Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-31T15:57:20.122Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of age, salinity and temperature on the metamorphosis and survival of Capitulum mitella cyprids (Cirripedia: Thoracica: Scalpellomorpha)

Published online by Cambridge University Press:  14 January 2020

Xiaozhen Rao Open the ORCID record for Xiaozhen Rao [Opens in a new window]  and
Gang Lin
Xiaozhen Rao*
Affiliation:
College of Life Sciences, Southern Institute of Oceanography, Fujian Normal University, Fuzhou350117, China
Gang Lin
Affiliation:
College of Life Sciences, Southern Institute of Oceanography, Fujian Normal University, Fuzhou350117, China
*
Author for correspondence: X. Rao, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Capitulum mitella is a tropical/sub-tropical intertidal barnacle of high economic value. However, no studies have yet focused on the effects of the extrinsic and intrinsic factors that affect the metamorphosis of this species. The current study stored cyprids at room temperature (24–26°C) and low temperature (7°C) and then compared the effects of age and storage temperature on cyprid metamorphosis. The effects of salinity and temperature on cyprid metamorphosis and survival were examined. Results showed the following. (1) Young 0-day cyprids were not competent to metamorphose, and C. mitella cyprids had a pre-competent phase. (2) The cyprid metamorphosis percentage at different storage temperatures with the same age was higher at room temperature than at 7°C. Low temperature storage of cyprids appeared to be unsuitable for C. mitella. The ideal storage time at room temperature for cyprids was 3–5 days. (3) The cyprids could complete metamorphosis at a salinity range of 20–45 mg l−1, and the optimum salinity range for metamorphosis was 25–35 mg l−1. At 15 mg l−1 salinity, the cyprids could survive but failed to metamorphose. (4) The cyprids could survive and complete metamorphosis at 18–36°C, and the optimum temperature range for metamorphosis was 21–33°C. The metamorphosis of C. mitella cyprids can tolerate a wide spectrum of salinity and temperature, which is related to the distribution location, habitat environment and lifestyle. Results of this study may provide a basis for the settlement biology, recruitment ecology and aquaculture of this species.

Keywords

AgeCapitulum mitellacypridmetamorphosissalinitytemperature
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 1 , February 2020 , pp. 55 - 62
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aldred, N and Clare, AS (2008) The adhesive strategies of cyprids and development of barnacle-resistant marine coatings. Biofouling 24, 351–363.CrossRefGoogle ScholarPubMed
Aldred, N, Alsaab, A and Clare, AS (2018) Quantitative analysis of the complete larval settlement process confirms Crisp's model of surface selectivity by barnacles. Proceedings of the Royal Society B–Biological Science 285, 20171957.CrossRefGoogle ScholarPubMed
Anil, AC and Khandeparkar, RDS (1998) Influence of bacterial exopolymers, conspecific adult extract and salinity on cyprid metamorphosis of Balanus amphitrite (Cirripedia: Thoracica). Marine Ecology 19, 279–292.CrossRefGoogle Scholar
Anil, AC, Desai, D and Khandeparker, L (2000) Larval development and metamorphosis in Balanus amphitrite Darwin (Cirripedia: Thoracica): significance of food concentration, temperature and nucleic acids. Journal of Experimental Marine Biology and Ecology 263, 125–141.CrossRefGoogle Scholar
Anil, AC, Desai, D and Khandeparkar, L (2001) Larval development and metamorphosis in Balanus amphitrite Darwin (Cirripedia: Thoracica): significance of food concentration, temperature and nucleic acids. Journal of Experimental Marine Biology and Ecology 263, 125–141.CrossRefGoogle Scholar
Anil, AC, Khandeparker, L, Desai, DV, Baragi, LV and Gaonkar, CA (2010) Larval development, sensory mechanisms and physiological adaptations in acorn barnacles with special reference to Balanus amphitrite. Journal of Experimental Marine Biology and Ecology 392, 89–98.CrossRefGoogle Scholar
Barnes, M (1996) Pedunculate cirripedes of the genus Pollicipes. Oceanography and Marine Biology: An Annual Review 34, 303–394.Google Scholar
Clare, AS and Matsumura, K (2000) Nature and perception of barnacle settlement pheromones. Biofouling 15, 57–71.CrossRefGoogle ScholarPubMed
Clare, AS, Freet, RK and McClary, MJ (1994) On the antennular secretion of the cyprid of Balanus amphitrite amphitrite, and its role as a settlement pheromone. Journal of the Marine Biological Association of the United Kingdom 74, 243–250.CrossRefGoogle Scholar
Clare, AS, Thomas, RF and Rittschof, D (1995) Evidence for the involvement of cyclic AMP in the pheromonal modulation of barnacle settlement. Journal of Experimental Biology 198, 655–664.Google ScholarPubMed
Cruz, T, Castro, JJ and Hawkins, SJ (2010) Recruitment, growth and population size structure of Pollicipes pollicipes in SW Portugal. Journal of Experimental Biology 392, 200–209.CrossRefGoogle Scholar
Dineen, JF and Hines, AH (1992) Interactive effects of salinity and adult extract upon settlement of the estuarine barnacle Balanus improvisus. Journal of Experimental Marine Biology and Ecology 156, 239–252.CrossRefGoogle Scholar
Dineen, JF and Hines, AH (1994) Larval settlement of the polyhaline barnacle Balanus eburneus (Gould): cue interactions and comparisons with two estuarine congeners. Journal of Experimental Marine Biology and Ecology 179, 223–234.CrossRefGoogle Scholar
Dreyer, N, Olesen, J, Dahl, RB, Chan, BKK and Høeg, JT (2018) Sex-specific metamorphosis of cypris larvae in the androdioecious barnacle Scalpellum scalpellum (Crustacea: Cirripedia: Thoracica) and its implications for the adaptive evolution of dwarf males. PLoS ONE 13, e0191963–e0191982.CrossRefGoogle ScholarPubMed
Franco, SC, Aldred, N, Cruz, T and Clare, AS (2016) Modulation of gregarious settlement of stalked barnacle, Pollicipes pollicipes: a laboratory study. Scientia Marina 80, 217–228.CrossRefGoogle Scholar
Franco, SC, Aldred, N, Cruz, T and Clare, AS (2017) Effects of culture conditions on larval growth and survival of stalked barnacles (Pollicipes pollicipes). Aquaculture Research 48, 2920–2933.CrossRefGoogle Scholar
Fraschetti, S, Giangrande, A, Terlizzi, A and Boero, F (2003) Pre and post-settlement events in benthic community dynamics. Oceanologica Acta 25, 285–295.CrossRefGoogle Scholar
Hadfield, MG (1986) Settlement and recruitment of marine invertebrates: a perspective and some proposals. Bulletin of Marine Science 39, 418–425.Google Scholar
Hadfeld, MG, Carpizo-Ituarte, E, del Carmen, K and Nedved, BT (2001) Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. American Zoologist 41, 1123–1131.Google Scholar
Harder, T, Thiyagarajan, V and Qian, PY (2001a) Effect of cyprid age on the settlement of Balanus amphitrite Darwin in response to natural biofilms. Biofouling 17, 211–219.CrossRefGoogle Scholar
Harder, T, Thiyagarajan, V and Qian, PY (2001b) Combined effect of cyprid age and lipid content on larval settlement and metamorphosis of Balanus amphitrite Darwin. Biofouling 17, 257–262.CrossRefGoogle Scholar
Head, RM, Berntsson, KM, Dahlström, M, Overbeke, K and Thomason, JC (2004) Gregarious settlement in cypris larvae: the effects of cyprid age and assay duration. Biofouling 20, 123–128.CrossRefGoogle ScholarPubMed
Hodin, J, Ferner, MC, Ng, G, Lowe, CJ and Gaylord, B (2015) Rethinking competence in marine life cycles: ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence. Royal Society Open Science 2, 150114–150130.CrossRefGoogle Scholar
Høeg, JT, Maruzzo, D, Okano, K, Glenner, H and Chan, BKK (2012) Metamorphosis in balanomorphan, pedunculated and parasitic barnacles: a video based analysis. Integrative and Comparative Biology 52(3), 337–347.CrossRefGoogle ScholarPubMed
Khandeparker, L, Anil, AC and Raghukumar, S (2002) Exploration and metamorphosis in Balanus amphitrite Darwin (Cirripedia: Thoracica) cyprids: significance of sugars and adult extract. Journal of Experimental Marine Biology and Ecology 281, 77–88.CrossRefGoogle Scholar
Kitamura, H and Nakashima, Y (1996) Influence of storage temperatures and period on settlement rate and substrate discrimination in cyprids of the barnacle Balanus amphitrite. Fisheries Sciences 62, 998–999.CrossRefGoogle Scholar
Kon-Ya, K and Miki, W (1994) Effects of environmental-factors on larval settlement of the barnacle Balanus amphitrite reared in the laboratory. Fisheries Science 60, 563–565.CrossRefGoogle Scholar
Kugele, M and Yule, AB (1996) The larval morphology of Pollicipes pollicipes (Gmelin 1970) (Cirripedia: Lepadomorpha) with notes on cyprid settlement. Scientia Marina 60, 469–480.Google Scholar
Lagersson, N and Høeg, JT (2002) Settlement behaviour and antennulary biomechanics in cypris larvae of Balanus amphitrite (Crustacea: Thecostraca: Cirripedia). Marine Biology 141, 513–526.Google Scholar
Lee, C, Shim, JM and Kim, CH (2000) Larval development of Capitulum mitella (Cirripedia: Pedunculata) reared in the laboratory. Journal of the Marine Biological Association of the United Kingdom 80, 457–464.CrossRefGoogle Scholar
Lin, G and Rao, X (2017) Metamorphosis of the pedunculate barnacle Capitulum mitella Linnaeus, 1758 (Cirripedia: Scalpelliformes). Journal of the Marine Biological Association of the United Kingdom 97, 1643–1650.CrossRefGoogle Scholar
Lin, G, Qiu, W and Qi, Q (1994) Breeding, settlement and growth of Pollicipes mitella in Fujian coastal area. Acta Oceanologica Sinica 16, 108–115.Google Scholar
Lin, G, Xu, Y, Rao, X and Cheng, M (2002) The effects of salinity on embryonic and larval development of Pollicipes mitella in vitro. Journal of Fujian Normal University Natural Sciences 18, 76–78.Google Scholar
Lucas, MI, Walker, G, Holiand, DL and Crisp, DJ (1979) An energy budget for the free swimming and metamorphosing larvae of Balanus balanoides (Crustacea: Cirripedia). Marine Biology 55, 221–229.CrossRefGoogle Scholar
Maréchal, JP and Hellio, C (2011) Antifouling activity against barnacle cypris larvae: do target species matter (Amphibalanus amphitrite vs Semibalanus balanoides)? International Biodeterioration & Biodegradation 65, 92–101.CrossRefGoogle Scholar
Maréchal, JP, Matsumura, K, Conlan, S and Hellio, C (2012) Competence and discrimination during cyprid settlement in Amphibalanus amphitrite. International Biodeterioration & Biodegradation 72, 59–66.CrossRefGoogle Scholar
Maruzzo, D, Aldred, N, Clare, AS and Høeg, JT (2012) Metamorphosis in the Cirripede crustacean Balanus amphitrite. PLoS ONE 7, e37408–e37415.CrossRefGoogle ScholarPubMed
Matsumura, K, Nagano, M and Fusetani, N (1998) Purification of a larval settlement-inducing protein complex (SIPC) of the barnacle Balanus amphitrite. Journal of Experimental Zoology 281, 12–20.3.0.CO;2-F>CrossRefGoogle Scholar
Miron, G, Walters, LJ, Tremblay, R and Bourget, E (2000) Physiological condition and barnacle behavior: a preliminary look at the relationship between TAG/DNA ratio and larval substratum exploration in Balanus amphitrite. Marine Ecology Progress Series 198, 303–310.CrossRefGoogle Scholar
Molares, J, Tilves, F and Pascual, C (1994) Larval development of the pedunculate barnacle Pollicipes cornucopia (Cirripedia: Scalpellomorpha) reared in the laboratory. Marine Biology 120, 261–264.CrossRefGoogle Scholar
Morse, DE, Duncan, H, Hooker, N, Baloun, A and Young, G (1980) GABA induces behavioural developmental metamorphosis in planktonic molluscan larvae. Federal Proceedings 39, 3237–3241.Google Scholar
Moyse, J (1987) Larvae of lepadomorph barnacles. In Southward, AJ (ed.), Barnacle Biology, Crustacean Issues, No. 5. Rotterdam: Balkema AA, pp. 329–362.Google Scholar
Nasrolahi, A, Pansch, C, Lenz, M and Wahl, M (2012) Being young in a changing world: how temperature and salinity changes interactively modify the performance of larval stages of the barnacle Amphibalanus improvisus. Marine Biology 159, 331–340.CrossRefGoogle Scholar
O'Connor, NJ and Richardson, DL (1994) Comparative attachment of barnacle cyprids (Balanus amphitrite Darwin, 1854; B. improvisus Darwin, 1854; and B. eburneus Gould, 1841) to polystyrene and glass substrata. Journal of Experimental Marine Biology and Ecology 183, 213–225.CrossRefGoogle Scholar
Olivier, F, Tremblay, R, Bourget, E and Rittschof, D (2000) Barnacle settlement: field experiments on the influence of larval supply, tidal level, biofilm quality and age on Balanus amphitrite cyprids. Marine Ecology Progress Series 199, 185–204.CrossRefGoogle Scholar
Pechenik, JA, Rittschof, D and Schmidt, AR (1993) Influence of delayed metamorphosis on survival and growth of juvenile barnacles Balanus amphitrite. Marine Biology 115, 287–294.CrossRefGoogle Scholar
Pechenik, JA, Wendt, DE and Jarrett, JN (1998) Metamorphosis is not a new beginning: larval experience influences juvenile performance. Bioscience 48, 901–910.CrossRefGoogle Scholar
Qiu, JW and Qian, PY (1999) Tolerance of the barnacle Balanus amphitrite amphitrite to salinity and temperature stress: effects of previous experience. Marine Ecology Progress Series 188, 123–132.CrossRefGoogle Scholar
Rao, X and Lin, G (2014) Scanning electron microscopy of the cypris larvae of Capitulum mitella (Cirripedia: Thoracica: Scalpellomorpha). Journal of the Marine Biological Association of the United Kingdom 94, 361–368.CrossRefGoogle Scholar
Rao, X, Lin, G, Zhang, D, Chen, Y and Xu, Y (2010) Combined effects of temperature and salinity on embryonic development and larval growth of Capitulum mitella. Acta Ecologica Sinica 30, 6530–6537.Google Scholar
Rittschof, D, Branscomb, ES and Costlow, JD (1984) Settlement and behaviour in relation to flow and surface in larval barnacles, Balanus amphitrite Darwin. Journal of Experimental Marine Biology and Ecology 82, 131–146.CrossRefGoogle Scholar
Rittschof, D, Forward, RB, Cannon, G, Welch, JM, McClary, M, Holm, ER, Clare, AS, Conova, S, McKelvey, LM, Bryan, P and van Dover, CL (1998) Cues and context: larval responses to physical and chemical cues. Biofouling 12, 31–44.CrossRefGoogle Scholar
Satuito, CG, Shimizu, K, Natoyama, K, Yamazaki, M and Fusetani, N (1996) Age-related settlement success by cyprids of the barnacle Balanus amphitrite, with special reference to consumption of cyprid storage protein. Marine Biology 127, 125–130.CrossRefGoogle Scholar
Satuito, CG, Shimizu, K and Fusetani, N (1997) Studies on the factors influencing larval settlement in Balanus amphitrite and Mytilus galloprovincialis. Hydrobiologia 358, 275–280.CrossRefGoogle Scholar
Shimizu, K, Saikawa, W and Fusetani, N (1996) Identification and partial characterization of vitellin from the barnacle Balanus amphitrite. Comparative Biochemistry and Physiology 115B, 111–119.CrossRefGoogle Scholar
Spremberg, U, Høeg, JT, Buhl-Mortensen, L and Yusa, Y (2012) Cypris settlement and dwarf male formation in the barnacle Scalpellum scalpellum: a model for an androdioecious reproductive system. Journal of Experimental Marine Biology and Ecology 422–423, 39–47.CrossRefGoogle Scholar
Thiyagarajan, V (2010) A review on the role of chemical cues in habitat selection by barnacles: new insights from larval proteomics. Journal of Experimental Marine Biology and Ecology 392, 22–36.CrossRefGoogle Scholar
Thiyagarajan, V, Harder, T and Qian, PY (2002a) Effect of the physiological condition of cyprids and laboratory-mimicked seasonal conditions on the metamorphic successs of Balanus amphitrite Darwin (Cirripedia; Thoracica). Journal of Experimental Marine Biology and Ecology 274, 65–74.CrossRefGoogle Scholar
Thiyagarajan, V, Harder, T and Qian, PY (2002b) Relationship between cyprid energy reserves and metamorphosis in the barnacle Balanus amphitrite Darwin (Cirripedia: Thoracica). Journal of Experimental Marine Biology and Ecology 280, 79–93.CrossRefGoogle Scholar
Thiyagarajan, V, Harder, T and Qian, PY (2003a) Combined effects of temperature and salinity on larval development and attachment of the subtidal barnacle Balanus trigonus Darwin. Journal of Experimental Marine Biology and Ecology 287, 223–236.CrossRefGoogle Scholar
Thiyagarajan, V, Harder, T, Qiu, JW and Qian, PY (2003b) Energy content at metamorphosis and growth rate of the early juvenile barnacle Balanus amphitrite. Marine Biology 143, 543–554.CrossRefGoogle Scholar
Tremblay, R, Olivier, F, Bourget, E and Rittschof, D (2007) Physiological condition of Balanus amphitrite cyprid larvae determines habitat selection success. Marine Ecology Progress Series 340, 1–8.CrossRefGoogle Scholar
Underwood, AJ (1997) Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge: Cambridge University Press.Google Scholar
Yamamoto, H, Kawaii, S, Yoshimura, E, Tachibana, A and Fusetani, N (1997) 20-hydroxyecdysone regulates larval metamorphosis of the barnacle, Balanus amphitrite. Zoological Science (Tokyo) 14, 887–892.CrossRefGoogle Scholar
Zhang, D, Rao, X, Lin, G and Cheng, N (2009) The effect of temperature on embryonic and larval development of Pollicipes mitella Linnaeus. Journal of Fujian Normal University Natural Sciences 25, 94–100.Google Scholar