12
Fisheries Research, 8 (1990) 323-334 323 Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands Age Determination in Squid using Statolith Growth Increments P.G. RODHOUSE and E.M.C. HATFIELD Marine Life Sciences Division, British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET (Gt. Britain) (Accepted for publication 19 April 1988 ) ABSTRACT Rodhouse, P.G. and Hatfield, E.M.C., 1990. Age determination in squid using statolith growth increments. Fish. Res., 8: 323-334. Growth increments have been reported to occur in the squid beak, radula, gladius and statolith. Of these, the statolith, which is part of the organ responsible for detection of linear and angular acceleration, has proved most promising for age determination. Growth increments in the stato- lith are formed from aragonite crystals in an organic matrix. They are best viewed after sectioning the statolith or after decalcification in weak acid. The statolith grows in concert with the rest of the squid. Experiments with squid in which chemical markers have been incorporated at a known time in the statolith, and experiments with cultured squid of known age, appear to confirm the hypothesis that growth increments in the statolith are laid down daily. Increments are produced in the laboratory in the absence of tidal, feeding or temperature cycles, which suggests that there is a firmly entrained endogenous circadian rhythm associated with their formation. However, the possibility that increment formation can be disrupted by environmental factors, or that rings in the statolith are produced coincidentally at the rate of approximately one per day, should not be fully discounted without further experimental corroboration. Data on squid age, derived from growth increments in the statolith, clearly have value in fisheries investigations, but they should be treated with caution until they have been validated. INTRODUCTION Increasing recognition of the considerable commercial potential of cephal- opod stocks worldwide {Worms, 1983; Rathjen and Voss, 1987) has highlighted the necessity for effective management of the fishieries for these molluscs. The requirement for information on growth rate and life span, to support studies of population biology, has recently led cephalopod biologists to focus attention on the problem of assessing age in squid. Apparent growth increments have been found in the squid beak (Tinbergen and Verwey, 1945; Clarke, 1965), the radula (Wirz, 1963 ), the gladius (Spratt, 1978) and were first described in the statolith by Clarke (1966). Increments 0165-7836/90/$03.50 © 1990 Elsevier Science Publishers B.V.

Age determination in squid using statolith growth increments

Embed Size (px)

Citation preview

Page 1: Age determination in squid using statolith growth increments

Fisheries Research, 8 (1990) 323-334 323 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

Age Determination in Squid using Statolith Growth Increments

P.G. RODHOUSE and E.M.C. HATFIELD

Marine Life Sciences Division, British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET (Gt. Britain)

(Accepted for publication 19 April 1988 )

ABSTRACT

Rodhouse, P.G. and Hatfield, E.M.C., 1990. Age determination in squid using statolith growth increments. Fish. Res., 8: 323-334.

Growth increments have been reported to occur in the squid beak, radula, gladius and statolith. Of these, the statolith, which is part of the organ responsible for detection of linear and angular acceleration, has proved most promising for age determination. Growth increments in the stato- lith are formed from aragonite crystals in an organic matrix. They are best viewed after sectioning the statolith or after decalcification in weak acid. The statolith grows in concert with the rest of the squid. Experiments with squid in which chemical markers have been incorporated at a known time in the statolith, and experiments with cultured squid of known age, appear to confirm the hypothesis that growth increments in the statolith are laid down daily. Increments are produced in the laboratory in the absence of tidal, feeding or temperature cycles, which suggests that there is a firmly entrained endogenous circadian rhythm associated with their formation. However, the possibility that increment formation can be disrupted by environmental factors, or that rings in the statolith are produced coincidentally at the rate of approximately one per day, should not be fully discounted without further experimental corroboration. Data on squid age, derived from growth increments in the statolith, clearly have value in fisheries investigations, but they should be treated with caution until they have been validated.

INTRODUCTION

Increasing recognition of the considerable commercial potential of cephal- opod stocks worldwide {Worms, 1983; Rathjen and Voss, 1987) has highlighted the necessity for effective management of the fishieries for these molluscs. The requirement for information on growth rate and life span, to support studies of population biology, has recently led cephalopod biologists to focus attention on the problem of assessing age in squid.

Apparent growth increments have been found in the squid beak (Tinbergen and Verwey, 1945; Clarke, 1965), the radula (Wirz, 1963 ), the gladius (Spratt, 1978) and were first described in the statolith by Clarke (1966). Increments

0165-7836/90/$03.50 © 1990 Elsevier Science Publishers B.V.

Page 2: Age determination in squid using statolith growth increments

324

in the beak and radula have subsequently received little attention but there have been a number of studies on growth increments in the statolith. In this paper, we review data on the structure of the squid statolith and the techniques used to prepare them for age studies. We consider the published evidence in support of the hypothesis that growth increments in the statolith are formed daily.

STRUCTURE OF THE SQUID STATOLITH

Squid statoliths are paired calcareous concretions that lie loosely attached at the anterior end of the statocysts. These saccular organs, in the ventro- posterior region of the cartilaginous skull behind the brain, are the sense or- gans responsible for the detection of linear and angular acceleration in squid (Budelmann, 1975, 1977; Stephens and Young, 1978, 1982; Young, 1984; Mad- dock and Young, 1984), and the statolith is functionally analogous to fish oto- liths. It should be noted that in squid the functional body axis is almost per- pendicular to the longitudinal embryonic axis. For convenience and clarity, orientation is referred to, in this review and generally elsewhere, in terms of the functional axis.

A description of the external morphology of the statolith and an account of interspecific differences in squid, cuttlefish and octopods is given by Clarke (1978) and Clarke and Maddock (1988a,b). The statolith consists of 4 parts: the dorsal dome, lateral dome, rostrum and wing (Fig. 1 ). It is mostly a hard,

~/~ / ~ Dorsal dome

~ Lateral dome

~.. N~ Area o f attprCihnm:;: ~~ to macula

w i n g

~ / ~ Rostrum

Fig. 1. Major structural features of a squid statolith: right-hand statolith, anterior view.

Page 3: Age determination in squid using statolith growth increments

325

Fig. 2. Ground, anterio-lateral sections of the statoliths of (a) Illex argentinus (male: mantle length, 245 mm; statolith length, 1.14 mm) and (b) Loligo gahi (male: mantle length, 110 mm: statolith length, 1.73 mm) showing growth increments. Scale bars: 250 #m.

translucent structure, but the anterior side of the wing, which is the area of a t tachment to the macula princeps (Dilly, 1976), is softer, opaque white and composed of loosely-packed crystals.

Statoliths are composed of calcium carbonate in the aragonite crystal form, with an organic matrix (Dilly, 1976; Radtke, 1983). The crystaline subunits, the statoconia, vary in size but are usually elongated and hexagonal with pointed ends. In Illex illecebrosus from Newfoundland, the organic matrix comprises 4.5-5.6% of the total weight of the statolith and over this range the organic component shows a significant negative linear relationship with squid size (Radke, 1983 ). The organic matter is proteinaceous and largely comprised of acidic amino acids, notably aspartic acid, glutamic acid and glycine, which are known to be implicated in biological calcification (Hare, 1963; Weiner and Hood, 1975; Miterer, 1978; Weiner, 1979).

During development, the statolith of/. illecebrosus, and other ommastrephid species, passes through 5 recognisable stages before attaining the final com- plexity of the adult stage (Morris and Aldrich, 1984; Arkhipkin and Murzov, 1986). The primordial stage has a lachrymiform shape and it develops after the formation of the nucleus. The definitive stage follows, in which all the

Page 4: Age determination in squid using statolith growth increments

326

features illustrated in Fig. 1 become visible, and then there is continuous de- velopment through the pre-juvenile and juvenile stages to the adult stage. This is followed by an advanced stage.

Although growth increments can sometimes be seen in the untreated stato- lith, they are best viewed after sectioning by grinding on the concave anterio- lateral plane (Hurley and Beck, 1979). Scanning electron microscope exami- nation shows that increments are formed by aragonite crystals in a protein matrix. The crystals radiate from the kernel and disruptions and/or thicken- ings define the boundaries of the increments (Radtke, 1983). In section, the increment-bearing portion of the statolith of adult/, illecebrosus is divided into 3 regions according to variations in the widths of the increments. These regions reflect different stages in the growth and development of the squid (Morris and Aldrich, 1985).

A growth increment consists of 2 lamellae, one light and one dark (Fig. 2). Pannella (1980) makes the distinction between growth rings and increments in fish otoliths. Each dark lamella is termed a growth ring and an increment consists of one light lamella and the immediately following dark lamella. This terminology has been adopted for the analogous features in the squid statolith (Morris, 1983; Morris and Aldrich, 1985). For the purposes of counting, how- ever, the ring or increment count is effectively identical.

METHODOLOGY

Examination of statoliths for growth studies requires dissection and removal from the skull, mounting, sectioning and observation.

Dissection and removal

Three techniques exist for dissecting statoliths from the squid head. The first is by removing the funnel, flexing the head dorsally and making a series of horizontal incisions through the cephalic cartilage to expose the statocysts (Clarke, 1978; Arkhipkin and Murzov, 1985 ). Alternatively, the funnel can be removed, the head placed on its dorsal surface and vertical incisions made through the cartilage exposing the statocysts; a horizontal incision through the ventral wall of the statocysts then exposes the statoliths (Morris and Aldrich, 1984). The head may also be placed on its ventral surface and a series of ver- tical incisions made through the cephalic cartilage, starting at the posterior end; slicing until the statocysts are exposed.

Statoliths have also been extracted by dissolving the cartilaginous skull in sodium hypochlorite (Hurley and Beck, 1979).

As with fish otoliths, statoliths are acellular, mineralized structures, so de- composition should not occur under relatively dry conditions (Campana and Neilson, 1985). However, Dawe et al. (1985) found that drying sometimes

Page 5: Age determination in squid using statolith growth increments

327

causes the statolith to become opaque. This is overcome by storage in absolute alcohol, 70% ethanol, gelatin capsules or glycerol.

Tissue fragments attached to the statolith after dissection are removed be- fore mounting. Morris and Aldrich (1985) achieved this by soaking in 5% hy- pochlorite solution in water. Careful removal of debris using a mounting needle and fine forceps, followed by immersion in 90% industrial methylated spirit (IMS) for 5 min, produces a specimen suitable for mounting.

Mounting Whole statoliths may be mounted in liquid paraffin (Lipinski, 1986) but for

preparing sections, hard-setting resins are used. Suitable mountants for light microscopy include: "Protexx" (Rosenberg et al., 1980; Dawe et al., 1985; Hur- ley et al., 1985), "Lakeside 70" (Kristensen, 1980), "Epon 812" (Morris and Aldrich, 1985 ) and "Polarbed 812".

Statoliths must be mounted at the correct angle with the concave, anterior surface facing upwards (Morris, 1983 ). Occulting crystals on the anterior sur- face are then ground away to expose the increments below. Increments are obliterated from the periphery of the statolith if the angle of orientation is incorrect. Dawe et al. (1985) mounted statoliths with the convex dorsal surface facing upwards. However, the nucleus is easily obliterated when the statolith is mounted in this way.

Preparation Grinding is done with silica carbide (carborundum) paper or powder. Wet-

grinding with water or glycerine using 1000-grit carborundum paper, glued to a glass slide, gives good results. Media used to enhance increments and coun- teract scratches produced during grinding include "Lakeside 70" (Kristensen, 1980), immersion oil (Rosenberg et al., 1980) and glycerol (Morris, 1983).

Observation A drawing arm mounted on a microscope allows a permanent record of growth

increments to be made and enhances counting accuracy. High-resolution pho- tomicrographs are difficult to produce, because the growth increments do not all occur in the same focal plane under high power (Dawe et al., 1985 ). Morris and Aldrich (1985) used a microprojector to produce an image of the incre- ments onto paper via a mirror. The resulting magnification (690 X ) gave good results and facilitated accurate counting.

Two studies have used whole statoliths to view increments. Hixon and Vil- loch (1983) and Yang et al. (1986) decalcified statoliths in a 1:1 mixture of 4% EDTA in distilled water and 0.2 M cacodylate buffer (pH 7.4). Using this method it was not possible to count increments in squid older than 65 days because decalcification distorted larger statoliths. Lipinski (1986) dissolved the inorganic part of the statolith in 0.1 N hydrochloric acid and 10% trichlor

Page 6: Age determination in squid using statolith growth increments

328

acetic acid and stained the resultant 'ghost' with Coomassie Brilliant Blue G- 250. This technique revealed the increments very clearly, except near the edge of the statolith.

Scanning electron microscopy (SEM) has been used to examine statolith microstructure (Dilly, 1976; Radtke, 1983; Dawe et al., 1985; Lipinski, 1986), but light microscopy is more suitable for routine examination in growth studies.

Storage Statoliths readily dissolve in weak acid and so are rarely found in specimens

of squid fixed in unbuffered formalin (Kristensen, 1980). The effect of long- term storage on clarity of growth increments following removal of the statolith is unknown. However, when stored for up to 7 months in glycerol, they are easy to read after processing. Statoliths from squid frozen for 18 months can be read as easily as those from fresh specimens. After sectioning, growth increments fade on prolonged exposure to air. Increments in statoliths of I. argentinus and Loligo gahi, have faded after 6 months (unpublished observation, 1987) and in statoliths from/, illecebrosus they have faded after 12 months (C.C. Morris, personal communication, 1987).

FREQUENCY OF INCREMENT FORMATION

Micro-growth increments are laid down in the shells of bivalve molluscs (cockles) at intervals corresponding to a semi-diurnal period of tidal immer- sion (Richardson et al., 1980b). Increment formation in cockles is subject to an endogenous rhythm which is entrained and reinforced by regular tidal im- mersions (Richardson et al., 1980a). In fish, micro-growth increments are laid down daily in otoliths and scales (Pannella, 1971, 1974; Brothers et al., 1976; Ralston, 1976; Struhsaker and Uchiyama, 1976; Taubert and Coble, 1977; Ottaway, 1978). Sub-daily increments have also been noted in some species (Campana and Neilson, 1985). There is apparently an endogenous circadian rhythm of increment formation in fish, which is thought to be entrained by photoperiod (Campana and Neilson, 1985 ). Daily growth markings, related to temperature, salinity and feeding, are also present in the cuttlefish shell (Choe, 1963).

By analogy with the fish otolith, and with regard to the fact that cephalopod physiology is influenced by a diurnal rhythm, it is proposed that increments in the squid statolith are produced on a daily basis (Spratt, 1978; Kristensen, 1980; and see review by Dawe, 1981 ). In addition, Kristensen (1980) has also suggested that second-order rings are laid down at fortnightly and monthly intervals.

In a number of squid species there is a strong positive relationship between statolith size and measurements of squid body size, such as mantle length, and strong relationships also exist between the number of growth increments in

Page 7: Age determination in squid using statolith growth increments

329

the statolith, size of the statolith and mantle length (Hurley and Beck, 1979; Kristensen, 1980; Radtke, 1983, Morris and Aldrich, 1985). These observa- tions support the view that the statolith grows in concert with the rest of the animal and that increments are laid down regularly during growth.

If growth increments are formed daily in the squid statolith, it should be possible to follow the modal length of a wild squid population by regular sam- pling, and relate the increase in number of increments, in the statoliths from squid at the mode, to the number of days elapsed between samples. Sampling and counting increments in this way with populations of Loligo opalescens (Spratt, 1978) and L illecebrosus (Hurley and Beck, 1979) indicated that the number of rings produced underestimated the number of days elapsed. This may have been because of the presence of mixed age groups in the population, caused by immigration or emigration. Dawe et al. (1985) repeated the experi- ment with inshore and offshore populations ofL illecebrosus off Newfoundland and found good agreement between the number of days elapsed and the num-

TABLE 1

Results of experiments to determine the relationship between elapsed time, following the incor- poration of a chemical marker, and number of growth increments subsequently produced

Species and source Chemical marker Sex Mantle Elapsed Number of length (mm) time (days) increments

Hlex illecebrosus Stront ium M 220 14 11 (Dawe et al., 1985) F 240 21 20

F 240 19 18 F 248 13 13 F 265 17 17

Tetracycline M 215 4 4 M 220 8 8 F 240 15 13 F 240 19 16 F 248 24 24 F 260 3 3 F 280 6 6

Alloteuth~ subulata Tetracycline M 70 22 22 (Lipinski, 1986) M 75 30 24

M 83 14 16 M 123 38 35 M 134 34 24 F 46 10 14 F 66 7 8 F 66 9 8 F 71 16 16 F 77 20 19

57 5 5

Page 8: Age determination in squid using statolith growth increments

330

ber of increments formed in the inshore population, but not in the offshore population. The discrepancy in the offshore population cannot be explained in terms of counting errors and is most likely to be caused by the confounding effect of migrations into, and out of, the population.

Experiments in which squid have been held in the laboratory for known periods of time, following incorporation of chemical markers in the statolith, have provided convincing evidence that growth increments are produced daily in adult squid. Hurley et al. (1985) incorporated strontium chloride and Dawe et al. (1985) incorporated strontium chloride and oxytetracycline in the diets of samples of/. illecebrosus. In both experiments, which were run for between 3 and 24 days, there was good agreement between the number of increments laid down and the number of days elapsed since the deposition of the chemical marker (Table 1). Lipinski (1986) injected oxytetracycline or chlortetracyc- line into a small sample ofAlloteuthis subulata, held them in the laboratory for up to 38 days, and also found agreement between the number of increments produced and the number of days elapsed (Table 1 ).

Good correspondence between the number of growth increments and the number of days elapsed since hatching has been found in culture experiments with the squid, L. opalescens, where specimens of known age are available for analysis of growth increments (Hixon and Villoch, 1983; Yang et al., 1986). The regression equation relating number of increments (N) to age in days (D) was:

N = -7 .24 ÷ 1.13D (n -- 43; r 2 -- 0.90)

Counts of increments differed from age in days by - 1 2 to +8 days (mean _+ 4.2) in squid from 21-65 days old.

INITIATION OF INCREMENT FORMATION

The general conclusion has been reached that formation of growth incre- ments is initiated in the squid statolith at the time of hatching (Kristensen, 1980; Hixon and Villoch, 1983; Radtke, 1983; Yang et al., 1986; Balch et al., 1988). It has been assumed by Morris and Aldrich ( 1985 ) that approximately 40 increments are laid down prior to hatching. Given this assumption, pre- dicted time of hatching of I. illecebrosus corresponds with field observations on the time of appearance of hatchlings. However, Dawe et al. (1985) examined the statolith of a 3-day-old I. iUecebrosus and found that it corresponded in size to the nucleus from adult specimens. The first growth increment was not vis- ible, suggesting that no increments are formed prior to hatching and also that there may be a short period following hatching before the initiation of incre- ment formation.

In spite of the circumstantial evidence that growth increments are produced

Page 9: Age determination in squid using statolith growth increments

331

daily in the squid statolith, the mechanism of increment formation is not understood. It may be related to feeding, because increments were produced in statoliths of L. opalescens, grown in culture with constant light and tempera- ture conditions, but with a 24oh feeding cycle (Yang et al., 1986). However,/. iUecebrosus, maintained in the laboratory, deposited daily growth increments in the absence of tidal, feeding or temperature cycles and without the oppor- tunity to undergo the extensive vertical migrations which occur in the wild (Dawe et al., 1985). It therefore seems likely that, if growth increments are daily in origin, there is a firmly entrained endogenous circadian rhythm of formation. However, the possibility that rings are simply part of the structural organisation of the statolith, and that their formation coincidentally occurs at the rate of about 1 day-1, cannot be fully discounted without further experi- mental evidence.

GROWTH DATA FROM INCREMENTS IN THE STATOLITH

Increments in the statolith have been used to derive growth data for Gonatus [abricii (Kristensen, 1983; Wiborg et al., 1984), Todarodes sagittatus (Rosen- berg et al., 1980; Wiborg and Beck, 1984), I. illecebrosus (Hurley and Beck, 1979; Radtke, 1983) Loligo forbesi (Martins, 1982), Idiosepius pygmaeus (Jackson, 1988) and Photololigo edulis (Natsukari et al., 1988). In each case the rate of growth was shown to be rapid and the results indicated that the largest squid in each population sampled were no more than about 1 year old. This is with the exception of G. fabricii from Greenland where growth is ap- parently somewhat slower than in the same species from Norway, and the max- imum age is nearly 2 years (Kristensen, 1983 ). These data are consistent with the expectation, from population studies of a number of species, that cephal- opod growth is generally rapid and that death follows shortly after a single spawning, the whole life cycle being completed in approximately 1 year (see reviews of cephalopod life histories in Boyle, 1983, 1987 ).

CONCLUSIONS AND DISCUSSION

There is a growing body of circumstantial and direct experimental evidence that growth increments in the squid statolith are formed on a daily basis. Cul- ture experiments with juveniles, in which number of increments correspond to the number of days since hatching, and experiments with adults in which in- crement formation following the deposition of a chemical marker corresponds to days elapsed, seem to confirm the daily nature of growth increments throughout the life cycle. However, the mechanism of increment formation and the environmental cues which initiate what appears to be an endogenous cycle, have not as yet been identified. If increments are formed daily it is pos- sible that their formation may be subject to the influence of environmental

Page 10: Age determination in squid using statolith growth increments

332

fac to r s in the wild, wh ich could d i s rup t t he d iu rna l r h y t h m a n d so inva l ida te t he i r use as a t i m e m a r k e r for g rowth s tudies .

In view of the diff icul t ies o f a s sess ing squid g rowth by cohor t ana lys i s (Rod- house e t al., 1988) t he r e is a good case for the cau t ious use of g rowth i n c r e m e n t s in the squid s t a to l i t h for a s sess ing age in g rowth s tudies . Howeve r , f u r t he r e x p e r i m e n t a l work to e luc ida te t he m e c h a n i s m of i n c r e m e n t f o r m a t i o n in the squid s t a to l i t h a n d to iden t i fy poss ib le sources of e r ro r in the i r use as age m a r k - ers is to be encouraged .

ACKNOWLEDGEMENTS

We t h a n k M a r t i n W h i t e a n d Claude M or r i s for t he i r advice a n d c r i t i c i sm whi l s t p r e p a r i n g th i s review.

R e s e a r c h a t the Br i t i sh A n t a r c t i c Survey , on age d e t e r m i n a t i o n in squid, is f unded b y the F a l k l a n d I s l ands G o v e r n m e n t .

REFERENCES

Arkhipkin, A.I. and Murzov, S.A., 1985. A method of preparation of statoliths for growth studies and age determination in squids. Zool. Zh., 64:1721-1726 (in Russian with English abstract ).

Arkhipkin, A.I. and Murzov, S.A., 1986. Statolith morphology, growth and development in squids of the family Ommastrephidae from the south-eastern part of the Pacific Ocean. Zool. Zh., 65: 499-505 (in Russian with English abstract).

Balch, N., Sirois, A. and Hurley, G.V., 1988. Growth increments in statoliths from paralarvae of the ommastrephid squid IUex ( Cephalopoda: Teuthoidea). Malacologia, 29:103-112.

Boyle, P.R. (Editor), 1983. Cephalopod Life Cycles Vol. 1. Academic Press, London, 475 pp. Boyle, P.R. (Editor), 1987. Cephalopod Life Cycles Vol. 2. Academic Press, London, 441 pp. Brothers, E.B., Matthews, C.P. and Lasker, R., 1976. Daily growth increments in otoliths from

larval and adult fishes. Fish. Bull., 74: 1-8. Budelmann, B.-U., 1975. Gravity receptor function in cephalopods with particular reference to

Sepia officinalis. Fortschr. Zool., 23: 84-96. Budelmann, B.-U., 1977. Structure and function of the angular acceleration receptor systems in

the statocysts of cephalopods. Symp. Zooi. Soc. Lond., No. 38: 309-324. Campana, S.E. and Neilson, J.D., 1985. Microstructure of fish otoliths. Can. J. Fish. Aquat. Sci.,

42: 1014-1032. Choe, S., 1963. Daily markings in the shell of cuttlefishes. Nature (London), 197: 306-307. Clarke, M.R., 1965. "Growth rings" in the beaks of the squid Moroteuthis ingens (Oegopsida:

Onychoteuthidae). Malacologia, 3: 287-307. Clarke, M.R., 1966. Review of the systematics and ecology of oceanic squids. Adv. Mar. Biol., 4:

93-325. Clarke, M.R., 1978. The cephalopod statolith - an introduction to its form. J. Mar. Biol. Assoc.

U.K., 58: 701-712. Clarke, M.R. and Maddock, L., 1988a. Statoliths of fossil coleoid cephalopods. In: M.R. Clarke

and E.R. Trueman (Editors), The Mollusca, Vol. 12. Academic Press, London, pp. 153-168. Clarke, M.R. and Maddock, L., 1988b. Statoliths from living species of cephalopods and evolution.

In: M.R. Clarke and E.R. Trueman (Editors), The Mollusca, Vol. 12. Academic Press, London, pp. 169-184.

Page 11: Age determination in squid using statolith growth increments

333

Dawe, E., 1981. Overview of present progress towards ageing short-finned squid (IUex illecebro- sus) using statoliths. J. Shellfish Res., 1: 193-195.

Dawe, E.G., O'Dor, R.K., Odense, P.H. and Hurley, G.V., 1985. Validation and application of an ageing technique for short-finned squid (IUex iUecebrosus). J. Northwest Atl. Fish. Sci., 6: 107-116.

Dilly, P.N., 1976. The structure of some cephalopod statoliths. Cell. Tiss. Res., 175: 147-163. Hare, P.E., 1963. Amino acids in the proteins from aragonite and calcite in the shells of Mytilus

californianus. Science, 205: 216-217. Hixon, R.F. and Villoch, M.R., 1983. Growth rings in the statoliths of young laboratory cultured

squids (Loligo opalescens). Am. Malacol. Bull., 2: 93. Hurley, G.V. and Beck, P., 1979. The observation of growth rings in statoliths from the ommas-

trephid squid, IUex iUecebrosus. Bull. Am. Malacol. Union Inc., 1979: 23-29. Hurley, G.V., Odense, P.H., O'Dor, R.K. and Dawe, E.G., 1985. Strontium labelling for verifying

daily growth increments in the statolith of the short-finned squid (IUex iUecebrosus). Can. J. Fish. Aquat. Sci., 42: 380-383.

Jackson, G.D., 1988. The use of statolith microstructures to analyze life history events in the small tropical cephalopod Idiosepius pygmaeus. Fish. Bull., 87: 265-272.

Kristensen, T.K., 1980. Periodical growth rings in cephalopod statoliths. Dana. 1: 39-51. Kristensen, T.K., 1983. Gonatus fabricii. In: P.R. Boyle (Editor), Cephalopod Life Cycles Vol. 1.

Academic Press, London, 475 pp. Lipinski, M., 1986. Methods for the validation of squid age from statoliths. J. Mar. Biol. Assoc.

U.K., 66: 505-526. Maddock, L. and Young, J.Z., 1984. Some dimensions of the angular acceleration receptor systems

of cephalopods. J. Mar. Biol. Assoc. U.K., 64: 55-879. Martins, H.R., 1982. Biological studies of the exploited stock of Loligo forbesi (Mollusca: Ce-

phalopoda) in the Azores. J. Mar. Biol. Assoc. U.K., 62: 799-808. Miterer, R.M., 1978. Amino acid composition and metal binding capability of the skeletal protein

of corals. Bull. Mar. Sci., 28: 173-180. Morris, C.C., 1983. Statolith development and age determination in the ommastrephid squid Illex

iUecebrosus (Lesueur, 1821 ). M.Sc. Thesis, Memorial University of Newfoundland, St. John's, Newfoundland, Canada, 121 pp.

Morris, C.C. and Aldrich, F.A., 1984. Statolith development in the ommastrephid squid Illex iUecebrosus (Lesueur, 1821) (Cephalopoda, Ommastrephidae). Am. Malacol. Bull., 2: 51-56.

Morris, C.C. and Aldrich, F.A., 1985. Statolith length and increment number for age determina- tion ofIUex illecebrosus (Leseur, 1821) (Cephalopoda, Ommastrephidae). NAFO Sci. Counc. Studies, 9: 101-106.

Natsukari, Y., Nakanose, T. and Oda, K., 1988. Age and growth of squid Photololigo edulis (Hoyle, 1885). J. Exp. Mar. Biol. Ecol., 116: 177-190.

Ottaway, E.M., 1978. Rhythmic growth activity in fish scales. J. Fish. Biol., 12: 615-623. Pannella, G., 1971. Fish otoliths: daily growth layers and periodical patterns. Science, 173:1124-

1127. Pannella, G., 1974. Otolith growth patterns: an aid in age determination in temperate and tropical

fishes. In: T.B. Bagenal (Editor), Ageing of Fishes. Unwin, London, pp. 28-39. Pannella, G., 1980. Growth patterns in fish sagittae. In: D.C. Rhoads and R.A. Lutz (Editors),

Skeletal Growth of Aquatic Organisms: Biological Records of Environmental Change. Plenum Press, New York, NY, pp. 519-560.

Radtke, R.L., 1983. Chemical and structural characteristics of statoliths from the short-finned squid IUex iUecebrosus. Mar. Biol., 76: 47-54.

Ralston, S., 1976. Age determination of a tropical reef butterflyfish utilizing daily growth rings of otoliths. Fish. Bull., 74: 990-994.

Page 12: Age determination in squid using statolith growth increments

334

Rathjen, W.F. and Voss, G.L., 1987. The cephalopod fisheries: a review. In: P.R. Boyle (Editor), Cephalopod Life Cycles Vol. 2. Academic Press, London, 441 pp.

Richardson, C.A. Crisp, D.J. and Runham, N.W., 1980a. An endogenous rhythm in shell deposi- tion in Cerastoderma edule. J. Mar. Biol. Assoc. U.K., 60: 991-1004.

Richardson, C.A., Crisp, D.J., Runham, N.W. and Gruffydd, L.D., 1980b. The use of tidal growth bands in the shell of Cerastoderma edule to measure seasonal growth rates under cool temper- ate and sub-arctic conditions. J. Mar. Biol. Assoc. U.K., 60: 977-989.

Rodhouse, P.G., Swinfen, R.C. and Murray, A.W.A., 1988. Life cycle, demography and reproduc- tive investment in the myopsid squid Alloteuthis subulata. Mar. Ecol. Prog. Ser., 45: 245-253.

Rosenberg, A.A., Wiborg, K.F. and Bech, I.M., 1980. Growth of Todarodes sagittatus (L.) (Ce- phaiopoda, Ommastrephidae) from the Northeast Atlantic, based on counts of statolith growth rings. Sarsia, 66: 53-57.

Spratt, J.D., 1978. Age and growth of the market squid, Loligo opalescens Berry, in Monterey Bay. Fish. Bull., 169: 35-44.

Stephens, P.R. and Young, J.Z., 1978. Semicircular canals in squid. Nature (London), 271: 444- 445.

Stephens, P.R. and Young, J.Z., 1982. The statocyst of the squid Loligo. J. Zool., 197: 241-266. Struhsaker, P. and Uchiyama, J.H., 1976. Age and growth of the nehu, Stolephorus purpureus

(Engraulidae), from the Hawaiian Islands as indicated by daily growth increments of sagittae. Fish. Bull., 74: 9-17.

Taubert, B.D. and Coble, D.W., 1977. Daily rings in otoliths of three species of Lepomis and Tilapia mossambica. J. Fish. Res. Board Can., 34: 332-340.

Tinbergen, L. and Verwey, J., 1945. Zur biologie von Loligo vulgaris. Lain. Arch. Neerl. Zool., 7: 213-286.

Weiner, S., 1979. Aspartic acid-rich proteins: major components of the soluble organic matrix of mollusc shells. Calcif. Tissue Res., 29: 163-167.

Weiner, S. and Hood, L., 1975. Soluble protein of the organic matrix of mollusc shells: a potential template for shell formation. Science, 190: 987-989.

Wiborg, K.F. and Beck, I.M., 1984. Akkar Todarodes sagittatus (Lamarck). Undersokelser i Norske kyst- og bankfarvann i Juli-November 1983. Fisken Havet, 2: 13-23.

Wiborg, K.F., Gjosaeter, J. and Beck, I.M., 1984. Gonatus fabricii (Lichtenstein). Undersokelser i Norskehavet og det vestlige Barentshavet og Juni-September 1982 i 1983. Fisken Havet, 2: 1-11.

Wirz, K.M., 1963. Biologie des cephalopodes benthiques et nectoniques de la Mer Catalane. Vie Milieu Suppl., 13: 1-285.

Worms, J., 1983. World fisheries for cephalopods: a synoptic overview. In: J.F. Caddy (Editor), Advances in Assessment of World Cephalopod Resources. F.A.O. Fish. Tech. Pap., 231: 1-20.

Yang, W.T., Hixon, R.F., Turk, P.E., Krejci, M.E., Hulet, W.H. and Hanlon, R.T., 1986. Growth, behaviour and sexual maturation of the market squid, Loligo opalescens, cultured through the life cycle. Fish. Bull., 84: 771-798.

Young, J.Z., 1984. The statocysts of cranchiid squids (Cephalopoda). J. Zool., 203:1-21.