- Email: [email protected]
Phosphorus-rich waters at Glovers Reef, Belize?
Marine Pollution Bulletin 48 (2004) 193–195 www.elsevier.com/locate/marpolbul
Correspondence Phosphorus-rich waters at Glovers Reef, Belize? Coral reefs worldwide are experiencing increasing anthropogenic impacts on local, regional and global scales. Two major human impacts––nutrient enrichment and overfishing––were recently assessed by McClanahan et al. (2002) at Glovers Reef, an atoll offshore the Belize Barrier Reef in the western Caribbean Sea. The most significant finding from this experimental study was the dramatic effect of phosphorus enrichment in stimulating increased cover of algal turf and macroalgae blooms of the green seaweed Enteromorpha. These results are important because many coral reef biologists have thought that algal blooms on Caribbean reefs in recent decades resulted only from reduction of grazing pressure (top–down controls) via overfishing of herbivorous fishes (parrotfishes, surgeonfishes) and/or mortality and die-off of the long-spined sea urchin Diadema antillarum (Hughes, 1994; Jackson et al., 2001). However, as was evident in the McClanahan et al. (2002) study, nutrient availability––not consumption by grazers––is a critical factor that regulates growth and reproduction of macroalgae. Inasmuch as grazing studies on coral reefs rarely include consideration of nutrients, the essential role of nutrient availability has been confounded within much of the ‘‘top–down’’ literature (Lapointe, 1999). As such, the McClanahan et al. (2002) study provided an important and much needed demonstration of the effects of nutrient enrichment (bottom-up controls) in triggering proliferation of algal turfs and macroalgae in coral reef environments. The McClanahan et al. (2002) study could have been improved even more by considering previous work on nutrient limitation of macroalgae on the Belize Barrier Reef. McClanahan et al. (2002) stated that ‘‘phosphorus is likely to be among the most limiting and influential nutrient in this carbonate environment’’ and accordingly, their experiments focused on phosphorus (P) enrichment. While the primary importance of P may be true, supporting data for this assumption––such as ambient concentrations of dissolved inorganic nitrogen (DIN ¼ NHþ 4 + NO3 + NO2 ) or macroalgal tissue carbon:nitrogen (C:N) ratios from Glovers Reef––were not provided to ensure that nitrogen (N) was not also limiting growth. Lapointe et al. (1987) reported relatively low concentrations of NHþ 4 (<0.41 lM), NO3 (<0.16 3 lM) and PO4 –P (<0.03 lM) from the back reef at 0025-326X/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2003.10.003
Curlew Reef on the outer Belize Barrier Reef 15 km west of Glovers Reef (Table 1). Experimental nutrient enrichment assays with red, green and brown macroalgae indicated that both N and P were limiting the productivity of macroalgal communities in these oligotrophic waters of the outer Belizean Reef––but that the relative importance of N and P were species- and site-specific (Lapointe et al., 1987). Studies by Tomasko and Lapointe (1991) provided further evidence of very low or undetectable DIN concentrations on the Belize Barrier Reef, including Glovers Reef (Table 1). Lapointe et al. (1993) reported very low or undetectable DIN and PO3 4 –P concentrations at Curlew Reef and Tobacco Reef on the outer Belize Barrier Reef (Table 1) and also high C:N ratios (>36:1) in a variety of macroalgae that were above the mean value for marine plants (22:1, Atkinson and Smith, 1983) and indicative of N-limitation. McClanahan et al. (2002) did provide some background measurements of PO3 4 –P concentrations from their experimental sites at Glovers Reef. They reported mean PO3 4 –P concentrations of 0.03 mg/l for the ‘‘control’’ site and 0.06 mg/l for the ‘‘fertilized’’ site, although it was unclear exactly how many samples were analyzed. They converted these weight/volume units to molar concentrations of 0.35 and 0.77 lM for the ‘‘control’’ and ‘‘fertilized’’ sites, respectively, to facilitate comparison with the marine chemistry literature. Apparently, their conversion of ‘‘measured’’ PO3 4 –P from mg/l to molar concentrations was incorrect, as 0.03 mg/l is equivalent to 1.0 lM, not 0.35 lM as they stated; likewise, their 0.06 mg/l would be 2.0 lM, much higher than their reported 0.77 lM. These PO3 4 –P concentrations would be considered high for many coastal water, but especially for oligotrophic waters that typically occur on Caribbean coral reefs. Table 1 provides published PO3 4 –P data (equivalent to soluable reactive phosphorus, SRP) for several carbonaterich Caribbean reefs, including Glovers Reef, which shows that concentrations are typically <0.1 lM. Accordingly, the background PO3 4 –P concentration (0.03 mg/l) reported by McClanahan et al. (2002) would appear some twenty-fold higher than concentrations reported previously for Glovers Reef and at last ten-fold higher than those reported for coral reefs experiencing eutrophication and associated macroalgal blooms in the Florida Keys and Jamaica (Table 1).
194
Correspondence / Marine Pollution Bulletin 48 (2004) 193–195
Table 1 Concentrations (lM) of ammonium, nitrate, dissolved inorganic nitrogen (DIN ¼ ammonium + nitrate + nitrite), PO3 4 –P (¼ soluble reactive phosphorus, SRP) and the DIN:PO3 4 –P ratio reported for shallow carbonate-rich coral reefs in the Caribbean region Location Belize Barrier Reef
Jamaica
Florida Keys
Date
NHþ 4
NO 3
DIN
PO3 4 –P
DIN:PO3 4 –P NA NA 5.4
12 16 8
2.8
2
Reference
n
Curlew Cay Curlew Cay Tobacco Reef Glovers Reef
Apr-85 May-90 May-90
0.29 ± 0.17 <0.10 0.43
0.08 ± 0.05 U.D. U.D.
0.37 ± 0.22 <0.10 0.43
U.D. U.D. 0.08
May-90
U.D.
0.14
0.14
0.05
Glovers Reef
NA
NA
NA
NA
0.35–1.0
NA
Negril Marine Park
Winter 98
0.93 ± 1.08
0.44 ± 0.22
1.12 ± 1.08
0.017 ± 0.010
58.7
48
Summer 98
0.80 ± 0.83
0.41 ± 0.16
1.19 ± 0.89
0.047 ± 0.029
38.5
48
1984 1987 1996 1998
0.34 ± 0.29 0.23 ± 0.18 0.39 ± 0.54 0.64 ± 0.47
0.15 ± 0.16 0.39 ± 0.30 0.55 ± 0.41 0.54 ± 0.36
0.49 ± 0.22 0.63 ± 0.32 0.88 ± 0.68 1.18 ± 0.69
0.05 ± 0.07 0.04 ± 0.07 0.04 ± 0.03 0.09 ± 0.02
9.8 15.8 22 13.1
258 48 90 52
Looe Key
NA
Lapointe et al. (1987) Lapointe et al. (1993) Lapointe et al. (1993) Tomasko and Lapointe (1991) McClanahan et al. (2002) Lapointe and Thacker (2002) Lapointe and Thacker (2002) Lapointe Lapointe Lapointe Lapointe
et et et et
al. al. al. al.
(2002) (2002) (2002) (2002)
Values represent means ± 1 SD. U.D. denotes concentration below analytical detection limits. NA denotes information is not available.
However, a more serious problem arises with the analytical method that McClanahan et al. (2002) used for PO3 4 –P analysis that is inappropriate given the very low PO3 4 –P concentrations reported for the Belize Barrier Reef and other Caribbean coral reefs (Table 1). McClanahan et al. (2002) used a Hach DR 3000 spectrophotometer and the ascorbic acid method to measure PO3 4 –P in the ‘‘low range of 0–2.0 mg/l’’. However, because of inherent optical and instrumental limitations, this method has an estimated detection limit (EDL) of only 0.01 mg/l, or 0.35 lM, for PO3 4 (Hach, Method 8048). Consequently, this method does not have sufficient sensitivity to accurately measure PO3 4 –P concentrations that are typically <0.1 lM on the Belize Barrier Reef and Glovers Reef. For this reason, more sensitive analytical methods commonly used for monitoring nutrient concentrations on coral reefs have low detection limits (e.g. use of spectrophotometers with 10-cm cells can provide detection limits for PO3 4 –P of 0.03 lM, Lapointe et al., 1993), which together with ‘‘clean handling techniques,’’ are required to obtain high quality data representative of these environments. This analytical limitation undermines McClanahan et al.’s (2002) conclusion that their data ‘‘do not support a threshold hypothesis’’ for PO3 4 –P concentration at which macroalgal blooms can develop at Glovers Reef. Previous field studies along natural nutrient gradients on the Belize Barrier Reef (Lapointe et al., 1993) and Jamaican fringing reefs experiencing eutrophication from land-based runoff (Lapointe, 1997, 1999; Lapointe and Thacker, 2002) all suggest a DIN threshold of 1.0 lM (Table 1). This threshold is supported by detailed laboratory and field studies that have quantified DINlimited growth rates of a variety of tropical macroalgae
that typically occur at concentrations of 0.5–1.0 lM; above these concentrations, growth rate becomes DINsaturated in a fashion similar to Michaelis–Menten kinetics (Lapointe, 1999). Considering that macroalgae require N:P in a ratio of 10:1, a corresponding PO3 4 –P threshold concentration of 0.05–0.1 lM would be needed to support P uptake and balanced growth for the development of algal blooms. Indeed, macroalgal blooms have been reported for tropical coastal waters having this range of PO3 4 –P concentrations (Table 1) as a result of P enrichment from natural sources (mangroves, seabird guano) in localized areas of the Belize Barrier Reef (Lapointe et al., 1993) or on much larger spatial scales due to escalating anthropogenic nutrient enrichment (sewage, agricultural runoff) of the Negril Marine Park, Jamaica (Lapointe and Thacker, 2002) and Looe Key in the Florida Keys National marine Sanctuary (Lapointe et al., 2002). These quantitative relationships between macroalgal blooms and PO3 4 –P concentrations illustrate why removal of grazers via overfishing on oligotrophic coral reefs with very low PO3 4 –P concentrations (<0.03 lM) do not result in macroalgal blooms (Lapointe, 1999), but rather the expansion of more diminutive algal turfs as predicted by the Relative Dominance Model (RDM, Littler and Littler, 1984). Although McClanahan et al. (2002) found a significant and dramatic effect of PO3 4 –P enrichment on macroalgal cover and blooms of Enteromorpha, even greater nutrient effects could have occurred had stronger DIN enrichment been utilized in their experimental design. Many green filamentous seaweeds in the genera Enteromorpha, Chaetomorpha and Cladophora are wellknown indicators of ‘‘nutrient enrichment’’ and typi-
Correspondence / Marine Pollution Bulletin 48 (2004) 193–195
cally form blooms around mangrove islands from P-rich seabird guano (Lapointe et al., 1993) or in coral reef habitats impacted by land-based nutrient pollution from sewage, agricultural runoff and top soil loss (Lapointe, 1997; Lapointe and Thacker, 2002). In locations like the Negril Marine Park and Discovery Bay, Jamaica, DINrich groundwater inputs from the limestone watersheds typically have very high N:P ratios (>35:1), which result in strong P-limitation of macroalgal growth on downstream reefs (Lapointe, 1997; Lapointe, 1999). However, such high DIN concentrations, N:P ratios and strong Plimitation would not be expected at Glover’s Reef, which is a remote offshore atoll with relatively little groundwater DIN input. Instead, the water column at Glovers Reef would likely have lower N:P ratios (<15:1, see DIN:PO3 4 –P ratios in Table 1) that would favor colimitation by both N and P and an overall ‘‘weaker’’ degree of P-limitation. Indeed, comparative studies of reef macroalgae from Discovery Bay, Jamaica and Curlew Reef on the outer Belize Barrier Reef using alkaline phosphatase activity (APA) as an index of Plimitation showed significantly (two-fold) lower values on the more oligotrophic Belizean site as a result of lower DIN concentrations and P-limitation (Lapointe et al., 1997). The land-based DIN enrichment (largely via submarine groundwater discharges) on reefs offshore Discovery Bay enriches the percentage N content of the brown seaweed Lobophora variegata to at least 36 m depths, supporting increased P-limitation in the superabundant and multi-layered macroalgal blooms that have developed on those reefs in recent decades (Lapointe et al., 1997). Despite the offshore location of Glovers Reef, satellite imagery shows that land-based runoff via river discharges from Honduras have impacted this remote area periodically during the rainy season over the past several decades, especially following Hurricane Mitch in late October, 1998; the recurrent sedimentation and nutrient enrichment associated with these events helps to explain the recent phase shift from hermatypic corals to macroalgae in the Glovers Reef lagoon (Andrefouet et al., 2002).
Acknowledgements This correspondence was supported by a grant from the United States Environmental Protection Agency through the Ecology and Oceanography of Harmful Algal Blooms program. This is contribution No. 1534 from the Harbor Branch Oceanographic Institution, Inc.
195
References Andrefouet, S., Mumby, P.J., McField, M., Hu, C., Karger, F.E., 2002. Revisiting coral reef connectivity. Coral Reefs 21 (1), 43–48. Atkinson, M.J., Smith, S.V., 1983. C:N:P ratios of benthic marine plants. Limnol. Oceanogr. 28, 568–574. Hughes, T.P., 1994. Catastrophes, phase-shifts and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551. Jackson, J. et al., 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–638. Lapointe, B.E., 1997. Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol. Oceanogr. 42 (5–2), 1119–1131. Lapointe, B.E., 1999. Simultaneous top–down and bottom-up forces control macroalgal blooms on coral reefs (reply to the comment by Hughes et al.). Limnol. Oceanogr. 44 (6), 1586–1592. Lapointe, B.E., Thacker, K., 2002. Community-based water quality and coral reef monitoring in the Negril Marine Park, Jamaica: Land-based nutrient inputs and their ecological consequences. In: Porter, J.W., Porter, K.G. (Eds.), The Everglades, Florida Bay and Coral Reefs of the Florida Keys: An Ecosystem Sourcebook. CRC Press, Boca Raton, FL, pp. 939–963. Lapointe, B.E., Littler, M.M., Littler, D.S., 1987. A comparison of nutrient-limited productivity in macroalgae from a Caribbean barrier reef and from a mangrove ecosystem. Aquat. Bot. 28, 243– 255. Lapointe, B.E., Littler, M.M., Littler, D.S., 1993. Modification of benthic community structure by natural eutrophication: the Belize Barrier Reef. Proceedings of the Seventh International Coral Reef Symposium, Guam 1, 323–334. Lapointe, B.E., Littler, M.M., Littler, D.S., 1997. Macroalgal overgrowth of fringing coral reefs at Discovery Bay, Jamaica: bottom-up versus top–down control. Proceedings of the Eighth International Coral Reef Symposium, Panama, 1, 927–932. Lapointe, B.E., Matzie, W.R., Barile, P.J., 2002. Biotic phase-shifts in Florida Bay and fore reef communities of the Florida Keys: Linkages with historical freshwater flows and nitrogen loading from Everglades runoff. In: Porter, J.W., Porter, K.G. (Eds.), The Everglades, Florida Bay and Coral Reefs of the Florida Keys: An Ecosystem Sourcebook. CRC Press, Boca Raton, FL, pp. 629–648. Littler, M.M., Littler, D.S., 1984. Models of tropical reef biogenesis. Prog. Phycol. Res. 3, 323–364. McClanahan, T.R., Cokos, B.A., Sala, E., 2002. Algal growth and species composition under experimental control of herbivory, phosphorus and coral abundance in Glovers Reef, Belize. Mar. Pollut. Bull. 44, 441–451. Tomasko, D.A., Lapointe, B.E., 1991. Productivity and biomass of Thalassia testudinum as related to water column nutrient availability and epiphyte levels: field observations and experimental studies. Mar. Ecol. Prog. Ser. 75, 9–17.
Brian E. Lapointe Division of Marine Science Harbor Branch Oceanographic Institution, Inc. 5600 US 1 North Ft. Pierce FL 34946 USA Tel.: +1-772-465-2400; fax: +1-772-468-0757 E-mail address: [email protected]
Correspondence Phosphorus-rich waters at Glovers Reef, Belize? Coral reefs worldwide are experiencing increasing anthropogenic impacts on local, regional and global scales. Two major human impacts––nutrient enrichment and overfishing––were recently assessed by McClanahan et al. (2002) at Glovers Reef, an atoll offshore the Belize Barrier Reef in the western Caribbean Sea. The most significant finding from this experimental study was the dramatic effect of phosphorus enrichment in stimulating increased cover of algal turf and macroalgae blooms of the green seaweed Enteromorpha. These results are important because many coral reef biologists have thought that algal blooms on Caribbean reefs in recent decades resulted only from reduction of grazing pressure (top–down controls) via overfishing of herbivorous fishes (parrotfishes, surgeonfishes) and/or mortality and die-off of the long-spined sea urchin Diadema antillarum (Hughes, 1994; Jackson et al., 2001). However, as was evident in the McClanahan et al. (2002) study, nutrient availability––not consumption by grazers––is a critical factor that regulates growth and reproduction of macroalgae. Inasmuch as grazing studies on coral reefs rarely include consideration of nutrients, the essential role of nutrient availability has been confounded within much of the ‘‘top–down’’ literature (Lapointe, 1999). As such, the McClanahan et al. (2002) study provided an important and much needed demonstration of the effects of nutrient enrichment (bottom-up controls) in triggering proliferation of algal turfs and macroalgae in coral reef environments. The McClanahan et al. (2002) study could have been improved even more by considering previous work on nutrient limitation of macroalgae on the Belize Barrier Reef. McClanahan et al. (2002) stated that ‘‘phosphorus is likely to be among the most limiting and influential nutrient in this carbonate environment’’ and accordingly, their experiments focused on phosphorus (P) enrichment. While the primary importance of P may be true, supporting data for this assumption––such as ambient concentrations of dissolved inorganic nitrogen (DIN ¼ NHþ 4 + NO3 + NO2 ) or macroalgal tissue carbon:nitrogen (C:N) ratios from Glovers Reef––were not provided to ensure that nitrogen (N) was not also limiting growth. Lapointe et al. (1987) reported relatively low concentrations of NHþ 4 (<0.41 lM), NO3 (<0.16 3 lM) and PO4 –P (<0.03 lM) from the back reef at 0025-326X/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2003.10.003
Curlew Reef on the outer Belize Barrier Reef 15 km west of Glovers Reef (Table 1). Experimental nutrient enrichment assays with red, green and brown macroalgae indicated that both N and P were limiting the productivity of macroalgal communities in these oligotrophic waters of the outer Belizean Reef––but that the relative importance of N and P were species- and site-specific (Lapointe et al., 1987). Studies by Tomasko and Lapointe (1991) provided further evidence of very low or undetectable DIN concentrations on the Belize Barrier Reef, including Glovers Reef (Table 1). Lapointe et al. (1993) reported very low or undetectable DIN and PO3 4 –P concentrations at Curlew Reef and Tobacco Reef on the outer Belize Barrier Reef (Table 1) and also high C:N ratios (>36:1) in a variety of macroalgae that were above the mean value for marine plants (22:1, Atkinson and Smith, 1983) and indicative of N-limitation. McClanahan et al. (2002) did provide some background measurements of PO3 4 –P concentrations from their experimental sites at Glovers Reef. They reported mean PO3 4 –P concentrations of 0.03 mg/l for the ‘‘control’’ site and 0.06 mg/l for the ‘‘fertilized’’ site, although it was unclear exactly how many samples were analyzed. They converted these weight/volume units to molar concentrations of 0.35 and 0.77 lM for the ‘‘control’’ and ‘‘fertilized’’ sites, respectively, to facilitate comparison with the marine chemistry literature. Apparently, their conversion of ‘‘measured’’ PO3 4 –P from mg/l to molar concentrations was incorrect, as 0.03 mg/l is equivalent to 1.0 lM, not 0.35 lM as they stated; likewise, their 0.06 mg/l would be 2.0 lM, much higher than their reported 0.77 lM. These PO3 4 –P concentrations would be considered high for many coastal water, but especially for oligotrophic waters that typically occur on Caribbean coral reefs. Table 1 provides published PO3 4 –P data (equivalent to soluable reactive phosphorus, SRP) for several carbonaterich Caribbean reefs, including Glovers Reef, which shows that concentrations are typically <0.1 lM. Accordingly, the background PO3 4 –P concentration (0.03 mg/l) reported by McClanahan et al. (2002) would appear some twenty-fold higher than concentrations reported previously for Glovers Reef and at last ten-fold higher than those reported for coral reefs experiencing eutrophication and associated macroalgal blooms in the Florida Keys and Jamaica (Table 1).
194
Correspondence / Marine Pollution Bulletin 48 (2004) 193–195
Table 1 Concentrations (lM) of ammonium, nitrate, dissolved inorganic nitrogen (DIN ¼ ammonium + nitrate + nitrite), PO3 4 –P (¼ soluble reactive phosphorus, SRP) and the DIN:PO3 4 –P ratio reported for shallow carbonate-rich coral reefs in the Caribbean region Location Belize Barrier Reef
Jamaica
Florida Keys
Date
NHþ 4
NO 3
DIN
PO3 4 –P
DIN:PO3 4 –P NA NA 5.4
12 16 8
2.8
2
Reference
n
Curlew Cay Curlew Cay Tobacco Reef Glovers Reef
Apr-85 May-90 May-90
0.29 ± 0.17 <0.10 0.43
0.08 ± 0.05 U.D. U.D.
0.37 ± 0.22 <0.10 0.43
U.D. U.D. 0.08
May-90
U.D.
0.14
0.14
0.05
Glovers Reef
NA
NA
NA
NA
0.35–1.0
NA
Negril Marine Park
Winter 98
0.93 ± 1.08
0.44 ± 0.22
1.12 ± 1.08
0.017 ± 0.010
58.7
48
Summer 98
0.80 ± 0.83
0.41 ± 0.16
1.19 ± 0.89
0.047 ± 0.029
38.5
48
1984 1987 1996 1998
0.34 ± 0.29 0.23 ± 0.18 0.39 ± 0.54 0.64 ± 0.47
0.15 ± 0.16 0.39 ± 0.30 0.55 ± 0.41 0.54 ± 0.36
0.49 ± 0.22 0.63 ± 0.32 0.88 ± 0.68 1.18 ± 0.69
0.05 ± 0.07 0.04 ± 0.07 0.04 ± 0.03 0.09 ± 0.02
9.8 15.8 22 13.1
258 48 90 52
Looe Key
NA
Lapointe et al. (1987) Lapointe et al. (1993) Lapointe et al. (1993) Tomasko and Lapointe (1991) McClanahan et al. (2002) Lapointe and Thacker (2002) Lapointe and Thacker (2002) Lapointe Lapointe Lapointe Lapointe
et et et et
al. al. al. al.
(2002) (2002) (2002) (2002)
Values represent means ± 1 SD. U.D. denotes concentration below analytical detection limits. NA denotes information is not available.
However, a more serious problem arises with the analytical method that McClanahan et al. (2002) used for PO3 4 –P analysis that is inappropriate given the very low PO3 4 –P concentrations reported for the Belize Barrier Reef and other Caribbean coral reefs (Table 1). McClanahan et al. (2002) used a Hach DR 3000 spectrophotometer and the ascorbic acid method to measure PO3 4 –P in the ‘‘low range of 0–2.0 mg/l’’. However, because of inherent optical and instrumental limitations, this method has an estimated detection limit (EDL) of only 0.01 mg/l, or 0.35 lM, for PO3 4 (Hach, Method 8048). Consequently, this method does not have sufficient sensitivity to accurately measure PO3 4 –P concentrations that are typically <0.1 lM on the Belize Barrier Reef and Glovers Reef. For this reason, more sensitive analytical methods commonly used for monitoring nutrient concentrations on coral reefs have low detection limits (e.g. use of spectrophotometers with 10-cm cells can provide detection limits for PO3 4 –P of 0.03 lM, Lapointe et al., 1993), which together with ‘‘clean handling techniques,’’ are required to obtain high quality data representative of these environments. This analytical limitation undermines McClanahan et al.’s (2002) conclusion that their data ‘‘do not support a threshold hypothesis’’ for PO3 4 –P concentration at which macroalgal blooms can develop at Glovers Reef. Previous field studies along natural nutrient gradients on the Belize Barrier Reef (Lapointe et al., 1993) and Jamaican fringing reefs experiencing eutrophication from land-based runoff (Lapointe, 1997, 1999; Lapointe and Thacker, 2002) all suggest a DIN threshold of 1.0 lM (Table 1). This threshold is supported by detailed laboratory and field studies that have quantified DINlimited growth rates of a variety of tropical macroalgae
that typically occur at concentrations of 0.5–1.0 lM; above these concentrations, growth rate becomes DINsaturated in a fashion similar to Michaelis–Menten kinetics (Lapointe, 1999). Considering that macroalgae require N:P in a ratio of 10:1, a corresponding PO3 4 –P threshold concentration of 0.05–0.1 lM would be needed to support P uptake and balanced growth for the development of algal blooms. Indeed, macroalgal blooms have been reported for tropical coastal waters having this range of PO3 4 –P concentrations (Table 1) as a result of P enrichment from natural sources (mangroves, seabird guano) in localized areas of the Belize Barrier Reef (Lapointe et al., 1993) or on much larger spatial scales due to escalating anthropogenic nutrient enrichment (sewage, agricultural runoff) of the Negril Marine Park, Jamaica (Lapointe and Thacker, 2002) and Looe Key in the Florida Keys National marine Sanctuary (Lapointe et al., 2002). These quantitative relationships between macroalgal blooms and PO3 4 –P concentrations illustrate why removal of grazers via overfishing on oligotrophic coral reefs with very low PO3 4 –P concentrations (<0.03 lM) do not result in macroalgal blooms (Lapointe, 1999), but rather the expansion of more diminutive algal turfs as predicted by the Relative Dominance Model (RDM, Littler and Littler, 1984). Although McClanahan et al. (2002) found a significant and dramatic effect of PO3 4 –P enrichment on macroalgal cover and blooms of Enteromorpha, even greater nutrient effects could have occurred had stronger DIN enrichment been utilized in their experimental design. Many green filamentous seaweeds in the genera Enteromorpha, Chaetomorpha and Cladophora are wellknown indicators of ‘‘nutrient enrichment’’ and typi-
Correspondence / Marine Pollution Bulletin 48 (2004) 193–195
cally form blooms around mangrove islands from P-rich seabird guano (Lapointe et al., 1993) or in coral reef habitats impacted by land-based nutrient pollution from sewage, agricultural runoff and top soil loss (Lapointe, 1997; Lapointe and Thacker, 2002). In locations like the Negril Marine Park and Discovery Bay, Jamaica, DINrich groundwater inputs from the limestone watersheds typically have very high N:P ratios (>35:1), which result in strong P-limitation of macroalgal growth on downstream reefs (Lapointe, 1997; Lapointe, 1999). However, such high DIN concentrations, N:P ratios and strong Plimitation would not be expected at Glover’s Reef, which is a remote offshore atoll with relatively little groundwater DIN input. Instead, the water column at Glovers Reef would likely have lower N:P ratios (<15:1, see DIN:PO3 4 –P ratios in Table 1) that would favor colimitation by both N and P and an overall ‘‘weaker’’ degree of P-limitation. Indeed, comparative studies of reef macroalgae from Discovery Bay, Jamaica and Curlew Reef on the outer Belize Barrier Reef using alkaline phosphatase activity (APA) as an index of Plimitation showed significantly (two-fold) lower values on the more oligotrophic Belizean site as a result of lower DIN concentrations and P-limitation (Lapointe et al., 1997). The land-based DIN enrichment (largely via submarine groundwater discharges) on reefs offshore Discovery Bay enriches the percentage N content of the brown seaweed Lobophora variegata to at least 36 m depths, supporting increased P-limitation in the superabundant and multi-layered macroalgal blooms that have developed on those reefs in recent decades (Lapointe et al., 1997). Despite the offshore location of Glovers Reef, satellite imagery shows that land-based runoff via river discharges from Honduras have impacted this remote area periodically during the rainy season over the past several decades, especially following Hurricane Mitch in late October, 1998; the recurrent sedimentation and nutrient enrichment associated with these events helps to explain the recent phase shift from hermatypic corals to macroalgae in the Glovers Reef lagoon (Andrefouet et al., 2002).
Acknowledgements This correspondence was supported by a grant from the United States Environmental Protection Agency through the Ecology and Oceanography of Harmful Algal Blooms program. This is contribution No. 1534 from the Harbor Branch Oceanographic Institution, Inc.
195
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Brian E. Lapointe Division of Marine Science Harbor Branch Oceanographic Institution, Inc. 5600 US 1 North Ft. Pierce FL 34946 USA Tel.: +1-772-465-2400; fax: +1-772-468-0757 E-mail address: [email protected]