Marine Biology

, 165:155 | Cite as

Pre-hatching development in the intertidal zone negatively affects juvenile survival and physiology in the muricid gastropod Acanthina monodon

  • O. R. ChaparroEmail author
  • L. P. Salas-Yanquin
  • A. S. Matos
  • J. A. Bűchner-Miranda
  • M. W. Gray
  • V. M. Cubillos
  • J. A. Pechenik
Original paper


Encapsulated development in the intertidal environment can potentially expose developing embryos to environmental stresses, particularly during low tides. Such stresses can affect juvenile performance after hatching. Capsules-containing advanced pre-hatching stages of the snail Acanthina monodon were collected during July–August 2017 from rocks in the intertidal and subtidal environments along the coast of Valdivia, Chile (Calfuco beach, 39°79′27″S; 73°39′27″W) and brought to the laboratory, where hatching of the juveniles took place. The number of embryos per capsule in relationship to capsule size was determined for capsules from the two environments, as were the juvenile hatching size and the number of juveniles hatching from each capsule. Survival and respiratory performance were also monitored for juveniles from the two locations. Neither embryonic packaging nor the number of juveniles hatched per capsule, nor the hatching size of the juveniles evidenced any differences for capsules that were collected in the two different environments. In general, juvenile survival was low (< 10% at 4 week post-hatching) regardless of capsule origin. However, survival and standardized rates of oxygen consumption were substantially higher for juveniles from subtidal capsules. This suggests that environmental stressors had a detrimental effect on embryos from intertidal capsules.



This work was supported by the Fondo Nacional de Investigación Científica y Tecnológica-Chile (Fondecyt) through the Grant 1180643 to OC.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human/animal rights statement

All applicable national, state, and University guidelines for the care and use of animals were followed. Only invertebrates were used in this study.

Supplementary material

227_2018_3412_MOESM1_ESM.pdf (623 kb)
Supplementary material 1 (PDF 622 kb)
227_2018_3412_MOESM2_ESM.pdf (564 kb)
Supplementary material 2 (PDF 564 kb)
227_2018_3412_MOESM3_ESM.pdf (568 kb)
Supplementary material 3 (PDF 567 kb)
227_2018_3412_MOESM4_ESM.pdf (564 kb)
Supplementary material 4 (PDF 563 kb)


  1. Allen RM, Marshall DJ (2010) The larval legacy: cascading effects of recruit phenotype on post-recruitment interactions. Oikos 119:1977–1983CrossRefGoogle Scholar
  2. Bashevkin SM, Chaparro OR, Mardones-Toledo DA, Cubillos VM, Pechenik JA (2017) Growing safe: acute size escape from desiccation in juvenile Crepipatella peruviana (Mollusca: Gastropoda). Biol Bull 233:123–134CrossRefGoogle Scholar
  3. Bayne BL, Hawkins AJS, Navarro E (1987) Feeding and digestion by the mussel Mytilus edulis L. (Bivalvia: Mollusca) in mixtures of silt and algal cells at low concentrations. J Exp Mar Biol Ecol 111:1–22CrossRefGoogle Scholar
  4. Blake JA, Grassle JP, Eckelbarger KJ (2009) Capitella teleta, a new species designation for the opportunistic and experimental Capitella sp. I, with a review of the literature for confirmed records. Zoosymposia 2:25–53Google Scholar
  5. Brante A (2006) An alternative mechanism to reduce intracapsular hypoxia in ovicapsules of Fusitriton oregonensis (Gastropoda). Mar Biol 149:269–274CrossRefGoogle Scholar
  6. Brante A, Fernández M, Viard F (2008) Effect of oxygen conditions on intracapsular development in two calyptraeid species with different modes of larval development. Mar Ecol Prog Ser 368:197–207CrossRefGoogle Scholar
  7. Carriker MR, Gruber GL (1999) Uniqueness of the gastropod accessory organ (ABO): comparative biology, an update. J Shell Res 18:579–595Google Scholar
  8. Chaparro OR, Cubillos VM, Montiel YA, Paschke KA, Pechenik JA (2008) Embryonic encapsulation and maternal incubation: requirements for survival of the early stages of the estuarine gastropod Crepipatella dilatata. J Exp Mar Biol Ecol 365:38–45CrossRefGoogle Scholar
  9. Chaparro OR, Segura CJ, Osores SJA, Pechenik JA, Pardo LM, Cubillos VM (2014) Consequences of maternal isolation from salinity stress for brooded embryos and future juveniles in the estuarine direct developing gastropod Crepipatella dilatata. Mar Biol 161:619–629CrossRefGoogle Scholar
  10. Chiu JMY, Ng TYT, Wang WX, Thiyagarajan V, Qian PY (2007) Latent effects of larval food limitation on filtration rate, carbon assimilation and growth in juvenile gastropod Crepidula onyx. Mar Ecol Prog Ser 343:173–182CrossRefGoogle Scholar
  11. Diederich CM, Jarrett JN, Chaparro OR, Segura CJ, Arellano SM, Pechenik JA (2011) Low salinity stress experienced by larvae does not affect post-metamorphic growth or survival in three calyptraeid gastropods. J Exp Mar Biol Ecol 397:94–105CrossRefGoogle Scholar
  12. Dye A (1991) Food preferences of Nucella crassilabrum and juveniles of Concholepas concholepas (Gastropoda: Muricidae) from a rocky shore in southern Chile. J Molluscan Stud 57:301–307CrossRefGoogle Scholar
  13. Gallardo CS (1979) Developmental pattern and adaptations for reproduction in Nucella crassilabrum and other muricacean gastropods. Biol Bull 157:453–463CrossRefGoogle Scholar
  14. Garrido O, Gallardo CS (1993) Ultrastructure of the egg capsule of Concholepas concholepas (Brugiere, 1789) (Gastropoda: Muricidae). Rev Biol Mar Valparaiso 28:191–201Google Scholar
  15. Gosselin LA, Qian P-Y (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282CrossRefGoogle Scholar
  16. Hettinger A, Sanford E, Hill TM, Russell AD, Sato KNS, Hoey J, Forsch M, Page HN, Gaylord B (2012) Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster. Ecology 93:2758–2768CrossRefGoogle Scholar
  17. Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 55:269–301CrossRefGoogle Scholar
  18. Jenewein BT, Gosselin LA (2013) Ontogenetic shift in stress tolerance thresholds of Mytilus trossulus: effects of desiccation and heat on juvenile mortality. Mar Ecol Prog Ser 481:147–159CrossRefGoogle Scholar
  19. Lardiés MA, Fernández M (2002) Effect of oxygen availability in determining clutch size in Acanthina monodon. Mar Ecol Prog Ser 239:139–146CrossRefGoogle Scholar
  20. Moran AL (1999) Size and performance of juvenile marine invertebrates: potential contrasts between intertidal and subtidal benthic habitats. Am Zool 39:304–312CrossRefGoogle Scholar
  21. Ng TY-T, Keough MJ (2003) Delayed effects of larval exposure to Cu in the bryozoan Watersipora subtorquata. Mar Ecol Prog Ser 257:77–85CrossRefGoogle Scholar
  22. Osorio C, Atria J, Mann S (1979) Moluscos marinos de importancia económica en Chile. Biología Pesquera 11:347Google Scholar
  23. Pechenik JA (1979) The role of encapsulation in the life histories of marine invertebrates. Am Nat 114:859–870CrossRefGoogle Scholar
  24. Pechenik JA (1982) Ability of some gastropod egg capsules to protect against low-salinity stress. J Exp Mar Biol Ecol 63:195–208CrossRefGoogle Scholar
  25. Pechenik JA (2006) Larval experience and latent effects–metamorphosis is not a new beginning. Integr Comp Biol 43:323–333CrossRefGoogle Scholar
  26. Pechenik JA (2018) Latent effects: surprising consequences of embryonic and larval experience on life after metamorphosis. In: Carrier TJ, Reitzel AM, Heyland A (eds) Evolutionary ecology of marine invertebrate larvae. Oxford Universito Press, OxfordGoogle Scholar
  27. Pechenik JA, Gleason T, Daniels D, Champlin D (2001) Influence of larval exposure to salinity and cadmium stress on juvenile performance of two marine invertebrates (Capitella sp. I and Crepidula fornicata). J Exp Mar Biol Ecol 264:101–114CrossRefGoogle Scholar
  28. Pechenik JA, Jarrett J, Rooney J (2002) Relationship between larval nutritional experience, larval growth rates, and juvenile growth rates in the prosobranch gastropod Crepidula fornicata. J Exp Mar Biol Ecol 280:63–78CrossRefGoogle Scholar
  29. Pechenik JA, Chaparro OR, Pilnick A, Karp M, Acquafredda M, Burns R (2016) Effects of embryonic exposure to salinity stress or hypoxia on post-metamorphic growth and survival of the polychaete Capitella teleta. Biol Bull 231:103–112CrossRefGoogle Scholar
  30. Phillips NE (2004) Variable timing of larval food has consequences for early juvenile performance in a marine mussel. Ecology 85:2341–2346CrossRefGoogle Scholar
  31. 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
  32. Przeslawski R, Davis AR, Benkendorff K (2004) Effects of ultraviolet radiation and visible light on the development of encapsulated molluscan embryos. Mar Ecol Prog Ser 268:151–160CrossRefGoogle Scholar
  33. 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
  34. Rawlings TA (1999) Adaptations to physical stresses in the intertidal zone: the egg capsules of Neogastropod molluscs. Am Zool 39:230–243CrossRefGoogle Scholar
  35. Reid D, Osorio C (2000) The shallow-water marine Mollusca of the Estero Elefantes and Laguna San Rafael, southern Chile. Bull Nat Hist Mus Lond (Zoology) 66:109–146Google Scholar
  36. Sánchez R, Sepúlveda RD, Brante A, Cárdenas L (2011) Spatial pattern of genetic and morphological diversity in the direct developer Acanthina monodon (Gastropoda: Mollusca). Mar Ecol Prog Ser 434:121–131CrossRefGoogle Scholar
  37. Segura CJ, Chaparro OR, Paschke KA, Pechenik JA (2010) Capsule walls as barriers to oxygen availability: implications for the development of brooded embryos by the estuarine gastropod Crepipatella dilatata (Calyptraeidae). J Exp Mar Biol Ecol 390:49–57CrossRefGoogle Scholar
  38. Segura CJ, Chaparro OR, Pechenik JA, Paschke KA, Osores SJA, Navarro JM, Cubillos VM (2014) Delayed effects of severe hypoxia experienced by marine gastropod embryos. Mar Ecol Prog Ser 510:59–71CrossRefGoogle Scholar
  39. Soto RE, Castilla JC, Bozinovic F (2004) Conducta de forrajeo del gastrópodo Acanthina monodon Pallas, 1774 (Gastropoda: Muricidae) en el intermareal rocoso de Chile central. Rev Chilena Hist Nat 77:157–175Google Scholar
  40. Strathmann RR, Strathmann MF (1995) Oxygen supply and limits on aggregation of embryos. J Mar Biol Assoc UK 75:413–428CrossRefGoogle Scholar
  41. Thiyagarajan V, Pechenik JA, Gosselin LA, Qian PY (2007) Juvenile growth in barnacles: combined effect of delayed metamorphosis and sub-lethal exposure of cyprids to low-salinity stress. Mar Ecol Prog Ser 344:173–184CrossRefGoogle Scholar
  42. Windfinder (2018) Accessed Jan–Feb 2018

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • O. R. Chaparro
    • 1
    Email author
  • L. P. Salas-Yanquin
    • 1
  • A. S. Matos
    • 2
  • J. A. Bűchner-Miranda
    • 1
  • M. W. Gray
    • 3
  • V. M. Cubillos
    • 1
  • J. A. Pechenik
    • 4
  1. 1.Instituto de Ciencias Marinas y LimnológicasUniversidad Austral de ChileValdiviaChile
  2. 2.Laboratório de Invertebrados Marinhos, Departamento de Biologia, Centro de CiênciasUniversidade Federal do CearáFortalezaBrazil
  3. 3.Center for Environmental Science, Horn Point LaboratoryUniversity of MarylandCambridgeUSA
  4. 4.Biology DepartmentTufts UniversityMedfordUSA

Personalised recommendations