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Biol. Bull. 202: 97-99. (April 2002)
© 2002 Marine Biological Laboratory

Egg Energetics for the Facultative Planktotroph Clypeaster rosaceus (Echinodermata: Echinoidea), Revisited

Benjamin G. Miner*, Jonathan D. Cowart and Larry R. MCEdward{dagger}

Department of Zoology, University of Florida, Gainesville, FL 32611

* To whom correspondence should be addressed. E-mail: miner{at}zoo.ufl.edu

The sand dollar Clypeaster rosaceus has an unusual reproductive strategy known as facultative planktotrophy. The egg energy previously reported by Emlet (1) for C. rosaceus is low, and because it is used to estimate values of an important parameter in marine invertebrate life-history models (s), we remeasured the egg energy content. Our measurement of egg energy content was approximately 2-fold greater than Emlet’s (0.11 ± 0.014 SD joules (J) egg -1 vs. 0.047 ± 0.007 SD J egg-1) with no difference in egg diameter (274 ± 4.38 SD µm vs. 280 ± 7.67 SD µm). This result is unlikely to be due to temporal or spatial variation among populations of C. rosaceus. Given the improved technique used to measure egg energy content, an egg energy density (J ml-1) more consistent with other observations, and the improved fit of egg size vs. egg energy regressions for echinoderm planktotrophs, we conclude that our estimate is more accurate. In addition, we detected small annual variation (10%) in egg energy content between females sampled during 2000 and 2001.

Facultative planktotrophy is intermediate between the two common types of echinoid larval development: planktotrophy and lecithotrophy (1). Planktotrophic larvae develop from small, energy-poor eggs and require exogenous food to complete development and metamorphosis. In contrast, lecithotrophic larvae develop from large, energy-rich eggs and can complete development without feeding. Although rare, facultative planktotrophs such as Clypeaster rosaceus may represent an important transition in the evolution of marine invertebrate life- history strategies (2, 3).

Models of the evolution of larval strategies in marine invertebrates characterize reproductive strategies in terms of the level of egg provisioning (s) (4). These models evaluate the trade-off between fecundity and mortality as a function of s, and assume that selection acts on this character. It is therefore important to estimate values of s for numerous species to compare the natural distribution of s with model results. An informative method for calculating values of s requires comparing egg energy content against a reference species that is near the boundary between planktotrophy and lecithotrophy (5). Clypeaster rosaceus has a level of egg provisioning close to, though greater than, the minimum necessary for lecithotrophic development (1) and can therefore be used as a reference species to calculate values of s.

Emlet (1) reported the eggs of C. rosaceus to be 280 ± 7.67 SD µm in diameter and to contain 0.020 ± 0.003 SD joules of energy per egg (J egg-1). This value of egg energy is low, relative to egg size, compared to other species of planktotrophic echinoderms—C. rosaceus has the lowest estimated egg energy density (1.79 J ml-1) of all echinoid species for which there are data (minimum value = 2.41 J ml -1; mean = 6.10 J ml-1; maximum = 11.71 J ml-1). Additionally, the egg of the echinoid Encope michelini is smaller than that of C. rosaceus (175 µm vs. 280 µm), but its energy content is greater (6) (0.046 J egg-1 vs. 0.020 J egg-1). Yet E. michelini is an obligate planktotroph (7). Considering the importance of C. rosaceus in estimating values of s in marine invertebrate life-history models, it is important to verify the published estimate of egg energy (1).

The egg energy content we estimated for C. rosaceus ranged from 0.104 to 0.120 J egg-1 in 2000 and from 0.076 to 0.120 J egg-1 in 2001, with a mean for all eight females of 0.11 ± 0.014 SD J egg-1 (Table 1). This mean value (0.11 J egg-1) is much greater than that previously reported (1) (0.020 ± 0.003 SD J egg-1). However, it has been brought to our attention that improper units were published in Emlet (1). The correct units are actually micrograms of carbon (R. B. Emlet, pers. comm.), not micrograms of organic matter as originally reported. Therefore, the actual egg energy measured by Emlet was 0.047 ± 0.007 SD J egg-1. Despite this error, our egg energy measurement is still approximately 2-fold greater than the previous one, with no difference in egg size (274 ± 4.38 SD µm and 280 ± 7.67 SD µm). There are two possible explanations for this discrepancy: geographical and temporal differences in egg energy content among populations, or inaccurate measurements of egg energy content.


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  		TABLE 1 Mean diameter, volume, and energy of eggs from five (2000) and three (2001) females of Clypeaster rosaceus.

 
This study used adult C. rosaceus from a different population and different years than Emlet (1); the Florida Keys (east Caribbean) in 2000 and 2001, and Panama (west Caribbean) in 1983, respectively. Although we sampled different populations, no other studies comparing intraspecific variation in egg energy content report differences as great as the discrepancy between Emlet’s measurements and ours (8–10). Additionally, equivalent (>=2-fold) interspecific variation in egg energy content is correlated with large increases in egg size (11–1314151617). Furthermore, we detected only a small temporal difference in egg energy between 2000 and 2001 (0.110 ± 0.006 SD J egg-1 and 0.098 ± 0.016 SD J egg-1).

We used improved methods, directly counting a small number of eggs for each replicate (exactly 20 eggs) and measuring egg energy content for 5 females in 2000 and 3 females in 2001. Also, our value of egg energy density for C. rosaceus (9.8 J ml-1) is within the range of other planktotrophic species of echinoids, and improves McEdward and Morgan’s (17) regression of egg size vs. egg energy (Fig. 1). We conclude that the value of 0.11 J egg-1 should be used to estimate parameters for future models, and for re-examining existing models (2,3).



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  		Figure 1. Linear regressions of egg size (volume) vs. egg energy content for planktotrophic echinoderms. The open circle represents Emlet’s estimate of Clypeaster rosaceus, and the open square represents our estimate. Each regression was calculated with data from McEdward and Morgan (17) for 21 species of planktotrophic echinoderms (solid circles) and one of the C. rosaceus egg energy estimates. The solid line represents the regression with Emlet’s estimate and the dotted line with our estimate.

Collections. Adult Clypeaster rosaceus were collected at a depth of 3–7 m during September 2000 and October 2001 at Long Key Channel, Florida. They were maintained in aquaria with recirculating seawater (18– 20 °C).

Egg volume and biochemical measurements. Bioenergetic measurements were made on 13 October 2000 and 21 October 2001. Vigorous shaking of adults induced spawning. Eggs from 5 females in 2000 and 3 females in 2001 were collected in separate 100-ml glass beakers containing 0.45-µm Millipore-filtered seawater (MPFSW). After being rinsed three times with MPFSW, the eggs were fertilized (>98% fertilization), which reduces breakage during counting. The diameter (d) of 20 fertilized eggs from each female was measured with an ocular micrometer on a light microscope (magnification 20x). Egg volume was calculated using the formula (1/6) {pi} d 3. Egg energy content was measured by the dichromate oxidation method of Parsons et al. (18) as modified by McEdward and Carson (9) with glucose as the standard (0–150 µg carbon). Total egg energy content was measured on five replicate batches of 20 eggs per female. Eggs were placed in separate acid-washed (0.3% acid dichromate) 13 x 100-mm glass test tubes, and almost all seawater was removed using a micropipette. Each replicate was incubated in concentrated (70%) phosphoric acid (1 ml, 15 min, 105 °C) to remove residual chloride and then oxidized with potassium dichromate (0.3%) in concentrated sulfuric acid (2 ml, 15 min, 105 °C). Samples were diluted (3.5 ml distilled water) and measured spectrophotometrically (440 nm, 1-cm path length). Energy content was calculated against the weight of glucose (µg) yielding equivalent reduction in dichromate oxidation and was reported as joules per egg (J egg-1) using the conversion 1 µg C = 3.90 x 10-2 J (9).

 


   Acknowledgments
 
We thank Richard Emlet, John Lawrence, John Pearse, Melissa Wilson, and two anonymous reviewers for comments that improved this manuscript. In addition, we thank Kevin McCarthy and the Keys Marine Laboratory staff for help with animal collection. Funding was provided by NSF grant OCE 9819593.


   Footnotes
 
Received 15 October 2001; accepted 4 February 2002.

{dagger} Deceased. Back


   Literature Cited
TOP
 Literature Cited
 

  1. Emlet, R. B. 1986. Facultative planktotrophy in the tropical echinoid Clypeaster rosaceus (Linnaeus) and a comparison with obligate planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida: Echinoidea). J. Exp. Mar. Biol. Ecol. 95: 183–202.
  2. McEdward, L. R. 1997. Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae. Am. Nat. 150: 48–72.[ISI]
  3. Levitan, D. R. 2000. Optimal egg size in marine invertebrates: theory and phylogentic analysis of the critical relationship between egg size and development time in echinoids. Am. Nat. 156: 175–192.[Medline]
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  6. George, S. B., C. M. Young, and L. Fenaux. 1997. Proximate composition of eggs and larvae of the sand dollar Encope michelini (Agassiz): the advantage of higher investment in planktotrophic eggs. Invertebr. Reprod. Dev. 32: 11–19.
  7. Eckert, G. L. 1995. A novel larval feeding strategy of the tropical sand dollar, Encope michelini (Agassiz): adaptation to food limitation and an evolutionary link between planktotrophy and lecithotrophy. J. Exp. Mar. Biol. Ecol. 187: 103–128.
  8. Thompson, R. J. 1983. The relationship between food ration and reproductive effort in the green sea urchin, Strongylocentrotus droebachiensis. Oecologia 56: 50–57.
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  10. George, S. B., C. Cellario, and L. Fenaux. 1990. Population differences in egg quality of Arbacia lixula (Echinodermata: Echinoidea): proximate composition of eggs and larval development. J. Exp. Mar. Biol. Ecol. 141: 107–118.
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  13. McEdward, L. R., and F. S. Chia. 1991. Size and energy content of eggs from echinoderms with pelagic lecithotrophic development. J. Exp. Mar. Biol. Ecol. 147: 95–102.
  14. Bridges, T. S. 1993. Reproductive investment in four developmental morphs of Streblospio (Polychaeta: Spionidae). Biol. Bull. 184: 144–152.[Abstract]
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  16. Bridges, T. S., and S. Heppell. 1996. Fitness consequences of maternal effects in Streblospio benedicti (Annelida: Polychaeta). Am. Zool. 36: 132–146.
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  18. Parsons, T. R., Y. Maita, and C. M. Lalli. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, New York.



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