Skip to main content
Log in

Post-metamorphic impact of brief hyposaline stress on recently hatched veligers of the gastropod Crepipatella peruviana (Calyptraeidae)

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Intertidal environments experience low salinity during heavy rainfall, creating stressful conditions for organisms, including invertebrate pelagic larvae, which can affect post-metamorphic development. Salinity in tide pools was monitored at low tide during a rainfall event in November 2013 at Puerto Montt, southern Chile. Water samples were taken to identify the presence and size of veligers of the gastropod Crepipatella peruviana. In addition, newly hatched veligers were exposed to different salinities [32 (control), 25, 20, and 15] in the laboratory for 6 h and then cultured at the control salinity until metamorphosis. Shell length (SL), oxygen consumption (OCR) and clearance (CR) rates of juveniles, and survival and growth in the first 2 weeks post-metamorphosis were quantified. The salinity of tide pools decreased to ten during heavy rains and yet contained an abundance of living veliger larvae; more than 85 % of the C. peruviana veligers collected had a SL ≤400 µm, which implies that they had only recently hatched. Exposing early veligers to low salinities (15 and 20) decreased size at metamorphosis and early juvenile survival by approximately 10 and 20 %, respectively. Also, the CR was lower at 5 days post-metamorphosis, decreasing by 30 % in individuals that had been exposed to salinity 15 as larvae. However, the OCR (5 and 15 days post-metamorphosis) and CR (15 days post-metamorphosis) were not different from the control treatment with an average value of 1.7 (×10−2 mg O2 h−1 juv−1) and 0.07 (L h−1 juv−1) for OCR and CR at 15 days post-metamorphosis, respectively. Also there was no effect on juvenile growth rate. This study shows that short hyposaline events suffered by early veligers of C. peruviana can cause reduced size at metamorphosis and potentially reduce juvenile survival, factors that could affect the fitness of future adult populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen BJ, Rodgers B, Tuan Y, Levinton JS (2012) Size-dependent temperature and desiccation constraints on performance capacity: implications for sexual selection in a fiddler crab. J Exp Mar Biol Ecol 438:93–99

    Article  Google Scholar 

  • Amado EM, Vilodin D, Freire CA, Souza MM (2011) Distinct patterns of water and osmolyte control between intertidal (Bunodosoma caissarum) and subtidal (Anemonia sargassensis) sea anemones. Comp Biochem Physiol 158(A):542–551

    Article  Google Scholar 

  • Anger K (2006) Contributions of larval biology to crustacean research: a review. Invert Reprod Dev 49:175–205

    Article  Google Scholar 

  • Barria A, Gebauer P, Molinet C (2012) Variabilidad espacial y temporal del suministro larval de mitílidos en el Seno del Reloncaví, sur de Chile. Rev Biol Mar Oceanog 47:461–473

    Article  Google Scholar 

  • Bashevkin S, Pechenik JP (2015) The interactive influence of temperature and salinity on larval and juvenile growth in the gastropod Crepidula fornicata (L.). J Exp Mar Biol Ecol 470:78–91

    Article  CAS  Google Scholar 

  • 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 111:1–22

    Article  Google Scholar 

  • Berger VJ, Kharazova AD (1997) Mechanisms of salinity adaptations in marine molluscs. Hydrobiologia 355:115–126

    Article  CAS  Google Scholar 

  • Bodinier C, Boulo V, Lorin-Nebel C, Charmantier G (2009) Influence of salinity on the localization and expression of the CFTR chloride channel in the ionocytes of Dicentrarchus labrax during ontogeny. J Anat 214:318–329

    Article  CAS  Google Scholar 

  • Cebrian E, Uriz MJ (2007) Contrasting effects of heavy metals and hydrocarbons on larval settlement and juvenile survival in sponges. Aquat Toxicol 81:137–143

    Article  CAS  Google Scholar 

  • Chaparro OR, Charpentier JL, Collin R (2002) Embryonic velar structure and function of two sibling species of Crepidula with different modes of development. Biol Bull 203:80–86

    Article  CAS  Google Scholar 

  • Chaparro OR, Saldivia CL, Pereda SV, Segura CJ, Montiel YA, Collin R (2005) The reproductive cycle and development of Crepidula fecunda (Gastropoda: Calyptraeidae) from southern Chile. J Mar Biol Assoc UK 85:157–161

    Article  Google Scholar 

  • 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 161:619–629

    Article  Google Scholar 

  • 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 343:173–182

    Article  CAS  Google Scholar 

  • Chiu JMY, Wang H, Thiyagarajan V, Qian PY (2008) Differential timing of larval starvation effects on filtration rate and growth in juvenile Crepidula onyx. Mar Biol 154:91–98

    Article  CAS  Google Scholar 

  • Choi HJ, Ji J, Chung K-H, Ahn I-Y (2007) Cadmium bioaccumulation and detoxification in the gill and digestive gland of the Antarctic bivalve Laternula elliptica. Comp Biochem Physiol C 145:227–235

    Google Scholar 

  • Collin R (2003) Worldwide patterns in mode of development in calyptraeid gastropods. Mar Ecol Prog Ser 247:103–122

    Article  Google Scholar 

  • Coughlan J (1969) The estimation of filtering rate from the clearance suspensions. Mar Biol 2:356–358

    Article  Google Scholar 

  • 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 397:94–105

    Article  CAS  Google Scholar 

  • Gallardo CS (1979) Especies gemelas del género Crepidula (Gastropoda, Calyptraeidae) en la costa de Chile; una redescripción de C. dilatata Lamarck y descripción de C. fecunda n. sp. Stud Neotrop Fauna Environ 14:215–226

    Article  Google Scholar 

  • Gallardo CS, Penchaszadeh PE (2001) Hatching mode and latitude in marine gastropods: revisiting Thorson’s paradigm in the Southern hemisphere. Mar Biol 138:547–552

    Article  Google Scholar 

  • Gebauer P, Paschke K, Anger K (1999) Costs of delayed metamorphosis: reduced growth and survival in early juveniles of an estuarine grapsid crab, Chasmagnathus granulata. J Exp Mar Biol Ecol 59:133–143

    Google Scholar 

  • Gebauer P, Paschke K, Anger K (2003) Delayed metamorphosis in decapod crustaceans, evidence and consequences. Rev Chil Hist Nat 76:169–175

    Article  Google Scholar 

  • Génio L, Sousa A, Vaz N, Dias JM, Barroso C (2008) Effect of low salinity on the survival of recently hatched veligers of Nassarius reticulatus (L.) in estuarine habitats: a case study of Ria de Aveiro. J Sea Res 59:133–143

    Article  Google Scholar 

  • Giménez L (2002) Effects of prehatching salinity and initial larval biomass on survival and duration of development in the zoea 1 of the estuarine crab, Chasmagnathus granulata, under nutritional stress. J Exp Mar Biol Ecol 270:93–110

    Article  Google Scholar 

  • Giménez L (2006) Phenotypic links in complex life cycles: conclusions from studies with decapod crustaceans. Integr Comp Biol 46:615–622

    Article  Google Scholar 

  • Goodman RM (2008) Latent effects of egg incubation temperature on growth in the lizard Anolis carolinensis. J Exp Zool 309A:525–533

    Article  Google Scholar 

  • Gosselin LA, Qian P-Y (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282

    Article  Google Scholar 

  • Handy RD (1994) Intermittent exposure to aquatic pollutants: assessment, toxicity and sublethal responses in fish and invertebrates. Comp Biochem Physiol C 107:171–184

    Article  Google Scholar 

  • Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301

    Article  Google Scholar 

  • Iriarte JL, González HE, Liu KK, Rivas C, Valenzuela C (2007) Spatial and temporal variability of chlorophyll and primary productivity in surface waters of southern Chile (41.5–43°S). Estuar Coast Shelf Sci 74:471–480

    Article  Google Scholar 

  • Kemp JOG (2009) Effects of temperature and salinity on resting metabolism in two South African rock pool fish: the resident gobiid Caffrogobius caffer and the transient sparid Diplodus sargus capensis. Afr Zool 44:151–158

    Article  Google Scholar 

  • Li A, Chiu JMY (2013) Latent effects of hypoxia on the gastropod Crepidula onyx. Mar Ecol Prog Ser 480:145–154

    Article  Google Scholar 

  • Maldonado M, Young CM (1999) Effects of the duration of larval life on postlarval stages of the demosponge Sigmadocia caerulea. J Exp Mar Biol Ecol 232:9–21

    Article  Google Scholar 

  • Mann R, Campos BM, Luckenbach MW (1991) Swimming rate and responses of larvae of three mactrid bivalves to salinity discontinuities. Mar Ecol Prog Ser 68:257–269

    Article  Google Scholar 

  • Mardones ML, Chaparro OR, Pechenik JA, Segura CJ, Osores SJA (2013) Embryonic brooding in Crepipatella fecunda: implications for processes related to maternal feeding. J Exp Mar Biol Ecol 443:141–146

    Article  Google Scholar 

  • Marshall DJ, Pechenik JA, Keough MJ (2003) Larval activity and delayed metamorphosis affect post-larval performance in the colonial ascidian Diplosoma listerianum. Mar Ecol Prog Ser 246:153–162

    Article  Google Scholar 

  • Montiel YA, Chaparro OR, Segura CJ (2005) Changes in feeding mechanisms during early ontogeny in juveniles of Crepipatella fecunda (Gastropoda, Calyptraeidae). Mar Biol 147:1333–1342

    Article  Google Scholar 

  • Montory JA, Chaparro OR, Pechenik JA, Diederich CM, Cubillos VM (2014a) Impact of short-term salinity stress on larval development of the marine gastropod Crepipatella fecunda (Calyptraeidae). J Exp Mar Biol Ecol 458:39–45

    Article  CAS  Google Scholar 

  • Montory JA, Pechenik JA, Diederich CM, Chaparro OR (2014b) Effects of low salinity on adult behavior and larval performance in the intertidal gastropod Crepipatella peruviana (Calyptraeidae). PLoS ONE 9:e103820

    Article  Google Scholar 

  • Navarro JM, Chaparro OR (2002) Grazing–filtration as feeding mechanisms in motile specimens of Crepidula fecunda (Gastropoda: Calyptraeidae). J Exp Mar Biol Ecol 270:111–122

    Article  Google Scholar 

  • Onitsuka T, Kawamaru T, Ohashi S, Iwanaga S, Horii T, Watanabe Y (2010) Effects of delayed metamorphosis and delayed post-settlement feeding on post-larval survival and growth of the abalone Haliotis diversicolor. Aquaculture 298:239–244

    Article  Google Scholar 

  • Pechenik JA (1980) Growth and energy balance during the larval lives of three prosobranch gastropods. J Exp Mar Biol Ecol 44:1–28

    Article  CAS  Google Scholar 

  • Pechenik JA (1984) The relationship between temperature, growth rate, and duration of planktonic life for larvae of the gastropod Crepidula fornicata (L.). J Exp Mar Biol Ecol 74:241–257

    Article  Google Scholar 

  • Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46:323–333

    Article  Google Scholar 

  • Pechenik JA, Hammer K, Weise C (1996) The effect of starvation on acquisition of competence and postmetamorphic performance in the marine prosobranch gastropod Crepidula fornicata (L.). J Exp Mar Biol Ecol 199:137–152

    Article  Google Scholar 

  • Pechenik JA, Wendt DE, Jarrett JN (1998) Metamorphosis is not a new beginning. Bioscience 48:901–910

    Article  Google Scholar 

  • 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 264:101–114

    Article  CAS  Google Scholar 

  • Pechenik JA, Jarrett JN, Rooney J (2002) Relationships between larval nutritional experience, larval growth rates, juvenile growth rates, and juvenile feeding rates in the prosobranch gastropod Crepidula fornicata. J Exp Mar Biol Ecol 280:63–78

    Article  Google Scholar 

  • Phillips NE (2002) Effects of nutrition-mediated larval condition on juvenile performance in a marine mussel. Ecology 83:2562–2574

    Article  Google Scholar 

  • Phillips NE (2004) Variable timing of larval food has consequences for early juvenile performance in a marine mussel. Ecology 85:2341–2346

    Article  Google Scholar 

  • Qian P-Y, Pechenik JA (1998) Effects of larval starvation and delayed metamorphosis on juvenile survival and growth of the tube-dwelling polychaete Hydroides elegans (Haswell). J Exp Mar Biol Ecol 227:169–185

    Article  Google Scholar 

  • Qiu JW, Qian PY (1999) Tolerance of the barnacle Balanus amphitrite amphitrite to salinity and temperature stress: effects of previous experience. Mar Ecol Prog Ser 188:123–132

    Article  Google Scholar 

  • Raftopoulou EK, Dimitriadis VK (2011) Comparative study of the accumulation and detoxification of Cu (essential metal) and Hg (nonessential metal) in the digestive gland and gills of mussels Mytilus galloprovincialis, using analytical and histochemical techniques. Chemosphere 83:1155–1165

    Article  CAS  Google Scholar 

  • Relyea RA, Hoverman JT (2003) The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134:596–604

    Article  Google Scholar 

  • Rivest BR (1983) Development and the influence of nurse egg allotment on hatching size in Searlesia dira (Reeve, 1846) (Prosobranchia: Buccinidae). J Exp Mar Biol Ecol 69:217–241

    Article  Google Scholar 

  • Rodhes-Ondi SE, Turner RL (2010) Salinity tolerance and osmotic response of the estuarine hermit crab Pagurus maclaughlinae in the Indian River Lagoon, Florida. Estuar Coast Shelf Sci 86:189–196

    Article  Google Scholar 

  • Roller RA, Stickle WB (1985) Effects of salinity on larval tolerance and early developmental rates of four species of echinoderms. Can J Zool 63:1531–1538

    Article  Google Scholar 

  • Sameoto JA, Metaxas A (2008) Can salinity-induced mortality explain larval vertical distribution with respect to a halocline? Biol Bull 214:329–338

    Article  Google Scholar 

  • 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 510:59–71

    Article  CAS  Google Scholar 

  • Simith DJB, Diele K, Abrunhosa FA (2013) Carry-over effects of delayed larval metamorphosis on early juvenile performance in the mangrove crab Ucides cordatus (Ucididae). J Exp Mar Biol Ecol 440:61–68

    Article  Google Scholar 

  • Spicer JI, Strömberg J-O (2003) Metabolic responses to low salinity of the shipworm Teredo navalis (L.). Sarsia 88:302–305

    Article  Google Scholar 

  • Spight TM (1976) Ecology of hatching size for marine snails. Oecologia (Berl) 24:283–294

    Article  Google Scholar 

  • Stickle WB, Denoux GJ (1976) Effects of in situ tidal salinity fluctuations on osmotic and ionic composition of body fluid in Southeastern Alaska rocky intertidal fauna. Mar Biol 37:125–135

    Article  CAS  Google Scholar 

  • Thiyagarajan V, Qian PY (2003) Effect of temperature, salinity and delayed attachment on development of the solitary ascidian Styela plicata (Lesueur). J Exp Mar Biol Ecol 290:133–146

    Article  Google Scholar 

  • Thiyagarajan V, Pechenik J, Gosselin LA, Qian PY (2007) Juvenile growth in barnacles: combined effects of delayed metamorphosis and sub-lethal exposure of cyprids to low-salinity stress. Mar Ecol Prog Ser 344:173–184

    Article  Google Scholar 

  • Torres G, Anger K, Giménez L (2006) Effects of reduced salinities on metamorphosis of a freshwater-tolerant sesarmid crab, Armases roberti: is upstream migration in the megalopa stage constrained by increasing osmotic stress? J Exp Mar Biol Ecol 338:134–139

    Article  CAS  Google Scholar 

  • Underwood AJ (1979) The ecology of intertidal gastropods. Adv Mar Biol 16:111–210

    Article  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology. Their logical design and interpretation using analysis of variance, 1st edn. Cambridge University Press, Sydney

    Google Scholar 

  • Wendt DE (1996) Effect of larval swimming duration on success of metamorphosis and size of the ancestrular lophophore in Bugula neritina (Bryozoa). Biol Bull 191:224–233

    Article  Google Scholar 

  • Zimmerman KM, Pechenik JA (1991) How do temperature and salinity affect relative rates of growth, morphological differentiation, and time to metamorphic competence in larvae of the marine gastropod Crepidula plana? Biol Bull 180:372–386

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Comision Nacional de Investigación Científica y Tecnológica (CONICYT-Chile) for the Doctoral Fellowship 24121345 given to JAM and Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT-Chile) Grant 1141052 to ORC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jaime A. Montory.

Additional information

Responsible Editor: J. Grassle.

Reviewed by undisclosed experts.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Montory, J.A., Chaparro, O.R., Navarro, J.M. et al. Post-metamorphic impact of brief hyposaline stress on recently hatched veligers of the gastropod Crepipatella peruviana (Calyptraeidae). Mar Biol 163, 7 (2016). https://doi.org/10.1007/s00227-015-2791-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-015-2791-9

Keywords

Navigation