Abstract
We report theoretical values of the target strength (TS) of four myctophid fish (Ceratoscopelus warmingii, Myctophum asperum, Diaphus garmani, and Diaphus chrysorhynchus) based on morphometry of the swimbladder. None of the D. chrysorhynchus had an inflated swimbladder, but the other species had both inflated and non-inflated swimbladders, depending on body size. The relationships between swimbladder and body length showed that once gas production started, the swimbladders grew faster than the rest of the body (positive allometric growth). However, M. asperum showed regression of the swimbladder after positive allometric growth, so larger specimens had non-inflated swimbladders. Based on the measurements of swimbladder and body length, the theoretical TS values at 38 and 120 kHz were calculated using existing sound-scattering models. In fish with inflated swimbladders, TS values were relatively low (less than −67 dB, reduced TScm) at both frequencies. Regression slopes on TS–body length (log) plots were >20, suggesting that their scattering cross sections were not proportional to the square of the body length. In contrast, the TS values of M. asperum decreased with growth in large fish (60–80 mm long) through swimbladder regression. Scattering cross sections of fish without swimbladders were not proportional to the square of the body length over the whole size range.Yasuma, H., Sawada, K., Takao, Y., Miyashita, K., and Aoki, I. 2010. Swimbladder condition and target strength of myctophid fish in the temperate zone of the Northwest Pacific. – ICES Journal of Marine Science, 67: 135–144.
Introduction
Myctophids are the dominant mesopelagic fish taxon in temperate and subtropical waters of the Northwest Pacific, and reliable biomass estimates are needed. The use of acoustic methods is thought to be the best way to do this (Gjøsaeter and Kawaguchi, 1980).
Acoustic surveys measure the scattered sound in the water column, so we need to know the target strength (TS) of individual fish to convert the measured backscattered energy into an estimate of fish biomass. The paradigm that the acoustic cross section is proportional to the square of body length and the “20 log length” relationship is often used to estimate fish TS over a range of sizes (Foote, 1979; MacLennan and Simmonds, 1992), but some fish groups, especially deep-water fish, do not follow the rule. This is because the growth of the main scattering structure (the swimbladder) often does not grow in proportion to the rest of the body (McClatchie et al., 2003; Yasuma et al., 2003). Moreover, myctophid swimbladder condition varies both among and within species, so there is huge variation in TS (Capen, 1967; Neighbors and Nafpaktitis, 1982; Yasuma et al., 2003). It is important to know how this condition changes with growth in each species. The confidence intervals for even a relative biomass assessment would need to be quite wide until we understand the relationship between swimbladder condition and TS better.
Many theoretical models have been developed to estimate the TS of marine organisms (Horne and Clay, 1998). Theoretical models approximate the main source of soundscatter, i.e. the swimbladder (or the body of fish without swimbladders), as a geometric configuration. The use of these models has several merits; they can reduce the number of experimental measurements, estimate the backscatter pattern relative to fish orientation, and estimate the TS of small-bodied fish with reduced or no swimbladders, or deep-sea fish, which have a very weak soundscatter and for which there are no in situ measurements. Using 14 species of myctophid around Japan, Yasuma (2004) computed the pitch-angle shifts of TS values using theoretical models after making morphological measurements of the swimbladder and the fish body, and compared these results with experimental measurements conducted in a tank. The study showed that the TS values and the shifts computed by the vacant prorate-spheroid model (PSM; Furusawa, 1988) closely matched the results of experimental measurements for fish with a well-inflated swimbladder. The computed results using the liquid deformed-cylinder model (DCM; Ye et al., 1997) closely matched the results of experimental measurements for fish with a non-inflated swimbladder.
The purpose of the present study was to estimate the TS–length relationships for four myctophid species (Ceratoscopelus warmingii, Myctophum asperum, Diaphus garmani, and Diaphus chrysorhynchus) that are abundant in temperate and subtropical waters of the Northwest Pacific. First, we describe the morphological characteristics and growth of the swimbladder based on X-rays. Then, using morphological parameters of the swimbladders or fish body, theoretical sound-scattering models were applied to estimate the TS at 38 and 120 kHz, which are used commonly in scientific echosounders.
Material and methods
Samples were obtained from five surveys conducted around southern Japan (36–25°N 145–128°E) from August 2001 to June 2003 (Yasuma, 2004). Nine tows were carried out with an Isaacs–Kidd midwater trawl with codend mesh of 333 µm and five with a 4-m2 MOCNESS with 2-mm mesh. Each tow was conducted at night, and the target layer was identified with an echosounder. The target sound-scattering layers were between 20 and 200 m deep. Hauling speeds were kept as slow as possible (0.1–0.5 m s−1) to reduce the damage to the fish. Live fish were selected from the catch and kept for several hours in a tank on board to naturalize swimbladder condition, then placed in plastic bottles containing seawater and frozen rapidly (within 30 min) to below −40°C. The effect of rapid freezing on swimbladder shape was considered to be negligible after preliminary experimentation (HY, unpublished).
Swimbladder measurement and allometry
In the laboratory, the bottles were thawed slowly in cold water over 24 h so the swimbladder shape would not change. In all, 123 C. warmingii (23–83 mm standard length), 93 M. asperum (18–86 mm), 171 D. garmani (21–57 mm), and 85 D. chrysorhynchus (62–100 mm) were collected in this manner for swimbladder observation and TS estimation.
After external morphological measurements of the fish, a specialized “soft X-ray” imaging system (Softex PRO-TEST 100) was used to map the outlines of the swimbladders. All fish were X-rayed from lateral and dorsal sides, following Sawada et al. (1999), then dissected to confirm the shape of the swimbladder. The swimbladders of myctophids are thin-walled and gas-filled, atrophied without gas, and lack any structure (Butler and Pearcy, 1972; Yasuma et al., 2003). To estimate the acoustic scattering properties, we need to know the shape occupied by the gas. If there was no gas in the swimbladder, we treated the fish as a “swimbladderless” fish. If gas was found, we treated the fish as a “swimbladdered” fish and mapped the shape occupied by the gas as the shape of the swimbladder. Outlines of the body shape of the swimbladderless fish were selected for subsequent TS model estimation using digital photo imagery. We measured swimbladder length la, swimbladder height lb, and swimbladder width lc to the nearest 0.1 mm on outlines of the lateral and dorsal aspects. The main axis of the lateral image was used as swimbladder length. The swimbladder tilt angle was also measured using the outline of the lateral aspect (Figure 1).
Morphometry on lateral and dorsal swimbladder X-ray images. The symbols la, lb, and lc represent swimbladder length, swimbladder height, and swimbladder width, respectively.
Swimbladder volume Vb was calculated from the formula of Capen (1967), i.e. Vb = 4π/3 (la/2)(lb/2)(lc/2), to estimate its contribution to whole-body volume, which was estimated by submersion in a graduated cylinder.
Organ growth usually follows simple allometric law (Huxley, 1972). Let L be fish standard length, and r the equivalent spherical radius of the swimbladder. Then, the allometric relationship is r = kLq, where q is the allometric exponent (Saenger, 1989). Distinct types of swimbladder growth are associated with different ranges of q. We defined four types of growth: regressive growth (q < 0), negative allometric growth (0 < q < 1), isometric growth (q = 1), and positive allometric growth (q > 1). Introducing x = log(L) and y = log(r), allometric law can be expressed in the linear form y = a + qx, with a = log(k). The equivalent spherical radius r, given by r = (lalblc)1/3, can be used to observe trends in swimbladder growth because it can reduce the number of parameters. The effects of reducing parameters on swimbladder resonance scattering frequencies are negligible (<5%) when the proportions of the minor and the major axes (aspect ratio) are relatively low (lb/la and lc/la >0.3), where the lower aspect (near spherical) is close to the value 1 (Strasberg, 1953; Andreeva, 1964).
Sound-scattering model
The swimbladder is the main source of echoes in fish with swimbladders (Foote, 1980a; Ye and Farmer, 1997). Therefore, model calculations were applied to swimbladder shape in swimbladdered fish and for body shape in swimbladderless fish.
Based on the morphological measurements of the swimbladder and body shape, we calculated theoretical values of TS related to fish pitch angle. According to Yasuma et al. (2003) and Yasuma (2004), we selected the vacant PSM (Furusawa, 1988) for swimbladdered fish and the liquid DCM (Ye, 1997; Ye et al., 1997) for swimbladderless fish, which matched the experimental TS measurements for the species we collected (Yasuma, 2004).
The PSM approximates a swimbladder by a simple spheroid using swimbladder length, height, and width. We followed the procedure of Sawada et al. (1999) and Yasuma et al. (2003) for PSM calculation. The main parameters, sound speed in seawater and in the swimbladder, were 1488 and 340 m s−1, respectively. The sound speed in seawater was calculated from the equation of Mackenzie (1981) using the CTD data obtained while collecting the fish. Details of the PSM are described in Furusawa (1988).
The DCM describes a fish body as a series of adjacent, disc-like, cylindrical elements. We divided each outline into 20 equal parts, with 19 lines drawn perpendicular to the major axis, following Sawada et al. (1999) and Yasuma et al. (2003). Details of the DCM are described in Ye (1997) and Ye et al. (1997). The model requires the relative mass density (g) and the relative sound speed (h) of fish flesh against seawater. These parameters were measured previously using a density-bottle method (Greenlaw, 1977) and a time-average-approach method using a T-tube (Mikami et al., 2000). Details of these measurements are described by Yasuma (2004) and Yasuma et al. (2006). Based on the temperature range of their main habitat (10–15°C), the values of g and h were 1.05 and 1.03 for M. asperum, and 1.01 and 1.03 for the other three species.
For both models, we calculated TS shifts with body pitch angle from −90° (head-down) to +90° (head-up) in 1° steps. Then, according to Foote (1980b), the averaged value of the TS calculated from a TS shift using the given pitch-angle distribution was used as the TS of the fish. Here, we applied a distribution within a mean of 0° (horizontal direction) and a standard deviation of 15°.
It is convenient to normalize the TS value by the square of fish length. This is termed the reduced TS (dB) and given as TScm when the fish length is in centimetres. The relationship between TS and fish standard length was summarized by the linear expression y = mx + b, where y represents the value of TS (dB), and x the log of standard length (cm). If the acoustic cross section is proportional to length squared, the regression slope m is assumed to be 20 when TScm is represented by the intercept b and takes a constant value over a range of sizes.
Results
Swimbladder morphology
Our samples included juvenile, immature, and mature C. warmingii, M. asperum, and D. garmani, and immature and mature D. chrysorhynchus. Swimbladder length is plotted against fish standard length in Figure 2. Ceratoscopelus warmingii, M. asperum, and D. garmani included swimbladdered and swimbladderless fish, but D. chrysorhynchus included only swimbladderless fish. In C. warmingii, the swimbladderless fish were small (23–43 mm), and there was an unformed swimbladder in each fish, seen under dissection. Swimbladdered fish were >33 mm, and all fish >44 mm had inflated swimbladders. In M. asperum, swimbladderless fish were separated out into two groups (18–33 and 74–86 mm), and swimbladdered fish were of intermediate but overlapping length (31–77 mm). Fish in the smaller swimbladderless group had unformed swimbladders, and those in the larger group had visible swimbladders, but atrophied and without gas. Swimbladder length increased with growth under ∼50 mm, but it decreased with growth over ∼60 mm. In D. garmani, all fish <31 mm were swimbladderless, but >31 mm there were both swimbladderless and swimbladdered fish. Swimbladders of small fish (<30 mm) were unformed, but in larger fish, swimbladders were visible even when categorized as swimbladderless fish, where the swimbladders were atrophied. All D. chrysorhynchus had atrophied swimbladders without gas.
Plots of swimbladder length of (a) Ceratoscopelus warmingii, (b) Myctophum asperum, (c) Diaphus garmani, and (d) Diaphus chrysorhynchus, against fish standard length.
The number of swimbladdered fish, the swimbladder aspect ratio (minor/major axis), the swimbladder tilt angle, and the percentage of swimbladder volume Vb to the body volume are listed in Table 1. We defined the main axis of lateral images la as the main axis, and the mean values of swimbladder height lb and swimbladder width lc as the minor axis in aspect ratio calculations. The highest aspect ratio was 0.3, and most fish had values from 0.5 to 1, in all four species. Smaller swimbladders have lower aspect ratios (closer to 1) and are nearly spherical, although the relationships between swimbladder length and aspect ratio were not significant. The Vb percentage ranged from 0.01 to 2.63 and was <0.5 in most fish.
Ranges of swimbladder aspect ratio, swimbladder tilt angle, and percentage of swimbladder volume Vb in body volume (mean ± s.d.).
| Species | n | Aspect ratio | Tilt angle (°) | Vb percentage |
|---|---|---|---|---|
| Ceratoscopelus warmingii | 83 | 0.28–0.97 (0.61 ± 0.22) | 0.0–24.8 (14.9 ± 9.9) | 0.01–2.63 (0.49 ± 0.50) |
| Myctophum asperum | 43 | 0.32–1.00 (0.75 ± 0.19) | 0.0–21.8 (10.6 ± 8.7) | 0.01–1.48 (0.39 ± 0.37) |
| Diaphus garmani | 82 | 0.27–1.00 (0.57 ± 0.23) | 0.0–19.7 (8.7 ± 7.2) | 0.01–1.53 (0.38 ± 0.37) |
| Species | n | Aspect ratio | Tilt angle (°) | Vb percentage |
|---|---|---|---|---|
| Ceratoscopelus warmingii | 83 | 0.28–0.97 (0.61 ± 0.22) | 0.0–24.8 (14.9 ± 9.9) | 0.01–2.63 (0.49 ± 0.50) |
| Myctophum asperum | 43 | 0.32–1.00 (0.75 ± 0.19) | 0.0–21.8 (10.6 ± 8.7) | 0.01–1.48 (0.39 ± 0.37) |
| Diaphus garmani | 82 | 0.27–1.00 (0.57 ± 0.23) | 0.0–19.7 (8.7 ± 7.2) | 0.01–1.53 (0.38 ± 0.37) |
Ranges of swimbladder aspect ratio, swimbladder tilt angle, and percentage of swimbladder volume Vb in body volume (mean ± s.d.).
| Species | n | Aspect ratio | Tilt angle (°) | Vb percentage |
|---|---|---|---|---|
| Ceratoscopelus warmingii | 83 | 0.28–0.97 (0.61 ± 0.22) | 0.0–24.8 (14.9 ± 9.9) | 0.01–2.63 (0.49 ± 0.50) |
| Myctophum asperum | 43 | 0.32–1.00 (0.75 ± 0.19) | 0.0–21.8 (10.6 ± 8.7) | 0.01–1.48 (0.39 ± 0.37) |
| Diaphus garmani | 82 | 0.27–1.00 (0.57 ± 0.23) | 0.0–19.7 (8.7 ± 7.2) | 0.01–1.53 (0.38 ± 0.37) |
| Species | n | Aspect ratio | Tilt angle (°) | Vb percentage |
|---|---|---|---|---|
| Ceratoscopelus warmingii | 83 | 0.28–0.97 (0.61 ± 0.22) | 0.0–24.8 (14.9 ± 9.9) | 0.01–2.63 (0.49 ± 0.50) |
| Myctophum asperum | 43 | 0.32–1.00 (0.75 ± 0.19) | 0.0–21.8 (10.6 ± 8.7) | 0.01–1.48 (0.39 ± 0.37) |
| Diaphus garmani | 82 | 0.27–1.00 (0.57 ± 0.23) | 0.0–19.7 (8.7 ± 7.2) | 0.01–1.53 (0.38 ± 0.37) |
The relationship between the logarithmic scale of swimbladder equivalent radius and standard length is shown in Figure 3. The regression coefficient in each relationship represents the allometric exponent q. Values of q were 1.3 in C. warmingii and 1.7 in D. garmani, implying that their swimbladders had positive allometric growth. We divided the swimbladder growth of M. asperum into two body length groups (<50 and >60 mm), because the plot of swimbladder length in Figure 2 implied different growth patterns. Allometric growth was positive (q = 2.6) for the smaller group and regressive (q = −1.7) for the larger group.
Relationship between logarithmic scale of the swimbladder equivalent radius r and standard length L of (a) C. warmingii, (b) M. asperum, and (c) D. garmani. Regression lines and equations are shown. The β (in parenthesis) indicates 95% confidence limits of the regression line.
TS estimation using theoretical models
Typical TS shifts of a swimbladdered and a swimbladderless fish estimated by the PSM and the DCM are shown as a function of fish pitch angle in Figure 4. The TS shifts of swimbladdered fish estimated by the PSM are smooth at 38 and 120 kHz, suggesting a relatively small effect of fish orientation. On the other hand, the TS shifts of swimbladderless fish estimated by the DCM show relatively narrow and pronounced peaks at 38 and 120 kHz, suggesting that changes in fish orientation would have a major effect on TS variance. The results showed that those effects were more pronounced in large fish at high frequencies.
Examples of the theoretical TS shift of a swimbladdered (left panel) and a swimbladderless (right panel) fish, as a function of fish pitch angle. Positive angles are head-up and negative angles head-down. The bold and dotted lines denote the TS at 38 and 120 kHz, respectively. The left panel shows the TS of a C. warmingii (standard length 60 mm; swimbladder length 9.1 mm; aspect ratio 0.45), the right panel the TS of a D. chrysorhynchus (standard length 74 mm).
The relationship between estimated tilt-averaged TS and the log of the standard length (cm) of swimbladdered fish is shown in Figure 5. The equations of the linear regression in Figure 5 and the ranges of TScm are listed in Table 2. In C. warmingii and D. garmani, the regression slope m was >20 at both frequencies. This suggests that the acoustic cross section is not proportional to the square of body length and that the TS increases faster than body length. In M. asperum, the TS increased significantly with body length (m > 35) in the small size class (31–48 mm), but it decreased with body length in the large size class (61–77 mm), indicating regressive allometric growth of the swimbladder in that species (Figure 5, Table 2). No major differences between the TS value at 38 and 120 kHz were seen in any swimbladdered fish (ANCOVA, p > 0.05).
Plots of TS against log of standard length (cm) for swimbladdered (a) C. warmingii, (b) M. asperum, and (c) D. garmani at 38 kHz (left column) and at 120 kHz (right column).
Equations of the linear regressions plotted in Figure 5 and the ranges of standard length.
| Species | Length range (mm) | n | Frequency (kHz) | y = mx + b | TScm range (dB) | |||
|---|---|---|---|---|---|---|---|---|
| m | b | r2 | ± β | |||||
| Ceratoscopelus warmingii | 33–83 | 81 | 38 | 26.3 | −78.1 | 0.30 | 9.1 | −82.3 to −67.7 |
| 120 | 26.1 | −79.2 | 0.31 | 8.7 | −82.6 to −68.6 | |||
| Myctophum asperum | 31–48 | 31 | 38 | 45.4 | −88.6 | 0.45 | 15.9 | −79.9 to −68.8 |
| 120 | 36.3 | −84.6 | 0.44 | 12.6 | −80.2 to −69.7 | |||
| 61–77 | 8 | 38 | −135.2 | −57.3 | 0.69 | 80.1 | −87.2 to −69.8 | |
| 120 | −130.8 | −52.4 | 0.67 | 82.5 | −87.6 to −70.4 | |||
| Diaphus garmani | 31–57 | 75 | 38 | 34.5 | −83.5 | 0.46 | 8.1 | −81.7 to −68.7 |
| 120 | 32.7 | −83.3 | 0.49 | 7.6 | −82.6 to −69.4 | |||
| Species | Length range (mm) | n | Frequency (kHz) | y = mx + b | TScm range (dB) | |||
|---|---|---|---|---|---|---|---|---|
| m | b | r2 | ± β | |||||
| Ceratoscopelus warmingii | 33–83 | 81 | 38 | 26.3 | −78.1 | 0.30 | 9.1 | −82.3 to −67.7 |
| 120 | 26.1 | −79.2 | 0.31 | 8.7 | −82.6 to −68.6 | |||
| Myctophum asperum | 31–48 | 31 | 38 | 45.4 | −88.6 | 0.45 | 15.9 | −79.9 to −68.8 |
| 120 | 36.3 | −84.6 | 0.44 | 12.6 | −80.2 to −69.7 | |||
| 61–77 | 8 | 38 | −135.2 | −57.3 | 0.69 | 80.1 | −87.2 to −69.8 | |
| 120 | −130.8 | −52.4 | 0.67 | 82.5 | −87.6 to −70.4 | |||
| Diaphus garmani | 31–57 | 75 | 38 | 34.5 | −83.5 | 0.46 | 8.1 | −81.7 to −68.7 |
| 120 | 32.7 | −83.3 | 0.49 | 7.6 | −82.6 to −69.4 | |||
The y-values represent TS (dB), and the x-values the log of the standard length (cm). β indicates the 95% confidence limits of the regression slope m. Ranges of TScm at each length range are also shown.
Equations of the linear regressions plotted in Figure 5 and the ranges of standard length.
| Species | Length range (mm) | n | Frequency (kHz) | y = mx + b | TScm range (dB) | |||
|---|---|---|---|---|---|---|---|---|
| m | b | r2 | ± β | |||||
| Ceratoscopelus warmingii | 33–83 | 81 | 38 | 26.3 | −78.1 | 0.30 | 9.1 | −82.3 to −67.7 |
| 120 | 26.1 | −79.2 | 0.31 | 8.7 | −82.6 to −68.6 | |||
| Myctophum asperum | 31–48 | 31 | 38 | 45.4 | −88.6 | 0.45 | 15.9 | −79.9 to −68.8 |
| 120 | 36.3 | −84.6 | 0.44 | 12.6 | −80.2 to −69.7 | |||
| 61–77 | 8 | 38 | −135.2 | −57.3 | 0.69 | 80.1 | −87.2 to −69.8 | |
| 120 | −130.8 | −52.4 | 0.67 | 82.5 | −87.6 to −70.4 | |||
| Diaphus garmani | 31–57 | 75 | 38 | 34.5 | −83.5 | 0.46 | 8.1 | −81.7 to −68.7 |
| 120 | 32.7 | −83.3 | 0.49 | 7.6 | −82.6 to −69.4 | |||
| Species | Length range (mm) | n | Frequency (kHz) | y = mx + b | TScm range (dB) | |||
|---|---|---|---|---|---|---|---|---|
| m | b | r2 | ± β | |||||
| Ceratoscopelus warmingii | 33–83 | 81 | 38 | 26.3 | −78.1 | 0.30 | 9.1 | −82.3 to −67.7 |
| 120 | 26.1 | −79.2 | 0.31 | 8.7 | −82.6 to −68.6 | |||
| Myctophum asperum | 31–48 | 31 | 38 | 45.4 | −88.6 | 0.45 | 15.9 | −79.9 to −68.8 |
| 120 | 36.3 | −84.6 | 0.44 | 12.6 | −80.2 to −69.7 | |||
| 61–77 | 8 | 38 | −135.2 | −57.3 | 0.69 | 80.1 | −87.2 to −69.8 | |
| 120 | −130.8 | −52.4 | 0.67 | 82.5 | −87.6 to −70.4 | |||
| Diaphus garmani | 31–57 | 75 | 38 | 34.5 | −83.5 | 0.46 | 8.1 | −81.7 to −68.7 |
| 120 | 32.7 | −83.3 | 0.49 | 7.6 | −82.6 to −69.4 | |||
The y-values represent TS (dB), and the x-values the log of the standard length (cm). β indicates the 95% confidence limits of the regression slope m. Ranges of TScm at each length range are also shown.
The relationship between the tilt-averaged TS and the log of standard length (cm) of swimbladderless fish is shown in Figure 6. The equations of the linear regression shown in Figure 6, and the ranges of TScm are listed in Table 3. We selected 25 C. warmingii, 25 D. chrysorhynchus, 50 M. asperum, and 50 D. garmani from the entire length range of swimbladderless fish. TScm values were much lower in swimbladderless than in swimbladdered fish. The regression slope m was high (>30) at 38 kHz in each species, suggesting that the increase in TS is faster than that of body length. On the other hand, the regression slope was <20 at 120 kHz in each species, suggesting that the increase in TS is slower than that of body length.
Plots of TS against log of standard length (cm) for swimbladderless (a) C. warmingii, (b) M. asperum, (c) D. garmani, and (d) D. chrysorhynchus at 38 kHz (left column) and at 120 kHz (right column).
Equations of the linear regressions plotted in Figure 6 and the ranges of standard length.
| Species | Length range (mm) | n | Frequency (kHz) | y = mx + b | TScm range (dB) (average) | |||
|---|---|---|---|---|---|---|---|---|
| m | b | r2 | ± β | |||||
| Ceratoscopelus warmingii | 23–43 | 25 | 38 | 49.4 | −112.2 | 0.93 | 6.0 | −103.9 to −92.1 (−96.7) |
| 120 | 10.4 | −82.6 | 0.45 | 5.0 | −90.6 to −86.1 (−87.6) | |||
| Myctophum asperum | 18–33 | 50 | 38 | 52.7 | −108.3 | 0.98 | 2.3 | −100.5 to −75.9 (−90.4) |
| 74–86 | 120 | 17.9 | −80.9 | 0.85 | 1.9 | −85.0 to −77.1 (−82.1) | ||
| Diaphus garmani | 21–53 | 50 | 38 | 54.0 | −113.5 | 0.94 | 4.2 | −105.2 to −86.9 (−94.4) |
| 120 | 6.9 | −8.4 | 0.34 | 3.0 | −92.5 to −85.5 (−88.8) | |||
| Diaphus chrysorhynchus | 62–100 | 25 | 38 | 30.5 | −96.3 | 0.81 | 5.8 | −88.2 to −85.3 (−86.9) |
| 120 | −9.1 | −63.2 | 0.24 | 8.5 | −92.3 to −87.5 (−89.2) | |||
| Species | Length range (mm) | n | Frequency (kHz) | y = mx + b | TScm range (dB) (average) | |||
|---|---|---|---|---|---|---|---|---|
| m | b | r2 | ± β | |||||
| Ceratoscopelus warmingii | 23–43 | 25 | 38 | 49.4 | −112.2 | 0.93 | 6.0 | −103.9 to −92.1 (−96.7) |
| 120 | 10.4 | −82.6 | 0.45 | 5.0 | −90.6 to −86.1 (−87.6) | |||
| Myctophum asperum | 18–33 | 50 | 38 | 52.7 | −108.3 | 0.98 | 2.3 | −100.5 to −75.9 (−90.4) |
| 74–86 | 120 | 17.9 | −80.9 | 0.85 | 1.9 | −85.0 to −77.1 (−82.1) | ||
| Diaphus garmani | 21–53 | 50 | 38 | 54.0 | −113.5 | 0.94 | 4.2 | −105.2 to −86.9 (−94.4) |
| 120 | 6.9 | −8.4 | 0.34 | 3.0 | −92.5 to −85.5 (−88.8) | |||
| Diaphus chrysorhynchus | 62–100 | 25 | 38 | 30.5 | −96.3 | 0.81 | 5.8 | −88.2 to −85.3 (−86.9) |
| 120 | −9.1 | −63.2 | 0.24 | 8.5 | −92.3 to −87.5 (−89.2) | |||
The y-values represent TS (dB), and the x-values the log of the standard length (cm). β indicates the 95% confidence limits of the regression slope m. Ranges (and average) of TScm at each length range are also shown.
Equations of the linear regressions plotted in Figure 6 and the ranges of standard length.
| Species | Length range (mm) | n | Frequency (kHz) | y = mx + b | TScm range (dB) (average) | |||
|---|---|---|---|---|---|---|---|---|
| m | b | r2 | ± β | |||||
| Ceratoscopelus warmingii | 23–43 | 25 | 38 | 49.4 | −112.2 | 0.93 | 6.0 | −103.9 to −92.1 (−96.7) |
| 120 | 10.4 | −82.6 | 0.45 | 5.0 | −90.6 to −86.1 (−87.6) | |||
| Myctophum asperum | 18–33 | 50 | 38 | 52.7 | −108.3 | 0.98 | 2.3 | −100.5 to −75.9 (−90.4) |
| 74–86 | 120 | 17.9 | −80.9 | 0.85 | 1.9 | −85.0 to −77.1 (−82.1) | ||
| Diaphus garmani | 21–53 | 50 | 38 | 54.0 | −113.5 | 0.94 | 4.2 | −105.2 to −86.9 (−94.4) |
| 120 | 6.9 | −8.4 | 0.34 | 3.0 | −92.5 to −85.5 (−88.8) | |||
| Diaphus chrysorhynchus | 62–100 | 25 | 38 | 30.5 | −96.3 | 0.81 | 5.8 | −88.2 to −85.3 (−86.9) |
| 120 | −9.1 | −63.2 | 0.24 | 8.5 | −92.3 to −87.5 (−89.2) | |||
| Species | Length range (mm) | n | Frequency (kHz) | y = mx + b | TScm range (dB) (average) | |||
|---|---|---|---|---|---|---|---|---|
| m | b | r2 | ± β | |||||
| Ceratoscopelus warmingii | 23–43 | 25 | 38 | 49.4 | −112.2 | 0.93 | 6.0 | −103.9 to −92.1 (−96.7) |
| 120 | 10.4 | −82.6 | 0.45 | 5.0 | −90.6 to −86.1 (−87.6) | |||
| Myctophum asperum | 18–33 | 50 | 38 | 52.7 | −108.3 | 0.98 | 2.3 | −100.5 to −75.9 (−90.4) |
| 74–86 | 120 | 17.9 | −80.9 | 0.85 | 1.9 | −85.0 to −77.1 (−82.1) | ||
| Diaphus garmani | 21–53 | 50 | 38 | 54.0 | −113.5 | 0.94 | 4.2 | −105.2 to −86.9 (−94.4) |
| 120 | 6.9 | −8.4 | 0.34 | 3.0 | −92.5 to −85.5 (−88.8) | |||
| Diaphus chrysorhynchus | 62–100 | 25 | 38 | 30.5 | −96.3 | 0.81 | 5.8 | −88.2 to −85.3 (−86.9) |
| 120 | −9.1 | −63.2 | 0.24 | 8.5 | −92.3 to −87.5 (−89.2) | |||
The y-values represent TS (dB), and the x-values the log of the standard length (cm). β indicates the 95% confidence limits of the regression slope m. Ranges (and average) of TScm at each length range are also shown.
Discussion
Potential diel differences in swimbladder shape
All our fish samples were captured relatively shallow (<200 m) at night. Many myctophids undertake diel vertical migration, and this might lead to a diel difference in swimbladder volume (Kanwisher and Ebeling, 1957). However, acoustic studies of deep-water fish suggest that they maintain a constant volume or a constant mass of gas in their swimbladders during vertical migration (Vent and Pickwell, 1977; Benoit-Bird et al., 2003). A constant gas volume is needed to maintain neutral buoyancy, and many mesopelagic fish achieve this through gas exchange (D'Aoust, 1971; Suetsugu and Ohta, 2004). This suggests that swimbladder shape does not change unless there are artefact effects, e.g. rapid pressure changes caused by fast towing. Our samples were free of these effects because the sampling gear was towed as slowly as possible and live fish were selected for the swimbladder observations.
Swimbladder morphology in acoustic perspective
The C. warmingii, M. asperum, and D. garmani had inflated swimbladders at some period of their life. Although the swimbladder shape varied with species and life stage, they had common features different from other families of fish. The swimbladder length of common pelagic fish is about one-third of the standard length, swimbladder volume is from 4 to 10% of body volume, the aspect ratios range from 0.1 to 0.3, and the tilt angle is ∼5 or 6° (Capen, 1967; Furusawa, 1989). On the other hand, the swimbladder volumes of the species investigated here were <0.5% of body volume in most fish, implying that the values of TScm would be lower than that of other pelagic species. Moreover, most swimbladdered fish had short bodies and egg-shaped (i.e. low aspect ratio) swimbladders, showing a relatively broad distribution of the tilt angle (Table 1). Wider tilt-angle distributions may introduce biases for pitch-averaged values of TS estimated by the theoretical model. However, that effect would be negligible at 38 or 120 kHz, because the swimbladder lengths of the current species were too small to detect a measurable change in TS with pitch angle (Yasuma, 2004).
Unformed swimbladders were observed in juvenile C. warmingii, M. asperum, and D. garmani (Figure 2). The swimbladder of many fish species becomes physoclistous at some point in its early life history, and gas secretion does not occur until then (Powers, 1932). Our results reveal the timing of first gas production in three species (Figure 2, Table 2), likely important information because the value of TS changes critically in the presence of gas. We have no information on juvenile D. chrysorhynchus, but perhaps they too have a gas-containing swimbladder early in life, though further observation is necessary to confirm this.
All swimbladdered species showed positive allometric growth after the onset of gas secretion into the swimbladder, but in D. garmani, both swimbladdered and swimbladderless specimens were observed over a broad range of body lengths. Further, larger M. asperum showed regressive growth, and mature fish were mainly swimbladderless. The co-occurrence of swimbladdered and swimbladderless fish in a single species, in this case D. garmani, has been reported for other myctophids, e.g. Diaphus theta and Symbolophorus californiensis (Butler and Pearcy, 1972; Neighbors and Nafpaktitis, 1982). The relative growth rate (body length vs. swimbladder length) varies in many fish species (Kitajima et al., 1985; Sadayasu, 2005). However, regressive growth or atrophy of the swimbladder is specific to myctophids and a few other mesopelagic fish (Marshall, 1971; Saenger, 1989).
Although the causes of these unique features are unclear, diel vertical migration is thought to be one of the major triggers. An inflated swimbladder would be unfavourable for fish migrating vertically because the maintenance of a constant swimbladder volume throughout their vertical range would require considerable gas secretion and resorption. Therefore, their conditions may reflect species-dependent or ontogenetic changes in migratory behaviour. Many mesopelagic fish that either lack or have a small swimbladder retain their buoyancy by increasing lipid content (Marshall, 1960; Butler and Pearcy, 1972; Neighbors and Nafpaktitis, 1982).
Reliability of model estimation
Yasuma (2004) compared theoretical estimates with experimental measurements using examples of the same species and confirmed that each fish showed similar patterns of TS shift between theoretical (represented in Figure 4) and experimental results. The reliability of our theoretical estimations is supported by this observation. However, if the fish undergo a steep orientation in the field, the averaged TS, which applies the stated value of pitch-angle distribution, would have potential error, especially for swimbladderless fish. There is little information about the swimming behaviour (orientation) of myctophids. Barham (1970) observed it using a diving camera and reported that many fish have a nearly vertical orientation at night, although most are orientated in the almost horizontal by day. The pitch-angle distributions of myctophids are still unknown, so direct visual observations with a video camera are required to estimate the TS more precisely.
TS of swimbladdered fish and the potential effect of acoustic resonance
McClatchie et al. (2003) stated that deep-water fish such as macrourids and oreosomatids have small swimbladders and low values of TS. They also noted that the TS of these deep-water fish did not follow the 20 log L relationship because the swimbladder cross section grew rapidly in relation to fish length. The TScm values of other swimbladdered fish, such as gadoids and clupeoids, range from −65 to −72 dB (MacLennan and Simmonds, 1992). However, our results show that many swimbladdered fish have a low TScm (less than −75 dB), suggesting a lower TS in proportion to body length (Table 2). Additionally, the TS values of the species we examined did not follow the 20 log L relationship and increased rapidly in relation to body size (Figure 5, Table 2). These results support the suggestion of McClatchie et al. (2003) and underscore the importance of information on species-specific swimbladder condition and its growth for development of theoretical estimation of TS. There are very few reports about the TS regression in fish such as M. asperum (Figure 5), but atrophy of the inflated swimbladder occurs in many myctophids and they may have potential TS regression (Butler and Pearcy, 1972; Neighbors and Nafpaktitis, 1982; Saenger, 1989; Neighbors, 1992; Yasuma et al., 2003).
Acoustic backscatter from the swimbladder increases the effect of resonance when the swimbladder is small, in relation to acoustic wavelength (e.g. kr << 1, where k is the wave number and r the equivalent spherical radius of the gas field), and this effect becomes larger in deeper water (Capen, 1967; Love, 1978). As described above, the swimbladder size of the four species examined here is small, and these species occupy relatively deep layers, so the effect of swimbladder resonance should be considered. The acoustic backscatter cross section (σ) at 38 and 120 kHz, computed by the resonance model (Love, 1978), was normalized by the square of equivalent spherical radius r2, and plotted in relation to the equivalent spherical radius in Figure 7. Peaks of each line are the point of resonance at each depth, and the effect of resonance is negligible where the equivalent radius is sufficiently large and the σ/r2 takes an asymptotic value. At 38 kHz, the resonance would be negligible shallower than 300 m if the equivalent radius is >1 mm. However, there would be an effect of resonance deeper than 300 m if the equivalent radius is <1 mm. At 120 kHz, the resonance is negligible shallower than 300 m if the equivalent radius is >0.5 mm. Figure 8 shows the relationship between the equivalent radius of the swimbladder (log) and fish standard length, as obtained here. Among swimbladdered fish, small C. warmingii (<55 mm), small M. asperum (<40 mm), and all size classes of D. garmani contained many fish with small swimbladders (<1 mm). This suggests that they would be under the effect of resonance at a depth of 300 m (or even at 100 m) at 38 kHz. Myctophid fish live in relatively deep water, and the use of low frequencies (e.g. 38 kHz), when there is less absorption, may be appropriate to the field biomass survey. However, if the target fish school consists mainly of small fish, adequate ways of measurement, including the use of high frequencies (e.g. 120 kHz) and the use of data collected at night when the schools ascend, should be considered to preclude any effect of resonance. In contrast, differences in TS values (at 38 vs. at 120 kHz) under the effect of resonance may be helpful to other analyses, such as for school detection.
Normalized acoustic backscatter cross section σ/r2 at depths of 0, 50, 100, and 300 m computed by Love (1978) as functions of r at 38 kHz (top panel) and 120 kHz (lower panel).
Log of the swimbladder equivalent spherical radius of (a) C. warmingii, (b) M. asperum, and (c) D. garmani as a function of fish standard length. The dotted, solid, dashed, and dotted-dashed lines indicate 3, 2, 1, and 0.5 mm, respectively.
TS of swimbladderless fish
Using 11 swimbladderless species of myctophid, Yasuma (2004) determined the values of tilt-averaged TS at four frequencies (38, 70, 120, and 200 kHz) obtained by experimental measurement and the DCM and summarized the TScm values as a function of L/λ, where λ is the wavelength (Figure 9). According to that analysis, values of TScm increase rapidly until L/λ approaches ∼2 (∼7.8 cm at 38 kHz and ∼2.5 cm at 120 kHz), and then becomes asymptotic, with little fluctuation. Most swimbladderless specimens of the present species had low values of L/λ (<2) at 38 kHz, which is why the coefficients of the TS–length relationships were well above 20 and the TS increased rapidly with body growth (Figure 6, Table 3). On the other hand, the L/λ values of most fish were >2 at 120 kHz, where TScm vary about asymptotic values.
Although there is little information about the TS of swimbladderless fish (Foote, 1980a; McClatchie and Ye, 2000), Foote (1980a) reported that the TScm of a swimbladderless pelagic fish ranged from −90 to −80 dB when L/λ was >2. This is similar to our results, although some M. asperum, which have a notably larger body density, had higher values of TS. TS values of smaller fish (<7.8 cm) would be lower at 38 kHz than at 120 kHz. This may be helpful for detecting schools in the field, if the target school consists mainly of such smaller fish.
Complexity of the TS–length relationship caused by a biphasic swimbladder condition
The TS–length equations listed in Tables 2 and 3 are proposed for use in analyses of field data, and they provide a lot of the information needed for understanding the ecological structure of the deep-scattering layer in the Northwest Pacific. However, C. warmingii, M. asperum, and D. garmani have overlaps between swimbladdered and swimbladderless fish at certain size ranges (Figure 2, Tables 2 and 3), and this causes an intricacy in determining the TS of a fish in these size ranges. Especially for D. garmani, the overlap is over a wide size range from juvenile to mature, and this may preclude reliable estimation of biomass. Similar overlaps have been found in other myctophid species, such as Myctophum aurolaternatum, D. theta, and S. californiensis (Capen, 1967; Butler and Pearcy, 1972; Neighbors, 1992). Neighbors (1992) found different conditions of the swimbladder in a similar size class of S. californiensis and suggested that the difference was attributable to the depth of capture. Butler and Pearcy (1972) also found a biphasic swimbladder condition in S. californiensis and suggested the possibility of regional, seasonal, or sex-related differences. We collected our samples under different environmental conditions and divided them based only on species and body size. Therefore, we do not know what environmental factors contribute to the biphasic swimbladder condition. Further work may, however, allow us to evaluate swimbladder condition and determine a better TS–length equation, by typifying the swimbladder condition against other variables such as season of the year, sampling site, sampling depth, or sampling time.
Acknowledgements
We thank the captains and crews of the RV “Hakuho Maru”, the RV “Tansei Maru”, and the RV “Wakataka Maru” for their cooperation in fish sampling. The work was supported by a grant from the Fisheries Research Agency of Japan, and a Grant-in-Aid for Scientific Research (No. 14560142) from the Japan Society for the Promotion of Science.
