© 2003 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
The dynamics of the summer-spawning population of the loliginid squid Sepioteuthis australis in Tasmania, Australia—a conveyor belt of recruits
a Institute of Antarctic and Southern Ocean Studies, University of Tasmania PO Box 252-77, Hobart, Tasmania 7001, Australia
b Marine Research Laboratories, Tasmanian Aquaculture and Fisheries Institute, University of Tasmania Hobart, Tasmania 7001, Australia
*Correspondence to G. D. Jackson; tel: +61 3 6226 2975; fax: +61 3 6226 2973. e-mail: george.jackson{at}utas.edu.au; gretta.pecl{at}utas.edu.au.
The population dynamics of the loliginid squid Sepioteuthis australis was examined on a fine temporal scale during a 2-month period of rising sea-surface temperatures on the summer inshore spawning grounds of Coles Bay, Tasmania, Australia. Samples were taken regularly (generally weekly) to discern any short-term population changes in age, growth or reproductive parameters. There was no change in the mean age, mantle length or weight of males or females through the study period (November and December 1996). This indicated that instead of following one or a few discrete cohorts of spawning individuals, there were continuous waves of new individuals moving onto the spawning beds, which may be best described by a conveyer belt of new recruits. There was an abrupt and significant difference in the mean oviduct egg size in females caught between November and December but the factors responsible for this remain unknown. Few squid showed evidence of recent feeding, suggesting that they move off the spawning grounds to feed.
Keywords: squid spawning, reproduction, age, statoliths, loliginidae, cohorts, population dynamics
Received 8 July 2002; revision received 10 December 2002; accepted 11 December 2002.
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Introduction |
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Loliginid squid populations are important components of many marine near-shore ecosystems. Understanding the life history of these short-lived mobile predators is essential for fishery policy development, particularly because of cephalopods replacing more traditional finfish stocks in certain regions (Caddy and Rodhouse, 1998), and collapses of major squid fisheries in others. Recently, a topical area of research has been describing the reproductive tactics of cephalopods with flexible life-history patterns (Boyle et al., 1995; Pecl, 2001; McGrath and Jackson, 2002) and quantifying spawning frequency (Maxwell and Hanlon, 2000). Near-shore loliginid populations are characterised by short life spans, early maturity and extreme plasticity in growth rates, especially in relation to changes in environmental conditions (Brodziak and Macy, 1996; Jackson, 1994, 1998; Hatfield, 2000; Jackson and O'Dor, 2001). Thus life histories are in "fast forward" for these organisms, and at a varying pace depending upon the environmental conditions in which individuals are hatched into and subsequently grow through.
The typical loliginid strategy is for individuals to be dispersed during much of their life history over the continental shelf. At certain periods, mature individuals of some species move into specific near-shore spawning grounds where they congregate short term or for extended periods (Segawa, 1987; Sauer et al., 1992, 1997; Collins et al., 1995; Boyle and Boletzky, 1996; Jackson, 1998). However, it is unknown whether mature individuals remain on the spawning grounds during the spawning season or whether there is a more complex movement of individuals on and off these grounds. Statolith ageing techniques can provide information on the dynamics of such movements. However, only a few studies have employed statolith ageing for subsequent samples taken over a short period of time (Arkhipkin, 1993, 2000).
The squid Sepioteuthis australis is endemic to southern Australian and northern New Zealand waters (Lu and Tait, 1983) and can reach sizes of up to 3.6 kg and 54 cm dorsal mantle length (ML) (Lyle and Hodgson, 2001). It is closely related to the congener Sepioteuthis lessoniana, which is widespread throughout the Indo-Pacific region. Recent genetic analysis of S. australis has revealed that the stock structure is complex and consists of two species and a hybrid. On the east coast of Tasmania, Triantafillos and Adams (2001) found that 98% of the population examined are the one genetic type. S. australis forms large spawning aggregations in shallow waters in areas of seagrass and algal beds, where they produce benthic egg mops (Moltschaniwskyj et al., in press).
Previous work (Pecl, 2001) indicated that S. australis is a multiple spawner in Tasmanian waters with considerable growth taking place during the reproductive phase of the life cycle. Pecl (2001) also noted seasonal differences in reproductive investment. Mature summer-caught individuals had higher gonadosomatic indices indicating they were laying larger batches of eggs compared with mature winter-caught squid. Summer-caught females also showed a negative correlation between oviduct egg size and egg number.
We focus here on short-term dynamics of the spawning population of squid occurring on the spawning grounds in Coles Bay, Tasmania, during summer. To elucidate temporal changes, we took a series of consecutive samples during November and December 1996 and investigated feeding, size, age and reproductive parameters of mature individuals.
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Methods |
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TopIntroductionMethodsResultsDiscussionReferences |
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Squid were collected approximately weekly by hand jigging or with commercial purse-seiners on spawning grounds in the Coles Bay and Hazards Bay region on the western shore of Great Oyster Bay, Tasmania (Figure 1) between 5 November and 31 December 1996. In the absence of obvious differences in the size distribution of squid caught with either gear, all animals were pooled in subsequent analyses. Squid caught on adjacent days were also pooled. All samples were taken in shallow water (<10 m) over areas of seagrass and algae interspersed with patches of sand. Samples were processed fresh within 3–6 h of capture. Temperature information for the sampling area was estimated from interpolated sea surface temperature data produced weekly on a 1° grid by the National Centre for Environmental Modelling (USA).
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Parameters measured included ML, whole wet weight (W), maturity stage, mantle weight, fin weight, and for females ovary weight, oviduct weight, nidamental gland weight, oviducal gland weight, oviduct weight, oviduct fullness (Pecl, 2001) and mean oviduct egg size (mean length of 20 formalin preserved oviduct eggs sampled randomly and measured along the long axis using an ocular micrometer and a stereomicroscope). Testis weight and the combined weight of all other reproductive structures were taken for males. Three males and five females were either immature or maturing and were excluded from all analyses. Mean egg size was determined for females from five sampling dates.
Individuals were aged using statolith increment counts to estimate individual age in days. The technique for viewing and enumeration of increments involved sectioning the statolith in the transverse plane and viewing the section with an image analysis system (Pecl, 2001). Statolith increment periodicity has been validated daily in known aged individuals up to 102 days (Pecl, 2001).
Stomach fullness was recorded for each individual on a scale from 0 (empty) to 4 (full) and digestive stage was noted on a scale from 1 (fresh) to 5 (highly digested; Jackson et al., 1998). Stomachs were removed and frozen for later analysis. In the laboratory, contents were sieved and sorted by prey type using a dissecting microscope. Fish otoliths and bones, and cephalopod beaks were extracted and kept dry.
ANOVA was used to compare population parameters for each sampling date and temporal trends were analysed using Pearson's correlation. Significance levels were adjusted using the sequential Bonferroni method to control for type I error rates as a result of multiple comparisons (Quinn and Keough, 2002). The 
2 statistic was used to test sex ratios for each sample.
To explore trends in reproductive investment over time we calculated a size-independent "reproductive investment residual" for males and females. Mantle weight–total reproductive weight geometric mean regression (Model II) equations were calculated separately for males and females, using log-transformed data to linearise the relationship. Based on these equations, residuals were calculated for each individual and standardised by dividing each residual by the standard deviation of the predicted values. Individuals with positive residual values had a greater reproductive investment compared to the average population, individuals with a negative residual a smaller one.
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Results |
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Temporal dynamics
Water temperature showed an increasing trend particularly from the beginning of December onwards (Figure 2). Overall, significantly more males than females were caught, but only on two occasions were the sex ratio different from 1 (Table 1). The age range of both females and males observed at different sampling dates was considerable (overall 127–264 and 128–254 days), respectively. There was no difference in the mean age by sample over time (F=1.94, df=6,175), or for either sex over time (sexxtime interaction F=0.79, df=5,175; Figure 2a, b). Similarly, there was no significant correlation between mean age and temperature for either females (r=–0.54, n=6) or males (r=–0.79, n=7).
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Size varied widely among mature females (ML = 165–358 mm, W = 210–1700 g) and males (ML = 172–501 mm, W = 175–2830 g). As with age, differences in either parameters were not significant for either sex over time (Figure 3; sexxtime interaction FML=0.53, df=6,246; FW=0.96, df=6,246), while differences between mean MLs (F=48.76, df=1,246, p<0.0001) and weights (F=11.50, df=1,246, p=0.001) of females and males were significant. No significant correlations were found between temperature and mean female W (r=–0.73, n=7), female ML (r=–0.56, n=7), male W (r=–0.47, n=7) or male ML (r=–0.40, n=7).
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ANOVA of the reproductive investment residuals also did not reveal any trend with time for either females (F=0.81, df=6,100; Figure 4a) or males (F=0.31, df=6,146; Figure 4b). Oviduct egg size of spawning females (Figure 4c) showed a significant trend through time (F=39.78, df=4,72, p<0.0001). A Tukey's HSD post hoc test revealed two completely separate subsets in the data: females in November had smaller mean oviduct egg size (6.46–7.17 mm) than did females caught in December (8.24–8.54 mm). There was no significant correlation between mean egg size (n=5) over time and mean ML (r=0.64), weight (r=0.52), oviduct fullness (r=0.05), oviduct weight (r=0.21), ovary weight (r=0.19), oviduct egg number (r=–0.41), GSI (r=–0.22) or temperature (r=0.33).
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Diet
Diet analysis was undertaken for 60 stomachs containing food (Table 1). Most stomachs were either empty or contained only a small amount of food, while the stage of digestion indicated that there was little recently ingested prey (Table 2). The main prey types were fish, octopus and crustaceans. Because of the erosion of the otoliths, species identification was impossible, but at least five different "types" of otoliths were present. Fifty-two stomachs (87%) out of the 60 analysed had fish remains, 14 (23%) had octopus remains (three species) and only four (7%) individuals had ingested crustaceans. There were no obvious differences in diet composition between sexes. Cannibalism was not recorded.
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Discussion |
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The only consistent pattern found was the apparent lack of one. Surprisingly, there was no temporal change in the age, size and/or reproductive parameters (other than egg size) examined. This lack of a consistent pattern is in itself an interesting feature of the population dynamics of S. australis on the spawning grounds in Tasmania, especially in relation to individual age. Our time series of age data reveals complex dynamics occurring over a relatively short time period. Because age (or size for that matter) did not change from week to week, we were essentially sampling a new group of animals in each sample. There appears to be a conveyor belt of squid moving through the spawning area and not staying on the spawning grounds. While preliminary tagging suggested that some females did stay in the general area (Pecl, 2001) there is obviously a constant influx of new individuals on, and outflux from the spawning grounds.
At an oceanic scale, Arkhipkin (1993, 2000) obtained population age samples of Illex argentinus over 10-day periods in a South Atlantic region and found that often waves of individuals were moving through the sampling region. In many ways the life history of S. australis is similar to Loligo vulgaris reynaudii in South Africa (Sauer et al., 1992, 1997; Melo and Sauer, 1999). Both are large near-shore loliginids that congregate in shallow water for spawning and are subject to fishing pressure during this critical period. Sauer et al. (2000) showed from tagging studies that individuals moved between spawning sites over a period of weeks, suggesting similar dynamics as revealed here. Acoustic tagging (Sauer et al., 1997) further showed that although some spawners moved away from the spawning site, they did return to the same location indicating some site fidelity.
Detailed analysis of the spawning activity of Loligo pealeii (Maxwell and Hanlon, 2000) indicated a strategy that consisted of egg laying over at least several weeks, with multiple mates and multiple batches, possibly in different locations. Such a strategy may also apply to S. australis, which apparently continues to move to different spawning sites rather than maintaining any degree of site fidelity. Leos (1998) took daily samples of Loligo opalescens from fishing operations off central California and found that fishing activity possibly affected squid schooling and spawning behaviour, because there were more spent squid on a Monday after a weekend closure and catches generally declined during the week. Thus, changes in spawning activity could be detected at a daily level of resolution for this species.
Previous work (Pecl, 2001) showed marked differences in reproductive investment between summer- and winter-caught females of S. australis, suggesting that summer-spawning females produced larger batches of eggs than winter-spawning females. Our data therefore represent spawning activity that is at the higher end of the reproductive investment continuum. The significant difference in oviduct egg size between November and December is intriguing and worthy of further investigation but currently remains unexplained. Pecl (2001) found a weak but significant negative correlation between oviduct egg size and oviduct egg number suggesting a possible trade-off between fewer larger vs. more smaller eggs. A weak but significant relationship between body size and oviduct egg size in Loligo forbesi was found by Boyle et al. (1995) suggesting that larger squid may produce larger eggs. Laptikhovsky and Nigmatullin (1993) observed that in oceanic environments oviduct egg size in Illex was not dependent on size but appeared to be influenced more by the marine environment. Lewis and Choat (1993) showed that under experimental conditions food intake did not affect egg size in the sepioid Idisepius pygmaeus although low food intake resulted in smaller batch size. The extreme differences in oviduct egg size during adjacent months observed here suggests a strong but unknown environmental or physiological influence.
Diet analysis suggests that squid are not coming to the spawning region to feed. Very few individuals had recently ingested large amounts of prey. However, squid took jigs indicating that they would feed if preys were available. This has also been suggested to be the case for L. v. reynaudii in inshore South African waters (Augustyn, 1990) where there was little feeding on spawning grounds. S. australis is predominantly a fish/cephalopod predator, like other loliginids (Augustyn, 1990; Coelho et al., 1997). The common occurrence of octopus in the diet suggests some foraging near the bottom. While the samples taken on the spawning grounds did not provide evidence of cannibalism, continuing research has revealed that S. australis may feed on itself. On two occasions, three to four hatchlings were observed attacking and feeding on another hatchling and pieces of S. australis tissue have been recorded in stomachs of adults.
Repeated sampling over short intervals has revealed dynamics that would have been missed had we used a more common monthly sampling strategy. This suggests that we might need to re-think the time scales used in population studies of loliginid squid.
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Acknowledgements |
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The commercial fishers in Tasmania were a great help with procuring squid samples. J. Harrington, C. Jackson, N. Moltschaniwskyj, J. Semmens and S. Wilcox assisted with field collections. This research was made possible by the Merit Research Grants Scheme, James Cook University and the Australian Research Council Discovery Grants scheme.
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