Skip to main content

Effects of body-size and season on digestive organ size and the energy balance of cockles fed with a constant diet of phytoplankton

Journal of Comparative Physiology B volume 178, pages 501–514 (2008)Cite this article

Abstract

Seasonal variation in size-dependence of seawater clearance rate, absorption efficiency, oxygen consumption, gill area, length of the crystalline style and dry weight of digestive gland was analyzed in cockles Cerastoderma edule from the Mundaka Estuary, Spain. Experimental determinations were performed monthly (from July 1998 to November 1999) in cockles being fed with Tetraselmis suecica (organic content: 87.84 ± 1.95%) at a concentration of 3 mm3/l for 3 days. Analysis of covariance reveals no seasonal differences in both size-dependence of seawater clearance rate and oxygen consumption, which were found to scale to dry body weight with mass-exponents of 0.56 and 0.62, respectively. No significant correlation was found between absorption efficiency and body weight. Mass-exponents for gill area, dry weight of the digestive gland and length of the crystalline style remained constant among seasons showing values of 0.62, 0.34 and 0.82, respectively. Seasonal trends for every physiological determination were calculated for a standard size (200 mg) cockle: standardized clearance rates and oxygen consumptions followed a similar trend with minimum values in winter (≈0.5 l/h and ≈100 μl O2/h, respectively) and maximum values during spring–summer (≈1.7 l/h and ≈250 μl O2/h, respectively), whereas absorption efficiency and food throughput time showed both the opposite pattern with highest values corresponding to winter months (≈50–60% and ≈5–6 h, respectively), and lowest (≈30% and ≈3–4 h, respectively) to summer–autumn. Scope for growth exhibited minimum values in winter followed by a rapid increase along the winter–spring transition, maximum values being attained in spring (May) and summer (July). Exponential decline of seasonal values of absorption efficiency associated to rising ingestion rates of organic matter presented an asymptotic minimum at 0.35. Absorption efficiency was positively related to food throughput time, whereas the latter fell to a minimum of 3.548 h with increasing food intake. So, maintenance of throughput time—and consequently absorption efficiency—along with enhanced filtering activity provided cockles with higher absorption rates improving scopes for growth registers during spring and summer. These dynamics might be explained as the consequence of the seasonal digestive adjustments in cockles, which, in fact, were found to increase the size of the digestive organs during that period.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

AE:

Food absorption efficiency

AR:

Food absorption rate

CR:

Seawater clearance rate

GA:

Gill area

L CS :

Length of the crystalline style

OIR:

Ingestion rate of organic matter

R :

Metabolic rate

SFG:

Energetic scope for growth

TT:

Food Throughput time

VO2 :

Oxygen consumption

W DG :

Dry weight of the digestive gland

References

  • Ansell AD, Lagardere F (1980) Observations on the biology of Donax trunculus L. And D. Vittatus at Ile d´ Olèron (French Atlantic coast). Mar Biol 57:287–300

    Article  Google Scholar 

  • Ansotegui A, Trigueros JM, Orive E (2001) The use of pigment signatures to assess phytoplankton assemblage structure in estuarine watters. Estuar Coast Shelf Sci 52(6):297–313

    Article  CAS  Google Scholar 

  • Arnold WS, Marelli DC, Bert TM, Jones DS, Quitmyer IR (1991) Habitat specific growth of hard clams Mercenaria mercenaria (L.) from the Indian river, Florida. J Exp Mar Biol Ecol 147:245–265

    Article  Google Scholar 

  • Bachelet G, (1980) Growth and recruitment of the tellini bivalve Macoma balthica at the southern limit of its geographical distribution, the Gironde Estuary (SW France). Mar Biol 59:105–117

    Article  Google Scholar 

  • Bayne BL (1993) Feeding physiology of bivalves: time-dependence and compensation for changes in food availability. In: Dame RF (ed) Bivalve Filter Feeders in Estuarine and Coastal Ecosystem Processes. NATO ASI Series, vol G33, Springer, Berlin, pp 1–24

  • 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 

  • Bayne BL, Newell RC (1983) Physiological energetics of marine molluscs. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca. Vol IV Physiology, Part 1. Academic Press, New York, pp 407–515

    Google Scholar 

  • Bernard FR (1983) Physiology and the mariculture of some northeastern Pacific bivalve molluscs. Can Spec Publ Fish Aquat Sci 63:24

    Google Scholar 

  • Beukema JJ (1982) Calcimass and carbonate production by molluscs on the tidal flats in the Ducth Wadden sea: II The edible cockle Cerastoderma edule. Neth J Sea Res 15:391–405

    Article  Google Scholar 

  • Bodoy A (1982) Croisance saisonniere du bivalve Donax trunculus (L.) en Mediterranee Nord-Occidentale (France). Malacologia 22:353–358

    Google Scholar 

  • Brousseau DJ (1979) Analysis of growth rate in Mya arenaria using the Von Bertalanffy equation. Mar Biol 51:221–227

    Article  Google Scholar 

  • Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnol Oceanograph 11:338–358

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dong B, Xue QZ, Li J (2000) Environmental factors affecting the feeding physiological ecology of Manila clam, Ruditapes phillipinarum. Oceanol Limnol Sin 31:636–642

    Google Scholar 

  • Gnaiger E (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Gnaiger E, Forstner H (eds) Polarographic oxygen sensors. Springer, Berlin, pp 337–345

    Google Scholar 

  • Goulletquer P, Heral M, Deslous-Paoli JM, Prou J, Garnier J, Razet D, Boromtharanad W (1989) Ecophysiologie et bilan énergétique de la palourde japoneise d’élevage Ruditapes phillipinarum. J Exp Mar Biol Ecol 132:85–108

    Article  Google Scholar 

  • Hawkins AJS, Bayne BL (1992) Physiological interrelations and the regulation of production. In: Gosling E (ed) The mussel Mytilus, ecology, physiology and culture. Elsevier, Amsterdam, pp 171–222

    Google Scholar 

  • Hawkins AJS, Navarro E, Iglesias JIP (1990) Comparative allometries of gut passage time, gut content and metabolic faecal loss in Mytilus edulis and Cerastoderma edule. Mar Biol 105:197–204

    Article  Google Scholar 

  • Hibbert CJ (1977) Growth and survivorship in a tidal-flat population of the bivalve Mercenaria mercenaria from Southampton Water. Mar Biol 44:71–76

    Article  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation. Mechanism and process in physiological evolution. University Press, Oxford

    Google Scholar 

  • Huang S, Newell RIE (2002) Seasonal variations in the rates of aquatic and aerial respiration and ammonia excretion of the ribbed mussel Geukensia demissa. J Exp Mar Biol Ecol 270:241–255

    Article  CAS  Google Scholar 

  • Hummel H, De Bruin W, Niewland G, Hummel-Poel IF, (1988) Seasonal and tidal changes in the length of the crystalline style intertidally living Macoma balthica (Mollusca, Bivalvia). Mar Biol 98:529–534

    Article  Google Scholar 

  • Ibarrola I, Navarro E, Iglesias JIP (1998a) Short-term adaptation of digestive processes in the cockle Cerastoderma edule exposed to different food quantity and quality. J Comp Physiol B 168:32–40

    Article  Google Scholar 

  • Ibarrola I, Larretxea X, Iglesias JIP, Urrutia MB, Navarro E (1998b) Seasonal variation of digestive enzyme activities in the digestive gland and the crystalline style of the common cockle Cerastoderma edule. Comp Biochem Physiol A 121:25–34

    Article  Google Scholar 

  • Ibarrola I, Navarro E, Iglesias JIP, Urrutia MB (1999) Time-course of digestive-enzyme acclimation in the cockle Cerastoderma edule. Mar Biol 135:45–56

    Article  Google Scholar 

  • Ibarrola I, Navarro E, Iglesias JIP, Urrutia MB (2000a) Temporal changes in feeding and absorption of biochemical components in Cerastoderma edule fed an algal diet. J Mar Biol Ass UK 80:119–125

    Article  Google Scholar 

  • Ibarrola I, Navarro E, Urrutia MB (2000b) Acute and acclimated digestive responses of the cockle Cerastoderma edule (L.) to changes in the food quality and quantity. I. Feeding and absorption of biochemical components. J Exp Mar Biol Ecol 252:181–198

    PubMed  Article  CAS  Google Scholar 

  • Ibarrola I, Etxeberria M, Iglesias JIP, Urrutia MB, Angulo E (2000c) Acute and acclimated digestive responses of the cockle Cerastoderma edule (L.) to changes in the food quality and quantity. II. Enzymatic, cellular and tissular responses of the digestive gland. J Exp Mar Biol Ecol 252:199–219

    PubMed  Article  CAS  Google Scholar 

  • Iglesias JIP, Navarro E (1990) Shell growth of the cockle Cerastoderma edule in the Mundaka estuary. J Moll Stud 56:229–238

    Article  Google Scholar 

  • Iglesias JIP, Navarro E (1991) Energetics of growth and reproduction in cockles (Cerastoderma edule): seasonal and age dependent variations. Mar Biol 111:359–368

    Article  Google Scholar 

  • Jones HD, Richards OG, Southern TA (1992) Gill dimensions, water pumping rate and body size in the mussel Mytilus edulis L. J Exp Mar Biol Ecol 155:213–237

    Article  Google Scholar 

  • Kreeger DA (1993) Seasonal patterns in the utilization of dietary protein by the mussel Mytilus trossulus. Mar Ecol Prog Ser 95:215–232

    Google Scholar 

  • Kreeger DA, Newell RIE (2001) Seasonal utilization of different seston carbon sources by the ribbed mussel Geukensia demissa (Dillwyn) in a mid-Atlantic salt marsh. J Exp Mar Biol Ecol 260:71–91

    PubMed  Article  Google Scholar 

  • Marigómez I, Orbea A, Olabarrieta I, Etxebarria M, Cajaraville MP (1996) Structural changes in the digestive lysosomal system of sentinel mussel as biomarkers of environmental stress in Mussel-Watch programmes. Comp Biochem Physiol C 103:43–51

    Google Scholar 

  • Moschino V, Marin MG (2006) Seasonal changes in physiological responses and evaluation of “well-being” in the Venus clam Chamelea gallina from the Northern Adriatic Sea. Comp Biochem Physiol A 145:433–440

    Article  CAS  Google Scholar 

  • Møhlenberg F, Riisgard HU, (1979) Filtration rate using a new indirect technique, in thirteen species of suspension-feeding bivalves. Mar Biol 54:143–147

    Article  Google Scholar 

  • Navarro E, Iglesias JIP (1993) Infaunal filter-feeding bivalves and the physiological response to short-term fluctuations in food availability and composition. In: Dame RF (ed) Bivalve Filter Feeders in Estuarine and Coastal Ecosystem Processes. NATO ASI Series, vol G33, Springer, Berlin, pp 25–26

  • Navarro E, Iglesias JIP, Ortega MM, Larretxea X (1994) The basis for a functional response to variable food quantity and quality in cockles Cerastoderma edule (Bivalvia, Cardiidae). Physiol Zool 67:468–498

    Google Scholar 

  • Newell RIE Bayne BL (1980) Seasonal changes in the physiology, reproductive condition and carbohydrate content of the cockle Cardium (=Cerastoderma) edule (Bivalvia: Cardiidae). Mar Biol 56:11–19

    Article  Google Scholar 

  • Nichols FH, Thompson JK (1982) Seasonal growth in the bivalve Macoma balthica near the southern limit of its range. Estuaries 5:110–120

    Article  Google Scholar 

  • Pérez-Camacho A, Labarta U, Navarro E (2000) Energy balance of mussels Mytilus galloprovincialis: the effect of length and age. Mar Ecol Prog Ser 199:149–158

    Article  Google Scholar 

  • Reid RGB, Rauchert K (1976) Catheptic endopeptidases and protein digestion in the horse clam Tresus capax (Gould). Comp Biochem Physiol B 54:467–472

    PubMed  Article  CAS  Google Scholar 

  • Revilla M, Iriarte A, Madariaga I, Orive E (2000) Bacterial and phytoplankton dynamics along a throphic gradient in a shallow temperate estuary. Est Coast Shelf Sci 50(3):297–313

    Article  Google Scholar 

  • Rueda JL, Smaal AC (2004) Variation of the physiological energetics of the bivalve Spisula subtruncata (da Costa, 1778) within an anual cycle. J Exp Mar Biol Ecol 301:141–157

    Article  Google Scholar 

  • Seed R (1976) Ecology. In: BL Bayne (ed) Marine mussels:their ecology and physiology. Cambridge University Press, Cambridge, pp 13–66

    Google Scholar 

  • Smaal AC, Verhagen JGH, Coosen J, Haas HA (1986) Interactions between seston quantity and quality and benthic suspension feeders in the Oosterschelde, The Netherlands. Ophelia 26:385–399

    Google Scholar 

  • Smaal AC, Vonck APMA, Bakker M (1997) Seasonal variation in physiological energetics of Mytilus edulis and Cerastoderma edule of different size classes. J Mar Biol Ass UK 77:817–838

    Article  Google Scholar 

  • Urrutia MB, Ibarrola I, Iglesias JIP, Navarro E, (1999) Energetic of growth and reproduction in a high-tidal population of the clam Ruditapes decussatus from Urdaibai Estuary (Basque Country, N.Spain). J Sea Res 42:35–48

    Article  Google Scholar 

  • Vahl O (1973) Pumping and oxygen consumption rates of Mytilus edulis L. of different sizes. Ophelia 12:45–52

    Google Scholar 

  • Ward JE Shumway SE (2004) Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. J Exp Mar Biol Ecol 300:83–130

    Article  Google Scholar 

  • Winter JE (1969) Ueber den Einfluss der Nahrungskonzentration und anderer Factoren auf Filtrierleistung und Nahrungsausnutzung der Muscheln Arctica islandica und Modiolus modiolus. Mar Biol 99:87–135

    Article  Google Scholar 

  • Whyte JNC, (1987) Biochemical composition and energy content of six species of phytoplankton used in mariculture of bivalves. Aquaculture 60:231–241

    Article  CAS  Google Scholar 

  • Wong WH, Cheung SG, (2003) Seasonal variation in the feeding physiology and scope for growth of green mussels, Perna viridis in estuarine Ma Wan, Hong Kong. J Mar Biol Ass UK 83:543–552

    Article  Google Scholar 

  • Zar JH (1984) Bioestadistical analysis. Prentice-Hall, Englewood Cliffs

    Google Scholar 

  • Zhuang SH, Wang ZQ (2004) Influence of size, habitat and food concentration on the feeding ecology of the bivalve Meretrix meretrix Linnaeus. Aquaculture 241:689–699

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. M.M. Ortega for critically commenting on the manuscript. The comments of an anonymous referee helped considerably in improving this article.

Author information

Affiliations

  1. Dpto de Genética, Antropología Física y Fisiología Animal, Facultad de Ciencia y Tecnología, Universidad del País Vasco/Euskal Herriko Unibertsitatea, E-48080, Bilbao, Spain

    I. Ibarrola, X. Larretxea, E. Navarro, J. I. P. Iglesias & M. B. Urrutia

Authors
  1. I. Ibarrola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. X. Larretxea
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. I. P. Iglesias
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. B. Urrutia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Ibarrola.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ibarrola, I., Larretxea, X., Navarro, E. et al. Effects of body-size and season on digestive organ size and the energy balance of cockles fed with a constant diet of phytoplankton. J Comp Physiol B 178, 501–514 (2008). https://doi.org/10.1007/s00360-007-0243-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-007-0243-7

Keywords

  • Bivalves
  • Scope for growth
  • Digestive acclimation
  • Seasonal variation
  • Allometric relationships