Coral Reefs

, Volume 32, Issue 2, pp 401–409 | Cite as

A simple temperature-based model predicts the upper latitudinal limit of the temperate coral Astrangia poculata

  • J. L. Dimond
  • A. H. Kerwin
  • R. Rotjan
  • K. Sharp
  • F. J. Stewart
  • D. J. Thornhill
Report

Abstract

A few hardy ahermatypic scleractinian corals occur in shallow waters well outside of the tropics, but little is known concerning their distribution limits at high latitudes. Using field data on the growth of Astrangia poculata over an annual period near its northern range limit in Rhode Island, USA, we tested the hypothesis that the distribution of this coral is limited by low temperature. A simple model based on satellite sea surface temperature and field growth data at monthly temporal resolution was used to estimate annual net coral growth north and south of the known range limit of A. poculata. Annual net coral growth was the result of new polyp budding above ~10 °C minus polyp loss below ~10 °C, which is caused by a state of torpor that leads to overgrowth by encroaching and settling organisms. The model accurately predicted A. poculata’s range limit around Cape Cod, Massachusetts, predicting no net growth northward as a result of corals’ inability to counteract polyp loss during winter with sufficient polyp budding during summer. The model also indicated that the range limit of A. poculata coincides with a decline in the benefit of associating with symbiotic dinoflagellates (Symbiodinium B2/S. psygmophilum), suggesting that symbiosis may become a liability under colder temperatures. While we cannot exclude the potential role of other coral life history traits or environmental factors in setting A. poculata’s northern range limit, our analysis suggests that low temperature constrains the growth and persistence of adult corals and would preclude coral growth northward of Cape Cod.

Keywords

Biogeography Facultative symbiosis Physiological tolerance Species range Symbiodinium B2 Symbiodinium psygmophilum 

References

  1. Bruno JF, Witman JD (1996) Defense mechanisms of scleractinian cup corals against overgrowth by colonial invertebrates. J Exp Mar Biol Ecol 207:229–241CrossRefGoogle Scholar
  2. Cairns SD (2007) Deep-water corals: an overview with special reference to diversity and distribution of deep-water scleractinian corals. Bull Mar Sci 81:311–322Google Scholar
  3. Casey KS, Brandon TB, Cornillon P, Evans R (2010) The past, present and future of the AVHRR Pathfinder SST program. In: Barale V, Gower JFR, Alberotanza L (eds) Oceanography from space: revisited. Springer, New York, pp 323–341Google Scholar
  4. Churchill JH, Pettigrew NR, Signell RP (2005) Structure and variability of the Western Maine Coastal Current. Deep-Sea Res II 52:2392–2410CrossRefGoogle Scholar
  5. Cummings C (1983) The biology of Astrangia danae. PhD thesis, University of Rhode Island, Kingston, p 147Google Scholar
  6. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261PubMedCrossRefGoogle Scholar
  7. Dimond J, Carrington E (2007) Temporal variation in the symbiosis and growth of the temperate scleractinian coral Astrangia poculata. Mar Ecol Prog Ser 341:161–172CrossRefGoogle Scholar
  8. Dimond J, Carrington E (2008) Symbiosis regulation in a facultatively symbiotic temperate coral: zooxanthellae division and expulsion. Coral Reefs 27:601–604CrossRefGoogle Scholar
  9. Engle VD, Summers JK (2000) Biogeography of benthic macroinvertebrates in estuaries along the Gulf of Mexico and western Atlantic coasts. Hydrobiologia 436:17–33CrossRefGoogle Scholar
  10. Eytan RI, Hayes M, Arbour-Reily P, Miller M, Hellberg ME (2009) Nuclear sequences reveal mid-range isolation of an imperilled deep-water coral population. Mol Ecol 18:2375–2389PubMedCrossRefGoogle Scholar
  11. Ferrier-Pagès C, Peirano A, Abbate M, Cocito S, Negri A, Rottier C, Riera P, Rodolfo-Metalpa R, Reynaud S (2011) Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol Oceanogr 56:1429–1438CrossRefGoogle Scholar
  12. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685CrossRefGoogle Scholar
  13. Gaston KJ (2009) Geographic range limits: achieving synthesis. Proc R Soc B 276:1395–1406PubMedCrossRefGoogle Scholar
  14. Grace SP (1996) The effects of water flow on Astrangia poculata. University of Rhode Island, Kingston, MS thesis, p 146Google Scholar
  15. Grace SP (2004) Ecomorphology of the temperate scleractinian Astrangia poculata: coral–macroalgal interactions in Narragansett Bay (Rhode Island). PhD thesis, University of Rhode Island, Kingston, p 182Google Scholar
  16. Hale SS (2010) Biogeographical patterns of marine benthic macroinvertebrates along the Atlantic coast of the Northeastern USA. Estuaries Coasts 33:1039–1053CrossRefGoogle Scholar
  17. Hare JA, Churchill JH, Cowen RK, Berger TJ, Cornillon PC, Dragos P, Glenn SM, Govoni JJ, Lee TN (2002) Routes and rates of larval fish transport from the southeast to the northeast United States continental shelf. Limnol Oceanogr 47:1774–1789CrossRefGoogle Scholar
  18. Hargitt CW (1914) The Anthozoa of the Woods Hole region. Bull US Bureau Fish 32:223–254Google Scholar
  19. Holcomb M, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). J Exp Mar Biol Ecol 386:27–33CrossRefGoogle Scholar
  20. Holcomb M, Cohen AL, McCorkle DC (2012) An investigation of the calcification response of the scleractinian coral Astrangia poculata to elevated pCO2 and the effects of nutrients, zooxanthellae and gender. Biogeosciences 9:29–39CrossRefGoogle Scholar
  21. Hoogenboom MO, Rodolfo-Metalpa R, Ferrier-Pagès C (2010) Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa. J Exp Biol 213:2399–2409PubMedCrossRefGoogle Scholar
  22. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2011) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Climate Change 2:116–120CrossRefGoogle Scholar
  23. Jacques TG, Marshall N, Pilson MEQ (1983) Experimental ecology of the temperate scleractinian Astrangia danae. II. Effect of temperature, light intensity and symbiosis with zooxanthellae on metabolic rate and calcification. Mar Biol 76:135–148CrossRefGoogle Scholar
  24. Johannes RE, Weibe WJ, Crossland CJ, Rimmer DW, Smith SV (1983) Latitudinal limits to coral reef growth. Mar Ecol Prog Ser 11:201–208CrossRefGoogle Scholar
  25. Kleypas JA, McManus JW, Meñez LAB (1999) Environmental limits to coral reef development: Where do we draw the line? Am Zool 39:146–159Google Scholar
  26. LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with Cnidaria. J Phycol. doi:10.1111/j.1529-8817.2012.01217.x
  27. Lentz SJ (2008) Observations and a model of the mean circulation over the Middle Atlantic Bight continental shelf. J Phys Oceanogr 38:1203–1221CrossRefGoogle Scholar
  28. Markle DF, Scott WB, Kohler AC (1980) New and rare records of Canadian fishes and the influence of hydrography on resident and nonresident Scotian Shelf ichthyofauna. Can J Fish Aquat Sci 37:49–65CrossRefGoogle Scholar
  29. Miller MW (1995) Growth of a temperate coral: effects of temperature, light, depth, and heterotrophy. Mar Ecol Prog Ser 122:217–225CrossRefGoogle Scholar
  30. Miller MW (1998) Coral/seaweed competition and the control of reef community structure within and between latitudes. Oceanogr Mar Biol Annu Rev 36:65–96Google Scholar
  31. Miller MW, Hay ME (1996) Coral–seaweed–grazer–nutrient interactions on temperate reefs. Ecol Monogr 66:323–344CrossRefGoogle Scholar
  32. Muller-Parker G, Davy SK (2001) Temperate and tropical sea anemone symbioses. Invertebr Biol 120:104–123CrossRefGoogle Scholar
  33. Peters EC, Pilson MEQ (1985) A comparative study of the effects of sediment on symbiotic and asymbiotic colonies of the coral Astrangia danae Milne Edwards and Haime, 1849. J Exp Mar Biol Ecol 92:215–230CrossRefGoogle Scholar
  34. Peters EC, Cairns SD, Pilson MEQ, Wells JW, Jaap WC, Lang JC, Vasleski CE, St. Pierre Gollahon L (1988) Nomenclature and biology of Astrangia poculata (=A. danae, =A.astreiformis) (Cnidaria: Anthozoa). Proc Biol Soc Wash 101:234–250Google Scholar
  35. Pörtner HO (2002) Climate change and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol 132A:739–761Google Scholar
  36. Ries JB, Cohen AL, McCorkle DC (2010) A nonlinear calcification response to CO2-induced ocean acidification by the temperate coral Oculina arbuscula. Coral Reefs 29:661–674CrossRefGoogle Scholar
  37. Rodolfo-Metalpa R, Martin S, Ferrier-Pages C, Gattuso JP (2010) Response of the temperate coral Cladocora caespitosa to mid and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences 7:289–300CrossRefGoogle Scholar
  38. Rützler K (2002) Impact of crustose clionid sponges on Caribbean reef corals. Acta Geol Hispanica 37:61–72Google Scholar
  39. Salisbury J, Green M, Hunt C, Campbell J (2008) Coastal acidification by rivers: a threat to shellfish? EOS Trans Am Geophys Union 89:513–514CrossRefGoogle Scholar
  40. Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535CrossRefGoogle Scholar
  41. Sanford E, Holzman SB, Haney RA, Rand DM, Bertness MD (2006) Larval tolerance, gene flow, and the northern geographic range limit of fiddler crabs. Ecology 87:2882–2894PubMedCrossRefGoogle Scholar
  42. Schuhmacher H, Zibrowius H (1985) What is hermatypic? A redefinition of ecological groups in corals and other organisms. Coral Reefs 4:1–9CrossRefGoogle Scholar
  43. Sexton JP, Mcintyre PJ, Angert AL, Rice KJ (2009) Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 40:415–436CrossRefGoogle Scholar
  44. Smale DA, Wernberg T (2009) Satellite-derived SST data as a proxy for water temperature in nearshore benthic ecology. Mar Ecol Prog Ser 387:27–37CrossRefGoogle Scholar
  45. Smith-Keune C, van Oppen M (2006) Genetic structure of a reef-building coral from thermally distinct environments on the Great Barrier Reef. Coral Reefs 25:493–502CrossRefGoogle Scholar
  46. Stachowicz JJ, Hay ME (1999) Mutualism and coral persistence: the role of herbivore resistance to algal chemical defense. Ecology 80:2085–2101CrossRefGoogle Scholar
  47. Stanley GD (2003) The evolution of modern corals and their early history. Earth-Sci Rev 60:195–225CrossRefGoogle Scholar
  48. Stanley GD, Swart PK (1995) Evolution of the coral-zooxanthellae symbiosis during the Triassic: A geochemical approach. Paleobiology 21:179–199Google Scholar
  49. Steen RG (1986) Evidence for heterotrophy by zooxanthellae in symbiosis with Aiptasia pulchella. Biol Bull 170:267–278CrossRefGoogle Scholar
  50. Szmant-Froelich A, Pilson MEQ (1980) The effects of feeding frequency and symbiosis with zooxanthellae on the biochemical composition of Astrangia danae Milne Edwards & Haime 1848. J Exp Mar Biol Ecol 48:85–97CrossRefGoogle Scholar
  51. Szmant-Froelich A, Yevich P, Pilson MEQ (1980) Gametogenesis and early development of the temperate coral Astrangia danae (Anthozoa: Scleractinia). Biol Bull 158:257–269CrossRefGoogle Scholar
  52. Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW (2008) Correspondence between cold tolerance and temperate biogeography in a western Atlantic Symbiodinium (Dinophyta) lineage. J Phycol 44:1126–1135CrossRefGoogle Scholar
  53. Tremblay P, Peirano A, Ferrier-Pagès C (2011) Heterotrophy in the Mediterranean symbiotic coral Cladocora caespitosa: comparison with two other scleractinian species. Mar Ecol Prog Ser 422:165–177CrossRefGoogle Scholar
  54. Veron JEN (2000) Corals of the world, Vol 1–3. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  55. Wares JP (2002) Community genetics in the northwestern Atlantic intertidal. Mol Ecol 11:1131–1144PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • J. L. Dimond
    • 1
  • A. H. Kerwin
    • 2
  • R. Rotjan
    • 3
  • K. Sharp
    • 4
  • F. J. Stewart
    • 5
  • D. J. Thornhill
    • 6
  1. 1.Shannon Point Marine CenterWestern Washington UniversityAnacortesUSA
  2. 2.Department of Molecular and Cellular BiologyUniversity of ConnecticutStorrsUSA
  3. 3.John H Prescott Marine LaboratoryNew England AquariumBostonUSA
  4. 4.Galbraith Marine Sciences LaboratoryEckerd CollegePetersburgUSA
  5. 5.School of BiologyGeorgia Institute of TechnologyAtlantaUSA
  6. 6.Department of Conservation Science and PolicyDefenders of WildlifeWashingtonUSA

Personalised recommendations