ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on December 20, 2007
ICES Journal of Marine Science: Journal du Conseil 2008 65(2):164-170; doi:10.1093/icesjms/fsm184
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Fecundity of the European lobster (Homarus gammarus) off southwestern Norway after stock enhancement: do cultured females produce as many eggs as wild females?
Institute of Marine Research, PO Box 1872, Nordnes, 5817 Bergen, Norway
tel: +47 5523 6368; fax: +47 5523 5384; e-mail: ann-lisbeth.agnalt{at}imr.no
Agnalt A-L. 2008. Fecundity of the European lobster (Homarus gammarus) off southwestern Norway after stock enhancement; do cultured females produce as many eggs as wild females? – ICES Journal of Marine Science, 65: 164–170.An enhancement project with European lobster (Homarus gammarus) began in 1990, and over the following 5 years some 128 000 hatchery-produced juveniles of average age about 9 months were released around the islands of Kvitsøy, southwestern Norway. Recaptures of reproductive female lobsters of cultured origin raised the question as to whether hatchery-reared females could perform as well as wild females in terms of egg production. A fecundity study therefore compared females of wild and cultured origin during autumn of 1996, and spring and autumn of 1997. No significant differences were found in size-specific fecundity (F = 0.0045 CL3.22; n = 215; r2 = 0.88; CL is carapace length), weight of egg mass, embryonic development, or egg size (diameter or dry weight). Further, the number of eggs produced per female was in the same range as it was about 90 years ago, i.e. before the local stock collapsed. There were no indications of significant differences in fecundity between seasons and therefore no egg loss for the incubation period from October 1996 to the end of May 1997. The results suggest that more eggs are produced by the larger females than in lobsters elsewhere in Europe, but compare well with American lobsters (H. americanus) of the same size range and living in the same temperature regime (off Newfoundland).
Keywords: egg dry weight, egg size, European lobster, fecundity, southwestern Norway, stock enhancement
Received 12 December 2006; accepted 24 June 2007; advance access publication 20 December 2007.
| Introduction |
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In 1990, an enhancement project with the European lobster (Homarus gammarus) began in Norway (Agnalt et al., 1999, 2004). Some 128 000 hatchery-reared juveniles (
9 months old, and CL 15 mm) were released at Kvitsøy (Figure 1), a group of islands off the southwestern coast, over a period of 5 years. The main aim was to increase recruitment in the release area and to rehabilitate the collapsed stock on a long-term basis. Recruitment is clearly linked with reproduction, and fecundity is one critical parameter. In managing lobster stocks in other parts of the world, egg-production models are used to define important reference points (Campbell and Pezzack, 1986; Fogarty and Idoine, 1988; Ennis and Fogarty, 1997; Hobday and Ryan, 1997; Gendron, 2005), and to estimate size-specific fecundity is one of the principal parameters. Rørvik and Tveite (1982) carried out the first stock assessment of European lobsters in Norway, and although they included egg production in their analysis, they provided no indication of from where the data were derived. Such research on European lobster off Norway has been limited (Appelöf, 1909, counted the eggs of ten lobsters collected off Kvitsøy in 1906). The lack of such information has usually been compensated for by using data derived from other stocks. For instance, van der Meeren et al. (1995) used UK data in their analysis, with the main assumption that size-specific fecundity is similar for the species.
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An important measure in an enhancement project is to assess whether hatchery-produced juveniles grow and survive in the wild, but it is equally important to determine whether released animals perform in a similar manner to wild conspecifics. Agnalt et al. (1999, 2004) reported a substantial number of ovigerous females of cultured origin in the landings in the release area (Kvitsøy), and concluded that cultured lobster contributed to the spawning stock. However, the question arose as to whether they produced as many eggs, of similar quality, as wild females. This study on fecundity provides information for the local lobster stock at Kvitsøy, focusing on potential differences between wild and cultured females in terms of egg production.
| Material and methods |
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As part of the monitoring programme described by Agnalt et al. (1999, 2004), ovigerous females were recorded in the commercial landings at Kvitsøy. Hatchery-reared females released as juveniles were identified from the presence of a magnetic microwire tag (Agnalt et al., 1999). Morphometric measurements included CL and the maximum width of the second abdominal segment (abdominal width; AW). All recordings were made to the millimetre (mm) below, and body weight to the nearest gramme. Ovigerous females used for fecundity analysis were collected mainly during the commercial fishing season of autumn 1996. Samples from spring 1997 were included to assess possible egg loss during the incubation period, i.e. from October 1996 to the end of May 1997. Further, samples collected during autumn 1997 were included to evaluate whether egg production could differ from season to season, as well as to cover a wider size range of cultured females. The females were purchased from fishers, and special care was taken to include only animals captured the same day or the day before. Previously, it had been observed that berried females lost their eggs if exposed to too much handling or to high densities in the storage phase. Females were collected from as wide a size range as possible, including animals below the legal size (88 mm CL).
Females were held vertically with their heads pointing downwards on a polystyrene plate while the eggs were removed manually. Thereafter, all wild females were tagged with a numbered streamer tag (Hallprint Ltd) and returned to a storage basin until released later at a known site. This seemingly brutal means of collecting eggs did not cause mortality, but where a single walking leg was removed (for genetic analysis) as well as this treatment, a few animals died. As a result, genetic sampling was postponed until a few days after the eggs had been removed, and mortalities were again zero.
The weight of the fresh egg mass was recorded to the nearest 0.01 g. To estimate fecundity, the number of eggs in two subsamples of 1–1.5 g was determined, and the average of the two counts was used as the estimate of total fecundity. The correlation between the two counts was >0.99 (Pearson's product-moment correlation coefficient, p < 0.001). The diameter of 20 eggs was measured, with a calibration factor, to the nearest 0.01 mm. As no samples were collected close to hatching, even at the end of May, the eggs were still spherical rather than the oblong shape they take later (Herrick, 1909). A note was also made of eggs with developing embryos (i.e. eyed), and the dry weight was estimated by drying a sample of 50 eggs at 70ºC for a minimum of 3 d.
Analysis of covariance (ANCOVA) was used to analyse differences between seasons and between wild and cultured lobsters, using CL as the covariate. When other statistical tests were used, the test is specified below.
| Results |
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In all, 111 wild and 104 cultured, ovigerous female lobsters were collected during the three seasons, autumn 1996, autumn 1997, and spring 1997 (Table 1). The hatchery-reared females released from 1990 to 1994 were, on average, smaller than the wild females as a result of their not being grown to larger sizes. Ovigerous cultured females ranged in size from 74 to 113 mm CL, and the largest wild, berried female was 151 mm CL, so making the size ranges being compared rather uneven. The total number of eggs per lobster varied from
4000 for the smallest female of 74 mm CL (cultured) to as many as 40 000 for the largest of 151 mm CL (wild) (Figure 2). Females below the minimum legal size of 88 mm CL all had fewer than 11 000 eggs.
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There were no significant differences in the size–fecundity relationship between seasons (p > 0.05) or between wild and cultured lobster (p > 0.05). A linear model best described the relationship between fecundity and CL, though power-fitted and log-fitted models also gave a high coefficient of determination (Table 2). Examination of the residuals revealed that the data exhibited homoscedasticity, i.e. with neither outliers nor increased variability in the number of eggs with increasing values of CL, so the linear model would likely be the most appropriate. However, the difference between the models (linear, power, or logarithm) was very small, and the power-fitted model was preferred because of its volumetric measure (fecundity F = 0.0045 CL3.22). The relationships were similarly determined for fecundity vs. AW, because the eggs are stored ventrally on the abdomen. The coefficients of determination were similar to those found when considering CL (Table 2).
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The total egg weight, recorded fresh and wet, varied from 13 g for the smallest female of 74 mm CL to as much as 196 g in a female of 147 mm CL (Figure 3). There was a tendency for egg weight in late May to be slightly greater than in October, but the difference was not significant (p > 0.05). In this case, no differences were found between wild and cultured lobster (p > 0.05). A linear correlation best described the relationship between CL and egg weight (total egg weight = 2.38 CL – 178.3).
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The eggs clearly increased in size during the incubation period, in this case comparing October data (recently spawned) with those of May (before hatching) (Figure 4). There was a great variation in egg size with mother size, especially just after spawning, i.e. in autumn. For instance, in autumn 1997, a female of 87 mm CL yielded the smallest eggs with a mean diameter of 1.50 mm, whereas another female of the same size had eggs 1.84 mm in diameter. There was a tendency, although not significant, that larger females produced larger eggs overall than smaller females, especially in spring 1997. The relationship appears to reach an asymptote at
2.0–2.1 mm egg diameter, few eggs being found larger than that.
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The mean dry weight of eggs per mother size did not vary between season (p > 0.05), nor between wild and cultured lobster (p > 0.05; Figure 5). There was, however, large variation with mother size, especially below 90–100 mm CL, and in general the dry weight per egg increased with increasing mother size. Whether linear-, power-, or log-fitted, 53–55% of the observations could be explained, but the log function fitted best (dry weight per egg = 1.2286 ln CL – 4.1827). There was also great variation in the number of eggs produced per gramme of total egg mass. It decreased with increasing mother size from an average of 320 eggs g–1 egg mass to
200 eggs g–1. The last value seemed to be the asymptotic value for females
100 mm CL.
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Eyed eggs were found in all seasons, and obviously all eggs were eyed close to hatching in late May (in this case in spring 1997; Figure 6). Differences between wild and cultured lobster in the percentage of eggs eyed were not significant in any season (p > 0.5; Mann–Whitney U-test). Some 12.5% and 10.6% of wild and cultured females, respectively, had eyed eggs during October 1996. The corresponding percentages for 1997 were much higher, 75% and 63.8% for wild and cultured lobster, respectively. There seemed to be a size-specific trend in autumn 1996, larger females having a greater percentage of eyed eggs, but this was not the case in autumn 1997 (Figure 6).
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| Discussion |
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No significant differences in size-specific fecundity, weight of egg mass, and development of embryo and egg size (diameter and dry weight) between cultured lobster, i.e. hatchery-reared and released as juveniles, and wild lobsters could be found. Egg loss was not found for either category. These results are important when considering future stock-enhancement or restocking programmes aimed at increasing wild lobster populations. They also shed light on aspects of egg production of the lobster population off southwestern Norway, as discussed later.
Three models were fitted to size-specific fecundity, simple linear, power curve, and logarithmic (Table 2), to illustrate that the difference in the correlation, an average of 3%, is very small. Therefore, which model to apply seems of little relevance. This was also the conclusion Somers (1991) made after attempting to find a general model for the size–fecundity relationship in 17 crustacean species. The choice of model is perhaps more important for comparisons with other studies. In publications on European lobster, a linear function is most often applied (Hepper and Gough, 1978; Latrouite et al., 1984; Bennet and Howard, 1987; Free et al., 1992; Roberts, 1992), and that is also the model with the best correlation in this study. However, the power function seems to have been preferred more recently (Tully et al., 2001; Lizárraga-Cubedo et al., 2003). Studies on American lobster (Homarus americanus) have generally used a power-fitted model (Saila et al., 1969; Perkins, 1971; Ennis, 1981; Campbell and Robinson, 1983; Campbell and Brattey, 1986; Estrella and Cadrin, 1995). The power-fitted model is also chosen here mainly because of its volumetric nature.
Fecundity estimates for the European lobster from various geographical regions from southwest France to northeast England vary considerably (Table 3). For instance, the number of eggs for a female of 100 mm CL varies from 5200 to 12 500. Two areas stand out; southwest Scotland (Lizárraga-Cubedo et al., 2003) and southwest Norway (this paper). Lobsters sampled in southwest Scotland had the lowest individual estimates of fecundity and those sampled off southwest Norway had some of the highest estimates across size groups, perhaps indicative of stock differences. Tully et al. (2001) did not find significant differences in the relationships between size and fecundity of European lobsters for four regions around Ireland. Nor did Lizárraga-Cubedo et al. (2003) find significant differences when comparing lobsters from the Hebrides with those of southwest Scotland. However, Bennet and Howard (1987) did find a significant difference between lobsters off northeast and southwest England. In most of these studies, the samples were collected from cooperatives or at landing points. This could contribute to the variability observed because berried females tend to lose their eggs if handled too much or when kept at high densities (Herrick, 1909). The methodologies and sampling procedures applied across studies likely preclude detecting real population differences.
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American lobster fecundity estimates are in general higher than those of the European lobster, e.g. the studies made in the Gulf of Maine and outer Cape Cod (Estrella and Cadrin, 1995), Newfoundland (Ennis, 1981), Nova Scotia (Campbell and Robinson, 1983), and the Grand Manan area (Campbell and Brattey, 1986). In the current comparison, southwest Norway falls within estimates for lobster <110 mm CL, but at larger size, American lobsters are clearly more fecund than Norway's European lobsters.
The water content in a lobster egg increases as the embryo develops (Pandian, 1970; Sasaki et al., 1986; Roberts, 1992). Ethanol (Lizárraga-Cubedo et al., 2003), formalin (Estrella and Cadrin, 1995), ethanol-glycerin solution (Silbert et al., 2004), and formol–saline solution (Free, 1994), as well as freezing (Quellet and Plante, 2004) have been used to preserve lobster eggs before measuring the diameter. Therefore, comparing egg diameter between species, regions or populations might lead to erroneous conclusions when different methods have been applied and a conversion factor between the different preservation methods is not available. Silbert et al. (2004) measured fresh egg diameter in seven American lobster females from August in one year to June the following year. Fresh egg size varied from 1.65 to 1.83 mm just after being spawned, and from 1.75 to 2.0 mm towards the end of the incubation period. This is within the size range found in this study on European lobster.
Dry weight is another measure of the size of an egg, and in this study, it varied from
1.0 to 1.9 mg, comparable with results for southern England (Roberts, 1992) and Ireland (Tully et al., 2001). In the latter study, there was a slight tendency for eggs from lobsters sampled off the western coast of Ireland to be somewhat heavier than those of lobsters caught off the southeast coast of Ireland, indicating the possibility of regional or population differences, although the authors did not highlight this point. On the other hand, the egg dry weight of American lobsters is reported to be in general <1.0 mg (Attard and Hudon, 1987; Silbert et al., 2004), revealing a difference between the two species. In this study, there was a general increase in egg diameter and egg dry weight with increasing mother size. Egg dry weight did not vary throughout the incubation period and is unlikely to be affected by the method of preservation, thus making dry weight a better measure of egg size.
Fecundity studies have most commonly been made on female lobsters when the eggs are close to hatching, because egg loss is considered to be significant during the long incubation period of
9 months (Aiken and Waddy, 1986; Attard and Hudon, 1987; Talbot, 1991). However, few studies have documented regular loss. In American lobster, the only study of egg loss during incubation is that of Perkins (1971), which documents a decrease from October to April, and further to June, giving a total egg loss of 36%. In that study, the lobsters were captured with an otter trawl, so it is possible that the method of capture may have influenced egg loss. Trawling-induced egg loss (11–22%) has, for instance, been documented for Norway lobster (Nephrops norvegicus) by Chapman and Ballantyne (1980) and Briggs et al. (2002). For a stock of European lobsters off France, Latrouite et al. (1984) found a difference of 27% egg loss between females with less advanced (eye index < 200) and those with advanced developed eggs (eye index > 500). Those samples came from commercial lobster dealers. Free (1994) also documented an egg loss of 6–20%, but the range in size-specific fecundity was greater, making it unlikely that the data, and therefore the analysis, were sufficiently robust to support the overall conclusion on egg loss.
In this study, no significant differences in the size–fecundity relationship between seasons were found, so I conclude that no egg loss took place between October 1996 and May 1997. Likewise, Lizárraga-Cubedo et al. (2003) did not record egg loss in lobsters from the Hebrides, nor off southwest Scotland. However, females carrying eggs close to hatching have a greater chance of losing their eggs in handling. One explanation might be that the egg stalk holds a larger egg when close to hatching and the attachment might therefore be weaker. It is in any case important that care be taken when studying egg loss as a natural phenomenon, to minimize errors attributable to handling-induced loss. It is not likely, based on the published literature, that egg loss is regular over every incubation period. However, it cannot be ruled out that egg loss might be significant in some seasons, for reasons such as insufficiency of food or environmental fluctuations, neither of which have yet been studied as a cause.
| Acknowledgements |
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I thank the Kvitsøy fishers who provided the berried females for their genuine interest in the work and fruitful discussions. I am also indebted to Knut E. Jørstad, Tore Kristiansen, Eva Farestveit, Harald Ness, and Einar Nøstvold for their support, and particularly for providing their insights on lobster biology and their willingness to share thoughts and ideas. Thanks are also due to the anonymous referee who took time to review and improve the draft manuscript.
| References |
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-
Agnalt A-L., Jørstad K. E., Kristiansen T., Nøstvold E., Farestveit E., Næss H., Paulsen O. I., et al. Enhancing the European lobster (Homarus gammarus) stock at Kvitsøy Islands; perspectives of rebuilding Norwegian stocks. In: Stock Enhancement and Sea Ranching—Leber K. M., Kitada S., Blankenship H. L., Svåsand T., eds. (2004) Oxford: Blackwell. 415–426. Developments, Pitfalls and Opportunities.
Agnalt A-L., van der Meeren G. I., Jørstad K. E., Næss H., Farestveit E., Nøstvold E., Svåsand T., et al. Stock enhancement of European lobster (Homarus gammarus); a large-scale experiment off south-western Norway (Kvitsøy). In: Stock Enhancement and Sea Ranching—Howell B., Moksness E., Svåsand T., eds. (1999) Oxford: Fishing News Books. 401–419.
Aiken D. E., Waddy S. L. Environmental influence on recruitment of the American lobster, Homarus americanus: a perspective. Canadian Journal of Fisheries and Aquatic Sciences (1986) 43:2258–2270.
Appelöf A. Undersøkelser over hummeren (Homarus vulgaris) med særskilt hensyn til dens optræden ved Norges kyster [Investigations of lobster (Homarus vulgaris) with special emphasis on its behavior on the Norwegian coast]. In: Efter foranstaltning av Stavanger filial av selskapet for de Norske fiskeriers fremme. (1909) Bergen: A. S. Johns Griegs Boktrykkeri. 154. +10 illustrations.
Attard J., Hudon C. Embryonic development and energetic investment in egg production in relation to size of female lobster (Homarus americanus). Canadian Journal of Fisheries and Aquatic Sciences (1987) 44:1157–1164.
Bennet D. B., Howard A. E. Estimates of lobster (Homarus gammarus) fecundity from east and west Britain. (1987) ICES Document CM 1987/K: 47.
Briggs R. P., Armstrong M. J., Dickey-Collas M., Allen M., McQuaid N., Whitmore J. The application of fecundity estimates to determine the spawning stock biomass of Irish Sea Nephrops norvegicus (L.) using the annual larval production method. ICES Journal of Marine Science (2002) 59:109–119.
Campbell A., Brattey J. Egg loss from the American lobster, Homarus americanus, in relation to nemertean, Pseudocarcinonemertes homari, infestation. Canadian Journal of Fisheries and Aquatic Sciences (1986) 43:772–780.
Campbell A., Pezzack D. S. Relative egg production and abundance of berried lobsters, Homarus americanus, in the Bay of Fundy and off southwestern Nova Scotia. Canadian Journal of Fisheries and Aquatic Sciences (1986) 43:2190–2196.
Campbell A., Robinson D. G. Reproductive potential of three American lobster (Homarus americanus) stocks in the Canadian maritimes. Canadian Journal of Fisheries and Aquatic Sciences (1983) 40:1958–1967.
Chapman C. J., Ballantyne K. A. Some observations on the fecundity of Norway lobsters in Scottish waters. (1980) . ICES Document CM 1980/K: 25.
Ennis G. P. Fecundity of the American lobster, Homarus americanus, in Newfoundland waters. Fishery Bulletin US (1981) 79:796–800.
Ennis G. P., Fogarty M. J. Recruitment overfishing reference point for the American lobster, Homarus americanus. Marine and Freshwater Research (1997) 48:1029–1034.[CrossRef][Web of Science]
Estrella B. T., Cadrin S. X. Fecundity of the American lobster (Homarus americanus) in Massachusetts coastal waters. ICES Marine Science Symposia (1995) 199:61–72.
Fogarty M. J., Idoine J. S. Application of yield and egg production model based on size to an offshore American lobster population. Transactions of the American Fisheries Society (1988) 117:350–362.[CrossRef]
Free E. K. Reproductive processes in the European lobster, Homarus gammarus. (1994) University of Southampton. 447. PhD thesis.
Free E. K., Tyler P. A., Addison J. T. Lobster (Homarus gammarus) fecundity and maturity in England and Wales. (1992) ICES Document CM 1992/K: 43.
Gendron L. Impact of minimum legal size increases on egg-per-recruit production, size structure, and ovigerous females in the American lobster (Homarus americanus) population off the Magdalen Islands (Quebec, Canada): a case study. New Zealand Journal of Marine and Freshwater Research (2005) 39:661–674.[Web of Science]
Hepper B. T., Gough C. J. Fecundity and rate of embryonic development of the lobster, Homarus gammarus (L), off the coast of North Wales. Journal du Conseil International pour l'Exploration de la Mer (1978) 38:54–57.
Herrick F. H. Natural history of the American lobster. Bulletin of the US Bureau of Fisheries (1909) 29:148–408.
Hobday D. K., Ryan T. J. Contrasting sizes at sexual maturity of southern rock lobsters (Jasus edwardsii) in the two Victorian fishing zones: implications for total egg production and management. Marine and Freshwater Research (1997) 48:1009–1014.[CrossRef][Web of Science]
Latrouite D., Morizur Y., Raguenes G. Fecondites individuelles et par recrue du homard Europeen. (1984) ICES Document CM 1984/K: 38.
Lizárraga-Cubedo H. A., Tuck I., Bailey N., Pierce G. J., Kinnear J. A. M. Comparisons of size at maturity and fecundity of two Scottish populations of the European lobster, Homarus gammarus. Fisheries Research (2003) 65:137–152.[CrossRef][Web of Science]
Pandian T. J. Ecophysiological studies on the developing eggs and embryos of the European lobster Homarus gammarus. Marine Biology (1970) 5:154–167.[CrossRef]
Perkins H. C. Egg loss during incubation from offshore northern lobsters (Decapoda: Homaridae). Fishery Bulletin US (1971) 69:451–453.
Quellet P., Plante F. An investigation of the sources of variability in American lobster (Homarus americanus) eggs and larvae: female size and reproductive status, and interannual and interpopulation comparisons. Journal of Crustacean Biology (2004) 24:481–495.[CrossRef][Web of Science]
Roberts E. A. Fecundity of the European lobster Homarus gammarus (L.) from the central south coast of England. (1992) University of Southampton. 53. MSc thesis.
Rørvik C. J., Tveite S. A stock assessment of lobster (Homarus gammarus) on the Norwegian Skagerrak coast. Flødevigen Rapportserie (1982) 3:1–20.
Saila S. B., Flowers J. M., Hughes J. T. Fecundity of the American lobster, Homarus americanus. Transactions of the American Fisheries Society (1969) 98:537–539.[CrossRef]
Sasaki G. C., Capuzzo J. M., Biesiot P. Nutritional and bioenergetic considerations in the development of the American lobster Homarus americanus. Canadian Journal of Fisheries and Aquatic Sciences (1986) 43:2311–2319.
Silbert V., Quellet P., Brêthes C. Changes in yolk total proteins and lipid components and embryonic growth rates during lobster (Homarus americanus) egg development under a simulated seasonal temperature cycle. Marine Biology (2004) 144:1075–1086.[CrossRef]
Somers K. M. Characterizing size-specific fecundity in crustaceans. In: Crustacean Egg Production—Wenner A., Kuris A., eds. (1991) Rotterdam: Balkema. 357–378. Crustacean Issues, 7.
Talbot P. Ovulation, attachment and retention of lobster eggs. In: Crustacean Egg Production—Wenner A., Kuris A., eds. (1991) Rotterdam: Balkema. 9–18. Crustacean Issues, 7.
Tully O., Roantree V., Robinson M. Maturity, fecundity and reproductive potential of the European lobster (Homarus gammarus) in Ireland. Journal of the Marine Biological Association of the UK (2001) 81:61–68.[CrossRef]
van der Meeren G. I., Uglem I., Tveite S., Korsøen E., Jørstad K. E. Hummer – biologi, fiske og forvaltning [Lobster – biology, fishery and management]. Fisken og Havet (1995) 20:36.
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