Marine Biology

, Volume 152, Issue 4, pp 991–1002 | Cite as

Does spawning behavior minimize exposure to environmental stressors for encapsulated gastropod embryos on rocky shores?

  • R. PrzeslawskiEmail author
  • A. R. Davis
Research Article


Adults of motile intertidal invertebrates are able to seek shelter to avoid environmental stress associated with low tides, but embryos within egg masses are effectively sessile for the duration of their encapsulation. Gastropod egg masses from 34 taxa on two rocky shores in SE Australia (34°37′08″S, 150°92′03″E and 34°35′45″S, 150°53′20″E) were surveyed over 2 years (June 2002–May 2004) to test the hypothesis that eggs are deposited in patterns that minimize exposure to environmental stress. Egg masses were expected to be predominantly deposited in shaded habitats not prone to environmental extremes. It was also anticipated that the deposition of egg masses in habitats exposed to UVR, desiccation, and/or extremes in temperature would occur when exposure to these abiotic factors was minimized. Among the taxa investigated, only four species spawned in full sun (Bembicium nanum, Nerita morio, Siphonaria zelandica and S. denticulata). Summer had the highest UVR index, water temperature, and air temperature as well as the lowest daytime tides. Univariate and multivariate analyses confirmed that egg mass abundance was highest during summer, with no change in egg mass size. This study shows that those species depositing egg masses on the surfaces of rock platforms do not adjust the seasonal timing or macrohabitat location of their spawning to avoid physiologically stressful conditions, particularly UVR. Alternate reasons for the evolution of egg mass deposition behavior in apparently sub-optimal habitats are discussed, and it is almost certainly the complex interplay of a variety of highly species-specific factors that is responsible for the patterns observed.


Rock Platform Intertidal Organism Permutational MANOVA Encapsulate Embryo Standard Erythemal Dose 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors are grateful to K. Benkendorff, B. Rudman , P. Middlefart, and D. Beechey for assistance in species identification. M. Byrne and several anonymous reviewers provided valuable comments on this manuscript. This represents contribution 279 from the Ecology and Genetics group at the University of Wollongong.


  1. Adams NL, Shick JM (2001) Mycosporine-like amino acids prevent UVB-induced abnormalities during early development of the green sea urchin Strongylocentrotus droebachiensis. Mar Biol 138:267–280CrossRefGoogle Scholar
  2. Anderson DT (1966) Further observations on the life histories of littoral gastropods in New South Wales. Proc Lin Soc NSW 90:242–251Google Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46Google Scholar
  4. Beardall J, Raven JA (2004) The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43:26–40CrossRefGoogle Scholar
  5. Beesley PL, Ross GLB, Wells A (1998) Mollusca: the southern synthesis, Part B. CSIRO Publishing, MelbourneGoogle Scholar
  6. Benkendorff K, Davis AR (2002) Identifying hotspots of molluscan species richness on rocky intertidal reefs. Biodivers Conserv 11:1959–1973CrossRefGoogle Scholar
  7. Benkendorff K, Davis AR (2004) Gastropod egg mass deposition on a temperate, wave-exposed coastline in New South Wales, Australia: implications for intertidal conservation. Aquat Conserv 14:263–280CrossRefGoogle Scholar
  8. Biermann C, Schinner G, Strathmann R (1992) Influence of solar radiation, microalgal fouling, and current on deposition site and survival of embryos of a dorid nudibranch gastropod. Mar Ecol Prog Ser 86:205–215CrossRefGoogle Scholar
  9. Carefoot TH, Harris M, Taylor BE, Donovan D, Karentz D (1998) Mycosporine-like amino acids: possible UV protection in eggs of the sea hare Aplysia dactylomela. Mar Biol 130:389–396CrossRefGoogle Scholar
  10. Carefoot TH, Karentz D, Pennings S, Young C (2000) Distribution of mycosporine-like amino acids in the sea hare Aplysia dactylomela: effects of diet on amounts and types sequestered over time in tissues and spawn. Comp Biochem Phys C 126:91–104Google Scholar
  11. Chatterjee S, Price B (2000) Regression analysis by example, 3rd edn. Wiley, New YorkGoogle Scholar
  12. Clark K, Goetzfried A (1978) Zoogeographic influences on development patterns of North Atlantic sacoglossa and nudibranchia, with a discussion of factors affecting egg size and number. J Mollus Stud 44:283–294Google Scholar
  13. Collin R (2003) Worldwide patterns in mode of development in Calyptraied gastropods. Mar Ecol Prog Ser 247:103–122CrossRefGoogle Scholar
  14. Creese RG (1980) Reproductive cycles and fecundities of two species of Siphonaria (Mollusca: Pulmonata) in South-eastern Australia. Aust J Mar Freshw Res 31:37–47CrossRefGoogle Scholar
  15. Edgar GJ (2001) Australian marine life: the plants and animals of temperate waters. New Holland Publishers, ChatswoodGoogle Scholar
  16. Eyster L (1986) The embryonic capsules of nudibranch molluscs: literature review and new studies on albumen and capsule wall ultrastructure. Am Malacol Bull 4:205–216Google Scholar
  17. Gosselin LA, Chia FS (1995) Characterizing temperate rocky shores from the perspective of an early juvenile snail: the main threats to survival of newly hatched Nucella emarginata. Mar Biol 122:625–635CrossRefGoogle Scholar
  18. Havenhand J (1993) Egg to juvenile period, generation time, and the evolution of larval type in marine invertebrates. Mar Ecol Prog Ser 97:247–260CrossRefGoogle Scholar
  19. Hoagland KE (1986) Patterns of encapsulation and brooding in the Calyptraeidae (Prosobranchia: Mesogastropoda). Am Malacol Bull 4:173–183Google Scholar
  20. Hoegh-Guldberg O, Pearse JS (1995) Temperature, food availability, and the development of marine invertebrate larvae. Am Zool 35:415–425CrossRefGoogle Scholar
  21. Hoffman JR, Hansen LJ, Klinger T (2003) Interactions between UV radiation and temperature limit inferences from single-factor experiments. J Phycol 39:268–272CrossRefGoogle Scholar
  22. Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301CrossRefGoogle Scholar
  23. Jackson GA, Strathmann RR (1981) Larval mortality from offshore mixing as a link between precompetent and competent periods of development. Am Nat 118:16–26CrossRefGoogle Scholar
  24. Kasugai T, Ikeda Y (2003) Description of the egg mass of the pygmy cuttlefish, Idiosepius paradoxus (Cephalopoda: Idiosepiidae), with special reference to its multiple gelatinous layers. Veliger 46:105–110Google Scholar
  25. Laxton JH (1969) Reproduction in some New Zealand Cymatiidae (Gastropoda: Prosobranchia). Zool J Linn Soc Lond 48:237–253CrossRefGoogle Scholar
  26. Loch I (1989) Some light on dark Mitres. Aust Shell News 65:4–5Google Scholar
  27. Mileikovsky SA (1970) Seasonal and daily dynamics of pelagic larvae of marine shelf bottom invertebrates in nearshore waters of Kankalaksha Bay (White Sea). Mar Biol 5:180–194CrossRefGoogle Scholar
  28. Moran AL (1999) Size and performance of juvenile marine invertebrates: potential contrasts between intertidal and subtidal benthic habitats. Am Zool 39:304–312CrossRefGoogle Scholar
  29. Newell RC (1970) Biology of intertidal animals. American Elsevier Publishing, New YorkGoogle Scholar
  30. Ocana TMJ, Emson RH (1999) Maturation, spawning and development in Siphonaria pectinata linnaeus (Gastropoda: Pulmonata) at Gibraltar. J Moll Stud 65:185–193CrossRefGoogle Scholar
  31. Palmer AR (1994) Temperature sensitivity, rate of development, and time to maturity: geographic variation in laboratory-reared Nucella and a cross-phyletic overview. In: Wilson Jr WH, Stricker SA, Shinn GL (eds) Reproduction and development of marine invertebrates. Johns Hopkins University Press, Baltimore, pp 177–194Google Scholar
  32. Pechenik J (1978) Adaptation to intertidal development: studies on Nassarius obsoletus. Biol Bull 154:282–291CrossRefGoogle Scholar
  33. Pechenik J (1979) Role of encapsulation in invertebrate life histories. Am Nat 114:870CrossRefGoogle Scholar
  34. Pechenik J (1982) Ability of some gastropod egg capsules to protect against low-salinity stress. J Exp Mar Biol Ecol 3:195–208CrossRefGoogle Scholar
  35. Pechenik J, Marsden ID, Pechenik O (2003) Effects of temperature, salinity, and air exposure on development of the estuarine pulmonate gastropod Amphibola crenata. J Exp Mar Biol Ecol 292:159–176CrossRefGoogle Scholar
  36. Pilkington M (1974) The eggs and hatching of some New Zealand Prosobranch molluscs. J R Soc N Z 4:411–431CrossRefGoogle Scholar
  37. Podolsky RD (2003) Integrating development and environment to model reproductive performance in natural populations of an intertidal gastropod. Integr Comp Biol 43:450–458CrossRefGoogle Scholar
  38. Podolsky RD, Hoffmann GE (1998) Embryo development during tide-related thermal stress: evidence of a protective role for heat-shock proteins. Am Nat 38:186Google Scholar
  39. Przeslawski R (2004) A review of the effects of environmental stress on embryonic development within intertidal gastropod egg masses. Moll Res 24:43–63CrossRefGoogle Scholar
  40. Przeslawski R (2005) Combined effects of solar radiation and desiccation on the mortality and development of encapsulated embryos of rocky shore gastropods. Mar Ecol Prog Ser 298:169–177CrossRefGoogle Scholar
  41. Przeslawski R, Benkendorff K (2005) The role of surface fouling in the development of encapsulated gastropod embryos. J Moll Stud 71:75–83CrossRefGoogle Scholar
  42. Przeslawski R, Benkendorff K, Davis AR (2005a) A quantitative survey of mycosporine-like amino acids (MAAs) in intertidal egg masses from temperate rocky shores. J Chem Ecol 31:2417–2438CrossRefGoogle Scholar
  43. Przeslawski R, Davis AR, Benkendorff K (2005b) Synergies, climate change and the development of rocky shore invertebrates. Glob Change Biol 11:515–522CrossRefGoogle Scholar
  44. Rawlings TA (1996) Shields against ultraviolet radiation: an additional protective role for the egg capsules of benthic marine gastropods. Mar Ecol Prog Ser 136:81–95CrossRefGoogle Scholar
  45. Rawlings TA (1999) Adaptations to physical stresses in the intertidal zone: the egg capsules of neogastropod molluscs. Am Zool 39:240–243CrossRefGoogle Scholar
  46. Rose RA (1985a) The spawn and development of 29 NSW Opisthobranchs (Mollusca: Gastropoda). Proc Linn Soc NSW 108:23–36Google Scholar
  47. Rose RA (1985b) The spawn and embryonic development of colour variants of Dendrodoris nigra Stimpson (Mollusca: Nudibranchia). J Malacol Soc Aust 7:75–88Google Scholar
  48. Rose RA (1986) Direct development in Rostanga arbutus (Angas) (Mollusca: Nudibranchia) and the effects of temperature and salinity on embryos reared in the laboratory. J Malacol Soc Aust 7:141–154Google Scholar
  49. Rudman WB (2007) Sea slug forum. Australian museum. (accessed 17 May 2007)Google Scholar
  50. Sanford E (2002) The feeding, growth, and energetics of two rocky intertidal predators (Pisaster ochraceus and Nucella canaliculata) under water temperatures simulating episodic upwelling. J Exp Mar Biol Ecol 273:199–218CrossRefGoogle Scholar
  51. Smith B, Black JH, Sheperd SA (1989) Molluscan egg masses and capsules. In: Shepherd SA, Thomas IM (eds) Marine invertebrates of southern Australia, part 2. Southern Australia Government Printing Division, Adelaide, pp 841–891Google Scholar
  52. Smith BJ (1972) Don’t kill the young. Survival 2:86–87Google Scholar
  53. Sorte CJB, Hoffman GE (2005) Thermotolerance and heat-shock protein expression in Northeastern Pacific Nucella species with different biogeographic ranges. Mar Biol 146:985–993CrossRefGoogle Scholar
  54. Spight TM (1977) Do intertidal snails spawn in the right places? Evolution 31:682–691CrossRefGoogle Scholar
  55. Switzer-Dunlap M, Hadfield MG (1977) Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda: Opisthobranchia) in laboratory culture. J Exp Mar Biol Ecol 29:245–261CrossRefGoogle Scholar
  56. Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45CrossRefGoogle Scholar
  57. Underwood AJ (1979) The ecology of intertidal gastropods. Adv Mar Biol 16:111–210CrossRefGoogle Scholar
  58. Ushakova O (2003) Combined effect of salinity and temperature on Spirorbis spirorbis L. and Circeus spirillum L. larvae from the White Sea. J Exp Mar Biol Ecol 296:23–33CrossRefGoogle Scholar
  59. Ventura CRR, Falcao APC, Santos JS, Fiori CS (1997) Reproductive cycle and feeding periodicity in the starfish Astropecten brasiliensis in the Cabo Frio upwelling ecosystem (Brazil). Invertebr Reprod Dev 31:135–141CrossRefGoogle Scholar
  60. Waters JM, King TM, O’Loughlin PM, Spencer HG (2005) Phylogeographical disjunction in abundant high-dispersal littoral gastropods. Mol Ecol 14:483–494CrossRefGoogle Scholar
  61. Woods HA, DeSilets RJ (1997) Egg-mass gel of Melanochlamys diomedea (Bergh) protects embryos from low salinity. Biol Bull 193:341–349CrossRefGoogle Scholar
  62. Wraith J, Przeslawski R, Davis AR (2006) UV-induced mortality in encapsulated intertidal embryos: are MAAs an effective sunscreen? J Chem Ecol 32:993–1004CrossRefGoogle Scholar
  63. Yamahira K (1996) The role of intertidal egg deposition on survival of the puffer, Takifugu niphobles (Jordan et Snyder), embryos. J Exp Mar Biol Ecol 98:291–306CrossRefGoogle Scholar
  64. Yaroslavtseva LM, Sergeeva EP, Kulikova VA (2001) The effectiveness of the protection of embryos and larvae within egg masses of the gastropod Epheria turrita against changes in salinity and desiccation. Russ J Mar Biol 27:8–13CrossRefGoogle Scholar
  65. Zar JH (1998) Biostatistical analysis. Prentice Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Institute for Conservation Biology, School of Biological SciencesUniversity of WollongongWollongongAustralia
  2. 2.Department of Ecology and EvolutionStony Brook UniversityStony BrookUSA

Personalised recommendations