- Email: [email protected]
Phosphorus and nitrogen enrichment do not enhance brown frondose “macroalgae”
Marine Pollution Bulletin 48 (2004) 196–199 www.elsevier.com/locate/marpolbul
Correspondence Phosphorus and nitrogen enrichment do not enhance brown frondose ‘‘macroalgae’’ Caribbean coral reefs have experienced a loss of coral cover from around 50% to <10% of their substratum in the past 30 years (Gardner et al., 2003) and in many cases this space has been occupied by frondose algae, specifically the brown frondose algal taxa in the genera Dictyota, Lobophora, Padina, Sargassum, and Turbinaria. This has occurred in reefs throughout the region, largely irrespective of the level of human influences or nutrient status of the reefs (Hughes, 1994; Shulman and Robertson, 1996; Lapointe, 1997; McClanahan and Muthiga, 1998; Ostrander et al., 2000; Gardner et al., 2003). Suggested factors are many and include disease, loss of herbivores, thermal anomalies, dust, hurricanes, and nutrients enrichment (McClanahan, 2002). Given the spatial extent of this problem it is unlikely that the ecological change is due to localized factors such as ground water or point-source nutrient pollution. At that scale oceanographic factors are considerably stronger than local influences by as much as two orders of magnitude (Leichter et al., 2003). Remote areas such as Glovers reef are, therefore, very unlikely to be regularly influenced by groundwater or terrestrial runoff, but could experience upwelling by both regular trade winds and hurricanes and on rare occasions by terrestrial runoff (Andrefouet et al., 2002). The remote location provides a good location to experimentally evaluate nutrient influences on reef organisms as direct human pollution is likely to uncommon and the site provides a good baseline for experimentally increasing possible human influences. Lapointe reinterprets the results of our study to claim support for the statement that nutrients enhance ‘‘macroalgae’’. Our study showed that the addition of a fertilizer mixed with both phosphorus and nitrogen enhanced the cover and colonization of the green turf alga Enteromorpha prolifera but not the brown frondose algae of the above taxa that are common to these and other disturbed reefs (McClanahan et al., 2002). E. prolifera, which has a thallus width of 100 lm and branchlets <500 lm (Littler and Littler, 2000), formed turfs about 1 cm tall in our fertilized treatment. The definition of ‘‘macroalgae’’ varies between investigators but we would consider ‘‘macroalgae’’ to be those macrophytes with morphologies that have a cortex and 0025-326X/$ - see front matter Ó 2003 Published by Elsevier Ltd. doi:10.1016/j.marpolbul.2003.10.004
medulla, a thallus size >1 cm, and gross standing height of >5 cm (Steneck and Dethier, 1994), and hence E. prolifera does not, to us, qualify as ‘‘macroalgae’’. Because of definitional problems among investigators, we did not use this terminology to describe our algae as the term is vague, can be too inclusive to be useful, and, therefore, susceptible to misuse in support of favoured hypotheses. In fact, we said ‘‘phosphorus enrichment can lead to rapid colonization of space by filamentous turf communities but not high biomass and dominance of erect frondose algae’’. Moreover, the cover of E. prolifera in our fertilized treatment, although greater than in the other treatments, was of only 32% of total algal cover. This increase in cover of a small turf alga, although statistically significant, is not the dramatic increase in ‘‘macroalgal’’ cover suggested by Lapointe. Our findings do not support some predictions of the Relative Dominance Model (RDM––Littler et al., 1991), notably the predication that high nutrients and low grazing will enhance large algae. In fact, the opposite appears to be true. High nutrients suppress the large brown frondose algae in a competitive field environment (as opposed to physiological studies in containers) and subsequent studies indicate that this result is not due to the level of enhancement or proportion of nitrogen and phosphorus (McClanahan et al., 2003). This may, however, not be the case for large red and green algae (McClanahan et al., 2003). There are likely to be differences in the physiological limitations and growth response of various algae to different concentrations and ratios of nitrogen and phosphorus (Delgado and Lapointe, 1994; Littler et al., 1991) but we do not believe the addition of more nitrogen would improve conditions in the field for frondose brown algae and significantly change our results. In the contested study we used a high phosphorus fertilizer where each application had 500 g of P2 O5 and 100 g of NH4 . Although we believed phosphorus was likely to be the more limiting of the two nutrients we included nitrogen at levels such that it should not limit production. In a subsequent experiment in the following year we nearly tripled the dosage of nitrogen to 270 g with the nitrogen being a mixture of ammonium and nitrate (McClanahan et al., 2003). This study produced the same results, high turf and low frondose dominance in the nutrient-enriched treatments. It may prove useful to continue studies with even higher levels of nitrogen or reduced P:N ratios to determine the
Correspondence / Marine Pollution Bulletin 48 (2004) 196–199
possible effects on high nitrogen, but we are sceptical that this will improve conditions for frondose algae as poor success of frondose algae is probably not due to physiological limitations but more likely due to competitive abilities in the presence of high nutrients. Species with smaller thalli and higher surface area to volume ratios are more likely to do well under these conditions and competitively exclude the larger frondose taxa (Carpenter, 1990). Phosphorus and nitrogen are dissolved with oxygen in seawater and spectrophotometric methods measure the concentrations of the total molecule and not just these elements alone. Consequently, when calculating molar concentrations by the methods we used it is necessary to use the full molecular weight of PO34- of 95 and not just that of phosphorus of 31. Our reported concentration of 0.3 lM is correct and fits well with other reports for this region and reef atolls. For example, an unpublished study in this same reef by Mumby using an Autoanalyzer and a 1 cm cell, found SRP absolute levels to be 0.35–0.39 M. Nearby in the Chinchorro Bank of Mexico Chavez et al. (1985) reported 0.78 lM and in other reef atolls such as the Abrolhos Islands, Indian Ocean 0.21–0.37 lM (Johannes et al., 1983), Kavaratti Atoll, Indian Ocean, 0.34 lM (Wafar et al., 1985), Maldives 0.43–0.58 lM (Rayner and Drew, 1984), and Canton Atoll, Phoenix Islands, 0.56 lM (Smith and Jokiel, 1978). The levels of SRP levels for Glovers Atoll are greater than those reported at nearshore area of Twin Cays of 0.14 lM (Lapointe et al., 1993) and those reported by Lapointe in his Table 1. Our study in Glovers in the subsequent year reports 0.16 lM (McClanahan et al., 2003), which is closer to Lapointe’s numbers for the barrier reef and the global average for coral reefs reported as 0.13 lM (Kleypas et al., 1999). Lapointe’s undetectable values in offshore areas of Belize have not been found in other studies of the same reef environment and are anomalous compared to other nutrient studies in remote reef atolls. Studies of physiological limitations and growth experiments of isolated algae in containers (Littler et al., 1991; Delgado and Lapointe, 1994) with different concentrations of nutrients are likely to be a poor analogue for field situations. Extrapolation of these container studies to establishing nutrient ‘‘thresholds’’ in the field is likely to be fraught with scaling and other real-world problems. There is no assurance that growth estimates taken from containers will result in an accumulation of biomass in the field where physical disturbances, competition, and predation can produces losses that can more than compensate for growth. The establishment of ‘‘nutrient thresholds’’ has been used prematurely before being tested and confirmed in field situations and is possibly deceptive and overused guideline that should be used cautiously if not eliminated from our science.
197
The proposed thresholds may have found utility or produced significant correlations in some limited situations (see the correlative papers cited in Lapointe (1999)). When examining coral reefs on a larger scale it becomes clear, however, that the correlations between nutrients and erect or frondose algae abundance are not the cause of frondose algal dominance as they do not predict the ecological responses for all reefs. For example, Lapointe et al. (1993) used the low nutrient concentrations and frondose algal cover reported in a few visited sites in Belize to support the nutrient limitation hypothesis. But, when viewed across more sites in Belize it is clear that brown frondose algae dominate many of the barrier and reef atoll environments, often being more than 50% of the benthic cover (McClanahan and Muthiga, 1998; McClanahan et al., 1999). The threshold concept can largely be rejected outright or be seen as highly contingent on other environmental factors because the suggested thresholds (Bell, 1992; Lapointe, 1997) are below the mean nutrient concentrations reported for 1000 coral reefs (Kleypas et al., 1999). If we were to strictly apply these thresholds the frondose algae should dominate over half of the reefs in the world, which is not the case, particularly outside the Caribbean. Some of the nutrients, particularly nitrogen, are highly variable in the reef environment and can easily range over an order of magnitude within days to months (Leichter et al., 2003). This sort of variation would make it difficult to make a limited number of measurements in time and space and establish a clear point where reefs are eutrophied. Finally, for those investigators that favour the nutrient limitation any coincidence between measurable nutrients and frondose algae can be used as support for this hypothesis. They are less likely to apply the same criteria for reefs where nutrients are measurable but erect frondose algal cover low. The utility of low thresholds may also be a problem in applying. As pointed out by Lapointe (2004) the low levels of nutrients found in corals reefs are difficult to measure and the lowest levels may require special tools such as a longer absorption cell and a specialized spectrophotometer. Aspects of handling the samples and the laboratory conditions also become very important at these low levels. For example, commonly purchased distilled water often has higher nutrient concentrations than the reef water being sampled and the use of distilled water for rinsing glassware can contaminate samples. This means that acid needs be used for washing glassware. Lapointe and others will seldom bring their specialized and expensive laboratories to the field and it is common practice to freeze samples, ship, and analyze them later. We have found, however, that this process can produce errors possibly by the long time it takes to freeze seawater in insulated coolers or by releasing phosphorus from organisms that may have been repeatedly frozen and thawed. Therefore, we prefer to
198
Correspondence / Marine Pollution Bulletin 48 (2004) 196–199
analyze samples in the field within a short period after the collection. We, therefore, used a portable spectrophotometer and the ascorbic acid method (Method 8048) and a 2.5 cm cell that has a lower limit of 0.02 mg/l or 0.2 lM. This is the one of nine possible methods that Hach gives for phosphates and the one that gives the lowest detection levels. The digital read out gives values of 0.01, which we use but may be below values were measurements are reliable. Preliminary tests of known concentrations suggest that the coefficient of variation around the means increases from <9% to 25% below 0.5 lM (Jones, S., unpublished data). This indicates that at the low levels reported for coral reefs that it may be very hard to distinguish sites or values reported in the literature, assuming these reports use similar methods. Nonetheless, we view the blue coloration from the reaction and this indicates that phosphates are in the water and at detectable levels, but the sensitivity of the spectrophotometer or cell length used to test for absorption may improve the accuracy of the measurements, these factors do not account for the measurable and average quantities of phosphates we found in Glovers Reef. Our study underpins the lack of efficacy of nutrient thresholds and the difficulties of reliably measuring low values or distinguishing between reefs over time and space. We believe that nutrients are an ecological problem for coral reefs. The two most likely problems arising from scientific studies is that nutrients reduce calcification in corals (Ferrier-Pages et al., 2000) and increase the abundance of small green and blue-green algae and other microrganisms that the erode the reef substratum (Holmes et al., 2000). In fact, these same experiments have shown that fertilization increased estimates of erosion by microbes, mostly microscopic algae, by a factor of 10 and that herbivores were only able to reduce these erosion rates by one half (Carriero-Silva et al., in press). We should, therefore expect nutrients to reduce coral reef growth and accumulation rates. There are probably other unexpected influences of microbes stimulated by nutrients such as increasing disease prevalence or virulence that may be uncovered with future studies. Nevertheless, the often-stated cause for a rapid shift in reef ecology towards high frondose algal cover through a slight elevation in seawater nutrient concentrations that are near the levels of detection is simply not supported by recent experimental evidence (Miller et al., 1999; Diaz-Pulido and McCook, 2003; McClanahan et al., 2002, 2003) and should not be perpetuated into the popular and semi-popular literature.
References Andrefouet, S., Mumby, P.J., McField, M., Hu, C., Muller-Karger, F.E., 2002. Revisiting coral reef connectivity. Coral Reefs 21, 43–48.
Bell, P.R.F., 1992. Eutrophication and coral reefs––some examples in the Great Barrier Reef lagoon. Water Research 26, 553–568. Carpenter, R.C., 1990. Competition among marine macroalgae: a physiological perspective. Journal of Phycology 26, 6–12. Carriero-Silva, M., McClanahan, T.R., Kiene, W., in press. The role of inorganic nutrients and herbivory in controlling microbioerosion of carbonate substrate. Coral Reefs. Chavez, E.A., Hidalgo, E., Izaguirre, M.A., 1985. A comparative analysis of Yucatan coral reefs. In: Proceedings of the 5th International Coral Reef Symposium 3, pp. 395–399. Delgado, O., Lapointe, B.E., 1994. Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13, 151–159. Diaz-Pulido, G., McCook, L.J., 2003. Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84, 2026–2033. Ferrier-Pages, C., Gattuso, J.-P., Dallot, S., Jaubert, J., 2000. Effect of nutrient enrichment on growth and photosynthesis of the zooanthellate coral Stylophora pistillata. Coral Reefs 19, 103–113. Gardner, T.A., Cote, I.M., Gill, J.A., Grant, A., Watkinson, A.R., 2003. Long-term region-wide declines in Caribbean corals. Science 301, 958–960. Holmes, K.E., Edinger, E.N., Limmon, H.G.V., Risk, M.J., 2000. Bioerosion of live massive corals and branching coral rubble on Indonesian coral reefs. Marine Pollution Bulletin 40, 606– 617. Hughes, T.P., 1994. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551. Johannes, R.E., Wiebe, W.J., Crossland, C.J., Rimmer, D.W., Smith, S.V., 1983. Latitudinal limits of coral reef growth. Marine Ecology Progress Series 11, 105–111. Kleypas, J.A., McManus, J.W., Menez, L.A.B., 1999. Environmental limits to coral reef development: where do we draw the line? American Zoologist 39, 146–159. Lapointe, B.E., 1997. Nutrient thresholds for bottom-up control of macroalgal blooms on corals reefs in Jamaica and Southeast Florida. Limnology and Oceanography 42, 1119–1131. Lapointe, B.E., 1999. Simultaneous top-down and bottom-up forces control macroalgal blooms on coral reefs. Limnology and Oceanography 44, 1586–1592. Lapointe, B.E., 2004. Phosphorus-rich waters at Glovers Reef, Belize? Marine Pollution Bulletin, doi:10.1016/j.marpolbul.2003.10.003. Lapointe, B.E., Littler, M.M., Littler, D.S., 1993. Modification of benthic community structure by natural eutrophication: the Belize Barrier Reef. In: Proceedings of the 7th International Coral Reef Symposium, Guam 1, pp. 323–334. Leichter, J.J., Stewart, H.L., Miller, S.L., 2003. Episodie nutrient transport of Florida coral reefs. Limnology and Oceanography 48, 1394–1407. Littler, D.S., Littler, M.M., 2000. Caribbean Reef Plants. Offshore Graphics, Inc., Washington, DC. 542 pp. Littler, M.M., Littler, D.S., Titlyanov, E.A., 1991. Comparisons of Nand P-limited productivity between high granitic islands versus low carbonate atolls in the Seychelles Archipelago: a test of the relativedominance paradigm. Coral Reefs 10, 199–209. McClanahan, T.R., 2002. The near future of coral reefs. Environmental Conservation 29, 460–483. McClanahan, T.R., Muthiga, N.A., 1998. An ecological shift in a remote coral atoll of Belize over 25 years. Environmental Conservation 25, 122–130. McClanahan, T.R., Aronson, R.B., Precht, W.F., Muthiga, N.A., 1999. Fleshy algae dominate remote coral reefs of Belize. Coral Reefs 18, 61–62. 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. Marine Pollution Bulletin 44, 441–451.
Correspondence / Marine Pollution Bulletin 48 (2004) 196–199 McClanahan, T.R., Sala, E., Stickels, P., Cokos, B.A., Baker, A., Starger, C.J., Jones, S., 2003. Interaction between nutrients and herbivory in controlling algal communities and coral condition on Glover’s Reef, Belize. Marine Ecology Progress Series 261, 135–147. Miller, M.W., Hay, M.E., Miller, S.L., Malone, D., Sotka, E.E., Szmant, A.M., 1999. Effects of nutrients versus herbivores on reef algae: a new method for manipulating nutrients on coral reefs. Limnology and Oceanography 44, 1847–1861. Ostrander, G.K., Armstrong, K.M., Knobbe, E.T., Gerace, D., Scully, E.P., 2000. Rapid transition in the structure of a coral reef community: the effects of coral bleaching and physical disturbance. Ecology 97, 5297–5302. Rayner, R.F., Drew, E.A., 1984. Nutrient concentrations and primary productivity at the Peros Banhos and Salomon Atolls in the Chagos Archipelago. Estuarine Coastal and Shelf Science 18, 121–132. Shulman, M.J., Robertson, D.R., 1996. Changes in the coral reef of San Blas, Caribbean Panama:1983 to 1990. Coral Reefs 15, 231– 236. Smith, S.V., Jokiel, P.L., 1978. Water composition and biogeochemical gradients in the Canton Atoll Lagoon. Atoll Research Bulletin 221, 15–53. Steneck, R.S., Dethier, M.N., 1994. A functional group approach to the structure of algal-dominated communities. Oikos 69, 476–498. Wafar, M.V.M., Devassy, V.P., Slawyk, G., Goes, J., Jayakumar, D.A., Rajendran, A., 1985. Nitrogen uptake by phytoplankton and zooxanthellae in a coral atoll. In: Proceedings of the 5th International Coral Reef Symposium 6, pp. 29–37.
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T.R. McClanahan The Wildlife Conservation Society Bronx, NY, USA E-mail address: [email protected] E. Sala Center for Marine Biodiversity and Conservation Scripps Institution of Oceanography La Jolla, CA, USA P.J. Mumby Marine Spatial Ecology Lab School of Biological Sciences Hatherly Laboratory University of Exeter Exeter United Kingdom S. Jones CERC, Columbia University NY, USA
Correspondence Phosphorus and nitrogen enrichment do not enhance brown frondose ‘‘macroalgae’’ Caribbean coral reefs have experienced a loss of coral cover from around 50% to <10% of their substratum in the past 30 years (Gardner et al., 2003) and in many cases this space has been occupied by frondose algae, specifically the brown frondose algal taxa in the genera Dictyota, Lobophora, Padina, Sargassum, and Turbinaria. This has occurred in reefs throughout the region, largely irrespective of the level of human influences or nutrient status of the reefs (Hughes, 1994; Shulman and Robertson, 1996; Lapointe, 1997; McClanahan and Muthiga, 1998; Ostrander et al., 2000; Gardner et al., 2003). Suggested factors are many and include disease, loss of herbivores, thermal anomalies, dust, hurricanes, and nutrients enrichment (McClanahan, 2002). Given the spatial extent of this problem it is unlikely that the ecological change is due to localized factors such as ground water or point-source nutrient pollution. At that scale oceanographic factors are considerably stronger than local influences by as much as two orders of magnitude (Leichter et al., 2003). Remote areas such as Glovers reef are, therefore, very unlikely to be regularly influenced by groundwater or terrestrial runoff, but could experience upwelling by both regular trade winds and hurricanes and on rare occasions by terrestrial runoff (Andrefouet et al., 2002). The remote location provides a good location to experimentally evaluate nutrient influences on reef organisms as direct human pollution is likely to uncommon and the site provides a good baseline for experimentally increasing possible human influences. Lapointe reinterprets the results of our study to claim support for the statement that nutrients enhance ‘‘macroalgae’’. Our study showed that the addition of a fertilizer mixed with both phosphorus and nitrogen enhanced the cover and colonization of the green turf alga Enteromorpha prolifera but not the brown frondose algae of the above taxa that are common to these and other disturbed reefs (McClanahan et al., 2002). E. prolifera, which has a thallus width of 100 lm and branchlets <500 lm (Littler and Littler, 2000), formed turfs about 1 cm tall in our fertilized treatment. The definition of ‘‘macroalgae’’ varies between investigators but we would consider ‘‘macroalgae’’ to be those macrophytes with morphologies that have a cortex and 0025-326X/$ - see front matter Ó 2003 Published by Elsevier Ltd. doi:10.1016/j.marpolbul.2003.10.004
medulla, a thallus size >1 cm, and gross standing height of >5 cm (Steneck and Dethier, 1994), and hence E. prolifera does not, to us, qualify as ‘‘macroalgae’’. Because of definitional problems among investigators, we did not use this terminology to describe our algae as the term is vague, can be too inclusive to be useful, and, therefore, susceptible to misuse in support of favoured hypotheses. In fact, we said ‘‘phosphorus enrichment can lead to rapid colonization of space by filamentous turf communities but not high biomass and dominance of erect frondose algae’’. Moreover, the cover of E. prolifera in our fertilized treatment, although greater than in the other treatments, was of only 32% of total algal cover. This increase in cover of a small turf alga, although statistically significant, is not the dramatic increase in ‘‘macroalgal’’ cover suggested by Lapointe. Our findings do not support some predictions of the Relative Dominance Model (RDM––Littler et al., 1991), notably the predication that high nutrients and low grazing will enhance large algae. In fact, the opposite appears to be true. High nutrients suppress the large brown frondose algae in a competitive field environment (as opposed to physiological studies in containers) and subsequent studies indicate that this result is not due to the level of enhancement or proportion of nitrogen and phosphorus (McClanahan et al., 2003). This may, however, not be the case for large red and green algae (McClanahan et al., 2003). There are likely to be differences in the physiological limitations and growth response of various algae to different concentrations and ratios of nitrogen and phosphorus (Delgado and Lapointe, 1994; Littler et al., 1991) but we do not believe the addition of more nitrogen would improve conditions in the field for frondose brown algae and significantly change our results. In the contested study we used a high phosphorus fertilizer where each application had 500 g of P2 O5 and 100 g of NH4 . Although we believed phosphorus was likely to be the more limiting of the two nutrients we included nitrogen at levels such that it should not limit production. In a subsequent experiment in the following year we nearly tripled the dosage of nitrogen to 270 g with the nitrogen being a mixture of ammonium and nitrate (McClanahan et al., 2003). This study produced the same results, high turf and low frondose dominance in the nutrient-enriched treatments. It may prove useful to continue studies with even higher levels of nitrogen or reduced P:N ratios to determine the
Correspondence / Marine Pollution Bulletin 48 (2004) 196–199
possible effects on high nitrogen, but we are sceptical that this will improve conditions for frondose algae as poor success of frondose algae is probably not due to physiological limitations but more likely due to competitive abilities in the presence of high nutrients. Species with smaller thalli and higher surface area to volume ratios are more likely to do well under these conditions and competitively exclude the larger frondose taxa (Carpenter, 1990). Phosphorus and nitrogen are dissolved with oxygen in seawater and spectrophotometric methods measure the concentrations of the total molecule and not just these elements alone. Consequently, when calculating molar concentrations by the methods we used it is necessary to use the full molecular weight of PO34- of 95 and not just that of phosphorus of 31. Our reported concentration of 0.3 lM is correct and fits well with other reports for this region and reef atolls. For example, an unpublished study in this same reef by Mumby using an Autoanalyzer and a 1 cm cell, found SRP absolute levels to be 0.35–0.39 M. Nearby in the Chinchorro Bank of Mexico Chavez et al. (1985) reported 0.78 lM and in other reef atolls such as the Abrolhos Islands, Indian Ocean 0.21–0.37 lM (Johannes et al., 1983), Kavaratti Atoll, Indian Ocean, 0.34 lM (Wafar et al., 1985), Maldives 0.43–0.58 lM (Rayner and Drew, 1984), and Canton Atoll, Phoenix Islands, 0.56 lM (Smith and Jokiel, 1978). The levels of SRP levels for Glovers Atoll are greater than those reported at nearshore area of Twin Cays of 0.14 lM (Lapointe et al., 1993) and those reported by Lapointe in his Table 1. Our study in Glovers in the subsequent year reports 0.16 lM (McClanahan et al., 2003), which is closer to Lapointe’s numbers for the barrier reef and the global average for coral reefs reported as 0.13 lM (Kleypas et al., 1999). Lapointe’s undetectable values in offshore areas of Belize have not been found in other studies of the same reef environment and are anomalous compared to other nutrient studies in remote reef atolls. Studies of physiological limitations and growth experiments of isolated algae in containers (Littler et al., 1991; Delgado and Lapointe, 1994) with different concentrations of nutrients are likely to be a poor analogue for field situations. Extrapolation of these container studies to establishing nutrient ‘‘thresholds’’ in the field is likely to be fraught with scaling and other real-world problems. There is no assurance that growth estimates taken from containers will result in an accumulation of biomass in the field where physical disturbances, competition, and predation can produces losses that can more than compensate for growth. The establishment of ‘‘nutrient thresholds’’ has been used prematurely before being tested and confirmed in field situations and is possibly deceptive and overused guideline that should be used cautiously if not eliminated from our science.
197
The proposed thresholds may have found utility or produced significant correlations in some limited situations (see the correlative papers cited in Lapointe (1999)). When examining coral reefs on a larger scale it becomes clear, however, that the correlations between nutrients and erect or frondose algae abundance are not the cause of frondose algal dominance as they do not predict the ecological responses for all reefs. For example, Lapointe et al. (1993) used the low nutrient concentrations and frondose algal cover reported in a few visited sites in Belize to support the nutrient limitation hypothesis. But, when viewed across more sites in Belize it is clear that brown frondose algae dominate many of the barrier and reef atoll environments, often being more than 50% of the benthic cover (McClanahan and Muthiga, 1998; McClanahan et al., 1999). The threshold concept can largely be rejected outright or be seen as highly contingent on other environmental factors because the suggested thresholds (Bell, 1992; Lapointe, 1997) are below the mean nutrient concentrations reported for 1000 coral reefs (Kleypas et al., 1999). If we were to strictly apply these thresholds the frondose algae should dominate over half of the reefs in the world, which is not the case, particularly outside the Caribbean. Some of the nutrients, particularly nitrogen, are highly variable in the reef environment and can easily range over an order of magnitude within days to months (Leichter et al., 2003). This sort of variation would make it difficult to make a limited number of measurements in time and space and establish a clear point where reefs are eutrophied. Finally, for those investigators that favour the nutrient limitation any coincidence between measurable nutrients and frondose algae can be used as support for this hypothesis. They are less likely to apply the same criteria for reefs where nutrients are measurable but erect frondose algal cover low. The utility of low thresholds may also be a problem in applying. As pointed out by Lapointe (2004) the low levels of nutrients found in corals reefs are difficult to measure and the lowest levels may require special tools such as a longer absorption cell and a specialized spectrophotometer. Aspects of handling the samples and the laboratory conditions also become very important at these low levels. For example, commonly purchased distilled water often has higher nutrient concentrations than the reef water being sampled and the use of distilled water for rinsing glassware can contaminate samples. This means that acid needs be used for washing glassware. Lapointe and others will seldom bring their specialized and expensive laboratories to the field and it is common practice to freeze samples, ship, and analyze them later. We have found, however, that this process can produce errors possibly by the long time it takes to freeze seawater in insulated coolers or by releasing phosphorus from organisms that may have been repeatedly frozen and thawed. Therefore, we prefer to
198
Correspondence / Marine Pollution Bulletin 48 (2004) 196–199
analyze samples in the field within a short period after the collection. We, therefore, used a portable spectrophotometer and the ascorbic acid method (Method 8048) and a 2.5 cm cell that has a lower limit of 0.02 mg/l or 0.2 lM. This is the one of nine possible methods that Hach gives for phosphates and the one that gives the lowest detection levels. The digital read out gives values of 0.01, which we use but may be below values were measurements are reliable. Preliminary tests of known concentrations suggest that the coefficient of variation around the means increases from <9% to 25% below 0.5 lM (Jones, S., unpublished data). This indicates that at the low levels reported for coral reefs that it may be very hard to distinguish sites or values reported in the literature, assuming these reports use similar methods. Nonetheless, we view the blue coloration from the reaction and this indicates that phosphates are in the water and at detectable levels, but the sensitivity of the spectrophotometer or cell length used to test for absorption may improve the accuracy of the measurements, these factors do not account for the measurable and average quantities of phosphates we found in Glovers Reef. Our study underpins the lack of efficacy of nutrient thresholds and the difficulties of reliably measuring low values or distinguishing between reefs over time and space. We believe that nutrients are an ecological problem for coral reefs. The two most likely problems arising from scientific studies is that nutrients reduce calcification in corals (Ferrier-Pages et al., 2000) and increase the abundance of small green and blue-green algae and other microrganisms that the erode the reef substratum (Holmes et al., 2000). In fact, these same experiments have shown that fertilization increased estimates of erosion by microbes, mostly microscopic algae, by a factor of 10 and that herbivores were only able to reduce these erosion rates by one half (Carriero-Silva et al., in press). We should, therefore expect nutrients to reduce coral reef growth and accumulation rates. There are probably other unexpected influences of microbes stimulated by nutrients such as increasing disease prevalence or virulence that may be uncovered with future studies. Nevertheless, the often-stated cause for a rapid shift in reef ecology towards high frondose algal cover through a slight elevation in seawater nutrient concentrations that are near the levels of detection is simply not supported by recent experimental evidence (Miller et al., 1999; Diaz-Pulido and McCook, 2003; McClanahan et al., 2002, 2003) and should not be perpetuated into the popular and semi-popular literature.
References Andrefouet, S., Mumby, P.J., McField, M., Hu, C., Muller-Karger, F.E., 2002. Revisiting coral reef connectivity. Coral Reefs 21, 43–48.
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T.R. McClanahan The Wildlife Conservation Society Bronx, NY, USA E-mail address: [email protected] E. Sala Center for Marine Biodiversity and Conservation Scripps Institution of Oceanography La Jolla, CA, USA P.J. Mumby Marine Spatial Ecology Lab School of Biological Sciences Hatherly Laboratory University of Exeter Exeter United Kingdom S. Jones CERC, Columbia University NY, USA