Session 6: behaviour and physiology with respect to target strength

Rapp. P.-v. Rcun. Cons. int. Explor. Mer, 189: 233—244. 1990

Swimbladder “behaviour” and target strength

J. H. S. Blaxter and R. S. Batty

Blaxter, J.H .S., and Batty, R.S. 1990. Swimbladder "behaviour” and target strength. - Rapp. P.-v. Réun. Cons. int. Explor. Mer, 189: 233-244.

The target strength (TS) of fish is higher when a swimbladder is present. TS depends on the swimbladder volume which increases with fish size and varies with depth. Changes of volume occur during vertical migration; the volume then remains rather stable in physostomes apart from slow losses of gas by diffusion, but physoclists secrete or absorb gas, so tending to restore the original volume. Such adaptation to a depth change is slow compared with the speed of movement of vertical migrants whose TS will change at dusk and dawn. TS also varies with the orientation of the fish to the echo-sounding beam and may vary with its swimming speed. The highest TS is found with the head tilted down 5-10°. The swimbladder axis is, however, tilted up by the same amount so that it lies normal to the beam. In many species there are day:night differences in activity, swimming speed, tilt angle, density, and vertical stacking, all affecting TS. It is unfortunate that TS depends on a labile organ with a role in buoyancy and posture.

J. H. S. Blaxter and R. S. Batty: Dunstaffnage Marine Laboratory, P. O. Box 3, Oban, Argyll, Scotland.

(3) physoclists which have a closed swimbladder, a gas Introduction gland for gas secretion, and an occlusible oval for Since the bodies of fish have an acoustic impedance gas resorption; close to that of water as much as 90 % of the backscat- (4) some bathypelagic species which have a swimblad­ tering of sound from echo sounders or sonars depends der filled with oil or invested with fat. on gas-filled structures such as the swimbladder. The extent of backscattering also depends, amongst other In the past it has been supposed that the swimbladder’s things, on the cross-sectional area of the gas phase main role is to confer neutral buoyancy on the fish and perpendicular to the incident acoustic beam, and it so mechanisms have evolved to maintain its volume at would be enhanced if the gas-filled structure were of a some optimum value, with a clear requirement for a size and shape to resonate at the frequency of enson- compensation mechanism to allow the fish to make ification. vertical movements involving changes of hydrostatic Although the swimbladder is the main gas-filled pressure. A neat solution to this problem would seem to structure, gas could be present in the gut as a result of be a non-compressible flotation organ such as the squa- the activity of micro-organisms while in all clupeoids lene-filled liver of or the oil-filled or fat-invested there are gas-filled paired otic bullae within the skull. It swimbladder of some bathypelagic species (Marshall, is likely that the volumes concerned will be small com­ 1960; Butler and Pearcy, 1972) or to reduce ossification pared with the swimbladder. and increase the water content of the flesh (Denton and For our purpose fish can be grouped into four cate­ Marshall, 1958; Blaxter el al., 1971) or to increase the gories: oil content of the bones (Bone, 1972; Lee et al., 1975). The swimbladder may, however, have other roles to (1) those with no swimbladder, especially , sand- play in hearing and sound production (Blaxter and Tyt- , Ammodytes spp., and the Atlantic ler, 1978) that require it to be gas-filled. (Scomber scombrus) ; Most physostomes obtain gas by swallowing air at the (2) physostomes which have an open swimbladder with surface. During a subsequent descent the swimbladder a duct or ducts to the exterior and which usually contracts, and it is unlikely that a fish will be neutrally lack a gas secretion mechanism, e.g., clupeoids, buoyant at any depth unless it has positive buoyancy at salmonids, and cyprinids; the surface. There is no evidence for such a phenom-

233 Table 1. Swimbladder volumes.

Species Stage/size Volumes as % of fish weight Reference ± s.d. (n)

Cod 13-50 cm 3.6±0.46 (11) Hawkins (1977) 25-50 cm 4.5-5.4 Harden Jones and Scholes (1985) Pollack 32-45 cm 2.8±0.33 (13) Foote (1985a) Whiting 24 g, 62 g 4.4, 2.8 Alexander (1959b) Pout 69 g 4.9 Alexander (1959b) 9-25 g 4.1a±0.6 (16) Brawn (1962) Herring 45-200 g 4.3-2.31’ Ona (1984a) Herring Larvae 0.2-1.6 (13) Blaxter and Batty (1984) (see Fig. 1) Juveniles 1 Adults J 1.5-5 (46) Spawners 0(6)

“4.2 % expressed as % of fish volume. hsb vol. = 0.017 wt + 1.157 (226).

enon although some additional buoyancy may be ob­ Swimbladder volume tained from a high tissue fat content. During an ascent there should be no excess gas and no need therefore to There is abundant evidence, which will not be reviewed void gas from the swimbladder. Why some species such here, that the target strength of fish is related to their as the herring do release gas (Sundnes and Bratland. size. Furthermore, size-for-size fish without swimblad- 1972) is something of a mystery. Nevertheless all clupe­ ders such as mackerel and sandeels have lower target oids have one or more ducts from the swimbladder to strengths (Foote, 1980a; Armstrong and Edwards, the exterior (Whitehead and Blaxter, 1989). While the 1985). Implicit in these findings is a relationship be­ pneumatic duct from the gut can be seen as the route for tween fish size, swimbladder volume, and target swallowed gas to enter the swimbladder, the anal duct strength. In order to provide neutral buoyancy the seems to involve gas release to the exterior. A few swimbladder should occupy 5 % of the body volume in a physostomes such as some eels (Fänge, 1983; Kleckner, fully marine fish and 7% in a (Harden 1980) and goldfish Carassius auratus (Overfield and Jones and Marshall, 1953). Although many of their data Kylstra, 1971) can secrete gas. and some of Alexander's (1959a. b) support this as­ The physoclists are much more constrained in their sertion. other data (Horn, 1975; Brooks. 1977) do not. vertical movements. A descent presents no problems There is also considerable evidence from commercial that are different from a physostome’s, i.e., an increas­ marine species recently studied that: ing negative buoyancy. If a physoclist is adapted to a ( 1 ) swimbladder volumes are often much less than 5 % ; particular depth, as it ascends from that depth the swim­ (2) there is a wide variation in swimbladder volume in a bladder expands. Gas is then resorbed, but if the ascent given fish population; is not controlled the swimbladder may rupture. Adapta­ (3) there are effects of age and spawning condition. tions are to be found that increase the depth range by improving the gas secretion/resorption mechanisms. In Some data are given in Table 1 and Figure 1. particular the rete of the gas gland may be elongated in There is other less direct evidence that swimbladder deep-sea species (Marshall, I960, 1972; Horn, 1975; volume might be very variable in terms of its impor­ Kleckner, 1980). tance in target-strength measurement. Sand and Haw­ It is unfortunate that the target strength of fish is kins (1973) found that the resonance frequencies of cod largely determined by such a labile organ. The volume (Gadus morhua) swimbladders were highly variable at of the swimbladder depends on the size of the fish and the depth of adaptation, being 100% to 700% of the the extent of inflation, which in turn depends on the resonance frequency of a free gas bubble at the adapta­ recent depth “history” of the fish. The cross-sectional tion depth. area depends on the shape of the swimbladder and the Other factors may be related to swimbladder volume, angle of tilt of the fish to the horizontal. The resonance in particular the fat content of the fish. Fat content frequency of the swimbladder depends on its shape, varies with gonad maturation state, season, or feeding wall thickness, any differential internal gas pressure, conditions (Love. 1970); in herring (Clupea harengus) and possibly its mode of attachment to the body wall. there is an inverse relationship between fat content and These problems will be considered in the following swimbladder volume (Brawn, 1969; Ona, 1984a, Fig. 2) pages. so that swimbladder volume (and target strength) can

234 Figure 1. Swimbladder volume related to size of herring (redrawn from Blaxter and Batty, 1984).

4-

*— 001 01 10 100 9 i---- 1— i— i— i— — 1---- 1------1-- 1— I------7 10 15 20 25 30 cm Fish size

Figure 2. Swimbladder volume as % body weight related to oil content as % body weight of herring, x Atlantic herring and 5 O Pacific herring, from Brawn (1969); oo 0 Norwegian herring, from Ona (1984a). I?

3 »•V 2

0 510 15 20 25

Oil content (%)

Table 2. Swimbladder pressure differentials.

Species Pressure differential in cm H:0: Reference + above ambient — below ambient

Cod + <1.0-2.4a Sand and Hawkins (1974) Cod - 600-900b Sundnes and Gytre (1972) Herring + 15 Brawn (1962) Herring + 17.4± 10.9 Blaxter and Batty (1984) Sockeye + 0.3± 7.5 Harvey el al. (1968) Pinfish + 3.6 McCutcheon (1958) Most cyprinids + 27-41 Alexander (1959a) Bream + 147 Alexander (1959a) Roach + 95 Alexander (1959a) Rudd + 83 Alexander (1959a)

“Even if internal pressure is doubled by gas injection, internal excess pressure rapidly falls to +6.2 cm H;0. '’Held for 15-20 min after increasing pressure from 1 to 11 ATA.

2 3 5 be expected to vary seasonally. Some of the loss of Clupea harengus buoyancy of herring with a smaller swimbladder will then be compensated for by the increased fat content. Brawn (1969) equated the upthrust of 1 ml of gas with

10.7 ml of oil so that very high fat levels are required to pneumatic compensate for small reductions in swimbladder vol­ duct ume.The effect of pressure on swimbladder volume will be considered later. Suffice it to say that swimbladders are usually compliant. Some measurements (Table 2) have shown small excess pressures of a few cm of H ,0 above ambient. Sundnes and Gytre (1972), however, found quite large negative pressure, equivalent to nearly 1 m of H:0 held for 15-20 min when cod were subjected to pressure increases from 1 ATA to 5-11 Opisthopterus tardoore ATA. This is an interesting result because it suggests that a cod can increase the flotation effect of its swim­ bladder at depth, presumably by expansion of the body cavity using the lateral muscles. caudal sac

Swimbladder resonance If the swimbladder acted as an ideal spherical gas bub­ ble, its resonance frequency fra l/a x P1'2 where a is the radius of the bubble and P is the hydrostatic pressure (Cushing. 1973; Hawkins, 1977). Weston (quoted by Cushing, 1973) gives useful theoretical data on reso­ nance frequencies based on the equation: fr = 8PI/2 L tongue where fr is kHz, L is the fish body length in cm, and P the hydrostatic pressure in atmospheres (see Table 3). The swimbladders of commercial fish should thus res­ Figure 3. Swimbladders of different clupeoids (scale bars 1 cm onate at 80—2000 Hz (far lower than the frequency of long) (redrawn from Whitehead and Blaxter, 1989). commercial echo sounders), those of fish from the deep scattering layer at 1 — 15 kHz, and those of fish larvae at 10-40 kHz (Cushing, 1973). wall may be constrained by surrounding tissue so damp­ The resonance frequency also depends on the shape ing resonance, or it may contain gas at a different static of the swimbladder which is often elongated, ranging pressure from the external hydrostatic pressure (see from a prolate spheroid to a cylinder. Different species above). may have different thicknesses of swimbladder wall, In practical terms it is clear that larger fish have larger muscle attachments, constrictions between chambers, swimbladders and therefore lower resonance frequen­ or attachments to the dorsal wall of the body cavity, that cies. Løvik and Hovem (1979), for example, have re­ might influence resonance. As an example some of the lated the resonance frequency of the swimbladder to different shapes and attachments in clupeoid swimblad­ fish length in six species (Fig. 4). ders are shown in Figure 3. In addition the swimbladder The effect of changing depth on swimbladder volume, and therefore on resonance frequency, depends on the rate of adaptation to depth change by the swimbladder. Table 3. Resonance frequencies (kHz) of swimbladders of fish Physostomes will not be able to compensate (except by of different sizes at different depths (from Weston, in Cushing, release or slow diffusion of gas) while physoclists will 1973). adapt depending on their ability to secrete or resorb Depth (m) 10 30 50 100 gas. If the mass of gas remains constant (i.e., there is no secretion or absorption) then: fra P 5/6. If the volume Length of fish (cm) remains constant as the result of secretion or absorption then, after a period of adaptation: fra P 1/2. 0.5 16.0 22.4 35.5 49.6 1.0 8.0 11.2 17.6 24.8 A number of workers (e.g., Sand and Hawkins, 1973; 10.0 0.8 1.12 1.76 2.48 Løvik and Hovem, 1979) have measured resonance fre­ 30.0 0.27 0.37 0.58 0.83 quency changes after imposing pressure changes on cod, 50.0 0.16 0.22 0.35 0.49 saithe (Pollachius virens), herring, and (Sprattus 100.0 0.08 0.11 0.18 0.25 sprattus). In general the above laws are followed, but

236 Figure 4. Swimbladder resonance frequency related to length in six □ cod species (redrawn from Løvik and X coalfish Hovem, 1979). A herring O pollack N X V sprat • u>N 4>C 3 cr Ay \X X a> u oC c o X X'- 0) OC

XL

0 10 20 3 0 4 0 Length (cm) there are interesting complexities in the responses to is angled upwards at the anterior end (Fig. 5; Table 4). which the reader should refer in the original publi­ This angle can be quite steep, for example 18° in the cations. deep-bodied menhaden (Brevoortia tyrannus). This has implications for providing gas for the otic bulla in clupe­ oids during a descent into deep water (Blaxter, 1981). There is abundant evidence that the aspect of the fish Tilt angles affects the target strength. Flarden Jones and Pearce The sound energy reflected by a swimbladder depends ( 1958) found the highest target strength from the lateral on the orientation and extension, relative to wave­ aspect of perch (Perea fluviatilis). According to Foote length, of the swimbladder surface, namely the acoustic ( 1980b) theoretical calculations made on the cod predict cross-section. This will depend on size and shape of the that the highest target strength from the dorsal aspect swimbladder as well as on the aspect (extent of tilt or should be obtained when the major scattering compo­ pitch and roll) of the fish. nent of the fish is perpendicular (tilt or pitch angle is It should not be assumed that the swimbladder neces­ zero) to the sound. The effect of tilt on target strength is sarily lies horizontally within the fish. In some species it more extreme with high-frequency ensonification

Figure 5. Swimbladder angles in four species with total fish length in cm (from Blaxter, 1981; A.D. Flawkins, pers. comm.).

237 Table 4. Swimbladder angles in relation to longitudinal body axis of fish (from x radiographs).

Species Length (cm) Swimbladder angle ± s.d. (n) Reference

Herring 16-17 7.6°±1.5 (13) Blaxter (1981) Menhaden 13-18 18.0°±1.5 (10) Blaxter (1981) Saithe 15-17 7.0°±0.8 (10) Blaxter (1981) Cod 35 5°—10° Sand and Hawkins (1973) Cod 25-30 8° (3) A.D. Hawkins (pers. comm.) Whiting c. 25 5° A. D. Hawkins (pers. comm.) Poor cod 12-15 5° Denton and Marshall (1958)

(Johannesson and Mitson, 1983). Nakken and Olsen of tilt angles of commercial fish in the sea and in cages, (1977) reported the highest target strength of saithe at made as part of target-strength measurements. These tilt angles of - 4 to —11° (i.e., head down), and Foote are summarized in Table 5. There is evidence both of a (1985a) found similar results for pollack. With the angle wide scatter of tilt angles under all conditions (from the of the swimbladder axis lying at about 7° to the longitu­ standard deviations) and a tendency for mean tilt angles dinal axis of the fish (Fig. 6) this would make the swim­ to be positive and larger at night (i.e., the fish tend to be bladder near to the horizontal and so normal to the head-up). This may result from the fish's being nega­ incident sound. Nakken and Olsen also found that the tively buoyant and less active at night and so requiring a angle of roll had a marked effect on the target strength head-up posture to obtain a lift and so maintain depth of cod above about 30°. Angles of roll up to 40°, how­ by slow swimming. It is also possible that the downwell- ever, had little effect on the target strength of saithe and ing light is insufficient for the dorsal light reaction to herring. operate and the fish are thus disorientated. There is some evidence that fish dive in front of There are few observations of changes in tilt angle boats or midwater trawls. This would increase after a vertical migration. Olsen (1976) reported in­ the tilt angles and reduce the target strength. There is stances of swimming at tilt angles of +45° to +60° also considerable evidence of herring lying or swimming for 6 h after being lowered from 5 to 12 m in a cage and at a range of tilt angles at night (Radakov and Solovyev, a trout (Salmo trutta) lowered from 6 to 22 m with a tilt 1959; Zaitsev and Radakov, I960). Barham (1971) ob­ angle of +5 to +10°. served a number of species of bathypelagic fish from submersibles and found high proportions of myctophids at tilt angles as great as ±90°. Many of these myctophids Swimming have fat-invested swimbladders; they are near neutral buoyancy, and can probably maintain depth by jetting The effect of fish swimming on target strength has not respiratory current water through the opercular open­ been adequately studied. Nakken and Olsen (1977) ing. found a correlation between target strength and tail- There are also extensive photographic observations beat cycle of swimming cod which suggests that results on dead fish may sometimes be suspect. Foote (1985b), however, concluded from theoretical considerations that swimming would not affect the target strength of pollack and considered that the use of restrained fish in such experiments could lead to spurious results. A fur­ ther complication is that swimming and tilt angle are also likely to be connected since slow-swimming fish may depend on some degree of tilt to give hydrody­ a - 2 1 -r namic lift from propulsive thrust produced by the body. It has been found that Atlantic mackerel tilt their bodies with head up at speeds below 0.8 body length/s (He and S "25- Wardle, 1986). The maximum recorded angle of attack head up “ -29- head down was 27° in a 32 cm long fish swimming at 0.45 body 0) o> -33: length/s. I -41-

40 20 0 20 4 0 Tilt a n g le ° Vertical migration and day:night effects Figure 6. Above: Swimbladder angle in saithe; 17-cm total length (from Blaxter, 1981 ). Below: Target strength in relation Since swimbladders are usually compliant, for example to tilt angle of saithe (from Nakken and Olsen, 1977). in cod (Sand and Hawkins, 1973) in charr (Salmo al-

238 Table 5. Tilt angle of fish under different conditions; adapted from Foote and Ona (1985). References without dates not seen in original. Negative values indicate head below the horizontal.

Species Depth Location Tilt angle degrees Reference (m) (± s.d.) Day Night

Saithe 4 Large pen —0.9(±5.4) - Foote and Ona (1985) Capelin 44 Sea 3.3(118.4) - Carscadden and Miller Herring 2-5 Large pen —3.2(± 13.6) 3.8(±6.0) Beltestad Herring 20 Sea —3.4(± 10.3) 12.0( ±23.5) Buerkle

Herring 2.5 Small cage 2.9(±14.2) - Foote —3.1(± 11.5) -

Herring 1.5 Small pen —3.9(± 12.8) - Ona (1984b) 4 Large cage —0.2(±11.9) - 30 Large cage 8.1(± 16.9) - Mackerel 717.5 Cage 8.8 18.1“ Edwards et al. (1984) Cage 8.3 12.3°

•‘Tilt angle significantly higher during the night (PcO.Ol). pinus) (Sundnes and Sand, 1975) and in herring (Ona, target strength as a result of the changing volume of the 1984a; Blaxter and Batty, 1984), they will change vol­ swimbladder and a change in tilt angles. Because there ume roughly in relation to Boyle’s law when the fish are day:night differences in tilt angles, a diel cycle of change depth in the water. There is little good evidence vertical migration with combined depth and light effects that physostomes, apart from the eels Anguilla anguilla is likely to complicate the estimation of biomass in and Conger conger which have a gas gland (Fänge. surveys run over a 24-h period. 1983), and possibly charr (Sundnes and Sand, 1975), is a widespread phenomenon can secrete gas; they are likely therefore to become (Woodhead, 1966). Generally fish move away from the increasingly negatively buoyant as they descend. Physo­ seabed at dusk and move back towards the seabed at clists secrete or resorb gas in an attempt to compensate dawn. The amplitude of the vertical movement tends to for any depth change. be much greater in physostomes like the clupeoids than A number of workers have shown changes in target in physoclists like the gadoids (Table 6). Clupeoids of­ strength after a natural or enforced vertical migration. ten come near the surface at night (Blaxter and Holli­ Olsen (1976) found a fall in target strength of physosto- day, 1963; Blaxter and Hunter, 1982), whereas cod and matous trout and physoclistous saithe when lowered in a haddock (Melanogrammus aeglefinus) move over cage. It is not certain how much this change was due to smaller amplitudes near the seabed (Ellis, 1958; Beam­ compression of the swimbladder and how much to a ish, 1966). Only the saithe has been reported to make change in tilt angle. Edwards and Armstrong (1983a) rather wide-amplitude vertical migrations of 100 m or found that the target strength of herring fell by 2 -3 dB so, from about 160 m to 60 m, but not to the surface in three out of four experiments after lowering them in a (Schmidt, 1955). In his published echotraces an ascent net cage from 17.5 to 47.5 m. A similar fall did not of 50 m (110 to 60 m) can be seen in 1 h at dusk and a occur with mackerel, which have no swimbladder. The descent of 40 m (80 to 120 m) in 1 h at dawn, a pressure tilt angle was not measured in either species. decrease of 41% and a pressure increase of 44% Edwards and Armstrong (1983a) also found that the respectively. target strength of caged herring varied over the 24-h period, being generally lower at night by 2 -3 dB. Tray- nor and Williamson (1983) reported that the target Control of swimbladder volume strength of walleye ( Theragra chalcogramma) in the eastern Bering Sea was about 3 dB lower by night The ability of clupeoids to make extensive diel vertical than by day (for a given depth). Edwards and Arm­ migrations depends on their physostomatous character. strong (1983b) also found that the target strength of There is no strong evidence that they overfill the swim­ caged mackerel decreased by 4 -5 dB at night com­ bladder when swallowing air at the surface nor that they pared with day but were not able to relate this to a can secrete or obtain gas from other sources such as gut behavioural factor at the time. Edwards et al. (1984) bacteria at depth (Brawn, 1962; Fahlen, 1967; Sundnes later found a higher tilt angle of mackerel at night and Bratland, 1972; Blaxter etal., 1979; Blaxter and (Table 5). Batty, 1984). At depth they are therefore negatively A change of depth may have a substantial effect on buoyant although a high fat content may reduce the

239 Table 6. Reported maximum vertical excursions by fish and time required to adapt to neutral buoyancy using Harden Jones and Scholes' (1985) gas secretion/absorption data.

Species Diel change % pressure Time required Reference in depth change to adapt at 10°C

Cod 203 m -> 148 m - 26% 1.27 h Ellis (1956) 148 m —» 203 m + 35% 55 h Cod 190 m -» 139 m - 26% 1.25 h Beamish (1966) 139 m —> 190 m -I- 34 % 51 h Cod 128 m -» 108 m - 14% 0.67 h Beamish (1966) 108 m —» 128 m + 17% 20 h Haddock 170 m —» 110 m - 33% 1.7 hh Beamish (1966) 110 m —» 170 m + 50% 60 hb Saithe 160 m —» 60 m - 59% 3.75 hb Schmidt (1955) 60 m —» 160 m + 143% 100 h1’ Perch 20 m —» 8 m ‘ 1 10 m —» 2 m" J - 40% 8 h Harden Jones (1952)

"Hypothetical examples. ’’Assuming gas secretion and absorption same as cod.

extent of negative buoyancy (see Fig. 2). The target o access to surface strength should then approximate to the 5/6 power law • 7 days at 17m with depth, and any contravention of this law should be 0-2 caused by behavioural effects such as changing tilt an­ gles with depth. If fish such as herring remain at depth another factor comes into play; gas is then lost by diffusion through the swimbladder wall. The partial pressure of the swimblad­ der gases is much higher than that of the surrounding -o 0-1 tissue and so gas loss occurs with relative rates of diffu­ sion of CO:, O,, and N2 in the ratio 1:1/40:1/80. This diffusion is reduced by guanine depositions in the swim­ bladder wall. Blaxter and Batty (1984) found that gas loss was substantial in larvae and juveniles up to about 12 cm in length. For example, larvae lost all the gas within 5 h at 3.8 ATA while the swimbladders of juve­ 0 1 2 3 4 5 6 niles about 7 cm long had emptied after 7 days in a cage Weight (g) at 2.7 ATA (17-m depth). Edwards and Armstrong (1983b) found a large progressive fall in target strength -26 of these 7 cm long herring during 6 days of the same experiment (Fig. 7). Loss of gas from fish larvae seems to be so high that (Engraulis mordax) and menhaden (Brevoortia patronus) larvae refill their swimbladders nightly (Hunter and Sanchez, 1976; Hoss and Phonlor, 1984). Since physostomes are not usually buoyant at depth, it seems unlikely that they should have excess gas in the swimbladder requiring release during an ascent. It is surprising to find that herring, for example, are known -38- to release gas when ascending (Sundnes and Bratland, 2 3 54 6 1972; Thorne and Thomas, 1990). Such a release on a large scale, with gas bubbles ascending rapidly to the Days surface (and expanding), could play havoc with biomass Figure 7. Above: Changes in swimbladder volume of herring estimates.1 with access to the surface or held at 17-m depth in a cage (from Blaxter and Batty, 1984). Below: The change in target strength of the same fish held at 17 m (from Edwards and Armstrong, 'See note at end of references added in proof. 1983b).

240 Table 7. Gas secretion and resorption rates (from Tytler and Blaxter, 1973; Fänge, 1983; and Harden Jones and Scholes, 1985).

Species Secretion ml (STP)/kg/h Resorption ml (STP)/kg/h Remarks

Cod 1.2-6.6 8.4-92.4 Induced by pressure changes at 0-17°C; secretion temperature-dependent; resorption pressure-dependent Saithe 1.67-2.50 7.80 Induced by pressure changes at 9—13 °C Sunfish 1.36-3.0 - Induced by deflation of swimbladder at (Lepomis macrochirus) 12-32 °C

Eel 0.28 - Physostome, 18-20°C (Anguilla anguilla) Goldfish 0.18-0.48 — Physostome, induced by deflation of swimbladder at 29 °C

It is possible that release of gas in this way is an the same time. As gas resorption is pressure-dependent anti-predator device; it certainly cannot enhance the in cod the percentage fall in pressure which would be rate of ascent. Other species such as konakee and sock- “safe" for cod should be greater at increased depths. eye salmon (both forms of Oncorhynchus nerka) release Cod should thus be able to make considerably larger gas as they descend (Harvey et al., 1968) with an aver­ amplitude ascents in deep water than near the surface age excess pressure of 38 cm H:0 being required to and remain near neutral buoyancy. force gas from the swimbladder. Such excess pressure is Some evidence for adaptation of the swimbladder presumably achieved by contraction of the swimbladder after vertical migration is shown in Table 8 using buoy­ muscles. There were average gas losses of 23-34% of ancy and resonance frequency measurements. Although the swimbladder volume in these species. Gas release such adaptations undoubtedly take place, the time scale on descent could be a different sort of anti-predator of vertical migration suggests that physoclistous fish are device, allowing the fish to move down more rapidly. likely to be adapted only at the top of their depth range Gas secretion and absorption rates are of importance (Alexander, 1966; Blaxter and Tytler, 1978; Harden in allowing physoclists to adapt to changes of pressure Jones and Scholes, 1985). The estimated times for dif­ and determine their ability to withstand falls of pressure ferent species to adapt their buoyancy after observed that might cause the swimbladder to burst. Tytler and vertical migrations are shown in Table 6. Harden Jones Blaxter (1973) showed in cod, haddock, saithe, and and Scholes (1985) state that their laboratory observa­ whiting ( merlangus) that the swimbladder tions could be reconciled with the view that cod rest on ruptured if the pressure was suddenly reduced by 1/2 to the bottom by day with only partially inflated swimblad­ 1/4, i.e. from 1 ATA to 0.5—0.25 ATA. ders. At dusk they swim up without restriction to a Gas secretion and resorption rates for various species depth where they are neutrally buoyant. Carey and are given in Table 7. In general resorption is faster than Robinson (1981) also reported that swordfish (Xiphias secretion. Harden Jones and Scholes (1985) looked in gladias) appear to maintain buoyancy only at the top of detail at the cod over a wide range of pressures from 1.2 their vertical range. They have been observed from to 7.5 ATA and at temperatures from 0 to 17 °C. Gas submersibles lying on the seabed and can apparently secretion rates increased over fivefold between 0 and ascend from a depth of 100 m to the surface, where they 17°C but increased only slightly with pressure. Gas have neutral buoyancy, in less than 5 min. The rather resorption rates were not temperature-dependent but small vertical range of gadoids reported by Ellis (1956) increased markedly with pressure by a factor of ten and Beamish (1966) certainly supports the view that times between 1.5 and 7.0 ATA. they are severely constrained by their inability to resorb The risk for a physoclist is to ascend so far and so fast gas quickly enough. Even the wider amplitude move­ that the swimbladder bursts. Decompression schedules ments of saithe (Schmidt, 1951) seem to be taking place for cod and saithe show that they can withstand sequen­ within the theoretical limitations of the species. Even if tial halving of the ambient pressure every 5 h (Tytler they are adapted and neutrally buoyant at the night­ and Blaxter, 1973). Such rapid ascents are improbable time depth the gas secretion rates will never allow them in nature since highly buoyant fish might lose control of to maintain neutral buoyancy during the dawn descent. their ascent. While Tytler and Blaxter (1973) found that They might, however, be able to secrete gas at the cod became neutrally buoyant in 5 h after a sudden daytime depth to bring themselves to neutral buoyancy halving of the ambient pressure, Harden Jones and near the end of the day, if the amplitude of the descent Scholes (1985) give a value of 176 min for cod. In 1 h a (and the percentage increase in pressure) has not been cod should be able to withstand an ascent involving a too great. The most likely scenario is that there is a lag 21 % fall in pressure and maintain neutral buoyancy at in the adjustment of buoyancy in physoclists since the

16 Rapports et Procès-Verbaux 241 Table 8. Evidence from buoyancy and resonance frequencies for adaptation of the swimbladder after vertical migration.

Species Conditions Time to restore resonance Reference frequency (RF)/neutral buoyancy (NB) or rate of vertical migration to maintain NB

Cod 15 - 8 m 30 min (RF) Sand and Hawkins (1973) Cod ( ) ■ 6 m Saithe 4 —> 56 m 12-24 h (RF) Løvik and Hovem (1979) Saithe Ascent 3.2 m/h (NB) Ross (1979) Cod, saithe 1 —* 12 m 24 h (NB) Tytler and Blaxter (1973) Cod, saithe 1 -»• 33 m 48 + h (NB) Tytler and Blaxter (1973)

Cod, saithe 12 —» 1 m 5 h (NB) Tytler and Blaxter (1973) Cod Ascent NB with 21 % pressure reduction/h Harden Jones and Scholes (1985) Descent NB at 1 m/h Harden Jones and Scholes (1985)

Tilapia Juveniles • 33 m A few min at 22°C (NB) Caulton and Hill (1973) Large adults ■ 11.5 m 4 -7 days at 22°C (NB) Caulton and Hill (1973) Large adults •21m 3 days at 30°C (NB) Caulton and Hill (1975) Haplochromis livingstonii • 10 m 48-60 h (NB) Ribbink and Hill (1979) H. polystigma • 10 m 48-96 h (NB) Ribbink and Hill (1979)

rates of vertical migration and the amplitude of the There appears to be an element of population conser­ movements are too great for gas secretion and resorp­ vation of swimbladder volume. Both physostomes and tion to maintain the volume of the swimbladder con­ physoclists in the same conditions show a wide range of stant. On the assumption that vertical migration has swimbladder volumes. This may result, for example, adaptive value, this lag actually allows greater ampli­ from individual variations of fat content or motivation tude of vertical migration to take place. to adjust buoyancy, and from different gas secretion and absorption rates. This may tend to increase the variance of target-strength measurements but reduce the effect of changing behaviour. Conclusions The biological evidence suggests the following final Although swimbladder volume seems to be paramount conclusions: in determining target strength, many authors have con­ cluded that tilt angle and other behaviour also play a (1) The ubiquitous phenomena of diel vertical migra­ major part in determining target strength by changing tion mean that acoustic surveys on fish with swim­ the acoustic cross-section of the fish. Behaviour may bladders cannot be carried on by day and night also have a serious effect on the accuracy of biomass without a sophisticated (and as yet unavailable) cor­ estimates if there are shadowing effects when the fish rection for target-strength changes during the verti­ are stacked in the water column. cal migration cycle, with an appropriate allowance The use of fish held in acoustically transparent cages (in physoclists) for gas secretion or resorption. for estimating target strength is open to criticism be­ (2) Daytime acoustic surveys are unsatisfactory if the cause of the effect of handling, confinement, tidal cur­ fish are close to the seabed. Night-time surveys rents, and flash photography on swimming speeds, rates might seem to be more satisfactory since the fish are of turning, tilt angles, and vertical stacking. at the top of the vertical migration cycle, and swim­ Diel changes in vertical distribution and behaviour bladder volume is likely to be at its maximum and must be considered in relation to the physoclistous or the fish nearest to neutral buoyancy. On the other physostomatous nature of the species, or whether the hand, activity is known to be lower at night and swimbladder is absent. In some conditions species such there is more chance that the fish adopt head-up as smaller saithe (Schmidt, 1955), haddock (Beamish, postures (increasing the tilt angle) to compensate 1966b) and cod (Konstantinov, 1968) may make a re­ for negative buoyancy. verse migration at night and move to the bottom, per­ (3) More information is required on the relationship haps to feed on benthos. between buoyancy and tilt angle and on target-

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