Biol. Bull. 212: 12-19. (February 2007)
© 2007 Marine Biological Laboratory
High Variability in Egg Size and Energetic Content Among Intertidal Mussels
Nicole E. Phillips*
Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California
* Current Address: School of Biological Sciences, P. O. Box 600, Victoria University of Wellington, Wellington, New Zealand, 6140. E-mail: Nicole.Phillips{at}vuw.ac.nz
 |
Abstract
|
|---|
Maternal investment is a fundamentally important parameter in life-history theory and models, yet the scales at which it varies (among individuals vs. among populations) is rarely reported. In this study, variability in attributes of eggs and early larvae of Mytilus californianus was examined from four sites spanning Point Conception, California, in June and September 2001. The effects of female, site, and month were examined for the following variables: egg volume (µl), egg energy content (µg carbon per egg), and initial larval size (µm). The only significant effect on both egg traits was that of female. Females differed by up to 57% in mean egg volume and 116% in mean egg energetic content. Although there were significant effects of rearing environment, female, site, and month on initial larval size, variability in larval length was small compared to the egg traits. Mean larval length was maximally 11% different among females. Neither female body weight nor length was correlated to mean offspring traits, and there were also no significant relationships between egg traits and initial larval size. The primary source of variation in maternal investment in this system appears to be among individual females rather than over space or time.
|
Introduction
|
|---|
Egg size is a fundamentally important trait both ecologically and evolutionarily, as it reflects maternal investment and influences both maternal and offspring fitness. Interspecific studies of the relationships of egg size with life-history traits (e.g., fecundity) and larval strategies are widespread, and many correlations are well-supported at this level (McEdward and Coulter, 1987). Several studies have also examined intraspecific spatial patterns of variability in egg size for different populations of marine invertebrates (e.g., Lönning and Wennerberg, 1963; Bayne et al., 1983; Lessios, 1987; McEdward and Carson, 1987), yet explicit comparisons of variability in maternal investment among individuals versus among populations are rarely reported.
Most life-history theory predicts that variation in parental resources should lead to variation in the number of offspring, not the investment per offspring, which should be optimized for a given environment (e.g., Smith and Fretwell, 1974). According to optimal egg size theory, selection should favor a single optimal investment per offspring that depends only on offspring fitness and not on maternal attributes (i.e., age or condition); therefore increased parental resources should be used to increase the number, not the size or quality, of offspring (Glazier, 2000). This body of theory would predict that there should be little difference among females or among sites in egg size or quality, even when individual adults vary tremendously in performance. Other theories do not assume a single optimal investment per offspring, and instead suggest that maternal effects will have a strong influence on both egg size and quality and number (Venable, 1992; Bernardo, 1996), where limited resources may limit both the size and number of offspring (Glazier, 2000).
One region where neighboring populations of benthic invertebrates vary greatly in adult performance is the coast of California, spanning Point Conception. Point Conception marks an abrupt transition in oceanographic conditions (Hickey, 1993). North of the Point the water is generally colder, and upwelling is frequent and strong. In contrast, south of the Point, in the Southern California Bight, the waters are generally warmer and contain fewer nutrients, and upwelling is weaker and infrequent (Hickey, 1993). Populations of the mussel Mytilus californianus spanning Point Conception show substantial spatial variation in both growth and condition: populations north of the Point have lower body weights and lower growth rates than those south of the Point (Phillips, 2005), and they may also be less fecund (Phillips, 2002a).
Nothing is known about whether these patterns of adult performance in the field generate corresponding patterns of variability in maternal investment in eggs. The alternative views of optimal life-history theory described above make differing predictions for how females from sites on either side of Point Conception may respond to the differences in adult conditions. Studies that manipulate adult nutritional stress in the laboratory appear to favor the hypothesis that field variation in female performance will lead to corresponding variance in initial egg size or quality as well as quantity (Bayne, 1972; Bayne et al., 1975; Thompson, 1982; Guisande et al., 1996). Moreover, given the known differences among populations in average adult condition, I also predicted that differences among sites should be substantially greater than differences among females within a given site. To test these predictions, I examined variability in egg traits and initial larval size among females from M. californianus at sites spanning Point Conception, California.
|
Materials and Methods
|
|---|
I haphazardly collected individual Mytilus californianus (Conrad) of roughly intermediate adult size (shell length 52–83.6 mm, mean 69.3 mm, ± 6.98 mm st. dev.) from the mid-zone of the rocky intertidal in California in June (8–10) and September (18–19), 2001. In June, I collected mussels from three sites: Piedras, Lompoc Landing, and Arroyo Hondo; in September, mussels were collected from those sites and an additional site (Coal Oil Point, or COP). Lompoc Landing and Piedras are north of Point Conception, and Arroyo Hondo and COP are south of it (for site descriptions, see Phillips, 2005; Menge et al., 2004). After collection, I brought all mussels to the laboratory and maintained them in running seawater. I conducted the spawning experiment within a day of the final collection date in each collection series.
Mussels were spawned using a method described elsewhere (Phillips, 2002b). Briefly, I immersed mussels in jars of seawater with the pH raised to about 9 with TRIS buffer. Then I added diluted hydrogen peroxide to the seawater and allowed the mussels to incubate for an hour. After an hour, the mussels were rinsed thoroughly and repeatedly with filtered seawater (FSW, final mesh size = 0.2 µm). After being rinsed, each mussel was placed in an individual bowl of FSW. Mussels spawned within 2–3 h of exposure to treated seawater and subsequent rinsing. Mussels were spawned on two consecutive days, beginning the day following the final field collection.
All females that spawned and were used in subsequent analyses were measured for shell length and dry body weight. To obtain dry body weights, the body flesh was dissected out separately from the remaining mantle tissue (where the gonads reside), dried at about 70 °C for 48 h, then weighed. Mantle tissue was not included in the calculation of body weight because some females may not have spawned all their eggs.
Eggs were roughly spherical. I measured the diameter of 18–20 eggs from each female that spawned, and calculated egg volume assuming that they were spheres. I then made a suspension of eggs from each female in a beaker of 300 ml of FSW and counted the eggs in three separate 1-ml samples of well-stirred egg suspension. To obtain egg energy content, I calculated the amount of the egg suspension needed to obtain 7500 eggs and filtered this volume onto a glass fiber filter that had been pre-combusted at 450 °C for 30 min. A pilot study indicated that this number of eggs resulted in reliable and repeatable results from elemental analysis (CHN) using the Dumas combustion method. Filters were dried (four per female) and sent to the analytical laboratory at the University of California Santa Barbara Marine Science Institute for elemental analysis (model CEC 440HA, Exeter Analytical Corp). I used the amount of carbon (C) per filter (in micrograms) divided by 7500 to obtain the amount of carbon per egg.
From each female, I fertilized a suspension of eggs in FSW. To control for possible paternity effects, I mixed the sperm from three males from each site into one beaker (9 males total in June, 12 in September). I did not quantify sperm concentration but visually approximated sperm density from each male, adding aliquots of each to the beaker. I fertilized the eggs with an equivalent volume of the well-stirred sperm mixture for each female’s eggs. Fertilization success ranged from 93% to 100%. Fertilized eggs were distributed in bowls with 500 ml of FSW at a density of 200 eggs/ml, with three replicate bowls for each female. These bowls were held at 17–19 °C in a cold room. After 3 days of development the embryos had reached the straight hinge, or D, stage, when the larval shell has initially formed and feeding begins. At this point, I measured the shell length of 20–26 larvae from each bowl.
I used nested ANOVAs to examine the effects of month, site, and female (random factor, nested within site and month) on egg volume and egg energetic content. Because COP was sampled only in September, data from this site were excluded from the full model. When month and the interaction between month and site were found to be insignificant, I used a reduced model to further explore the possible effect of site. Factors in the reduced model were site and female (nested within site), and the data from COP was included. I used similar nested analyses to examine the effects of month, site, female (random factor, nested within site and month), and bowl (random factor, nested within female, site and month) on initial larval length. To further explore whether location (north or south of Point Conception) was an important factor, I also conducted a series of nested ANOVAs on both egg traits and larval length, only for September, when I had data for two northern and two southern sites. These three nested ANOVAs (on the response variables egg volume, egg energetic content, and larval length) were the same as the models described above with the addition of the factor "location," in which sites were nested.
Significant differences in all models were explored further using post hoc Tukey or SNK tests. All data were examined graphically to ensure the fulfillment of ANOVA assumptions prior to analyses. Analyses were done using the statistical software JMP (ver. 4.0.4, developed by the SAS Institute).
The number of females used from each site on each date varied (Table 1). Occasionally, some females whose eggs were used for egg size were not used for other analyses. Because of the variable numbers of females, the design is unbalanced; therefore, analyses used restricted maximum likelihood estimation rather than the maximum likelihood suggested by Quinn and Keough (2002) and others. However, a comparison of results obtained with the two procedures demonstrated only trivial differences between them.
Finally, I also examined possible correlations between mean values of egg and larval traits among females, and with the offspring traits and female traits (body weight and shell length).
|
Results
|
|---|
For egg volume and egg energetic content, the effect of females was always significant (Fig. 1; Tables 2 and 3). In the initial full model, there was also a significant site effect for egg volume (Table 2). A post hoc Tukey test indicated that this was because eggs from Arroyo Hondo were significantly smaller than eggs from Lompoc Landing (Fig. 1A). In the reduced model used to further examine the effects of site and female without the month term and including data from COP (the other southern site), there was no longer a significant effect of site on egg volume (Table 2). Further, there was no significant effect of location of sites (north vs. south of Point Conception) on egg volume or egg energetic content in September (Table 3). Apparently, therefore, variability in egg traits has no spatial pattern.
View larger version (13K):
[in this window]
[in a new window]
|
Figure 1. Egg volume (A) and egg energetic content (B) from Mytilus californianus collected from four sites in California. Bars represent means ±1 SE: open bars are from June; black bars are from September. Note: COP (Coal Oil Point) was sampled only in September. Lowercase letters above bars represent significant differences among sites from the initial full statistical model (see Results). Different letters represent groupings from a post hoc Tukey test (P < 0.05); data from COP were not included in that analysis.
|
|
View this table:
[in this window]
[in a new window]
|
Table 2 Results of nested ANOVAs on egg traits, followed by reduced models that exclude month as a term (because of its nonsignificance in the full models); the reduced models include data from Coal Oil Point in September
|
|
View this table:
[in this window]
[in a new window]
|
Table 3 Results of nested ANOVAs on egg traits from September only, nesting sites within location (north or south of Point Conception)
|
|
From the reduced model using all the data, 20% of the variance in egg volume was attributed to females, and 80% was residual. The pattern was opposite for egg energetic content: 86% of the variation in egg energetic content was attributable to females, and 14% was residual. Thus, although the effect of females was large for both egg traits (among females, mean egg volume differed by up to 57%, whereas mean energetic content differed by up to 116%), egg volume also showed substantial variability within females. This can also be seen from the coefficients of variation (CV) for each female for egg traits: CVs of egg volume among all females ranged from 5.5% to 24.4%, whereas CVs of egg energetic content were lower, ranging from 1.2% to 13.3%. These values were very similar across collections, indicating a lack of patterns in variability in these attributes across sites or months.
For larval length, all main effects in the initial full model (site, month, female, and bowl) and the interaction between month and site were significant (Fig. 2, Table 4). Post hoc analyses on each month indicate that the interaction between month and site occurred because in June larvae from Arroyo Hondo were slightly smaller than those from Piedras and Lompoc Landing, whereas in September the pattern was reversed, with larvae from Piedras slightly smaller than those from Arroyo Hondo. Although all main effects and the interaction of month and site were significant on influencing initial larval size, the magnitude of the differences in larval length was much smaller than for the egg traits (Fig. 2); for example, initial larval size differed only by a maximum of 11% among females.
View larger version (9K):
[in this window]
[in a new window]
|
Figure 2. Initial larval length from the same sites as in Fig 1. Bars represent means ±1 SE: open bars are from June; black bars are from September. COP = Coil Oil Point.
|
|
In the nested analysis on data from September only, location of sites was not significant; however, differences in larval size among sites became significant (Table 5). A post hoc SNK test revealed that larvae from the northernmost site (Piedras) and the southernmost site (COP) were smaller than larvae from the other two sites. Again, these differences, although significant, were very small (2%).
View this table:
[in this window]
[in a new window]
|
Table 5 Results of nested ANOVA on larval length (µm), using data from September only, and nesting sites within location (north or south of Point Conception)
|
|
Although the bowl effect was significant (indicating that the rearing environment had an effect on initial larval size), it was relatively small; thus I used pooled larval measurements per female to calculate a CV of larval length for each female. These ranged from 1.9% to 6.2%, considerably lower than for either of the egg traits; again these values were similar regardless of site or month of collection. Thus, egg volume was the most variable trait within females (and also highly variable among females), followed by egg energy content (which had the highest variability among females), and initial larval size (which appeared to have relatively low variability both within and among females).
Using mean values for each female, I found no predictive relationships (1) between egg volume and egg energetic content, (2) between either egg attribute and initial larval length, or (3) between female body weight or shell length and any of the offspring traits, either within each collection (where each female collected from the same site in the same month represents an independent sample), or using all females combined.
|
Discussion
|
|---|
Contrary to a priori predictions, the large differences previously documented in adult performance among sites spanning Point Conception did not correspond to variability in egg and larval traits of Mytilus californianus. Although females at sites south of Point Conception are consistently larger, with greater body weight and better condition, than females from north of the Point (Phillips, 2002a; 2005), there were no consistent differences in egg and larval traits when the potential effects of adult size were removed by comparing adults of similar size. Laboratory studies on several bivalve species have found strong influences of stress in adults on egg attributes and larval performance (Bayne, 1972; Helm et al., 1973; Bayne et al., 1975, 1978; Gallager and Mann, 1986). Although field studies of these traits are rare, differences among populations in egg and larval attributes have been found. Barber and Blake (1983) reported a reduction in egg size with decreasing latitude in the bivalve Argopecten irradians on the East Coast of the United States, which they attributed to decreasing food availability. Bertram and Strathmann (1998), George (1990), and George et al. (1990) reported differences in egg sizes or egg quality (as measured by biochemical composition) when comparing two populations of sea urchins, and they attributed these to differences in the availability of food to adults at the sites as well. McEdward and Carson (1987) found differences not only in egg size but also in egg organic content among sea star populations from different sites. Finally, George (1996) summarized the results from several studies on echinoderms on variability in egg and larval attributes in the context of favorable and unfavorable adult sites, and found that females from favorable sites (in terms of food availability) were often larger and spawned more numerous, larger, and better quality eggs.
Bayne et al. (1978) manipulated adult food and temperature prior to spawning Mytilus edulis, and achieved up to a 6-fold difference in egg energetic content. The authors report that these differences across treatments in their experiments were largely due to changes in the lipid fraction (rather than protein or carbohydrates). Their results suggest that the differences in egg energetic content among females in the current study may also be primarily due to changes in lipid, although I did not explicitly examine the biochemical composition of the eggs.
One hypothesis for the lack of a site effect in this study may be that even though adult performance at these sites does show marked variation, the across-site variability in resources is insufficient to produce differences in egg attributes (such as can be produced in the laboratory for bivalves, or that has been found in the field for echinoderms). Perhaps the earlier laboratory experiments used extremes of nutritional stress not encountered in this field system. Results from a previous study (Phillips, 2005) point to the fact that the differences in adult performance among sites spanning Point Conception are probably not due primarily to patterns of variability in food supply, supporting the idea that animals from the sites north of Point Conception are not under extremes of nutritional stress compared to those from the south.
Although there was no spatial pattern of variability in egg or early larval traits, there was considerable variability among females. What might account for this large variability in egg traits among female M. californianus in this study? Differences in female body size or condition were not related to variability in egg attributes, although I tried to minimize the effects of adult size by collecting animals in a relatively narrow size range. Other studies that explicitly examined the effects of maternal size on offspring size or quality have had mixed results. Many researchers have found positive correlations between female size or condition and egg or offspring size (sea star—George, 1994; fish—Marteinsdottir and Steinarsson, 1998; gastropod— Ito, 1997; insects—McIntyre and Gooding, 2000; birds—Robb et al., 1992), yet some have found negative relationships between maternal size and egg size (fish—Iguchi and Yamaguchi, 1994), and still others, like this study, have found no relationship between maternal characteristics and egg or offspring size (fish—Marsh, 1984; amphipod—Glazier, 2000; insects—Corkum et al., 1997; echinoids—Lessios, 1987).
It is possible that variability in egg attributes among females in the current study could be artificially inflated if the induction of spawning causes females to release eggs that would not have been released in a natural spawning situation. This cannot be ruled out as a factor, but the high fertilization success of eggs from all females used in this study supports the contention that the females were in fact releasing mature eggs. Thus, potential confounding effects of induced spawning appear unlikely to be a major influence. Existing estimates of egg size and biochemical content for Mytilus spp. (and other bivalves as well) are all from animals that were induced to spawn by various methods (e.g., Helm et al., 1973; Bayne et al., 1975, 1978; Gallager and Mann, 1986).
Potential contributions to the large variability in egg attributes among females within a site include small-scale variability in microhabitat, previous reproductive history, genetics, or some combination of these factors. Evidence from experiments on growth (Phillips, 2005) and thermal stress (Helmuth and Hofmann, 2001) demonstrate that these physiological responses can vary extensively, on very small spatial scales, among individuals. Because mussels are essentially immobile as adults, individuals are likely strongly influenced by the proximity of neighbors (which may influence the feeding rate of these filter-feeders), the geomorphology of the rocky substrate, the presence or absence of shade from other organisms or rock outcroppings (which may influence thermal or desiccation stress), or other factors. Dittman and Robles (1991) found that the presence or absence of algal epiphytes on M. californianus shells had strong effects on mussel growth and reproduction (although they did not measure egg characteristics) from individuals immediately adjacent to each other. Any or all of these factors (neighbors, shade, substrate characteristics, epiphytes) can vary on small spatial scales and may potentially influence allocation to eggs. In the laboratory, stressed adult mussels do in fact produce lower quality eggs and larvae (e.g., Bayne, 1972). If this variable microhabitat hypothesis is correct, the distribution of microhabitat stresses would have to be relatively consistent among sites; otherwise, I should have found a site effect on egg and larval attributes as well.
An alternative explanation for the large variability among individuals comes from their reproductive histories. Individual mussels spawn repeatedly throughout the year. There is no way to know the reproductive history of any given individual collected in this study, but other organisms that spawn multiple times show evidence that egg size and quality can vary substantially among spawning events of the same individual: egg size or quality generally decline with increased spawning (Qian and Chia, 1992; Ito, 1997). Gallager and Mann (1986) found that repeated spawning of the same broodstock of the bivalve Mercenaria mercenaria over an extended time had detrimental effects on egg characteristics and larval survival from those adults.
Given that development is reliant on endogenous stores until the first larval stage is reached and feeding begins, the significant effects of site and month of collection on larval size are surprising considering that these factors were not significant for egg traits. In contrast to the high variability among females in egg traits, however, variability in initial larval length was relatively low. This may indicate that the significant effects found here on initial larval length were, although inexplicable, trivial. The relatively low variability in initial larval size may be the result of selective mortality or may indicate strong constraints on initial larval size.
Unfortunately, studies explicitly examining among-individual variability in egg attributes are scarce for marine invertebrates (Lessios, 1987), and attributing cause to that variability is necessarily speculative. The current study does support empirical work from other systems demonstrating that intraspecific and intrapopulation variability in egg traits can be common (Bernardo, 1996). Most life-history models predict that such variation should be small in natural populations. As a result of this mismatch between theory and observation, some are suggesting that traditional life-history theory, with its strong reliance on an optimal egg size, is insufficient (Bernardo, 1996). In a thoughtful treatment of this issue, Bernardo (1996) suggested that life-history theorists should pay more attention to understanding (1) the variance of the trait of egg size rather than focusing on the mean, and (2) "how joint influences of local resource environments and maternal characters have affected the evolution of egg size." This empirical study supports his contentions.
|
Acknowledgments
|
|---|
This research was supported by funds from a National Science Foundation graduate fellowship to the author, and in part by NSF BIR94-13141 and NSF GER93-54870 to W. Murdoch. This is contribution number 229 from PISCO, the Partnership for Interdisciplinary Studies of Coastal Oceans, funded primarily by the Gordon and Betty Moore Foundation and the David and Lucile Packard Foundation.
|
Footnotes
|
|---|
Received 22 June 2006; accepted 17 November 2006.
|
Literature Cited
|
|---|
Barber, B. J., and N. J. Blake. 1983. Growth and reproduction of the bay scallop, Argopecten irradians (Lamarck) at its southern distributional limit. J. Exp. Mar. Biol. Ecol.66:247–256.
Bayne, B. L. 1972. Some effects of stress in the adult on the larval development of Mytilus edulis. Nature 237:459.[Medline]
Bayne, B. L, P. A. Gabbott, and J. Widdows. 1975. Some effects of stress in the adult on the eggs and larvae of Mytilus edulis L. J. Mar. Biol. Assoc. UK 55:675–689.
Bayne, B. L., D. L. Holland, M. N. Moore, D. M. Lowe, and J. Widdows. 1978. Further studies on the effects of stress in the adult on the eggs of Mytilus edulis. J. Mar. Biol. Assoc. UK 58:824–841.
Bayne, B. L., P. N. Salkeld, and C. M. Worrall. 1983. Reproductive effort and value in different populations of the marine mussel, Mytilus edulis L. Oecologia 59:18–26.[Medline]
Bernardo, J. 1996. The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am. Zool. 36:216–236.
Bertram, D. F., and R. R. Strathmann. 1998. Effects of maternal and larval nutrition on growth and form of planktotrophic larvae. Ecology 79:315–327.
Corkum, L. D., J. J. H. Ciborowski, and R. G. Poulin. 1997. Effects of emergence date and maternal size on egg development and sizes of eggs and first-instar nymphs of a semelparous aquatic insect. Oecologia 111:69–75.
Dittman, D., and C. Robles. 1991. Effect of algal epiphytes on the mussel Mytilus californianus. Ecology 72:286–296.
Gallager, S. M., and R. Mann. 1986. Growth and survival of larvae of Mercenaria mercenaria (L.) and Crassostrea virginica (Gmelin) relative to broodstock conditioning and lipid content of eggs. Aquaculture 56:105–121.[ISI]
George, S. B. 1990. Population and seasonal differences in egg quality of Arbacia lixula (Echinodermata: Echinoidea). Invertebr. Reprod. Dev. 17:111–121.
George, S. B. 1994. Population differences in maternal size and offspring quality for Leptasterias epichlora (Brandt) (Echinodermata: Asteroidea). J. Exp. Mar. Biol. Ecol. 175:121–131.
George, S. B. 1996. Echinoderm egg and larval quality as a function of adult nutritional state. Oceanol. Acta 19:297–308.
George, S. B., C. Cellario, and L. Fenaux. 1990. Population differences in egg quality of Arbacia lixula (Echinodermata: Echinoidea): proximate composition of egg and larval development. J. Exp. Mar. Biol. Ecol. 141:107–118.
Glazier, D. S. 2000. Is fatter fitter? Body storage and reproduction in ten populations of the freshwater amphipod Gammarus minus. Oecologia 122:335–345.
Guisande, C., J. Sanchez, I. Maneiro, and A. Miranda. 1996. Trade-off between offspring number and offspring size in the marine copepod Euterpina acutifrons at different food concentrations. Mar. Ecol. Prog. Ser. 143:37–44.
Helm, M. M., D. L. Holland, and R. R. Stephenson. 1973. The effect of supplementary algal feeding of a hatchery breeding stock of Ostrea edulis L. on larval vigour. J. Mar. Biol. Assoc. UK 53:673–684.
Helmuth, B. S. T., and G. E. Hofmann. 2001. Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol. Bull. 201:374–384.[Abstract/Free Full Text]
Hickey, B. M. 1993. Physical oceanography. P. 1970 in Ecology of the Southern California Bight: A Synthesis and Interpretation, M. D. Dailey, D. J. Reish, and J. W. Anderson, eds. University of California Press, Berkeley.
Iguchi, K., and M. Yamaguchi. 1994. Adaptive significance of inter- and intrapopulational egg size variation in Ayu Plecoglossus altivelis (Osmeridae). Copeia 1994:184–190.
Ito, K. 1997. Egg-size and -number variations related to maternal size and age, and the relationship between egg size and larval characteristics in an annual marine gastropod, Haloa japonica (Opisthobranchia; Cephalaspidea). Mar. Ecol. Prog. Ser. 152:187–195.
Lessios, H. A. 1987. Temporal and spatial variation in egg size of thirteen Panamian echinoids. J. Exp. Mar. Biol. Ecol. 114:217–239.
Lönning, S., and C. Wennerberg. 1963. Biometric studies of echinoderm eggs. Sarsia 11:25–27.
Marsh, E. 1984. Egg size variation in central Texas populations of Etheostoma spectabile (Pisces: Percidae). Copeia 1984:291–301.
Marteinsdottir, G., and A. Steinarsson. 1998. Maternal influence on the size and viability of Iceland cod Gadus morhua eggs and larvae. J. Fish Biol. 52:1241–1258.
McEdward, L. R., and S. F. Carson. 1987. Variation in egg content and its relationship with egg size in the starfish Solaster stimpsoni. Mar. Ecol. Prog. Ser. 37:159–169.
McEdward, L. R., and L. K. Coulter. 1987. Egg volume and energetic content are not correlated among sibling offspring of starfish: implications for life-history theory. Evolution 41:914–917.[ISI]
McIntyre, G. S., and R. H. Gooding. 2000. Egg size, contents, and quality: maternal-age and -size effects on house fly eggs. Can. J. Zool. 78:1544–1551.
Menge, B. A., C. Blanchette, P. Raimondi, T. Freidenburg, S. Gaines, J. Lubchenco, D. Lohse, G. Hudson, M. Foley, and J. Pamplin. 2004. Species interaction strength: testing model predictions along an upwelling gradient. Ecol. Monogr. 74:663–684.
Phillips, N. E. 2002a. Benthic-pelagic coupling in intertidal communities: integrating across the life cycle of filter-feeding marine invertebrates. Ph.D. dissertation, University of California, Santa Barbara.
Phillips, N. E. 2002b. Effects of nutrition-mediated larval condition on juvenile performance in a marine mussel. Ecology 83:2562–2574.[ISI]
Phillips, N. E. 2005. Growth of filter-feeding benthic invertebrates from a region with variable upwelling intensity. Mar. Ecol. Prog. Ser. 295:79–89.
Qian, P.-Y., and F.-S. Chia. 1992. Effect of aging on reproduction in a marine polychaete Capitella sp. J. Exp. Mar. Biol. Ecol. 156:23–38.
Quinn, G. P., and M. J. Keough. 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
Robb, L., A. K. Martin, and S. J. Hannon. 1992. Spring body condition, fecundity and survival in the willow ptarmigan. J. Anim. Ecol. 61:215–223.
Smith, C. C. and. S. D. Fretwell. 1974. The optimal balance between size and number of offspring. Am. Nat. 108:499–506.[ISI]
Thompson, R. J. 1982. The relationship between food ration and reproductive effort in the green sea urchin, Strongylocentrotus droebachiensis. Oecologia 56:50–57.
Venable, D. L. 1992. Size-number trade-offs and the variation of seed size with plant resource status. Am. Nat. 140:287–304.[ISI]
TOP
Abstract
Introduction
