Organic and energetic content of eggs and juveniles of antarctic echinoids and asterids with lecithotrophic development

Camp. Biochem. Physiol. Vol. 85A, No. 2, pp. 341-345. 1986 Printed

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ORGANIC AND ENERGETIC CONTENT OF EGGS AND JUVENILES OF ANTARCTIC ECHINOIDS AND ASTEROIDS WITH LECITHOTROPHIC DEVELOPMENT JAMES B. MCCLINTOCK and JOHN S. PEARSE Institute of Marine Sciences, University of California, Santa Cruz, CA 95064, USA (Receirled 4 February 1986)

Egg diameters (mm) of the spatangoid echinoids Abatus shackletoni, Abatus nimrodi and the asteroids Notasterias armata, Diplasterias brucei, and Perknasler Jiiscus antarcticus were 1.28, 1.97, 3.54,2.80 and 1.20, respectively. A. shackletoni, A. nimrodi, N. armata and D. brucei, brood their embryos to a juvenile stage; P. fuscus anrarcficus apparently is a broadcast spawner with pelagic lecithotrophic larvae. 2. Eggs were composed primarily of protein (33-53%) and lipid (36-59%). Juveniles had higher levels of insoluble protein and ash due to the formation of structural and skeletal material. 3. There was little decrease in the amount of energy from egg to juvenile during development This supports the hypothesis that large egg size in marine invertebrates with lecithotrophic development is more important in producing a large juvenile than in the provision of a large amount of energy for development 4. Comparisons of reproductive output and reproduotive effort in echinoderms with lecithotrophic development reveal a high degree of interspecific variability. 5. This variability is related to the differential allocation of energy to somatic and gametic tissues based on differences in functional morphologies. 6. Variable reproductive efforts in species with lecithotrophic development confound comparisons with species with planktotrophic development and make tests of energetic hypotheses for alternate life-history strategies in marine invertebrates difficult. Abstract-l.

INTRODWTION The energetics of egg production are central to several hypotheses concerning the adaptiveness of alternative life-history strategies in marine invertebrates (Chia, 1974; Menge, 1975; Strathmann and Strathmann, 1982; Strathmann, 1985). One such hypothesis proposes that because there is a high larval mortality in the plankton, planktotrophic modes of development demand a higher proportion of energy directed to the production of numerous small eggs than lecithotrophic modes where the planktonic phase is abbreviated or bypassed. Thus, species with higher sources of energy have the resources to produce planktotrophic larvae while those with smaller sources of energy have lecithotrophic development. This hypothesis fits particularly well with Thorson’s (1950) hypothesis that there is a high proportion of lecithotrophic species in high latitudes due to poor food conditions over most of the year (Jablonski and Lutz, 1983). Nevertheless, there are few data available with which to test these hypotheses. Large egg size in marine invertebrates with lecithotrophic development is classically assumed to be related to the provision of energy for development (Mortensen, 1921). On the other hand, Lawrence et al. (1984) found little difference in energy content of early embryos and fully developed juveniles of several brooding species of subantarctic echinoderms; they suggested that large egg size is related mainly to the production of large juveniles. In the present paper information is provided on the size, biochemical composition and energy content

of the eggs of five species of echinoderms with lecithotrophic development from McMurdo Sound, Antarctica. High interspecific variability was found among these and comparable lecithotrophic species in fecundity, reproductive output and reproductive effort. In addition, the energy content of early juveniles of three of the species was nearly the same as that of the early embryos. Nevertheless, lipid content decreased and insoluble protein content increased, suggesting that lipids are used for synthesis of proteins during development. MATERIALS The

AND METHODS

animals were collected using scuba from 2&30 m of water in McMurdo Sound, Antarctica (77”51’S, 166”39’E) during November and December, 1984. The spatangoid echinoids Abatus shackletoni and A. nimrodi brood their embryos in aboral marsupiums and release juveniles (Pawson, 1969). All the embryos were removed from one individual of each species and divided into two categories: early embryos (eggs) without external differentiation and late embryos with spines (juveniles) that were near the time of release. In addition, recently released juveniles were collected from beneath one brooding female of A. nimrodi. The forcipulate asteroids Notasterias armata and Diplasrerias brucei brood their embryos orally and also release juveniles (Pearse et a/., in press). All the embryos in a brood are at the same stage of development. All the early embryos (eggs) were removed from one individual of N. armatu and two individuals of Diplasferias brucei. A third individual of D. brucei held fully-developed juveniles nearly ready to release; these were collected and treated as juveniles. The spinulosan asteroid Perknaster fuscus antarcticus broadcast spawns and has pelagic lecithotrophic development (Pearse and Giese. 1966; Pearse et al., in press). All the eggs

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JAMS B. MCCLINKKKand JOHN S. PEARSE

342

(full-grown oocytes) were separated from the fullydeveloped ovaries of one individual of P. Jiiscus anrarcticus; these were discrete cells and did not include any accessory cells or associated ovarian material. The eggs and juveniles of each individual were counted, measured, weighed, lyophilized and re-weighed. Eggs and juveniles removed from single individuals were pooled for biochemical and energetic analyses. NaOH-soluble protein was measured using the spectrophotometric technique of Lowry ef al. (1951). Carbohydrate was measured using the spectrophotometric technique of Dubois et al. (1953). Lipid was measured using the gravimetric technique of Freeman et al. (1957). Percent ash was determined by placing tissues in a muffle furnace at 500°C for 4 hr. Insoluble protein was measured by subtraction as done by Lawrence and Guille (1982) and Lawrence et al. (1984). The joules (J) per egg or juvenile were calculated indirectly by multiplying the dry wt per egg or juvenile by the level of each organic class and their energetic equivalents (Brody, 1945). The total energy devoted to egg production (reproductive output) was calculated by multiplying the J/egg by the total number of eggs/female. The ratio of the amount of energy invested in total eggs to the total amount of energy invested in the intact individual x 100 (reproductive effort) was calculated by measuring the organic composition of the pyloric ceca, body wall and gonad of the asteroids, and the gut and body wall of the echinoids. Energy contents of these body components were calculated by multiplying the level of each organic class by the dry wt of each body component. The total energy in each body component was summed to yield the total energy in an intact individual.

RESULTS The eggs are and insoluble protein ranged ticus to 52.7%

composed primarily of NaOH-soluble protein and lipid (Table 1). Total from 33.5 in Perknaster fuscus antarcin Notasterias armata. Lipid ranged

from 35.6 in N. armata to 59.1% in Abatus shackletoni. Levels of carbohydrate were low (1 A-4.1%). Lipid and carbohydrate levels in the eggs of P. fuscus antarcticus were similar to those found in the ovaries of this species by Pearse and Giese (1966) (49.3-56.0 and 2.1%, respectively). Levels of ash were also low with the highest level (9.1%) occurring in the eggs of N. armata. Combined levels of NaOH-soluble and insoluble protein did not change appreciably from egg to juvenile. However, there were higher levels of insoluble protein and lower levels of soluble protein in juveniles. Levels of lipid decreased markedly in juveniles while levels of carbohydrate remained constant. Percent ash showed an increase from egg to juvenile, particularly in the irregular spatangoid echinoids. The egg sizes, egg dry wts. juvenile dry wts and energy/egg and juvenile are presented in Table 2. Egg sizes ranged from 1.20 mm dia in Perknaster fuscus antarcticus to 3.54 mm in Notasterias armata. There was a 7-fold range in the amount of energy/egg, with Abatus shackletoni having the least and N. armata the most J/egg. There was no significant decrease in the amount of energy from egg to juvenile for either species of Abatus and only a slight decrease in Diplasterias brucei.

Figure 1 presents the total amount of energy in intact individuals, fecundities, reproductive outputs and reproductive efforts of the five antarctic echinoderms investigated in this study, in addition to available data on other species of echinoderms with lecithotrophic development. Body weights of these species vary substantially from 2 g in the asteroid Echinaster sp. II to 245 g in the asteroid Notasterias armata. The sizes of all these echinoderm species

Table I. Proximate composition of eggs and juveniles of echinoids and asteroids from McMurdo Sound, Antarctica, with lecithotrophic development % dry wt Species

NaOH-soluble protein

Insoluble protein

Lipid

I

24.2 22.1

9.2 21.6

59.1 48.4

4.1 3.5

2 I I

19.1,21.9 20.0 21.8

26.9, 30.3 32.1 11.7

39.0,41.8 35.6 58.8

3.4.4.0 2.6 1.8

5.6,8.4 9.1 5.9

1 2

16.7 14.3, 17.1

30.4 27.1.28.9

23.7 14.3, 17.1

4.1

I .9, 3.3

25. I 30.0, 36.7

I

23.0

32.2

2.7

10.6

N

Carbohydrate

Ash

Eggs Abatus shackletoni Abatus nimrodi Diplasterias brucei Notasterias armata Perknaster fuscus Jureniles Abatus shackletoni Abatus nimrodi Dipiasterias brucei

1

31.5

3.4 3.8

The proximate composition values are averages for eggs and juveniles of individualechinoids and asteroids [the number of individuals (N) is given].

Table 2. Characteristics of eggs and juveniles of echinoids and asteroids from McMurdo Sound, Antarctica, with lecithotrophic development Species Abatus shackletoni Abatus nimrodi Diplasterias brucei

Egg diameters (mm)

Dry wt/egg (mg)

I .28 (58)

Dry wtijuvenile (mg) -

1.97 (17)

OS8 I s2

0.87 2.68, 3.10

2.80 (87) 3.54 (20) I .20 (43)

5.84.6.02 5.59 2.64

3.59

Joules/egg 22 52

Joules/juvenile 31 48,56

142,150 II4 I51 Perknaster fuscus 83 The egg diameters are means (numbers of eggs in parentheses). The dry wts and joules per egg and the dry wts and joules per juvenile are average values for eggs and juveniles of individual echinoids and asteroids. The dry wt/juvenile and joules/juvenile are presented for two individuals of A. nimrodi. The dry wt/egg and joules/egg are presented for two individuals of D. brucei. Norasterias

armata

Reproductive energetics of Antarctic echinoderms

Fig. 1. Total body weight, fecundity, lecithotrophic development. The data asteroid Anasferias pert-i& are taken Echimzsrer spp. I and

reproductive output and reproductive effort of echinoderms with for the subantarctic echinoid Abutus eordum and the subantarctic from Lawrence ef al. (1984). The data for the Caribbean asteroids II are taken from Scheibling and Lawrence (1982).

reflect average sizes of adult individuals (Scheibling and Lawrence, 1982; Magniez, 1983; Bosch, McClintack and Pearse, unpublished data). Fecundities were highest among those echinoderms with broadcasting l~i~otrophic modes (Perknaster ftiscus untarcticus, Echinaster spp. I and II); all the other species brood their embryos and have no larval stage. Reproductive output and reproductive effort values were highly variable, with reproductive effort ranging from 4.2 in the antarctic spatangoid echinoid Abatus nimrodi to 64.7% in the antarctic spinulosan asteroid Perknaster fuscus antarcticus.

DISCUSSION

The eggs and juveniles of these antarctic echinoderms are similar in composition to the eggs and juveniles of brooding subantarctic echinoderms (Lawrence et al., 1984) as well as those of other echinoderms with lecithotrophic development 1976; Turner and (Turner and Rutherford, Dearborn, 1979; Scheibling and Lawrence, 1982) and planktotrophic development (Turner, 1977). There was an increase in levels of insoluble protein and ash from egg to juvenile. The increase in insoluble protein can most likely be attributed to an increase in the amount of structural protein in the juvenile stage. Increases in ash are associated with the development of skeletal ossicles. This is particularly pronounced with the formation of the test and spines of the spatangoid echinoids Abatus shackzetoni and A. nimc.9 P. 85,2.4--J

343

rodi. Both echinoids showed an g-10-fold increase in ash level. Similarily, Lawrence et al. (1984) found a 1Zfold increase in ash from egg to juvenile for the subantarctic congener A. cordatus. Egg sizes ranged 3-fold among these antarctic echinoids and asteroids. The smallest egg size (1.20 mm diameter) was found in the broadcasting lecithotrophic asteroid Perknaster fuscus antarcticus. A similar egg size was reported for P. fuscus antarcticus by Pearse and Giese (1966). Broadcasting lecithotrophic echinoderms are known to generally have smaller eggs than brooding species (Emlet et al., in press; Pearse et al., in press). The eggs of these antarctic echinoderms are at least one order of magnitude larger than those of echinoderms with planktotrophic development (egg sizes reviewed by Emlet et al., in press). The eggs of Notasterias armata are among the largest echinoderm eggs known. There was not a direct relationship between the sizes of eggs and the amount of energy they contained. For example, the eggs of Notasterias armata are 21% greater in diameter than the eggs of Diplasterias brucei, yet their energy contents are not significantly different. This is consistent with the observations of Turner and Lawrence (1979) who proposed that qualitative differences in the biochemical composition and differences in dry wt of echinoderm eggs can be attributed to these indirect relationships. Egg size is positively correlated with body size in the spatangoid echinoids, with Abutus nimrodi having the largest egg and the largest adult body size.

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JAMES

B. MCCLINTOCK and JOHN S.

The lack of significant decreases in the amount of energy between egg and juvenile in Diplasterias brucei, Abatus shackletoni, and A. nimrodi supports the hypothesis that the significance of large egg size in direct developing echinoderms is in the production of a large juvenile and not in the provision of a large amount of energy for development (Lawrence et al., 1984). Emlet et al. (in press) have noted a positive correlation between egg size and size at metamorphosis in echinoderms. They suggest that the advantage in growth and survival of large metamorphosed juveniles may balance the decrease in fecundity typically associated with a lecithotrophic mode. The cost of development also may be offset by the absorption of dissolved organic material. The absorption of dissolved organic material (amino acids) has been noted in adult (Bamford, 1982) and larval (Fenaux, 1982) echinoderms. Among larval echinoderms, Manahan et al. (1983) have found that up to 76% of the energy budget of the pluteus larvae of the echinoid Strongylocentrotus purpuratus can be attributed to the uptake of amino acids. There does not appear to be any consistent relationship between body size and developmental mode among lecithotrophic echinoderms (Fig. I). Body sizes range from 2-245 g. The brooding asteroid Notasterius armata, with the largest body size, is much larger than the broadcasting lecithotrophic species. Perknaster fiuscus antarcticus, Echinaster sp. I, and Echinaster sp. II. Strathmann and Strathmann (1982) have noted that brooding echinoderms tend to have smaller body sizes than broadcasting planktotrophic species. Apparently this relationship may not hold for brooding and broadcasting echinoderms with lecithotrophic development. There is a consistent relationship between developmental mode and fecundity in species with lecithotrophic development. The three broadcasting lecithotrophic species presented in Fig. I have much higher fecundities than brooding species. Higher fecundity in broadcasting lecithotrophic species may be necessary to offset an expected increase in larval mortality due to predation, offshore drift and other environmental factors when compared to protected, brooded embryos. Low egg number in brooding species may be related in part to constraints imposed by the limited volume of the brood chamber (e.g. in the spatangoid echinoids) (Strathmann and Strathmann. 1982) and other volumetric constraints of egg masses (Chaffee and Strathmann, 1984; Strathmann and Chaffee, 1984). The low number of brooded embryos held by the large individual of N. armata is particularly interesting. The reproductive output (energy invested in total eggs) was not strongly correlated with fecundity or body size in these species. Reproductive output was particularly high in the asteroids Diplasterias brucei and Perknaster fuscus antarcticus. Higher reproductive output in these species translates into higher reproductive effort (energy invested in total eggs/ energy in total individual). However, high reproductive output is not a necessary correlate of high reproductive effort. Echinaster sp. II has a relatively high reproductive effort and low reproductive output. High variability in reproductive effort among these echinoderms is related to differences in the relative allocation of energy to gametic and somatic tissues.

PEARSE

For example, Abatus nimrodi has a greater adult body size than A. shackletoni or A. cordatus. However, A. nimrodi does not invest proportionately more energy into egg production and consequently has a lower reproductive effort that either congener. Larger egg size in this species may offset lower reproductive effort through production of a larger, more robust juvenile. In fact the dry wt of juvenile A. nimrodi is greater than for other Abatus species (Table 2: Lawrence et al., 1984). Variability in reproductive efforts of these species is related to differences in functional morphologies, which are ultimately linked to differences in feeding mode and/or body armor (Lawrence et al., 1984). For example, both Notasterias armata and Echinaster sp. II put a similar amount of energy into egg production (Fig. I), yet the heavy body armature of N. armata requires a much higher energy input into somatic tissue with a resultant low reproductive effort. Highly variable reproductive efforts in echinoderms with lecithotrophic development confound direct comparisons with species with planktotrophic development. Tests of energetic hypotheses for the evolution of planktotrophic and lecithotrophic developmental modes in marine invertebrates must take into consideration these differences in body form. Moreover, information on the lifespan of an organism is necessary to estimate the energy invested in eggs over the entire life history. Species with different reproductive modes yet similar functional morphologies and life spans may ultimately provide an appropriate test of energetic hypotheses. Acknowledgemenrs-The authors wish to thank lsidro Bosch, Baldo Marinovic and Ron Britton for diving support, and the staff of the Ecklund Biological Laboratory at McMurdo Station, Antarctica. This study was supported by Polar Program National Science Foundation grant No. DPP-83 17082. REFERENCES Bamford D. (1982) Epithelial transport. In Echinoderm Nutrition (Edited by Jangoux M. and Lawrence J. M.), pp. 3 17-330. Balkema Press, Rotterdam. Brody S. (1945) Bioenergetics and Growth. Hafner Publishing Co.. New York. Chaffee C. and Strathmann R. R. (1984) Constraints on egg masses. I. Retarded development within thick egg masses. J. exp. mar. Biol. Ecol. 84, 73.~83. Chia F. S. (1974) Classification and adaptive significance of developmental patterns in marine invertebrates. Thal. Jugosiac. 10, 121-130. Dubois M.. Gilles K. A., Hamilton J. K., Rebers P. A. and Smith R. (1953) Calorimetric method for determination of sugars and related substances. Analyf. Chem. 28, 350-356. Emlet R. B., McEdward L. R. and Strathmann R. R. (in press) Echinoderm larval ecology viewed from the egg. In Echinoderm Bioloav Series (Edited bv Jangoux M. and Lawrence J. M.).%alkema Press, Roiterda& Fenaux L. (1982) Nutrition of larvae. In Echinoderm Nutrition (Edited by Jangoux M. and Lawrence J. M.). pp. 479498. Balkema Press, Rotterdam. Freeman N. K.. Lindgren F. T.. Ng N. Y. and Nichols A. V. (1957) Infrared spectra of some lipoproteins and related lipids. J. hiol. Chem. 203, 293-304. Jablonski D. and Lutz R. A. (1983) Larval ecology of marine benthic invertebrates: paleobiological implications. Biol. Rec. 58. 21-89.

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