Advertisement

Marine Biology

, Volume 162, Issue 12, pp 2327–2338 | Cite as

Nitrogen transfer in a Caribbean mutualistic network

  • C. E. Cantrell
  • R. P. Henry
  • N. E. Chadwick
Feature Article

Abstract

Coral reef symbioses are well-established models for studying multi-level networks of species interactions that provide nutritional benefits to partners. While the contributions of endosymbionts to cnidarian hosts have been extensively documented, relatively little is known about how exosymbionts contribute to nutrient cycling in coral reef cnidarians. We investigated exosymbiotic sources of ammonia and their contributions to physiological processes in Caribbean corkscrew sea anemones Bartholomea annulata. In laboratory experiments, anemones absorbed ammonia from seawater, which significantly enhanced the mitotic index of their endosymbiotic microalgae Symbiodinium, while anemone shrimp presence alone had no effect. Anemone shrimps excreted ammonia at much slower rates than anemones were able to absorb it, indicating that shrimp alone were not able to meet host nitrogen demand. Client fishes excreted ammonia ~10× more rapidly than did associated shrimps. On Caribbean coral reefs, anemone shrimps attract diverse client fishes through their parasite-cleaning behavior; these fishes excrete substantial ammonia near anemones while being cleaned. Exosymbiotic anemone shrimps thus may provide nutritional benefits to host anemones and microalgae indirectly, through their attraction of nitrogen-excreting fishes. This multi-level mutualistic network facilitates tight nutrient cycling among diverse species belonging to several phyla on coral reefs. While we assessed the rates and benefits of nutrient transfer under laboratory conditions, further research is needed to quantify the contributions of ammonia and other nutrients from client fishes through cleaner shrimps to host sea anemones in the field.

Keywords

Microalgae Coral Reef Ammonia Excretion Ammonia Uptake Symbiodinium Cell 
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.

Notes

Acknowledgments

We thank Jessica Gilpin, Mark Stuart, and Erin O’Reilly for assistance with animal collection in Florida and animal culture in the laboratory, Anthony Moss for the use of laboratory equipment, Megan Goodnight for assistance with the figure graphics, and Lindsay Huebner for the design of Fig. 4. This project was funded in part by the Intramural Grants Program, Office of the Vice President for Research, Auburn University. This work was submitted in partial fulfillment of the M.Sc. degree to CEC at Auburn University.

References

  1. Achituv Y, Mizrahi L (1996) Recycling of ammonium within a hydrocoral (Millepora dichotoma)-zooxanthellae-cirripede (Savignium milleporum) symbiotic association. Bull Mar Sci 58:856–860Google Scholar
  2. Allgiers JE, Layman CA, Mumby PJ, Rosemund AD (2014) Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems. Global Change Biol 20:2459–2472CrossRefGoogle Scholar
  3. Battey JF, Patton JS (1987) Glycerol translocation in Condylactis gigantea. Mar Biol 95:37–46CrossRefGoogle Scholar
  4. Briones-Fourzán P, Pérez-Ortiz M, Negrete-Soto F, Barradas-Ortiz C, Lozano-Álvarez E (2012) Ecological traits of Caribbean sea anemones and symbiotic crustaceans. Mar Ecol Prog Ser 470:55–68CrossRefGoogle Scholar
  5. Bshary R (2003) The cleaner wrasse, Labriodes dimidiatus, is a key organism for reef fish diversity at Ras Mohammed Nation Park. Egypt J Anim Ecol 72:169–176CrossRefGoogle Scholar
  6. Bunkley-Williams L, Williams EH (1998) Ability of Pederson cleaner shrimp to remove juveniles of the parasitic cymothiod iospod, Anilocra haemuli, from the host. Crustaceana 71:862–869CrossRefGoogle Scholar
  7. Chadwick NE, Ďuriš Z, Horká I (2008) Biodiversity and behavior of shrimps and fishes symbiotic with sea anemones in the Gulf of Aqaba, northern Red Sea. In: Por FD (ed) Aqaba-Eilat, the improbable gulf: environment, biodiversity, and preservation. Magnes Press, Hebrew University, Jerusalem, pp 209–223Google Scholar
  8. Chadwick-Furman NE, Nir I, Spiegel M (2000) Sexual reproduction in the tropical corallimorpharian Rhodactis rhodostoma. Invert Biol 119:361–369CrossRefGoogle Scholar
  9. Cheney KL, Coté IM (2001) Are Caribbean cleaning symbioses mutualistic? Costs and benefits of visiting cleaning stations to longfin damselfish. Anim Behav 62:927–933CrossRefGoogle Scholar
  10. Cleveland A, Verde EA, Lee RW (2011) Nutritional exchange in a tropical tripartite symbiosis: direct evidence for the transfer of nutrients from anemonefish to host anemone and zooxanthallae. Mar Biol 158:589–602CrossRefGoogle Scholar
  11. Day RJ (1994) Algal symbiosis in Bunodeopsis: sea anemones with “auxiliary” structures. Biol Bull 186:182–192CrossRefGoogle Scholar
  12. Dixon AK, Needham D, Al-Horani FA, Chadwick NE (2014) Microhabitat use and photoacclimation in the clownfish sea anemone Entacmaea quadricolor. J Mar Biol Assoc UK 94:473–480CrossRefGoogle Scholar
  13. Fitt WK (2000) Cellular growth of host and symbiont in a cnidarian-zooxanthellar symbiosis. Biol Bull 189:110–120CrossRefGoogle Scholar
  14. Fitt WK, Cook CB (2001) The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical marine cnidarian. Mar Biol 139:507–517CrossRefGoogle Scholar
  15. Godinot C, Chadwick NE (2009) Phosphate excretion by anemonefish and uptake by giant sea anemones: demand outstrips supply. Bull Mar Sci 85:1–9Google Scholar
  16. Godwin J, Fautin DG (1992) Defense of host actinians by anemonefishes. Copeia 3:902–908CrossRefGoogle Scholar
  17. Grutter AS (2003) Cleaner fish drives local fish diversity on coral reefs. Curr Biol 13:64–67CrossRefGoogle Scholar
  18. Hattori A (2005) High mobility of the protandrous anemonefish Amphiprion frenatus: non-random pair formation in limited shelter space. Ichthyol Res 52:57–63CrossRefGoogle Scholar
  19. Hirose Y (1985) Habitat, distribution and abundance of coral reef sea-anemones (Actiniidae and Stichodactylidae) in Sesoko Island, Okinawa, with notes of expansion and contraction behavior. Galaxea 4:113–127Google Scholar
  20. Hoegh-Guldberg O (2006) The population dynamics of symbiotic zooxanthallae in the coral Pocillopora damicornis exposed to elevated ammonium (NH4 +Cl) concentrations. Pac Sci 48:263–272Google Scholar
  21. Hoegh-Guldberg O, McCloskey LR, Muscatine L (1987) Expulsion of zooxanthellae by symbiotic cnidarians from the Red Sea. Coral Reefs 5:201–204CrossRefGoogle Scholar
  22. Holbrook SJ, Schmitt RJ (2005) Growth, reproduction and survival of a tropical sea anemone (Actinaria): benefits of hosting anemonefish. Coral Reefs 24:67–73CrossRefGoogle Scholar
  23. Holmlund CM, Hammer M (1999) Ecosystem services generated by fish populations. Ecol Econ 29:253–268CrossRefGoogle Scholar
  24. Hubbell SP (1997) A unified theory of biogeography and relative species abundance and its application to tropical rain forests and coral reefs. Coral Reefs 16:S9–S21CrossRefGoogle Scholar
  25. Huebner LK, Chadwick NE (2012a) Reef fishes use sea anemones as visual cues for cleaning interactions with shrimp. J Exp Mar Biol Ecol 416–417:237–242CrossRefGoogle Scholar
  26. Huebner LK, Chadwick NE (2012b) Patterns of cleaning behaviour on coral reef fish by the anemoneshrimp Ancylomenes pedersoni. J Mar Biol Assoc UK 92:1557–1562CrossRefGoogle Scholar
  27. Huebner LK, Dailey B, Titus BM, Khalaf M, Chadwick NE (2012) Host preference and habitat segregation among Red Sea anemonefish: effects of sea anemone traits and fish life stage. Mar Ecol Prog Ser 464:1–15CrossRefGoogle Scholar
  28. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefGoogle Scholar
  29. Jeffrey SW, Humphrey GF (1975) New spectrometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae, and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194CrossRefGoogle Scholar
  30. Johannes RE, Wiebe WJ, Crossland CJ, Rimmer DW, Smith SV (1983) Latitudinal limits of coral reef growth. Mar Ecol Prog Ser 11:105–111CrossRefGoogle Scholar
  31. Johnson WS, Ruben P (1988) Cleaning behavior of Bodianus rufus, Thalassoma bifasciatum, Gobiosoma evelynae, and Periclimenes pedersoni along a depth gradient at Salt River Submarine Canyon. St Croix Environ Biol Fish 23:225–232CrossRefGoogle Scholar
  32. Kuguru B, Winters G, Beer S, Santos SR, Chadwick NE (2007) Adaptation strategies of the corallimorpharian Rhodactis rhodostoma to irradiance and temperature. Mar Biol 151:1287–1298CrossRefGoogle Scholar
  33. LaJeunesse T (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  34. Lee RW, Childress JJ (1994) Assimilation of inorganic nitrogen by marine invertebrates and their chemoautotrophic and methanotrophic symbionts. Appl Environ Microbiol 60:1852–1858PubMedPubMedCentralGoogle Scholar
  35. Linton DM, Warner GF (2003) Biological indicators in the Caribbean coastal zone and their role in integrated coastal management. Ocean Coast Manag 46:261–276CrossRefGoogle Scholar
  36. Lipshultz F, Cook CB (2002) Uptake and assimilation of 15N-ammonium by the symbiotic sea anemones Bartholomea annulata and Aiptasia pallida: conservation versus recycling of nitrogen. Mar Biol 140:489–502CrossRefGoogle Scholar
  37. Mahnken C (1972) Observations on cleaner shrimps of the genus Periclimenes. Bull Nat Hist Mus Los Angeles County 14:71–83Google Scholar
  38. McCammon AM, Brooks WR (2014) Protection of host anemones by snapping shrimps: a case for symbiotic mutualism? Symbiosis 63:71–78CrossRefGoogle Scholar
  39. McCammon A, Sikkel P, Nemeth D (2010) Effects of three Caribbean cleaner shrimps on ectoparasitic monogeneans in a semi-natural environment. Coral Reefs 29:419–426CrossRefGoogle Scholar
  40. Meyer JL, Schultz ET (1985) Migrating haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnol Oceanogr 30:146–156CrossRefGoogle Scholar
  41. Mitchell JS, Dill LM (2005) Why is group size correlated with the size of the host anemone in the false clown anemonefish? Can J Zool 83:372–376CrossRefGoogle Scholar
  42. Mokady O, Loya Y, Lazar B (1998) Ammonium contribution from boring bivalves to their coral host—a mutualistic symbiosis? Mar Ecol Prog Ser 169:295–301CrossRefGoogle Scholar
  43. Muller-Parker G (1987) Seasonal variation in light-shade adaption of natural populations of the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943) in Hawaii. J Exp Mar Biol Ecol 112:165–183CrossRefGoogle Scholar
  44. Muller-Parker G, McCloskey LR, Hoegh-Guldberg O, McAuley PJ (1994) Effect of ammonium enrichment on animal and algal biomass of the coral Pocillopora damicornis. Pac Sci 48:273–283Google Scholar
  45. Muscatine L (1980) Uptake retention and release of dissolved inorganic nutrients by marine alga-invertebrate associations. In: Cook CB (ed) Cellular interaction in symbiosis and parasitism. Ohio State University Press, Columbus, pp 229–243Google Scholar
  46. Muscatine L, D’Elia CF (1978) The uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23:725–734CrossRefGoogle Scholar
  47. Muscatine L, Porter PW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bio Sci 27:454–460Google Scholar
  48. Nagelkerken IA, Bothwell J, Nemeth RS, Pitt JM, van der Velde G (2008) Interlinkage between Caribbean coral reefs and seagrass beds through feeding migrations by grunts (Haemulidae) depends on habitat accessibility. Mar Ecol Prog Ser 368:155–164CrossRefGoogle Scholar
  49. Nelsen MW (2008) Population dynamic modeling of the corkscrew sea anemone Bartholomea annulata on Caribbean coral reefs. M.Sc. Thesis, Auburn University, USAGoogle Scholar
  50. Porat D, Chadwick-Furman NE (2004) Effects of anemonefish on giant sea anemones: expansion behavior, growth and survival. Hydrobiol 530:513–520Google Scholar
  51. Porat D, Chadwick-Furman NE (2005) Effects of anemonefish on giant sea anemones: ammonium uptake, zooxanthella content and tissue regeneration. Mar Freshw Behav Physiol 38:43–51CrossRefGoogle Scholar
  52. Poulin R, Grutter A (1996) Cleaning symbiosis: proximate and adaptive explanations. Bioscience 47:512–517CrossRefGoogle Scholar
  53. Ricciardi F, Boyer M, Ollerton J (2010) Assemblage and interaction structure of the anemonefish-anemone mutualism across the Manado region of Sulawesi, Indonesia. Environ Biol Fish 87:333–347CrossRefGoogle Scholar
  54. Roopin M, Chadwick NE (2009) Benefits to host sea anemones from ammonia contributions of resident anemonefish. J Exp Mar Biol Ecol 370:27–34CrossRefGoogle Scholar
  55. Roopin M, Henry RP, Chadwick NE (2008) Nutrient transfer in a marine mutualism: patterns of ammonia excretion by anemonefish and uptake by giant sea anemones. Mar Biol 154:547–556CrossRefGoogle Scholar
  56. Roopin M, Thornhill DJ, Santos SR, Chadwick NE (2011) Ammonia flux, physiological parameters, and Symbiodinium diversity in the anemonefish symbiosis on Red Sea coral reefs. Symbiosis 53:63–74CrossRefGoogle Scholar
  57. Schmitt RJ, Holbrook SJ (2000) Habitat-limited recruitment of coral reef damselfish. Ecology 81:3479–3494CrossRefGoogle Scholar
  58. Sikkel PC, Fuller CA, Hunter W (2000) Habitat/sex differences in time at cleaning stations and ectoparasite loads in a Caribbean reef fish. Mar Ecol Prog Ser 193:191–199CrossRefGoogle Scholar
  59. Sikkel PC, Cheney KL, Côté IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish. Anim Behav 68:241–247CrossRefGoogle Scholar
  60. Sikkel PC, Herzleib SE, Kramer DL (2005) Compensatory cleaner-seeking behavior following spawning in female yellowtail damselfish. Mar Ecol Prog Ser 296:1–11CrossRefGoogle Scholar
  61. Silvano RAM, Tibbetts IR, Grutter AS (2012) Potential effects of fishing on cleaning interactions in a tropical reef. Coral Reefs 31:1193–1198CrossRefGoogle Scholar
  62. Sluka R, Chiappone M, Sullivan KM, DeGarine-Wichatitsky M (1997) Benthic habitat characterization and space utilization by juvenile epinepheline groupers in the Exuma Cays Land and Sea Park, Central Bahamas. In: Proceedings of the 45th Gulf Caribbean Fish Institute, vol 45. pp 23–36Google Scholar
  63. Smith GJ (1986) Ontogenetic influences on carbon flux in Aulactinia stelloides polyps (Anthozoa: Actiniaria) and their endosymbiotic algae. Mar Biol 92:361–369CrossRefGoogle Scholar
  64. Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801CrossRefGoogle Scholar
  65. Spotte S (1996) Supply of regenerated nitrogen to sea anemones by their symbiotic shrimp. J Exp Mar Biol Ecol 198:27–36CrossRefGoogle Scholar
  66. Stambler N, Dubinsky Z (1987) Energy relationships between Anemonia sulcata and its endosymbiotic zooxanthellae. Symbiosis 3:233–248Google Scholar
  67. Szczebak JT, Henry RP, Al-Horani FA, Chadwick NE (2013) Anemonefish oxygenate their anemone hosts at night. J Exp Biol 216:970–976CrossRefGoogle Scholar
  68. Trench RK (1979) The cell biology of plant-animal symbiosis. Annu Rev Plant Physiol 30:485–531CrossRefGoogle Scholar
  69. Verweij MC, Nagelkerken I, Wartenbergh SL, Pen IR, van der Velde G (2006) Caribbean mangroves and seagrass beds as daytime feeding habitats for juvenile French grunts, Haemulon flavolineatum. Mar Biol 149:1291–1299CrossRefGoogle Scholar
  70. Wicksten MK (1995) Associations of fishes and their cleaners on coral reefs of Bonaire, Netherlands Antilles. Copeia 2:477–481CrossRefGoogle Scholar
  71. Wicksten MK (1998) Behaviour of cleaners and their client fishes at Bonaire Netherlands Antilles. J Nat Hist 32:13–30CrossRefGoogle Scholar
  72. Wilkerson FP, Muscatine L (1984) Uptake and assimilation of dissolved inorganic nitrogen by a symbiotic sea anemone. Proc Royal Soc Lond B 221:71–86CrossRefGoogle Scholar
  73. Wilkerson FP, Muller-Parker G, Muscatine L (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28:1009–1014CrossRefGoogle Scholar
  74. Wilkerson FP, Kobayashi D, Muscatine L (1988) Mitotic Index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7:29–36CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • C. E. Cantrell
    • 1
  • R. P. Henry
    • 1
  • N. E. Chadwick
    • 1
  1. 1.Department of Biological SciencesAuburn UniversityAuburnUSA

Personalised recommendations