Factors affecting tolerance to herbivory in a calcifying alga on coral reefs
Herbivores greatly influence the productivity of algae but their impact can depend on the nuances of the timing, location, and intensity of herbivory. While plants can escape herbivory in spatial refugia, small-scale variations in habitat quality play a critical role in plant tolerance to herbivory and might generate complex trade-offs. On coral reefs, overstory branching corals provide a refuge from fish herbivory but also provide refugia for many small fish that excrete nutrients. Therefore, algae living in this habitat might also benefit from higher nutrient delivery. However, because coral branches occlude sunlight, algal growth rates might be impaired despite experiencing elevated nutrients and lower herbivory. In lab-based experiments, light, nutrients, and simulated herbivory were manipulated in summer and winter to investigate how these processes interact to influence the tolerance of herbivory in the calcifying green algae Halimeda, an important producer of reef carbonate sediments worldwide. Halimeda heteromorpha which is commonly found associated with branching corals tolerated tissue damage by increasing rates of segment production. Greater tolerance was observed at levels of light resembling those experienced under the coral’s canopy. Nutrient additions increased compensatory segment growth in winter but not summer. Levels of tolerance were seasonal and nutrient dependent. Results show that small-scale variations in habitat quality may influence tolerance to herbivory in Halimeda. This suggests that if coral habitats are degraded or lost and oceans continue to warm, a likely negative impact on Halimeda populations and its contribution to carbonate sediments could be expected if high levels of herbivory are maintained.
KeywordsCompensatory growth Coral habitats Grazing pressure Light attenuation Coral structural complexity Limiting resource model (LRM) Carbonate production
We thank the Heron Island Research Station (HIRS) and the Australian Coral Reef Society for funding to C.C.S and an Australian Research Council Laureate Fellowship to P.J.M. Special thanks to C. Birrell for setting up the flume system, field assistants H. Bravo, M. Briand, D. Jackson, A. Chai and G. Bernal and to the staff of HIRS, CRE, J.C. Ortiz, Y-M. Bozec, C. Doropoulos, G. Roff, and MSEL colleagues for their helpful advice. We also thank S. Blomberg for his invaluable advice on statistics.
Compliance with ethical standards
Conflict of interest
The authors have declared that no competing interests exist.
This research does not contain any studies with human participants or animals performed by any of the authors. Research was conducted under GBRMPA permit #G13/36037.1.
- Diaz-Pulido G et al (2007) Vulnerability of macroalgae of the Great Barrier Reef to climate change. In: Johnson JE, Marshall PA (eds). Climate change and the Great Barrier Reef. Great Barrier Reef Marine Park Authority & Australian Greenhouse Office, Townsville, pp 153–192Google Scholar
- Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 1714–1726Google Scholar
- Hothorn T, Bretz F, Westfall P, Heiberger RM (2008) Multcomp: simultaneous inference in general parametric models. R package version 1.0Google Scholar
- Kraft GT (2007) Algae of Australia: Marine benthic algae of Lord Howe Island and the Southern Great Barrier Reef. 1. Green Algae. CSIRO publishing, MelbourneGoogle Scholar
- Kuznetsova A, Brockhoff PB, Christensen RHB (2012) lmerTest: tests in linear mixed effects models. R package version 1.0Google Scholar
- Mason BM (2009) The importance of detritus and microenvironment nutrient enrichment to the growth of coral reef macroalgae, Halimeda and Dictyota. Master of Science Thesis. University of North Carolina at WilmingtonGoogle Scholar
- Mejia AY, Puncher GN, Engelen AH (2012) Macroalgae in tropical marine coastal systems. In: Wiencke C, Bischof K (eds) Seaweed Biology. Novel insights into ecophysiology, ecology and utilization, vol Part III. vol Ecological studies. Springer, Berlin Heidelberg, pp 329–357Google Scholar
- R Development Core Team (2010) R: A language and environment fot statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Smith JE, Smith CM, Vroom PS, Beach KL, Miller S (2004) Nutrient and growth dynamics of Halimeda tuna on Conch Reef, Florida Keys: Possible influence of internal tides on nutrient status and physiology Limnol Oceanogr:1923–1936Google Scholar
- Thimijan RW, Heins RD (1983) Photometric, radiometric, and quantum light units of measure: a review of procedures for interconversion. HortScience 18:818–822Google Scholar
- Vroom PS, Smith CM, Coyer JA, Walters LJ, Hunter CL, Beach KS, Smith JE (2003) Field biology of Halimeda tuna (Bryopsidales, Chlorophyta) across a depth gradient: Comparative growth, survivorship, recruitment, and reproduction. Hydrobiologia 501:149–166. doi: 10.1023/a:1026287816324 CrossRefGoogle Scholar
- Yñiguez AT (2007) Spatial dynamics in the growth and spread of Halimeda and Dictyota in Florida reefs: a simulation modeling approach. PhD dissertation, University of Miami, FloridaGoogle Scholar