Final Report: Physiology and Ecology of Macroalgal Blooms on Coral Reefs off Southeast Florida

EPA Grant Number: R830414
Title: Physiology and Ecology of Macroalgal Blooms on Coral Reefs off Southeast Florida
Investigators: Lapointe, Brian E. , Barile, Peter J. , Yentsch, Charles S.
Institution: Harbor Branch Oceanographic Institution, Inc. , Plankton Research and Instruments
EPA Project Officer: Hiscock, Michael
Project Period: October 14, 2002 through October 13, 2004 (Extended to October 13, 2005)
Project Amount: $279,098
RFA: Ecology and Oceanography of Harmful Algal Blooms (2002) RFA Text |  Recipients Lists
Research Category: Water Quality , Ecosystems , Water , Aquatic Ecosystems

Objective:

The objectives of this research project were to: (1) use digital underwater video imagery to determine seasonal (quarterly) variation in growth of the invasive green seaweeds Codium isthmocladum, Caulerpa verticillata, and Caulerpa brachypus at two reef sites (Princess Anne [PA], North Colonel’s Ledge [NCL]) in northern Palm Beach County; (2) analyze quarterly tissue samples of the invasive seaweeds at the two reef sites for their carbon, nitrogen, and phosphorus contents (C:N:P ratios) and δ15N (15N/14N) contents; (3) perform studies on the photophysiology (Photosynthetic Efficiency = Fv/Fm) of the target species; (4) determine the relative importance of ammonium (NH4) versus nitrate (NO3) to the nitrogenous nutrition of the target species; and (5) perform laboratory and field grazing assays to determine the potential for herbivores to control these blooms.

The scope of our ecology and oceanography of harmful algal blooms (HABs) research concerned the colonization and overgrowth of a relic coral reef off northern Palm Beach County, Florida, by macroalgal HABs of the chlorophyte genera Codium and Caulerpa. These genera are not common on oligotrophic, tropical, and subtropical coral reefs but can occur in abundance in habitats enriched with nutrients from either natural or anthropogenic sources. Both these genera are well known to have invasive properties and can cause ecological problems when they occur in abundance as a result of nutrient enrichment. For example, after two decades of invasion, Caulerpa taxifolia in the northern Mediterranean Sea is out of control. This introduced species, which originated from the Monaco aquarium, already has reached six Mediterranean countries and more than 131 km2 of coastal area are affected. The spreading centers for the C. taxifolia invasion were centered around urban wastewater and stormwater discharges, where anthropogenic nutrient pollution supported bloom formation, fragmentation, and dispersion. This chlorophyte deeply modified the benthic habitat of the Mediterranean and has had incisive impacts on the native flora and fauna.

Summary/Accomplishments (Outputs/Outcomes):

Objective 1

We tracked successfully the seasonal growth patterns of the invasive green macroalgae using digital video imagery with the random point count method in 2003/2004. The resulting biotic cover data demonstrates how C. brachypus var. parvifolia became the dominant organism (60-90% cover) at both reef sites in 2003/2004. This research is important because it documented the expansion of this alien species (Pacific native) on reefs in northern Palm Beach County. We also have quantified the presence of lesser abundant (< 30% cover) invasive macroalgae on these reefs, which include C. isthmocladum, C. verticillata, Caulerpa racemosa, Caulerpa mexicana, and Caulerpa prolifera.

Biotic Cover of HAB Macroalgae  at PA Site.

Figure 1. Biotic Cover of HAB Macroalgae at PA Site. Vales represent means ± 1 SD (n = 6).

Biotic Cover of HAB Macroalgae at the NCL Site.

Figure 2. Biotic Cover of HAB Macroalgae at the NCL Site. Values represent means ± SD (n = 6).

Objective 2

We successfully collected and analyzed the quarterly macroalgae samples from the two reef sites for C:N:P ratios and δ15N values in 2003/2004. Overall, the tissue C:N:P data revealed significant variability over the period of record for C. brachypus and C. racemosa. For example, the C:N ratio of C. brachypus increased from approximately 10:1 to greater than 20:1 between winter and spring of 2003 but remained less than 15:1 throughout the 2004 samplings. With the exception of the April 2003 sampling, there were no significant (P > 0.05) differences in C:N ratio in C. brachypus between the PA and NCL sites in 2003/2004. The C:P ratio of C. brachypus varied between approximately 400-600 at both reef sites with significant differences among sites occurring only in October 2003. Considerable variability occurred in the N:P ratio of C. brachypus, which ranged from approximately 22 to 58 in 2003/2004. In general, N:P ratios greater than 35 are indicative of P-limited growth, whereas ratios less than 30 are indicative of N-limited growth. Hence, these blooms of C. brachypus may be limited by both N and P, depending on the time of year.

Overall, there were no significant differences in δ15N of C. brachypus, C. racemosa, C. verticillata, and C. isthmocladum between the PA and NCL sites during the 2-year study. These values ranged from approximately +2 to +9 percent in C. brachypus and C. racemosa and varied significantly over the period of study (Kruskall Wallis, P < 0.0001). Relatively high values of 5 to 9 percent occurred from February to July of 2003 compared to low values of 2 to 4 percent in the fall 2003 and winter 2004 samplings. This pattern suggests a significant seasonal variation in N source to these blooms, switching from sewage (+4 to +9%) in the winter, spring, and summer months to other sources, such as agricultural runoff (< +4%) in the fall when N loading from stormwater runoff is maximum.

Objective 3

The major goal of objective 3 was to establish what combination of environmental and geophysical factors promoted the bloom at these particular locations. The biological/optical approach used was measurement of fluorescence yield that is an established index of the efficiency of light harvesting by photo systems of the HAB species involved. Using this approach, we established that the high efficiency of C. brachypus and other Caulerpa spp that dominated the biotic cover of the reef provided a light harvesting advantage over the local primary producers. Hence, the bloom constituted invasive phenomena. The environmental features favoring this and promoting invasiveness are ample sunlight, relatively high water clarity, and a close proximity to replete nutrient concentrations from local sediments and offshore water masses. This provided a reef environment some 30 m below the surface where the invasive HABs competed successfully with native reef biota. The geophysical features of the region, such as proximity to longshore current flow, upwelling, and highly conductive geological substrata, are believed to provide an excellent habitat for the growth of these rhizoidal attached algae.

Objective 4

Progress towards this objective included the successful completion of controlled, laboratory 15N uptake experiments with C. isthmocladum, C. brachypus, and C. racemosa in summer 2004. These factorial experiments were conducted in Lunaire incubators and examined the main effects and interactions of irradiance (low = 50 μmol photons m-2 s-1; high = 200 μmol photons m-2 s-1 ), temperature (18°C, 23°C, and 28°C), and N source (NH4 vs. NO3) using 15N-labeled substrate. The data indicate that both C. isthmocladum and C. brachypus have a strong kinetic preference (up to a 5-fold increase in uptake rate) for NH4 compared to NO3. This would explain why blooms of these HAB species have not developed historically in response to episodic, NO3-rich upwelling during summer months and supports the hypothesis that these blooms are being driven by low-level buildup of NH4 from land-based sources of nutrient pollution.

Objective 5

In Year 2, herbivory of C. brachypus by a specialist mesoherbivore, an Elysiid nudibranch, was evaluated in laboratory trials to meet Objective 5. Elysia subornata, a native to the nearby Indian River Lagoon, was assessed previously for potential biocontrol of the Mediterranean strain of C. taxifolia as this slug is abundant seasonally and relies strictly on a diet of coenocytic Caulerpa species. Although E. subornata is efficient at consumption of the native congener C. prolifera and the invasive C. taxifolia, these mesoherbivores did not consume C. brachypus in exhaustive laboratory trials. We suspect that this may be the result of the thin, sheet-like morphology of this alga as the slugs did not appear to be able to remove the cell-sap through radular piercing as is readily achieved in the congeners C. prolifera and C. taxifolia.

In comparative organic extraction analyses, C. brachypus also appears to have a significantly lower concentration of the antipredator compound caulerpenyne as compared to native Caulerpa congeners. This may explain why this alga can be consumed by herbivorous icthyofauna, in contrast to congeners that generally are not consumed by this trophic guild. These results are not supported by the current theory of herbivory on coral reefs that suggests palatability by any specific trophic group equates to categoric and complete consumption in field conditions. Rather, these results support the hypothesis that invasive species subvert pressure from established trophic pyramids and persist in previously unexploited habitats.

With support from the State of Florida and in collaboration with the Florida Fish and Wildlife Research Institute, we expanded our monitoring of HABs off southeast Florida in late August 2004 to survey reefs between Miami-Dade County and St. Lucie County. These reef surveys were temporarily delayed because of hurricanes Frances and Jeanne in September 2004 and hurricane Wilma in October 2005. The work resumed in November 2005 and will continue through the summer of 2006.


Journal Articles on this Report : 14 Displayed | Download in RIS Format

Other project views: All 47 publications 16 publications in selected types All 16 journal articles
Type Citation Project Document Sources
Journal Article Barile PJ. Comments on: “Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll”. Ecological Modelling 2004;178(1):51-57. R830414 (Final)
not available
Journal Article Barile PJ, Lapointe BE, Capo TR. Dietary nitrogen availability in macroalgae enhances growth of the sea hare Aplysia californica (Opisthobranchia:Anaspidea). Journal of Experimental Marine Biology and Ecology 2004;303(1):65-78. R830414 (2003)
R830414 (Final)
not available
Journal Article Barile PJ. Evidence of anthropogenic nitrogen enrichment of the littoral waters of east central Florida. Journal of Coastal Research 2004;20(4):1237-1245 R830414 (2004)
R830414 (Final)
not available
Journal Article Barile PJ, Lapointe BE. Atmospheric nitrogen deposition from a remote source enriches macroalgae in a coral reef ecosystem at Green Turtle Cay, Abacos, Bahamas. Marine Pollution Bulletin 2005;50(11):1262-1272. R830414 (2004)
R830414 (Final)
not available
Journal Article Lapointe BE, Barile PJ, Matzie WR. Anthropogenic nutrient enrichment of seagrass and coral reef communities in the Lower Florida Keys: discrimination of local versus regional nitrogen sources. Journal of Experimental Marine Biology and Ecology 2004;308(1):23-58. R830414 (2004)
R830414 (Final)
not available
Journal Article Lapointe BE, Barile PJ. Comment on J. C. Zieman, J. W. Fourqurean,' and T. A Frankovich. 1999. Seagrass die-off in Florida Bay: Long-term trends in abundance and growth of turtle grass, Thalassia testudinum. Estuaries 22 : 460-470. Estuaries 2004;27(1):157-164 R830414 (Final)
not available
Journal Article Lapointe BE. Phosphorus-rich waters at Glovers Reef, Belize? Marine Pollution Bulletin 2004;48(1-2):193-195. R830414 (2004)
R830414 (Final)
not available
Journal Article Lapointe BE, Barile PJ, Yentsch CS. The physiology and ecology of macroalgal blooms (green tides) on coral reefs off northern Palm Beach County, Florida (USA). Harmful Algae 2004;3:185-268 R830414 (Final)
not available
Journal Article Lapointe BE, Barile PJ, Yentsch CS, Littler MM, Littler DS, Kakuk B. The relative importance of nutrient enrichment and herbivory on macroalgal communities near Norman’s Pond Cay, Exumas Cays, Bahamas: a “natural” enrichment experiment. Journal of Experimental Marine Biology and Ecology 2004;298(2):275-301. R830414 (2003)
R830414 (Final)
not available
Journal Article Lapointe BE, Barile PJ, Littler MM, Littler DS, Bedford BJ, Gasque C. Macroalgal blooms on southeast Florida coral reefs I. Nutrient stoichiometry of the invasive green alga Codium isthmocladum in the wider Caribbean indicates nutrient enrichment. Harmful Algae 2005;4(6):1092-1105 R830414 (2004)
R830414 (Final)
not available
Journal Article Lapointe BE, Barile PJ, Littler MM, Littler DS. Macroalgal blooms on southeast Florida coral reefs: II. Cross-shelf discrimination of nitrogen sources indicates widespread assimilation of sewage nitrogen. Harmful Algae 2005;4(6):1106-1122. R830414 (Final)
not available
Journal Article Lapointe BE, Barile PJ, Wynne MJ, Yentsch CS. Reciprocal Caulerpa invasion: Mediterranean native Caulerpa ollivieri in the Bahamas supported by human nitrogen enrichment. Aquatic Invaders 2005;16(2):1-5. R830414 (Final)
not available
Journal Article Lapointe BE, Bedford BJ, Baumberger R. Hurricanes Frances and Jeanne remove blooms of the invasive green alga Caulerpa brachypus forma parvifolia (Harvey) cribb on coral reefs off Northern Palm Beach County, Florida, USA. Estuaries and Coasts 2006;29(6):966-971. R830414 (Final)
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  • Journal Article Yentsch CS, Yentsch CM, Phinney DA, Lapointe BE, Yentsch SFW. The odyssey of new production. Journal of Experimental Marine Biology and Ecology 2004;300(1-2):15-30. R830414 (2003)
    R830414 (2004)
    R830414 (Final)
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    Supplemental Keywords:

    carbon, nitrogen, phosphorus, macroalgae, photosynthesis, fluorescence, herbivores, coral reefs, sewage pollution, aquatic ecosystems, algal blooms, nutrient enrichment, bloom dynamics,, RFA, Scientific Discipline, Water, ECOSYSTEMS, Ecosystem Protection/Environmental Exposure & Risk, Aquatic Ecosystems & Estuarine Research, Oceanography, Aquatic Ecosystem, Environmental Microbiology, Aquatic Ecosystems, algal blooms, Ecological Risk Assessment, Ecology and Ecosystems, marine ecosystem, nutrient dynamics, macroalgal blooms, ocean outfalls, bloom dynamics, coral reefs, nutrient enrichment, nutrient kinetics, coral-algal symbiosis, benthic algae, coral reef communities, macroalgal populations, algal bloom detection, sewage outflows, groundwater, nitrogen

    Relevant Websites:

    http://www.hboi.edu Exit

    Progress and Final Reports:

    Original Abstract
  • 2003 Progress Report
  • 2004 Progress Report