© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
An allozyme investigation of the stock structure of arrow squid Nototodarus gouldi (Cephalopoda: Ommastrephidae) from Australia
a Institute of Antarctic and Southern Ocean Studies, University of Tasmania Private Bag 77, Hobart, Tasmania 7001, Australia
b Evolutionary Biology Unit South Australian Museum, North Terrace, Adelaide, SA 5000, Australia
*Correspondence to G. D. Jackson: tel: +61 3 6226 2975; fax: +61 3 6226 2973. e-mail: george.jackson{at}utas.edu.au.
Allozyme electrophoresis was used to examine the stock structure of arrow squid Nototodarus gouldi (McCoy 1888) from Australia. Samples collected from six localities around southern Australia, separated by distances of between 700 and 4300 km, were examined for allozyme variation at 48 loci. The data revealed no evidence of more than a single species among the 203 squid examined. Nine polymorphic loci were detected, although only three were sufficiently variable to provide real insight into the population structure of arrow squid. There were no significant deviations from Hardy–Weinberg expectations for any locus, population, or for the metapopulation. Pairwise comparisons of allele frequencies revealed minor evidence of stock structure, with the Iluka (north New South Wales) sample set displaying significant allelic differences from the Tasmanian sample set at Acyc and from the Ulladulla (south New South Wales) sample set at Sordh. F-statistics also provided weak support that the Australian metapopulation is not panmictic. Further studies are needed to delineate the degree of stock segregation within the Australian/New Zealand region in order to successfully manage the arrow squid fishery in these waters.
Keywords: allozyme electrophoresis, cephalopods, genetics, ommastrephids, squid populations
Received 21 July 2003; accepted 10 December 2003.
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Introduction |
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 Top Introduction Materials and methodsResultsDiscussionReferences |
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The arrow squid, Nototodarus gouldi (McCoy 1888), is an oceanic and neritic squid, endemic to southern Australia and northern New Zealand. For most of its distribution, N. gouldi inhabits the waters <500 m in depth on the continental shelf and slope, and is most common at depths from 50 to 200 m (Uozumi, 1998). In Australia, this species has been shown to occur between latitudes 27°13'S and 43°40'S, in seawater temperatures ranging from 11°C to over 25°C (Dunning, 1998). Throughout these waters, and those off the northern and central New Zealand coast, N. gouldi is the dominant ommastrephid squid and is subject to commercial and recreational harvesting (Dunning and Forch, 1998). Arrow squid are also a key component of offshore ecosystems as they are eaten in large numbers by numerous predatory species (Coleman, 1984; Gales et al., 1994).
Little is known of the early life history of this species. Reproduction is presumed to be typical of ommastrephids, where a large pelagic egg "balloon" is produced and released in midwater, possibly in the region of a pycnocline (Sakurai et al., 2000). Hatchlings have been collected in late spring to summer over a broad area of the southern Australian continental shelf, from 28°S in southern Queensland to 34°S in the western Great Australian Bight, as well as off central New South Wales from midsummer to midwinter (Dunning and Forch, 1998).
Prior to this study, the only information concerning the stock structure of this species in Australian waters was a preliminary allozyme study by Richardson (1983), which found no evidence of genetic differentiation in southeast Australia. However, more extensive genetic and morphological work in New Zealand waters has since revealed the presence of two species of Nototodarus, with a second species, N. sloanii, occurring around the South Island and south to the Auckland Islands Shelf (Smith et al., 1987). With increasing fishing pressure on N. gouldi, there is a growing need to understand the stock structure of this species in Australian waters. It is presumed that arrow squid should display high levels of gene flow throughout its range, given its mode of spawning via pelagic egg "balloons", the pelagic nature of the juvenile stages, and the mobile habit of adults. However, given its extensive distribution in Australia, a consequential association with several different current systems, and the presence of two species in New Zealand within a much smaller geographic region, there is clearly a need to comprehensively examine the genetic structure of arrow squid throughout their entire Australian range.
This project is part of a larger study of N. gouldi in Australian waters, aimed at describing the important biological characteristics of this species. Preliminary data to date indicate that this species has a life cycle spanning 
1 yr or less, with highly variable growth rates that are heavily influenced by environmental parameters (Jackson et al., 2003). A reproductive study of this species in Tasmanian waters has indicated that N. gouldi is a multiple spawner, with energy for reproduction being acquired from food rather than at the cost of somatic condition (McGrath and Jackson, 2002). Given the general unpredictability of marine environments and a short lifespan, it is not surprising to find that recruitment in this species is highly variable on a spatial and temporal scale. This variability is reflected in catch and fishing effort, which also fluctuates widely between years and regions (Nowara and Walker, 1998). Since the fishery targets a new generation of squid every year, there is concern that the combination of a year of high fishing effort coinciding with low recruitment could lead to overfishing. For this reason there is the need to collect and monitor important biological parameters of the population of N. gouldi in Australian waters.
Genetic studies have demonstrated that cryptic species are a common occurrence in squid (Augustyn and Grant, 1988; Brierley et al., 1993; Yeatman and Benzie, 1994; Izuka et al., 1996; Triantafillos and Adams, 2001). Consequently, a genetic systematic assessment of species boundaries deserves to be one of the first steps in any serious study of squid biology. Such a study should first identify whether the various populations are conspecific prior to undertaking any assessment of population structure. Of the numerous genetic techniques available, allozyme electrophoresis remains one of the most appropriate for an initial investigation of both species boundaries (Avise, 1994; Hillis et al., 1996; Richardson et al., 1986) and broad population structure (Ihssen et al., 1981; Ryman and Utter, 1987). Allozyme data have already proved useful for assessing intraspecific differentiation in a number of economically important cephalopod species (e.g. Katugin, 1995; Triantafillos and Adams, 2001; Kassahn et al., 2003). The present study uses allozyme electrophoresis to clarify the taxonomic status of Australian N. gouldi and to provide insight into its population genetic structure throughout southern Australia.
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Materials and methods |
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TopIntroductionMaterials and methodsResultsDiscussionReferences |
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Sample collection
Samples of Nototodarus gouldi were collected using a variety of techniques from five sites along the coast of southern Australia between January 2000 and December 2002 (Figure 1; Table 1). Distances between sites ranged from 700 to 4300 km. Tasmania was represented by a spatial replicate sample set, with the replicate (Storm Bay) collected on the same day, but from a location 15 km from the initial site (Wedge Island).
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Animals from Bunbury, Wedge Island, and Storm Bay were frozen whole at the site of capture after being stored on ice for up to 48 h. Tissues obtained from these animals displayed consistently lower levels of enzyme activity and did not stain for a couple of the less-important polymorphic markers. Animals from Kangaroo Island, Ulladulla, and Iluka were collected fresh and a small piece of tentacle tissue (
1 g) was immediately removed from each individual and placed in liquid nitrogen. Tissue samples were returned to the laboratory and stored at –80°C, pending genetic analysis.
Allozyme electrophoresis
The allozyme study was carried out in two stages, according to the rationale outlined by Triantafillos and Adams (2001). Initially, a large number of allozyme loci were screened in an overview study of 30 individuals, comprising seven animals each from Bunbury, Kangaroo Island, Ulladulla, and Iluka, and two animals from Wedge Island. Having determined that enough polymorphic loci were present to permit an assessment of population structure, a second stage of allozyme analysis was undertaken. Here, a large number of animals from all sample sites (Table 1) were genotyped at the polymorphic loci plus at a selection of monomorphic loci which could be reliably typed as "double-stains" without increasing the number of gels run (for technical details, see Richardson et al., 1986). Based on the overview study, the optimum sample size was set at 50 individuals per sample set, although this number was not always available.
Allozyme electrophoresis was conducted according to the principles and methodology of Richardson et al. (1986). Tissues were homogenized by sonication in two volumes of homogenizing solution (deionized water containing 0.2% 2-mercaptoethanol and 0.2 mg ml–1 NADP). In total, 37 enzymes displayed zymograms of sufficient activity and resolution to permit allozymic interpretations in the overview study (Table 2). The nomenclature for referring to loci and allozymes followed Adams et al. (1987).
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Data analyses
The allozyme data were analysed for a range of population genetic measures using the computer program GENEPOP, version 3.1b (Raymond and Rousset, 1995). These were (i) deviation from Hardy–Weinberg expectations for each locus/sample set combination, (ii) linkage disequilibrium between genotypes at different loci, and (iii) differences in allele frequency for pairwise comparisons of sample sets at each locus. All p values were adjusted using the sequential Bonferroni technique (Rice, 1989) to compensate for multiple tests, starting with an initial significance level of 0.05. F-statistics were calculated using the program FSTAT version 2.8 (Goudet, 1995, 1999). Genetic differentiation among sample sets was estimated using Nei's unbiased measure of genetic distance (Nei, 1978), under the assumption that the loci found to be monomorphic in the overview study were invariant in all sample sets.
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Results |
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TopIntroductionMaterials and methodsResultsDiscussionReferences |
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Allozyme variation
A total of 48 putative allozyme loci were examined in the overview study. Of these, 39 were monomorphic across all 30 specimens, while nine loci displayed electrophoretic variation consistent with the presence of two or more co-dominant alleles. The remaining 173 specimens were then screened for these nine polymorphic loci plus four invariant loci (Ak, Est2, PepA, and PepB), chosen anecdotally for their potential to display allelic variation (Table 3).
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Species boundaries
There was no evidence of cryptic species within N. gouldi for the sites sampled in this study. No fixed differences were present between any localities and indeed all sample sets displayed very similar allele frequencies at the nine polymorphic loci (maximum difference in allele frequency = 36% for allele Sordhd; see Table 3). This high degree of genetic similarity was reflected in the Nei Distances between sample sets, which ranged from 0.000 to 0.003. The single species hypothesis was further supported by the lack of linkage disequilibrium or departures from Hardy–Weinberg expectations outlined in the following paragraph.
Population structure
No significant deviations from Hardy–Weinberg expectations were found for any locus or site, and homogeneity tests revealed no evidence of linkage between any two loci in any sample set. As such there is no evidence that sample sets were not representative of single, panmictic populations at each locality. Importantly, these analyses also confirmed that each genetic marker could provide an independent test of between-locality stock structure in N. gouldi.
An initial comparison of allele frequencies between the two replicate sample sets from Tasmania revealed no significant differences at any locus, and as a consequence these were pooled to form a combined sample set (TAS). Thereafter, pairwise comparisons of allele frequencies between all sample sets revealed only two departures from homogeneity, both involving the Iluka sample set (0.01< p<0.05 for Acyc, NSW2 vs. TAS; 0.01< p<0.05 for Sordh, NSW2 vs. NSW1). No attempt was made to further explore the nature of any population substructuring, given the small genetic distances and overall similarities in allele frequency encountered.
F-statistics
F-statistics were calculated for the five major sample sets (WA, SA, TAS, NSW1, and NSW2) using the genotypic data for all nine polymorphic loci. The FIS values for both analyses did not differ significantly from zero, supporting the assumption of panmixia within sample sets. A marginally significant positive value was obtained for FST (FST=0.009; 95% confidence intervals 0.001–0.012; p<0.05), supporting the assertion that there was significant genetic divergence among sample sets. This value remained marginally significant when the data were re-analysed after the removal of the Iluka sample set, suggesting that whatever genetic divergence may exist in the metapopulation is not just a function of a northern (i.e. Iluka) vs. southern (i.e. the other sites) genetic dichotomy.
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Discussion |
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Cryptic species
The allozyme data presented herein provide no evidence for the presence of cryptic species in Nototodarus gouldi among over 200 squid from six localities spanning its Australian distribution. This finding is consistent with studies of most other oegopsids. Indeed, of the 20 or so oegopsid squid examined using genetic techniques to date, the presence of cryptic species has been suggested only in Martialia hyadesi from the Patagonian and Antarctic Polar Front (Brierley et al., 1993) and a sub-species of Berryteuthis magister from the North Pacific (Katugin, 2000). By comparison, cryptic speciation is much more prevalent in myopsid squid (e.g., Izuka et al., 1994, 1996). Highlighting this contrasting pattern for the two groups is the fact that cryptic species have been found in all five loliginids examined so far from Australia (Photololigo chinensis and P. edulis, Yeatman and Benzie, 1994; Sepioteuthis australis, Triantafillos and Adams, 2001; Loliolus noctiluca, Citroen, 2001; and Sepioteuthis lessoniana, Triantafillos, unpublished data). These differences probably reflect the more neritic habitat of loliginids, their nearshore benthic spawning habits, and their larger hatchlings, which would be less likely to drift in the pelagic environment than their smaller ommastrephid and other oegopsid counterparts. Taken together, these biological attributes presumably provide loliginids with greater opportunities to form localized, genetically isolated populations, some of which may occasionally become full species (without necessarily undergoing morphological change) given sufficient time.
Population structure
Population genetic analysis of the allozyme data revealed no evidence of within-site heterogeneity at any of the localities sampled but did infer that the entire Australian metapopulation is not panmictic. Pairwise comparisons of allele frequencies and F-statistics revealed marginally significant differences in allele frequencies at two loci between Iluka and one other site. This suggests that the Iluka sample in northern NSW may represent a separate stock when compared to sites further to the south and west. Moreover, F-statistics also suggested additional between-site heterogeneity among these other sites.
Beyond these inferences, the data provide no support for any obvious population substructuring within N. gouldi. Allele frequencies at every site were broadly similar for all polymorphic loci for localities separated by distances of up to 4300 km. Such data are consistent with a single, randomly mating stock across southern Australia and compatible with the predicted effects of recruitment via sexually produced offspring with high dispersal ability. Similar patterns of genetic homogeneity have been observed in other oegopsid squid. For example, only a low level of population differentiation was found in the circum-polar sub-Antarctic squid Moroteuthis ingens on a global scale (Sands et al., 2003). This outcome was explained in terms of eggs and hatchlings being transported long distances in circum-polar currents and jet streams associated with frontal zones.
Our results however should be viewed cautiously, for two reasons. Although allozyme analysis can provide valuable insight into species boundaries and therefore is an appropriate starting point for a molecular systematic assessment, its utility for detailed population structure analysis is usually constrained by an inability to generate both adequate numbers of genetic markers overall and adequate numbers of alleles per marker (Hillis et al., 1996). Such is the case herein for arrow squid, where only three of the nine polymorphic loci were sufficiently variable (i.e. the combined frequency of rarer allele(s) > 10%; see Richardson et al., 1986) to be useful indicators of population structure. Low levels of allozyme diversity have been found in other squids such as Loligo pealei (Garthwaite et al., 1989), Loligo opalescens (Reichow and Smith, 2001), and appear to be characteristic of squid in general (Ally and Keck, 1978; Brierley et al., 1995). Caution should also be exercised due to the low numbers of individuals in two sample sets (Western Australia and Tasmania), which reduce the chances that any real differences in allele frequency can be shown to be statistically significant. Taken together, these caveats increase the probability of a type II error i.e. that genuine population substructuring will remain undetected due to the null hypothesis of panmixia being falsely accepted (Richardson et al., 1986).
Furthermore, from a fisheries management perspective, genetic uniformity does not always equate to stock uniformity. This is because in the absence of strong selection pressures, the effective number of migrants that is necessary to maintain uniformity at the genetic level detectable by allozymes between otherwise "isolated" stocks is small, i.e. 1–10 individuals per generation (Allendorf et al., 1987). Clearly, such small exchange would not be sufficient to maintain stock integrity if stocks were functionally isolated.
Implications for management of arrow squid fishery
The results of this study have clear implications for the management of arrow squid. At present, they are managed in Australia as if all individuals are members of a single, interbreeding stock. The results presented here indicate the possibility of more than one stock, particularly along the east coast. If indeed there is a discrete stock in the northeastern region of the distribution of N. gouldi, management strategies need to be modified so that these stocks can be managed separately. Given the likelihood of increased harvesting of this ecologically vulnerable species, there is clearly a pressing need to extend this study further to determine exactly how many stocks are present in the Australian region. Without this information, there is some concern that localized stocks may become depleted and result in a recruitment failure. This, combined with heavy fishing pressure, has already contributed to the collapse of the fisheries for Illex illecebrosus and Todarodes pacificus in the Northwest Atlantic and Northwest Pacific Oceans, respectively (Dawe and Warren, 1993).
Future directions
Despite some general limitations, our allozyme analyses demonstrate that further molecular investigation of fine-scale population structure is warranted for N. gouldi. The two most suitable approaches here are likely to be (i) microsatellite analysis and (ii) analysis of mitochondrial DNA sequence data (Adcock et al., 1999a, b; Shaw et al., 1999; Reichow and Smith, 2001).
Given that its distribution encompasses both Australia and New Zealand, any future study of population structure in N. gouldi should ideally include some New Zealand populations to assess to what degree, if any, the New Zealand stock is genetically connected to the Australian stock. There is the possibility that the New Zealand squid might be genetically associated with one of the Australian east coast stocks. The biological status and potential connection of the arrow squid stocks between these two countries clearly needs resolving. Future sampling would ideally also be structured to consider any degree of temporal genetic differences (e.g., Katugin and Mokrin, 2001). While this study presents preliminary work, research needs to now take the next step with more powerful genetic analyses and larger spatial and temporal sample sizes from both Australian and New Zealand sites. There is also the likelihood of increased fishing pressure on Australian populations of arrow squid which underscores the urgency of obtaining better genetic resolution for this species.
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