Journal of Experimental Marine Biology and Ecology 246 (2000) 103–123
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Elemental composition of Mysis mixta (Crustacea, Mysidacea) and energy costs of reproduction and embryogenesis under laboratory conditions Elena Gorokhova*, Sture Hansson Department of Systems Ecology, Stockholm University, 106 91 Stockholm, Sweden Received 2 May 1999; received in revised form 3 September 1999; accepted 30 November 1999
Abstract Mysis mixta were reared under laboratory conditions (temperature: 9–108C; salinity: 7‰, ad libitum food). Dry weight, ash, total carbon and nitrogen content of mysids (muscle tissue, eggs, and embryos of different developmental stages) have been analyzed. We found significant variations in ash content and elemental composition during growth and maturation for both sexes. The proportion of carbon in abdominal muscle decreased gradually from juveniles with body weight of 3–4 mg (42.9%) to males and gravid females ( | 40.0%). The nitrogen content was relatively constant (11.4% in average) with significant differences only between juveniles (11.3%) and mature females (11.6%). In embryos, carbon and nitrogen content were highest in early stages (58.6 and 14.3%, respectively). By the end of the marsupial development, carbon had decreased to 51.4% and nitrogen to 12.6%. The C:N ratio reflected the change in somatic carbon content, and the ratio decreased 6.2% from juveniles to gravid females, indicating lipids to be an energy source during maturation and reproduction. The weight-specific female investment in reproduction increases with body size. In gravid females, intersegmental growth during brooding period was observed, while males appear to store energy only for copulation and die after mating. Ontogenetic variation in body composition has implications for elemental budgets of M. mixta, its value as prey for fish and in modeling energy and nutrient cycling. 2000 Elsevier Science B.V. All rights reserved. Keywords: Mysis mixta; Energy costs; Reproduction; Embryogenesis
1. Introduction The changes that accompany development and reproduction in crustaceans are related *Corresponding author. Tel.: 1 46-8-164-256; fax: 1 46-8-158-417. E-mail address:
[email protected] (E. Gorokhova) 0022-0981 / 00 / $ – see front matter 2000 Elsevier Science B.V. All rights reserved. PII: S0022-0981( 99 )00173-2
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to considerable energetic losses and variations in elemental ratios (Nicol et al., 1995). Information on the chemical and biochemical composition of animals at different developmental stages is needed to describe these changes, to understand ecological and life history traits, and to evaluate how these patterns are further affected by environmental factors. Some aspects of elemental composition and fluctuations associated with maturation and egg production have been reported for both macro- and microinvertebrates (e.g. for copepods, Arashkevich and Drits, 1997; krill, Ikeda, 1984, 1985; Falk-Petersen, 1981; cephalopods, Bouchaud, 1991; decapod larvae, Anger and Schun, 1992; Minagawa et al., 1993). In the Baltic Sea, mysids play an important role as major forage species for herring and smelt (Aneer, 1980; Arrhenius and Hansson, 1993) and are important zooplankton predators (Hansson et al. 1990; Rudstam et al., 1992). Among the mysids, Mysis mixta (Lilljeborg, 1852) is the numerically dominant pelagic species (Rudstam et al., 1986), but very little direct information on its elemental composition is available, and in general this kind of data exists mainly for freshwater species (Salonen et al., 1976; Hakala, 1979). Mysis mixta is a boreal relict species of North-Atlantic origin, which inhabits Eastern Atlantic regions from the White Sea, Spitsbergen, Scandinavia and central and southern part of the Baltic Sea and westward to Iceland. In the Western Atlantic, it has been found in Greenland coastal waters and the eastern United States down to Cape Cod (Wigley and Burns, 1971, Blaxter et al., 1980). Generally, it is considered an annual species, although some individuals survive a second year (Grabe and Hatch, 1982; Salemaa et al., 1986; Shvetsova and Shvetsov, 1990). The species is semelparous and a cold-season breeder. In December, the population consists of mating mature males and females, and the males die shortly after copulation. The overwintering population is almost entirely composed of gravid females (Shvetsova, 1980, Rudstam et al., 1986). The young offspring are released in early spring through the beginning of summer, with a peak presumably in March, although protracted spawning periods (to July–August) have been observed (Shvetsova, 1980; Salemaa et al., 1986). Spawned females gradually disappear from the population and by the end of June, very few individuals of the previous year’s generation are normally found (Simm and Kotta, 1992). Newly released juveniles grow slowly and start to develop secondary sexual characters in June–September and complete maturation by November–December (Simm and Kotta, 1992). Like in other mysids, the embryonic and post-embryonic development of M. mixta takes place in the marsupium of the female. No information, so far, has been available on the energy investment in reproduction or about the intermediary metabolism in the developing embryos. A first step towards understanding these life history trade-offs is to observe the variations in reproductive effort in population under controlled conditions. Thus, knowledge of the reproductive life history traits and lifetime variations of biomass and body composition in terms of carbon and nitrogen in laboratory reared M. mixta is likely to provide important information about the biology and ecology of this species. The present laboratory study considers (1) the costs of reproduction and the energy losses associated with sexual differentiation and gonad development, and (2) energy expenditure for metabolic activity during egg development from early embryo to hatching. To calculate energetic equivalents, we analyzed the biomass composition in
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terms of dry weight, carbon, nitrogen and ash content of eggs, embryos at different developmental stages, juvenile, subadults, and adult individuals of M. mixta.
2. Materials and methods
2.1. Collecting and rearing of mysids Specimens of M. mixta were collected in a coastal area of the northern Baltic proper (588 499 N, 178 359 E, bottom depth of 25–35 m), in August 1995 and August 1996, with a large plankton net (1 m 2 opening, mesh size 0.5 mm). Immediately after collection, specimens covering the entire representative size range were length measured and prepared for ash content, carbon and nitrogen analysis. Simultaneously, materials were collected for the development of regression models between various body variables, such as total body length, carapace length, uropod length, wet and dry weight. The rest of the animals were transported to the laboratory where the animals collected in 1995 and 1996 were maintained for 8 and 5 months, respectively, as part of a study on mysid growth, moulting and stable isotope fractionation. These animals were kept in darkness in natural brackish water (6–7‰) at 9–108C, i.e. conditions similar to those in their natural environment. The mysids were fed with a surplus of a freshly hatched brine shrimp (Artemia spp., San Francisco Bay Brand), which were also regularly sampled for analyses of C and N content. Details on rearing, feeding regime, consumption rates, and food composition are published elsewhere (Gorokhova, 1998, 1999). Initial values of the animals used in the experiments were assumed to be those of mysids from the same size group (60.5 mm) sampled at the start of the experiments.
2.2. Experiment I During the period from August 1995 until April 1996, groups of 30–50 mysids (initial length 7–12 mm) were kept in 50-l aerated aquaria. The conditions provided permitted for growth, gonad development and reproduction. After 5–9 months, in December– April, adult individuals (16.960.9 mm) from the laboratory culture were sampled for analyses, separating males, non-gravid, gravid, and postspawned females. Mysid length, dry weight, fecundity, size and stage of development for embryos present in the brood pouch were recorded. Embryos were dissected out and transferred into pre-weighed tin capsules. While moulting in ovigerous females is arrested, growth might still occur through stretching of the abdominal joints as has been found for some other malacostracan crustaceans including mysids (Mauchline, 1973a). Consequently, this intersegmental growth leads to changes in body morphometry and particularly in carapace to total body length ratio, due to expansion of segmented abdomen and little changes in rigid carapace. To estimate the intermoult growth in gravid M. mixta, the regression lines between body length and carapace length was calculated using females with embryos at earliest and latest developmental stages.
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2.3. Experiment II In August to December 1997, specimens of M. mixta (initial length 8–11 mm) were kept individually in 1-l plastic beakers. The food was changed daily and the water was renewed weekly. Every week, three to five individuals were sacrificed, sized, staged in one of the categories described below, and prepared for the analysis. The experiment lasted for 18 weeks.
2.4. Developmental stages of mysids and embryos Seven life cycle stages were considered according to Mauchline (1980) and Mees et al. (1994). (1) Juveniles: no secondary sexual characteristics. (2) Immature males: 4th pleopods are elongated but do not reach the posterior edge of the last abdominal segment; the lobus masculinus is not fully developed and lacks setation. (3) Immature females: oostegites are visible only from the ventral side. (4) Adult males: 4th pleopods reach the posterior edge of the last abdominal segment; the lobus masculinus is setose. (5) Adult females: marsupia are visible from the lateral side but empty. (6) Gravid females: marsupia are filled with eggs / embryos. (7) Postspawned females: embryos have been released from marsupia. Embryo stages were classified using descriptions of Mauchline (1980), Cuzin-Roudy and Tchernigovtzeff (1985), and Wittmann (1981a). (1) Embryonic egg: embryos in the initial state of marsupial development (stages of early embryo and ovoid eggs, still within the egg membrane). (2) Eyeless larvae: newly hatched and developing nauplioid larvae with eye pigmentation and large yolk mass. Wittmann referred to this stage as ‘naupliar’, and Cuzin-Roudy and Tchernigovtzeff as ‘naulioid phase’. (3) Eyed larvae: moulted nauplioid larvae with the eyes on stalks and almost absorbed yolk. In the terminology of Wittmann and Cuzin-Roudy and Tchernigovtzeff this was ‘postnaupliar’ and ‘postnauplioid’ stages, respectively.
2.5. Length measurements Measurements of the total mysid body length (BL, mm) were taken from the tip of the rostrum to the posterior edge of the last abdominal segment, using calipers (60.02 mm) under a stereomicroscope. Length measurements of the carapace, uropods, and embryos were made using a binocular microscope fitted with an ocular micrometer. Carapace length (CL, mm) was measured as the distance from the tip of the rostrum to the mediodorsal margin of the carapace. Uropod length (UL, mm) was from the posterior margin of the last abdominal segment to the posterior edge of the outer uropod, excluding the setae. Larval size was measured in seawater as the largest diameter for the egg stage and the length from the terminal to the frontal tip of the body for the eyeless and eyed stages.
2.6. Drying and weighting The samples of mysids, eggs / embryos, and Artemia were dried in 608C to constant
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weight (6–8 days for mysids and 3 days for eggs / embryos and Artemia). The dry weights (DW, mg) were determined using a Sartorius M3P microbalance to the nearest microgram. When preparing mysid abdominal tissue, abdomens were carefully separated while dried and transferred to the pre-weighed tin capsules. Whole abdomen or its aliquot, depending on size, 15–20 eggs / embryos, or 30–50 Artemia nauplii comprised each sample. All the samples were kept frozen (2208C) until analysis.
2.7. CN elemental analyses Elemental carbon and nitrogen content were measured by combusting the tin capsules in a CHN-analyzer (CHN-900, 600-800-300, Leco Corporation). For calibration, EDTA of analytical quality (Sigma-Aldrich) was used. The standard deviation among replicate standard samples was within 0.2% for both carbon and nitrogen.
2.8. Ash content After dry weight determinations, five to ten replicate samples from the same set that had been analyzed for elemental composition, were incinerated at 5008C for 4 h in a muffle furnace (Hirota and Szyper, 1975). The remaining ash, containing only inorganic substances, were cooled in dessicator and weighed in the same way as DW.
2.9. Energy densities Caloric values of mysid body, muscle tissue and eggs / embryos were calculated from formula given in Salonen et al. (1976), using values of mysid DW, carbon, and ash content. The proportion of inorganic carbon was assumed to be the same as in Mysis relicta (0.044% of DW, Salonen et al., 1976) and to be independent on mysid size. For calculations of the total energy of ovigerous females, we used the observed fecundity, eggs / embryos energy content and energy content of the female muscle tissue.
2.10. Data analysis When comparing two groups, unpaired t-test was applied followed by F-test to compare variances. Comparisons of three and more groups were performed with a one-way ANOVA with Bartlett’s test for equal variances followed by Bonferroni’s multiple comparison test. The length–weight (both exponential and log-transformed), length–length and fecundity–length relationships were determined by regression analyses. Significant differences between regression lines within a given category (by life stage and sex) were analyzed by testing slopes for equality by analysis of variance (ANOVA) and then by testing elevations of lines with homogeneous slopes for equality by analysis of covariance (ANCOVA). Unless specified otherwise, data are given as means and standard deviations. Ash and element proportions are given in percentage of the DW.
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3. Results
3.1. Growth, development and body size Juveniles brought into the laboratory in August developed secondary sexual characteristics during September–November, underwent gonadogenesis (experiment I and II), and mated (experiment I). In the later, by the middle of December, about 30% of females were ovigerous. Simultaneously, mortality of males increased and, no males were present in the culture by the mid-February. At this point, all females were fertilized and bearing embryos. The first offspring hatched in the middle of March and by the end of April, all the females were postspawned. There were no significant difference between the sampling occasions and between the experiments with regard to the mysid size in different life stages (juveniles, immature and mature males and immature and mature females) (ANOVA, p . 0.05 in all cases). Pooled data on size variability within each category from the field and laboratory observations are presented in Table 1. Embryos (all stages) ranged in size from 0.35 to 3.00 mm, with an overlap between neighboring stages (Table 1). As free-living mysids, larvae were released at a mean size of 2.960.08 mm, corresponding well to the smallest M. mixta observed in the field samples (3.0 mm) in both 1995 and 1997. The embryo undergoes a substantial dry weight reduction (32%) during the marsupial development (Table 1). In some female specimens, oostegites can be seen already at a size of 8.5–8.7 mm, but in most mysids, sex is not distinguishable until they have reached 10–12 mm. Fully mature individuals also varied in size from about 14 to 16 mm and 13 to 17 mm in males and females, respectively. The size dimorphism in M. mixta does not appear until the brooding: there were no significant differences in length ( p . 0.6) or DW ( p . 0.3) between males and non-gravid females. No significant body length difference was found between mature and gravid females ( p . 0.05), while the DW of ovigerous and larvigerous females was significantly higher due to the presence of eggs or embryos Table 1 M. mixta: mean size6S.D. in body length (BL) and dry weight (DW), and size ranges of different life-cycle categories (n denotes the number of observations) Life stage
Eggs Eyeless embryos Eyed embryos Juveniles Immature males Immature females Mature males Mature females Gravid females Postspawned females
Mean6S.D., range
n
BL (mm)
DW (mg)
0.5460.13, 0.35–0.71 1.5860.21, 1.26–2.19 2.6660.28, 2.07–3.00 6.161.83, 2.9–9.7 10.862.14, 9.0–15.2 11.661.25, 8.7–14.7 15.060.94, 13.8–16.3 15.261.66, 12.8–16.9 15.361.26, 13.4–17.2 16.661.22, 14.9–17.4
0.03560.002, 0.031–0.037 0.03160.003, 0.029–0.034 0.02460.003, 0.020–0.028 0.5260.38, 0.05–2.81 2.4361.62, 1.63–7.12 3.2061.14, 1.50–6.96 6.2460.84, 5.38–8.62 6.5261.05, 4.83–9.59 11.1561.08, 8.53–12.47 9.6561.87, 6.73–11.72
11 16 12 58 37 46 22 27 39 16
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( p , 0.001). The length of postspawned females did not differ significantly from that of females bearing embryos ( p . 0.05) while their weight was lower ( p , 0.0003), reflecting loss of marsupial content during hatching. The allometric relationships between DW and body length (BL) are shown in Table 2. No significant differences ( p . 0.5) were found between log–log linear regressions of DW against BL for juveniles and subadults, neither between those for males and non-ovigerous females nor for wild and laboratory reared subadults. Consequently, all these categories were pooled for a common regression line as a power function (Table 2). The regression of DW to BL for gravid females was poor (r 2 5 0.51) and differed from that for the other life-cycle categories as indicated by significantly different slopes ( p , 0.05). Regression lines for the carapace length to body length were similar (both slopes and intercepts are not significantly different, p . 0.3 for slopes and p . 0.05 for intercepts) between females having egg-like embryos and younger stages (juveniles, immature and mature males and females; Table 2). The line for females carrying eyed embryos, however, had significantly different intercept ( p , 0.02) indicating elongated abdomen, i.e. increase in linear dimension during brooding period. Overall, females with eggs were significantly smaller than those with eyed larvae (length 15.6761.08 vs. 16.1260.97 mm, p , 0.01) yielding the intermoult growth of 2.9% in body length.
3.2. Reproductive life history traits The brood size in experiment I ranged from 14 to 35 (27.265.3) eggs or embryos per female. The number of eggs and embryos per individual female (F), tended to increase with female size, though the relationship with either BL or CL was poor (Table 2). However if only the eyed embryos were considered, the regression improved slightly (Table 2). Furthermore, the average number of eggs per brood compared to that of Table 2 M. mixta: morphometric relationships describing dry weight (DW, mg), carapace length (CL, mm), uropod length (UL, mm) and fecundity (F, number of young per brood) as functions of mysid body length (BL, mm) for different life-cycle categories a Life-cycle stages (age and sex) Juveniles, immature and mature males and females Gravid females Juveniles, immature and mature males and females Gravid females with eggs Gravid females with eyed embryos All stages Gravid females Gravid females with eyeless and eyed embryos a
Type of regression DW 5 a*BL
b
a
b
r2
n
0.0032
2.850
0.98
190
DW 5 a*BL b CL 5 a*BL 1 b
0.7140 0.42
1.582 0.12
0.51 0.98
39 64
CL 5 a*BL 1 b CL 5 a*BL 1 b UL 5 a*BL 2 b F 5 a*BL 1 b F 5 a*BL 1 b
0.40 0.42 0.28 3.76 4.46
0.94 0.82 0.98 0.34 0.44
11 12 67 39 28
0.43 20.05 20.39 231.98 243.73
n denotes number of observations and r 2 is the corresponding regression coefficient. Value for all linear regressions p,0.0001. Size ranges are presented in Table 1.
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Fig. 1. M. mixta. Number of embryos in all developmental stages, fertilized eggs, and eyed embryos per brood. The box extends from the 25th percentile to the 75th percentile, with a horizontal line at the median. Whiskers show the range of the data.
embryos was significantly higher (29.265.1 vs. 24.364.5; p , 0.04; Fig. 1) indicating either embryo loss from marsupia or prenatal mortality during marsupial development. Larger females carried larger eggs, with a linear relationship between egg DW and female DW: Eggs DW 5 0.0012 ? Female DW 1 0.022 (r 2 5 0.61, p , 0.005).
3.3. Carbon and nitrogen content The elemental composition did not differ between years and within the different life stage categories (juveniles, immature males and females; p . 0.05 in all cases). Pooled data on the carbon and nitrogen content within each category from field and laboratory (experiments I and II) observations are presented in Fig. 2. There was a considerable variation in carbon content in somatic tissues both within and between different life-cycle stages of M. mixta (Fig. 2a). The proportion of carbon in abdominal muscle decreased gradually from juveniles (42.961.12%) to mature males and gravid females (40.061.61%). The carbon content in muscle tissue did not differ between sexes until after the peak of the mating period (Table 3, Fig. 2a). In specimens sampled from the end of December to the mid-January (males: 38.5560.76, n 5 11 and gravid females: 39.2760.88, n 5 15), a significantly lower percentage of carbon was found in the males ( p , 0.04). The nitrogen content was relatively constant (11.4% in average) with significant differences only between juveniles and mature females (11.3 vs. 11.6% respectively; Table 4). The C:N ratio reflected the change in somatic carbon content, and the ratio decreased 6.2% from juveniles and subadult to mature males and gravid females (Fig. 2c). Thus, at the conditions provided, the specific content of carbon (C, %) changed with size of mysids (C 5 2 0.32 ? Body DW 1 43.30; r 2 5 0.31, p , 0.0001), while size specific nitrogen (N, %) content showed lower variability (N 5 0.019 ? Body
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Fig. 2. M. mixta. Pooled data on carbon (A) and nitrogen (B) content, and C:N (C) ratio for different age and sex categories (field samples, experiments 1 and 2). J, juveniles; IM, immature males; IF, immature females; MM, mature males; MF, mature females; GF, gravid females; PF, postspawned females. The box and whiskers parameters are the same as in Fig. 1.
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Table 3 M. mixta: Results of ANOVA and Bonferroni’s test for multiple comparisons on carbon content in abdominal muscle tissue a ANOVA results p value F R2
,0.0001 8.131 0.3040
Bartlett’s test for equal variances Bartlett’s statistics (corrected) p value
10.91 .0.09
ANOVA table
SS
df
MS
Treatment (between groups) Residual (within groups) Total
56.86 178.3 235.2
6 153 159
9.476 1.166
Bonferroni’s multiply comparison test
Mean difference
t
p value
J vs. IM J vs. IF IM vs. IF IM vs. MM IF vs. MF MM vs. MF MF vs. GF PF vs. GF
1.389 1.227 20.1620 1.464 1.309 20.3164 0.651 0.9227
3.492 2.776 0.4022 4.786 3.590 1.248 2.507 2.153
,0.01 ,0.05 .0.05 ,0.001 ,0.01 .0.05 .0.05 .0.05
a
J, juveniles; IM, immature males; IF, immature females; MM, mature males; MF, mature females; GF, gravid females; PF, postspawned females.
DW 1 11.34; r 2 5 0.03, p , 0.03), resulting in a significant change in C:N ratio (C:N 5 2 0.033 ? Body DW 1 3.81; r 2 5 0.23, p , 0.0001). In embryos, carbon and nitrogen content were highest in early stages (58.6 and 14.3%, respectively), and decreased to 51.4% for carbon ( p , 0.0001, Fig. 3a) and to 12.6% for nitrogen ( p , 0.04, Fig. 3b) to the end of the marsupial development. In eggs, there was no correlation between DW versus carbon and nitrogen content (Pearson r 5 2 0.13, p . 0.7, R 2 5 0.02 and Pearson r 5 0.09, p . 0.8, R 2 5 0.01 for C and N, respectively). Variations in the C:N ratios in embryos were weak (Fig. 3c).
3.4. Ash content In mysids, the ash content was slightly, but not significantly ( p . 0.4), higher in juveniles than in older groups (Fig. 4), probably reflecting changes in the body surface to volume ratio. The overall mean value of 8.9% was used in calculations of ash-freedry-weight (AFDW, mg) for all age and sex categories of mysids. In developing embryo, ash content increased almost twice (Fig. 4) from fertilized egg (3.4%) to moulted larvae (6.4%).
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Table 4 M. mixta: Results of ANOVA and Bonferroni’s test for multiple comparisons on nitrogen content in abdominal muscle tissue a ANOVA results p value F R2
,0.02 2.757 0.0975
Bartlett’s test for equal variances Bartlett’s statistics (corrected) p value
12.12 .0.06
ANOVA table
SS
df
MS
Treatment (between groups) Residual (within groups) Total
3.106 18.05 20.22
6 153 159
0.5177 0.1345
Bonferroni’s multiply comparison test
Mean difference
t
p value
J vs. IM J vs. IF J vs. MF IM vs. IF IM vs. MM IF vs. MF MM vs. MF MF vs. GF PF vs. GF
0.0526 20.0868 0.2123 20.1394 20.1696 20.1772 20.1467 0.1632 0.0014
0.5603 0.8278 1.789 1.465 2.351 2.056 2.450 2.658 0.01292
.0.05 .0.05 ,0.05 .0.05 .0.05 .0.05 .0.05 .0.05 .0.05
a J, juveniles; IM, immature males; IF, immature females; MM, mature males; MF, mature females; GF, gravid females; PF, postspawned females.
3.5. Energy content The weight-specific energy content of the mysid muscle tissue fell from 20.0 KJ g 21 DW (20.9 KJ g 21 AFDW) in the young mysids in August (field samples) to 17.6 KJ g 21 DW (18.9 KJ g 21 AFDW) in mature animals in the winter (laboratory-reared mysids). The lowest caloric value (17.9 KJ g 21 AFDW) was obtained for males in the end of mating period. The total energy content of ovigerous females (somatic tissues and fertilized eggs) was 18.7 KJ g 21 DW (or 207.7 J ind 21 ) in the beginning of the marsupial development (December–January). By this time energy contained in ripe eggs composed about 10–17% of the total female energy content (Fig. 5a). The relationship between female body size and the energy they devote to reproduction (Fig. 5b), based on regressions describing fecundity and egg size as functions of female DW and egg elemental composition, could be established. Larger females invest more to their offspring both in terms of the absolute values and relative to their DW. The energy density of embryos varied from 29.7 KJ g 21 AFDW in earliest embryos to 25.9 KJ g 21 AFDW in eyed larvae. About 40% of individual embryo energy content were lost during marsupial development. Considering both intermediary metabolic losses
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Fig. 3. M. mixta. Carbon (A) and nitrogen (B) content, and C:N ratio (C) for different developmental stages of embryo (experiments 1). The box and whiskers parameters are the same as in Fig. 1.
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Fig. 4. M. mixta. Ash content for all ontogenetic stages (field samples, experiments 1 and 2). E, egg; ELE, eyeless embryo; EE, eyed embryo; J, juveniles; IM, immature males; IF, immature females; MM, mature males; MF, mature females; GF, gravid females; PF, postspawned females. The box and whiskers parameters are the same as in Fig. 1. Numbers above plots show the number of analyses.
of embryos and their prenatal mortality, the energy content of brood decreased by 50% during the complete embryogenesis.
4. Discussion Only a few mysid species have been laboratory reared for studies of development and growth: Leptomysis lingvura (Wittmann, 1981a,b), Neomysis intermedia (Toda et al., 1987), Siriella armata (Cuzin-Roudy and Saleuddin, 1989), Rhopalophthalmus terranatalis (Wooldridge, 1986), and Holmesmysis costata (Turpen et al., 1994). The results from such studies under controlled conditions are usually of lower variability than results from studies on natural populations, where inter-population differences might occur due to genetic or environmental variations. However, the investigators have not focused on the changes in chemical composition associated with development and reproduction. According to previous observations, behaviour, size distribution, and chemical composition of Mysis species including M. mixta, are influenced by various factors, for example, by season and life cycle stage (Hakala, 1979; Gardner et al., 1985; Adare and Lasenby, 1994). The results presented here show that age and sexual maturity has marked effects on the chemical composition of the somatic tissues of M. mixta even if environmental conditions and food supply remain invariable. It is possible, however, that stable and relatively high temperature and absence of the seasonal day / night variations in the light regime during our experiments may have influenced chemical composition of the reared mysids. Mysids are highly temperaturesensitive, with temperature having a great influence on growth and maturation
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Fig. 5. M. mixta. Panel A shows calculated total energy content (E) of gravid female (E tot, s, J ind 21 ) and energy accumulated in the eggs in relation to female DW (E egg, %, j, J mg 21 ). Panel B: empirical models for energy invested in reproduction as an absolute value (thin line, J ind 21 ) and relative to female size (thick line, J mg 21 ). These are based on fecundity and egg DW as functions of female DW (Table 2).
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(Wittmann, 1981b). Indeed, if accumulation of lipids for overwintering require an environmental stimulus (e.g. decrease of temperature and / or light period), then this process might be inhibited in the laboratory. Another possible source of bias in our observations is an inadequacy of the Artemia as a sole food item for M. mixta. Artemia nauplii have commonly been used as a diet for marine crustaceans including mysids (for review, see Leger et al., 1986). However, many studies indicate that the dietary quality of Artemia varies with its geographical origin (Beck and Bengtson, 1982; Leger and Sorgeloos, 1984). The nutritional value of Artemia nauplii is most often correlated with the lipid quality, particularly variations in the composition of highly unsaturated fatty acids (Leger et al., 1986; Kreeger et al., 1991). When testing culture and dietary conditions for mysid crustaceans, survival, growth, and reproduction output are usually used as indicators (Johns et al., 1981; Leger et al., 1986; Kreeger et al., 1991). In our study, the low mortality, successful breeding, and the size attained by adults indicate that the laboratory treatment provided conditions that fulfill the requirements of M. mixta for growth and reproduction. Moreover, growth rates and fecundity in laboratory cultured mysids match previous estimates from field populations (Shvetsova, 1980; Rudstam, 1989; Simm and Kotta, 1992; Gorokhova and Hansson, 2000). Consequently, the results of this study may be of general relevance until comparable field data become available.
4.1. Growth, development and body size Despite differences in laboratory and natural conditions, timing of sexual maturation, mating and brood duration were virtually synchronous with phenological events observed in the wild (Salemaa et al., 1986; Simm and Kotta, 1992). At the same time, the selection of specimens within a narrow size range for experiments, together with identical growth conditions, resulted in lower size variability of the reared individuals (Table 1) compared to that of M. mixta in the wild (12–22 mm in October, mostly matured individuals, Wiktor and Szaniawska, 1988). In general, the ranges of length and weight found in laboratory reared M. mixta agree with field observations from the Baltic (Shvetsova, 1980; Rudstam et al., 1986; Wiktor and Szaniawska, 1988) and that of Grabe and Hatch (1982) in New Hampshire coastal waters. However, the length–weight regressions between these studies varied considerably (Fig. 6), most probably due to the difficulties related to positioning of a mysid when measuring length. Until the brooding period begins, mysids show uniform sizes and biometrical relationships regardless of sex, while females with a brood pouch require different equations for interconversions. Inter-moult ( 5 intersegmental) growth of | 3% in length was observed in gravid females, during the brooding period. Mauchline (1973a) and Fenton (1994) examined inter-moult growth in several mysid species and found it to range between 3–10% (7% in average) and between 2–14% (6% in average), respectively. The question as to what extent field population follows this growth pattern under general food depletion during most part of the cold period needs to be carefully analyzed together with studies on food consumption and assimilation.
4.2. Reproductive life history traits In most mysid species, brood size has been shown to increase with female body size
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Fig. 6. M. mixta. Total length to body dry weight relationships obtained in different studies. To compare the varying length–weight and length–length relationships to those obtained by Shvetsova (1987), Shvetsova et al. (1992), Simm and Kotta (1992), Rudstam et al. (1986), and Wiktor and Szaniawska (1988), differences in the lengths measured must be taken into account. The total body length in these studies corresponds to the sum of body length (BL) and either uropod (UL) or telson length (TL) measured in our study (Table 2).
(Mauchline, 1980; Wittmann, 1984). Due to the low variability in the female size in our study, the relationships between brood size and female length and between egg DW and female DW were weak. Considerable variations in the brood size of M. mixta have been reported: 9–97 eggs by Mauchline (1980), 21–255 by Grabe and Hatch (1982), 8–87 by Shvetsova et al. (1992), 8–42 by Shvetsova (1980), and 13–53 by Simm and Kotta (1992). The average fecundity obtained in the laboratory (27.2) was surprisingly close to the values reported from the Gulf of Riga for females of the corresponding length (28.4 embryos, Simm and Kotta, 1992; 19.6 embryos, Shvetsova, 1980). During the embryogenesis, which occurs in the marsupium, M. mixta passes through the main larval stages (as described by Mauchline, 1980; Wittmann, 1981a; CuzinRoudy and Tchernigovtzeff, 1985, etc.) characteristic of other mysid species. The decrease in number of embryos that was observed as the brood aged indicates either embryo loss from marsupia or prenatal mortality during the brood pouch development. Mortality of young has been shown to occur during marsupial development in several mysid species (up to 20% according to Mauchline, 1973b, 1980; 26%, Morgan, 1980; 6–44%, Fenton, 1994). Mortality in the brood pouch of M. mixta was relatively high
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(17% in numbers) but no comparative field data are available to conclude if this value is different in natural population. However, the differences between fecundity estimates using egg numbers and that based on embryo numbers are important for assessment of the recruitment stock and parental investment in the offspring.
4.3. Energy costs of embryogenesis and reproduction The utilization of the yolk material by the developing embryo results in a decrease in egg dry weight. Unfortunately, no data on variations in M. mixta egg and embryo DW and elemental or biochemical composition are available, but compared with data from other marine crustaceans of similar size, our data correspond well with values given by Khmeleva and Romanova (1978). The latter authors compare water content, dry mass, ash, and caloric content in fertilized eggs and embryos of marine Idoteidae (seven species), Gammaridae (one species) and Decapoda (six species) from different localities. In their study, the decrease in DW during embryo development varied from 24.0% in amphipods to 41.2% in isopods. At the same time, ash content increased two to four times from 3.0–5.4 to 8.2–19.5%. Consequently, the caloric value was reduced 14.2 to 16.7%. The overall loss of embryo energy content was estimated to be 35.9% in decapods, 44.6% in amphipods, and 49.1% in isopods. Similar changes were observed in developing embryos of M. mixta: loss of 31.4% of the initial DW and 13% in caloric value, together with an increase from 3.4 to 6.4% in ash content. This resulted in a 40% energy loss for intermediary metabolic needs and metamorphoses during the marsupial development. Female M. mixta invests a significant amount of energy in the offspring. The proportional amount of energy devoted to reproduction increase with female size in different manners (Fig. 5b). Using the same regression of carbon against energy as we used, Hakala (1979) estimated that the carbon loss of M. relicta females for egg production was 8%. Apparently, our estimates of egg production costs in M. mixta ( | 14%) were higher. The lower caloric values in males after mating than in gravid females indicate that male energy losses for spermatogenesis and copulation is even higher.
4.4. Elemental composition and energy content The ranges and means of the elemental composition of M. mixta muscle tissues (C: 37–44% and N: 10–13%) are somewhat different from those reported for freshwater mysids. These differences were rather expected, due to analyzing abdominal muscle instead of the whole body (somatic plus generative tissues), the latter being more common. Salonen et al. (1976) and Hakala (1979) studied Mysis relicta from Lake ¨¨ ¨ Paajarvi (southern Finland), and found higher values for C (44.8–58.3%) and lower for N (9.1%). However, carbon values for embryos of the same species are remarkably close to our estimates (52.2–57.9% reported by Hakala vs. 51.4–58.6% found in this study). The carbon concentration of the estuarine mysid Neomysis intermedia in Lake Kasumigaura (Japan, Toda et al., 1987, 45.260.012%) also exceeded that we found for M. mixta.
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Wiktor and Szaniawska (1988) reported the weight-specific energy content of M. mixta (size 4–30 mm) from the southern Baltic to be 24.8 KJ g 21 DW on average, which is higher than our estimates. However, for the size group 6–13 mm, which is similar to animals used in our experiments, their and our values are similar (20.6 and 20.0 KJ g 21 DW). In contrast to Wiktor and Szaniawska (1988), the caloric value of M. mixta reported by Rumohr et al. (1987), 15.1 KJ g 21 DW, was much lower than our estimates. The weight specific energy content of other mysid species varies. Observations on another North-Atlantic species, Mysis stenolepsis (Tyler, 1973) and on freshwater Neomysis mercedis from Lake Washington (Chigbu and Sibley, 1996) were consistent with our findings for M. mixta. Values ranging from 13.5 to 20.8 KJ g 21 DW have been found for Neomysis integer in different parts of the Baltic (Healey, 1972; Szaniawska et al., 1986; Rumohr et al., 1987). To a considerable extent, the variation in the carbon-to-dry weight ratio mirrors variation in lipid content, as lipids are richer in C (70–80%) than carbohydrates (40–44%) and proteins (50–54%, Winberg, 1971). A seasonal cycle in the carbon content of M. relicta was described by Hakala (1979), who found values between 45 and 58% in a population with a 2-year life cycle. In immature animals, carbon accumulated in the autumn, while adults lost carbon during August to December. Hakala (1979) also described ontogenetic variation in the energy content of M. relicta with the highest values for young embryos (27.85 KJ g 21 DW) and lowest in the young mysids (20.77 KJ g 21 DW). Seasonal changes in the percent total lipid content of M. relicta with 1and 2-year life cycles (southern Ontario, Adare and Lasenby, 1994) followed the same pattern. In that study, juvenile mysids had approximately 10% less lipid than adults, a difference similar to that recorded between adult female and juveniles of the depositfeeding amphipods Pontoporeia hoyi (Quigley et al., 1989) and Monoporeia affinis and P. femorata (Hill et al., 1992). In adult M. relicta, the percent lipid reached a peak between July and the end of August, and then gradually declined until November– December (Gardner et al., 1985; Adare and Lasenby, 1994). The authors concluded that this decline reflected seasonal changes in the quality and quantity of food or resulted from physiological changes coupled to reproduction and development. The reduction of ˚ lipids in Meganyctiphanes norvegica (Bamstedt, 1976; Falk-Petersen, 1981), copepods (Arashkevich and Drits, 1997), as well as the decrease in carbon described for cladocerans (Manca et al., 1994) have also been linked to sexual maturation. Our carbon data, with higher values in August than in winter and a decline with size (and with developing of ovarian / testis tissues), indicate a similar change in lipid content in Baltic M. mixta with a 1-year life cycle as in the second year of life in M. relicta. In our experiment, however, the mysids had a surplus of food and the decline can not be ˚ explained by winter starvation as with Meganyctiphanes norvegica (Bamstedt, 1976). Probably, a rapid growth period coupled with maturation, in contrast to mysids with 2-year life cycle, leads to an increased proportion of structural (i.e. protein) tissues that have low carbon content. It could be speculated that this growth strategy in males results in small energy reserves that are sufficient only for mating, which might explain the disappearance of males soon after the breeding (Hakala, 1979; Rudstam et al., 1986; this study). Thus, a genetically fixed developmental program for M. mixta can be described as strongly dependent on reserves accumulated during the juvenile period. Whether
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females that survive a second year reproduce twice is unknown; it would be to a female’s advantage to devote a high proportion of her energy reserves to somatic growth during first year and to oogenesis during second year of life. Further studies using both elemental composition and in situ growth analysis would lead to a more comprehensive understanding of the mysid energetics.
Acknowledgements This study was financially supported by the Helge Ax:son Johnson and the Wallenberg Foundations, the Swedish Natural Science Research Council and the European Union through MAST / BASYS. We also thank the Stockholm Centre for Marine Research for ´ is providing facilities and technical support at the Asko¨ Laboratory. Ulrika Hamren thanked for field and laboratory assistance. [SS]
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