Download review—coral reefs - Ecosystem

J. Phycol. 34, 393–406 (1998)
REVIEW
CORAL REEFS: ALGAL STRUCTURED AND MEDIATED ECOSYSTEMS IN SHALLOW,
TURBULENT, ALKALINE WATERS
Walter H. Adey
Marine Systems Laboratory, Smithsonian Institution, Washington, D.C. 20560; [email protected]
high magnesium calcite far exceeding the others.
Traditionally the deposition of calcium carbonate as
external tests and skeleta has been thought of as
energy driven, a specialized process that evolved as
protection against predation or improvement in
performance. More recent studies indicate that calcification often results from the high pH of tropical
ocean seawater and the removal of CO2 by photosynthesis. Calcification could, in turn, be supportive
of photosynthesis by locally converting seawater
HCO 3 2 into scarce CO 2 (the preferred carbon
source) (McConnaughey and Whelan 1996). Algae
are responsible for most reef accretion of CaCO3,
either directly (e.g. the green alga Halimeda, coralline red algae) or through photosynthesis-mediated
deposition by the dinoflagellate Symbiodinium in
stony corals or by diatoms and chlorophytes in foraminifera (Lee et al. 1989, Hallock and Peebles
1993; Fig. 1).
Many algae in reefs are weakly calcified (Udotea,
Penicillus, dasycladaceans, Liagora, Galaxaura, squamariaceans, Padina, etc.), and under sporadic weak
wave and current situations, a ‘‘dust’’ of aragonite
crystals is often found coating virtually all algal surfaces. The cyanobacteria-rich, algal turfs that dominate so many reefs (see below) can approach stromatolites in terms of photosynthesis-induced calcium carbonate build-up, and have been demonstrated recently to provide a major portion of buried
reef carbonate as ‘‘micritic’’ interlayers with stony
corals and coralline algal crusts (Camoin and Montaggioni 1994). In contrast, many species of macroalgae probably employ chemistries that prevent the
initiation of aragonite crystals; this is particularly
likely in high sun species with abundant tissue cavities (e.g. many members of the red algal order Rhodymeniales).
The first reef boring, carried out from a back reef
island at Funa-Futi Atoll (Sollas 1904), showed for
the Pleistocene and Holocene that the biotic source
of reef carbonates was, in order of volume: 1) coralline algae, 2) foraminifera, 3) Halimeda, and 4)
scleractinian coral. In retrospect, for an open ocean,
trade wind atoll with a well-developed algal ridge to
seaward, it is reasonable that corallines would dominate the deposition of carbonate. Recently, submerged Halimeda-dominated bioherms lying in the
lee of the primary reef line were documented in the
northern section of the Great Barrier Reef (Orme
and Salama, and Marshall and Davies in Roberts and
Key index words: algae; calcification; community structure; coral reef; primary production; zooxanthellae
With a million species or more (Reaka-Kudla
1996), and specific and phyletic biodiversities greater than that of any of earth’s other biomes (more
than 80% being animal or protozoan), coral reefs
would seem to be truly animal ecosystems, the antithesis of rain forests on land. Prior to mid-century,
scientists generally assumed that the primary source
of energy for coral reefs was derived from the plankton brought by ocean currents and trade wind seas.
However, the largely algal photosynthetic component of coral reefs, which greatly exceeds the animal
component in biomass, is mostly diminutive, often
symbiotic within animal tissues, and easily overlooked.
Odum and Odum (1955) demonstrated for an
Eniwetok reef flat that on a biomass basis, algae
dominated the reef flat; they invoked the ‘‘traditional’’ trophic pyramid of biomass with 85% algae,
13.8% herbivores, and 1.1% carnivores. However,
most striking was the finding that only about 20%
of that algal biomass was symbiotic (6% was macroalgae and 73% algal turfs, borers, and crusts). The
reef literature has grown enormously since that
time, along with our understanding of reef metabolism and community structure and function. However, the basic picture has not changed. Algae directly or indirectly construct and determine coral
reefs. They also possess the potential to alter the
character of a reef, given natural or human perturbation involving nutrients or grazing. Stony corals
(scleractinians) have evolved a mechanism that allows extremely high rates of calcification, but that
greatly limits the area covered by coral tissue to the
pinnacles of a framework. Algae occupy the lateral
surfaces of the framework and fill its holes with
more carbonate. Increased nutrients or reduced
grazing cause a ‘‘phase shift’’ of community structure, wherein framework construction by corals is
greatly reduced and macroalgae come to dominate.
These matters, as we have come to understand them
in the last 20 years, are reviewed in brief below.
Calcification. Over 50 minerals have been adapted
by many phyla of living organisms for use as protective shells, internal skeletons, teeth, and sensory devices (Simkiss and Wilbur 1989). In the aquatic
world, the carbonate minerals dominate this array
with calcium carbonate as aragonite, calcite, and
393
394
WALTER H. ADEY
MacIntyre 1988). These Halimeda bioherms have a
Holocene thickness as great or greater than the
windward reef and occupy an area that is many
times larger. Even in a modern, coral-dominated
reef, average coral coverage over many kilometers
typically ranges from 10%–30% (Dullo et al. 1990),
and the most predictable component is an algal turfdominated carbonate (Green et al. 1987). Reef bore
holes rarely pass through solid coral for many meters, but more characteristically show 50%–80% carbonate-sand-filled cavities. Typically, corals build
frameworks on a narrow band of reef with moderate
wave energy, but the spaces are largely filled with an
algal and foraminiferan sand. Deeper fore reefs, unless vertical walls with low accretion rates, are often
dominated by coralline red algae (Dullo et al. 1990)
and Halimeda, and the lee section of back reefs are
the primary province of Halimeda or coralline algae.
Significant biomineralization occurs under four
key conditions of progressively greater organismic
control: 1) enclosure by tissues (or within cells) of
a volume of water in which ion concentrations can
be elevated, 2) specific organic molecules to provide
crystal initiation sites, 3) active transport of the requisite ions, and 4) an organic matrix to control crystalline shape or texture (Simkiss and Wilbur 1989).
In Halimeda spp., only the first two processes occur,
and disorientated aragonite crystals fill the interutricular spaces when CO2 is removed from those
spaces by photosynthesis (Borowitzka 1987). Halimeda is probably the most important bulk calcifier
in coral reef ecosystems at the generic level, although it rarely provides reef framework, but rather
sedimentary infill within the reef framework or in
the lagoon.
Occurring in hard bottom benthic photic zones
throughout the world ocean, the many genera and
species of the Corallinales are important framework
builders, framework cementers, and infill elements
in coral reef environments (Bjork et al. 1995). Calcification in corallines is not as well understood as
in Halimeda (see e.g. Lobban and Harrison 1994).
However, it seems clear that corallines deposit high
magnesium calcite in a definitive pattern within
their cell walls via membrane pumps that control
the flux of calcium and carbonate with control of
crystal orientation by organic wall components.
Thus, while corallines can be the deepest algae
(Dullo et al. 1990) (and many species occur in great
abundance into the arctic and subarctic), their proportional carbonate accretion rates are slower,
20%–50% of that in stony corals, though sometimes
more than in Halimeda (Chisholm et al. 1990). Under high wave conditions, where the survival of neither the articulated Halimeda nor scleractinian corals is possible and where active grazing of the slowgrowing corallines is more limited, frameworks of
crustose corallines become extensive. Algal ridges
ring most Pacific Atolls, where trade wind sea energies are high; they also are widespread in the Ca-
ribbean in those circumstances where the more limited trade wind seas are the highest (Adey 1978).
The high magnesium calcite of coralline skeleta is
clearly defensive. Nevertheless, there are grazers
(primarily chitons and limpets; Littler et al. 1995)
that bear a mutualistic relationship to their coralline
hosts by preventing the establishment of the spores
of macroalgae that would overgrow the corallines.
In reef zones of moderate energy, scleractinian
corals, with their zooxanthellae, are the primary producers of an aragonite framework. Recent research
(McConnaughey and Whelan 1996) indicates that
the basal disk cells of coral polyps pump calcium
into and hydrogen ions out of the spaces that underlie the polyps, resulting in conditions for organic-molecule-mediated development of aragonite
crystals. In the coelenteron, which acidifies as a result of calcification, bicarbonate ions (from seawater) react with hydrogen ions to produce CO2.
Blockage of the process by accumulation of CO2 in
the coelenteron is prevented by rapid CO2 removal
through photosynthesis by zooxanthellae. This concept is in agreement with most studies that show that
the majority of reef calcification occurs during daylight. For example, recent investigation of a reef on
the Pacific island of Moorea, with a moderately high
yearly calcification rate (8.9 kg CaCO3·m22·year21)
showed that 73% occurred during daylight (Gattuso
et al. 1993). It is important to note that the degree
of enhancement of calcification by zooxanthellae
likely varies widely, as does the calcification rate, in
various genera and species of corals. Some scleractinian corals lack zooxanthellae and still calcify.
However, these species calcify only slowly and are
considered nonhermatypic (i.e. nonreef building).
Although the coral symbiont Symbiodinium microadriaticum has been treated as a single species, the taxonomic relationships of zooxanthellae are uncertain
(Buddemeier 1994, McNally et al. 1994, Rowan and
Knowlton 1995, Rowan 1998). For this reason, in the
remainder of this review, I will refer to the coral
symbionts as Symbiodinium spp.
In summary, the primary producers of carbonate,
both framework and infill, in coral reefs are algae
(including cyanophytes), or algal (zooxanthellae)mediated animals. Many of the secondary or tertiary
animal (or protist) calcifiers also have algal symbionts (foraminifera, giant clams, etc.). In reef-building species of corals, extraordinarily high rates of
calcification are achieved through the utilization of
abundant seawater HCO32 and zooxanthellae to remove CO2. The basic quantitative/area relationships
between calcium carbonate deposition in coral reef
communities and the primary reef components responsible for that deposition and that occurring
elsewhere in the world ocean are shown in Figure 2.
Community structure. Coral reefs, as we treat them
in this article, are recent, less than 10,000 years old,
though often sited on antecedent reef platforms
that have developed throughout the Pleistocene and
CORAL REEFS: ALGAL ECOSYSTEMS
395
FIG. 1. Primary mechanisms of calcification in key reef-building algae and algal-mediated scleractinia. Modified from Borowitzka
(1987) (Halimeda) and McConnaughey and Whelan (1996) (scleractinia); note that McConnaughey and Whelan refer to active transport
as the ‘‘ping-pong pump.’’
396
WALTER H. ADEY
later Tertiary. By definition, significant past calcification and framework build-up (at least a few meters) must have occurred to differentiate a coral reef
from a coral community. Two major patterns of reef
development can be recognized: 1) immature or recently matured reefs, with high spatial heterogeneity
(1.5–3.0 m2/m2), often 10–20 m thick (these are
common in the Caribbean and less so in the IndoPacific); and 2) reefs that reached sea level 3000–
5000 years ago and have a low spatial heterogeneity
(1–2 m2/m2) (these are abundant in the Indo-Pacific and scattered in the Caribbean) (Adey 1978,
MacIntyre 1988) (note that units of spatial heterogeneity refer to the number of square meters of
large scale and noncryptic carbonate surface area
per horizontally projected square meter). Reefs
(and portions of reefs) are structured by wave energy, with coralline algae dominating at high energies (algal ridges), corals dominating at intermediate energies, and Halimeda bioherms and coralline
algae again at low wave energies. Coralline red algae
(different genera and morphologies, and a few specialized species of Halimeda) can also dominate on
deep banks and in fore reef zones (.60 m), if slopes
are moderate (Dullo et al. 1990). This discussion
specifically relates to the highly constructional, highly productive reef communities that occur in less
than 20-m depths.
Basic patterns of community structure are shown
in Table 1, based on four ‘‘type’’ reefs. Except for
spatial heterogeneity, community structure at the
functional group level is quite similar between Pacific and Caribbean examples. Algal turfs are almost
always the dominant reef community, followed by
corals or macroalgae, depending upon the reef type.
However, there are several omissions to these data
that need to be considered. The reef crest (between
fore reef and back reef) is not included because this
is the surf zone where it is difficult to work and adequate quantitative data have not been collected.
Here, the crustose corallines dominate, and under
very high wave energies (scattered eastern Caribbean and most open Pacific atolls), the crustose corallines, often along with vermetid molluscs and
sometimes Millepora spp., frequently create algal
ridges. Thus, although corals appear to occupy onequarter to nearly one- third of reef surfaces, and
corallines 7%–16%, a full section from 20-m depth
in the fore reef to the beginning of the lagoon
would balance out these figures at about 20% each.
Also, data from the large Halimeda bioherms at the
back of the main reef line in the northern Great
Barrier Reef (as noted above) would markedly alter
the proportions of macroalgae to corals in this very
large system if it were to be included. The information cited above for sediment composition in lagoons and back reef flat borings suggests that although perhaps not so extreme, Halimeda dominance of back reef margins is common beyond
where flat transects are typically terminated.
Finally, high island fringing reef flats (Table 1; see
also Adey and Burke 1976, Gattuso et al. 1997) often
lose their coral and coralline coverage in favor of
macroalgae. Fore reefs, in more open water, may
retain coral cover, but still show an increase in macroalgae at the expense of other assemblages. An increase in macroalgae also follows eutrophication
(see below).
Primary productivity. In a recent review of reef
gross primary production (GPP) relative to global
warming and reef exploitation, Crossland et al.
(1991) concluded that tropical reef communities
worldwide (6 3 105·km2) fixed 700 3 1012·g C year21
(or 3.2 g C m22·day21). This is indeed relatively high
for a biome scale ecosystem. However, based on the
definition of coral reefs by Crossland et al., the surface covered ranged from the photic limit on the
ocean side to shore (or photic limit on the other
side of an atoll) and included many deep carbonate
banks. Thus, for the systems we are discussing in this
article, that figure is very much a minimum. In addition to information covering this rather expanded
reef area, Crossland et al. (1991) also collated global
data on reef flats to provide a mean GPP of 7 6 0.6
g C·m22·day21. The value that is appropriate for coral reef ecosystems as we circumscribed them above
can be estimated to lie between that for their expanded reef area and the reef flat, at about 5 g
C·m22·year21. The highest recently recorded level
based on flow respirometry is 23.2 g C·m22·day21
(Adey and Steneck 1985—St. Croix).
Crossland et al. (1991) point out that because
community respiration (i.e. internal use of photosynthate) is typically high, net primary production
(NPP; that which is either exported or available for
export) is only about 3% of gross. However, reef
flats across the Pacific were considerably higher than
3% of gross (1.0 6 0.1 g C). Our typical coral reef,
from 20-m depths in the fore reef to the beginning
of the mostly sandy lagoon, on the same basis as
mean GPP, can be estimated to have a mean NPP
of about 0.6 g C·m22·day21. If a reef is dominated
by algae, and particularly if carbonate spatial heterogeneity remains high, levels of .10 g
C·m22·day21 are possible.
As a rough measure of the relationship between
calcification and biomass production in branching
hermatypic corals, we can take the data of Guillaume (1991) for Porites colonies on a reef flat in
Moorea. At a calcification rate of 13 kg·m22·year21,
for the dense colonies, and a mean yearly extension
of 1 cm year21, and using a value of NPP available
for biomass construction of ,0.5 g C·m22 (see
above), less than 10% of the annual CaCO3 extension of a branch could be provided with new tissue.
A more recent compilation by Lough and Barnes
(1997) for Porites spp. in a wide variety of Indo-Pacific localities, based on extension rates and coral
skeleton densities, shows even higher calcification/
extension rates that cannot be attributed to colony
CORAL REEFS: ALGAL ECOSYSTEMS
397
FIG. 2. Comparison of productivity and global surface area
of various carbonate environments. While coral reefs occupy
only about 0.02% of the area of
the deep sea, their rate of carbonate production (per unit
area) is about 200 times greater
than deep-sea carbonates. Other
neritic environments also occupy small areas of the global
ocean, but collectively they produce nearly as much carbonate
as the deep sea. Total carbonate
accumulation is about equally
divided between shallow and
deep-water environments. Note
that total deposition in the deep
sea (primarily by coccolithophores) approximately equals
that in reefs and on shallow
banks. (After Milliman, 1993).
infill or other extraneous sources. Allowing for minimal predation, on average, the tissue of most
branching and pillar-forming corals must continue
to grow upward at the tips without significantly increasing biomass. It may well be that nutrients (perhaps through local plankton capture) are sufficient
to build an initial biomass during colony initiation,
typically within the algal turf microclimate. As the
colony ‘‘climbs’’ into the water column, this advantage is lost. These hypotheses need testing, but they
are particularly well demonstrated on most actively
growing Caribbean Acropora palmata thickets. In
these colonies, where the calcification can be determined for individual branch tips, living tissue is very
thin, and basal ‘‘die back’’ is a conspicuous and regular feature (Adey and Steneck 1985).
Coral reefs, given elevated levels of nutrients in
the water column, can undergo a phase shift to
fleshy, macroalga-dominated communities with high
gross and net primary productivities (Done 1992,
Hughes 1994). In this state, production of calcified
framework is low. As a result of constant carbonate
bioerosion, the reef begins to degenerate to a more
or less flat pavement. In the more typical active reef
that has high GPP and low net production and export, algal turfs and crusts on antecedent, coral, or
coralline carbonate provide 30%–40% of the surface
cover and biomass of a reef, and a considerably
higher proportion of the primary production (see
e.g. Williams and Carpenter 1990).
Components of coral reef primary production. In a review of carbon and energy flux in stony corals, Muscatine (1990) concluded that the GPP of the coral/
dinoflagellate symbiosis (as a coral colony in situ)
was typically between 2.0–2.6 g C·m22·day21 (with extremes of 1.4 and 13.7 g C·m22·day21). Carpenter
(1985) and Larkum (1983) had earlier determined
that reef algal turfs were in about the same range,
perhaps a little higher at 2.3–3.3 g C·m22·day21
(Larkum data are recalculated as GPP and range
from 1–6 g C·m22·day21). Klumpp and McKinnon
(1992), in their extensive work on the Great Barrier
Reef, found algal turf biomass levels (using similar
methods) that were about the same (;30 g
[dry]·m22) as Carpenter, but their productivities
were a little lower (1.1–2.2 g C·m22·day21). This
could be due to a failure to use surge stirring in
their chambers (Carpenter et al. 1991).
If the St. Croix cover data of Adey and Steneck
(1985) are combined with the quite similar Great
Barrier Reef data of Klumpp and McKinnon (1992)
(as an approximate mean of open water coral reefs),
and the productivity values cited above are applied
to obtain mean component productivities, the zooxanthellae of scleractinian corals can be seen to provide about one-third of mean reef productivity and
algal turfs approximately one-half. However, the
whole reef summation is about 30% lower than the
figure cited by Crossland et al. (1991). The productivity values for algal turfs cited here were derived
from dried and slabbed carbonate plates allowed to
redevelop algal turfs on a reef from 6 months to a
year. The biomass levels of turf achieved are about
30 g dry·m22, about one-fifth of that found by Odum
and Odum (1955) in their direct extraction analysis
(148 g dry·m22). It seems likely that insufficient incubation time was allowed by these methodologies
to develop a fully mature turf community, especially
one with the boring components. The productivity
values cited for algal turfs are probably low. Johnson
et al. (1995), in applying Klumpp and McKinnon’s
results, reached the same conclusion with regard to
the relationship between component and whole
production, but concluded instead that Muscatine’s
2.30
1.27
20.3
7.1
31.5
27.1
Stony
corals
0.9
,1
0.2
10.3
Other
1.5
2.3
2.8
26.5
Corallines
Back reef (reef flat)
35.2
50.5
38.5
32.8
Algal
turf
21.5
36.3
8.1
1.9
Macroalgae
20.5
3.8
18.9
1.2
Sand
Algal
ridges
;90%
coralline
?
23 width
back reef
;80%
coralline
?
Reef
crest a
2.25
1.27
Spatial
hetero.
25.9
21.1
22.7
Stony
corals
6.9
5.4
2.2
Other
0.4
10.9
5.6
Corallines
Fore reef
25.9
38.4
37.2
Algal
turf
28.7
6.2
1.3
Macroalgae
12.4
14.4
26.2
Sand
a Reef crests can be as wide or wider than fore reefs or back reef zones where wave energy is high and the crest lies at 0.5–3 m below mean low water. Once an algal ridge has
formed, it typically narrows to ,10-m width.
b Klumpp and McKinnon (1992).
c Adey and Steneck (1985).
d Morrissey (1980).
e Adey et al. (1977).
Martinique
(three reefs)e
High island reefs
GBR
Magnetic Isl
(one reef)d
Caribbean
St. Croix
(three reefs)c
Shelf reefs
Great Barrier
Reef
(seven reefs)
Spatial
hetero.
TABLE 1. Comparative community structure Great Barrier Reef/Caribbean (% cover of carbonate surface).
398
WALTER H. ADEY
CORAL REEFS: ALGAL ECOSYSTEMS
numbers for primary production by corals must be
too low. As we have noted, there is a strong basis for
an alternate approach, which would elevate the algal
turf component of whole reef GPP from about 50%–
60%. This approach is also the only way to achieve
the relative increase in GPP resulting from change
of coral cover to algal turf cover in maturing reefs
of St. Croix (Adey and Steneck 1985).
Grazing, nutrients, and reef health: the role of algal
communities. It has become axiomatic in reef science
that actively calcifying coral and algal turf-rich reefs
can quickly (months to years) be transformed, by
storm disturbance, increase of nutrients, or overfishing, to a high standing crop (.1 kg·m22) macroalgal-dominated community (Adey and Burke 1976,
Kinsey 1988, Hughes 1994, Gattuso et al. 1997).
Whether it is possible for a reef to return to the
coral/algal turf-dominated state once it has been
transformed is not known, but it is widely accepted
that the transformation represents serious environmental degradation (Done 1992). The ‘‘delicate balance’’ between nutrients, grazing, and reef community structure has been extensively studied in the
past decade or two. A brief discussion of each of the
components is necessary to explore this issue.
Johnson et al. (1995) developed the argument
(based on Davies Reef, Great Barrier Reef) that a
significant shift from coral to algal turf cover (e.g.
in a reef with living coral removed by the crown-ofthorns starfish, e.g. Acanthaster or other means)
would not significantly change the primary production but would greatly change trophic structure and
carbon flux. Their reasoning is that production by
the zooxanthellae is held within the reef, whereas
algal turfs are grazed inefficiently, with much of the
turf leaving the reef as current-carried detritus. This
concept may be valid if largely inedible macroalgae
replace the coral (rather than algal turfs). However,
a very large proportion of the primary production
of stony corals is released as mucous to the water
column (Muscatine 1990). Thus, coral primary production would seem to be as much subject to loss
from the reef community as algal turf fragments.
An excessive shift from coral to algal turf is a serious issue for a coral reef community over the long
term because coral calcification produces most of
the framework that is responsible for spatial heterogeneity. Primary production, trophic structure and
dynamics, and species diversity are all highly dependent upon spatial heterogeneity. Adey and Steneck
(1985), based on St. Croix reefs, make the argument
that, as a mature reef with high coral cover and high
spatial heterogeneity approaches sea level, a more
abundant living coral surface is replaced by algal
turf. As a result, extremely high levels of primary
and net productivity are achieved for short periods
(centuries) with a full and complex trophic structure, until spatial heterogeneity is lost and reef pavements are formed. By contrast, the phase shift of
coral and algal turf cover to macroalgae (due to el-
399
evated nutrients, the overharvest of herbivorous fish,
or the disturbance of hurricanes) rapidly changes
reef community structure and trophic dynamics. Although gross and net primary productivity may
greatly increase (Adey et al. 1977, Guttuso et al.
1997), the net result is the loss of the reef as a community and the export of most of the productivity
to lagoons or offshore to deeper water.
Algal turfs dominate most actively calcifying coral
reefs, covering more than 50% of the carbonate surface not occupied by living coral tissue. Table 2 lists
species of each major algal group by anatomical type
for algal turf assemblages in the Caribbean (see also
Price and Scott 1992). It is not widely appreciated
among most reef workers that in biomass, cyanobacteria, particularly Calothrix spp. and Schizothrix spp.,
are about as important as rhodophytes (e.g. smaller
Jania spp., Amphiroa spp., Polysiphonia spp., Ceramium
spp., and Herposiphonia spp.), at 30%–50% each.
Chlorophytes and phaeophytes are lesser elements
of algal turf, with species of Cladophora, Derbesia, Giffordia, and Sphacelaria being common. Cyanobacterial, red, and green borers are endolithic in the carbonate substrate, and it has long been known that
these can extend under living coral tissue. Some
workers have recently proposed the existence of a
symbiotic association involving fungal filaments for
this situation (Le Campion-Alsumard et al. 1995).
Algal turf assemblages in coral reef environments
are net nitrogen fixers and achieve high levels of
primary production when strongly lit and provided
with intense oscillation (wave surge) motion to
break up boundary layers and overcome self shading
(Hackney et al. 1989, Williams and Carpenter 1990,
Carpenter et al. 1991, Carpenter and Williams
1993). Grazing by fish (especially by parrotfish, surgeonfish, and damselfish) and by a host of invertebrates (including echinoids, snails, crabs, and small
crustaceans) is crucial to the maintenance of algal
turfs by preventing the macroalgal sporelings, which
are a persistent minor element of turf communities,
from overgrowing and shading the smaller turfs.
Nevertheless, fish grazers remove only about onehalf of NPP (Polunin and Klumpp 1992), the remainder being lost to invertebrate grazers or as algal
fragments lost to the lagoon as a result of inefficient
grazing.
Many macro- and mesoinvertebrates, particularly
echinoids, crustacea, gastropods, and annelids,
graze on algal turfs, and because they are constantly
preyed on by larger invertebrates and fish, are rarely
able to reduce turf dry biomass below 50–200 g·m2.
In some cases, invertebrates are more important
(Carpenter 1990), and in others, fish are the dominant grazers (McClanahan 1992). It is clear that algal community structure is greatly affected by the
spectrum of grazers present on an individual reef,
and, in turn, fishing pressure can significantly alter
the type of grazing pressure (McClanahan 1997).
Macroalgae are minor elements in the best devel-
400
WALTER H. ADEY
oped coral reef communities. Nevertheless, their
role and performance is interesting for two critical
reasons: 1) given elevated nutrients or reduced grazing, they are capable of overgrowing both corals and
algal turfs, significantly degrading community structure (Done 1992, Naim 1993, Hughes 1994, Tanner
1995); and 2) the algal defense mechanisms, both
physical and chemical, that allow many macroalgae
to maintain a presence, are significant to the understanding of community dynamics, and in the
case of the secondary compounds, offer potentially
valuable chemicals to human societies. It is important to note that recent studies indicate that not only
do elevated nutrients increase macroalgae and reduce coral settlement and cover, but they also directly reduce coral calcification (Marubini and Davies 1996). This phenomenon is not fully understood at this point, but it probably relates to the
dynamic metabolic interaction between the animal
coral cells and the zooxanthellae.
Zooxanthellae receive their CO2 in part from animal (coral cell) respiration but also from calcification. Nitrogen (and phosphorus) is normally received from coral cells, probably originally derived
primarily from captured plankton. Roughly 80% of
the photosynthate produced by the zooxanthellae is
transferred to the host as glycerol, but coral cells
may mediate this transfer by controlling the nitrogen delivered to the zooxanthellae (Muscatine
1990). Zooxanthellae that receive very limited nutrients can photosynthesize and respire but are restricted in growth, so most of their photosynthate is
expelled. Excess nitrogen in the form of nitrate appears to upset this balance, allowing zooxanthellae
to grow and reducing glycerol transfer to the host
(Marubini and Davies 1996). Thus, it seems likely
that host metabolism and ultimately the energy
available for active transport of calcium and hydrogen ions is reduced.
Coral reef macroalgae can provide resistance to
grazing by both physical (Littler et al. 1983, Coen
and Tanner 1989) and chemical means. Perhaps in
part because of the potential human pharmacopeia
interest, considerable scientific effort is being directed to understanding the nature and function of
such secondary compounds (though much of it is
still confusing; Meyer and Paul 1992, Lumbang and
Paul 1996). In contrast, there is little question that
the large, green, leafy seaweed Avrainvillea longicaulis is defended from fishes by the brominated compound avrainvilleol (Hay et al. 1990). In this case,
the value of the compound is extended, in that several invertebrates feed on the alga and additionally
derive protection either from the presence of the
compound in their own tissues or in the surrounding algae when used for cover. In other cases, it
would seem that multiple mechanisms, including
calcification, toughness, shape, and secondary metabolites, offer protection from herbivores (Schupp
and Paul 1994).
Much additional work is needed to gain a comprehensive view of the role of secondary compounds
in the macroalgae of reef ecosystems. However, several general points can be made: 1) both physical
characteristics (e.g. calcification) and secondary
compounds can provide some protection from grazing, especially by fish; 2) no method provides complete protection and ultimately the principles of the
‘‘arms race’’ apply; and 3) defenses require energy
and often nutrients, or in other ways reduce growth
or reproductive potential. In the extreme oligotrophic reef environment, particularly above the ‘‘microclimate’’ of the algal turf, algal growth will always
be limited to some degree by lack of nutrients.
Therefore, an increase of water column nutrients is
likely to offset potential restrictions to growth incurred by defense against herbivory. Both a reduction in grazing (by fishing or hurricanes) or an increase in nutrients (by hurricanes or cultural eutrophication) will increase macroalgal growth and
physically reduce coral calcification and settlement
(also see Tanner 1995).
The chemical defenses against grazing of many
macroalgae and the role of nutrients in causing a
phase shift of dominance of macroalgae over corals
and coralline algae have been discussed. However,
we have barely begun to scratch the surface of the
role of chemical cues in controlling coral reef community structure, as is seen by the recent discovery
of the role of coralline algae in controlling the settlement of coral larvae (Morse et al. 1994).
Summary. Coral reefs are benthic communities in
high light, low nutrient, low plankton, moderate to
high wave and current energy open waters, where
physical factors show little annual variability. As in
most shallow benthic communities not subject to severe physical limitations, competition for space is a
significant factor, and yet, since oceanic plankton
provides only a limited food/energy resource, the
filter feeding barnacles, mussels, hydroids, and bryozoans that can occupy large areas on temperate/
boreal shores are of minimal importance.
Scleractinian corals become a significant part of
an ecosystem in which they would otherwise be highly restricted because of symbiotic association with dinoflagellate algae. By evolving a mechanism to utilize the abundant bicarbonate for calcification, at
least the dominant hermatypic genera became highly competitive for space with the highest organismic
mineralization rate yet developed in the earth’s biosphere. So efficient is this mechanism that it far outruns the concomitant growth potential of the living
tissue. Limited in nitrogen and phosphorus supply,
most of the zooxanthellar production is therefore
released as mucous. Thus, at the community level,
hermatypic corals build pedestals that continually
raise their biomass to the sun, but leave behind a
large and spatially heterogeneous mass of calcium
carbonate; this results in an even greater area for
algal growth than would otherwise be available to
CORAL REEFS: ALGAL ECOSYSTEMS
those algae that would occupy this community in the
absence of coral construction. The ‘‘pedestals’’ can
form a framework; however, numerous other calcifiers, mostly algae such as Halimeda or non-coral animals, many also with symbiotic algae, provide the
infill.
The carbonate-based, spatial heterogeneity, which
is significantly further increased by the boring of algae and invertebrates, also provides cover for the
high biodiversity characteristic of these ecosystems.
Specifically, it provides cover for numerous fish and
invertebrate grazers, which would otherwise be limited in abundance by lack of cover. Thus, in a stony–
coral framework reef, in which three-quarters of the
surface is not occupied by living coral, algal turfs,
which have low biomass in most shallow, benthic environments, come to dominate much of the framework’s surface. This is equivalent to some grasslands
in terrestrial environments and owes its continued
existence to the grazers with which, in a sense, it
holds a ‘‘symbiotic’’ relationship. The dominance of
the algal turf is enhanced in this nutrient-poor environment in that nitrogen-fixing cyanobacteria are
a significant component. Also, since most grazers remain under cover in the community when not feeding, much of the nutrients in the system are continually recycled. Energy flux is high, but exportable
production is low, generally more or less in balance
with incoming planktonic biomass.
In the ecosystem described above, many macroalgae are limited by intensive herbivory to small refuges around toxic invertebrates or to sites where
wave action or exposure to heavy predation limit
grazing. Others survive by developing a variety of
strategies that deter grazing to various degrees.
Thus, unless the basic environmental parameters
are upset, macroalgae are a third, minor component
of the coral reef ecosystem. By contrast, given a natural or anthropogenic increase of nutrients (which
both increase algal growth rate and decrease calcification) or a reduction in grazing (by fishing or
storms), the macroalgal component can and does
overpower the reef community. When this phase
shift happens, macroalgal standing crops can become very high and productivity even higher than
on the previously existing reef. However, much of
the algal production is lost from the reef. As algal
fragments float to the lagoon and net calcification
is lost, the ‘‘reef’’ floor gradually becomes a flat
pavement, in part due to boring and scraping, with
a relatively low faunal diversity.
An extremely turbulent, wave-breaking zone (the
reef crest) exists for most open water reef systems
that grow to within 5–10 m of the surface. In this
zone, grazing is very limited, coral colonies are consistently broken or damaged by wave action, and
crustose corallines (e.g. Porolithon, Lithophyllum and
Neogoniolithon), with one-fifth to one-tenth of the calcification potential of scleractinian corals, build significant calcified structures (algal ridges).
401
Question (Rowan): One aspect of coralline red algae puzzles me. Many studies strongly imply that
they induce the settlement of coral (and other) larvae that, once settled, will certainly compete with
the algae for resources. This doesn’t seem to be in
an alga’s best interest, to be a ‘‘settling plate’’ for
its competitors. Do the algae have no other choice?
Then again, maybe the corals will eventually provide
substrate for the coralline algae either directly or
indirectly, by promoting reef growth in general.
Could it be that coralline algae actually ‘‘farm’’ future real estate?
Answer: It has been recognized for some 35 years
that crustose corallines have an intercalary meristem, like a cambium, that produces a usually colorless epithallium upward and the main tissue of the
alga, perithallium, downward. At least since my
Ph.D. thesis, in the early 1960s, it was known that
the epithallium constantly sloughs off as an antifouling device, and more recently, Keats et al.
(1997), reviewing the issue, demonstrated two
modes of shedding, reiterating the antifouling property. Also, since my early publications, it has been
recognized that some genera delay release of the
epithallial cells producing a specialized photosynthetic zone of lesser calcification. Steneck (e.g.
1985) has suggested that these genera require grazing of this thickened epithallium to prevent fouling
by other organisms, though Keats et al. question
that grazing is really necessary in this case.
Thus, crustose corallines constantly shed their surfaces and tend to be free of fouling. However, surface damage, often by grazing through the meristem, damages or kills spots that are then settled on
by other algae and invertebrates. Under some conditions, a ‘‘brainlike’’ irregular surface of thick coralline crust forms, in which the ‘‘infolds’’ are continuously occupied by an algal turf community. This
is probably not advantageous in any way to the corallines, but rather demonstrates the imperfection of
all evolved defenses.
As you have noted, it has also been known for
some time that some invertebrates key into coralline
bottoms for larval settlement. If the corallines are
constantly releasing necrotic tissue, a plethora of organic compounds are certainly released, allowing
ample opportunity for species to evolve that can recognize this bottom. But why key onto a bottom that
you cannot land on (or at least successfully establish
upon)?
And finally, my anecdotal, or at least hypothetical,
answer. Coralline surfaces are largely free of other
organisms, but there are damaged ‘‘niches’’—mostly created by grazers—that could be occupied. It is
probably worth it at the population level for the settling invertebrate larva to go for the small chance
of an open hole. Having found this ‘‘niche,’’ it is
virtually free of space competition because corallines are slow growers and the settlement of other
larvae and algae is limited. Does this benefit the cor-
Isthmia sp.
Navicula sp.
Nitzchia sp.
Synedra sp.
Numerous
unidentified
spp.
Spores
and sporelings
Pseudotetraspora
antillarum
Chlorophyta
(green algae)
Anacystis
dimiduata
Additional cocooid forms
Bacillariophyceae
(diatoms)
[Cyanobacteria]
Cyanophyceae
(blue-green
algae)
Unicellular
Chaetomorpha*
minima
Valonia
Thalassionema sp.
Tabellaria sp.
Anabaena
oscillarioides
Calothrix
crustacea
Entophysalis sp.
Microcoleus
lyngbyacea
Nostoc
spumigena
Oscillatoria
submembranacea
Schizothrix
calcicola
Schizothrix
mexicana
Simple
Branching
Acetabularia1
Avrainvillea1
Bryopsis pennata
Bryopsis sp.
Chamaedoris
penicilum
Cladophora laetevirens
Cladophora
montagneana
Cladophora vagabunda
Cladophoropsis*
macromeres
Cladophoropsis
membranacea
Derbesia marina
Ernodesmus spp.
Neomeris spp.1
Penicillus spp.1
Pseudobryopsis spp.
Rhizoclonium spp.
Struvea spp.
Udotea spp.1
Licmophora sp.
Scytonema hofmannii
Filamentous
Enteromorpha
chaetomorphoides
Enteromorpha sp.
Protoderma marinum
Multiseriate,
polysiphonous,
or weakly corticated
Complexly corticated
Pseudoparenchymatous
Caulerpa spp.
Codium
Dictyosphaeria
Halimeda1
Ulva
Parenchymatous
TABLE 2. Genera and species consistently present in numerous surveys of Caribbean and western tropical Atlantic coral reefs. Species listed in regular type are common, persistent components of the coral
reef algal turf assemblage. Genera in bold contain no persistent turf components and are treated as macroalgae. Crustose coralline genera are indicated in parenthesis. Asterisks designate genera that contain
both the listed turf component species and other species that do not persist within the assemblage. Plus signs designate calcareous genera. After Adey and Hackney (1989).
402
WALTER H. ADEY
Spores and
sporelings
Rhodophyta
(red algae)
Unicellular
Spores and
sporelings
Phaeophyceae
(brown algae)
TABLE 2. Continued.
Erythrotrichia
carnea
Simple
Branching
Acrochaetium spp.
Antithamnion
antillarum
Antithamnion sp.
Asterocytis ramosa
Bangiopsis subsimplex
Callithamnion halliae
Callithamnion sp.
Crouania attenuata
Dohrniella antillarum
Erythrocladia
subintegra
Goniotrichum alsidii
Grallatoria reptans
Griffithsia barbata
Griffithsia globulifera
Griffithsia schousboei
Gymnothamnion
elegans
Halodictyon mirabile
Pleonosporium
caribaem
Spermothamnion
investiens
Bachelotia antillarum
Ectocarpus
elachistaeformis
Giffordia rallsiae
Filamentous
furcigera
fusca
tribuloides
spp.
Bangia atropurpurea
Ceramium brevizonatum
Ceramium byssoideum
Ceramium comptum
Ceramium corniculatum
Ceramium cruciatum
Ceramium fastigiatum
Ceramium flaccidum
Ceramium leptozonum
Ceramium leutzelburgii
Ceramium nitens
Dasya* rigidula
Dasya sp.
Dasyopsis antillarum
Falkenbergia hillebrandii
Herposiphonia pectenveneris
Herposiphonia secunda
Herposiphonia tenella
Herposiphonia sp.
Heterosiphonia
wurdemanni
(Hydrolithon1)
Hypoglossum
(Lithophyllum1)
(Lithothamnium1)
Lophosiphonia cristata
Martensia
(Neogoniolithon 1)
Peysonellia spp.1
Polysiphonia atlantica
Polysiphonia binneyi
Polysiphonia denudata
Polysiphonia exilis
Polysiphonia ferulacea
Polysiphonia flaccidisima
Sphacelaria
Sphacelaria
Sphacelaria
Sphacelaria
Acanthophora spp.
Amphiroa1*
fragillisima
Amphiroa spp.
Asparagopsis
Bryothamnion
Centrocerus
clavulatum
Champia parvula
Chondria* collinsiana
Coelothrix irregularis
Digenia simplex
Eucheuma spp.
Galaxaura spp.1
Gelidiella*
trinitatensis
Gelidiella sanctarum
Gelidiopsis intricata
Gelidium* pusillum
Gracilaria spp.
Halymenia spp.
Hypnea spp.
Jania1* adherens
Jania capillacea
Jania pumila
Jania rubens
Laurencia * caraibica
Liagora spp.1
Lomentaria spp.
Meristotheca spp.
Pterocladia spp.
Wurdemannia miniata
Complexly corticated
Pseudoparenchymatous
Multiseriate,
polysiphonous,
or weakly corticated
Parenchymatous
Colpomenia spp.
Dictyopteris spp.
Dictyota spp.
Dilophus spp.
Lobophora spp.
Padina spp.
Sargassum spp.
Turbinaria spp.
CORAL REEFS: ALGAL ECOSYSTEMS
403
404
WALTER H. ADEY
allines in any way? Probably, in most cases, no. Perhaps in algal ridges and cup reefs, it could be argued that the frequent coinhabitors, vermetid gastropods, provide structural strength to the ridge,
providing for community longevity (and greater
spore production by the corallines). Perhaps coralline surfaces with vermetids, barnacles, or spirorbids
are harder to graze and in the end more productive
of spores because most conceptacles are not being
removed by grazers. Now we are out on the hypothetical limb.
Dunlap and Shick: Given that carbonate deposits
store nearly 3 3 104 times more inorganic carbon
than is in the atmosphere, that vast carbonate deposits have accumulated since the Precambrian (evidence of long residency), and that the bulk of carbonate rock is the result of biological precipitation,
it is clear that calcification has had a profound geologic effect in shaping our present biosphere. The
questions I present relate to the role of reef calcification on global C/CO2 cycling with consequence
to atmospheric CO2 (‘‘greenhouse gas’’) levels due
to chemical equilibria and exchange across the airsea interface.
Question (Dunlap and Shick): There is ongoing debate as to whether coral reefs contribute in the present geologic as a source or sink of atmospheric CO2
(Buddemeier 1996, Gattuso et al. 1996, Kayanne
1996). Would you comment on the scientific basis
of this debate? If coral reefs function as either a
source or sink of atmospheric CO2, is it likely to be
significant at the global scale?
Question (Dunlap and Shick): It has been estimated
that the ratio of released CO2/precipitated CO2 by
calcification is approximately 0.6 (accounting for
the buffering capacity of seawater) (Frankignoulle
et al. 1994). This suggests that community metabolism in a heavily calcifying reef would cause an evasion of CO2 to the atmosphere. However, net CO2
consumption is an apparent feature of macroalgaldominated reefs (Gattuso et al. 1997). Would you
comment on how community structure could influence metabolic equilibria in favor of CO2 release or
consumption?
Answers: These questions probably cannot be answered definitively today, but I will at least try to
place them in perspective, from my point of view.
If our averages for pantropic, coral reef function,
are correct, globally, reefs are slight net primary producers and large calcium carbonate sinks. The net
primary production is, at least in part, lost to sediments in lagoons and to some extent lost to the
deep ocean. On the calcification side, reefs are massive world-scale net sinks of carbon. The issues relate
more to where the carbon comes from and what the
time scales of the fluxes are.
Primary production carbon is in large measure
derived, in more or less short term, from CO2 (ultimately, from the atmosphere), although some almost certainly originates from alkalinity. Macroalgal-
dominated reefs are strong CO2 sinks. What percentage of pantropic reefs are macroalgal dominated? Probably less than 20%, and let’s hope that
modern human society does not accept that reef eutrophication is a good thing in order to provide a
new CO2 carbon sink. In the larger scale, as long as
most reefs retain their recent past community structure, atmospheric CO2 sinks by coral reefs would be
negligible, and the biodiversity loss associated with
the macroalgal phase shift enormous. Coral/algal
turf ecosystems, while very large recyclers of carbon,
are not likely significant sinks of CO2 carbon.
The carbon in coral reef calcification is primarily
derived from alkalinity (HCO32, CO35). Some of this
calcification by stony corals is derived from bicarbonate. In my view, only a few rapidly calcifying genera (including acroporids) use bicarbonate as a calcification substrate. However, this is not well established or even generally accepted at this time. Bicarbonate calcification results in some CO2 release
to the atmosphere, and some rapidly calcifying
reefs, rich in acroporids, undoubtedly transfer CO2
carbon to the atmosphere from the bicarbonate
pool. In my anecdotal view, this is not likely to be a
significant transfer on a pantropic scale. However,
we need better large-scale information on coral calcification and reef community structure to be certain. I tried to outline where we stand on this issue
in the review.
In summary, coral reefs are clearly a significant
sink, on the global scale, of oceanic alkalinity. Alkalinity carbon is ultimately carbon derived from atmospheric carbon through alkalinity pumps (see
e.g. Kemp and Kazmierczak 1994). However, this is
probably not of significance relative to our shortterm concern (decades to centuries) for fossil carbon introduction into earth’s atmosphere.
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