interaction between inorganic nutrients and organic matter in controlling coral reef communities in...

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Marine Pollution Bulletin 50 (2005) 566–575

Interaction between inorganic nutrients and organic matterin controlling coral reef communities in Glovers Reef Belize

T.R. McClanahan a,*, R.S. Steneck b, D. Pietri c, B. Cokos a, S. Jones d

a Wildlife Conservation Society, Marine Programs, 2300 Southern Boulevard, Bronx, New York 10460-1099, USAb School of Marine Sciences, University of Maine, Darling Marine Center, Walpole, Maine, 04573, USA

c Center for Environmental Research and Conservation, Columbia University, 1200 Amsterdam Avenue, New York, NY 10027, USAd Osborne Laboratories of Marine Sciences, New York Aquarium, Wildlife Conservation Society, Surf Avenue at West 8th Street,

Brooklyn, New York 11224, USA

Abstract

We studied the responses of algae, corals, and small fish to elevated inorganic fertilizer, organic matter, and their combination

over a 49-day summer period in cages that simulated the coral reef in the remote Glovers reef atoll, Belize. The addition of organic

matter reduced while fertilization had no effect on the numbers of herbivorous damsel and parrotfishes. All measures of algal bio-

mass were influenced by fertilization. The combined inorganic and organic enrichment produced the highest algal biomass, which is

most likely due to the combined effect of higher nutrients and lower herbivory. The cover of turf and total algae were influenced by

all treatments and their interactions and most strongly and positively influenced by fertilization followed by organic matter and the

combination of organic matter and inorganic fertilizer. The inorganic and combined treatments were both dominated by two turf

algae, Enteromorpha prolifera and Digenia simplex, while the nonfertilized treatments were dominated by brown frondose algae

Lobophora variegata, Padina sanctae, and Dictyota cervicornis. The organic matter treatment had greater cover of P. sanctae and

D. cervicornis than the untreated control, which was dominated by Lobophora variegata, also the dominant algae on the nearby

patch reefs. Crustose corallines grew slowly (�2.5 mm/49 days) and were not influenced by the treatments when grown on vertical

surfaces but decreased on horizontal coral plates in the combined organic matter and fertilization treatment. No mortality occurred

for the two coral species that were added to the cages. Porites furcata darkened in the fertilized cages while there was a mix of paling

and darkening for a small amount of the coral tissue of Diploria labyrinthiformes. Inorganic fertilization stimulates small filamentous

turf algae and Symbiodinium living in coral but inhibits brown frondose algae. Organic matter inhibits small herbivorous fish, L.

variegata, and encrusting coralline algae when growing on horizontal surfaces.

� 2005 Published by Elsevier Ltd.

Keywords: Algal growth; Brown algae; Coralline algae; Fertilization; Organic matter; Nitrogen; Phosphorus; Pollution

1. Introduction

The ecology of coral reefs has changed as a result of

recent disturbances (McClanahan, 2002; Szmant, 2002;

Hughes et al., 2003; Gardner et al., 2003). This change

0025-326X/$ - see front matter � 2005 Published by Elsevier Ltd.

doi:10.1016/j.marpolbul.2005.01.005

* Corresponding author. Address: Kibaki Flats #12, Coral Reef

Conservation Project, Kenyatta Beach Bamuri, P.O. Box 99470,

Mombasa, Kenya. Tel.: +254 11 485570; fax: +254 11 472215.

E-mail address: [email protected] (T.R. McClanahan).

has, in some instances, been explained by changes inwater quality associated with increased agriculture and

urbanization near coastal ecosystems (Smith et al.,

1981; Littler et al., 1991; Bell and Elmetri, 1995; Lapo-

inte, 1999). High levels of inorganic nitrogen and phos-

phorus concentrations are often considered to be the

main contribution to this change, although pollution

has many constituents. Organic matter is a second major

component of pollution associated with dead and decay-ing plants and human and animal waste. The role of

mailto:[email protected]

T.R. McClanahan et al. / Marine Pollution Bulletin 50 (2005) 566–575 567

organic matter, which is frequently associated with inor-

ganic nutrients, has not been separated from inorganic

enrichment or well studied on corals, algae, and the

associated fish communities. It is possible that other

constituents of pollution cause some of the observed

patterns of reef degradation often associated with nutri-ents. For example, inorganic nutrient enrichment exper-

iments have failed to find a clear relationship between

their concentrations and the enhanced abundance of

brown frondose algae (Miller et al., 1999; Koop et al.,

2001; Diaz-Pulido and McCook, 2003; McClanahan

et al., 2002, 2003), a common dominant on degraded

reefs (McClanahan, 2002; Gardner et al., 2003; Hughes

et al., 2003). In order to understand the full conse-quences of pollution, the other constituents of pollution

must be experimentally manipulated to determine their

potential role in reef degradation. Here, we studied inor-

ganic and organic enrichment in an experimental design

that allowed us to evaluate the individual factors and

their interaction. We examined the response of these

two factors on three aspects of the coral reef, namely

benthic algae, hard corals, and the small fish.

2. Methods

2.1. Study sites

This study was conducted in Glovers Reef, Belize in

the site described by McClanahan et al. (2002). Theimportant features of this site are that it is a large and

remote coral reef atoll situated approximately 45 km

off the coast of mainland Belize. The study was con-

ducted in a portion of the atoll lagoon where a marine

reserve has excluded fishing since 1995. The study was

conducted in a water depth of 2-m on the windward side

of one patch reef approximately 150 m offshore from the

Middle Cay Research Station dock. Therefore, the siteand background conditions were unlikely to be influ-

enced greatly by mainland or urban waste and runoff.

The waters in this area are calm with a small (<0.5 m)

tidal range; low currents (<1 m/s) and no waves or other

physical disturbances such as hurricanes were experi-

enced during this summer study period (June to August

2002).

2.2. Experimental design and measurements

Using 16 closed cages we exposed corals, algal, and

associated fish communities to two levels of organic

matter and an inorganic slow-release fertilizer in a

two-factor and two-level interactive design. One treat-

ment was the environmental background conditions

and additions of fertilizer and organic matter were ap-plied to the other treatments. There were four replicates

per treatment: (1) control or background conditions, (2)

the addition of organic matter, (3) the addition of inor-

ganic fertilizer and the (4) the addition of both organic

and inorganic fertilizer. Cages were constructed with

PVC frames with dimensions of 50-cm lengths and

widths and 20-cm heights and covered by a 3-cm mesh

plastic caging material. Cages were tied to cement ma-sonry blocks, which kept them solidly on the reef bot-

tom. Cages were cleaned of algae and other settling

organisms with wire brushes every other day.

Closed-top treatments exclude large herbivorous

fishes and larger predators but allow small fishes such

as damselfishes (Stegastes spp.), wrasses, and small par-

rotfish (Sparisoma aurofrenatum and Scarus iserti) to

enter and forage (McClanahan et al., 2002), and wecounted their abundance in each cage three times over

the study period. During counts each cage was observed

for 3 min, taking care not to disturb the area by stirring

sediments or abrupt movements. Within each cage, the

number of damselfish, parrotfish, and wrasses observed

during 1 min were counted.

Inorganic fertilizer was added to half of the cages as

previously described (McClanahan et al., 2002, 2003)such that each fertilized cage received two doses of

500 g P2O5, 215 g ammonium and 57.5 g nitrates distrib-

uted beneath the cage at a monthly interval. The addi-

tion of 5-kg of untreated and fine sawdust collected

from a sander at a local woodshop constituted the or-

ganic matter treatment. Wood dust was placed in fine

mesh nylon bag (i.e. mosquito netting) and placed be-

neath half of the cages. In the combined inorganic andorganic matter enrichment the fertilizer was added to

the wood dust in the same mesh bag.

Water samples were collected 1-cm above the coral

plates in acid-washed 100 ml and 500 ml bottles and

analyzed for suspended solids, nitrate, and soluble phos-

phates on the same day with a Hach DR/2500 spectro-

photometer using the cadmium reduction for nitrate

and ascorbic acid methods for phosphorus. Sampleswere collected twice, one week after the initiation of

the experiment and one week before the end of the

experiment. Unrealistically high values of phosphates

in the second sampling period in control cages indicated

contamination of these samples and these data were,

therefore, not presented.

Eight plates of dead Acropora palmata were placed in

each cage along with living coral to simulate the reefbenthos. Plates collected from the shallow reef flat on

the windward side of the atoll rim were scraped with a

wire brush and bumps removed with a stone blade of

a hacksaw to ensure similar initial conditions and to

make it easier to scrape algae from their surfaces. De-

spite the scraping, some crustose coralline algae re-

mained. Seven of the plates were used for the weekly

sampling of algal biomass and one was sampled at theend of the experiment for analysis of algal species com-

position. During the weekly sampling, the relative cover

568 T.R. McClanahan et al. / Marine Pollution Bulletin 50 (2005) 566–575

of algal functional groups (turf, coralline, and brown

frondose fleshy) was estimated by randomly dropping

the point of a pencil on each of five randomly selected

plates twenty times. Frondose algae include all large

Phaeophyta such as species in the genera Dictyota,

Lobophora, Padina, and Sargassum. No green calcare-ous algae (i.e. Halimeda) or red frondose algae were ob-

served during these weekly surveys.

Algal scrapping samples were removed with a razor

or sharp knife from a 10 · 10-cm area for weight and

20 · 20-cm area for species composition samples.

Weight samples were placed in pre-weighted tinfoil

and weighted for wet weights, oven-dried for 45–60

min at 90–120 �C and weighted again for dry weights.Dry samples were then placed in hydrochloric acid

(0.5 M HCl) overnight and then re-weighed after being

filtered and dried as above for decalcified weights.

The algal species composition samples were taken at

49 days and placed in 4% formaldehyde for microscopic

analysis of the species composition. All fragments of

alga that were >1 cm in length observed under a 100x

observational microscope and sorted to the lowest pos-sible taxon using the nomenclature of Littler and Littler

(2000). Finally, wet weights were taken with a Mettler

Balance (precision ± 0.001 mg) for each species.

Coralline algal cover and growth is often difficult to

determine from the above methods and we, therefore,

undertook a separate set of measurements to specifically

measure their growth rates under the experimental con-

ditions. We collected dead Millepora complanata fromthe reef edge that were approximately 100 cm2 in size

and entirely covered with the coralline alga Paragoniolit-

hum accretum. To measure growth, three quarters of the

specimen was submerged in water and the air-exposed

portion burned with a blowtorch. Immediately, the dead

burned portion of the thallus became discolored, thus

creating a clean growing edge. To identity the live/dead

transition for subsequent growth, a straight-line incisionwas made with a hacksaw on this edge. Two pieces of

these treated M. complanata skeletons were fastened to

the vertical sides of the cages with cable ties, one on

the inside and the other on the outside of the cage. This

was expected to simulate low and high herbivory condi-

tions. After 49 days the rubble was removed, dried and

examined under a binocular microscope and the maxi-

mum extension of coralline lateral growth beyond theincision line was measured with a dissecting microscope

to the nearest 0.5 mm. Growth rate for each rubble and

treatment was estimated as the maximum extension of

the coralline over the 49-day period and compared for

the treatments of inorganic fertilizer, organic matter,

and herbivory.

No less than six coral branches or fragments of Dipl-

oria labyrinthiformes and P. furcata were placed in eachof the cages. The condition and color of these corals

were examined for coloration and living and dead tissue

at the beginning and at weekly intervals during the

experiment. An estimate of the percentage of coral cover

that was normal, pale, or darkened in each cage was re-

corded for each species. Pale corals lost color and some

white skeleton could be seen through the tissue. Dark-

ened corals often turned dark green or brown.

2.3. Statistical analyses

The design of the experiment allowed us to perform a

two-factor multivariate repeated-measures ANOVA

with time, organic matter, and inorganic nutrient treat-

ments and their interactions being the factors examined.

A Detrended Correspondence Analysis (Sall et al., 2001)was performed to characterize the main patterns of var-

iation in the abundance of algal species with respect to

the treatments.

3. Results

3.1. Water qualilty

The addition of organic matter did not change the

concentrations of nitrates or phosphates in these treat-

ments (Table 1). Supended solids were not influenced

by the addition of organic matter in the first sampling

period but elevated in the second sampling period. Inor-

ganic nutrient fertilization increased nitrate concentra-

tions in the first but not the second sampling periodand mean phosphate levels increased from 0.04 mg/l to

0.07 mg/l in the first sampling period. Suspended solids

were also elevated 2 to 4 times above control levels dur-

ing both sampling periods in the fertilized treatment and

had a significant interaction with the organic matter

treatment.

3.2. Fish occupation of cages

Wrasse numbers were unaffected by the experimental

treatments but damselfish and parrotfish were less abun-

dant in the organic matter addition treatment than the

control or other treatments (Table 2). Parrotfish num-

bers increased over time in all cages but less so in the or-

ganic matter treatment which resulted in significant time

and time · organic matter interactions.

3.3. Algal abundance and species composition

Wet, dry, and decalcified algal biomass increased in

all treatments for the first 30 days before either stabilis-

ing or decreasing until the end of the experiment at 49

days (Fig. 1, Table 3). Fertilization influenced all while

organic matter alone did not influence any measure ofalgal biomass. The highest biomass of wet and dry

weights were, however, in the treatment with both

Table 1

Summary of nutrient and suspended solid concentrations in the four treatments and tests of statistical significance

Time Factors, n = 4 ANOVA, 1 df

Nitrate (mg/l) Phosphate (mg/l) Suspended solids (mg/l)

Mean Sem F p Mean Sem F p Mean Sem F p

Time 1 Control 0.01 0.003 0.04 0.03 13.3 1.4

Organic 0.02 0.005 0.37 NS 0.03 0.01 0.65 NS 12.5 4.3 1.5 NS

Fertilizer 0.03 0.006 4.97 0.05 0.07 0.02 4.28 0.06 23.5 8.5 5.9 0.03

Organic/fertilizer 0.03 0.009 0.04 NS 0.14 0.06 1.18 NS 46.0 15.2 1.7 NS

Time 2 Control 0.02 0.007 No data 6.8 1.7

Organic 0.03 0.005 0.49 NS 7.3 0.9 9.6 0.01

Fertilizer 0.02 0.004 0.05 NS 28.3 1.7 47.8 0.001

Organic/fertilizer 0.02 0.005 0.05 NS 14.8 3.4 11.1 0.01

Table 2

Statistical summary of the response of fish numbers in the cages to the experimental treatments

Damsel fish Wrasse Parrotfish Total fish

Mean Sem Mean Sem Mean Sem Mean Sem

Control 3.5 0.8 5.6 2.5 9.9 2.6 15 4.6

Organic 2.1 0.8 5.0 3.6 5.8 3.0 9.6 5.4

Fertilizer 3.9 0.7 4.4 2.6 8.2 2.0 15 4.0

Organic/fertilizer 2.6 0.7 2.9 1.3 4.1 4.5 5.4 2.3

Comparison of means

df F p df F p df F p df F p

Time 2 0.06 NS 2 0.77 NS 2 10.5 0.00 2 0.5 NS

Organic 1 8.76 0.01 1 0.27 NS 1 8.2 0.01 1 8.02 0.01

Fertilizer 1 0.97 NS 1 0.64 NS 1 2.1 NS 1 0.9 NS

Organic · fertilizer 1 0.01 NS 1 0.05 NS 1 0.6 NS 1 0.5 NS

Time · fertilizer 2 0.15 NS 2 1.69 NS 2 1.4 NS 2 0.5 NS

Time · organic 2 2.20 NS 2 1.36 NS 2 3.2 0.06 2 0.4 NS

Time · organic · fertilizer 2 0.39 NS 2 0.08 NS 1 2.4 NS 2 0.7 NS


organic matter and fertilization. The interaction of time,

organic matter, and fertilization influenced all measures

of algal biomass.

Total, turf, and frondose brown algae cover were

influenced by time while crustose corallines were not

(Fig. 2, Table 4). Turf and total algae were also influ-

enced by all treatments and their interactions but most

strongly by fertilization followed by time, organic mat-ter, and organic matter · fertilization. Total algal cover

increased up to about 28 days and leveled at different

values for the various treatments. The highest total algal

cover was achieved in the fertilized and organic matter

additions at about 80% cover and the dominant algae

were Enteromorpha prolifera and Digenia simplex (Fig.

3). The single-factor control and organic matter treat-

ments leveled at the lowest cover of 30% and the fertil-ized treatment was intermediate between these groups.

Frondose brown algae did not develop greatly until after

30 days and was also influenced by all treatments except

the combined organic and fertilization treatment or the

interaction of all factors. Frondose brown algae did best

in the control and organic matter treatments and did not

develop in any treatments with fertilization. Lobophora

variegata was dominant in the controls and Dictyota cer-

vicornis and Padina sanctae dominated the organic mat-

ter enriched treatement (Fig. 3).

Crustose corallines on the horizontal coral plates did

not change with time and decreased slightly in the

organic matter treatment (p < 0.08) and signficantly in

the combined organic matter and fertilizer treatment(Table 4). Growth of crustose corallines on the rubble at-

tached to the vertical sides of the cages was low at �2.5

mm in 49 days. None of the effects of herbivory, fertilza-

tion, organic matter, or their interactions were statisti-

cally significant for their linear growth rates (Table 5).

3.4. Coral survival and coloration

There was no coral mortality in any treatments but

there were notable changes in the coloration of the cor-

als for both studied species. Porites furcata did not pale

in any treatment but there was a gradual increase in the

darkening, affecting up to 18% of the tissue cover in the

fertilized and fertilized and organic matter addition

Fig. 1. Plots of the (a) wet, (b) dry, and (c) decalcified weights of the algae on the experimental coral plates with time in the four experimental

treatments. Bars are standard errors of the mean.

Table 3

Statistical summary of the response of the algal weights to experimental treatments

Factor Wet weight Dry weight Decalcified

df F p df F p df F p

Time 6 7.4 0.001 6 4.1 0.001 6 3.6 0.001

Organic 1 0.4 NS 1 0.1 NS 1 1.0 NS

Fertilizer 1 8.2 0.01 1 3.6 0.06 1 11.7 0.001

Organic/fertilizer 1 9.5 0.001 1 5.6 0.02 1 2.3 NS

Time · fertilizer 6 1.6 NS 6 0.8 NS 6 0.9 NS

Time · organic 6 1.2 NS 6 0.8 NS 6 0.6 NS

Time · organic · fertilizer 6 2.9 0.01 6 2.9 0.01 6 3.2 0.01


cages with fertilization being the strongest factor (Fig. 4,

Table 6). The response of Diploria labyrinthiformes was

more complex with some patchy paling of less than 10%

of the tissue cover after day 35, mostly in the fertilized

cages but also in the control and organic matter treat-

ments. There was also a small and patchy darkening

of tissue after 14 days in the fertilized and fertilized

and organic matter additions.

Fig. 2. Plots of the major components of cover on the algal plates as a function of time in the four treatments. Bars are standard errors of the mean.

(a) Crustose coralline, (b) frondose brown alage, (c) turf algae, (d) % total algal coverage.

Table 4

Statistical summary of the response of the major cover components growing on the algal plates to the experimental treatments

Coralline cover Frondose brown Turf algae Total algae

df F p df F p df F p df F p

Time 6 0.9 NS 6 21.2 0.001 6 71.3 0.001 6 85.9 0.001

Organic 1 3.0 0.08 1 33.9 0.001 1 54.8 0.001 1 33.9 0.001

Fertilizer 1 0.01 NS 1 10.7 0.001 1 417.7 0.001 1 322.4 0.001

Organic/fertilizer 1 8.6 0.00 1 0.00 NS 1 43.6 0.001 1 52.8 0.001

Time · fertilizer 6 1.5 NS 6 3.4 0.001 6 13.4 0.001 6 9.2 0.001

Time · organic 6 0.7 NS 6 12.5 0.001 6 8.9 0.001 6 6.9 0.001

Time · organic · fertilizer 6 1.2 NS 2 0.00 NS 6 9.4 0.00 6 10.8 0.00


4. Discussion

This study was developed to extend on two similar

studies where the influences of nutrients, grazing, and

coral on benthic algae have been explored (McClanahan

et al., 2002, 2003). This study was specifically under-

taken to evaluate the possible role of organic matter in

reef ecology, which is an often-overlooked constituentof pollution in tropical waters. We used closed-top cages

to minimize the possibly large effects of big grazers on

our experiment, but smaller bodied grazers and preda-

tors where commonly observed in the cages and may

have played some role in influencing results. The inor-

ganic nutrient additions were similar to the previous

studies and had the effect of doubling to tripling concen-

trations of dissolved nitrogen and phosphorus, but

remaining within ranges found for coral reefs (Kleypas

et al., 1999). Wood dust was used as a source of organic

matter. Wood dust was expected to simulate decaying

plant matter and to contain undetectable levels of inor-

ganic nutrients that would not confound the experimen-

tal design. Inorganic nutrient concentrations measured

in seawater from the cages confirmed that there wasno elevation of inorganic nutrients in the wood-dust

treatments. Wood dust was expected to increase water

turbidity as measured by suspended solids and we found

a small elevation for the second but not the first sam-

pling period, which may be an effect of the decay and

dissolution of the wood over time. The suspended solids

measure increased the most, however, in the presence of

-0.5

0.0

0.5

1.0

1.5

2.0

c1

Corallines

Digenia simplex

-0.5 0.0 0.5 1.0 1.5 2.0c2

Species

Treatment

Padina sanctae

Dictyota cervicornis

Organic

Control

Lobophora variegata

Enteromorpha prolifera

Fertilized/Organic Fertilized

Fig. 3. Detrended correspondence analysis of the dominant algal taxa found in the four treatments.

Table 5

Statistical summary of the growth rate (mm/49 days) of crustose

coralline algae fastened to the vertical side of the cages in (low

herbivory) and outside of cages (high herbivory)

Treatment Inside cage Outside cage

Mean Sem Mean Sem

Control 3.5 1.2 2.0 1.7

Organic 3.4 0.6 1.5 0.3

Fertilizer 2.7 0.7 2.0 1.1

Fertilizer/organic 2.4 0.7 2.5 0.9

Total 3.1 0.4 2.0 0.5

Source Nparm df Sum of squares F p

Means comparisons

Herbivory 1 1 7.6 2.0 NS

Organic 1 1 0.07 0.0 NS

Fertilizer 1 1 0.4 0.1 NS

Organic/fertilizer 1 1 0.4 0.1 NS

Fertilizer · herbivory 1 1 3.7 1.0 NS

Organic · herbivory 1 1 0.1 0.0 NS


inorganic enrichment suggesting that inorganic nutrients

are a stronger factor than organic matter for this mea-

sure of water quality.

4.1. Inorganic nutrient effects

As in our previous studies inorganic nutrients in-

creased filamentous turf algae and decreased brownfrondose algae colonization and cover (McClanahan

et al., 2002, 2003). There were some similarities and dif-

ferences in the dominance of the turf algae in the three

studies. The green alga Enteromorpha prolifera was

among the dominant taxa in all three studies. In one

study the brown filamentous turf Hincksia mitchelliae

was abundant while the blue-green Lyngbya confervoides

dominated in another, and in both cases they were in

closed-top cages. These three taxa are, therefore, ex-pected to do well under conditions of high inorganic

nutrients and low herbivory. The red filamentous Dige-

nia simplex, the subdominant in this study has been

found variably in a variety of other treatments in this

and previous studies. It may therefore have a more com-

plex ecology but also grows well in high nutrients and

low herbivory conditions. Since these studies were all

undertaken in the same reef area but in three consecu-tive years between 2000 and 2002, there is notable in-

ter-annual variability in turf algal dominance, which is

unexplained by herbivory and nutrients alone.

Inorganic nutrients have been predicted to increase

the abundance of both coralline and frondose algae (Lit-

tler and Littler, 1984). Our and other studies have, how-

ever, consistently shown that brown frondose algae are

unaffected or grow poorly in the presence of inorganicfertilization in field experiments (Miller et al., 1999;

Diaz-Pulido and McCook, 2003; McClanahan et al.,

2002, 2003). This hypothesis therefore is largely unsup-

ported by field experiments and needs to be revised to

be useful for predicting responses of algal communities

to pollution. Coralline algae in our studies also appeared

to grow slowly and were largely unaffected by inorganic

nutrients on both vertical and horizontal surfaces anddifferent levels of herbivory. Bjork et al. (1995) found re-

duced growth and calcification rates for the encrusting

red coralline Lithophyllum kotschyanum in the presence

of phosphate but most of this reduction was found at

levels greater than those used in our experiments. They

also found a slight elevation of growth at moderate ele-

vations of nitrate. Their results suggest that for our

Fig. 4. Plots of the darkening and paling of the corals inhabiting the four experimental treatments with time. (a) % Darkened P. furcata, (b) % paling

D. labyrinthiformis, and (c) % darkened D. labyrinthiformis.

Table 6

Statistical summary repeated measures ANOVA for the changes in coral color in the four treatments

Paling of

D. labyrinthiformes

Darkening of

D. labyrinthiformes

Darkening of

P. furcata

df F p df F p df F p

Time 6 78.4 0.00 6 3.1 0.01 6 39.4 0.001

Organic 1 43.8 0.09 1 8.0 0.01 1 8.7 0.001

Fertilizer 1 8.0 NS 1 43.6 0.00 1 1035.5 0.001

Organic/fertilizer 1 128.6 0.00 1 8.0 0.01 1 8.7 0.001

Time · fertilizer 6 3.4 NS 6 3.1 0.01 6 39.4 0.001

Time · organic 6 18.2 NS 6 2.0 0.07 6 0.6 NS

Time · organic · fertilizer 6 42.6 0.01 6 2.0 0.07 6 0.6 NS


treatment, where nitrate and phosphate were combined

and concentrations elevated only moderately, that the

two effects may have been small, or cancelled, and pro-

duced little measurable change.


4.2. Organic matter effects

Organic matter enrichment reduced the abundance of

small grazing damselfish and parrotfish and this pro-

duced indirect effects in our experiments. We counted

fish in our study in order to account for possible indirecteffects that are likely to occur in natural ecosystems. The

causes for this reduction are unknown but may be due to

aspects of water quality, such as reduced visibility or dis-

solved oxygen, or a response to the availability of their

food or foraging rates. Because water quality was poor-

est in this combined enrichment treatment and did not

influence fish numbers it is unlikely that water quality

greatly influenced herbivorous fish numbers. Morelikely, the presence of organic matter reduced the attrac-

tion to forage or the brown frondose algae in this treat-

ment repulsed the herbivores. Repulsion of herbivores

may be likely when D. cervicornis is dominant because

it has secondary metabolites that are avoided by fish

(Littler et al., 1983; Hay, 1991) but P. sanctae is pre-

ferred forage of coral reef herbivores (Hay, 1984; Lewis,

1985; McClanahan, 1999). Consequently, reduced for-aging in the organic matter treatment is likely to explain

the higher abundance of P. sanctae and suggests that the

presence of organic matter was more important than

chemically defended algae in reducing herbivores in this

treatment.

L. variegata dominated the controls and the natural

reef substratum on these reefs (McClanahan, 1999). It

is less preferred by herbivores (McClanahan, 1999)and the prostrate shape of its early growth form may

promote its smothering in the organic matter treatment.

It may, however, be a competitive dominant in the ab-

sence of organic and inorganic enrichment. The higher

abundance of D. cervicornis in the organic matter treat-

ment is more difficult to explain but was likely to be

influenced by reduced herbivory and less competition

with L. variegata. Organic matter mixed with algal foodis expected to reduce the nutrition of the forage, forag-

ing, and herbivore numbers. Conversely, in a past exper-

iment we found that damselfish bite rates increased in

inorganically fertilized treatments, although it did not

affect their numbers (McClanahan et al., 2003).

Regardless of the mechanism, this finding suggests

that the organic matter constituent of pollution has

the potential to reduce herbivores and therefore the po-tential for an indirect positive influence on some algae

that can avoid being smothered. In this study, the posi-

tive effect of organic matter was on D. cervicornis and P.

sanctae but also total algal biomass when combined with

the inorganic nutrient enrichment. In the combined

enrichment treatment the effect was to increase the bio-

mass of filamentous turf algae, largely E. prolifera. The

accumulation of organic matter on horizontal surfaces isalso detrimental coralline algae.

4.3. Conclusions

The results of this and previous related studies suggest

a complex interaction between herbivory, nutrients, and

organic matter on reef communities. Inorganic nutrients

increase the growth of a variety of small filamentous turf-forming species and organic matter reduces the abun-

dance of small herbivores. When organic matter alone

is added it increases the number of subdominant brown

frondose algae such as P. sanctae, which would be more

susceptible to herbivores in its absence. When added in

conjunction with inorganic nutrients it further increases

turf biomass. These results suggest that the affects of pol-

lution are not restricted to inorganic nutrients but thatthe organic portion of pollution has affects on foraging

fishes with consequent indirect effects on algae. Organic

matter also smothers and reduces cover of prostrate al-

gae growing on horizontal surfaces.

Acknowledgement

Research was supported by the Wildlife Conservation

Society (WCS), through grants from the Oaks, Tiffany,

and McBean Foundations, Columbia, University�s Cen-ter for Environmental Research and Conservation

(CERC) and the Pew Charitable Trust Fellows Pro-

gram. The Belizean Fisheries Department provided re-

search clearance. We are grateful for the logistic

support provided by the Middle Cay Research Stationand this is contribution 22 from this field station.

References

Bell, P.R.F., Elmetri, I., 1995. Ecological indicators of large-scale

eutrophication in the Great Barrier Reef Lagoon. Ambio 24, 208–

215.

Bjork, M., Mohammed, S.M., Bjorklund, M., Semesi, A., 1995.

Coralline algae, important coral-reef builders threatened by pollu-

tion. Ambio 24, 502–505.

Diaz-Pulido, G., McCook, L.J., 2003. Relative roles of herbivory and

nutrients in the recruitment of coral-reef seaweeds. Ecology 84,

2026–2033.

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.

Hay, M.E., 1984. Predictable spatial escapes from herbivory: how to

do these affect the evolution of herbivore resistance in tropical

marine communities? Oecologia 64, 396–407.

Hay, M.E., 1991. In: Sale, P.F. (Ed.), Fish-seaweed Interactions on

Coral Reefs: Effects of Herbivorous Fishes and Adaptations of

Their Prey. Academic Press, New York, pp. 96–119.

Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R.,

Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J.B.C.,

Kleypas, J., Lough, J.M., Marshall, P., Nystrom, M., Palumbi, S.,

Pandolfi, J.M., Rosen, B., Rougharden, J., 2003. Climate change,

human impacts, and the resilience of coral reefs. Science 301, 929–

933.


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.

Koop, K., Booth, D., Broadbent, A.D., Brodie, J., Bucher, D.,

Capone, D., Coll, J., Dennison, W.C., Erdmann, M., Harrison,

P.L., Hoegh-Guldberg, O., Hutching, P., Jones, G.B., Larkum,

A.W.D., O�Neil, J.O., Steven, A., Tentor, E., Ward, S., William-

son, J., Yellowlees, D., 2001. ENCORE: The effect of nutrient

enrichment on coral reefs. Synthesis of results and conclusions.

Marine Pollution Bulletin 42, 91–120.

Lapointe, B.E., 1999. Simultaneous top-down and bottom-up forces

control macroalgal blooms on coral reefs. Limnology and Ocean-

ography 44, 1586–1592.

Lewis, S.A., 1985. Herbivory on coral reefs: algal susceptibility to

herbivorous fishes. Oecologia 65, 370–375.

Littler, M.M., Littler, D.S., 1984. Models of tropical reef biogenesis:

The contribution of algae. Progress in Phycological Research 3,

322–365.

Littler, D.S., Littler, M.M., 2000. Caribbean Reef Plants. Offshore

Graphics, Washington D.C, 542 pp.

Littler, M.M., Littler, D.S., Titlyanov, E.A., 1991. Comparisons of N-

and P-limited productivity between high granitic islands versus low

carbonate atolls in the Seychelles Archipelago: A test of the

relative-dominance paradigm. Coral Reefs 10, 199–209.

Littler, M.M., Taylor, P.R., Littler, D.S., 1983. Algal resistance to

herbivory on a Caribbean barrier reef. Coral Reefs 2, 111–118.

McClanahan, T.R., 1999. Predation and the control of the sea urchin

Echinometra viridis and fleshy algae in the path reefs of Glovers

Reef, Belize. Ecosystems 2, 511–523.

McClanahan, T.R., 2002. The near future of coral reefs. Environmen-

tal Conservation 29, 460–483.

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.

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.

Sall, J., Lehmaan, A., Creighton, L., 2001. JMP Start Statistics.

Thomson Learning, Duxbury, p. 491.

Smith, S.V., Kimmerer, W.J., Laws, E.A., Brock, R.E., Walsh, T.W.,

1981. Kaneohe Bay sewage diversion experiment: perspectives on

ecosystem responses to nutritional perturbation. Pacific Science 35,

279–402.

Szmant, A.M., 2002. Nutrient enrichment on coral reefs: Is it a major

cause of coral reef decline? Estuaries 25, 743–766.

interaction between inorganic nutrients and organic matter in controlling coral reef communities in...

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