Target strengths of two abundant mesopelagic fish species

Target strengths of two abundant mesopelagic fish species

Ben Scouldinga)

School of Biological Sciences, Zoology Building, University of Aberdeen, Tillydrone Avenue, Aberdeen,AB24 2TZ, Scotland

Dezhang ChuNational Oceanic and Atmospheric Administration/National Marine Fisheries Service/Northwest FisheriesScience Center/Fishery Resource Analysis and Monitoring, 2725 Montlake Boulevard East, Seattle,Washington 98112

Egil OnaInstitute of Marine Research, P.O. Box 1870, 5024 Bergen, Norway

Paul. G. FernandesSchool of Biological Sciences, Zoology Building, University of Aberdeen, Tillydrone Avenue, Aberdeen,AB24 2TZ, Scotland

(Received 6 January 2014; revised 16 December 2014; accepted 21 December 2014)

Mesopelagic fish of the Myctophidae and Sternoptychidae families dominate the biomass of the

oceanic deep scattering layers and, therefore, have important ecological roles within these ecosys-

tems. Interest in the commercial exploitation of these fish is growing, so the development of techni-

ques for estimating their abundance, distribution and, ultimately, sustainable exploitation are

essential. The acoustic backscattering characteristics for two size classes of Maurolicus muelleriand Benthosema glaciale are reported here based on swimbladder morphology derived from digi-

tized soft x-ray images, and empirical (in situ) measurements of target strength (TS) derived from

an acoustic survey in a Norwegian Sea. A backscattering model based on a gas-filled prolate sphe-

roid was used to predict the theoretical TS for both species across a frequency range between 0 and

250 kHz. Sensitivity analyses of the TS model to the modeling parameters indicate that TS is rather

sensitive to the viscosity, swimbladder volume ratio, and tilt, which can result in substantial

changes to the TS. Theoretical TS predictions close to the resonance frequency were in good agree-

ment (62 dB) with mean in situ TS derived from the areas acoustically surveyed that were spatially

and temporally consistent with the trawl information for both species.VC 2015 Acoustical Society of America. [http://dx.doi.org/10.1121/1.4906177]

[APL] Pages: 989–1000

I. INTRODUCTION

Acoustic surveys are effective methods to quantify the

distribution and abundance of many pelagic marine fauna

(Simmonds and MacLennan, 2005). In the case of schooling

fish aggregating in large numbers, where echoes from indi-

vidual fish are not resolvable, the echo-integration technique

is used to estimate fish density (MacLennan, 1990).

Abundance estimates from echo integration do, however,

require that the morphological and acoustic properties of the

particular fish species being studied are known. The acoustic

properties are characterized by the target strength (TS, in

decibels, dB re 1 m2), a logarithmic description of the quan-

tity of acoustic backscattered energy from an individual fish.

TS values for many fish species of commercial importance

have been determined by various methods including:

Empirical measurements of tethered fish (Nakken and Olsen,

1977); fish contained in cages (Edwards and Armstrong,

1981); fish measured in situ (Soule et al., 1995); and esti-

mates from mathematical models of scattering from fish

body components (Love, 1978; Clay and Horne, 1994; Ye,

1997).

There are fewer estimates of TS for species that are not

fished commercially. Such species can be important in their

own right, for example, if the fish happen to be major forage

food for commercially fished species, such as the mycto-

phids (Prosch et al., 1989; O’Driscoll et al., 2009).

However, TS estimates of other species are also required

when estimating the abundance of a particular fish species

when it is mixed in with others, such that the echo integral

needs to be apportioned accordingly (Nakken and

Dommasnes, 1977). Species mixtures are common in scatter-

ing layers, such as the deep scattering layers (DSL, Barham,

1966; Burd et al., 1992; Magn�usson, 1996), which undergo

diurnal vertical migrations (DVM). Many taxonomic groups

are well known for systematically participating in DVM

(Lampert, 1989; Demer and Hewitt, 1995; Gauthier and

Rose, 2002), and echosounders are commonly used to assess

their distribution (e.g., Axenrot et al., 2004; Kaartvedt et al.,2009).

Two abundant species known for DVM and their pres-

ence in the DSL of the northeast Atlantic Ocean are the north-

ern lanternfish (Benthosema glaciale, Myctophidae) and

Mueller’s pearlside (Maurolicus muelleri, Sternoptychidae)

a)Author to whom correspondence should be addressed. Wageningen

IMARES, P.O. Box 68, 1970 AB Ijmuiden, The Netherlands. Electronic

mail: [email protected]

J. Acoust. Soc. Am. 137 (2), February 2015 VC 2015 Acoustical Society of America 9890001-4966/2015/137(2)/989/12/$30.00

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(Gjosater and Kawaguchi, 1980; Godø et al., 2009; Kaartvedt

et al., 2009). B. glaciale and M. muelleri can both be consid-

ered as “bladder fish” as described by Yasuma et al. (2003).

Previous studies have determined TS values for some mem-

bers of the Myctophidae and Sternoptychidae based on scat-

tering models, measurements of swimbladder condition and

morphology, and in situ TS data (Hamano, 1993; Yasuma

et al., 2003; Yasuma et al., 2010). Other studies have esti-

mated ranges of TS based exclusively on in situ TS data

obtained from DVM layers (Torgersen and Kaartvedt, 2001;

Godø et al., 2009; Sawada et al., 2011). The presence and

morphology of a swimbladder has also been shown to vary

greatly between species and to be very diverse within species

depending on the ontogenic stage of the individual (Butler

and Pearcy, 1972; Kleckner and Gibbs, 1972; Yasuma et al.,2003). For examples, some myctophid swimbladders have

been described as being thin-walled structures saturated with

waxy esters, whereas others are gas filled or absent (Butler

and Pearcy, 1972; Yasuma et al., 2003).

To date no studies have described swimbladder mor-

phology nor the specific TS values for individuals of varying

sizes of either M. muelleri or B. glaciale, with the exception

of Hamano (1993), who derived the relationship, TS¼ 17.4

log L -69.9, where L is fish length in cm, for M. muelleri at

the specific—and rarely used—frequency of 88 kHz, from a

theoretical model calculation (Love, 1977). Much of the bio-

mass of mid-water migratory layers in temperate waters

throughout the world oceans is composed of Myctophidae

and Sternoptychidae: Therefore these fish are considered to

have important ecological roles within these ecosystems

(Gjosater and Kawaguchi, 1980). As interest in the commer-

cial exploitation of these fish grows, knowledge of TS is

essential for the estimation of their abundance, distribution

and, ultimately, their sustainable exploitation.

Many components of a fish body contribute to the over-

all TS of fish (Ona, 1990; Horne, 2000). The predominant

feature is the air-filled or partly air-filled swimbladder,

which can contribute up to 95% of the acoustic backscatter

(Foote, 1980). There are numerous examples of swimbladder

morphological studies to estimate swimbladder volume.

Many of these, in common with most studies of TS, have

been geared toward species of commercial importance, such

as the gadoids (Foote, 1980; Hazen and Horne, 2003; Horne,

2003), tuna (Bertrand and Josse, 2000) and clupeids (Ona,

1990). The morphology of swimbladders was traditionally

determined using fixed-depth slicing microtomes (Ona,

1990) or through the dissection of frozen specimens

(Kleckner and Gibbs, 1972; Foote, 1985). More recent stud-

ies, such as the non-invasive technique developed by

Sawada et al. (1999), use specialized “soft x-rays” to visual-

ize the size, shape and angular position of the swimbladder.

This benign method, although costly, allows for rapid proc-

essing of large sample sizes without compromising the integ-

rity of the swimbladder. More advanced methods, such as

nuclear magnetic resonance (NMR) have also been used in

such studies (Pe~na and Foote, 2008).

The purpose of the study described in this paper was to

determine the TS of B. glaciale and M. muelleri based on

swimbladder morphology and multifrequency in situ TS data

collected with echosounders operating at 18, 38, 120, and

200 kHz. Digitized soft x-ray images were used to estimate

swimbladder volumes, which were then used to determine

theoretical values of TS for both species using a scattering

model which approximates the shape of the swimbladder as

an equivalent prolate ellipsoid. Sensitivities of the TS model

to the modeling parameters were investigated, and compari-

sons between the model predictions and in situ TS data were

made.

II. MATERIALS AND METHODS

A. Fish samples

Specimens of two species of mesopelagic fish were

obtained from the Osterfjord in Norway in November/

December of 2011 during a research cruise on the fisheries

research vessel Haakon Mosby. Benthosema glaciale and M.muelleri were captured with a macrozooplankton trawl

(“krill trawl”) during both day and night hours between 20

and 75 m. The trawl had an opening of 6� 6 m with a mesh

size of 3 mm throughout (6 mm stretched) and was towed

through target layers at an average speed of 1.44 ms–1. The

catch was sorted by species, and the species proportion by

number was estimated: The larger infrequent gadoid fish

species were all counted. Individuals were retained to gener-

ate a length-frequency distribution. Smaller subsamples

were collected in shallow scattering layers at a depth of

between 20 and 70 m. Of these, individuals were selected

and immediately frozen for radiograph analysis based on vis-

ual inspection of their external condition.

B. Acoustic data

Acoustic data from the research vessel were collected

continuously with a Simrad EK60 scientific multifrequency

echosounder system with split-beam transducers operating at

18, 38, 120, and 200 kHz. The beam widths were all 7�

except for the 18 kHz transducer, which has a beam width of

11�. The transducers were mounted close together on the

vessel’s extendable keel, which protruded 3 m below the hull

during surveying. Acoustic data consisted of mean volume

backscattering strengths (MVBS, in dB re 1 m–1) at each fre-

quency, collected simultaneously every 0.8 s during the day

(equivalent to 5.1 m distance traveled at a survey speed of

approximately 5 m s–1) increasing to every 0.2 s at night.

Pulse duration was 1 ms by day and 0.256 ms at night (at

night the targets were shallower allowing for a shorter pulse

length and better resolution), at all frequencies, to account

for change in layer depth associated with DVM. All echo

sounders (because both the GPT and the transducer is cali-

brated in this procedure) were calibrated using frequency

specific spheres (Foote et al., 1987). These were the copper

(CU) 64.0 mm diameter sphere for the 18 kHz system, the

CU 60.0 mm for the 38 kHz system, and the tungsten car-

bide, WC 38.1 mm sphere for the 120 and 200 kHz systems.

All frequencies were calibrated at the standard 1024 ls pulse

duration, and the 120 and 200 kHz systems were additionally

calibrated on the 256 ls pulse duration. The calibration dif-

ference between the 1024 and the 256 ls pulse durations for

990 J. Acoust. Soc. Am., Vol. 137, No. 2, February 2015 Scoulding et al.: Target strengths of two mesopelagic fish


https://www.researchgate.net/publication/242202400_Short_communication_Tuna_target-strength_related_to_fish_length_and_swimbladder_volume?el=1_x_8&enrichId=rgreq-52d3359b-d4be-4e2d-8bc7-21858c26f9c7&enrichSource=Y292ZXJQYWdlOzI3MjUxODQ1OTtBUzoyMTg5OTIxNTg0ODI0MzJAMTQyOTIyMzIwNzgxNw==

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https://www.researchgate.net/publication/253664540_Target_strength_of_an_individual_fish_at_any_aspect?el=1_x_8&enrichId=rgreq-52d3359b-d4be-4e2d-8bc7-21858c26f9c7&enrichSource=Y292ZXJQYWdlOzI3MjUxODQ1OTtBUzoyMTg5OTIxNTg0ODI0MzJAMTQyOTIyMzIwNzgxNw==

https://www.researchgate.net/publication/231939530_Physiological_factors_causing_natural_variations_in_acoustic_target_strength_of_fish_Journal_of_Marine_Biological_Association_of_the_United_Kingdom_70_107-127?el=1_x_8&enrichId=rgreq-52d3359b-d4be-4e2d-8bc7-21858c26f9c7&enrichSource=Y292ZXJQYWdlOzI3MjUxODQ1OTtBUzoyMTg5OTIxNTg0ODI0MzJAMTQyOTIyMzIwNzgxNw==

https://www.researchgate.net/publication/31275917_Modelling_the_target_strength_of_Trachurus_symmetricus_murphyi_based_on_high-resolution_swimbladder_morphometry_using_an_MRI_scanner?el=1_x_8&enrichId=rgreq-52d3359b-d4be-4e2d-8bc7-21858c26f9c7&enrichSource=Y292ZXJQYWdlOzI3MjUxODQ1OTtBUzoyMTg5OTIxNTg0ODI0MzJAMTQyOTIyMzIwNzgxNw==

the 38 kHz system was extrapolated from previous calibra-

tion data from R/V G.O.Sars.

In situ TS from the four frequencies were derived from

the echosounder using a single target detection algorithm

(e.g., Soule et al., 1997). Detections were isolated from sec-

tions of the echogram that were spatially and temporally

consistent with the trawl data for both species. Two possible

sources of bias exist that may have affected the mean in situTS values (Ona and Barange, 1999): A poor signal-to-noise

ratio (SNR) on the edge of the beam (which potentially leads

to an underestimation of the mean) and unwanted acceptance

of multiple targets as single targets (generally leading to an

overestimation of the mean).

A comprehensive filtering procedure was performed at

each frequency to produce more reliable TS distributions

based on the original measurements (Fig. 1). To reduce the

bias caused by the poor SNR, the TS distribution was first

examined as a function of the angular distance (a) of each

detection from the center of the acoustic beam, assuming cir-

cular symmetry. Angular distances, a, were then binned into

half-degree rings from the acoustic center, and the areas of

each half-degree ring were calculated based on the average

depth of the appropriate isolated echogram section. The den-

sities of in situ TS detections were then calculated for each

half-degree ring. Assuming the target density to be randomly

and evenly distributed in the beam, the density is expected to

be the same regardless of where in the beam the fish were

detected. Poor SNR at the edge of the beam would result in a

lower density of targets there. A threshold (aT) was then cho-

sen based on the distance at which the detected target density

began to decline. aT was typically around 3� from the on

axis (alongship or athwartship). Targets at a> aT were

removed to produce a SNR-filtered dataset.

The SNR-filtered datasets were then subject to further

density corrections to account for potential multiple targets.

First, a sub sampling process of the echogram sections was

carried out to determine if there were areas inside the echo-

gram section with different densities of single targets. Data

were split along the trawl region into 2 min subsamples,

resulting in 15 subsamples for large and small M. muelleri(based on 30-min trawls) and 5 subsamples for B. glaciale(based on a 10-min trawl). For each subsample, the mean

number of fish in the pulse volume (N) was calculated

according to the procedure described by Ona and Barange

(1999), and the corresponding probability of detecting multi-

ple targets (p) was derived. In situ TS from subsamples with

a probability of detecting multiple targets less than a thresh-

old (0.2 in this study) were retained; those with higher prob-

abilities were subject to further analysis. A probability of 0.2

was chosen as the limiting threshold as subsamples with

lower densities across all four frequencies were not observed

at a value less than this. This probability corresponds to a

mean density of N¼ 0.43 (see Table II.4, Ona and Barange

1999).

FIG. 1. Flow chart summarizing the filtering processes used to isolate in situ target strength measurements that were free from spurious values due to a low sig-

nal-to-noise ratio and high densities leading to multiple targets being interpreted as a single target.

J. Acoust. Soc. Am., Vol. 137, No. 2, February 2015 Scoulding et al.: Target strengths of two mesopelagic fish 991


https://www.researchgate.net/publication/228743085_Performance_of_a_new_phase_algorithm_for_discriminating_between_single_and_overlapping_echoes_in_a_split-beam_echosounder?el=1_x_8&enrichId=rgreq-52d3359b-d4be-4e2d-8bc7-21858c26f9c7&enrichSource=Y292ZXJQYWdlOzI3MjUxODQ1OTtBUzoyMTg5OTIxNTg0ODI0MzJAMTQyOTIyMzIwNzgxNw==

Two-sample Kolmogorov-Smirnov (KS) tests (Sidak

et al., 1999) were then run to test for differences between the

frequency distributions of TS derived from subsamples with

low (p� 0.2) and high-density (p> 0.2) volumes; in particu-

lar, the upper ends of the TS distribution were monitored for

possible erroneous acceptance of two or more targets as one.

If the probability that any in situ TS distribution from the

high density subsamples was not significantly different

(from each other according to a matrix of KS tests, and

p� 0.05), then the in situ TS measurements from the sub-

samples were retained. Those subsamples with a signifi-

cantly different distribution (p< 0.05) from the others were

rejected from the dataset.

Finally, a multifrequency analysis was performed on

those in situ TS from all subsamples arising from the KS dis-

tribution tests to further eliminate the possibility of identify-

ing multiple targets as single targets. Targets were retained

only if they were detected by more than one frequency.

Single targets were matched according to ping time and tar-

get range (to within 0.1 m of one another, see Demer et al.,1999).

C. Morphological measurements of swimbladder

Measurements were made of the external morphology of

the fish body, including, length, width, height, and weight in

the lab post-cruise. Frozen specimens were radiographed using

a specialized “soft x-ray” imaging suite (ADORA RSA,

Canon CXDI-1 system Digital Radiography CP1). The detec-

tor plate dimensions were 430 mm� 350 mm, and the pixel

size was 0.16 mm. Radiographs were taken at distance of 1 m

from the source. All fish were radiographed on their dorsal and

lateral aspects in accordance with previous studies (Sawada

et al., 1999; Yasuma et al., 2003). The lateral-aspect images

were exposed at 64 mA for 0.32 s at 40 kV potential (KVP),

and the dorsal-aspect images were exposed at 64 mA for 0.32 s

at 65 KVP. These radiograph parameters were selected on the

basis of extensive preliminary testing. A metallic disk with

known dimensions was placed level to and adjacent to the

swimbladder for scaling purposes. Based on swimbladder con-

dition, identified from analysis of radiograph images, the fish

were classified into three groups: (1) Fish with an inflated

swimbladder, (2) fish with a ruptured swimbladder, and (3)

fish with an absent swimbladder. Swimbladders were consid-

ered ruptured if there were obvious irregularities in the swim-

bladder wall or if gas was observed in the peritoneal

cavity. Measurements were made from digital images of the

three cross-sectional dimensions of the swimbladder: L(length), H (height), and W (width). The swimbladder volume

was then estimated, assuming a prolate spheroid shape,

according to

V ¼ 4

3pab2; (1)

where a ¼ L=2 and b ¼ffiffiffiffiffiffiffiffiffiffiffiffiffiHW=4

pare the semi-major and

semi-minor axes, respectively.

D. Acoustic scattering model

Because swimbladders contribute much more than fish

flesh to backscattered acoustic intensity, only swimbladders

were used in calculating the backscattering strength. The shape

of the swimbladder was assumed to be a prolate spheroid for

simplicity. Due to the small size of the two species and their

swimbladders, a resonance scattering model, where only the

omni-directional breathing mode was considered, was used to

describe the backscattering by these swimbladder-bearing fish,

and can be expressed as (Weston, 1967; Love, 1978; Ye, 1997)

rbs ¼v2 a2

esr

1� fres

f

� �2" #2

þ d2

; (2)

where aesr is the equivalent spherical radius (Strasberg,

1953), fres is the resonance frequency of the swimbladder,

f is the acoustic frequency, d is the damping factor includ-

ing radiation, viscous, and thermal processes, and v is the

coefficient accounting for the amplitude enhancement

due to swimbladder elongation. In modeling the backscat-

tering by swimbladders, the shape is approximated by a

prolate spheroid and the equivalent spherical radius can

be calculated by

aesr ¼ ðab2Þ1=3: (3)

Although the two species are physoclist (Marshall, 1960), a

constant mass assumption is still used as the fish cannot

reabsorb the gas fast enough when being captured rapidly

from depth. As a result, the volumes measured at the surface

were those that obeyed Boyle’s law. The resonance fre-

quency takes into account the elasticity of the tissue

(Andreeva, 1964) and the elongation of the swimbladder

(Strasberg, 1953)

fres ¼Ce

2p aesr

ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi3ca Pþ 4lr

qw

s; (4)

where ca is the ratio of the specific heat for air ðca ¼ 1:4Þ; Pis the ambient pressure at depth, lr is the real part of the

rigidity of fish flesh, and qw is the density of water. The elon-

gation factor Ce was presented by Love (1978) based on the

work of Strasberg (1953) and Weston (1967)

Ce ¼21=2 1� e2ð Þ1=4

e1=3ln

1þ 1� e2ð Þ1=2

1� 1� e2ð Þ1=2

24

35

8<:

9=;�1=2

; (5)

where e is the ratio of the semi-minor to the semi-major axis

of the prolate spheroid (b/a). The damping factor d, can be

expressed in terms of radiation, viscous, and thermal compo-

nents as (Love, 1978)

1

d¼ 1

dradþ 1

dvisþ 1

dth; (6)

where



https://www.researchgate.net/publication/250928465_Scattering_of_sound_by_air_bladders_of_fish_in_deep_sound-scattering_ocean_layers?el=1_x_8&enrichId=rgreq-52d3359b-d4be-4e2d-8bc7-21858c26f9c7&enrichSource=Y292ZXJQYWdlOzI3MjUxODQ1OTtBUzoyMTg5OTIxNTg0ODI0MzJAMTQyOTIyMzIwNzgxNw==

https://www.researchgate.net/publication/238986993_Resonant_acoustic_scattering_by_swimbladder-bearing_fish?el=1_x_8&enrichId=rgreq-52d3359b-d4be-4e2d-8bc7-21858c26f9c7&enrichSource=Y292ZXJQYWdlOzI3MjUxODQ1OTtBUzoyMTg5OTIxNTg0ODI0MzJAMTQyOTIyMzIwNzgxNw==

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1

drad¼

qf

qw

kaesr;

1

dvis¼

qf fresa2esr

n;

1

dth¼ 2pfres

3 ca�1ð Þqacpa

pf ja

� �1=2

1þ s

2p2qf f2resa

3esr

� ��1

; (7)

where k ¼ 2pf=cw is the acoustic wave number (cw is the

sound speed in water), s is the surface tension at the fish flesh

and swimbladder interface, n is the viscous coefficient, j is

the thermal conductivity of air, and cpa is the specific heat at

constant pressure for air. The subscripts f, w, and a represent

the quantities associated with fish flesh, surrounding water,

and air in the swimbladder, respectively. The coefficient vrepresents the enhancement of the backscattering amplitude

due to elongation and can be expressed by (Ye, 1997)

v ¼ e�2=3 1� e2ð Þ1=2

ln1þ 1� e2ð Þ1=2

e

: (8)

The values for the parameters of the model for the material

and environmental properties used to estimate the TS of the

two species from the resonant scattering model are given in

Table I. Many of the simulation parameters are adopted from

Love (1978).

It is well known that acoustic backscatter is a function

of angle of orientation for elongated objects. For the small

fish considered in this paper, the backscattering at or near

resonance frequency is independent of angle of orientation

[Eq. (2)], but at higher frequencies, the angular dependency

of the scattering becomes noticeable. To include this angular

dependency, we introduced a simple directivity function

described by a Sinc function (Stanton, 1988)

Dh ¼sin kL=2 sin hð Þ

kL=2 sin h

� �2

; (9)

where k is the wave number, L is the length of the swimblad-

der, and h is the angle of orientation (h¼ 0 is broadside inci-

dence). By combining Eqs. (2) and (9), we obtain

rtotalbs ¼ Dhrbs: (10)

III. RESULTS

A. Trawl data

A broad range of size classes of B. glaciale (10–74 mm

standard length, SL) and M. muelleri (12–56 mm SL) were

caught from the scattering layer. Maurolicus muelleri was

the only fish caught (in the absence of B. glaciale) in four of

the nine trawls (trawls 1, 5, 6, and 8; see Table II). There

was only one instance where B. glaciale comprised 100% of

the fish catch (trawl 2; see Table II). The two species co-

occurred in two of the nine trawls; however, M. muelleri was

by far the dominant species contributing 98% of the total

numbers for the two species for trawls on 25 November and

29 November (trawls 4 and 7; see Table II). The remaining

two trawls contained other swimbladdered species and thus

were not considered for analysis. The majority of the catches

were dominated by the krill Meganyctiphanes norvegicawhich contributed on average 56.7% of the numbers.

Species caught to a lesser extent included saithe (Pollachiusvirens), Norway pout (Trisopterus esmarkii), the amphipod

(Themisto abyssonum), and the pelagic shrimps Sergestesspp and Pasiphae spp (Table II).

B. Morphological features of swimbladders

All sampled fish displayed extreme variability in swim-

bladder size and shape between individuals of the same spe-

cies. B. glaciale had a smaller swimbladder relative to its

body size than M. muelleri (Fig. 2). The majority of the catch

was less than 35 mm SL, and as a result most of the specimens

were fragile and damaged easily during handling and prepara-

tion. Consequently, only a total of 30 M. muelleri were radio-

graphed. From radiograph inspection seven fish were found to

have ruptured swimbladders, and in a further six, swimblad-

ders were absent (probably severely ruptured). The bladders

were considered ruptured if obvious signs of damage to the

bladder wall and disfigurement of bladder shape were

observed. The bladders may have ruptured during capture,

freezing, transportation, or handling in the laboratory.

Individuals with ruptured swimbladders were excluded.

Measurements were, therefore, taken only of intact swimblad-

ders in good condition from 17 adult M. muelleri all of which

were greater than 36 mm. In the case of M. muelleri, the data

suggest that with an increase in the fish length, there is a cor-

responding increase in the swimbladder volume [linear regres-

sion, n¼ 17, r2¼ 0.48, p¼ 0.0011, Fig. 3(a)].

A total of 26 adult (>49 mm) B. glaciale were radio-

graphed with 11 having a swimbladder condition deemed

adequate for analysis. Bladders were absent in 13 individu-

als, and the remaining 2 specimens had ruptured swimblad-

ders. Conversely to findings for M. muelleri, B. glacialeindicated a negative relationship between the fish length and

swimbladder volume although this was not significant [linear

regression, n¼ 11, r2¼�0.09, p¼ 0.67, Fig. 3(b)]. The re-

sultant mean swimbladder lengths were 4.23 and 2.04 mm

with standard deviations of 1.64 and 0.58, which resulted in

an aspect ratio of 3.0 and 3.5 for large and small M. muelleri,respectively. The mean swimbladder length of B. glaciale

TABLE I. Constant parameters and values used to estimate the target

strength of mesopelagic fish according to the resonance scattering model

(see text). Values were the same for both species.

Name Symbol Unit

Value used

in model

Sound speed in sea water cw m s�1 1490

Density of sea water qw kg m�3 1026

Density of fish flesh qf kg m�3 1050

Ratio of specific heat

for air (swimbladders)

ca – 1.4

Specific heat at constant

pressure for air (swimbladders)

cpa cal kg�1 �C�1 240

Surface tension s N m�1 200

Thermal conductivity of air ja cal m�1s�1 �C�1 5.5� 10�3



was 2.91 mm with a standard deviation of 0.69 mm giving an

aspect ratio of 2.21.

C. Single target detection

The quality of the TS depends on how well echoes from

individual targets can be correctly identified and extracted. In

all three datasets, at least one subsample had a high probabil-

ity (p� 0.2) of accepting multiple targets as single targets

within the detection volumes. The subsequent KS test identi-

fied large variability between the numbers of high-probability

subsamples shown to have TS distributions originating from

the same population; this was true across all datasets and at

the four frequencies. Those TS distributions of the subsamples

accepted as valid from the KS test were subjected to multifre-

quency analysis, which showed fewest matches between

18 kHz and other frequencies with 38, 120, and 200 kHz

showing comparatively more matches between them. These

data were combined with TS distributions from subsamples

with low probability (p¼�0.2) to produce the most reliable

mean TS measurements (Table III).

The permutations for the single target recognition criteria

were too numerous to describe the outcome of the filtering

process for all species and size; therefore, large M muelleri at

38 kHz was used as an example. The original unfiltered single

target dataset comprised 798 single targets. Removal of weak

targets on the outskirts of the acoustic beam in the SNR filter

reduced the dataset to 638 targets. The pulse volume resolu-

tion analysis performed on subsamples of the SNR-filtered

dataset revealed that only one subsample (of 15) had a low

probability of detecting multiple targets (p¼� 0.2); this con-

sisted of 22 single target detections. Two-sample KS analysis

carried out on all high-probability subsamples resulted in a

subset of 556 targets; subsequent multifrequency analysis on

this dataset identified 103 targets that matched at one or more

other frequencies. The overall dataset consisted of 125 targets

on which the mean TS was based (see Table III).

TABLE II. Details of deployments (hauls) of the mesopelagic midwater trawl in the Norwegian Osterfjord in the winter of 2011: Time is start and end time of

the haul; depth¼ depth of the headline of the trawl, speed is the average speed during the haul; n¼ number of specimens in the catch; mean length refers to

the average length (6 standard deviation) of the specimens caught.

Haul number Date Time Depth Speed (ms�1) Species caught n Mean length (mm 6 s.d.)

1 22 November 06.39–07.09 40–44 1.57 M. muelleri 581 35.2 6 9.4

M. norvegica 10 679 27.9 6 4.1

2 23 November 23.31–23.41 40–45 1.57 B. glaciale 171 36.4 6 16.9

M. norvegica 6876 23.2 6 6.2

Pasiphacea 1 n/a

3 25 November 10.22–10.52 60–73 1.38 M. muelleri 66 960 22.7 6 2.9

P. virens 1 470

T. abyssonum 1 12

M. norvegica 1 24


B. glaciale 33 60.4 6 9.8

Sergestes 32 64.5 6 19.9

M. norvegica 7329 22.7 6 4.9

Pasiphacea 8 n/a


M. norvegica 8 24.3 6 6.9

T. abyssonum 2 13


M. norvegica 32 853 28.7 6 5.1

Pasiphacea 63 50.9 6 18.8


B. glaciale 214 58.0 6 10.7

M. norvegica 8479 19.9 6 3.2

Sergestes 165 39.4 6 15.5

8 01 December 15.02–15.12 60–67 1.65 M. muelleri 391 27.1 6 4.3

M. norvegica 1521 20.4 6 7.4

9 02 December 05.42–06.00 45–53 1.24 M. muelleri 2833 24.9 6 4.8

M. norvegica 2647 21.2 6 6.1

T. esmarkii 4 103–121

FIG. 2. Lateral radiographs of mesopelagic fish highlighting the position of

the swimbladder (white polygon): (a) M. muelleri (standard length,

SL¼ 41 mm); (b) B. glaciale (SL¼ 57 mm). Both images were exposed at

64 mA for 0.32 s at 40 kilo voltage potential.



D. Target strength modeling

Due to the limited sample size of radiographed fish,

Gaussian distributions were used to describe the swimblad-

der length distribution with the mean and standard deviation

values obtained from the standard length and swimbladder

volume measurements.

Because of the uncertainty in some of the modeling

parameters used in the simulations, a sensitivity analysis of

the parameters in the model was carried out using a mean

swimbladder length of 4.23 mm with a standard deviation

of 1.64 (Fig. 4). However, the measured dimensions of fish

swimbladders based on the radiographed images may not

be accurate. To account for this measuring uncertainty, a

sensitivity analysis was performed on the swimbladder vol-

ume ratio and the resultant TS curves with different vol-

umes are shown in Fig. 4(a). The shear module (real part)

of fish flesh has a moderate influence on TS, while the res-

onance peak amplitude was affected most by viscosity,

decreasing by approximately 8 dB when the viscosity (n)

increased from 1 to 10 kg m�1 s�1. In addition, the sensi-

tivities of the mean tilt angle and the standard deviation

of the tilt angle are also shown [Figs. 4(d) and 4(e),

respectively].

Due to the uncertainties of many of the modeling pa-

rameters, six parameters, volume ratio rvol; viscosity n; shear

modulus lr; mean tile angle �h; standard deviation of tilt

angle rh; and depth D were used as floating parameters

within the reasonable ranges listed in Table IV. A least

square criterion was used to minimize the difference

between the measured and the theoretically predicted TS

based on a set of the six chosen parameters

Err ¼X4

i¼1

jTSmodelðrvol; n; lr;�h; rh;DÞ

�TSmeasðrvol; n; lr;�h; rh;DÞj2; (11)

where fi refers to ith frequency. The data and model compar-

ison is shown in Fig. 5, and the parameters used in the final

model predictions are shown in Table IV.

The model fit at low frequencies (18 and 38 kHz) was

driven by changes in n and D, particularly around resonance,

whereas �h and lh drove the fit at higher frequencies (120 and

200 kHz). Volume ratio (rvol) lowered the overall level of

the model. To fit the model to the data, n needed to be

changed to fit the resonance peak for the two sizes of pearl-

side. The resonance peak shifted to higher frequencies with

an increase in lr and D. The depth, D, was fitted as close to

the mean trawl depth of the respective scattering layer as

possible.

The in situ TS data fit the model shapes closely for large

pearlside and B. glaciale, although the absolute levels of the

data are lower than models beyond the resonance peak

(>30 kHz). The model fitted small pearlside well around the

resonance peak, although the model shape under estimated

the absolute levels at frequencies higher than resonance

(>30 kHz). The resonance peak for large M. muelleri [Fig.

5(a)] was approximately �47 dB at about 10 kHz with a

sharp decline to �66 dB at 250 kHz, which is reflected in the

model showing a reduction in TS with increase in frequency.

Small M. muelleri [Fig. 5(b)] showed a resonance peak of

approximately �54 dB at 23 kHz with a gentler drop from

resonance down to �68 dB at 250 kHz and steady decrease

in TS with increase in frequency.

Model and in situ TS data comparisons for B. glaciale(ML¼ 37.4 mm) are presented in Fig. 5(c), showing a reso-

nance peak of �54 dB at 20 kHz with a rapid decrease to

�68 dB at 250 kHz and gentle decrease in TS with increase

in frequency.

IV. DISCUSSION

The swimbladder anatomies of Myctophidae and

Sternoptychidae have been described as being considerably

FIG. 3. Relationship between the

swimbladder volume (mm3) of meso-

pelagic fish and fish length (standard

length, mm): (a) M. muelleri; (b) B.glaciale. Black line shows fitted linear

regression.

TABLE III. Mean TS measurements derived from the comprehensive filter-

ing procedure and subsequently used in theoretical model predictions. The

percentage of targets which met the filtering criteria to estimate mean TS

are given in brackets.

18 kHz 38 kHz 120 kHz 200 kHz

Large M. muelleri �53.6 (31) �60.8 (16) �62.9 (16) �66.4 (19)

Small M. muelleri �57.1 (6) �60.3 (8) �62.0 (7) �65.0 (9)

B. glaciale �54.2 (84) �62.1 (60) �65.6 (33) �67.6 (35)



different (Kleckner and Gibbs, 1972). The present study sup-

ports this, and as such both species must be considered sepa-

rately. In the present study, adults of both B. glaciale and M.muelleri possessed inflated swimbladders, although many

specimens had ruptured swimbladders. Differences in the

occurrences of ruptured swimbladders have been attributed to

the associated differences in anatomy and physiology between

Myctophidae and Sternoptychidae (Kleckner and Gibbs, 1972).

FIG. 4. Sensitivity study of the reso-

nance scattering model outputs of tar-

get strength to various modeling

parameters: (a) Swimbladder volume

ratio (the percent values in the figure

legend represent the volume percent

relative to its measured volume of the

swimbladder); (b) viscosity; (c) shear

module of fish flesh; (d) mean tilt

angle; (e) standard deviation of mean

tilt angle; (f) depth.

TABLE IV. Fitted model parameters and fitting errors as well as parameter ranges used in sensitivity analysis.

Parameter Symbol Unit

Value used in model

Sensitivity range testedLarge M. muelleri Small M. muelleri B. glaciale

Volume factor rvol % 0.8 0.8 0.8 0.8–1.2

Viscosity n kg m�1 s�1 1 1 3 1–10

Shear modulus lr N m�2 7.50Eþ 05 1.00Eþ 06 7.50Eþ 05 105– 107

Mean tilt angle �h � 55 0 55 0–70

Standard deviation of tilt angle lh� 20 10 10 0–30

Depth D m 10 2 30 2 – 60

Error dB 0.65 6.15 0.38



Butler and Pearcy (1972) classified myctophid swim-

bladders as being thin-walled structures filled with gas, atro-

phied without gas, saturated with lipids or being entirely

absent of any structure. In the present study, 50% of B. gla-ciale had a gas-filled bladder saturated with fat and 50% had

no bladder at all. As myctophids mature, lipids steadily

replace the gas within the swimbladder, and as such swim-

bladder volume is not dependent on fish size (Neighbors and

Nafpakitus, 1982). This gradual replacement of gas may

explain the apparent absence of the swimbladder in some

individuals. Alternatively, the swimbladder may still be

present in some form but will not be displayed using the con-

ventional radiograph method employed here as the material

properties such as index of (optical) refraction of lipids

within the swimbladder, resemble the properties of the fish

flesh too closely. Past studies also suggest that other myctophid

species lose their swimbladders as they mature to adulthood

(e.g., Diaphus garmani, Diaphus theta, and Symbolophonuscali). This loss results in the occurrence of “bladder” and

“bladderless” individuals within a single species (Marshall,

1960; Butler and Pearcy, 1972; Neighbors and Nafpakitus,

1982; Yasuma et al., 2003; Yasuma et al., 2010).

It is accepted that in most fish species the swimbladder

grows proportionally with body length, but in myctophids,

the swimbladder atrophies, whereby the swimbladder

remains the same size but the gas is replaced by fatty acid.

Variability in the relative proportion that the swimbladder

volume contributes to the total body size is common for

myctophid species (Butler and Pearcy, 1972; Neighbors,

1992). Yasuma et al. (2010) reported a relatively low swim-

bladder proportion to total body size of <0.5%, while other

investigators found large disparity in swimbladder propor-

tion between different species ranging from 0.3% to 6%–7%

of the total body volume (Butler and Pearcy, 1972). This

appears to be a feature closely linked to DVM (Yasuma

et al., 2003). The relative reduction in swimbladder volume

associated with increasing body length has been attributed to

the high levels of gas absorption and secretion associated

with moving within a large vertical range and may be con-

sidered an unnecessary energetic expenditure. It has also

been suggested that individuals may inflate their swimblad-

ders only in the upper levels of their migration (Yasuma

et al., 2003). However, Benoit-Bird et al. (2003) proposed

that such species may retain swimbladder volume during

DVM. Differences in the ratio between body size and swim-

bladder volume among myctophids suggests variability in

the relative contribution of different species to the overall

backscattering of a deep scattering layer. McClatchie et al.(2003) noted that for deep water fish species such as mycto-

phids, where the swimbladder length does not always

increase with fish length, the TS cannot be standardized by

the square of the length as would be the case for other spe-

cies. This illustrates the importance of identifying variability

between and within species. Additionally, the occurrence of

“bladder” and “bladderless” individuals within a species

could result in the underestimation of biomass from acoustic

methods as the bladder fish would dominate the acoustic

scattering in spite of their numbers.

Sternoptychidae are described as possessing well devel-

oped but thin-walled, gas-filled swimbladders (Marshall,

1960; Brooks, 1977) and M. muelleri conforms to this. The

low proportion of M. muelleri without swimbladders is likely

a consequence of the complete collapse of the swimbladder

rather than total absence. Thin-walled bladders are subject to

FIG. 5. Target Strength of (a) M. muelleri (mean length¼ 35.2 mm), (b) M.muelleri (mean length¼ 23.2 mm), (c) B. glaciale (mean length¼ 55.60 mm)

against frequency. Black circles are the mean in situ TS collected with the

Simrad EK60 echosounders for appropriate hauls. The black line shows the

resonance scattering model output, and error bars show the upper and lower

95% confidence intervals of the mean estimates.



rupture as a consequence of the capture and handling phase

which may explain the relatively high number of individuals

with collapsed or ruptured swimbladder in this and other

studies (e.g., Yasuma et al., 2003). Alternatively, rapid

changes in pressure associated with capture from depth may

have caused gas to escape into the peritoneal cavity or may

have caused the over expansion and eventual rupture of the

bladder wall (Nichol and Chitron, 2006). The effects of this

can be reduced by targeting shallow migratory layers and

having a slow haul speed, thereby lessening rapid expansion

of the swimbladder wall. Based on swimbladder measure-

ments [Fig. 3(a)], M. muelleri conforms to the assumption

that the swimbladder grows proportionality with body length

and thus is a simpler species to model. The difficulty in the

present study was the occurrence of different size classes

within the trawl regions, which, as shown, give different TS

values [Figs. 5(a) and 5(b)].

The objective of the single target recognition criteria

was to determine the mean TS of both species with an accu-

racy of about 61 dB. A higher accuracy has little biological

foundation due to the variability in physiology over season,

ontogenetic stage, etc. (Ona, 1990). In the TS measurements

presented in this study, there were two possible sources of

bias that may have affected the mean TS. First, a bad signal-

to-noise-ratio (SNR) on the outskirts of the acoustic beam

leads to the unwanted rejection of weak data in the lower

end of the TS distribution. However, this error is not very

large because the targets are weak compared to those in the

upper end of the TS distribution. Second, and more impor-

tantly, multiple targets erroneously accepted as one target

bias the mean value toward higher mean TS. In this study,

there was a need to qualify whether the data came from high

or low densities, and it was important to take care that larger

targets (potentially multiple targets) in the distribution did

not affect the mean TS. As a result, data with varying den-

sities (or number of targets in the pulse resolution volume)

were compared. In particular, the upper ends of the TS distri-

bution were monitored for possible erroneous acceptance of

two or several targets as one. Pulse volume resolution analy-

sis revealed that not all datasets, at the four frequencies, had

at least one subsample with low probabilities (p¼�0.2) of

detecting multiple targets. As a result, all high-probability

subsamples were tested for similarity using the KS test, and

those subsamples shown to be similar were accepted as valid

for multifrequency analysis providing they met the criteria

set. The single target detection algorithm extracted targets

from each of the four frequencies separately. The present

study matched most single targets at 120 and 200 kHz. The

poor matches with 18 and 38 kHz are likely a result of the

larger distance between these transducers and the others on

the vessel’s hull or a higher noise level on the 18 kHz trans-

ducer and the larger pulse volume. Furthermore, the pulse

length was 0.256 ms at night, corresponding to when the fish

were caught, and the pulse was likely at the edge of the

18 kHz bandwidth. Increasing the range of target acceptance

and pulse length would increase the number of matches but

reduce the likelihood that the same target was being matched

on each occasion.

Compared to loosely aggregated or individually dis-

persed fish, fish in schools have almost homogeneous tilt

angle distributions (Blaxter and Batty, 1990). Even with

identical tilt angles, this may result in higher average TS for

schooling fish compared with individually dispersed fish.

When fish aggregate in dense schools/layers, the single echo

detector (SED) is more likely to mistake echoes from two

fish in close proximity with an echo from a single fish (Soule

et al., 1995). SEDs collect data without consideration for

fish density (Barange et al., 1996). This has been suggested

as a possible reason for higher than expected measurements

of in situ TS (Soule et al., 1995; Barange et al., 1996) as the

system unsuccessfully rejects echoes from multiple targets;

this may have considerable effects on measured TS. Isolated

individuals in low density parts of an aggregation may dis-

play different behaviors from fish inside the school, for

example, tilt angle which in turn lead to large variations in

TS distributions.

In this study, there was a need to qualify whether the

data came from high or low densities, and it was important

to take care that larger targets (potentially multiple targets)

in the distribution did not affect the mean TS. As a result

data with varying densities (or number of targets in the pulse

resolution volume) were compared. In particular, the upper

ends of the TS distribution were monitored for possible erro-

neous acceptance of two or several targets as one. Pulse vol-

ume resolution analysis revealed that not all datasets, at the

four frequencies, had at least one subsample with low proba-

bilities (p¼�0.2) of detecting multiple targets. As a result,

all high-probability subsamples were tested for similarity

using the KS test, and those subsamples shown to be similar

were accepted as valid for multifrequency analysis providing

they met the criteria set.

The single target detection algorithm extracted targets

from each of the four frequencies separately. The present

study matched most single targets at 120 and 200 kHz. The

poor matches with 18 and 38 kHz are likely a result of the

larger distance between these transducers and the others on

the vessel’s hull or a higher noise level on the 18 kHz trans-

ducer and the larger pulse volume. Furthermore, the pulse

length was 0.256 ms at night, corresponding to when the fish

were caught, and the pulse was likely at the edge of the

18 kHz bandwidth. Increasing the range of target acceptance

and pulse length would increase the number of matches but

reduce the likelihood that the same target was being matched

on each occasion.

The model sensitivity (Fig. 4) to a number of parameters

allowed for the flexibility of fitting these parameters in an

attempt to fit the model to the three data sets. These were in

an acceptable range as given in Love (1978). We assumed

pressure dependence for both species given that 43% of M.muelleri had swimbladders that were ruptured, absent, or

completely collapsed. Although swimbladders for B. gla-ciale were not affected to such a degree, the radiographs sug-

gested that the bladder ruptured and gas had escaped, as

small pockets of gas were visible close to the swimbladder

structure. Such an assumption provided a better fit of the

data.



Fish depth has a limited influence of on resonance fre-

quency and amplitude due to the small depth range covered

by the fish species reported in this paper. Because we assumed

a constant-mass model, the swimbladder volume obeys

Boyle’s law. If we use a constant-volume model, the reso-

nance frequency will be lower, and the agreement between

the model and data will be degraded (Fig. 5), indicating that

the volume of the swimbladder may change even for a physo-

clist species; this is consistent with the short-term change

experienced in hauling the trawl at speed from depth. When

brought to the surface from depth, the gas cannot be reab-

sorbed fast enough, and usually the swimbladder will rupture

and gas will escape. However, if not ruptured, the swimblad-

der expands and the dimensions do not reflect its size at depth,

and it must be reduced back to the size at its original depth.

To account for this, swimbladder volume ratio was also

treated as a floating parameter. Overall the theoretical TS

curve based on the base model (parameters listed in Tables I

and IV) predicted the mean TS reasonably well and the curves

from two species provided upper and lower (based on 95%

confidence intervals of the mean) bounds of the TS.

The resonance frequency is lower for larger pearlside

but displays a much higher resonance peak at a lower fre-

quency (about 10 kHz). Because the swimbladder size of B.glaciale is smaller than that of M. muelleri, the resonance

frequency of B. glaciale is higher [see Eq. (4)] and its overall

TS level is lower [see Eq. (2)]. The resonance peak for B.glaciale (�20 kHz) is similar to that predicted for mycto-

phids by Kloser et al. (2002). Yasuma et al. (2003) deter-

mined that for some bladderless myctophid species, the

angle of orientation would have a significant influence on TS

measurements, whereas the TS of some myctophid species

that possess a largely spherical swimbladder will not be

affected significantly by differences in the angle of orienta-

tion. Radiograph analysis in the present study showed that

both M. muelleri and B. glaciale possess ellipsoid-shaped

swimbladders, and therefore TS is likely to be influenced by

the angle of orientation, which is supported by the results.

Benoit-Bird and Au (2001) reported TS measurements

under ex situ conditions for eight myctophid species associated

with the Hawaiian mesopelagic communities and reported

TS¼ 20log (standard length in cm) �58.8 at 200 kHz. Using a

theoretical model, Hamano (1993) acquired the relationship,

TS¼ 17.4 log SL-69.9 (�59.4 dB for 40 mm SL) for M. muel-leri at 88 kHz, which corresponds to approximately a 4 dB dif-

ference in the value predicted using the current model. Sawada

et al. (2011) obtained average TS of �55.8 dB for Diaphustheta at 70 kHz. Torgersen and Kaartvedt (2001) derived TS

estimates that varied from �70 to �50 dB for M. muelleri and

B. glaciale using acoustic-tracking techniques at 38 kHz. The

present results agree with these findings; however, current esti-

mates are generally lower than those found in other similar

species.

TS-length relationships have not been obtained for

either species as a result of no clear relationships being iden-

tified between standard length and swimbladder volume.

Although the results hint that M. muelleri has a positive rela-

tionship between standard length and swimbladder volume

[Fig. 3(a)]; however, a greater sampling effort is required to

confirm this. We can additionally infer that there is a nega-

tive relationship between standard length and swimbladder

volume for B. glaciale [Fig. 3(b)]. This study offers the first

steps toward providing TS-length relationships for both spe-

cies and identifies some of the issues associated with deter-

mining TS values for these complex deep-water species.

ACKNOWLEDGMENTS

This project was funded by the research council of

Norway (Contract No. 190318/S40). Thanks to the crew of

the MRV Haakon Mosby and the technical staff at the

Institute of Marine Research, Norway. This work also

received funding from the Marine Alliance for Science and

Technology for Scotland (MASTS) pooling initiative and

their support is gratefully acknowledged. MASTS is funded

by the Scottish Funding Council (Grant Reference No.

HR09011) and contributing institutions. Thanks to Marine

Scotland Science for funding the collection of radiograph

data. Many thanks to Martin Downing at the Health Science

Building of the University of Aberdeen for his help with

radiographing the specimens.

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Target strengths of two abundant mesopelagic fish species