Comparisons between the reproductive biology of females of two species of deep sea crabs that live in different water depths.

ABSTRACT The reproductive biology of females of Hypothalassia acerba and Chaceon bicolor off the lower west coast of Australia, and of the former species off the southern coast of Western Australia, are compared. The trends exhibited throughout the year by the prevalence of different stages in ovarian development and of females bearing eggs and egg remnants, together with those of relative gonad weight, demonstrate that the reproduction of H. acerba on the lower west coast is highly seasonal. Thus, overall, gonads matured progressively between July and December and oviposition occurred between January and March. The characteristics of H. acerba on the south coast differed in the following ways from those on the lower west coast: (1) no ovigerous females and only two females with egg remnants were caught; (2) late yolk granule oocytes were not developed in ovaries until females had reached a larger size; and (3) investment in gonadal development was less. These results strongly indicate that conditions on the south coast are not as conducive for ovarian development and reproduction and that females migrate from the south to lower west coast for spawning. In contrast to H. acerba, C. bicolor reproduces throughout the year on the lower west coast, presumably reflecting its occupancy of far deeper waters where environmental conditions vary less during the year. Although the mean weights of ovigerous females of H. acerba and C. bicolor were not significantly different (P > 0.05), the mean fecundity of the former species (356,210) was significantly greater (P < 0.001) than the latter species (192,070). The greater fecundity of H. acerba may reflect adaptations by this seasonal spawner to optimize egg production during its short breeding season.

KEY WORDS: crabs, reproduction, spawning period, water depth, seasonality, gonadal investment

INTRODUCTION

Three species of deep sea crab are fished commercially in Western Australian waters, namely the champagne crab Hypothalasia acerba Koh and Ng, the crystal crab Chaceon bicolor Manning and Holthuis, and the king crab Pseudocarcinus gigas Lamarck (Anonymous 2002). Based on catches obtained by commercial fishers, the distribution of H. acerba ranges from a latitude at least as far north as about 27[degrees]S on the west coast, southwards, and then eastwards along the south coast to a longitude of at least 129[degrees]E (Anonymous 2002). Although C. bicolor occurs in the same geographical region as H. acerba, its distribution in Western Australia extends further north to a latitude of about 22[degrees]S (Melville-Smith et al. in press). In contrast, the distribution of P. gigas is essentially restricted to the south coast in Western Australia and extends eastwards across the full length of Australia, including Tasmania, and then northwards on the east coast to about 31[degrees]S (Kailola et al. 1993, Gardner 1998).

Recent depth-stratified sampling off the south-western Australian coast has demonstrated that H. acerba occurs predominantly in waters where temperatures lie between 13[degrees]C and 19[degrees]C, the depths range from 200-255 m on the lower west coast, and from 90-200 m on the south coast (Smith et al. 2004a). Temperatures recorded during commercial fishing for C. bicolor show that on the lower west coast of Australia this species typically occurs in waters of 4[degrees]C to 6.5[degrees]C (K. Smith unpublished data) and at water depths of 450-1220 m (Melville-Smith et al. in press); thus this species is located further offshore than H. acerba. Pseudocarcinus gigas is found in waters of 11 [degrees]C to 17[degrees]C and at depths of 120-340 m (Levings et al. 1996).

The commercial fisheries for H. acerba and C. bicolor in Western Australia started to develop during the late 1990s (Anonymous 2002). However, in contrast to the situation with P. gigas (see Levings et al. 1996, 2001, Gardner 1997, Gardner & Williams 2002), no biological studies have been conducted on the spawning period and location and fecundity of either of these two species.

The stages in development of the ovaries of several species of deep sea crabs belonging to the Geryonidae (e.g., Chaceon quinquedens, Smith; Chaceon maritae, Manning & Holthuis; and Chaceon affinis, Milne Edwards & Bouvier), have been described based on their macroscopic appearance and, in some cases, on the stages of maturation of their oocytes, as determined from histologic sections (Haefner 1977, Melville Smith 1987a, Fernandez-Vergaz et al. 2000, Lrpez Abellfin et al. 2002). No such combined macroscopic and histologic studies have been carried out on any deep sea species of the Eriphiidae, the family to which H. acerba belongs. Although some deep sea crab species, such as Chaceon fenneri (Manning & Holthuis), have an annual reproductive cycle (see Hastie 1995), no clear seasonal fluctuations in reproductive patterns were detected in C. maritae (Melville-Smith 1987a) and C. quinquedens (Wigley et al. 1975, Haefner 1978). It was proposed by Melville-Smith (1987a) that the absence of a distinct reproductive cycle in C. maritae was attributable to the absence, in the deep waters in which this species is found, of changes in day length and temperature and other potential environmental reproductive triggers.

The aims of this study are as follows. (1) Describe, on the basis of their macroscopic appearance, the sequential stages in the development of the ovaries of H. acerba and use histologic sections to determine the stages of maturation of the oocytes in ovaries at each of those stages. Attention is paid to elucidating whether the criteria developed for categorizing the ovarian stages of H. acerba were the same as those we developed concomitantly for C. bicolor and those described for other species of deep sea crab. (2) Use the trends exhibited throughout the year by the monthly prevalences of female crabs with ovaries at different stages in development and of females bearing either eggs or egg remnants, together with those of the mean monthly gonad weights of females, to determine the timing of reproduction in these two species. Particular emphasis is placed on testing the hypothesis that, as H. acerba lives in far shallower waters than C. bicolor, and thus in an environment which undergoes a greater degree of seasonal change and particularly in water temperature, it is far more likely to reproduce seasonally. (3) Determine the fecundities of H. acerba and C. bicolor and their relationships to the body size and body weight of these species. (4) Establish whether aspects of the reproductive biology of H. acerba on the lower west and southern coasts of Western Australia exhibit similar patterns. Because preliminary analyses indicated that H. acerba invests less in gonadal development on the south than west coasts, we examined whether the relative ovarian weights and diameters of the mature oocytes of females on the two coasts differed.

MATERIALS AND METHODS

Collection of Samples

Samples of Hypothalassia acerba were randomly selected from trap catches taken by commercial fishers off the lower west and south coasts of Western Australia between ca. 30[degrees] 10'S, 114[degrees]30'E and 32[degrees]30'S, 114[degrees]60'E and between 34[degrees]40'S, and 115[degrees]40'E and 34[degrees]45'S, 119[degrees]30'E, respectively. Chaceon bicolor was obtained from the trap catches taken by commercial fishers off the lower west coast of Australia between 24[degrees]15'S, 112[degrees]15'E and 33[degrees]04'S, and 114[degrees]23'E. The reader is referred to Smith et al. (2004b) for details of the sampling gear. The samples of H. acerba and C. bicolor, which were collected at regular intervals between July 1999 and April 2002 and between January 2000 and December 2003, respectively, were pooled with additional smaller samples that were collected by the same methods and purchased regularly from fish markets. This ensured that the monthly prevalences of females at different stages in development and mean monthly relative gonad weights were derived from data for individuals in catches representing, on at least one occasion, each calendar month of the year in the case of each species in the waters in which they were sampled.

Laboratory Processing

The carapace length (CL) and wet weight (W) of each female of H. acerba and C. bicolor were recorded to the nearest 1 mm and 1 g, respectively. For each female, a record was kept of the relative size and shape of the gonopores and whether mating abrasions were present around their gonopores. Most females of C. bicolor with a CL <100 mm possessed elliptical gonopores, indicating that they had not mated, a conclusion consistent with the absence of mating scars in the region of their gonopores (see also Melville-Smith 1987a, Haefner 1977). Although the gonopores of female H. acerba did not exhibit such a conspicuous dichotomy in shape as those of C. bicolor, the individuals of this species with a CL <ca. 70 mm had relatively very small gonopores and, unlike many larger individuals, they never bore mating scars in the region of their gonopores. The first and small group of H. acerba were thus considered not to have mated, which is consistent with the ovaries of all such individuals being at stage I (see Table 1 in results for description of the characteristics of the different stages in ovarian development).

The ovary of each female was removed and allocated to a numerical developmental stage on the basis of macroscopic criteria (see Results). The stages in development of the testes and vas deferentia were recorded during another study aimed at determining the size at maturity of the males of these two species (Smith et al. in prep.). The ovary of each female of H. acerba and C. bicolor was weighed to the nearest 0.1 g. The mean monthly ovarian weights ([+ or -]95% CIs) at standardized CLs were determined for H. acerba on the lower west and south coasts and for C. bicolor on the former coast using analysis of covariance (ANCOVA) of the natural logarithm of the gonad weight as the dependant variable, month as a fixed factor and the natural logarithm of the CL as a covariate. Note that the standardized CL was calculated separately for the lower west and south coast assemblages of H. acerba and the lower west-coast assemblage of C. bicolor. These constant CLs were a default value calculated by the ANCOVA. ANCOVA was also used in the manner (mentioned earlier) to calculate the mean gonad weight ([+ or -]95% CIs) for H. acerba with ovaries containing previtellogenic, early vitellogenic, and late vitellogenic oocytes on the lower west and south coasts. The standardized CL was calculated separately for each of these three developmental stages, but was common for a given stage on the two coasts. Data for the small individuals that were considered not to have mated were not used when calculating the monthly prevalences of females with ovaries at different stages in development, the mean monthly gonad weights for females at a standardized CL, and the mean gonad weights for west and south coast H. acerba with ovaries at different stages in development (see Figs. 2, 3, 4, and 5 in Results).

The method of Melville-Smith (1987a) was used for determining the fecundity of H. acerba and C. bicolor. Thus, alternate pleopods were removed from the abdomen of each ovigerous female and soaked for 1-4 h in 0.5 M NaOH to facilitate the separation of eggs from the pleopod setae. All of the eggs removed from each crab were pooled, oven dried at 70[degrees]C for 24 h and then weighed to the nearest 0.001 g. Subsamples of ca. 0.1 g of eggs (= ca. 300 eggs) were then weighed and counted, and the average weight of a single egg in each subsample was calculated. When estimates of the weight of a single egg in three subsamples differed by less than 5%, the mean of those weight estimates was then used, in conjunction with twice the weight of all eggs removed, to estimate the fecundity of the crab.

The right posterior side of the ovary was removed from up to 20 females of both species in each season, ensuring that these subsamples covered the full size range of those species in the total catch in each season. The ovarian material was fixed in 4% glutaraldehyde in a 0.025 M phosphate buffer solution (pH 7.0), dehydrated in a series of increasing concentrations of ethanols, embedded in paraffin wax, sectioned transversely at 6 [micro]m, and stained with Mallory's trichrome. The ovarian material was fixed in glutaraldehyde because it was not fixed well by traditional fixatives used for light microscopy, such as Bouin's and 10% formalin. The smallest and largest diameters of oocytes of H. acerba and C. bicolor at different developmental stages sectioned through their nuclei were measured to the nearest 5 [micro]m. The smallest and largest diameters of each oocyte were then averaged.

In addition to the earlier mentioned laboratory processing of crabs, the senior author also recorded, when on board fishing vessels, the total number of mature female crabs caught and the percentage of both ovigerous females and of females with egg remnants attached to their pleopods. Note that, due to inclement weather, the commercial fisher with whom we mainly worked did not operate in September in the deep waters off the lower west coast of Australia where C. bicolor is found, and thus there are no data on the above variables for that month.

RESULTS

Ovarian Maturation Stages

Based on their macroscopic appearance, the ovaries of the females of Hypothalassia acerba and Chaceon bicolor each followed essentially the same pattern of development (Table 1). Thus, for both species, six sequential stages were recognized (Table 1; Fig. 1). As they progress from stages I to IV, the ovaries increase progressively in size and change color (see Figs. 1a to d). However, the colors of the ovaries of the two species at stages III and IV differ. In both species, ovaries at stages V and VI are flaccid and could not be separated macroscopically.

[FIGURE 1 OMITTED]

At a histologic level, cortical alveolar oocytes first appeared in stage II ovaries of H. acerba (see Figs. 1a, b), and the presence of early and late yolk granule oocytes characterized stage III (see Fig. 1c) and IV ovaries (see Fig. 1d), respectively. Ovaries of recently spent females (stage V) of H. acerba contained some atretic oocytes (see Fig. 1e), whereas those of spent-recovering (stage VI) females possessed no such oocytes but did contain numerous early previtellogenic ooctytes (see Fig. 1f). The histologic characteristics of the ovaries of C. bicolor are essentially the same as those shown for H. acerba in Figures 1a to f. However, the mean diameters of the mature oocytes, as measured in stage IV ovaries, are significantly greater (P < 0.001) for C. bicolor than H. acerba.

Comparisons of the macroscopic and microscopic characteristics of our ovarian stages for H. acerba and C. bicolor with those of Haefner (1977) demonstrate that the ovaries of the former two species undergo the same pattern of development as Chaceon quinquedens. However, the maximum diameter of the oocytes in our stage I (70 [micro]m) is far less than that recorded by Haefner (1977) for his first stage for C. quinquedens (172 [micro]m) and yolk granule oocytes are already present in his stage II whereas they do not appear until stage III of our categorization for H. acerba and C. bicolor. In essence, Haefner (1977) did not recognize the presence of the early stage we have termed virgin/immature resting. However, that stage was recognized by de Lestang et al. (2003) in their description of ovarian development in Portunus pelagicus (Linnaeus) in inshore waters in Western Australia. Furthermore, unlike the study of Haefner (1977), our histologic staging criteria distinguish recently-spent ovaries from spent-recovering ovaries, which is useful for obtaining an idea of how recently ovulation had occurred.

Monthly Trends in Reproductive Indices

On the lower west coast, the prevalence of female H. acerba with ovaries containing late vitellogenic oocytes was greatest in September to February, during which months their contributions ranged from 58% to 76%, and was least in March to June when their monthly contributions ranged from 11% to 50% (Fig. 2a). The prevalence of female crabs with ovaries containing only previtellogenic oocytes was less than 12% in each month from September to February and in April and only exceeded 30% in March and August. Small numbers of spent females were collected between January and March and in May. The mean monthly gonad weight of H. acerba, standardized to a constant CL of 94.7 mm, rose progressively from 11.5 g in July to between 25.2 and 28.6 g in October to December, and then it declined sequentially to between 4.9 and 8.3 g in March to May (see Fig. 2b). The prevalence of female H. acerba bearing egg remnants declined sequentially from 12% in July to zero or close to zero in October to January before rising progressively to 21% in May. Small numbers of ovigerous females were caught in February, March, and May (see Fig. 2c) and a commercial fisher provided six ovigerous females and two females with egg remnants, which he had caught in January 2000.

[FIGURE 2 OMITTED]

On the south coast, the prevalence of female H. acerba containing late vitellogenic oocytes and the mean monthly gonad weights, standardized to a common CL of 95.2 mm, peaked in September (Figs. 3a, b). The prevalence of H. acerba with ovaries containing late vitellogenic oocytes never exceeded 47% in any month other than September and the prevalence of ovaries with previtellogenic oocytes exceeded 50% in 5 months (see Fig. 3a). Samples from the south coast yielded no ovigerous females and only two females bearing egg remnants, both of which were caught in August.

[FIGURE 3 OMITTED]

The prevalences of females of C. bicolor with ovaries containing late vitellogenic oocytes were greater in July to December than in January to April and in June (Fig. 4a). The mean monthly gonad weights, standardized to a constant CL of 110.0 ram, peaked at 42.2 g in September and 43.1 g in December before declining to 11.6 g in February, increasing to 37.1 g in May and then declining to 8.8 g in June (see Fig. 4b). Ovigerous females were caught in each of the 11 calendar months in which samples were obtained and females bearing egg remnants were found in 6 of those months (see Fig. 4c). The mean gonad weight [+ or -] 95% CIs, standardized to a constant CL, did not differ significantly (P > 0.05) between the assemblages on the lower west and south coasts when the females contained ovaries with either previtellogenic or early vitellogenic eggs (Fig. 5). In contrast, the mean gonad weight [+ or -]95% CIs for females of H. acerba with ovaries containing late vitellogenic oocytes was significantly greater (P < 0.001) for the assemblage on the lower west coast, 26.4 [+ or -] 1.71 g, than that on the south coast, 16.0 [+ or -] 1.85 g (see Fig. 5).

[FIGURES 4-5 OMITTED]

The relationships between gonad W and CL of west coast and south coast females of H. acerba with ovaries containing late vitellogenic oocytes (Fig. 6) are described by the following equations.

[FIGURE 6 OMITTED]

West coast: ln(W) = 2.561ln(CL) - 8.130; P < 0.001, R2 = 0.240, n = 228

South coast: ln(W) = 6.430ln(CL) - 26.311; P < 0.001, R2 = 0.442, n = 34

Although none of the females of H. acerba from the south coast, which had CLs <90 mm, contained ovaries with late vitellogenic oocytes, many females of H. acerba from the lower west coast with CLs of 75 to 90 mm possessed ovaries with oocytes at this advanced stage. The use of ANCOVA demonstrated that, in the case of H. acerba for a standardized selected CL, the mean gonad weight of crabs was significantly greater on the lower west coast than south coast (P < 0.001).

To enable predictions of CL from W and vice versa for H. acerba, the regression equations relating these 2 variables are:

West coast: ln(W) = 2.809ln(CL) - 6.400; P < 0.001, R2 = 0.946, n = 581

South coast: ln(W)= 2.768ln(CL) - 6.128; P < 0 0.001, R2 = 0.893, n = 185

The mean lengths ([+ or -]95% CIs) of females from the lower west (93.8 [+ or -] 2.02 mm) and south coasts (93.0 [+ or -] 1.39 mm) were not significantly different (P > 0.05) when the individuals contained previtellogenic oocytes, whereas the corresponding values of 94.7 [+ or -] 0.91 mm and 99.1 [+ or -] 1.37 mm for females with late vitellogenic oocytes on those two coasts were significantly different (P < 0.001). These differences are reflected in the fact that the distributions of the CLs of female H. acerba on the south coast were located more to the right than those on the lower west coast in the case of females with late vitellogenic oocytes, whereas this was not so with females with previtellogenic oocytes (Fig. 7a, b).

[FIGURE 7 OMITTED]

The mean diameters ([+ or -]95% CIs) of late vitellogenic oocytes of H. acerba from the lower west coast (357.7 [+ or -] 10.79 [micro]m, n = 342) and south coast (370.3 [+ or -] 8.16 [micro]m, n = 134) were not significantly different (P > 0.05).

The fecundities of H. acerba ranged from 202,295 to 488,758 for crabs with CLs of 90 mm and 102 mm, respectively. The minimum and maximum fecundities for C. bicolor were 15,592 and 288,512 respectively, for crabs with CLs of 98 and 133 mm respectively. The mean fecundities ([+ or -]95% CIs) of H. acerba (i.e., 356,210 [[+ or -] 64,297]) and C. bicolor (i.e., 192,070 [[+ or -] 33 640]), were significantly different (P < 0.001). Although the mean body weights ([+ or -] 95% CIs) of the ovigerous females of H. acerba used for the above fecundity estimates (i.e., 587.4 [[+ or -] 96.5 g]) were substantially less than that of C. bicolor (i.e., 651.9 [[+ or -]61.3 g]), those means were not significantly different (P > 0.05). The relationships between fecundity (F) and the CL and wet W of the two species are shown in Figures 8a to d and are described by the following regression equations:

[FIGURE 8 OMITTED]

Hypothalassia acerba

lnF = 3.44ln(CL) + 1.235, P < 0.05, R2 = 0.486, n = 10 F = 0.005W + 0.608, P < 0.05, R2 = 0.569, n = 10

Chaceon bicolor

lnF = 2.957ln(CL) + 1.686, P < 0.05, R2 = 0.127, n = 40 F = 0.003W + 0.1572, P < 0.05, R2 = 0.260, n = 40

DISCUSSION

Comparisons Between Hypothalassia acerba on the West and South Coasts

The trends exhibited by the three reproductive variables recorded for the females of Hypothalassia acerba on the lower west coast of Australia were consistent with each other and clearly imply that reproduction in this deep sea species is highly seasonal. Thus, the increase in the prevalence of females with ovaries containing late vitellogenic oocytes between July and October and subsequent leveling oft" to December was paralleled by a progressive rise and then leveling off in the mean monthly relative gonad weights. Likewise, the subsequent decline in the prevalence of females with this category of advanced ovary between December and March was accompanied by a pronounced decline in the mean monthly relative gonad weights. Furthermore, spent females were found in the short period of January to March, which yielded most of the ovigerous females obtained during this study. It is also highly relevant that the prevalence of female H. acerba bearing egg remnants rose progressively from zero or low levels in October to January to peak in May and subsequently declined sequentially to zero between July and October. The consistent trends exhibited by the monthly data for the three reproductive variables strongly suggest that oviposition occurs mainly in January to March.

The patterns exhibited by the reproductive variables for female H. acerba on the south coast of Western Australia differed markedly from those displayed by this species on the lower west coast. Thus, on the south coast, the prevalence of females with late vitellogenic oocytes and the mean monthly relative gonad weights both peaked in September rather than December and the overall prevalence of females with ovaries containing previtellogenic oocytes was far higher. Moreover, no ovigerous female crabs and only two females with egg remnants were collected on the south coast. This strongly suggests that very little reproduction occurs on the south coast.

The possibility that the lack of capture of ovigerous females of H. acerba on the south coast is due to females moving inshore prior to oviposition, as occurs, for example, with Chaceon affinis, Chaceon quinquedens, Chaceon maritae, and Chionoecetes opilio (Fabricus) (Haefner 1978, Melville-Smith 1987a, Comeau et al. 1998, Hastie 1995, Lopez Abellan et al. 2002) seems unlikely. This conclusion is based on the results of our stratified sampling in sequential water depth intervals from 35 m to 365 m, which showed that the females and males of H. acerba were both largely concentrated in a relatively narrow range of water depths of 200255 m off the lower west coast and of 90-200 m off the south coast, and that no crabs were caught in water depths of 35 m (Smith et al. 2004a). However, it is relevant that, although the catches of H. acerba on both coasts contained a greater number of males than females, that difference was substantially greater on the south coast (Smith et al. 2004a). The earlier mentioned data on H. acerba suggest that, at some stage prior to oviposition, the females of H. acerba on the south coast typically migrate eastwards and then northwards on the lower west coast where they extrude their eggs.

The conclusion that the females of large and maturing H. acerba undergo considerable migratory movements is consistent with the observation that such movements are undertaken, in particular, by mature females of some other species of deep sea crabs (e.g., Chaceon fenneri, C. quinquedens, and C. maritae [Melville-Smith 1987b, Lockhart et al. 1990]). Some species of lobster also move substantial distances, including the western rock lobster Panulirus cygnus George, along the west coast of Australia (Phillips 1983, Melville-Smith & Cheng 2002). In decapods, these types of movements are often related to reproduction and enable those species to return to their spawning locations as mature adults after they have been transported as larvae or juveniles away from the areas of spawning (e.g., Bennett & Brown 1983, Moore & MacFarlane 1984, Stewart & Kennelly 1988, Groeneveld & Branch 2002). In the context of possible larval movement in south western Australia, it is relevant that the important Leeuwin current flows southwards along the lower west coast of Australia and then eastwards along the south coast and extends to a depth of 350 m (Pearce & Griffiths 1991). It is thus proposed that the larvae of/4. acerba are planktonic, as has been shown by Gardner (1998) to be the case with those of the confamilial Pseudocarcinus gigas, and would thus be likely to be transported by this major current from the areas on the lower west coast where spawning occurs. The likelihood of such transport would be enhanced by the fact that the larvae of H. acerba on the west coast are released in autumn, when the Leeuwin current is strongest (Phillips et al. 1991).

Comparisons Between Hypothalassia acerba and Chaceon bicolor

The trends exhibited by the reproductive variables for Chaceon bicolor were far less seasonal than those displayed by H. acerba. Thus, although the prevalence of females of C. bicolor with ovaries containing late vitellogenic oocytes was high in October to December, it was also relatively high in August and May and, whereas the mean monthly relative gonad weight declined between December and February, it remained high from July to December. More importantly, however, C. bicolor with spent/spent-recovering ovaries were caught in 8 months and in each season of the year, thereby indicating that oviposition occurs in most months of the year. This conclusion is consistent with the fact that ovigerous females of C. bicolor were caught in each of the 11 months for which samples were obtained for deriving this variable and that, unlike the situation with H. acerba, the prevalence of such females did not exhibit a clear pattern of change during the year. The finding that, unlike the situation with H. acerba and P. gigas, which live in similar water depths (Levings et al. 1996), C. bicolor clearly does not reproduce within a restricted part of the year and is consistent with C. bicolor occupying far greater depths and thus living in an environment that undergoes little seasonal change. The lack of conspicuous seasonality in the reproduction of C. bicolor parallels that found by Melville-Smith (1987a) for Chaceon maritae, which likewise lives in deep water. It is also consistent with the fact that the physiologic processes of the majority of organisms living in deep waters do not exhibit seasonality (Tyler 1988).

Investment in Gonadal Development by Hypothalassia acerba

It was particularly noteworthy that the mean relative gonad weights of females with late vitellogenic oocytes were far greater for the assemblage on the west coast than for that on the south coast, especially as this did not apply to females with oocytes in earlier stages of development. This strongly indicates that the females of H. acerba on the west coast invest less energy in ovarian development than those on the south coast. Furthermore, the lack of a significant difference between the size of the late vitellogenic oocytes of females on the south and lower west coasts implies that any differences in energy allocation to ovarian development on the two coasts is not reflected in differences in an allocation to individual oocytes. From the earlier mentioned data and comparisons, it seems reasonable also to assume that the number of eggs per batch produced by females of H. acerba that originated on the south coast are likely to be less than those of the individuals that spent at least most of their life on the west coast.

It is also evident from the data shown in Figure 6 that the females of H. acerba on the south coast do not start producing mature (late vitellogenic) oocytes until they have reached a substantially larger size than those on the west coast. This implies that, in terms of size, the attainment of maturity is delayed on the south coast compared with the west coast.

In summary, our results provide good circumstantial evidence that conditions are less conducive for gonadal development and reproduction by H. acerba on the south than lower west coast of Western Australia. Furthermore, they also suggest that maturing females of H. acerba migrate from the south coast, which is at the southern and cool end of the distribution of this species, to the west coast for spawning. Reproduction on the lower west coast was shown to occur seasonally in H. acerba, but throughout at least much of the year with C. bicolor, which occurs in far deeper water and thus where environmental conditions remain more constant during the year. The seasonality of reproduction by H. acerba is accompanied by producing, at any one time, a greater number of eggs per given body weight than does C. bicolor.

TABLE 1.

Macroscopic and microscopic characteristics of sequential stages in
ovarian development of Hypothalassia acerba and Chaceorz bicolor. Range
in oocyte diameters at each stage of development are provided. Scheme
has been adapted from that of Haefner (1977).

      Ovary Stage                    Macroscopic Description

Stage I                    Ovaries small but generally visible
Virgin/immature resting      macroscopically, thin and 'H' shaped.
                             (Shape is maintained for all latter stages
                             except stage IV). Oocytes not visible
                             through ovarian wall. Color varies from
                             pale grey to ivory.
Stage II                   Ovaries always visible macroscopically,
Developing                   larger than stage I and slightly
                             dorso-ventrally compressed. Ovaries
                             beginning to displace hepatopancreas.
                             Oocytes not visible through ovarian wall.
                             Color varies from ivory to white.
Stage III                  Ovaries larger than at stage II and outer
Maturing                     membrane has wrinkled appearance. Oocytes
                             not visible through ovarian wall. Ovaries
                             are pale pink in H. acerba, but range from
                             very pale yellow to yellowish orange in C.
                             bicolor.
Stage IV                   Ovaries larger than at stage III and
Mature                       consequently are no longer 'H-shaped'.
                             Ovarian wall more folded. Oocytes visible
                             through ovarian wall. Ovaries pink to red
                             in H. acerba and brown to purple in C.
                             bicolor.
Stage V                    Ovaries similar in appearance to stage II,
Recently spent               but more flaccid and yellowish-grey in
                             colour.
Stage VI                   Same as stage V.
Spent-recovering

      Ovary Stage                    Histological Description

Stage I                    Ovaries contain oogonia and small
Virgin/immature resting      previtellogenic oocytes (chromatin
                             nucleolar and perinucleolar oocytes).
                             Connective tissue and oocytes stain blue
                             with Mallory's trichrome. For H. acerba,
                             oogonia 5-10 [micro]m and small
                             previtellogenic oocytes 10-60 [micro]m.
                             For C. bicolor, oogonia 5-10 [micro]m and
                             small previtellogenic oocytes 10-70
                             [micro]m.
Stage II                   Ovaries contain all oocyte stages present in
Developing                   stage I together with cortical alveolar
                             oocytes. Cortical alveolar oocytes 60-200
                             [micro]m in H. acerba, 70-210 [micro]m in
                             C. bicolor. Cortical alveolar oocytes
                             stain blue with Mallory's trichrome,
                             except for their lipid droplets and
                             nucleolei, which stain dark red.
Stage III                  Large numbers of early yolk granule oocytes
Maturing                     present. Yolk granules in peripheral
                             region of oocyte cytoplasm. Yolk granules
                             stain orange with Mallory's trichrome and
                             are larger than lipid droplets. For H.
                             acerba, yolk granule oocytes are 160-270
                             [micro]m and for C. bicolor are 140-390
                             [micro]m.
Stage IV                   Large numbers of late yolk granule oocytes.
Mature                       Yolk granules distributed throughout
                             cytoplasm. For H. acerba yolk granule
                             oocytes are 200-480 [micro]m and for C.
                             bicolor 350-560 [micro]m.
Stage V                    Ovary contains mainly connective tissue.
Recently spent               Some yolk granule oocytes present and
                             undergoing atresia.
Stage VI                   Ovaries comprise mainly connective tissue
Spent-recovering             and numerous small previtellogenic
                             oocytes.

ACKNOWLEDGMENTS

The authors thank fishers B. Maguire, C. Neave, G. Pateman, G. Wilson, R. Prior, and T. Goodall for help with collecting samples, S. de Lestang for helpful discussion, the Australian Fisheries Research and Development Corporation, and Murdoch University for financial support.

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KIM D. SMITH, IAN C. POTTER * AND S. ALEX HESP 

* Corresponding author. E-mail: [e-mail]

Centre for Fish and Fisheries Research, School of Biological Sciences and Biotechnology, Division of Science and Engineering, Murdoch University, Murdoch, Western Australia, 6150, Australia