Variability in egg and jelly-coat size and their contribution to target size for spermatozoa: a review for the Echinodermata
Dione J. Deaker A D , Shawna A. Foo B and Maria Byrne A C
+ Author Affiliations
- Author Affiliations
A School of Medical Sciences, Anderson Stuart Building (F13), The University of Sydney, Sydney, NSW 2006, Australia.
B Department of Global Ecology, Carnegie Institution for Science, 260 Panama Street, Stanford, CA 94305, USA.
C School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW 2006, Australia.
D Corresponding author. Email: dione.deaker@sydney.edu.au
Marine and Freshwater Research 70(7) 995-1006 https://doi.org/10.1071/MF18134
Submitted: 30 March 2018 Accepted: 27 November 2018 Published: 21 February 2019
Abstract
Fertilisation and development in broadcast-spawning marine invertebrates depends on the ability of the egg to attract spermatozoa and provision progeny. Echinoderm eggs have a jelly coat that facilitates sperm–egg collisions. We investigated variation in egg volume and target area for spermatozoa provided by the jelly coat within and between three sea urchin species (Heliocidaris erythrogramma, Heliocidaris tuberculata, Centrostephanus rodgersii), as well as across 22 echinoderm species for which data are available. Egg and jelly-coat size varied within spawns of individual females, between females of a species and between species. The jelly coat increased egg target area by 125–489% for echinoids with planktotrophic development. In general, planktotrophic echinoids (n = 16) with larger eggs had thicker jelly coats, as did H. tuberculata females with larger eggs. Variability in egg and jelly-coat size within a species indicates that these traits are prone to maternal effects and may be influenced by factors such as sperm environment and offspring fitness that drive selection on egg investment. The greater variability in jelly-coat size compared with that of the egg has a large potential to affect fertilisation and should be considered in models of fertilisation kinetics. Egg size alone cannot be used as a metric to infer target size for spermatozoa.
Additional keywords: broadcast spawning, Centrostephanus, Echinoderms, egg size, extracellular matrix, Heliocidaris, reproductive biology.
References
Alcorn, N. J., and Allen, J. D. (2009). How do changes in parental investment influence development in echinoid echinoderms? Evolution & Development 11, 719–727.| How do changes in parental investment influence development in echinoid echinoderms?Crossref | GoogleScholarGoogle Scholar |
Allen, J. D. (2008). Size-specific predation on marine invertebrate larvae. The Biological Bulletin 214, 42–49.
| Size-specific predation on marine invertebrate larvae.Crossref | GoogleScholarGoogle Scholar | 18258774PubMed |
Allen, R. M., Buckley, Y. M., and Marshall, D. J. (2008). Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages. American Naturalist 171, 225–237.
| Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages.Crossref | GoogleScholarGoogle Scholar | 18197775PubMed |
Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.
Babcock, R. C., and Mundy, C. N. (1992). Reproductive-biology, spawning and field fertilization rates of Acanthaster planci. Australian Journal of Marine and Freshwater Research 43, 525–534.
| Reproductive-biology, spawning and field fertilization rates of Acanthaster planci.Crossref | GoogleScholarGoogle Scholar |
Bernardo, J. (1996a). Maternal effects in animal ecology. American Zoologist 36, 83–105.
| Maternal effects in animal ecology.Crossref | GoogleScholarGoogle Scholar |
Bernardo, J. (1996b). The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. American Zoologist 36, 216–236.
| The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations.Crossref | GoogleScholarGoogle Scholar |
Bolton, T. F., Thomas, F. I. M., and Leonard, C. N. (2000). Maternal energy investment in eggs and jelly coats surrounding eggs of the echinoid Arbacia punctulata. The Biological Bulletin 199, 1–5.
| Maternal energy investment in eggs and jelly coats surrounding eggs of the echinoid Arbacia punctulata.Crossref | GoogleScholarGoogle Scholar | 10975636PubMed |
Bonnell, B. S., Larabell, C., and Chandler, D. E. (1993). The sea-urchin egg jelly coat is a 3-dimensional fibrous network as seen by intermediate voltage electron-microscopy and deep-etching analysis. Molecular Reproduction and Development 35, 181–188.
| The sea-urchin egg jelly coat is a 3-dimensional fibrous network as seen by intermediate voltage electron-microscopy and deep-etching analysis.Crossref | GoogleScholarGoogle Scholar | 8318223PubMed |
Bonnell, B. S., Keller, S. H., Vacquier, V. D., and Chandler, D. E. (1994). The sea-urchin egg jelly coat consists of globular glycoproteins bound to a fibrous fucan superstructure. Developmental Biology 162, 313–324.
| The sea-urchin egg jelly coat consists of globular glycoproteins bound to a fibrous fucan superstructure.Crossref | GoogleScholarGoogle Scholar | 8125196PubMed |
Caballes, C. F., Pratchett, M. S., Kerr, A. M., and Rivera-Posada, J. A. (2016). The role of maternal nutrition on oocyte size and quality, with respect to early larval development in the coral-eating starfish, Acanthaster planci. PLoS One 11, e0158007.
| The role of maternal nutrition on oocyte size and quality, with respect to early larval development in the coral-eating starfish, Acanthaster planci.Crossref | GoogleScholarGoogle Scholar | 27327627PubMed |
Collin, R. (2010). Repeatability of egg size in two marine gastropods: brood order and female size do not contribute to intraspecific variation. Marine Ecology Progress Series 410, 89–96.
| Repeatability of egg size in two marine gastropods: brood order and female size do not contribute to intraspecific variation.Crossref | GoogleScholarGoogle Scholar |
Crean, A. J., and Marshall, D. J. (2009). Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 364, 1087–1096.
| Coping with environmental uncertainty: dynamic bet hedging as a maternal effect.Crossref | GoogleScholarGoogle Scholar | 19324613PubMed |
Crean, A. J., and Marshall, D. J. (2015). Eggs with larger accessory structures are more likely to be fertilized in both low and high sperm concentrations in Styela plicata (Ascidiaceae). Marine Biology 162, 2251–2256.
| Eggs with larger accessory structures are more likely to be fertilized in both low and high sperm concentrations in Styela plicata (Ascidiaceae).Crossref | GoogleScholarGoogle Scholar |
Crimaldi, J. P., and Zimmer, R. K. (2014). The physics of broadcast spawning in benthic invertebrates. Annual Review of Marine Science 6, 141–165.
| The physics of broadcast spawning in benthic invertebrates.Crossref | GoogleScholarGoogle Scholar | 23957600PubMed |
Emlet, R. B., and Hoegh-Guldberg, O. (1997). Effects of egg size on postlarval performance: experimental evidence from a sea urchin. Evolution 51, 141–152.
| Effects of egg size on postlarval performance: experimental evidence from a sea urchin.Crossref | GoogleScholarGoogle Scholar | 28568783PubMed |
Emlet, R. B., and Sadro, S. S. (2006). Linking stages of life history: how larval quality translates into juvenile performance for an intertidal barnacle (Balanus glandula). Integrative and Comparative Biology 46, 334–346.
| Linking stages of life history: how larval quality translates into juvenile performance for an intertidal barnacle (Balanus glandula).Crossref | GoogleScholarGoogle Scholar | 21672746PubMed |
Evans, J. P., Garcia-Gonzalez, F., Almbro, M., Robinson, O., and Fitzpatrick, J. L. (2012). Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate. Proceedings of the Royal Society of London – B. Biological Sciences 279, 2855–2861.
| Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate.Crossref | GoogleScholarGoogle Scholar |
Farley, G. S., and Levitan, D. R. (2001). The role of jelly coats in sperm–egg encounters, fertilization success, and selection on egg size in broadcast spawners. American Naturalist 157, 626–636.
| 18707279PubMed |
Foo, S. A., Deaker, D., and Byrne, M. (2018). Cherchez la femme – impact of ocean acidification on the egg jelly coat and attractants for sperm. The Journal of Experimental Biology 221, jeb177188.
| Cherchez la femme – impact of ocean acidification on the egg jelly coat and attractants for sperm.Crossref | GoogleScholarGoogle Scholar | 29674376PubMed |
George, S. B. (1990). Population and seasonal differences in egg quality of Arbacia lixula (Echinodermata, Echinoidea). Invertebrate Reproduction & Development 17, 111–121.
| Population and seasonal differences in egg quality of Arbacia lixula (Echinodermata, Echinoidea).Crossref | GoogleScholarGoogle Scholar |
George, S. B. (1994). Population differences in maternal size and offspring quality for Leptasterias epichlora (Brant) (Echinodermata, Asteroidea). Journal of Experimental Marine Biology and Ecology 175, 121–131.
| Population differences in maternal size and offspring quality for Leptasterias epichlora (Brant) (Echinodermata, Asteroidea).Crossref | GoogleScholarGoogle Scholar |
George, S. B. (1996). Echinoderm egg and larval quality as a function of adult nutritional state. Oceanologica Acta 19, 297–308.
George, S. B. (1999). Egg quality, larval growth and phenotypic plasticity in a forcipulate seastar. Journal of Experimental Marine Biology and Ecology 237, 203–224.
| Egg quality, larval growth and phenotypic plasticity in a forcipulate seastar.Crossref | GoogleScholarGoogle Scholar |
Hagström, B. E. (1959). Further experiments on jelly-free sea urchin eggs. Experimental Cell Research 17, 256–261.
| Further experiments on jelly-free sea urchin eggs.Crossref | GoogleScholarGoogle Scholar | 13663878PubMed |
Hansbrough, J. R., and Garbers, D. L. (1981). Speract – purification and characterization of a peptide associated with eggs that activates spermatozoa. The Journal of Biological Chemistry 256, 1447–1452.
| 6256397PubMed |
Hirohashi, N., Kamei, N., Kubo, H., Sawada, H., Matsumoto, M., and Hoshi, M. (2008). Egg and sperm recognition systems during fertilization. Development, Growth & Differentiation 50, S221–S238.
| Egg and sperm recognition systems during fertilization.Crossref | GoogleScholarGoogle Scholar |
Hoshi, M., Nishigaki, T., Ushiyama, A., Okinaga, T., Chiba, K., and Matsumoto, M. (1994). Egg-jelly signal molecules for triggering the acrosome reaction in starfish spermatozoa. The International Journal of Developmental Biology 38, 167–174.
| 7981026PubMed |
Inamdar, M. V., Kim, T., Chung, Y. K., Was, A. M., Xiang, X., Wang, C. W., Takayama, S., Lastoskie, C. M., Thomas, F. I. M., and Sastry, A. M. (2007). Assessment of sperm chemokinesis with exposure to jelly coats of sea urchin eggs and resact: a microfluidic experiment and numerical study. The Journal of Experimental Biology 210, 3805–3820.
| Assessment of sperm chemokinesis with exposure to jelly coats of sea urchin eggs and resact: a microfluidic experiment and numerical study.Crossref | GoogleScholarGoogle Scholar | 17951422PubMed |
Jensen, N., Allen, R. M., and Marshall, D. J. (2014). Adaptive maternal and paternal effects: gamete plasticity in response to parental stress. Functional Ecology 28, 724–733.
| Adaptive maternal and paternal effects: gamete plasticity in response to parental stress.Crossref | GoogleScholarGoogle Scholar |
Jondeung, A., and Czihak, G. (1982). Histochemical-studies of jelly coat of sea-urchin eggs during oogenesis. Histochemistry 76, 123–136.
| Histochemical-studies of jelly coat of sea-urchin eggs during oogenesis.Crossref | GoogleScholarGoogle Scholar | 6217173PubMed |
Kidd, P. (1978). The jelly and vitelline coats of the sea urchin egg: new ultrastructural features. Journal of Ultrastructure Research 64, 204–215.
| The jelly and vitelline coats of the sea urchin egg: new ultrastructural features.Crossref | GoogleScholarGoogle Scholar | 568669PubMed |
Kjesbu, O. S., Solemdal, P., Bratland, P., and Fonn, M. (1996). Variation in annual egg production in individual captive Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 53, 610–620.
| Variation in annual egg production in individual captive Atlantic cod (Gadus morhua).Crossref | GoogleScholarGoogle Scholar |
Levitan, D. R. (1991). Influence of body size and population-density on fertilization success and reproductive output in a free-spawning invertebrate. The Biological Bulletin 181, 261–268.
| Influence of body size and population-density on fertilization success and reproductive output in a free-spawning invertebrate.Crossref | GoogleScholarGoogle Scholar | 29304646PubMed |
Levitan, D. R. (1993). The importance of sperm limitation to the evolution of egg size in marine invertebrates. American Naturalist 141, 517–536.
| The importance of sperm limitation to the evolution of egg size in marine invertebrates.Crossref | GoogleScholarGoogle Scholar | 19425997PubMed |
Levitan, D. (1998). Does Bateman’s principle apply to broadcast-spawning organisms? Egg traits influence in situ fertilization rates among congeneric sea urchins. Evolution 52, 1043–1056.
| Does Bateman’s principle apply to broadcast-spawning organisms? Egg traits influence in situ fertilization rates among congeneric sea urchins.Crossref | GoogleScholarGoogle Scholar | 28565227PubMed |
Levitan, D. R. (2000). Optimal egg size in marine invertebrates: theory and phylogenetic analysis of the critical relationship between egg size and development time in echinoids. American Naturalist 156, 175–192.
| Optimal egg size in marine invertebrates: theory and phylogenetic analysis of the critical relationship between egg size and development time in echinoids.Crossref | GoogleScholarGoogle Scholar | 10856200PubMed |
Levitan, D. R. (2006). The relationship between egg size and fertilization success in broadcast-spawning marine invertebrates. Integrative and Comparative Biology 46, 298–311.
| The relationship between egg size and fertilization success in broadcast-spawning marine invertebrates.Crossref | GoogleScholarGoogle Scholar | 21672743PubMed |
Levitan, D. R., and Irvine, S. D. (2001). Fertilization selection on egg and jelly-coat size in the sand dollar Dendraster excentricus. Evolution 55, 2479–2483.
| Fertilization selection on egg and jelly-coat size in the sand dollar Dendraster excentricus.Crossref | GoogleScholarGoogle Scholar | 11831663PubMed |
Luttikhuizen, P. C., Honkoop, P. J. C., and Drent, J. (2011). Intraspecific egg size variation and sperm limitation in the broadcast spawning bivalve Macoma balthica. Journal of Experimental Marine Biology and Ecology 396, 156–161.
| Intraspecific egg size variation and sperm limitation in the broadcast spawning bivalve Macoma balthica.Crossref | GoogleScholarGoogle Scholar |
Marshall, D. J., and Bolton, T. F. (2007). Effects of egg size on the development time of non-feeding larvae. The Biological Bulletin 212, 6–11.
| Effects of egg size on the development time of non-feeding larvae.Crossref | GoogleScholarGoogle Scholar | 17301326PubMed |
Marshall, D. J., and Keough, M. J. (2003). Sources of variation in larval quality for free-spawning marine invertebrates: egg size and the local sperm environment. Invertebrate Reproduction & Development 44, 63–70.
| Sources of variation in larval quality for free-spawning marine invertebrates: egg size and the local sperm environment.Crossref | GoogleScholarGoogle Scholar |
Marshall, D. J., and Keough, M. J. (2004). When the going gets rough: effect of maternal size manipulation on larval quality. Marine Ecology Progress Series 272, 301–305.
| When the going gets rough: effect of maternal size manipulation on larval quality.Crossref | GoogleScholarGoogle Scholar |
Marshall, D. J., and Keough, M. J. (2008). The evolutionary ecology of offspring size in marine invertebrates. Advances in Marine Biology 53, 1–60.
| The evolutionary ecology of offspring size in marine invertebrates.Crossref | GoogleScholarGoogle Scholar |
Marshall, D. J., and Uller, T. (2007). When is a maternal effect adaptive? Oikos 116, 1957–1963.
| When is a maternal effect adaptive?Crossref | GoogleScholarGoogle Scholar |
Marshall, D. J., Bonduriansky, R., and Bussiere, L. F. (2008). Offspring size variation within broods as a bet-hedging strategy in unpredictable environments. Ecology 89, 2506–2517.
| Offspring size variation within broods as a bet-hedging strategy in unpredictable environments.Crossref | GoogleScholarGoogle Scholar | 18831172PubMed |
Marzinelli, E. M., Penchaszadeh, P. E., and Bigatti, G. (2008). Egg strain in the sea urchin Pseudechinus magellanicus (Echinoidea: Temnopleuridae). Revista de Biología Tropical 56, 335–339.
McEdward, L. R., and Carson, S. F. (1987). Variation in egg organic content and its relationship with egg size in the starfish Solaster stimpsoni. Marine Ecology Progress Series 37, 159–169.
| Variation in egg organic content and its relationship with egg size in the starfish Solaster stimpsoni.Crossref | GoogleScholarGoogle Scholar |
McEdward, L. R., and Coulter, L. K. (1987). Egg volume and energetic content are not correlated among sibling offspring of starfish – implications for life-history theory. Evolution 41, 914–917.
| Egg volume and energetic content are not correlated among sibling offspring of starfish – implications for life-history theory.Crossref | GoogleScholarGoogle Scholar | 28564359PubMed |
McEdward, L. R., and Miner, B. G. (2006). Estimation and interpretation of egg provisioning in marine invertebrates. Integrative and Comparative Biology 46, 224–232.
| Estimation and interpretation of egg provisioning in marine invertebrates.Crossref | GoogleScholarGoogle Scholar | 21672737PubMed |
McEdward, L. R., and Morgan, K. H. (2001). Interspecific relationships between egg size and the level of parental investment per offspring in echinoderms. The Biological Bulletin 200, 33–50.
| Interspecific relationships between egg size and the level of parental investment per offspring in echinoderms.Crossref | GoogleScholarGoogle Scholar | 11249210PubMed |
Millar, R. B., and Anderson, M. J. (2003). The kinetics of monospermic and polyspermic fertilization in free-spawning marine invertebrates. Journal of Theoretical Biology 224, 79–85.
| The kinetics of monospermic and polyspermic fertilization in free-spawning marine invertebrates.Crossref | GoogleScholarGoogle Scholar | 12900205PubMed |
Moran, A. L., and McAlister, J. S. (2009). Egg size as a life history character of marine invertebrates: is it all it’s cracked up to be? The Biological Bulletin 216, 226–242.
| Egg size as a life history character of marine invertebrates: is it all it’s cracked up to be?Crossref | GoogleScholarGoogle Scholar | 19556591PubMed |
Moran, A. L., McAlister, J. S., and Whitehill, E. A. G. (2013). Eggs as energy: revisiting the scaling of egg size and energetic content among echinoderms. The Biological Bulletin 224, 184–191.
| Eggs as energy: revisiting the scaling of egg size and energetic content among echinoderms.Crossref | GoogleScholarGoogle Scholar | 23995742PubMed |
Mousseau, T. A., and Fox, C. W. (1998). The adaptive significance of maternal effects. Trends in Ecology & Evolution 13, 403–407.
| The adaptive significance of maternal effects.Crossref | GoogleScholarGoogle Scholar |
Oliver, M., and Evans, J. P. (2014). Chemically moderated gamete preferences predict offspring fitness in a broadcast spawning invertebrate. Proceedings of the Royal Society of London – B. Biological Sciences 281, 20140148.
| Chemically moderated gamete preferences predict offspring fitness in a broadcast spawning invertebrate.Crossref | GoogleScholarGoogle Scholar |
Palumbi, S. R. (2004). Fisheries science: why mothers matter. Nature 430, 621–622.
| Fisheries science: why mothers matter.Crossref | GoogleScholarGoogle Scholar | 15295581PubMed |
Phillips, N. E. (2004). Variable timing of larval food has consequences for early juvenile performance in a marine mussel. Ecology 85, 2341–2346.
| Variable timing of larval food has consequences for early juvenile performance in a marine mussel.Crossref | GoogleScholarGoogle Scholar |
Phillips, N. E. (2007). High variability in egg size and energetic content among intertidal mussels. The Biological Bulletin 212, 12–19.
| High variability in egg size and energetic content among intertidal mussels.Crossref | GoogleScholarGoogle Scholar | 17301327PubMed |
Podolsky, R. D. (2001). Evolution of egg target size: an analysis of selection on correlated characters. Evolution 55, 2470–2478.
| Evolution of egg target size: an analysis of selection on correlated characters.Crossref | GoogleScholarGoogle Scholar | 11831662PubMed |
Podolsky, R. D. (2002). Fertilization ecology of egg coats: physical versus chemical contributions to fertilization success of free-spawned eggs. The Journal of Experimental Biology 205, 1657–1668.
| 12000810PubMed |
Podolsky, R. D. (2004). Life-history consequences of investment in free-spawned eggs and their accessory coats. American Naturalist 163, 735–753.
| Life-history consequences of investment in free-spawned eggs and their accessory coats.Crossref | GoogleScholarGoogle Scholar | 15122491PubMed |
Podolsky, R. D., and Strathmann, R. R. (1996). Evolution of egg size in free-spawners: consequences of the fertilization–fecundity trade-off. American Naturalist 148, 160–173.
| Evolution of egg size in free-spawners: consequences of the fertilization–fecundity trade-off.Crossref | GoogleScholarGoogle Scholar |
Pomin, V. H. (2015). Sulfated glycans in sea urchin fertilization. Glycoconjugate Journal 32, 9–15.
| Sulfated glycans in sea urchin fertilization.Crossref | GoogleScholarGoogle Scholar | 25636273PubMed |
Prowse, T. A. A., Sewell, M. A., and Byrne, M. (2008). Fuels for development: evolution of maternal provisioning in asterinid sea stars. Marine Biology 153, 337–349.
| Fuels for development: evolution of maternal provisioning in asterinid sea stars.Crossref | GoogleScholarGoogle Scholar |
Prowse, T. A. A., Sewell, M. A., and Byrne, M. (2017). Three-stage lipid dynamics during development of planktotrophic echinoderm larvae. Marine Ecology Progress Series 583, 149–161.
| Three-stage lipid dynamics during development of planktotrophic echinoderm larvae.Crossref | GoogleScholarGoogle Scholar |
Raff, E. C., Popodi, E. M., Sly, B. J., Turner, F. R., Villinski, J. T., and Raff, R. A. (1999). A novel ontogenetic pathway in hybrid embryos between species with different modes of development. Development 126, 1937–1945.
| 10101127PubMed |
Rothschild, L., and Swann, M. M. (1951). The fertilization reaction in the sea-urchin. The probability of a successful sperm–egg collision. The Journal of Experimental Biology 28, 403–416.
Schroeder, T. E. (1980). The jelly canal marker of polarity for sea-urchin oocytes, eggs and embryos. Experimental Cell Research 128, 490–494.
| The jelly canal marker of polarity for sea-urchin oocytes, eggs and embryos.Crossref | GoogleScholarGoogle Scholar | 7409005PubMed |
Smith, C. C., and Fretwell, S. D. (1974). Optimal balance between size and number of offspring. American Naturalist 108, 499–506.
| Optimal balance between size and number of offspring.Crossref | GoogleScholarGoogle Scholar |
Styan, C. A. (1998). Polyspermy, egg size, and the fertilization kinetics of free-spawning marine invertebrates. American Naturalist 152, 290–297.
| 18811392PubMed |
Styan, C. A., Byrne, M., and Franke, E. (2005). Evolution of egg size and fertilisation efficiency in sea stars: large eggs are not fertilised more readily than small eggs in the genus Patiriella (Echinodermata: Asteroidea). Marine Biology 147, 235–242.
| Evolution of egg size and fertilisation efficiency in sea stars: large eggs are not fertilised more readily than small eggs in the genus Patiriella (Echinodermata: Asteroidea).Crossref | GoogleScholarGoogle Scholar |
Suzuki, N. (1995). Structure, function and biosynthesis of sperm-activating peptides and fucose sulfate glycoconjugate in the extracellular coat of sea-urchin eggs. Zoological Science 12, 13–27.
| Structure, function and biosynthesis of sperm-activating peptides and fucose sulfate glycoconjugate in the extracellular coat of sea-urchin eggs.Crossref | GoogleScholarGoogle Scholar | 7795487PubMed |
Suzuki, N., and Garbers, D. L. (1984). Stimulation of sperm respiration rates by speract and resact at alkaline extracellular pH. Biology of Reproduction 30, 1167–1174.
| Stimulation of sperm respiration rates by speract and resact at alkaline extracellular pH.Crossref | GoogleScholarGoogle Scholar | 6547354PubMed |
Thomas, F. I. M., Edwards, K. A., Bolton, T. F., Zande, J. M., and Sewell, M. A. (1999). Mechanical resistance to shear stress: the role of echinoderm egg extracellular layers. The Biological Bulletin 197, 7–10.
| Mechanical resistance to shear stress: the role of echinoderm egg extracellular layers.Crossref | GoogleScholarGoogle Scholar |
Thomas, F. I. M., Bolton, T. F., and Sastry, A. M. (2001). Mechanical forces imposed on echinoid eggs during spawning: mitigation of forces by fibrous networks within egg extracellular layers. The Journal of Experimental Biology 204, 815–821.
Vance, R. R. (1973). On reproductive strategies in marine benthic invertebrates. American Naturalist 107, 339–352.
| On reproductive strategies in marine benthic invertebrates.Crossref | GoogleScholarGoogle Scholar |
Wickham, H. (2016). ‘ggplot2: Create Elegant Data Visualisations Using the Grammar of Graphics.’ (Springer-Verlag: New York, NY, USA.)
Wolfe, K., Graba-Landry, A., Dworjanyn, S. A., and Byrne, M. (2015). Larval starvation to satiation: influence of nutrient regime on the success of Acanthaster planci. PLoS One 10, e0122010.
| Larval starvation to satiation: influence of nutrient regime on the success of Acanthaster planci.Crossref | GoogleScholarGoogle Scholar | 25790074PubMed |
Yund, P. O. (2000). How severe is sperm limitation in natural populations of marine free-spawners? Trends in Ecology & Evolution 15, 10–13.
| How severe is sperm limitation in natural populations of marine free-spawners?Crossref | GoogleScholarGoogle Scholar |
