Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T09:55:54.118Z Has data issue: false hasContentIssue false

Onshore–offshore distribution of Thecosomata (Gastropoda) in the Benguela Current upwelling region off Namibia: species diversity and trophic position

Published online by Cambridge University Press:  26 March 2013

Rolf Koppelmann*
Affiliation:
Universität Hamburg, Centrum für Erdsystemforschung und Nachhaltigkeit, Institut für Hydrobiologie und Fischereiwissenschaft, Große Elbstraße 133, 22767 Hamburg, Germany
Björn Kullmann
Affiliation:
Universität Hamburg, Centrum für Erdsystemforschung und Nachhaltigkeit, Institut für Hydrobiologie und Fischereiwissenschaft, Große Elbstraße 133, 22767 Hamburg, Germany
Niko Lahajnar
Affiliation:
Universität Hamburg, Centrum für Erdsystemforschung und Nachhaltigkeit, Institut für Biogeochemie und Meereschemie, Bundesstraße 55, 20146 Hamburg, Germany
Bettina Martin
Affiliation:
Universität Hamburg, Centrum für Erdsystemforschung und Nachhaltigkeit, Institut für Hydrobiologie und Fischereiwissenschaft, Große Elbstraße 133, 22767 Hamburg, Germany
Volker Mohrholz
Affiliation:
Leibniz-Institut für Ostseeforschung Warnemünde, Seestraße 15, 18119 Rostock, Germany
*
Correspondence should be addressed to: Rolf Koppelmann, Universität Hamburg, Centrum für Erdsystemforschung und Nachhaltigkeit, Institut für Hydrobiologie und Fischereiwissenschaft, Große Elbstraße 133, 22767 Hamburg, Germany email: rolf.koppelmann@uni-hamburg.de

Abstract

Many Thecosomata (Gastropoda) produce an aragonite shell and are potentially threatened by the increasing ocean acidification. Information about these species is very important for future monitoring of the fate of this group. This paper investigates the distribution, species composition and trophic role of Thecosomata along a transect from the coast into the open ocean off Walvis Bay, Namibia, in September 2010 and January/February 2011. Twenty species were detected, but three taxa (Limacina bulimoides, Limacina inflata and Desmopterus papilio) dominated the community with more than 80% of the total standing stock. Diel vertical migration was observed for both Limacina taxa with higher concentrations in surface waters during night. Desmopterus papilio revealed almost no day/night differences. The highest diversities and abundances were detected at the slope and offshore stations, indicating the oceanic preference of this group; some taxa aggregated at the shelf–open ocean interface. δ15N measurements confirmed the first trophic level of this group; however, significant differences were detected between seasons with higher values in February 2011. This can be related to differences in seston values as the primary food source. Possible biogeochemical causes for these differences like an exhaustion of the nitrate pool or denitrification processes under suboxic conditions are discussed.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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

REFERENCES

Alldredge, A.L. and Silver, M.W. (1988) Characteristics, dynamics and significance of marine snow. Progress in Oceanography 20, 4182.CrossRefGoogle Scholar
Angel, M.V. and Pugh, P.R. (2000) Quantification of diel vertical migration by micronektonic taxa in the northeast Atlantic. Hydrobiologia 440, 161179.CrossRefGoogle Scholar
Bank, M.G. van der, Utme-Palm, A.C., Pittman, K., Sweetman, A.K., Richoux, N.B., Brüchert, V. and Gibbons, M.J. (2011) Dietary success of a new key fish in an overfished ecosystem: evidence from fatty acid and stable isotope signatures. Marine Ecology Progress Series 428, 219233.CrossRefGoogle Scholar
Batistic, M., Krsinic, F., Jasprica, N., Graric, M., Vilicic, D. and Lucic, D. (2004) Gelatinous invertebrate zooplankton of the South Adriatic: species composition and vertical distribution. Journal of Plankton Research 26, 459474.CrossRefGoogle Scholar
, A.W. and Gilmer, R.W. (1977) A zoogeographic and taxonomic review of euthecosomatous Pteropoda. In Ramsay, A.T.S. (ed.) Oceanic micropaleontology. London: Academic Press, pp. 733808.Google Scholar
Berner, R.A. and Honjo, S. (1981) Pelagic sedimentation of aragonite—its geochemical significance. Science 211, 940942.CrossRefGoogle ScholarPubMed
Betzer, P.R., Byrne, R.H., Acker, J.G., Lewis, C.S., Jolley, R.R. and Feely, R.A. (1984) The oceanic carbonate system—a reassessment of biogenic control. Science 226, 10741077.CrossRefGoogle Scholar
Bouchet, P., Rocroi, J.P., Fryda, J., Hausdorf, B., Ponder, W., Valdes, A. and Waren, A. (2005) Classification and nomenclature of gastropod families. Malacologia 47, 1368.Google Scholar
Broecker, W.S. and Peng, T.H. (1982) Tracers in the sea. Palisades, NY: Lamont–Doherty Geological Observatory, Columbia University.Google Scholar
Broecker, W.S. and Takahashi, T. (1977) Neutralization of fossil fuel CO2 by marine calcium carbonate. In Andersen, N.R. and Malahoff, A. (eds) Fate of fossil fuel in the oceans. New York: Plenum Press, pp. 213241.CrossRefGoogle Scholar
Bruland, K.W. and Silver, M.W. (1981) Sinking rates of fecal pellets from gelatinous zooplankton (salps, pteropods, doliolods). Marine Biology 63, 295300.CrossRefGoogle Scholar
Checkley, D.M. and Miller, C.A. (1989) Nitrogen isotope fractionation by oceanic zooplankton. Deep-Sea Research I 36, 14491456.CrossRefGoogle Scholar
Chen, C. and , A.W.H. (1964) Seasonal distribution of euthecosomatous pteropods in the surface waters of five stations in the western North Atlantic. Bulletin of Marine Science of the Gulf and Caribbean 14, 185220.Google Scholar
Cline, J.D. and Kaplan, I.R. (1975) Isotopic fractionation of dissolved nitrate during denitrification in the eastern tropical North Pacific Ocean. Marine Chemistry 3, 271299.CrossRefGoogle Scholar
Cohen, A.L. and Holcomb, M. (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22, 118127.CrossRefGoogle Scholar
Comeau, S., Gorsky, G., Jeffree, R., Teyssie, J.-L. and Gattuso, J.-P. (2009) Impact of ocean acidification on a key Arctic pelagic molusc (Limacina helicina). Biogeosciences 6, 18771882.CrossRefGoogle Scholar
Comeau, S., Gorsky, G., Alliouane, S. and Gattuso, J.P. (2010) Larvae of the pteropod Cavolinia inflexa exposed to aragonite undersaturation are viable but shell-less. Marine Biology 157, 23412345.CrossRefGoogle Scholar
Dadon, J.R. and Masello, J.F. (1999) Mechanisms generating and maintaining the admixture of zooplanktonic molluscs (Euthecosomata: Opistobranchiata: Gastropoda) in the Subtropical Front of the South Atlantic. Marine Biology 135, 171179.CrossRefGoogle Scholar
Dittmar, T. and Birkicht, M. (2001) Regeneration of nutrients in the northern Benguela upwelling and the Angola–Benguela Front areas. South African Journal of Science 97, 239246.Google Scholar
Emeis, K.-C., Struck, U., Leipe, T. and Ferdelman, T.G. (2009) Variability in upwelling intensity and nutrient regime in the coastal upwelling system offshore Namibia: results from sediment archives. International Journal of Earth Sciences 98, 309326.CrossRefGoogle Scholar
Fabry, V.J., Seibel, B.A., Feely, R.A. and Orr, J.C. (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65, 414432.CrossRefGoogle Scholar
Feely, R.A., Sabine, C.L., Lee, K., Berelson, W., Kleypas, J., Fabry, V.J. and Millero, F.J. (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362366.CrossRefGoogle ScholarPubMed
Feely, R.A., Sabine, C.L., Hernandez-Ayon, J.M., Ianson, D. and Hales, B. (2008) Evidence for upwelling of corrosove ‘acidified’ water onto the continental shelf. Science 320, 14901492.CrossRefGoogle ScholarPubMed
Flynn, K.J., Richardson, A.J., Brierley, A.S., Boyer, D.C., Axelsen, B.E., Scott, L., Moroff, N.E., Kainge, P.I., Tjizoo, B.M. and Gibbons, M.J. (2012) Temporal and spatial patterns in the abundance of jellyfish in the northern Benguela upwelling ecosystem and their link to thwarted pelagic fishery recovery. African Journal of Marine Science 34, 151–146.CrossRefGoogle Scholar
Gilmer, R.W. (1974) Some aspects of feeding in thecosomatous pteropod molluscs. Journal of Experimental Marine Biology and Ecology 15, 127144.CrossRefGoogle Scholar
Glaçon, G., Rampal, J., Gaspard, D., Guillaumin, D. and Staerker, T.S. (1994) Thecosomata (pteropods) and their remains in late Quaternary deposits on the Bougainville Guyot and the Central New Hebrides Island Arc. Proceedings of the Ocean Drilling Program 134, 319336.Google Scholar
Hagen, E., Feistel, R., Agenbag, J.J. and Ohde, T. (2001) Seasonal and interannual changes in intense Benguela Upwelling (1982–1999). Oceanologica Acta 24, 557568.CrossRefGoogle Scholar
Hansen, F.C., Cloete, R.R. and Verheye, H.M. (2005) Seasonal and spatial variabilty of dominant copepods along a transect off Walvis Bay (23°S), Namibia. African Journal of Marine Science, 27, 5563.CrossRefGoogle Scholar
Heymans, J.J., Shannon, L.J. and Jarre, A. (2004) Changes in the northern Benguela ecosystem over three decades: 1970s, 1980s, and 1990s. Ecological Modelling 172, 175195.CrossRefGoogle Scholar
Hobson, K.A. and Welch, H.E. (1992) Determination of trophic relationships within a high Artic marine food web using delta13C and delta15N analysis. Marine Ecology Progress Series 84, 918.CrossRefGoogle Scholar
Holmes, E.M., Müller, P.J., Schneider, R.R., Segl, M., Pätzold, J. and Wefer, G. (1996) Stable nitrogen isotopes in Angola Basin surface sediments. Marine Geology 134, 112.CrossRefGoogle Scholar
Howard, W.R., Roberts, D., Moy, A.D., Lindsay, M.C.M., Hopcroft, R.R., Trull, T.W. and Bray, S.G. (2011) Distribution, abundance and seasonal flux of pteropods in the Sub-Antarctic Zone. Deep-Sea Research II 58, 22932300.CrossRefGoogle Scholar
Hüneke, H. and Henrich, R. (2011) Pelagic sedimentation in modern and ancient oceans. In Hüneke, H. and Mulder, T. (eds) Developments in sedimentology—Deep-Sea Sediments. Volume 63. Amsterdam: Elsevier, pp. 215351.CrossRefGoogle Scholar
Hunt, B.P.V., Pakhomov, E.A., Hosie, G.W., Siegel, V., Ward, P. and Bernard, K. (2008) Pteropods in Southern Ocean ecosystems. Progress in Oceanography 78, 193221.CrossRefGoogle Scholar
Hutchings, L., Verheye, H.M., Huggett, J.A., Demarcq, H., Cloete, R., Barlow, R.G., Louw, D. and Silva, A. da (2006) Variabilty of plankton with reference to fish variability in the Benguela Current Large Marine Ecosystem—an overview. Large Marine Ecosystems 14, 91124.CrossRefGoogle Scholar
Hutchings, L., van der Lingen, C.D., Shannon, L.J., Crawford, R.J.M., Verheye, H.M.S., Bartholomae, C.H., Plas, A.K. van der, Louw, D., Kreiner, A., Ostrowski, M., Fidel, Q., Barlow, R.G., Lamont, T., Coetzee, J., Shillington, F., Veitch, J., Currie, J.C. and Monteiro, P.M.S. (2009) The Benguela Current: an ecosystem of four components. Progress in Oceanography 83, 1532.CrossRefGoogle Scholar
Klussmann-Kolb, A. and Dinapoli, A. (2006) Systematic position of the pelagic Thecosomata and Gymnosomata within Opisthobranchia (Mollusca, Gastropoda)—revival of the Pteropoda. Journal of Zoological Systematics and Evolution Research 44, 118129.CrossRefGoogle Scholar
Koppelmann, R., Schäfer, P. and Schiebel, R. (2000) Organic carbon losses measured by heterotrophic activity of mesozooplankton and CaCO3 flux in the bathypelagic zone of the Arabian Sea. Deep-Sea Research II 47, 169187.CrossRefGoogle Scholar
Kostadinov, T.S., Siegel, D.A. and Maritorena, S. (2010) Global variability of phytoplankton functional types from space: assessment via the particle size distribution. Biogeosciences 7, 32393257.CrossRefGoogle Scholar
Lalli, C.M. and Gilmer, R.W. (1989) Pelagic snails: the biology of holoplanktonic gastropod molluscs. Palo Alto, CA: Stanford University Press.CrossRefGoogle Scholar
Lalli, C.M. and Wells, F.E. (1973) Brood protection in an epipelagic thecosomatous pteropod, Spiratella (Limacina) inflata (d'Orbigny). Bulletin of Marine Science 23, 933941.Google Scholar
Lalli, C.M. and Wells, F.E. (1978) Reproduction in genus Limacina (Opisthobranchia Thecosomata). Journal of Zoology 186, 95108.CrossRefGoogle Scholar
Lampitt, R.S. and Antia, A.N. (1997) Particle flux in deep seas: regional characteristics and temporal variability. Deep-Sea Research I 44, 13771403.CrossRefGoogle Scholar
Maas, A.E., Wishner, K.F. and Seibel, B.A. (2012a) The metabolic response of pteropods to acidification reflects natural CO2-exposure in oxygen minimum zones. Biogeosciences 9, 747757.CrossRefGoogle Scholar
Maas, A.E., Wishner, K. and Seibel, B.A. (2012b) Metabolic suppression in thecosomatous pteropods as an effect of low temperature and hypoxia in the eastern tropical North Pacific. Marine Biology 159, 19551967.CrossRefGoogle Scholar
Mackas, D.L. and Galbraith, M.D. (2012) Pteropod time-series from the NE Pacific. ICES Journal of Marine Science 69, 448459.CrossRefGoogle Scholar
Manno, C., Tirelli, V., Accornero, A. and Umani, S.F. (2010) Importance of the contribution of Limacina helicina faecal pellets to the carbon pump in Terra Nova Bay (Antarctica). Journal of Plankton Research 32, 145152.CrossRefGoogle Scholar
McGowan, J.A. (1968) The Thecosomata and Gymnosomata of California. Veliger 3, 102129.Google Scholar
Meehl, G.A., Stocker, T.F., Collins, W.D., Friedlingstein, P., Gaye, A.T., Gregory, J.M., Kitoh, A., Knutti, R., Murphy, J.M., Noda, A., Raper, S.C.B., Watterson, I.G., Weaver, A.J. and Zhao, Z.-C. (2007) Global climate projections. In Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M. and Miller, H.L. (eds) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, pp. 747845.Google Scholar
Minagawa, M. and Wada, E. (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 11351140.CrossRefGoogle Scholar
Mohrholz, V., Bartholomae, C.H., Plas, A.K van der. and Lass, H.U. (2008) The seasonal variability of the northern Benguela undercurrent and its relation to the oxygen budget on the shelf. Continental Shelf Research 28, 424441.CrossRefGoogle Scholar
Montoya, J.P., Carpenter, E.J. and Capone, D.G. (2002) Nitrogen fixation and nitrogen isotope abundance in zooplankton of the oligotrophic North Atlantic. Limnology and Oceanography 47, 16171628.CrossRefGoogle Scholar
Morton, J.E. (1954) The pelagic Mollusca of the Benguela current. I. First survey R.R.S. William Scoresby March 1950 with an account of the reproductive system and sexual succession of Limacina bulimoides. Discovery Report 27, 163199.Google Scholar
Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R.M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R.G., Plattner, G.-K., Rodgers, K.B., Sabine, C.L., Sarmiento, J.L., Schlitzer, R., Slater, R.D., Totterdell, I.J., Weirig, M.-F., Yamanaka, Y. and Yool, A. (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681686.CrossRefGoogle ScholarPubMed
Pakhomov, E.A. and Froneman, P.W. (2004) Zooplankton dynamics in the eastern Atlantic sector of the Southern Ocean during the austral summer 1997/1998—Part 1: community structure. Deep-Sea Research II 51, 25992616.CrossRefGoogle Scholar
Parra-Flores, A. and Gasca, R. (2009) Distribution of pteropods (Mollusca: Gastropoda: Thecosomata) in surface waters (0–100 m) of the Western Caribbean Sea (winter, 2007). Revista de Biologia Marina y Oceanografia 44, 647662.Google Scholar
Perry, R.I., Harding, G.C., Loder, J.W., Tremblay, M.J., Sinclair, M.M. and Drinkwater, K.F. (1993) Zooplankton distribution at the Georges Bank frontal system: retention or dispersion? Continental Shelf Research 13, 357383.CrossRefGoogle Scholar
Pichevin, L., Martinez, P., Bertrand, P., Schneider, R., Giraudeau, J. and Emeis, K. (2005) Nitrogen cycling on the Namibian shelf and slope over the last two climatic cycles: local and global forcings. Paleoceanography 20, 1424.CrossRefGoogle Scholar
Pielou, E.C. (1966) Shannon's formula as a measure of specific diversity: its use and disuse. American Naturalist 100, 463465.CrossRefGoogle Scholar
Ponder, W. and Lindberg, D.R. (1997) Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. Zoological Journal of the Linnean Society 119, 83265.CrossRefGoogle Scholar
Rottman, M. (1976) Euthecosomatous pteropods (Mollusca) in the Gulf of Thailand and the South China Sea: seasonal distribution and species associations. Naga Report 4, 1117.Google Scholar
Royal, Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy document 12/05, London.Google Scholar
Sakthivel, M. (1977) Further-studies of plankton ecosystems in eastern Indian-Ocean, 8. Seasonal, diurnal, and latitudinal variations in abundance of Euthecosomata along 110-degrees-E meridian. Australian Journal of Marine and Freshwater Research 28, 663671.CrossRefGoogle Scholar
Sánchez-Bidalgo y Anda, M. (1994) Distribución y abundancia de los Thecosomata (Gastropoda) recolectados con red Calvet en Agosto de 1985, frente a Bahía Magdalena, Baja Califonia Sur, México. Investigaciones Marinas CICIMAR 9, 6377.Google Scholar
Seibel, B.A. and Dierssen, H.M. (2003) Cascading trophic impacts of reduced biomass in the Ross Sea, Antarctica: just the tip of the iceberg? Biological Bulletin. Marine Biological Laboratory, Woods Hole 205, 9397.CrossRefGoogle ScholarPubMed
Shannon, C.E. and Weaver, W. (1949) The mathematical theory of communication. Champaign, IL: University of Illinois Press.Google Scholar
Shannon, L.V. (1985) The Benguela ecosystem. Part I. Evolution of the Benguela, physical features and processes. Oceanography and Marine Biology: an Annual Review 23, 105182.Google Scholar
Simpson, E.H. (1949) Measurement of diversity. Nature 163, 688.CrossRefGoogle Scholar
Sohm, J.A., Hilton, J.A., Noble, A.E., Zehr, J.P., Saito, M.A. and Webb, E.A. (2011) Nitrogen fixation in the South Atlantic Gyre and the Benguela Upwelling System. Geophysical Research Letters 38. doi:10.1029/2011GL048315.CrossRefGoogle Scholar
Spoel, S. van der (1996) Pteropoda. In Gasca, R. and Suárez-Morales, E. (eds) Introducción al estudio del zooplancton marino. México: ECOSUR/CONACYT, pp. 459528.Google Scholar
Spoel, S. van der and Dadon, J.R. (1999) Pteropoda. In Boltovskoy, D. (ed.) South Atlantic zooplankton. Leiden: Backhuys Publishers, pp. 649706.Google Scholar
Spoel, S. van der and Pierrot-Bults, A. (1979) Zoogeography of the Pacific Ocean. In Spoel, S. van der and Pierrot-Bults, A. (eds) Zoogeography and diversity of plankton. New York: Halted Press, pp. 193327.Google Scholar
Steedman, H.F. (1976) Zooplankton fixation and preservation. UNESCO Monographs on Oceanographic Methodology. Paris: Unesco Press, pp. 103154.Google Scholar
Tesch, J.J. (1946) The thecosomatous pteropods: I. The Atlantic. Dana Report 28, 182.Google Scholar
Turley, C., Eby, M., Ridgwell, A.J., Schmidt, D.N., Findlay, H.S., Brownlee, C., Riebesell, U., Fabry, V.J., Feely, R.A. and Gattuso, J.P. (2010) The societal challenge of ocean acidification. Marine Pollution Bulletin 60, 787792.CrossRefGoogle ScholarPubMed
Tyrrell, T. and Lucas, M.I. (2002) Geochemical evidence of denitrification in the Benguela Upwelling system. Continental Shelf Research 22, 24792511.CrossRefGoogle Scholar
Verheye, H.M., Richardson, A.J., Hutchings, L., Marska, G. and Gianakouras, D. (1998) Long-term trends in the abundance and community structure of the coastal zooplankton in the southern Benguela system, 1951–1996. South African Journal of Marine Science 19, 317332.CrossRefGoogle Scholar
Wada, E. and Hattori, A. (1978) Nitrogen isotope effects in the assimilation of inorganic nitrogenous compounds by marine diatoms. Geomicrobiology Journal 1, 85101.CrossRefGoogle Scholar
Wall-Palmer, D., Hart, M.B., Smart, C.W., Sparks, R.S.J., Friant, A. le, Boudon, G., Deplus, C. and Komorowski, J.C. (2012) Pteropods from the Caribian Sea: variation in calcification as an indicator of past ocean carbonate saturation. Biogeosciences 9, 309315.CrossRefGoogle Scholar
Waser, N.A.D., Harrison, P.J., Nielsen, B., Calvert, S.E. and Turpin, D.H. (1998) Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium, and urea by a marine diatom. Limnology and Oceanography 43, 215224.CrossRefGoogle Scholar
Wiebe, P.H., Morton, A.W., Bradley, A.M., Backus, R.H., Craddock, J.E., Barber, V., Cowles, T.J. and Flierl, G.R. (1985) New developments in the MOCNESS, an apparatus for sampling zooplankton and micronekton. Marine Biology 87, 313323.CrossRefGoogle Scholar
Xu, Z. and Li, C. (2006) Study on abundance variation of pteropods in the East China Sea. Acta Oceanologica Sinica 25, 100107.Google Scholar
Yool, A., Martin, A.P., Fernàndez, C. and Clark, D.R. (2007) The significance of nitrification for oceanic new production. Nature 447, 9991002.CrossRefGoogle ScholarPubMed
Supplementary material: File

Koppelmann et al. supplementary material

Supplementary tables

Download Koppelmann et al. supplementary material(File)
File 203.8 KB