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Ion regulatory capacity and the biogeography of Crustacea at high southern latitudes

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Abstract

Brachyuran and anomuran decapod crabs do not occur in the extremely cold waters of the Antarctic continental shelf whereas caridean and other shrimp-like decapods, amphipods and isopods are highly abundant. Differing capacities for extracellular ion regulation, especially concerning magnesium, have been hypothesised to determine cold tolerance and by that the biogeography of Antarctic crustaceans. Magnesium is known to have a paralysing effect, which is even more distinct in the cold. As only few or no data exist on haemolymph ionic composition of Sub-Antarctic and Antarctic crustaceans, haemolymph samples of 12 species from these regions were analysed for the concentrations of major inorganic ions (Na+, K+, Ca2+, Mg2+, Cl, SO4 2−) by ion chromatography. Cation relationships guaranteed neuromuscular excitability in all species. Sulphate and potassium correlated positively with magnesium concentration. The Antarctic caridean decapod as well as the amphipods maintained low (6–20% of ambient sea water magnesium concentration), Sub-Antarctic brachyuran and anomuran crabs as well as the Antarctic isopods high (54–96% of ambient sea water magnesium concentration) haemolymph magnesium levels. In conclusion, magnesium regulation may explain the biogeography of decapods, but not that of the peracarids.

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References

  • Arntz WE, Gutt J, Klages M (1997) Antarctic marine biodiversity: an overview. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 3–14

    Google Scholar 

  • Aronson RB, Thatje S, Clarke A, Peck LS, Blake DB, Wilga CD, Seibel BA (2007) Climate change and invasibility of the Antarctic benthos. Annu Rev Ecol Syst 38:129–154

    Article  Google Scholar 

  • Atkinson MJ, Bingman C (1997) Elemental composition of commercial seasalts. J Aquacult Aquat Sci 8:39–43

    Google Scholar 

  • Barnes D, Peck LS (2008) Vulnerability of Antarctic shelf biodiversity to predicted regional warming. Clim Res 37:149–163

    Article  Google Scholar 

  • Bock C, Frederich M, Wittig R-M, Pörtner HO (2001) Simultaneous observations of haemolymph flow and ventilation in marine spider crabs at different temperatures: a flow weighted MRI study. Magn Reson Imaging 19:1113–1124

    Article  CAS  PubMed  Google Scholar 

  • Brandt A (1999) On the origin and evolution of Antarctic Peracarida. Sci Mar 63:261–274

    Google Scholar 

  • Brey T, Dahm C, Gorny M, Klages M, Stiller M, Arntz WE (1996) Do Antarctic benthic invertebrates show an extended level of eurybathy? Antarct Sci 8:3–6

    Article  Google Scholar 

  • Burton RF (1995) Cation balance in crustacean haemolymph: relationship to cell membrane potentials and membrane surface charge. Comp Biochem Physiol A 111:125–131

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Clarke A, Barnes DKA, Hodgson DA (2005) How isolated is Antarctica? Trends Ecol Evol 20:1–3

    Article  PubMed  Google Scholar 

  • Clarke A, Griffiths HJ, Barnes DKA, Meredith MP, Grant SM (2009) Spatial variation in seabed temperatures in the Southern Ocean: implications for benthic ecology and biogeography. J Geophys Res 114:G03003. doi:10.1029/2008JG000886

    Article  Google Scholar 

  • Copeland DE, Fitzjarrell AT (1968) The salt absorbing cells in the gills of the blue crab (Callinectes sapidus Rathbun) with notes on modified mitochondria. Z Zellforsch 92:1–22

    Article  CAS  PubMed  Google Scholar 

  • Dall W (1974) Indices of nutritional state in the western rock lobster, Panulirus longipes (Milne Edwards). I. Blood and tissue constituents and water content. J Exp Mar Biol Ecol 16:167–180

    Article  CAS  Google Scholar 

  • Dunn TW, Mercier AJ (2003) Synaptic modulation by a neuropeptide depends on temperature and extracellular calcium. J Neurophysiol 89:1807–1814

    Article  CAS  PubMed  Google Scholar 

  • Eckert R, Randall D, Burggren WW, French K (2000) Tierphysiologie. Thieme, Stuttgart

    Google Scholar 

  • Feldmann RM, Zinsmeister WJ (1984a) First occurrence of fossil decapod crustaceans (Callianassidae) from the McMurdo Sound region, Antarctica. J Paleontol 58:1041–1045

    Google Scholar 

  • Feldmann RM, Zinsmeister WJ (1984b) New fossil crabs (Decapoda: Brachyura) from the La Meseta Formation (Eocene) of Antarctica: paleogeographic and biogeographic implications. J Paleontol 58:1046–1061

    Google Scholar 

  • Frederich M (1999) Ecophysiological limits to the geographical distribution of reptant decapod crustaceans in the Antarctic. Rep Polar Res 335

  • Frederich M, Pörtner HO (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in the spider crab, Maja squinado. Am J Physiol Regul Integr Comp Physiol R 279:1531–1538

    Google Scholar 

  • Frederich M, DeWachter B, Sartoris FJ, Pörtner HO (2000a) Cold tolerance and the regulation of cardiac performance and hemolymph distribution in Maja squinado (Crustacea: Decapoda). Physiol Biochem Zool 73:406–415

    Article  CAS  PubMed  Google Scholar 

  • Frederich M, Sartoris FJ, Arntz WE, Pörtner HO (2000b) Haemolymph Mg2+ regulation in decapod crustaceans: physiological correlates and ecological consequences in polar areas. J Exp Biol 203:1383–1393

    CAS  PubMed  Google Scholar 

  • Freire CA, Onken H, McNamara JC (2008) A structure-function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol A 151:272–304

    Article  Google Scholar 

  • F.-Tsukamoto Y, Kuwasawa K, Takeuchi S, Mano M (2000) Physiological saline suitable for the marine isopod crustacean Bathynomus doederleini. Zool Sci 17:425–430

    Google Scholar 

  • García Raso JE, Manjón-Cabeza ME, Ramos A, Olaso I (2005) New record of Lithodidae (Crustacea, Decapoda, Anomura) from the Antarctic (Bellingshausen Sea). Polar Biol 28:642–646

    Article  Google Scholar 

  • Gerencser GA, Ahearn GA, Zhang J, Cattey MA (2001) Sulfate transport mechanisms in epithelial systems. J Exp Zool 289:245–253

    Article  CAS  PubMed  Google Scholar 

  • Gorny M (1999) On the biogeography and ecology of the Southern Ocean decapod fauna. Sci Mar 63:367–382

    Article  Google Scholar 

  • Gutt J, Gorny M, Arntz WE (1991) Spatial distribution of Antarctic shrimps (Crustacea: Decapoda) by underwater photography. Antarct Sci 3:363–369

    Article  Google Scholar 

  • Gutt J, Sirenko BI, Smirnov IS, Arntz WE (2004) How many macrozoobenthic species might inhabit the Antarctic shelf? Antarct Sci 16:11–16

    Article  Google Scholar 

  • Hall S, Thatje S (2009) Global bottlenecks in the distribution of marine Crustacea: temperature constraints in the family Lithodidae. J Biogeogr. doi:10.1111/j.1365-2699.2009.02153.x

  • Heilmayer O, Thatje S, McClelland C, Conlan K, Brey T (2008) Changes in biomass and elemental composition during early ontogeny of the Antarctic isopod crustacean Ceratoserolis trilobitoides. Polar Biol 31:1325–1331

    Article  Google Scholar 

  • Held C (2000) Phylogeny and biogeography of serolid isopods (Crustacea, Isopoda, Serolidae) and the use of ribosomal expansion segments in molecular systematics. Mol Phylogen Evol 15:165–178

    Article  CAS  Google Scholar 

  • Iseri LT, French JH (1984) Magnesium: nature’s physiologic calcium blocker. Am Heart J 108:188–193

    Article  CAS  PubMed  Google Scholar 

  • Janssen HH, Hoese B (1993) Marsupium morphology and brooding biology of the Antarctic giant isopod Glyptonotus antarcticus Eights 1853 (Crustacea, Isopoda, Chaetiliidae). Polar Biol 13:145–149

    Article  Google Scholar 

  • Katz B (1936) Neuro-muscular transmission in crabs. J Physiol 87:199–221

    CAS  PubMed  Google Scholar 

  • Khodabandeh S, Charmantier G, Charmantier-Daures M (2005) Ultrastructural Studies and Na+, K+-ATPase immunolocalization in the antennal urinary glands of the lobster Homarus gammarus (Crustacea, Decapoda). J Histochem Cytochem 53:1203–1214

    Article  CAS  PubMed  Google Scholar 

  • Kiko R, Werner I, Wittmann A (2009) Osmotic and ionic regulation in response to salinity variations and cold resistance in the Arctic under-ice amphipod Apherusa glacialis. Polar Biol 32:393–398

    Article  Google Scholar 

  • Lawver LA, Gahagan LM (2003) Evolution of Cenozoic seaways in the circum-Antarctic region. Palaeogeogr Palaeoclimatol Palaeoecol 198:11–38

    Article  Google Scholar 

  • Lee C, Zhang X, Kwan WF (1996) Electromyographic and mechanomyographic characteristics of neuromuscular block by magnesium sulphate in the pig. Br J Anaesth 76:278–283

    CAS  PubMed  Google Scholar 

  • Locarnini RA, Mishonov AV, Antonov JI, Boyer TP, Garcia HE (2006) Temperature. In: Levitus S (ed) World Ocean Atlas 2005, vol 1. U.S. Government Printing Office, Washington D.C.

    Google Scholar 

  • Lucu C, Towle DW (2003) Na++K+-ATPase in gills of aquatic crustacea. Comp Biochem Physiol A 135:195–214

    Google Scholar 

  • Luxmoore RA (1982) The reproductive biology of some serolid isopods from the Antarctic. Polar Biol 1:3–11

    Article  Google Scholar 

  • Mackay WC, Prosser CL (1970) Ionic and osmotic regulation in the king crab and two other North Pacific crustaceans. Comp Biochem Physiol 34:273–280

    Article  CAS  PubMed  Google Scholar 

  • Mantel LH, Farmer LL (1983) Osmotic and ionic regulation. In: Bliss DE (ed) The biology of Crustacea, vol 5. Academic Press, New York, pp 53–161

    Google Scholar 

  • McAllen R, Taylor A, Freel J (2005) Seasonal variation in the ionic and protein content of haemolymph from seven deep-sea decapod genera from the Northeast Atlantic Ocean. Deep Sea Res (1 Oceanogr Res Pap) 52:2017–2028

    Article  Google Scholar 

  • Mileikovsky SA (1971) Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a re-evaluation. Mar Biol 10:193–213

    Article  Google Scholar 

  • Morritt D, Spicer JI (1993) A brief re-examination of the function and regulation of extracellular magnesium and its relationship to activity in crustacean arthropods. Comp Biochem Physiol A 106:19–23

    Article  Google Scholar 

  • Neufeld GJ, Holliday CW, Pritchard JB (1980) Salinity adaptation of gill Na, K-ATPase in the blue crab, Callinectes sapidus. J Exp Zool 211:215–224

    Article  CAS  Google Scholar 

  • Normant M, Kubicka M, Lapucki T, Czarnowski W, Michalowska M (2005) Osmotic and ionic haemolymph concentrations in the Baltic Sea amphipod Gammarus oceanicus in relation to water salinity. Comp Biochem Physiol A 141:94–99

    Article  Google Scholar 

  • Orsi AH, Whitworth T, Nowlin WD (1995) On the meridional extent and fronts of the Antarctic Circumpolar Current. Deep-Sea Res (1 Oceanogr Res Pap) 42:641–673

    Article  Google Scholar 

  • Pantin CFA (1948) Notes on microscopocal techniques for zoologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Parnas H, Parnas I, Ravin R, Yudelevitch B (1994) Glutamate and N-methyl-d-aspartate affect release from crayfish axon terminals in a voltage-dependent manner. Proc Natl Acad Sci USA 91:11586–11590

    Article  CAS  PubMed  Google Scholar 

  • Parry G (1953) Osmotic and ionic regulation in the isopod crustacean Ligia oceanica. J Exp Biol 30:567–574

    CAS  Google Scholar 

  • Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761

    Google Scholar 

  • Poulin E, Palma AT, Feral JP (2002) Evolutionary versus ecological success in Antarctic benthic invertebrates. Trends Ecol Evol 17:218–222

    Article  Google Scholar 

  • Richmond J, Sher E, Keller R, Haylett B, Reichwein B, Cooke I (1995) Regulation of calcium currents and secretion by magnesium in crustacean peptidergic neurons. Invertebr Neurosci 1:215–221

    Article  CAS  Google Scholar 

  • Robertson JD (1953) Further studies on ionic regulation in marine invertebrates. J Exp Biol 30:277–296

    CAS  Google Scholar 

  • Robertson JD (1960) Ionic regulation in the crab Carcinus maenas (L.) in relation to the moulting cycle. Comp Biochem Physiol 1:183–212

    Article  CAS  Google Scholar 

  • Ruppert EE, Barnes RD (1994) Invertebrate zoology, 6th edn. Saunders College Publishing, Orlando

    Google Scholar 

  • Sartoris FJ, Pörtner HO (1997a) Increased concentrations of haemolymph Mg2+ protect intracellular pH and ATP levels during temperature stress and anoxia in the common shrimp Crangon crangon. J Exp Biol 200:785–792

    CAS  PubMed  Google Scholar 

  • Sartoris FJ, Pörtner HO (1997b) Temperature dependence of ionic and acid-base regulation in boreal and arctic Crangon crangon and Pandalus borealis. J Exp Mar Biol Ecol 211:69–83

    Article  CAS  Google Scholar 

  • Sartoris FJ, Frederich M, Pörtner HO (1997) Does the capability to regulate magnesium determine the composition of the Antarctic crustacean fauna? Verh Dtsch Zool Ges 90:144

    Google Scholar 

  • Spicer JI, Morritt D, Taylor AC (1994) Effect of low temperature on oxygen uptake and haemolymph ions in the sandhopper Talitrus saltator (Crustacea: Amphipoda). J Mar Biol Assoc UK 74:313–321

    Article  CAS  Google Scholar 

  • Taylor AC, Moore PG (1995) The burrows and physiological adaptations to a burrowing lifestyle of Natatolana borealis (Isopoda: Cirolanidae). Mar Biol 123:805

    Article  Google Scholar 

  • Tentori E, Lockwood APM (1990) Haemolymph magnesium levels in some oceanic Crustacea. Comp Biochem Physiol A 95:545–548

    Article  Google Scholar 

  • Thatje S, Fuentes V (2003) First record of anomuran and brachyuran larvae (Crustacea: Decapoda) from Antarctic waters. Polar Biol 26:279–282

    Google Scholar 

  • Thatje S, Schnack-Schiel S, Arntz WE (2003) Developmental trade-offs in Subantarctic meroplankton communities and the enigma of low decapod diversity in high southern latitudes. Mar Ecol Prog Ser 260:195–207

    Article  Google Scholar 

  • Thatje S, Anger K, Calcagno GA, Lovrich GA, Pörtner HO, Arntz WE (2005) Challenging the cold: crabs reconquer the Antarctic. Ecology 86:619–625

    Article  Google Scholar 

  • Thatje S, Hall S, Hauton C, Held C, Tyler P (2008) Encounter of lithodid crab Paralomis birsteini on the continental slope off Antarctica, sampled by ROV. Polar Biol 31:1143–1148

    Article  Google Scholar 

  • Walters NJ, Uglow RF (1981) Haemolymph magnesium and relative heart activity of some species of marine decapod crustaceans. J Exp Mar Biol Ecol 55:255–265

    Article  CAS  Google Scholar 

  • Waterman TH (1941) A comparative study of the effects of ions on whole nerve and isolated single nerve fiber preparations of crustacean neuromuscular systems. J Cell Comp Physiol 18:109–126

    Article  CAS  Google Scholar 

  • Watt AJS, Whiteley NM, Taylor EW (1999) An in situ study of respiratory variables in three British sublittoral crabs with different routine rates of activity. J Exp Mar Biol Ecol 239:1–21

    Article  Google Scholar 

  • Young JS, Peck LS, Matheson T (2006) The effects of temperature on walking and righting in temperate and Antarctic crustaceans. Polar Biol 29:978–987

    Article  Google Scholar 

  • Zanders IP (1980) The control of magnesium and sulphate excretion in Carcinus maenas (L.). Comp Biochem Physiol A 66:69–76

    Article  Google Scholar 

  • Ziegler A, Grospietsch T, Carefoot TH, Danko JP, Zimmer M, Zerbst-Boroffka I, Pennings SC (2000) Hemolymph ion composition and volume changes in the supralittoral isopod Ligia pallasii Brandt, during molt. J Comp Physiol B 170:329–336

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Timo Hirse and Florian Leese for sample collection. We greatly appreciate the help of the crew of RV Polarstern during the transport of live animals. The experiments comply with the current laws of the country in which they were performed. This study was supported by Deutsche Forschungsgemeinschaft grants no. SA 1713 and He 3391/3 and by National Science Foundation grant no. OPP V01-32032. This is publication 25 of the ICEFISH cruise 2004.

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Wittmann, A.C., Held, C., Pörtner, H.O. et al. Ion regulatory capacity and the biogeography of Crustacea at high southern latitudes. Polar Biol 33, 919–928 (2010). https://doi.org/10.1007/s00300-010-0768-1

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  • DOI: https://doi.org/10.1007/s00300-010-0768-1

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