the observed backscattering (Sv) was !53 dB. By 02.30 h the swarm had spread throughout the cave and begun to go outside, and the backscattering signal had fallen to !55 dB. Since the backscattering signal represents only the adults, i.e. 55% of the total population, we estimate the density of organisms in the swarm, using the spherical shell TS of classes 3 and 4 (Table 2), to have been 46,000 individuals/m at 01.00 h and 28,000 individuals/m at 02.30 h. The mean value, 37,000 individuals/m, is very close to Passelaigue’s data. Given an average density of 37,000 Hemimysis/m, with a total weight of 86 g, and a TS of !98.6 dB, we calculated the volume backscattering for 1 kg of organic matter representing 418,000 Hemimysis, to be !42 dB/m. As the total Hemimysis population in the cave is estimated by this author at 10 million individuals, we estimate that it contains about 24 kg of organic matter or 1.44 kg of carbon (see Cushing et al., 1958). Outside the cave, the organisms were also observed at 120 kHz (Fig. 3). At 01.00 h the population was still in the cave. At 02.30 h there was a response from inside and outside the cave, which appeared to come from Hemimysis in the cave and from Siriella outside on its vertical migration. The maximum backscattering, measured outside, near the mouth of the cave, was !68.69 dB. The TS values calculated at 120 kHz for preserved specimen of Siriella are shown in the Table 3 from the three models. In calculating the density of Siriella in front of the cave, we used a TS value of !79 dB in order to be consistent with the Hemimysis estimates using the spherical shell model. Since the 120 kHz frequency can detect Hemimysis at a length of 2—4 mm, this frequency will detect the total adult and juvenile Siriella population whose shortest length is 11.5 mm.
328
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
From Eq. (1) and the maximum recorded backscattering (!68.69 dB), we calculated the population density of Siriella to be 13 individuals m\. This is three orders of magnitude less than Hemimysis density, but is in accord with the plankton samples taken in the evening and at night, which gave the following results between the surface and 15 m depth: Hour Individuals m\
21.20 0
01.00 0.25
02.30 4
The 38 kHz echograms (Fig. 4) show that none of the Hemimysis, not even the largest organisms (8 mm), were detected. Signals came only from outside the cave, from the Siriella population with a minimum length of 11.5 mm. Outside the cave, the maximum backscattering (Fig. 4) observed at 38 kHz was !82 dB. The TS of Siriella (Table 3), calculated using inverse methods, provide an estimate of the population density. Using the TS at 38 kHz, obtained with the spherical shell model in order to be consistent with the Hemimysis estimate and Eq. (1), we calculated a density of 16 animals m\. This is very close to the density calculated from the 120 kHz data and indicates that even the smallest individuals could be detected at 38 kHz. We therefore conclude that the minimum size of mysids that can be detected at 38 kHz is between 8 and 11.5 mm, i.e. approximatively one quarter of the wavelength. The TS values calculated at 120 and 38 kHz from the spherical shell model provide an estimate of the number of Hemimysis and Siriella. This model could be tried for other crustaceans. 4. Discussion The TS of mysids depends on the acoustic characteristics of the target, such as size, shape, speed of sound and density contrasts, and on the frequency of detection. The values of g and h measured for living crustaceans Hemimysis, according to the Greenlaw (1977) method, give g"1.067 and h"1.01, for a size range of 4 to 8 mm. The range of density contrast (g) reported in the literature for planktonic marine crustaceans, essentially euphausiids, varies from 1.016 to 1.12, while the values of sound speed contrast (h) range from 1.007 to 1.033 (Greenlaw, 1977; Holliday and Pieper, 1980; Kogeler et al., 1987; Chu et al., 1993). In addition, we observe, as did Kogeler et al. (1987) and Kristensen and Dalen (1986), that the density increases when the body length decreases, which can explain the high contrast values found here. Using the simplex method, the mean values g"1.085 and h"1.013 were calculated for four preserved Siriella. The preservation, but also the death, produces changes in the body composition leading to effects on the physical parameters. Flagg and Smith (1989) considered that the preserved non gelatinous plankter composition is relatively unchanged, but Greenlaw et al. (1977) noticed a 1.9% decrease. Nevertheless, g and h values for the studied crustaceans are very close to those quoted in the literature. Differences are also due to the very diverse experimental conditions, such as temperature, fresh or sea water, species, size, shape, preserved or living organism.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
329
All the TS values given for Hemimysis (Table 1) with the spherical shell and the fluid cylinder models are similar and close to the TS found in the literature for crustaceans of the same size range (Holliday and Pieper, 1980). The fluid sphere model always gives the lower TS. The difference between the TS at 38 and 120 kHz is about 19 dB. At 38 kHz the TS are less than !100 dB (Table 1), so this species is too small to be detected at this frequency. For Siriella, (Table 3) the fluid sphere and the spherical shell models give similar results, and the fluid cylinder gives lower TS (20 dB difference). Between 38 and 120 kHz the difference is 15 dB. From all these results, it appears that the spherical shell model is convenient for both species and gives TS close to the literature values. The range of TS reported in the literature for 30—40 mm length euphausiids varies from !89 to !84 dB at 38 kHz and from !74 to !80 dB at 120 kHz (Foote et al., 1990; Greene et al., 1991; Chu et al., 1993) and for 7 to 31 mm length mysids from !95 to !67 dB at 1.2 MHz and 420 kHz (Richter, 1985; Wiebe et al., 1990). As noted above, the relation between the length of the crustacean and the wavelength is particularly important for TS and biomass determination. The best estimate of TS of a population is obtained when the size of the individuals equals the wavelength. If the individuals of a population are similar in size, the backscattering signal can provide an estimate of biomass such that Sv is a linear function of the number of individuals. The biomass of the Hemimysis swarm calculated using a mean TS of !98.6 dB at 120 kHz is !42 dB kg\, for a mean length of 4.8 mm and a mean weight of 2.39 mg. At the same frequency, Macaulay et al. (1995) found !38 dB kg\ for 25—30 mm length, assuming an average weight of 200 mg/individual of the euphausiid Meganyctiphanes and using a TS of !75 dB. Brierley and Watkins (1996) found !38.77 dB kg\ for 25—55 mm length Antarctic krill at 120 kHz. The value of the biomass of Hemimysis (!42 dB kg\) seems to be weak compared with the results above, but in an actual study we measured a Meganyctiphanes mean weight of 400 mg for the same lengths, giving a biomass of !41 dB kg\ at 120 kHz and for a TS"!75 dB. It is therefore not recommended that a single TS value be used to calculate the biomass of a population with a wide size distribution and hence to establish a linear relationship between Sv and the biomass of a zooplankton population that is not uniform in size. Theoretical curves for backscattering as a function of individual size were calculated for Hemimysis using the Machlup diffusion model, at 120 kHz (Fig. 5). Two minima may be observed: the first one applies to the smaller individuals at the beginning of the Rayleigh zone (Rayleigh, 1896) and the second one at the end of the first resonance in the case of larger individuals. So, for a population, the measured Sv is essentially represented by the size class that is equal to the wavelength, whose TS is at the top of the curve. The energetic contribution of other classes, smaller and larger than the preponderant class, will be negligible, because of their lower TS. Estimates of biomass using the TS from the average size of all Hemimysis are therefore incorrect, because the average TS of the population is not that which is calculated from the average size of the population.
330
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
Fig. 5. Theoretical curves of volume scattering (Sv) at 120 kHz, using the spherical shell diffusion model, as a function of size for different numbers of particles, ranging from 1 to 100, 000. The bold line represents the volume scattering of Hemimysis speluncola, calculated from the theoretical TS of each size class in the real population.
The theoretical total backscattering of a wide size-range plankton population is Sv"10 log
i"1 2 N
N p /4n
where N is the number of individuals of size class i and p is the backscattering cross-section where TS"10 log (p /4n). However, if the size of the individuals in the population ranges widely between one-quarter and one wavelength, the TS of the largest animals will dominate the signal; the larvae and juveniles of Hemimysis, for example, will contribute weakly to the backscattering. Theoretical curves (Fig. 5) of volume scattering at 120 kHz as a function of individual size have been calculated for Hemimysis using the spherical shell diffusion theoretical model (Machlup, 1952). This shows that 1000 individuals of 1.4 mm give the same signal as a single individual at 6 mm if the threshold of the echo-sounder is !100 dB, and that only one organism greater than 5 mm will be detected. However, the volume backscattering of Hemimysis evaluated from the theoretical TS of each size class of the real population (Fig. 5, bold line) shows that individuals smaller than 3 mm could reflect enough energy at 120 kHz to be detectable. In practice, the measured Sv (Fig. 3) includes the signal of the population of juveniles
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
331
whose size is between 3 and 5 mm, but not the larvae whose size is smaller than 3 mm. In other words, small plankton, which may be big enough to be seen on their own, would not be detected if some individuals, close in size to the wavelength, were present. Though 120 kHz is a good frequency for detecting Hemimysis adults, it does not seem to be a good frequency for detecting Siriella. Indeed, the largest individuals are longer than the wavelength and are near the first resonance where TS changes rapidly. At this point, longer individuals can have a weaker TS than smaller ones. Conversely, 38 kHz is a good frequency to detect this species, as its response lies in the Rayleigh zone.
Acknowledgements This research was supported by the French National Centre of Scientific Research (CNRS). We thank Prof. Jack Matthews for critically reading the manuscript and for his valuable help in the preparation of the English manuscript.
References Anderson, V.C., 1950. Sound scattering from a fluid sphere. Journal of the Acoustical Society of America 22, 426—443. Artemov, A.T., 1983. Determination of acoustic backscatter cross section of small pelagic organisms in aggregation. Oceanology. URSS 23 (2), 52—61. Arzelies, P., 1979. Propagation des ondes dans un milieu peuple´ de diffuseurs isotropes. Revue du CETHEDEC, 16° anne´e, 3° trim. N°60, 3—8. Beamish, P., 1971. Quantitative measurement of acoustic scattering from zooplanktonic organisms. Deep-Sea Research 19, 811—822. Bourdillon, A., Castelbon, C., 1983. La re´partition spatio-temporelle des Mysidace´s. Socie´te´ Franiaise pour l’Etude du Comportement Animal. bulletin international 5, 105—117. Bourdillon, A., Harmelin, J.G., Passelaigue, F., Vacelet, J., 1986. Le peuplement des grottes sous-marines obscures. Bulletin de la Socie´te´ de Biospe´le´ologie 8, 4—7. Brierley, A.S., Watkins, J.L., 1996. Acoustic targets at South Georgia and the South Orkney Islands during a season of krill scarcity. Marine Ecology Progress Series 138, 51—61. Caceci, M.S., Cacheris, W.P., 1984. Fitting curves to data. The simplex algorithm is the answer. BYTE, May 84, 340—362. Chu, D., Foote, K.G., Stanton, T.K., 1993. Further analysis of target strength measurements of Antarctic krill at 38 and 120 kHz: Comparison with deformed cylinder model and inference of orientation distribution. Journal of the Acoustical Society of America 93(5), 2985—2988. Cushing D.H., Humphrey, G.F., Banse, K., Laevastu, T., 1958. Report of the committee on terms and equivalents. International Council for the Exploration of the Sea 144, 15—16. Flagg, C.N., Smith, S.L., 1989. On the use of the acoustic Doppler current profiler to measure zooplankton abundance. Deep-Sea Research 36(3), 455—474. Foote, K.G., Everson, I., Watkins, J.L., Bone, D.G., 1990. Target strengths of Antarctic krill (Euphausia superba) at 38 and 120 kHz. Journal of the Acoustical Society of America 87(1), 16—24. Gerard, O., 1991. Propagation acoustique dans un milieu diphasique: Eau-bulle d’air. Facteur (de re´flexion et de transmission d’un rideau de bulles. The`se de l’Universite´ Aix-Marseille II, 175pp.
332
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
Greene, C.H., Stanton, T.K., Wiebe, P.H., McClatchie, S., 1991. Acoustic estimates of Antarctic krill. Nature 349, 110. Greenlaw, C.F., 1977. Backscattering spectra of preserved zooplankton. Journal of the Acoustical Society of America 62, 44—52. Greenlaw, C.F., Johnson, R.K., 1983. Multiple frequency acoustical estimation. Biological Oceanography 2, 227—252. Guerin-Ancey, O., David, P.M., 1993. Use of a multibeam-multifrequency sounder to study the distribution of small zooplankton. Deep-Sea Research-I 40(1), 119—128. Holliday, D.V., Pieper, R.E., 1980. Volume scattering strength and zooplankton distribution at acoustic frequencies between 0.5—3.0 Mhz. Journal of the Acoustical Society of America 67, 135—146. Holliday, D.V., Pieper, R.E., Kleppel, G.S., 1989. Determination of plankton size distribution from multifrequency acoustic technology. International Council for the Exploration of the Sea 46, 52—61. Kogeler, J.W., Falk-Petersen, S., Kristensen, A., Pettersen, F., Dalen, J., 1987. Density- and sound speed contrasts in sub-Arctic zooplankton. Polar Biology 7, 231—235. Kristensen, A., Dalen, J., 1986. Acoustic estimation of size distribution and abundance of zooplankton. Journal of the Acoustical Society of America 80(2), 601—611. Laborel, J., Vacelet, J., 1958. Etude des peuplements d’une grotte sous-marine du golfe de Marseille. Bulletin de l’Institut Oce´anographique de Monaco, 1120, 1—20. Laborel, J., Vacelet, J., 1959. Les grottes sous-marines obscures en Me´diterrane´e. Comptes-Rendus de l’Acade´mie des Sciences Paris, Serie D 248, 2619—2612. Ledoyer, M., 1989. Les Mysidace´s (Crustacea) des grottes sous-marines obscures de Me´diterrane´e nordoccidentale et du proche Atlantique (Portugal et Made`re). Marine Nature 2(1), 39—62. Macaulay, M.C., Wishner, K.F., Daly, K.L., 1995. Acoustic scattering from zooplankton and micronekton in relation to a whale feeding site near Georges Bank and Cape Cod. Continental Shelf Research 15 (4—5), 509—537. Machlup, S., 1952. A theoretical model for sound scattering by marine crustaceans. Journal of the Acoustical Society of America 24(3), 290—293. Macquart-Moulin, C., Passelaigue, F., 1982. Mouvements nycthe´me´raux d’Hemimysis speluncola Ledoyer, espe`ce cavernicole, et de Leptomysis lingvura G.O. Sars, espe`ce non cavernicole (Crustacea, Mysidacea). Tethys 10(3), 221—228. Macquart-Moulin, C. Patriti, G., 1966. Remarque sur la biologie d’Hemimysis speluncola Ledoyer, Mysidace´ sciaphile des grottes sous-marines obscures de la re´gion de Marseille. Recueil des Travaux de la Station Marine d’Endoume 40(56), 253—258. Mitson, R.B., Wood, R.J., 1961. An automatic method of counting fish echoes. International Council for the Exploration of the Sea 26(3), 281—291. Passelaigue, F., 1989. Determinisme des migrations du Mysidace´ marin cavernicole Hemimysis speluncola Ledoyer. Oceanis 15(2), 131—132. Passelaigue, F., 1991. Les migrations journalie`res d’un Mysidace´ marin cavernicole Hemimysis speluncola Comparaison avec les migrations verticales du plancton. The`se d’Etat, Universite´ d’Aix-Marseille II, 209 pp. Passelaigue, F., Bourdillon, A., 1986. Distribution and Circadian Migrations of the Cavernicolous Mysid Hemimysis speluncola Ledoyer. In: Brill, E.J. (Ed.), Bermuda Marine Cave Symposium Stygologia. Vol. 2 (1/2), Leiden, 113—118. Pieper, R.E., Holliday, D.V., Kleppel, G.S., 1990. Quantitative zooplankton distributions from multifrequency acoustics. Journal of Plankton Research 22, 433—441. Rayleigh (Lord Strutt), J.W., 1896. The Theory of Sound, MacMillan, New York; Dover, New York Publ., 1945, 2, 149—154. Richter, K.E., 1985. Acoustic scattering at 1.2 Mhz from individual zooplankters and copepod populations. Deep-Sea Research 32(2), 149—161. Samovol’kin V.G., 1974. Acoustic backscattering cross section of small fish, Crustaceans and Medusae as function of their foreshortening. Oceanoloy URSS 14 (5), 660—665. Stanton, T.K., 1988. Sound scattering by cylinders of finite lengths. I. Fluid cylinders. Journal of the Acoustical Society of America 83(1) 55—63.
P.M. David et al. / Deep-Sea Research I 46 (1999) 319—333
333
Van Cuyck, J.P., Sessarego, J.P., David, P.M., Guerin-Ancey, O., 1992. Study of acoustical reflexion coefficient of a monospecific planktonic layer. In: Weydert, M. (Ed.), 1rst European Conference on Underwater Acoustic. Luxembourg, September 14—17. Wiebe, P.H., 1972. A field investigation of the relationship between length of tow, size of net and sampling error. International Council for the Exploration of the Sea 34, 268—275. Wiebe, P.H., Greene, C.H., Stanton, T.K., Burczynski, J., 1990. Sound scattering by live zooplankton and micronekton: Empirical studies with a dual-beam acoustical system. Journal of the Acoustical Society of America 85(1), 2346—2360.