Oecologia

, Volume 147, Issue 3, pp 426–433 | Cite as

Direct effects of physical stress can be counteracted by indirect benefits: oyster growth on a tidal elevation gradient

Population Ecology

Abstract

The paradigmatic gradient for intertidal marine organisms of increasing physical stress from low to high elevation has long served as the basis for using direct effects of duration of water coverage to predict many biological patterns. Accordingly, changes in potential feeding time may predict the direction and magnitude of differences between elevations in individual growth rates of sessile marine invertebrates. Oysters (triploid Crassostrea ariakensis) experimentally introduced at intertidal (MLW+0.05 m) and subtidal (MLW–0.25 m) elevations in racks provided a test of the ability to use duration of water coverage to predict changes in growth. During early-to-mid winter, a depression of 38–47% in shell growth of intertidal oysters matched the 36% reduction in available feeding time relative to subtidal oysters. In late winter as solar heating of exposed oysters increased, growth differences of 52–55% departed only slightly from the predicted 39%. In spring, however, duration of water coverage failed to predict even the correct direction of growth change with elevation as intertidal oysters grew 34% faster despite 39% less feeding time. Intense seasonal development of shell fouling by other suspension feeders like ascidians, mussels, and barnacles on subtidal (94% incidence) but not on aerially exposed intertidal (21–38% incidence) oysters may explain why duration of water cover failed to predict spring growth differences. Less intense fouling develops on intertidal oysters due to the physiological stress of aerial exposure on settlers, especially during higher temperatures and longer solar exposures of spring. Fouling by suspension feeders is known to reduce growth of the host through localized competition for food and added energetic costs. Thus, in springtime, indirect effects of aerial exposure providing a partial refuge from biological enemies overwhelmed direct effects of reduced duration of water coverage to reverse the expected pattern of slower intertidal growth of a marine invertebrate.

Keywords

Aerial exposure Crassostrea ariakensis Intertidal Oyster shell fouling Zonation 

References

  1. Barnes H, Powell HT (1953) The growth of Balanus balanoides (L.) and B. crenatus Brug. under varying conditions of submersion. J Mar Biol Assoc UK 32:107–128CrossRefGoogle Scholar
  2. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125CrossRefGoogle Scholar
  3. Burnett LE, Jorgensen DD, Carol AK, Scholnick D (1991) Physiological responses of the barnacle Balanus nubilis to air exposure. Am Zool 31:68AGoogle Scholar
  4. Buss LW, Jackson JBC (1981) Planktonic food availability and suspension-feeder abundance: evidence of in-situ depletion. J Exp Mar Biol Ecol 49:151–162CrossRefGoogle Scholar
  5. Connell JH (1961) The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42:710–723CrossRefGoogle Scholar
  6. Connell JH (1972) Community interactions on marine rocky intertidal shores. Ann Rev Ecol Syst 3:169–192CrossRefGoogle Scholar
  7. Dalby JE, Young CM (1992) Role of early post-settlement mortality in setting the upper depth limit of ascidians in Florida epifaunal communities. Mar Ecol Prog Ser 80:221–228CrossRefGoogle Scholar
  8. Dethier MN, Graham ES, Cohen S, Tear LM (1993) Visual versus random-point percent cover estimations: ‘objective’ is not always better. Mar Ecol Prog Ser 96:93–100CrossRefGoogle Scholar
  9. Griffiths RJ, Buffenstein R (1981) Aerial exposure and energy input into in the bivalve Choromytilus meridionalis (Kr.). J Exp Mar Biol Ecol 52:219–229CrossRefGoogle Scholar
  10. Handley SJ, Bergquist PR (1997) Spionid polychatete infestations of intertidal pacific oysters Crassostra gigas (Thunberg), Mahuragi Harbour, northern New Zealand. Aquaculture 153:191–205CrossRefGoogle Scholar
  11. Harvey M, Vincent B (1990) Density, size distribution, energy allocation and seasonal variations in shell and soft tissue growth at two tidal levels of a Macoma balthica (L.) population. J Exp Mar Biol Ecol 142:151–168CrossRefGoogle Scholar
  12. Hatton H (1938) Essais de bionomie explicative sur quelques especes intercotidales d’algues et d’animaux. Ann Inst Oceanogr Monaco 17:241–348Google Scholar
  13. Hofmann GE (1999) Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am Zool 41:3–16Google Scholar
  14. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229PubMedCrossRefGoogle Scholar
  15. Jackson JBC (1977) Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Am Nat 111:743–767CrossRefGoogle Scholar
  16. Kneib RT (1988) Testing for indirect effects of predation in an intertidal soft-bottom community. Ecology 69:1795–1805CrossRefGoogle Scholar
  17. Lesser MP, Shumway SE, Cucci T, Smith J (1992) Impact of fouling organisms on mussel rope culture: interspecific competition for food among suspension-feeding invertebrates. J Exp Mar Biol Ecol 165:91–102CrossRefGoogle Scholar
  18. Levine SH (1976) Competitive interactions in ecosystems. Am Nat 110:903–910CrossRefGoogle Scholar
  19. Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74CrossRefGoogle Scholar
  20. Muschenheim DK (1987) The dynamics of near-bed seston flux and suspension-feeding benthos. J Mar Res 45:473–496Google Scholar
  21. Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75CrossRefGoogle Scholar
  22. Peterson CH (1982) The importance of predation and intraspecific and interspecific competition in the population biology of two infaunal suspension-feeding bivalves, Protothaca staminea and Chione undatella. Ecol Monogr 52:437–475CrossRefGoogle Scholar
  23. Peterson CH (1983) Interactions between two infaunal bivalves, Chione undatella (Sowerby) and Protothaca staminea (Conrad), and two potential enemies, Crepidula onyx Sowerby and Cancer anthonyi (Rathbun). J Exp Mar Biol Ecol 68:145–158CrossRefGoogle Scholar
  24. Peterson CH, Black R (1987) Resource depletion by active suspension feeders on tidal flats: influence of local density and tidal elevation. Limnol Oceanogr 32:143–166CrossRefGoogle Scholar
  25. Peterson CH, Black R (1991) Preliminary evidence for progressive sestonic food depletion in incoming tide over a broad tidal sand flat. Est Coast Shelf Sci 32:405–413CrossRefGoogle Scholar
  26. Petraitis PS (1990) Direct and indirect effects of predation, herbivory and surface rugosity on mussel recruitment. Oecologia 83:405–413Google Scholar
  27. Rhoads DC, Young DK (1970) The influence of deposit-feeding organisms on sediment stability and trophic community structure. J Mar Res 28:150–178Google Scholar
  28. Riisgård HU, Christensen PB, Olesen NJ, Petersen JK, Moller MM, Anderson P (1995) Biological structure in a shallow cove (Kertinge Nor, Denmark). Control by benthic nutrient fluxes and suspension-feeding ascidians and jellyfish. Ophelia 41:329–344Google Scholar
  29. Schmitt RJ (1987) Indirect interactions between prey: apparent competition, predator aggression, and habitat segregation. Ecology 68:1887–1897CrossRefGoogle Scholar
  30. Seed R (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores. II. Growth and mortality. Oecologia 3:317–350CrossRefGoogle Scholar
  31. Suchanek TH (1978) The ecology of Mytilus edulis L. in exposed rocky intertidal communities. J Exp Mar Biol Ecol 31:105–120CrossRefGoogle Scholar
  32. Van Erkom, Schurink C, Griffiths CL (1993) Factors affecting relative rates of growth in four South African mussel species. Aquaculture 109:257–273CrossRefGoogle Scholar
  33. Widdows J, Bayne BL, Livingstone DR, Newell RIE, Donkin P (1979) Physiological and biochemical responses of bivalve molluscs to exposure to air. Comp Biochem Physiol 62:301–308CrossRefGoogle Scholar
  34. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Ann Rev Ecol Syst 25:443–466CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Institute of Marine SciencesUniversity of North Carolina at Chapel HillMorehead CityUSA
  2. 2.Department of Environmental SciencesUniversity of Technology SydneyGore HillAustralia

Personalised recommendations