Skip to main content

Advertisement

Log in

Extremes of metabolic strategy in Antarctic Bryozoa

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The physiology of many organisms in many places varies with seasonality of environment characteristics. Polar marine environments are amongst the least and most seasonal. For example, sea temperature varies by <3°C while light climate and primary productivity vary more than elsewhere. Polar nearshore invertebrates generally live life at a slow pace with recorded metabolic rates of 22–454 μg O2/g ash-free dry-mass/h. We measured oxygen uptake by three Antarctic cheilostomatid bryozoan species during summer and winter months. Our data suggest that, in many ways, bryozoans differ from other animals. They have enormous metabolic flexibility; more within the order Cheilostomatida than in all other polar marine animals measured to date. One species alone, Kymella polaris, had both the lowest (16.8) and highest (574.9 μg O2/g ash-free dry-mass/h levels recorded. Furthermore, Camptoplites bicornis showed no significant change in oxygen consumption with season whereas the final species, Isoseculiflustra tenuis, showed the highest winter to summer metabolic rise (ratio =3.45) reported for a polar species. They may not have a resting state analogous to other animals, but exhibit either full activity or ‘dormancy’ in which most organic tissues are reabsorbed. The concept of resting metabolism in this taxon may be inappropriate.

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
Fig. 6

Similar content being viewed by others

References

  • Ahn I-Y, Shim JH (1998) Summer metabolism of the Antarctic clam, Laternula elliptica (King and Broderip) in Maxwell Bay, King George Island and its implications. J Exp Mar Biol Ecol 224:253–264

    Article  Google Scholar 

  • Arntz WE, Brey T, Gallardo VA (1994) Antarctic zoobenthos. Oceanogr Mar Biol Annu Rev 32:251–303

    Google Scholar 

  • Bader B (2001) Bryozoan communities of the Weddell Sea, Antarctica: a first overview. In: Wyse Jackson P, Buttler C, Spencer Jones M (eds) Bryozoan studies 2001. Balkema, Rotterdam, pp 1–6

  • Barnes DKA (1995) Seasonal and annual growth in erect species of Antarctic bryozoans. J Exp Mar Biol Ecol 188:181–198

    Article  Google Scholar 

  • Barnes DKA (1999) Do life patterns differ between two Scotia Arc localities? Antarct Sci 11:275–282

    Google Scholar 

  • Barnes DKA, Clarke A (1994) Seasonal variation in the feeding activity of four species of Antarctic bryozoan in relation to environmental factors. J Exp Mar Biol Ecol 181:117–133

    Article  Google Scholar 

  • Barnes DKA, Clarke A (1995) Seasonality of feeding activity in Antarctic suspension feeders. Polar Biol 15:335–340

    Article  Google Scholar 

  • Barnes DKA, Clarke A (1998) Seasonality of polypide cycling and sexual reproduction in some erect Antarctic bryozoans. Mar Biol 131:647–658

    Article  Google Scholar 

  • Benson BB, Krause D (1984) The concentration and isotopic fraction of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnol Oceanogr 29:620–632

    CAS  Google Scholar 

  • Brey T, Pearse JS, Basch L, McClintock JB, Slattery M (1995) Growth and production of Sterechinus neumayeri (Echinoidea: Echinodermata) in McMurdo Sound, Antarctica. Mar Biol 124:279–292

    Article  Google Scholar 

  • Brey T, Gerdes D, Gutt J, Mackensen A, Starmans A (1999a) Growth and age of the Antarctic bryozoan Cellaria incula on the Weddell Sea shelf. Antarct Sci 11:408–414

    Google Scholar 

  • Brey T, Gutt J, Mackensen A, Starmans A (1999b) Growth and productivity of the high Antarctic bryozoan Melicerita obliqua. Mar Biol 132:327–333

    Article  Google Scholar 

  • Brockington S (2001) The seasonal energetics of the Antarctic bivalve Laternula elliptica (King and Broderip) at Rothera Point, Adelaide Island. Polar Biol 24:523–530

    Article  Google Scholar 

  • Brockington S, Peck LS (2001) Seasonality of respiration and ammonium excretion in the Antarctic echinoid Sterechinus neumayeri. Mar Ecol Prog Ser 219:159–168

    CAS  Google Scholar 

  • Cancino JM, Castaneda B, Munõz M (1991) Consequences on colony size of the metabolic rates of the bryozoans Membranipora isabelleana and Caulorhamphus spiniferum. In: Bigey FP, d’Hondt JL (eds) Bryozoaires actuels et fossils. Bulletin de la Societe sciences Naturellea de la Ouest de France, memoire H.S. 1. Nantes, pp 567–568

  • Cancino JM, Torres F, Moyano GHI (2001) Larval release pattern in Antarctic bryozoans. In: Wyse Jackson P, Buttler C, Spencer Jones M (eds) Bryozoan Studies 2001. Balkema, Rotterdam, pp 67–72

  • Chapelle G, Peck LS (1995) Acclimation and substratum effects on metabolism of the Antarctic amphipods Waldeckia obesa (Chevreux, 1905) and Bovallia gigantea (Pfeffer, 1888). Polar Biol 15:225–232

    Article  Google Scholar 

  • Clarke A (1988) Seasonality in the Antarctic marine environment. Comp Biochem Physiol 90B:461–473

    Google Scholar 

  • Clarke A, Johnston N (1999) Scaling of metabolic rate and temperature in teleost fish. J Anim Ecol 68:893–905

    Article  Google Scholar 

  • Clarke A, Leakey R (1996) The seasonal cycle of phytoplankton, macronutrients and microbial community in a nearshore Antarctic marine ecosystem. Limnol Oceanogr 41:1281–1294

    CAS  Google Scholar 

  • Coma R, Ribes M, Gili J-M, Zabala M (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453

    Article  PubMed  Google Scholar 

  • Coma R, Ribes M, Gili J-M, Zabala M (2001) Seasonality of in situ respiration rate in three temperate benthic suspension feeders. Limnol Oceanogr 47:324–331

    Google Scholar 

  • Davenport J (1988) Oxygen consumption and ventilation rate at low temperatures in the Antarctic Protobranch bivalve mollusc Yoldia (=Arquiyoldia) eightsi (Courthouy). Comp Biochem Physiol 90A:511–513

    Article  Google Scholar 

  • Dayton PK (1989) Interdecadal variation in an Antarctic sponge and its predators from oceanographic climate shifts. Science 245:1484–1486

    Google Scholar 

  • Dayton PK, Robilliard GA, Paine RT, Dayton LB (1974) Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol Monogr 44:105–128.

    Google Scholar 

  • Dyrynda PEJ (1981) a preliminary study of patterns of polypide generation-degeneration in marine cheilostome Bryozoa. In: Larwood GP, Nielsen C eds Recent and fossil Bryozoa. Olsen and Olsen, Fredensborg, pp 73–81

  • Dyrynda PEJ, Ryland JS (1982) Reproductive strategies and life histories in the cheilostome marine bryozoans Chartella papyracea and Bugula flabellata. Mar Biol 71:241–256

    Article  Google Scholar 

  • Emson R (1985) Bone idle, a recipe for success? In: Keegan BF, O’Connor BDS (eds) Echinodermata. Proceedings of the 5th International Echinoderm Conference.Balkema, Rotterdam, pp 25–30

  • Féral JP, Magniez P (1988) Relationship between rate of oxygen consumption and somatic and gonadal size in the subantarctic echinoid Abatus cordatus from Kerguelen. In: Burke RD, Mladenov PV, Lambert P, Parsley RL (eds) Proceedings of the 6th International echinoderm Conference. ( Balkema, Rotterdam, pp 581-587

  • Fraser KPP, Clarke A, Peck LS (2002) Feast and famine in Antarctica: seasonal physiology in the limpet Nacella concinna. Mar Ecol Prog Ser 242:169–177

    Google Scholar 

  • Gabbot P (1983) Developmental and seasonal metabolic activities in marine molluscs. In: Hochachka P, Wilbur K (eds) The mollusca, vol 2. Environmental biochemistry and physiology. ( Academic Press, New York, pp 165–217

  • Galéron J, Herman RL, Arnaud PM, Arntz WE, Hain S, Klages M (1992) Macrofaunal communities on the continental shelf and slope of the southeastern Weddell Sea, Antarctica. Polar biol 3:283–290

    Google Scholar 

  • Gatti S, Brey T, Müller WEG, Heilmayer O, Holst G (2002) Oxygen microoptodes: a new tool for oxygen measurements in aquatic animal ecology. Ber Polarforsch 434:37–57

    Google Scholar 

  • Gruzov EN (1977) Seasonal alterations in coastal communities in the Davies sea. In: Llano G (ed) Adaptations within ecosystems Smithsonian, Washington, D.C., pp 263–278

  • Harper E, Peck LS (2003). Feeding characteristics and metabolic costs in the Antarctic muricid gastropod Trophon longstaffi. Polar Biol 26:208–217

    Google Scholar 

  • Hayward PJ (1995) Antarctic Cheilostomatous Bryozoa. Oxford University Press, Oxford

  • Hemmingsen AM (1960) Energy metabolism as related to body size and respiratory surfaces, and its evolution. Reports of Steno Hospital 9:1-110

    Google Scholar 

  • Houlihan DF, Allan D (1982) Oxygen consmption of some Antarctic and British gastropods: and evaluation of cold adaptation. Comp Biochem Physiol 73A:383–387

    Article  Google Scholar 

  • Jaeckle WB (1994) Rates of energy consumption and acquisition by lecithotrophic larvae of Bugula neritina (Bryozoa, Cheilostomata). Mar Biol 119:517–523

    Article  Google Scholar 

  • James MA, Ansell AD, Collins MJ, Curry GB, Peck LS, Rhodes MC (1992) Recent advances in the study of living brachiopods. Adv Mar Biol 28:175–387

    Google Scholar 

  • Kowalke J (1999) Filtration in ascidians—striking a balance. J Exp Mar Biol Ecol 242:233–244

    Article  Google Scholar 

  • Kowalke J, Tatian M, Sahade R, Arntz WE (2001) Production and respiration of Antarctic ascidians. Polar Biol 24:663–669

    Article  Google Scholar 

  • Kühne S (1997) Solitäre Ascidien in der Potter Cove (King George Island, Antarktis). Ihre ökologische Bedeutung und Populationsdynamik. Rep Pol Res 252:1-153

    Google Scholar 

  • LaBarbera M (1986) The evolution and ecology of body size. In: Raup DM, Jablonski D (eds) Patterns and processes in the history of life. Dahlem Workshop Reports, Life Sciences Research Report 36. Springer, Berlin Heidelberg New York, pp 69–98

  • Lares MT, Pomory CM (1998) Use of body components during starvation in Lytechinus variegatus (Lamark)(Echinodermata: Echinoidea). J Exp Mar Biol Ecol 225:99–106

    Article  Google Scholar 

  • Lehtonen KK (1996) Ecophysiology of the benthic amphipod Monoporeia affinis in an open-sea area of the northern Baltic Sea: seasonal variations in oxygen consumption and ammonia excretion. Mar Biol 126:645-654

    Article  CAS  Google Scholar 

  • Luxmoore RA (1984) A comparison of the respiration rate of some Antarctic isopods with species from lower latitude. Br Antarct Surv Bull 62:53–65

    Google Scholar 

  • Munoz MR, Cancino JM (1989) Consequences of colony size on metabolic-rate of Cauloramphus spiniferum (Bryozoa). Rev Chil Hist Nat 62(2): 205–216

    Google Scholar 

  • Nakaya F, Saito Y, Motokawa T (2003) Switching of metabolic-rate scaling between allometry and isometry in colonial ascidians. Proc R Soc Lond B 270:1105–1113

    Article  Google Scholar 

  • Pearse JS (1969) Slow developing demersal embryos and larvae of the Antarctic sea star Odontaster validus. Mar Biol 3:110–116

    Article  Google Scholar 

  • Pearse JS, McClintock JB, Bosch I (1991) Reproduction in Antarctic benthic marine invertebrates: tempos, modes and timing. Am Zool 31:65–80

    Google Scholar 

  • Peck LS (1989) Temperature and basal metabolism in two Antarctic marine herbivores. J Exp Mar Biol Ecol 127:1–12

    Article  Google Scholar 

  • Peck LS (1996) Metabolism and feeding in the Antarctic brachiopod Liothyrella uva: a low energy lifestyle species with restricted metabolic scope. Proc R Soc Lond B 263:223–228

    CAS  Google Scholar 

  • Peck LS (1998) Feeding, metabolism and metabolic scope in Antarctic marine ectotherms. In: Pörtner HO, Playle RC (eds) Cold ocean physiology. Society for Experimental Biology Seminar Series 66. Cambridge University Press, Cambridge, pp 365–390

  • Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40

    Article  Google Scholar 

  • Peck LS, Barnes DKA (2003) Metabolic flexability: the key to long-term ecological success in Bryozoa? Proc R Soc Lond B [suppl] 271:18–21

    Google Scholar 

  • Peck LS, Conway LZ (2000) The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalves. In: Harper EM, Taylor JD, Crame JA (eds) The evolutionary biology of the Bivalvia. Special Publications 177, Geological Society, London, pp 441–445

  • Peck LS, Uglow R (1990) Two methods for assessing the oxygen content of small volumes of sea water. J Exp Mar Biol Ecol 141:53–62.

    Article  Google Scholar 

  • Peck LS, Whitehouse MJ (1992) An improved desorber design. for use in couloximetry. J Exp Mar Biol Ecol 163:163–167

    Article  Google Scholar 

  • Peck LS, Clarke A, Holmes LJ (1987). Summer metabolism and seasonal changes in biochemical composition of the Antarctic brachiopod Liuothyrella uva (Broderip, 1833). J Exp Mar Biol Ecol 114:85–97

    Article  Google Scholar 

  • Peck LS, Hayward P, Spencer-Jones M (1995) A pelagic bryozoan from Antarctica. Mar Biol 123:757–762

    Article  Google Scholar 

  • Peck LS, Brockington S, Brey T (1997) Growth and metabolism in the Antarctic brachiopod Liothyrella uva. Philos Trans R Soc Lond B 352:851–858

    Article  Google Scholar 

  • Pörtner HO, Peck LS, Zielinski S, Conway LZ (1999) Intracellular pH and energy metabolism in the highly stenothermal Antarctic bivalve Limopsis marionensis as a function of ambient temperature. Polar Biol 22:17–30

    Article  Google Scholar 

  • Pörtner HO (2002a) Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms. J Exp Biol 205:2217–2230

    PubMed  Google Scholar 

  • Pörtner HO (2002b) Environmental and functional limits to muscular exercise and body size in marine invertebrate athletes. Comp Biochem Physiol 133:303–321

    Google Scholar 

  • Ralph R, Maxwell JHG (1977) The oxygen consumption of the Antarctic limpet Nacella (Patinigera) concinna. Brit Antarct Surv Bull 45:19–23

    Google Scholar 

  • Rauschert M (1991) Ergebnisse der faunistischen Arbeiten im Benthal von King George Island (Südshetlandinseln, Antarktis). Ber Polarforsch 76:1–75

    Google Scholar 

  • Riisgard HU (1998) No foundation for a “3/4 power scaling law” for respiration in biology. Ecol Lett 1:71–73

    Article  Google Scholar 

  • Robertson RF, El-Haj AJ, Clarke A, Peck LS, Taylor EW (2001) The effects of temperature on metabolic rate and protein synthesis following a meal in the isopod Glyptonotus antarcticus Eights (1852). Polar Biol 24:677–686

    Article  Google Scholar 

  • Sahade R, Tatian M, Kowalke J, Kühne S, GB Esnal (1998) Benthic faunal associations on soft substrata at Potter Cove, South Shetland Islands, Antarctica. Polar Biol 19:85–91

    Article  Google Scholar 

  • Schmid M (1996) Oxygen consumption in Arctic marine invertebrates. Ber Polarforsch 94:1-102

    Google Scholar 

  • Schmidt-Nielsen K (1975) Scaling in biology: the consequences of size. J Exp Zool 194:287–308

    CAS  PubMed  Google Scholar 

  • Schmidt-Nielsen K (1983) Animal physiology. Cambridge university Press, Cambridge

  • Shabica SV (1976) The natural history of the Antarctic limpet Patinigera polaris (Hombron and Jacquinot). PhD thesis, Oregon State University, Corvallis

  • West GB, Brown JH, Enquist BJ (1999) The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284:1677–1679

    Article  CAS  PubMed  Google Scholar 

  • White MG (1975) Oxygen consumption and nitrogen excretion by the giant antarctic isopod Glyptonotus antarcticus Eights in relation to cold adapted metabolism in marine polar poikilotherms. In: Barnes H, (ed) European Marine Biology Symposium. Aberdeen University Press, pp 707–724

  • Winston JE (1983) Patterns of growth, reproduction and mortality in bryozoans from the Ross Sea, Antarctica. Bull Mar Sci 33:688–702

    Google Scholar 

  • Winston JE, Heimberg BF (1988) The role of bryozoans in the benthic community at Low Island, Antarctica. Antarctic J U S 21:188-189

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank all the base personnel at Rothera Base, particularly the diving officer and marine assistants. Finally, we would like to thank Dr Keiron Fraser, Prof. Andrew Clarke and two anonymous referees for comments leading to a much improved manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. K. A. Barnes.

Additional information

Communicated by J.P. Thorpe, Port Erin

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barnes, D.K.A., Peck, L.S. Extremes of metabolic strategy in Antarctic Bryozoa. Marine Biology 147, 979–988 (2005). https://doi.org/10.1007/s00227-005-1628-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-1628-3

Keywords

Navigation