Skip to main content

Advertisement

SpringerLink
Log in

In situ biomonitoring shows seasonal patterns and environmentally mediated gaping activity in the bivalve, Pinna nobilis

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

Abstract

The rhythms and responses of animals to environmental factors are important issues for their adaptation to natural cycles. These rhythms assure an optimum synchrony between organisms and their environment. Bio-logging enables monitoring these activity cycles remotely. To characterize rhythms and responses of fan mussels (Pinna nobilis) to environmental factors, six individuals were monitored from April 2009 to October 2011. The study was conducted at a station in the western Mediterranean at 11 m depth in Tabarca Island Marine Reserve (Alicante, Spain). Sensors at the station monitored dissolved oxygen (mg l−1), turbidity (ntu), temperature (°C), chlorophyll a concentration (chl a) (mg m−3), current speed (cm s−1), and direction (°). One pattern of gaping activity (P1) occurred from mid-July–early August–early November, whereas another pattern (P2) occurred the rest of the time (i.e., from early November–mid-July–early August). The activity was synchronized among the fan mussels and showed autocorrelation peaks at a period of 21.9–24 h. In P1, the fan mussels opened their valves according to the position and illumination of the sun and moon. In P2, however, individuals did not track sun and moonlight, although their gaping activity was regular and synchronized. Likewise, individuals were unaffected by high-frequency (daily) variation in dissolved oxygen and (chl a). Gaping activity was directly influenced by current intensity and direction. The shift between the two patterns and the presence of similar periods of autocorrelation in the activity time series indicate that P. nobilis has an internal clock.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bae MJ, Park YS (2014) Biological early warning system based on the responses of aquatic organisms to disturbances: a review. Sci Total Environ 466:635–649. doi:10.1016/j.scitotenv.2013.07.075

    Article  Google Scholar 

  • Basso L, Vázquez-Luis M, García-March JR, Deudero S, Alvarez E, Vicente N, Duarte CM, Hendriks IE (2015) The Pen Shell, Pinna nobilis: a review of population status and recommended research priorities in the Mediterranean Sea. In: Curry B (ed) Advances in marine biology, vol 71. Academic Press, London, pp 109–160. doi:10.1016/bs.amb.2015.06.002

    Google Scholar 

  • Borcherding J (2006) Ten years of practical experience with the Dreissena-Monitor, a biological early warning system for continuous water quality monitoring. Hydrobiologia 556:417–426. doi:10.1007/s10750-005-1203-4

    Article  CAS  Google Scholar 

  • Cabanellas-Reboredo M, Deudero S, Alos J, Valencia JM, March D, Hendriks IE, Alvarez E (2009) Recruitment of Pinna nobilis (Mollusca: Bivalvia) on artificial structures. Mar Biodivers Rec 2:1–5. doi:10.1017/S1755267209001274

    Article  Google Scholar 

  • Cabanellas-Reboredo M, Blanco A, Deudero S, Tejada S (2010) Effects of the invasive macroalga Lophocladia lallemandii on the diet and trophism of Pinna nobilis (Mollusca: Bivalvia) and its guests Pontonia pinnophylax and Nepinnotheres pinnotheres (Crustacea: Decapoda). Sci Mar 74:101–110. doi:10.3989/scimar.2010.74n1101

    Article  Google Scholar 

  • Davenport J, Ezgeta-Balic D, Peharda M, Skejic S, Nincevia-Gladan Z, Matijevic S (2011) Size-differential feeding in Pinna nobilis L, (Mollusca: Bivalvia): exploitation of detritus, phytoplankton and zooplankton. Estuar Coast Shelf Sci 92:246–254. doi:10.1016/j.ecss.2010.12.033

    Article  Google Scholar 

  • de Gaulejac B (1995) Mise en évidence de l’hermafroditisme successif à maturation asynchrone de Pinna nobilis (L.) (Bivalvia: Pteroidea). C R Acad Sci III Sci Vie 318:99–103

    Google Scholar 

  • Duffet-Smith P (1988) Practical astronomy with your calculator. Cambridge University Press, Cambridge

    Google Scholar 

  • Foster RG, Kreitzman L (2004) Rhythms of life. The biological clocks that control the daily lives of every living thing. Yale University Press, New Haven

    Google Scholar 

  • García-March JR, Ferrer JF (1995) Biometría de Pinna nobilis L, 1758: una revisión de la ecuación de De Gaulejac y Vicente (1990). Bol Inst Esp Oceanogr 11:175–181

    Google Scholar 

  • Garcia-March JR, Vicente N (2007) Protocol to study and monitor Pinna nobilis populations within marine protected areas. MEPA, La Valette

    Google Scholar 

  • García-March JR, Garcia-Carrascosa AM, Pena AL (2002) In situ measurement of Pinna nobilis shells for age and growth studies: a new device. Mar Ecol PSZN I 23(3):207–217. doi:10.1046/j.1439-0485.2002.02781.x

    Article  Google Scholar 

  • García-March JR, Perez-Rojas L, García-Carrascosa AM (2007) Influence of hydrodynamic forces on population structure of Pinna nobilis L, 1758 (Mollusca : Bivalvia): The critical combination of drag force, water depth, shell size and orientation. J Exp Mar Biol Ecol 342:202–212. doi:10.1016/j.jembe.2006.09.007

    Article  Google Scholar 

  • García-March JR, Sanchis-Solsona MA, García-Carrascosa AM (2008) Shell gaping behaviour of Pinna nobilis L, 1758: circadian and circalunar rhythms revealed by in situ monitoring. Mar Biol 153:689–698. doi:10.1007/s00227-007-0842-6

    Article  Google Scholar 

  • García-March JR, Surge D, Lees JM, Kersting DK (2011) Ecological information and water mass properties in the Mediterranean recorded by stable isotope ratios in Pinna nobilis shells. J Geophys Res Biogeosci 116:1–14. doi:10.1029/2010JG001461

    Article  Google Scholar 

  • Hendriks IE, Cabanellas-Reboredo M, Bouma TJ, Deudero S, Duarte CM (2011) Seagrass meadows modify drag forces on the shell of the fan mussel Pinna nobilis. Estuar Coasts 34:60–67. doi:10.1007/s12237-010-9309-y

    Article  Google Scholar 

  • Jou LJ, Lin SC, Chen BC, Chen WY, Liao CM (2013) Synthesis and measurement of valve activities by an improved online clam-based behavioral monitoring system. Comput Electron Agric 90:106–118. doi:10.1016/j.compag.2012.09.008

    Article  Google Scholar 

  • Katsanevakis S (2007) Growth and mortality rates of the fan mussel Pinna nobilis in Lake Vouliagmeni (Korinthiakos Gulf, Greece): a generalized additive modelling approach. Mar Biol 152:1319–1331. doi:10.1007/s00227-007-0781-2

    Article  Google Scholar 

  • Kennedy H, Richardson CA, Duarte CM, Kennedy DP (2001) Oxygen and carbon stable isotopic profiles of the fan mussel, Pinna nobilis, and reconstruction of sea surface temperatures in the Mediterranean. Mar Biol 139:1115–1124

    Article  Google Scholar 

  • Kim WS, Huh HT, Je JG, Han KN (2003) Evidence of two-clock control of endogenous rhythm in the Washington clam, Saxidomus purpuratus. Mar Biol 142:305–309. doi:10.1007/s00227-002-0952-0

    Google Scholar 

  • Liao CM, Jau SF, Lin CM, Jou LJ, Liu CW, Liao VHC, Chang FJ (2009) Valve movement response of the freshwater clam Corbicula fluminea following exposure to waterborne arsenic. Ecotoxicology 18:567–576. doi:10.1007/s10646-009-0314-5

    Article  CAS  Google Scholar 

  • Mat AM, Massabuau JC, Ciret P, Tran D (2012) Evidence for a plastic dual circadian rhythm in the oyster Crassostrea gigas. Chronobiol Int 29:857–867. doi:10.3109/07420528.2012.699126

    Article  Google Scholar 

  • McClintock JB, Watts SA (1990) The effects of photoperiod on gametogenesis in the tropical sea-urchin Eucidaris tribuloides (Lamarck) (Echinodermata, Echinoidea). J Exp Mar Biol Ecol 139:175–184. doi:10.1016/0022-0981(90)90145-3

    Article  Google Scholar 

  • Najdek M, Blazina M, Ezgeta-Balic D, Peharda M (2013) Diets of fan shells (Pinna nobilis) of different sizes: fatty acid profiling of digestive gland and adductor muscle. Mar Biol 160:921–930. doi:10.1007/s00227-012-2144-x

    Article  CAS  Google Scholar 

  • Ortmann C, Grieshaber MK (2003) Energy metabolism and valve closure behaviour in the Asian clam Corbicula fluminea. J Exp Biol 206:4167–4178. doi:10.1242/jeb.00656

    Article  CAS  Google Scholar 

  • Palmer JD (2000) The clocks controlling the tide-associated rhythms of intertidal animals. Bioessays 22:32–37

    Article  CAS  Google Scholar 

  • Rensing L, Meyer-Grahle U, Ruoff P (2001) Biological timing and the clock metaphor: oscillatory and hourglass mechanisms. Chronobiol Int 18:329–369. doi:10.1081/cbi-100103961

    Article  CAS  Google Scholar 

  • Rhoads DC, Lutz RA (1980) Skeletal growth of aquatic organisms. Plenum Publishing Corporation, New York

    Book  Google Scholar 

  • Riisgard HU, Kittner C, Seerup DF (2003) Regulation of opening state and filtration rate in filter-feeding bivalves (Cardium edule, Mytilus edulis, Mya arenaria) in response to low algal concentration. J Exp Mar Biol Ecol 284:105–127. doi:10.1016/S0022-0981(02)00496-3

    Article  Google Scholar 

  • Robson AA, De Leaniz CG, Wilson RP, Halsey LG (2010) Behavioural adaptations of mussels to varying levels of food availability and predation risk. J Moll Stud 76:348–353. doi:10.1093/mollus/eyq025

    Article  Google Scholar 

  • Rodland DL, Schöne BR, Baier S, Zhang ZJ, Dreyer W, Page NA (2009) Changes in gape frequency, siphon activity and thermal response in the freshwater bivalves Anodonta cygnea and Margaritifera falcata. J Moll Stud 75:51–57. doi:10.1093/mollus/eyn038

    Article  Google Scholar 

  • Scargle JD (1982) Studies in astronomical time-series analysis. II. Statistical aspects of spectral-analysis of unevenly spaced data. Astrophys J 263:835–853. doi:10.1086/160554

    Article  Google Scholar 

  • Schöne BR (2008) The curse of physiology—challenges and opportunities in the interpretation of geochemical data from mollusk shells. Geo-Mar Lett 28:269–285. doi:10.1007/s00367-008-0114-6

    Article  Google Scholar 

  • Schöne BR, Surge D (2012) Chapter 14. Bivalve sclerochronology and geochemistry. In: Seldon P, Hardesty J (eds) Treatise online 46: Part N, revised, vol 1. The University of Kansas, Paleontological Institute, Lawrence, pp 1–24

    Google Scholar 

  • Schwartzmann C, Durrieu G, Sow M, Ciret P, Lazareth CE, Massabuaua J (2011) In situ giant clam growth rate behavior in relation to temperature: a one-year coupled study of high-frequency noninvasive valvometry and sclerochronology. Limnol Oceanogr 56:1940–1951. doi:10.4319/lo.2011.56.5.1940

    Article  Google Scholar 

  • Sluyts H, VanHoof F, Cornet A, Paulussen J (1996) A dynamic new alarm system for use in biological early warning systems. Environ Toxicol Chem 15:1317–1323

    Article  CAS  Google Scholar 

  • Sobrino-Figueroa A, Caceres-Martinez C (2009) Alterations of valve closing behavior in juvenile Catarina scallops (Argopecten ventricosus Sowerby, 1842) exposed to toxic metals. Ecotoxicology 18:983–987. doi:10.1007/s10646-009-0358-6

    Article  CAS  Google Scholar 

  • Sow M, Durrieu G, Briollais L, Ciret P, Massabuau JC (2011) Water quality assessment by means of HFNI valvometry and high-frequency data modeling. Environ Monit Assess 182:155–170. doi:10.1007/s10661-010-1866-9

    Article  Google Scholar 

  • Suzuki K, Kiyomoto S, Koshiishi Y (2007) Observation on behavior of the large suspension feeding bivalve Atrina pectinata lisckeana under natural conditions. Bull Fish Res Agency 19:17–25

    Google Scholar 

  • Tran D, Fournier E, Durrieu G, Massabuau JC (2007) Inorganic mercury detection by valve closure response in the freshwater clam Corbicula fluminea: Integration of time and water metal concentration changes. Environ Toxicol Chem 26:1545–1551. doi:10.1897/06-390R1.1

    Article  CAS  Google Scholar 

  • Tran D, Nadau A, Durrieu G, Ciret P, Parisot JP, Massabuau JC (2011) Field chronobiology of a molluscan bivalve: how the moon and sun cycles interact to drive oyster activity rhythms. Chronobiol Int 28:307–317. doi:10.3109/07420528.2011.565897

    Article  Google Scholar 

  • Trigos S, García-March JR, Vicente N, Tena J, Torres J (2014) Utilization of muddy detritus as organic matter source by the fan mussel Pinna nobilis. Med Mar Sci 15:667–674. doi:10.12681/mms.836

    Google Scholar 

  • van Keulen M, Borowitzka MA (2002) Comparison of water velocity profiles through morphologically dissimilar seagrasses measured with a simple and inexpensive current meter. Bull Mar Sci 71:1257–1267

    Google Scholar 

  • Williams BG, Pilditch CA (1997) The entrainment of persistent tidal rhythmicity in a filter-feeding bivalve using cycles of food availability. J Biol Rhythm 12:173–181. doi:10.1177/074873049701200208

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The project was funded by “Obra Social Caja Madrid” of “Caja Madrid” Bank. We are grateful to Felio Lozano, the coordinator of Tabarca Island Marine Reserve, the guards of the Reserve, Silvia Revenga and the RMIP—SGM—MARM, for their permissions, collaboration, and inestimable help with the work in the MPA. We are also grateful to the anonymous reviewers and the editors for their comments that have strongly improved the final version of the manuscript.

Author information

Authors and Affiliations

  1. Institute of Environment and Marine Science Research (IMEDMAR), Universidad Católica de Valencia SVM, C/Explanada del Puerto s/n, 03710, Calpe, Alicante, Spain

    Jose R. Garcia-March, Miguel A. Sanchis, Sergio Monleon & Jose Tena-Medialdea

  2. Instituto de Ecología Litoral, El Campello, Alicante, Spain

    Santiago Jiménez

  3. Department of Geological Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    Jonathan Lees & Donna Surge

Authors
  1. Jose R. Garcia-March
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Santiago Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miguel A. Sanchis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sergio Monleon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jonathan Lees
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Donna Surge
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jose Tena-Medialdea
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jose R. Garcia-March.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: J. Grassle.

Reviewed by A. A. Robson and D. Tran.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garcia-March, J.R., Jiménez, S., Sanchis, M.A. et al. In situ biomonitoring shows seasonal patterns and environmentally mediated gaping activity in the bivalve, Pinna nobilis . Mar Biol 163, 29 (2016). https://doi.org/10.1007/s00227-016-2812-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2812-3

Keywords

Search

Navigation