Correspondence - Marine Spatial Ecology Lab


Correspondence - Marine Spatial Ecology Lab
Marine Pollution Bulletin 48 (2004) 196–199
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.
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
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
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.
Andrefouet, S., Mumby, P.J., McField, M., Hu, C., Muller-Karger,
F.E., 2002. Revisiting coral reef connectivity. Coral Reefs 21,
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,
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–
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,
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–
Smith, S.V., Jokiel, P.L., 1978. Water composition and biogeochemical
gradients in the Canton Atoll Lagoon. Atoll Research Bulletin 221,
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.
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
United Kingdom
S. Jones
CERC, Columbia University

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