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Phosphorus Limitation in Reef Macroalgae of South Florida PHOSPHORUS LIMITATION IN REEF MACROALGAE OF SOUTH FLORIDA by Courtney Kehler A Thesis Submitted to the Faculty of The Charles E. Schmidt College of Science In Partial Fulfillment of the Requirements for the Degree of Master of Science Florida Atlantic University Boca Raton, Florida December 2012 ii ACKNOWLEDGEMENTS The author would like to thank the staff and other graduate students at HBOI for their immense help in preparing this thesis and navigating the graduate requirements. I want to thank my advisor, Dr. Brian Lapointe, for his guidance, help in the field and use of his lab and data. A special thanks to Laura Herren, without her assistance my thesis would have never been completed. Finally, thanks to my parents for their endless support and love. iii ABSTRACT Author: Courtney Kehler Title: Phosphorus Limitation in Reef Macroalgae of South Florida Institution: Florida Atlantic University Thesis Advisor: Dr. Brian Lapointe Degree: Master of Science Year: 2012 Nitrogen (N) has traditionally been regarded as the primary limiting nutrient to algal growth in marine coastal waters, but recent studies suggest that phosphorus (P) can be limiting in carbonate-rich environments. To better understand the importance of P, alkaline phosphatase activity (APA) was measured in reef macroalgae in seven counties of south Florida; several significant trends emerged: 1) APA decreased geographically from the highest values in Dade > Monroe > Palm Beach > St. Lucie > Broward > Martin > Lee counties 2) APA varied temporally with increasing nutrient-rich runoff in the wet season 3) APA varied due to taxonomic division Phaeophyta > Rhodophyta > Chlorophyta 4) Nutrient enrichment experiments demonstrated that increased N- enrichment enhanced P-limitation while increased P decreased P-limitation. These results suggest that high APA observed in carbonate-rich waters of Dade County and low APA in Broward County resulted from high nutrient inputs associated with anthropogenic nutrient pollution. iv PHOSPHORUS LIMITATION IN REEF MACROALGAE OF SOUTH FLORIDA List of Figures………………………………………………………………………........vii List of Tables……………………………………………………………………………..ix Introduction…………………………………………………………………………….….1 Hypotheses………………………………………………………………………...6 Methods………………………………………………………………………………........7 Study Areas………………………………………………………………………..7 Measurement of Alkaline Phosphatase Activity…..…………………………........9 Nutrient Enrichment Experiment...........................................................................11 Results………………………………………………………………………………........13 Spatial Variation………………………………………………………………....13 Temporal Variation...….…....................................................................................14 Taxonomic Variation.............................................................................................16 Nutrient Enrichment Experiment…………………………………………...........17 Discussion………………………………………………………………………………..20 Spatial Variation…………………………………………………………………21 Temporal Variation………………………………………………………............26 Taxonomic Variation…………………………………………………………….27 Nutrient Enrichment Experiment...……………………….……………………...29 v Conclusions………………………………………………………………………............31 Appendix…………………………………………………………………………………33 References………………………………………………………………………………..49 vi FIGURES Figure 1. Macroalgae sampling location in south Florida……………………………….33 Figure 2. Spatial variation in mean APA……….……………………….……………….34 Figure 3. Taxonomic variation in mean APA……….………………………….………..34 Figure 4. Temporal variation in mean APA at Looe Key, Monroe County.…………….35 Figure 5. Temporal variation in mean APA at Pepper Park, St. Lucie County……….....35 Figure 6. APA of Cladophora catenata collected at Looe Key, Monroe County, in response to different levels of DIN and SRP enrichment .…………………..……....36 Figure 7. APA of Taonia sp. collected at Looe Key, Monroe County, in response to different levels of DIN and SRP enrichment ……………………….….……………36 Figure 8. APA of Laurencia poiteaui collected at Looe Key, Monroe County, in response to different levels of DIN and SRP enrichment ……………………..…....37 Figure 9. APA of Spatoglossum schroedi collected at Pepper Park, St. Lucie County, in response to different levels of DIN and SRP enrichment……………...……….....37 Figure 10. APA of Gracilaria tikvahiae collected at Pepper Park, St. Lucie County, in response to different levels of DIN and SRP enrichment ………..………..….....38 Figure 11. APA of Cladophora prolifera collected at Pepper Park, St. Lucie County, in response to different levels of DIN and SRP enrichment .……...………………..38 Figure 12. Taxonomic and spatial variation in mean APA in south Florida……..……...39 vii Figure 13. Mean APA versus water column TDN:TDP (a) and tissue N:P (b) by county in south Florida………………………………….……………………..……40 viii TABLES Table 1. South Florida macroalgal collection sites…………………......…...…………...41 Table 2. Summary of Two-Way ANOVA of APA as a function of phylum, season and the phylum*season interaction in Pepper Park, St. Lucie County and Looe Key, Monroe County…………………..…………………………..….............42 Table 3. Summary of Two-Way ANOVA of APA as a function of dissolved inorganic nitrogen (DIN), soluble reactive phosphorus (SRP), and the DIN*SRP interaction for species collected at Pepper Park, St. Lucie County……...43 Table 4. Summary of Two-Way ANOVA of APA as a function of dissolved inorganic nitrogen (DIN), soluble reactive phosphorus (SRP), and the DIN*SRP interaction for species collected at Looe Key, Monroe County……….....44 Table 5. Historical APA at Looe Key and Pine Channel, Monroe County…..……….....45 Table 6. Comprehensive list of sampled macroalgae from the seven counties………….46 ix INTRODUCTION Coral reefs are complex, biologically diverse ecosystems adapted to oligotrophic conditions. Anthropogenic activities inevitably add nitrogen (N) and phosphorus (P) to coastal waters resulting in eutrophication. Eutrophication is the increase in the rate of supply of organic matter to an ecosystem (Nixon 1995). With increasing eutrophication, coral reef ecosystems can undergo major ecological changes including increased coral disease and die-off, and most notably, the replacement of corals by benthic macroalgae (Lapointe 1997, NRC 2000, Lapointe et al. 2004, 2005 a, b). Macroalgal blooms are considered to be a major factor in coral reef decline around the world, including the Great Barrier Reef (Bell 1992, Schaffelke 2001), the Bahamas (Barile and Lapointe 2005), southeast Florida (Lapointe 1997, Lapointe et al. 2005 a, b, Lapointe 2007), Hawaii (Smith 1983), Jamaica (Lapointe et al. 2011) and the Florida Keys (Lapointe et al. 1994, Lapointe et al. 2004). Escalating anthropogenic influences alter the ecosystems ability to cope with disturbances and effect functional diversity (Nystrom et al. 2000). While N is the primary limiting nutrient to macroalgal growth in temperate siliciclastic environments, P-limitation has been documented in a variety of carbonate- rich environments, such as Bermuda, Jamaica, the Bahamas, and the Florida Keys (Lapointe 1989, Lapointe et al. 1992). P-limitation is attributed to the geochemical process of phosphate (PO₄³⁻) binding to calcium carbonate (CaCO₃²⁺), which reduces the amount of soluble reactive phosphorus (SRP) in groundwater, sediments and 1 subsequently, the water column (Lapointe et al. 1992, Teichberg 2007). The rock unit, Miami Limestone, which is composed of CaCO₃2+, extends up to Palm Beach County where it intercepts the coquina shell composed Anastasia Formation (Hine 2009). Therefore, counties sampled in the Miami Limestone will have mostly carbonate-rich sediments (Monroe, Dade and Broward counties), while counties above this formation will be composed of mostly siliciclastic-rich sediments (Palm Beach, Martin, St. Lucie and Lee counties, Scott 1997). Measurements of alkaline phosphatase activity (APA) have been used as a proxy of P-limitation in both freshwater and marine environments. Phosphatase is a class of enzymes that promotes the degradation of biologically unavailable complex organic phosphorus compounds into useable orthophosphates (Kuenzler and Perras 1965). Most macroalgae utilize inorganic P, known as soluble reactive phosphorus (SRP), yet most P is generally present in the ocean in the form of dissolved organic phosphorus (DOP; Lee 1999). Hence, marine macroalgae use alkaline phosphatase to cleave the needed SRP from the DOP pools (Hernandez et al. 1999, Hoppe 2003). APA of macroalgae in a wide variety of environments, including the carbonate-rich waters of Jamaica, the Bahamas, Belize, Bermuda, and the Florida Keys have high APA; whereas macroalgae in siliciclastic-rich waters such as Woods Hole, Massachusetts have generally low APA (Lapointe et al. 1992). This confirms strong P-limitation in carbonate-rich areas as well the use of APA as a proxy for estimating the degree of P-limitation (Lapointe and O’Connell 1989, Lapointe and Clark 1992, Lapointe et al. 1992, Lapointe et al. 2004). APA can be used as an accurate indicator of P-limitation in marine waters because a 2 significant linear relationship between APA and N:P ratios have been established (Lapointe et al. 1990, Urnezis 1995, Lapointe and Bedford 2010). Another method to assess P-limitation is through the use of the Redfield ratio. Redfield (1934) found that the ratio of carbon:nitrogen:phosphorus (C:N:P) for phytoplankton in marine waters averaged 106:16:1. Atkinson and Smith (1983) expanded this concept in their investigation of C:N:P of benthic marine plants and reported a mean C:N:P tissue ratio of 700:35:1,
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