Marine Biology

, Volume 154, Issue 5, pp 899–909 | Cite as

Temporal and spatial variability in stable isotope ratios of SPM link to local hydrography and longer term SPM averages suggest heavy dependence of mussels on nearshore production

  • Jaclyn M. HillEmail author
  • Christopher D. McQuaid
  • Sven Kaehler
Original Paper


Temporal changes in hydrography affect suspended particulate matter (SPM) composition and distribution in coastal systems, potentially influencing the diets of suspension feeders. Temporal variation in SPM and in the diet of the mussel Perna perna, were investigated using stable isotope analysis. The δ13C and δ15 N ratios of SPM, mussels and macroalgae were determined monthly, with SPM samples collected along a 10 km onshore–offshore transect, over 14 months at Kenton-on-Sea, on the south coast of South Africa. Clear nearshore (0 km) to offshore (10 km) carbon depletion gradients were seen in SPM during all months and extended for 50 km offshore on one occasion. Carbon enrichment of coastal SPM in winter (June–August 2004 and May 2005) indicated temporal changes in the nearshore detrital pool, presumably reflecting changes in macroalgal detritus, linked to local changes in coastal hydrography and algal seasonality. Nitrogen patterns were less clear, with SPM enrichment seen between July and October 2004 from 0 to 10 km. Nearshore SPM demonstrated cyclical patterns in carbon over 24-h periods that correlated closely with tidal cycles and mussel carbon signatures, sampled monthly, demonstrated fluctuations that could not be correlated to seasonal or monthly changes in SPM. Macroalgae showed extreme variability in isotopic signatures, with no discernable patterns. IsoSource mixing models indicated over 50% reliance of mussel tissue on nearshore carbon, highlighting the importance of nearshore SPM in mussel diet. Overall, carbon variation in SPM at both large and small temporal scales can be related to hydrographic processes, but is masked in mussels by long-term isotope integration.


Phytoplankton Macroalgae Suspend Particulate Matter Agulhas Current Suspend Particulate Matter Sample 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Dr. S. Davis and Dr. R. Kalin at the EERC, Queens University Belfast provided invaluable assistance, guidance and instruction as well as the use of their facilities. Dr. M. Villet and Dr. F. Porri, Rhodes University, provided statistical help and direction. Isotope analysis was done both through the EERC, Queens University Belfast and the stable light isotope unit, University of Cape Town. All of this help is gratefully acknowledged.


  1. Asmus R, Asmus H (1991) Mussel beds: limiting or promoting phytoplankton? J Exp Mar Biol Ecol 48:215–232CrossRefGoogle Scholar
  2. Allanson BR, Read GHL (1995) Further comment on the response of Eastern Cape Province estuaries in South Africa. S Afr J Aquat Sci 21:56–70Google Scholar
  3. Barlow R, Sessions H, Balarin M, Weeks S, Whittle C, Hutchings L (2005) Seasonal variation in phytoplankton in the southern Benguela: pigment indices and ocean colour. Afr J Mar Sci 27:275–287CrossRefGoogle Scholar
  4. Blanchette C, Broitman B, Gaines S (2006) Intertidal community structure and oceanographic patterns around Santa Cruz Island, CA, USA. Mar Biol 149:689–701CrossRefGoogle Scholar
  5. Brown PC (1992) Spatial and seasonal variation in chlorophyll distribution in the upper 30 m of the photic zone in the Southern Benguela/Agulhas ecosystem. S Afr J Mar Sci 12:515–525CrossRefGoogle Scholar
  6. Brown AC, McLachlan A (1990) Ecology of sandy shores. Elsevier, AmsterdamGoogle Scholar
  7. Bustamante RH, Branch G (1996) The dependence of intertidal consumers on kelp-derived organic matter on the west coast of South Africa. J Exp Mar Biol Ecol 196:1–28CrossRefGoogle Scholar
  8. Bustamante R, Branch G, Eekhout S, Robertson B, Zoutendyk P, Schleyer M, Dye A, Hanekom N, Keats D, Jurd M, McQuaid C (1995) Gradients of intertidal primary productivity around the coast of South Africa and their relationships with consumer biomass. Oecologia 102:189–201CrossRefGoogle Scholar
  9. Caldeira RMA, Russell P, Amorim A (2001) Evidence of an unproductive coastal front in Baía d’Abra, an embayment on the south east of Madeira Island, Portugal. Bull Mar Sci 69:1057–1072Google Scholar
  10. Dame R, Prins T (1998) Bivalve carrying capacity in coastal ecosystems. Aquat Ecol 31:409–421CrossRefGoogle Scholar
  11. Deegan L, Garritt RH (1997) Evidence for spatial variability in estuarine food webs. Mar Ecol Prog Ser 147:31–47CrossRefGoogle Scholar
  12. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  13. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  14. Duggins DO, Simenstad CA, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173CrossRefGoogle Scholar
  15. Dunton KH, Schell DM (1987) Dependence of consumers on macroalgal (Laminaria solidungula) carbon in an arctic kelp community: δ13C evidence. Mar Biol 93:615–625CrossRefGoogle Scholar
  16. Frazer TK, Ross RM, Quetin LB, Montoya JP (1997) Turnover of carbon and nitrogen during growth of larval krill, Euphausia superba Dana: a stable isotope approach. J Exp Mar Biol Ecol 212:259–275CrossRefGoogle Scholar
  17. Fréchette M, Butman CA, Geyer WR (1989) The importance of boundary-layer flows in supplying phytoplankton to the benthic suspension feeder, Mytilus edulis L. Limnol Oceanogr 34:19–36CrossRefGoogle Scholar
  18. Froneman PW (2002) Food web structure in three contrasting estuaries determined using stable isotope δ13C analysis. Afr J Aquat Sci 27:107–115CrossRefGoogle Scholar
  19. Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13–17Google Scholar
  20. Fry B (1988) Food web structure on Georges Bank from stable C, N and S isotopic compositions. Limnol Oceanogr 33:1182–1190CrossRefGoogle Scholar
  21. Goering J, Alexander V, Haubenstock N (1990) Seasonal variability of stable carbon and nitrogen isotope ratios of organisms in a North Pacific bay. Estuar Coast Shelf Sci 30:239–260CrossRefGoogle Scholar
  22. Hawkins A (1985) Relationships between the synthesis and breakdown of protein, dietary absorption and turnovers of nitrogen and carbon in the blue mussel, Mytilus edulis L. Oecologia 66:42–49CrossRefGoogle Scholar
  23. Hill J, McQuaid C, Kaehler S (2006) Biogeographic and nearshore/offshore trends in isotope ratios of intertidal mussels and their food sources around the coast of southern Africa. Mar Ecol Prog Ser 318:63–73CrossRefGoogle Scholar
  24. Holm-Hansen O, Reimann B (1978) Chlorophyll-a determination: improvements in methodology. Oikos 30:438–447CrossRefGoogle Scholar
  25. Hunter M, Price P (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732Google Scholar
  26. Kaehler S, Pakhomov E, McQuaid C (2000) Trophic structure of the marine food web at the Prince Edward Islands (Southern Ocean) determined by δ13C and δ15N analysis. Mar Ecol Prog Ser 208:13–20CrossRefGoogle Scholar
  27. Kaneta PJ, Levandowskyl M, Esaias W (1985) Multivariate analysis of the phytoplankton community in the New York Bight. Mar Ecol Prog Ser 23:231–239CrossRefGoogle Scholar
  28. Kang CK, Sauriau P-G, Richard P, Blanchard GF (1999) Food sources of the infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-Oléron Bay, as determined by analyses of carbon and nitrogen stable isotopes. Mar Ecol Prog Ser 187:147–158CrossRefGoogle Scholar
  29. Kreeger DA, Newell RIE (2001) Seasonal utilization of different seston carbon sources by the ribbed mussel, Geukenseia demissa (Dillwyn) in a mid-Atlantic salt marsh. J Exp Mar Biol Ecol 260:71–91CrossRefGoogle Scholar
  30. Kukert H, Riebesell U (1998) Phytoplankton carbon isotope fractionation during a diatom spring bloom in a Norwegian fjord. Mar Ecol Prog Ser 173:127–137CrossRefGoogle Scholar
  31. Lorrain A, Paulet Y-M, Chauvaud L, Savoye N, Donval A, Saout C (2002) Differential δ13C and δ15N signatures among scallop tissues: implications for ecology and physiology. J Exp Mar Biol Ecol 275:47–61CrossRefGoogle Scholar
  32. McQuaid CD (1985a) Seasonal variation in the ash-free calorific value of nine intertidal algae. Bot Mar XXVIII:545–548Google Scholar
  33. McQuaid CD (1985b) Seasonal variation in biomass and zonation of nine intertidal algae in relation to changes in radiation, sea temperature and tidal regime. Bot Mar XXVIII:539–544Google Scholar
  34. Megens L, van der Plicht J, de Leeuw JW (2001) Temporal variations in 13C and 14C concentrations in particulate organic matter from the southern North Sea. Geochim Cosmochim Acta 65:2899–2911CrossRefGoogle Scholar
  35. Menge B (1992) Community regulation: under what conditions are bottom-up factors important on rocky shores? Ecology 73:755–765CrossRefGoogle Scholar
  36. Menge B (2000) Top-down and bottom-up community regulation in marine rocky intertidal habitats. J Exp Mar Biol Ecol 250:257–289CrossRefGoogle Scholar
  37. Menge B, Daley B, Lubchenco J, Sanford E, Dahlhoff E, Halpin P, Hudson G, Burnaford J (1999) Top-down and bottom-up regulation of New Zealand rocky intertidal communities. Ecol Monogr 69:297–330CrossRefGoogle Scholar
  38. Menge B, Daley B, Wheeler P, Strub P (1997) Rocky intertidal oceanography: an association between community structure and nearshore phytoplankton concentration. Limnol Oceanogr 42:57–66CrossRefGoogle Scholar
  39. Menge B, Lubchenco J, Bracken M, Chan F, Foley M, Freidenburg T, Gaines S, Hudson G, Krenz C, Leslie H, Menge D, Russell R, Webster M (2003) Coastal oceanography sets the pace of rocky intertidal community dynamics. PNAS 100:12229–12234CrossRefGoogle Scholar
  40. Milke L, Ward J (2003) Influence of diet on pre-ingestive particle processing in bivalves. II. Residence time in the pallial cavity and handling time on the labial palps. J Exp Mar Biol Ecol 293:151–172CrossRefGoogle Scholar
  41. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: Further evidence and the relation between 15N and animal age. Geochim Cosmochim Acta 8:1135–1140CrossRefGoogle Scholar
  42. Miyake Y, Wada E (1967) The abundance ratio of 15N/14N in marine environments. Rec Oceanogr Work Jpn 9:32–53Google Scholar
  43. Moore SK, Suthers IM (2005) Can the nitrogen and carbon stable isotopes of the pygmy mussel, Xenostrobus securis, indicate catchment disturbance for estuaries in northern New South Wales, Australia? Estuaries 28:714–725CrossRefGoogle Scholar
  44. Newell R, Shumway S, Cucci T, Selvin R (1989) The effects of natural seston particle size and type of feeding rates, feeding selectivity and food resource availability for the mussel Mytilus edulis Linneaus, 1758 at bottom culture sites in Maine. J Shellfish Res 8:187–196Google Scholar
  45. Nielsen K, Navarrete S (2004) Mesoscale regulation comes from the bottom-up: intertidal interactions between consumers and upwelling. Ecol Lett 7:31–41CrossRefGoogle Scholar
  46. O’Reilly CM, Hecky RE, Cohen AS, Plisnier P-D (2002) Interpreting stable isotopes in food webs: recognizing the role of time averaging at different trophic levels. Limnol Oceanogr 47:306–309CrossRefGoogle Scholar
  47. Ostrom NE, Macko SA, Deibel D, Thompson RJ (1997) Seasonal variation in the stable carbon and nitrogen isotope biogeochemistry of a coastal cold ocean environment. Geochim Cosmochim Acta 61:2929–2942CrossRefGoogle Scholar
  48. Peterson B, Howarth R (1987) Sulfur, carbon, and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Island, Georgia. Limnol Oceanogr 32:1195–1213CrossRefGoogle Scholar
  49. Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269CrossRefGoogle Scholar
  50. Phillips D, Eldridge P (2006) Estimating the timing of diet shifts using stable isotopes. Oecologia 147:105–203CrossRefGoogle Scholar
  51. Posey M, Alphin T, Cahoon L (2006) Benthic community responses to nutrient enrichment and predator exclusion: influence of background nutrient concentrations and interactive effects. J Exp Mar Biol Ecol 330:105–118CrossRefGoogle Scholar
  52. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  53. Raikow DF, Hamilton SK (2001) Bivalve diets in a midwestern U.S. stream: a stable isotope enrichment study. Limnol Oceanogr 46:514–522CrossRefGoogle Scholar
  54. Reira P, Richard P (1997) Temporal variation of δ13C in particulate organic matter and oyster Crassostrea gigas in Marennes-Oleron Bay (France): effect of freshwater inflow. Mar Ecol Prog Ser 147:105–115CrossRefGoogle Scholar
  55. Rolff C (2000) Seasonal variation in δ13C and δ15N of size-fractionated plankton at a coastal station in the northern Baltic proper. Mar Ecol Prog Ser 203:47–65CrossRefGoogle Scholar
  56. Roughgarden J, Gaines S, Possingham H (1988) Recruitment dynamics in complex life cycles. Science 241:1460–1466CrossRefGoogle Scholar
  57. Seitz R, Lipcius R (2001) Variation in top-down and bottom-up control of marine bivalves at differing spatial scales. ICES J Mar Sci 58:689–699CrossRefGoogle Scholar
  58. Stuart V, Field J, Newell R (1982) Evidence for absorption of kelp detritus by the ribbed mussel Aulacomya ater using a new 51Cr-labelled microsphere technique. Mar Ecol Prog Ser 9:263–271CrossRefGoogle Scholar
  59. Vizzini S, Sara G, Michener RH, Mazzola A (2002) The role and contribution of the seagrass Posidonia oceanica (L.) Delile organic matter for secondary consumers as revealed by carbon and nitrogen stable isotope analysis. Acta Oecol 23:277–285CrossRefGoogle Scholar
  60. Vorwerk PD (2007) A preliminary examination of selected biological links between four eastern Cape estuaries and the inshore marine environment. PhD Thesis, Rhodes University, p 268Google Scholar
  61. Ward J, Levinton J, Shumway S, Cucci T (1998) Particle sorting in bivalves: in vivo determination of the pallial organs of selection. Mar Biol 131:283–292CrossRefGoogle Scholar
  62. Widdows J, Fieth P, Worrall CM (1979) Relationships between seston, available food and feeding activity in the common mussel Mytilus edulis. Mar Biol 50:195–207CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Jaclyn M. Hill
    • 1
    Email author
  • Christopher D. McQuaid
    • 1
  • Sven Kaehler
    • 1
  1. 1.Coastal Research Group, Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa

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