Multiple spawning in the tropical squid

Marine Biology (1995) 124:127-135

9 Springer-Verlag 1995

N. A. Moltschaniwskyj

Multiple spawning in the tropical squid Photololigo sp.: what is the cost in somatic growth?

Received: 17 May 1995/Accepted: 10 July 1995

Abstract This study assesses the potential of the tropical loliginid squid Photololi9o sp. to lay multiple batches of eggs and examines changes in somatic growth during reproduction. Histological analysis of the ovary and the relative size of the oviduct to mantle weight and ovary weight were used to determine the potential for multiple spawning. Ovaries of mature females always had immature and mature oocytes present, suggesting that not all the oocytes were maturing simultaneously and that multiple batches of eggs were being produced. Furthermore, poor correlations of oviduct weight with body size and ovary weight indicated that mature oocytes were not accumulating in the oviduct for a single spawning event. Both these observations supported the hypothesis that Photololigo sp. has the potential to lay multiple batches of eggs throughout its life. Specific growth rates, length-weight relationships, relative growth of somatic and reproductive tissue and microscopic assessment of muscle tissue were compared between immature and mature females. Growth rates of immature females were almost twice as fast as those of mature females. Mature females also had no large muscle fibres present, suggesting that energy for reproduction was mobilised from the muscle tissue.

Introduction

Energetic trade-offs are central in life-history theory, and provide the link between life-history traits such as growth rate, reproductive mode and longevity (Stearns 1992). As there is a finite amount of energy available to an animal, the allocation of energy to gonadal growth Communicated by G.F. Humphrey, Sydney Dr. N.A. Moltschaniwskyj Department of Marine Biology, James Cook University, Townsville, Queensland 4811, Australia

may be at the cost of somatic growth (Stearns 1992). These trade-offs would be expressed as competition for energy between somatic and reproductive structures. Assessing the cost of reproduction is often difficult to do, and although slowing of somatic growth may indicate the allocation of energy to oocyte production, an assessment of somatic tissue may provide a better indication of the cost of reproduction (Calow 1983). Iteroparity is not possible for most cephalopods because they have life spans of a year or less. However, different modes of semelparity may occur. There are species that only undertake one spawning event during their life-time and die shortly after spawning; a strategy that was, until recently, considered universal among squid (Calow 1987). However, many species lay multiple batches of eggs throughout their adult life-time (Harman et al. 1989; Sauer and Lipinski 1990; Lewis and Choat 1993). It is also becoming evident that no single growth curve is characteristic for squid, and it is likely that the diversity of spawning modes in cephalopods may be related to growth patterns (Mangold et al. 1993). Some cephalopods have fast growth, attain an asymptotic size, and die shortly after spawning (Calow 1987). Others have indeterminate growth (Forsythe and Van Heukelem 1987; Jackson and Choat 1992), and multiple spawning activities occur (Lewis and Choat 1993). A reliable way of obtaining information about the energy allocated to reproduction and growth is to maintain females in captivity (e.g. Lewis and Choat 1993), although extrapolating laboratory results must be carefully done. However, many squid species are difficult to hold in captivity, and indirect evidence for multiple spawning events in cephalopods may be obtained by examining the gametogenic cycle. Females that spawn once will often have a single batch of oocytes maturing in the ovary and no primary oocytes present in mature females (Knipe and Beeman 1978; Perez et al. 1990). Immature oocytes in the ovaries of females that have mature oocytes in the oviduct, ready

128

to be laid, suggest that new oocytes are being produced to be laid in subsequent batches (Harman et al. 1989; Lewis and Choat 1993). Relative growth of reproductive and somatic structures can also provide information about how energy is allocated. No correlation between female size and the number of oocytes in the oviduct suggests that mature oocytes do not accumulate to be laid in a single batch, but are released from the ovary into the oviduct where they are held for a short time before laying (Harman et al. 1989; Sauer and Lipinski 1990; Young and Mangold 1994). In contrast, terminal spawners accumulate mature oocytes in the oviduct, where they are stored for a single spawning episode. Therefore, positive allometric growth of reproductive organs, when gonad tissue increases in size at a faster rate than muscle weight, is expected in terminal spawning animals (Rodhouse et al. 1988; Rodhouse and Hatfield 1990) because energy is allocated to gonad growth and away from somatic growth. However, species that lay a number of egg batches will have slower gonadal growth because energy is divided between oocyte production and somatic growth. In some cephalopods, changes in the muscle tissue during oocyte production and spawning are obvious. The muscle tissue breaks down, resulting in a thin flaccid mantle (Fields 1965; Karpov and Cailliet 1978; Sauer and Lipinski 1990; Jackson and Mladenov 1994), but see (Hatfield et al. 1992). This loss of muscle tissue and changes in texture to the mantle may occur if the mantle muscle tissue is used as a major energy source (Packard 1972; O'Dor and Webber 1986) for the production of oocytes (O'Dor and Wells 1973). This depletion of protein from body tissues probably contributes to the death of females shortly after spawning (Tait 1986; Pollero and Iribarne 1988). Growth of the mantle muscle-tissue in adult Photololigo sp. occurs by the generation of new muscle fibres and growth of existing muscle fibres (Moltschaniwskyj 1994a). This growth can be recorded as an increase in the width of the circular muscle blocks and increase in size of the muscle fibres. Therefore, if energy for reproduction is at the cost of somatic growth, the size of muscle blocks and fibres may differ between individuals at different maturation stages.

PhoWloligo sp. is an inshore tropical loliginid squid species found along the central Queensland coast of Australia. The species used in this study is the most common in the Townsville region, and in the past has been referred to by the specific name chinensis (Jackson 1991; Jackson and Choat 1992); however, recent taxonomic work indicates that chinensis is the incorrect specific name (Yeatman 1993). As this species is one of two sibling species, all individuals in this study were identified as the same species by allozyme electrophoresis (Yeatman 1993). Photololigo sp. lives for ~-120d and growth continues at a constant rate throughout its life-time (Jackson and Choat 1992). There is a poor correlation between reproductive maturity and the age or size of female Photololigo sp. Therefore, it is likely that somatic growth continues during maturation and spawning, and females can spawn multiple times (Jackson 1993). However, more information about the dynamics of oocyte maturation and gonad growth is needed to provide support to this statement. The aims of this study were to determine the potential ability of females to spawn repeatedly throughout the adult life-span and to investigate how oocyte production affects the growth and condition of somatic tissue. Materials and methods Collection and processing Female Photololigo sp. were collected, using twin otter trawls, from 21 August 1991 to 27 November 1991 in Cleveland Bay, Townsville, Australia, (19~ 146~ Squid were captured during daylight hours (between 08.00 and 15.00 hrs Eastern Standard Time) and stored at 4 ~ for processing within 12 h. The dorsal mantle length and weight of mantle muscle, ovary and oviduct were measured for every female.

Gonad growth Reproductive maturity was assessed macroscopically based on the relative size and colour of the reproductive organs (Table 1). No Stage VI (spent) females were ever caught during this study. For microscopic inspection of the oocytes, ovary tissue was fixed in a formalin acetic-acid calcium-chloride solution [FAACC: 10 ml

Table 1 PhotoIoligo sp. Macroscopic reproductive-stage scale for males and females. Scale based on Lipinski's "universal scale" (Juanic6 1983) Stage

Category

Females

Males

I II III IV V VI

Juvenile Immature Preparatory Maturing Mature Spent

no gonad tissue visible traces of ovary and oviduct oviduct just visible, ovary and nidamental gland obvious ovary and nidamental gland large ovulated oocytes in oviduct, red accessory nidamental glands unknown

no gonad tissue visible spermatophoric complex just present spermatophoric complex clearly visible testis present, white streaks in Needham's sac spermatophores in penis and Needham's sac unknown

129 37% formaldehyde, 5 ml glacial acetic acid, 1.3 g calcium chloride (dihydrate); distilled water to 100 ml], sectioned (6 p,m), and stained with MaIlory-Heidenhain trichrome. Developing oocytes were assigned to one of 5 maturity stages (Table 2). Stage-frequency distributions of oocytes were obtained by staging the first 100 oocytes encountered along a transect across the ovary section. The number of oocytes in the single oviduct of mature females was estimated by counting the total number of oocytes in a 20 mg sample and scaling this number by oviduct weight. Oocyte diameter was measured using an ocular micrometer in a stereomicroscope.

Somatic growth and condition The relationship between body length and weight can be used as a condition index allowing an assessment of the loss of muscle tissue-mass, assuming no shrinkage in length. Condition of female squid was assessed by the relationship between dorsal mantle length and weight of wet mantle muscle. This relationship is usually logarithmic, and a log-transformation of both variables generates a linear relationship. If mantle muscle-mass is reduced, with no change in length during egg production, then this relationship would become shallower in mature individuals compared with immature females. The relative change of mass with length was described using the slope of the linear relationship between variables (iogl0-transformed) for females in each of the reproductive classes. The five slopes were compared using an analysis of covariance, with dorsal mantle length as the covariate. Age information was determined from the daily rings in the statolith (Jackson 1990a, 1991). Statoliths were ground along the dorso-ventral axis with 1200 btm grit wet and dry polishing paper, with a final polish with 0.3 btm alumina powder. Daily rings were counted from the natal ring under a light microscope with a polarised light source (Jackson 1990a, 1991). If the natal ring was not seen, or three consecutive counts within 10% of each other were not obtained, the statolith was discarded as unreadable. For microscopic examination of the mantle muscle-tissue, a sample of tissue from the ventral surface adjacent to the locking mechanism was removed and processed according to the methods outlined in Moltschaniwskyj (1994a). Histological sections (7 gin) were obtained allowing the circular muscle fibres to be seen in cross-section. The widths of 42 circular muscle fibre-blocks and 60 muscle-fibre diameters from each female were randomly selected and measured. The size-frequency distributions of the muscle blocks and muscle-fibre diameters were compared among females from the five reproductive stages.

Photololigo sp. Stages of oogenesis used to describe maturation of oocytes in ovary Table 2

Stage

Description

1

Primary oogonia and secondary oogonia; small oocytes with poorly defined nucleus and small cytoplasmic area Oocytes have a large germinal vesicle and follicular cells are becoming attached to oocyte Follicular cells proliferate on surface of oocyte and begin penetrating ooctye; once penetration occurs a syncytium is formed Vitellogenesis occurs and folicular synctium degenerates Final degeneration of synctium occurs and oocyte is ovulated

Results Gonad growth Female Photololigo sp. with small developing ovaries had a predominance of primary and secondary oocytes (Fig. 1). As maturation of oocytes progressed, the ovary continued to produce new primary oocytes, and mature (Stage IV and V) females had a range of oocyte types present in the ovary (Fig. 1). The presence of primary and secondary oocytes in the ovary of mature females suggests that oocytes are produced throughout the life time of an adult and that oocyte production does not cease. There was evidence of a cohort of oocytes maturing at the same time, and there was a predominance of vitellogenic (Stage 4) oocytes in mature females. It was also evident that these females had proportionally Stage I

30

n=lO

//

0 60

Stage II

n=13

30

6O

Stage III

d~

0 d] 13.

n=8 30

0 Stage IV

n=7

3O

~176 t 0

1

2

3

4

5

Egg maturity

Fig. 1 Photololigo sp. Oocyte-stage distribution in each of the five female reproductive stages (see Table 2 for staging descriptions) (n number of females examined)

130 1.8-

Y =-0.05+0.4" X r=0.8

1.6"

i

I

II

4 "6

N 1.4.g

"O

+

O

+

.I-

9I"

1-.

4.

+

+ @4.@

+,

,11,

4-

1.2-

#

~_+~ ~ + +'~++ + t=.--=...o

0

N"

I

,it"

2

I

i

4 Ovary (g)

1.0

6

Fig. 2 PhotoloIigo sp. Relationship between ovary weight and oviduct weight in mature females

9I-

O O

I

3

Fig. 4 Photololigo sp. Relationship between average size of ovulated oocytes and oviduct weight (Error bars standard errors)

+

+ 4.

"5 600

4.

Growth and mantle-muscle condition

+

+

E Z

I

the oviduct. The weight of the oviduct was not related to the average size of the oocytes (Fig. 4; r = 0.39, n = 12, P = 0.21), which suggests oocytes were not continuing to grow in the oviduct and, therefore, were ready to be laid.

1200

900

I

I 2 Oviduct weight (g)

9II" 9I.

300

I

§ .I.

4,

0

++

§

@.I9/, "k

I

50 100 Dorsal mantle length (mm)

+

I

150

Fig. 3 Photololigo sp. Number of oocytes in oviduct of mature females as a function of mantle length

fewer immature oocytes. However, > 50% of the oocytes were in the first three stages of oocyte development. Ovary and oviduct weight were poorly correlated with female size, suggesting that maturation in this species is not size-dependent ( r = 0 , 6 0 , n = 161, P < 0.0001 and r = 0.41, n = 62, P < 0.0001, respectively). If only one spawning event occurs, mature o0cytes would accumulate in the oviduct. However, in all but one individual the oviduct was lighter than the ovary (Fig. 2) and oviduct weight never exceeded 15% of the wet mantle weight. If mature oocytes were accumulating, the oviduct would have become heavier than the ovary. The number of oocytes in the oviduct ranged from 64 to 1271 (Fig. 3), and their length ranged from 0.96 to 2.00 mm (mean = 1.58 mm). Female size and the oocyte number were not significantly correlated (r = 0.26, df 27, P = 0.19), providing further evidence that females were not storing mature oocytes in

Sexual maturity of female Photololigo sp. was poorly correlated with size, suggesting that factors other than size determine sexual maturity (Fig. 5). There was an overlap of 20 mm mantle length between immature and fully mature females. It was evident that females as large as 129 mm were only just starting to become sexually mature, while some 80 mm females had mature oocytes. Condition of females, described by the length-weight relationship, was similar among the five reproductive groups (Table 3). It may be expected that the cost of using mantle muscle tissue as an energy source for reproduction would make females lighter. However, an analysis of covariance found no evidence that the linear relationshi p between dorsal mantle length and muscle mantle-mass differed among the reproductive stages (Table 4). Therefore, there was no evidence that maturation caused loss of condition by decreasing mantle muscle-mass. If energy is directed away from somatic growth during reproduction, then growth of ovary tissue may be expected to be faster than growth of mantle muscletissue. However, in the case of Photololigosp., an examination of the allometric growth between ovary and somatic tissue showed that the slope was significantly less than 1 (b = 0.34, SEb---0.04 Student's t = 20.85, P --- 0.03), indicating that growth rate of the ovary was never as fast as or faster than growth of mantle muscletissue. Comparisons of the growth rates among the females in the different reproductive stages were done using the

131 30

Stage I

Table 3 Photololigo sp. Length-weight relationship for females in each of the five reproductive stages

n=67

20

10

0 30-

Stage

Slope

[SE]

Intercept

r

(n)

I II III IV V

2.26 2.10 2.41 2.26 2.29

[0.06] [0.08] [0.1l] [0.28] [0.10]

-

0.97 0.97 0.98 0.91

(67) (37) (23) (16) (42)

7.53 6.74 8.12 7.45 7.63

0.92

Stage II n=37

20-

Table 4 Photololigosp. Analysis of covariance, testing for differences in slopes of the length weight relationships among the five female reproductive stages (SS sum of squares)

10-

Source

0-

30-

Stage III

SS

Stage Intercept Slopes Residual

0.0459 12.4800 0.0423 2.1486

df 4 1 4 196

Mean SS 0.0115 12.4800 0.0107 0.0110

F

Prob > F

1.05 1138.45 0.98

0.3838 0.0001 0.4172

n=23 20 r-

0.020 -

E

g_ lo 0.015 -

0 "O

30

Stage IV o.olo-

-r

20

t

o o 0.005-

10 0 30

Stage V

I

t

I

I

2

3

4

5

Stage

n=42

Fig. 6 Photololigosp. Specific growth rates, expressed as proportion of body weight increase each day, for females in each reproductive stage

20

10

53

73 93 113 133 Dorsal mantle length (mm)

153

Fig. 5 Photololigo sp. Size-frequency distribution of females in each of the five reproductive stages (n number of females measured)

exponential growth equation because this was the overall shape of the growth curve for Photololigo sp. Specific growth rates of females ranged from 0.066 in Stage V females to 0.120 in Stage III females (Fig. 6), which was significantly different (Table 5). Fastest growth rates were seen in immature (Stage I-III) individuals, almost twice as fast as the rates calculated for mature

females. Therefore, the growth rates suggest that allocation of energy to reproduction was slowing somatic growth. Both the muscle-block and muscle-fibre sizefrequencies were different among the five reproductive maturity stages. In all the reproductive stages, most of the muscle blocks were on a v e r a g e ~ 90 gm wide (Fig. 7). Stage III females had muscle blocks that were very wide ( > 210 gm wide), but muscle blocks in this size class were less abundant in mature (Stage IV and V) females (X2= 84.38, df 20, P < 0.0001). Muscle fibres in all the reproductive stages were predominantly 1 to 3 gm in diameter (Fig. 8). However, it was evident t h a t there were relatively more larger fibres in Stage III and IV females but fewer large fibres present in

132 Table5 Photololigo sp. Analysis of covariance, testing for differences in specific growth rates among five female reproductive stages Source

SS

Stage Intercept Slopes Residual

9405.58 4287.22 248.73 384.77

df 4 1 4 69

Mean SS

F

Prob > F

2351.39 4287.22 62.18 5.58

421.67 768.81 11.15

0.0001 0.0001 0.0001

~a

3O 20

50

10

Stage I

0 25'

30

~' 20

0

o 10

50

0) 3.

tage II

0

25 30 20 10

Stage Ill

0

g 25-

.o

O 13_

30 20 50

Stage IV

10 0

25

0

0

1

2 3 4 Fibre diameters (pm)

5

Fig. 8 Photololigosp. Size-frequency of mantle muscle-fibres in each reproductive stage.

5o 7

Staae V

Discussion

25-

0-

0

1O0 200 Block widths (gm)

300

Fig. 7 Photololi9o sp. Size-frequency of mantle muscle-blocks in each reproductive stage

Stage V females (Z2 = 99.11, df 36, P < 0.0001). Larger muscle blocks and muscle fibres were expected in mature females because these individuals are generally larger (Fig. 5), but a decrease in the proportion of large muscle blocks and muscle fibres suggests that some shrinkage of muscle fibres > 4 pm may have occurred, reducing the relative frequency of muscle blocks > 180 ~tm.

The presence of immature oocytes in the ovary of mature females and the absence of oocytes accumulating in the oviduct provided evidence that Photololi9o sp. has the potential to produce batches of eggs. Ovaries of all mature females examined had a population of primary and secondary oocytes present. The presence of immature oocytes in the ovary may not be sufficient evidence that a species is a multiple spawner, because oocytes may accumulate in the oviduct and be released in a single batch. However, asynchronous production of oocytes, with no distinct peaks of oocyte size in the ovary, indicates multiple spawning events in teleosts (de Vlaming 1983). Therefore, for multiple-spawning events to occur, new gametes must be generated whilst ovulated oocytes are laid (Harman et al. 1989). Support for this is provided from known multiple-spawning

133

cephalopods that always have immature oocytes in the failed to find individuals much larger than 150 mm ovary (e.g. Idiosepius pygmaeus, Lewis and Choat 1993). (Jackson 1991; Yeatman 1993; Moltschaniwskyj In contrast, ovaries of spent terminal spawners have no 1994b), suggesting that this is the maximum size for primordial cells (Knipe and Beeman 1978). females of this species. Therefore, later maturing squid The poor correlation between the number of mature that grow faster would be expected to live for a shorter oocytes in the oviduct and body size in Photololigo sp. time. These females would produce larger batches of suggested that females periodically spawn and empty eggs because of their size, but might produce few the oviduct. A strong relationship between body size batches because they are reproductive for a shorter and oviduct mass should be evident if females hold time. Conversely, earlier maturing females that grow ovulated oocytes in the oviduct until all oocytes com- slower, might expected to produce more smaller plete maturation (Harman et al. 1989). This is further batches of eggs. Maybe the variation in size at maturity supported by the lighter weight of the oviduct com- seen in Photololigo sp. allows a flexibility in their repropared to the ovary; the oviduct would eventually be- ductive strategy similar to that proposed for Loligo come heavier as more oocytes are accumulated. Fur- forbesi (Boyle et al. 1995). thermore, ovulated oocytes in the oviduct showed little Many tropical squid studied to date have either variation in size, suggesting that females produce sim- a linear or exponential growth curve; i.e. growth conilar-sized oocytes and growth of the oocyte does not tinues throughout their lifetime (Jackson 1989, 1990b; Jackson and Choat 1992). This means that food intake occur in the oviduct. Rodhouse et al. (1988) hypothesised that fast growth by Photololigo sp. must be high enough to sustain of the ovary, relative to the mantle tissue, is likely in reproduction and growth. It is likely that simultaneous terminal spawning squid because energy is diverted allocation of energy to reproduction and growth will from somatic growth to reproduction. This has been reduce the rate of oocyte production compared with observed in terminal spawning squid (Rodhouse et al. a species that ceases growth and allocates energy to 1988; Rodhouse and Hatfield 1990, 1992; Hatfield et al. oocyte growth. Photololigo sp. had 64 to 1271 mature 1992). However, for Photololigo sp., the relative growth oocytes in the oviduct (present study) compared with of the ovary was slower than the mantle tissue. This 1600 to 6350 mature oocytes in Lolliguncula brevis, difference suggests that the allocation of energy to a terminal spawner of comparable size (Haefner 1959, ovary and somatic growth differs between terminal and in Marigold 1987). Therefore, to produce a comparable number of oocytes, Photololigo sp. would need to promultiple-spawning individuals. An examination of length-weight relationships and duce as many as six batches of eggs. Possibly the only the relative growth of ovary and somatic tissue sug- spawning strategy feasible for a species that continues gested that energy required for reproduction did not growing is producing a number of small batches of affect somatic growth. However, an effect was ex- eggs. However, the inverse of this may not necessarily pressed in the growth rates of females and the muscle be the case. For example, Abralia triganura has detertissue at the cellular level. The relatively low abundance minate growth but produces multiple batches of eggs of muscle fibres > 4 ~tm in mature females suggests (Young and Mangold 1994). The energetic demands in oocyte production and that these larger fibres may have been partially or totally resorbed by the female. However, some growth spawning can result in flaccid, structureless muscle was still occurring and the length-weight relationship tissue and death if the muscle tissue is used as an energy did not indicate that dramatic shrinkage had taken source; either because feeding ceases or food levels place. The slower growth of mature females and the are low. However, extensive muscle-tissue degradation absence of large fibres may be a product of the mode of does not necessarily occur during oocyte production muscle-tissue growth. Growth by both hyperplasia (Hatfield et al. 1992; Rodhouse and Hatfield 1992), and (production of new muscle fibres) and hypertrophy may result from the cessation of feeding after spawning (growth of existing fibres) occurs in Photololigo sp. and the use of the mantle muscle-tissue as an energy (Moltschaniwskyj 1994a). It appears that hyperplasia source (Laptikhovsky and Nigmatullin 1993). It is unmay be more common in mature females and therefore clear whether senescence in squid is due to the metaboresponsible for slower growth rates in mature female lism of body protein for oocyte production or to metaPhotololigo sp. The consequence of this difference can bolic changes that occur after spawning (Guerra 1993). be seen if these growth rates are simulated. An imma- A clearer understanding of energy allocation during ture individual starting at 80 mm (the smallest Stage reproduction and growth may be achieved with bioV female) and growing at 1.2% per day reaches chemical techniques. It is possible that the proportion 120 mm in 20 d. In contrast, a mature individual, also of water increases in the muscle tissue as protein restarting at 80 mm mantle length and growing at 0.66% serves are used. Certainly, biochemical changes in per day would be 20 mm shorter after 20 d. It is unclear terminal-spawning squid and octopus have been detectwhat effect these differences in size at maturity have on ed during oocyte production (O'Dor and Wells 1978; the lifetime fecundity of Photololigo sp. Extensive col- Pollero and Iribarne 1988). However, Loligo gahi (a lections of Photololigo sp. in the Townsville region have terminal spawner) does not appear to be using protein

134 f r o m muscle tissue a n d is c a p a b l e of m e e t i n g the dem a n d of o o c y t e p r o d u c t i o n w i t h o u t mobilising reserves ( G u e r r a a n d C a s t r o 1994). A useful, a n d necessary, c o m p a r i s o n w o u l d be to e x a m i n e c h a n g e s in c e p h a l o p o d s t h a t s p a w n a n u m b e r of times d u r i n g their life a n d c o n t i n u e to g r o w at the s a m e time. It will be necessary to c o m p a r e the m e t a b o l i s m a n d e n e r g y efficiency of multiple- a n d t e r m i n a l - s p a w n i n g squid to allow us to u n d e r s t a n d the energetic d y n a m i c s of r e p r o duction and growth.

Acknowledgements This work was supported by a James Cook University Merit Research Grant. I would like to thank J.H. Choat, A. Lewis, G.D Jackson, M. Dunning and the Coral Discussion Group for providing valuable criticism of earlier versions of the manuscript. Thank-you to the crew of the RV "Kirby" and volunteers who assisted in the field. This research was conducted while N.A.M was on the Commonwealth Fellowship and Scholarship Scheme.

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