Limnol.
Oceanogr., 30(l),
0 1985, by the American
1985, 157-166
Society of Limnology
Tissue condition
and Oceanography,
Inc.
and growth rate of corals associated with schooling fish’
Judy L. Meyer and Eric T. Schultz2
Zoology
Department
and Institute
of Ecology, University
of Georgia, Athens 30602
Abstract
Juvenile french and white grunts (Haemulorlflavolineatum
and Haemulonplumieri)
form diurnal
resting schools over colonies of Porites furcata and Acropora palmata in St. Croix. We studied the
effect of these grunts on the tissue composition and growth rate of corals. Porites furcata colonies
with grunts had significantly more tissue cm- *, N cm-* and zooxanthellae cm-* than colonies
without grunts. Acropora palm&a colonies with grunts also showed elevated amounts of N cm-2
and P cm+. Seasonal changes were also observed in these parameters and in coral growth rates
and skeletal density, apparently related to light availability.
Several measures of coral growth rate
were significantly greater in P.furcata colonies with grunts. Grunts were removed from two colonies,
and growth rates before and after removal were compared to rates in reference colonies. Before
removal most growth rate measures were greater in the colonies with grunts; after removal growth
rates were lower or not significantly different. These data demonstrate that schools of resident fishes
can stimulate coral growth, perhaps by providing nitrogen supplements.
Abundant migrating vertebrates can be
effective transporters of nutrients and organic matter in terrestrial
(Hutchinson
1950), wetland (McCall and Burger 1976;
Onuf et al. 1977), freshwater (Richey et al.
1975; Durbin et al. 1979), and marine ecosystems (Ganning and Wulff 1969; Bray et
al. 198 1). Similarly, fishes that migrate between feeding areas away from coral reefs
and resting areas on the reef provide a nitrogen and phosphorus supplement to corals (Faulkner and Chesher 1979; Meyer et
al. 1983) and may also make a significant
contribution
of organic carbon (Ogden and
Ziemann 1977; Meyer and Schultz 1985).
Heterotypic schools ofjuvenile french and
white grunts (Haemulon flavolineatum and
Haemulon plumier) are abundant on many
Caribbean reefs. During the day these fishes
rest over coral colonies, and at dusk they
migrate to surrounding seagrass beds where
they feed on benthic invertebrates.
The
groups form again at dawn and return to the
same coral colony over precise migration
paths (Ogden and Ehrlich 1977; McFarland
et al. 1979; Helfman et al. 1982). Their guts
are full at dawn and empty by the time they
leave the reef (McFarland and Hillis 1982;
I This research was supported by NSF grant OCE
79-1046.
2 Present address: Department
of Biological
Sciences, University of California, Santa Barbara 93 106.
Meyer pers. obs.). On patch reefs in St. Croix,
where this study was done, the excretory
products of resident grunts added 3.9 mmol
N mm2d-l and 0.2 mmol Pm-2 d-l to Porites
furcata colonies and 9.6 mmol N rnM2 d-l
and 0.62 mmol P me2 d-l to Acropora palmata colonies (Meyer et al. 1983). The nitrogen supplement is primarily NH4+, a form
of nitrogen readily available to corals (Muscatine and Porter 1977; D’Elia and Webb
1977; Muscatine and D’Elia 1978).
Such nutrient supplements appear to be
particularly
valuable in the nutrient-poor
waters of a coral reef. We have previously
noted accelerated skeletal growth from a
limited sample of coral colonies of one
species (P. furcata) in the presence of resting
schools of grunts (Meyer et al. 1983). We
examine here several colonies of two coral
species, P. furcata and A. palmata. We present information
on the impact of resident
grunt schools on weight and nutrient content of coral tissue, zooxanthellae
abundance, skeletal density, and coral growth
rate, and on seasonal changes in these parameters.
We thank the staff of the West Indies Laboratory for their assistance. G. S. Helfman
provided advice and assistance in the fieldwork. R. and H. Carpenter assisted in the
grunt removal experiments. We also thank
G. S. Helfman, G. J. Smith, J. F. Battey, J.
W. Porter, and E. H. Gladfelter for com-
157
158
Meyer and Schultz
Fig. 1. The location of the five reefs (Romney Point and Patch Reefs 1, 6, 7, and 15) studied in Tague Bay.
Acropora palmata colonies with and without grunts are denoted as AW and A, while P. furcata colonies with
and without grunts are denoted as PW and P. The inset shows the location of Tague Bay on St. Croix.
ments on the manuscript. This is Contribution 126 of the West Indies Laboratory,
Fairleigh Dickinson University.
Procedures
Tague Bay, St. Croix, U.S. Virgin Islands,
lies behind a barrier reef and has extensive
seagrass beds dotted with patch reefs. All
sampling was done on colonies of A. palmata and P. furcata on five reefs in Tague
Bay (Fig. 1). Porites colonies ranged in size
from 5 to 53 m2 (52= 24) with an average
of 36 grunts m-2, while Acropora colonies
were from 18 to 77 m2 (X = 4 1) with‘ an
average of 15 grunts m-2 (Meyer and Schultz
198 5). On each reef we sampled at least one
colony with a resident grunt school and one
colony with no resident grunts. Colonies in
the same reef were at the same water depth,
but reef depth varied from 1.5 to 5.0 m.
Coral growth- We measured growth rates
of five P. furcata colonies, three with resi-
dent grunt schools and two without (Fig. l),
over five intervals: December 1979-December 1980 (Patch Reef 1 colonies only),
January-April,
April-August,
August-December 198 1, and December 198 l-June
1982 (Romney Point colonies only).
To measure coral growth, we marked 10
branches on each colony with cable tie wraps
and stained them by injecting 2 ml of a 0.5%
alizarin solution into Whirlpac bags secured
over the branches for two photoperiods.
When branches were collected, we removed
samples for tissue analyses as described below, then bleached and dried the branches.
The alizarin stain line was exposed by
cutting each branch along the growth axis.
To estimate the volume and weight of new
skeleton cut away by the saw, we used a
digitizer to measure the area of surfaces created by the saw cut distal to the stain line
from photographs of the samples. This area
times the width of the saw blade yields the
Efects ofJish on corals
volume cut away, and volume times density
(measured below) yields the weight cut away
(generally 10% of weight of new growth).
After filing away all skeleton proximal to
the stain line (i.e. all growth before staining),
we weighed each branch to derive weight of
new skeleton. This was then corrected for
the saw cut as described above. We measured linear growth as the distance between
the stain line and branch tip, carefully following the growth axis around bends and
summing the lengths of bifurcating branches.
After dipping each branch (cut and filed
as described above) in paraffin to seal it, we
measured volume of new growth (to the
nearest 0.1 cm3) by water displacement.
Volume was corrected for the width of the
saw blade as described above. The density
of new growth was calculated by dividing
the volume of new growth by its weight. To
measure surface area of new growth, we
dipped each wax-coated sample in liquid
latex, which hardened within 24 h. Latex
peeled from the branch was placed between
plates of glass, traced on transparent film,
and its surface area determined with a digitizer. This yielded surface area of new
growth after correcting for the surface area
cut by the saw.
We also calculated growth rate in terms
of amount of new tissue, new nitrogen, and
new phosphorus. These were calculated as
new surface area times the weight of tissue,
nitrogen, or phosphorus per cm2, as determined for each branch (set) below).
We compiled data on environmental
variables for the 198 1 growth periods. Data
on Tague Bay water temperature were obtained from the U.S. Virgin Islands Department of Conservation and Cultural Affairs. Temperature was measured monthly
at 1 m below the surface. Mean daylength
during each sampling period was calculated
from sunrise-sunset tables. Data on cloud
cover (recorded at the St. Croix airport) were
obtained from the National Climatic Center, Asheville, N.C. Mean daily cloud cover
was computed as the average of hourly readings from 0600 to 1900. These daily means
were then averaged to determine mean cloud
cover during each growth period. Since cloud
cover can reduce calcification by 50% (Go-
159
reau and Goreau 1959), we converted percent cloud cover to a factor ranging from
0.5 (100% cover) to 1.O (no cloud cover) (as
done by Gladfelter 1983b). Number of sun
hours was computed as this factor times the
mean day length.
Tissue analysis- Samples for tissue
chemistry were collected from A. palmata
in December 1980 and April and August
198 1 and from P. furcata on those dates
plus December 198 1 and June 1982. Zooxanthellae were collected from I’. furcata on
all dates except December 1980. Every patch
reef was not sampled on each date.
The branches used for tissue analysis had
been stained with alizarin and collected for
growth measurements. After collection they
were held in tanks of running seawater.
Samples for zooxanthellae were taken from
5 to 10 branches per colony and samples
for tissue chemistry from 9 to 13 branches
per colony. Within 6 h of coral collection,
we removed tissue with a Water-Pik (Johannes and Wiebe 1970), using filtered seawater for zooxanthellae samples and deionized water for the tissue chemistry samples.
On P. furcata branches, we removed tissue from a band around the branch. The
band width (generally 1 cm) and circumference of the branch were measured to calculate the area of tissue removed.. We compared the amount of tissue cm-2 at distances
1,2, and 3 cm from the tip of three branches.
Since the samples 3 cm from the tip had
significantly less tissue than the others, we
took our samples within 2 cm of the tip.
This represents tissue produced within the
past year.
Most branches stained were bifurcating;
therefore we first took samples for zooxanthellae from one branch and then took samples for tissue chemistry from the second.
This eliminated the problem of lysis of zooxanthellae upon exposure to deionized water
(Johannes and Wiebe 1970). Tissue samples
of A. palmata were removed from a measured rectangular area (generally -6 cm2)
in the center of the branch -2 cm from the
growing edge.
Zooxanthellae
samples were homogenized for 1 min in a Sorval Omni-Mixer,
the volume measured, and a 25-ml subsample centrifuged. The pellet was diluted to 5
160
Meyer and Schultz
Table 1. Tissue chemistry and abundance of zooxanthellae in Porites furcata colonies with and without
resident grunt schools. Values shown are means over all seasons t- 1 SE with number of samples in parentheses.
These data were subjected to a two-way ANOVA with presence or absence of fish as one class and season as
the second. Probability levels associated with the F-statistic for the effect of fish are indicated. The interaction
of fish presence with season was not significant (P > 0.05).
With
Tissue dry weight (mg cm-2)
Nitrogen (mg N cm-*)
Phosphorus (mg P cm-2)
N:P (atomic)
Zooxanthellae (cells x 1O6 cm-2)
(cells x lo6 mg-’ tissue)
Without
7.18kO.30
0.564kO.016
0.048+0.002
26.3-10.7
5.48kO.18
0.823kO.056
ml, and four subsamples were counted in a
corpuscle counting chamber. Counts were
expressed as zooxanthellae cmm2 and zooxanthellae mg-l tissue. Tissue weight was
determined later as part of the chemical
analysis.
After centrifuging the tissue chemistry
samples, we recorded the supernatant volume and froze a subsample to be used for
nitrogen and phosphorus determination.
The pellet was lyophilized and analyzed for
nitrogen and phosphorus after dry weight
was determined. We measured the nitrogen
and phosphorus content of supernatant and
pellet samples after digestion with hot sulfuric acid (Technicon 1977). Nitrogen and
phosphorus content of the supernatant and
pellet were summed and expressed as mg N
or P cm-2.
Two-way ANOVA of biomass and growth
data vs. fish presence and season were performed with the General Linear Models
procedure (SAS Inst. 1979).
Grunt removal experiments-Resident
grunt schools were removed from two P.
furcata colonies and growth rates of these
colonies compared with that of a nearby
colony that had no resident grunts. Grunts
were removed by placing a net across their
(72)
(71)
(62)
(62)
(52)
(47)
5.47t-0.24
0.45 1 +o.o 12
0.044+0.002
24.4+ 1.O
4.26kO.11
0.817kO.043
P
(102)
(98)
(99)
(97)
(81)
(76)
0.000 1
0.000 1
0.08
0.79
0.000 1
0.95
migration path at dusk and dawn (Meyer et
al. 1983). In December 1980, 304 grunts
were removed from a colony on Patch Reef
1. Few grunts remained on that colony; by
April 198 1 there were only 28 grunts. We
had greater difficulty removing and keeping
grunts away from the colony on Romney
Point. In December 198 1 we removed 760
grunts from that colony and about 250 more
in February and April 1982 before ending
the experiment in June 1982.
Results
Tissue analysis- Porites furcata colonies
with resident grunt schools had significantly
more coral tissue cm-2 of branch surface
(Table 1). Similarly, colonies with resident
grunt schools had greater amounts of tissue
N cm-2 and numbers of zooxanthellae cm-2;
tissue P cm-2 did not differ significantly.
The N:P ratio did not vary with fish presence.
Tissue chemistry of branches from A. palmata colonies (Table 2) showed somewhat
different patterns than those of P. furcata.
There was no significant
difference
in
amount of tissue cm-2 of branch surface;
however, the amounts ofN cmd2 and P cm-2
were significantly higher in colonies with
Table 2. Tissue chemistry for three colonies of Acropora palmata with and three without resident grunt
schools. Values are means over all seasons f 1 SE with number of samples in parentheses. Probability (P) levels
for the F-statistic from a one-way ANOVA are listed.
Tissue dry weight (mg cme2)
Nitrogen (mg N cm-*)
Phosphorus (mg P cm-2)
N:P (atomic)
5.8OkO.39
0.44-10.05
0.050~0.005
20.7k2.1
P
Without
With
(27)
(13)
(12)
(12)
5.86-t0.58
0.28kO.03
0.03 1 t-O.004
21.8kO.7
(29)
(29)
(29)
(29)
0.92
0.004
0.008
0.51
161
Eflkcts ofjish on corals
Table 3. Growth rates and density of new skeleton over three 4-month growth intervals for P. fircata colonies
with and without resident grunt schools. Values are means + 1 SE with number of samples in parentheses. These
data were subjected to a two-way ANOVA with presence or absence of fish as one class and season as the second.
Probability levels associated with the F-statistic for the effect of fish are indicated. Seasonal effects are indicated
in Table 4. The interaction of fish presence with season was never significant (P > 0.05).
Without
With
0.96kO.05
1.00~0.05
4.3OkO.17
0.91 -to.04
1.07kO.02
30.98k1.38
2.33f0.10
0.19+0.01
Skeleton deposited (g per 4 mo)
Linear expansion (cm per 4 mo)
Surface area (cm2 per 4 mo)
Volume (cm3 per 4 mo)
Density (g cm-3)
Tissue dry wt (mg per 4 mo)
Tissue N (mg N per 4 mo)
Tissue P (mg P per 4 mo)
resident grunt schools. The N:P ratio was
not affected by the grunts.
Porites colonies showed significant seasonal variation in amount of tissue, nitrogen, phosphorus, and zooxanthellae cm-2 of
branch surface. However, values for all parameters were not consistently high in one
season and low in another. For example,
amount of tissue was high in April, amount
of nitrogen was high in December, and zooxanthellae were abundant in August.
Coral growth-Growth rates of P. furcata
branches were generally higher in the presence of resident grunt schools (Table 3).
Weight of new skeleton, surface area and
volume of new growth, and amounts of new
tissue and new tissue nitrogen were all significantly greater in the presence of grunts.
Linear growth was not significantly greater,
probably because average branch diameter
differed between colonies. We found no significant difference in density of new growth
P
0.78 kO.03
1.04+0.03
3.85&O. 11
0.77kO.03
1.04+0.02
21.98f1.00
1.68kO.07
0.17f0.01
(148)
(149)
(149)
(149)
(148)
(139)
(134)
(113)
(202)
(203)
(202)
(201)
(201)
(182)
(174)
(174)
0.0008
0.37
0.04
0.005
0.23
0.000 1
0.000 1
0.06
between colonies with grunts and those
without.
Seasonal differences in growth rate of P.
furcata were also apparent (Table 4). All
growth measures except linear expansion
varied significantly with season. These data
were further analyzed with Duncan’s multiple range test to determine during which
seasons growth rates were different. Growth
rate measures showing significant seasonal
variation were consistently high during the
period from May to August. For some measures (amounts of new nitrogen and phosphorus) rates were lowest in the DecemberApril period, for others (surface area, volume, and amount of new tissue) in the September-December
period. There were also
significant seasonal differences in density of
new growth: the skeleton deposited from
May to August was most dense, that deposited from January to April was least
dense (Table 4).
Table 4. Seasonal differences in growth rates and density of new growth for P. furcata colonies measured
over three 4-month periods. Values are means -t 1 SE with number of samples in parentheses. These data were
subjected to a two-way ANOVA with presence or absence of fish schools as one class and season as the second.
Probability levels associated with the F-statistic for the seasonal effect are indicated. The effect of resident grunts
is indicated in Table 3. The interaction of fish presence with season was never significant (P > 0.05).
Jan-Apr
Skeleton deposited (g per 4 mo)
Linear expansion (cm per 4 mo)
Surface area (cm* per 4 mo)
Volume (cm3 per 4 mo)
Density (g cm-3)
Tissue dry wt (mg per 4 mo)
Tissue N (mg N per 4 mo)
Tissue P (mg P per 4 mo)
198 1
0.80+0.04 (103)
1.09+0.05 (103)
3.94kO.15 (103)
0.90+0.04 (102)
0.89kO.02 (102)
31.3k1.4
(94)
1.62kO.08 (89)
0.16+0.01 (87)
May-Aog
0.98kO.04
1.03f0.05
4.51-co.17
0.86kO.04
1.17kO.03
27.4& 1.6
2.24kO.12
0.21+0.02
198 1
(117)
(118)
(117)
(117)
(117)
(112)
(107)
(88)
Sep-Dee
0.8 140.06
0.9640.05
3.8340.19
0.75kO.05
1.10~0.02
21.5k1.3
1.9640.10
0.19+0.01
1981
(97)
(97)
(97)
(97)
(97)
(86)
(83)
(83)
P
0.003
0.23
0.0008
0.02
0.000 1
0.000 1
0.0003
0.006
162
Meyer and Schultz
Table 5. A comparison of growth rates on colonies of P. furcuta before and after removal of resident grunt
schools. These data are from two removal experiments: on Romney Point reef from December 198 1 through
June 1982 and on Patch Reef I from December 1980 through August 198 1. Colony W had a resident grunt
school before removal; colony WO had no grunts. All growth data are presented as mean annual rates, but were
collected over different periods, as indicated.
Romney
Point
Before removal
W
Patch Reef 1
After
wo
removal
W
Before removal
wo
Period of growth
Dee 80-Aug 8 1*
Dee 8 I-Jun
n
Skeleton (g yr-I)
Linear (cm yr-l)
Surface area (cm2 yr-I)
Volume (cm3 yr-I)
Tissue (mg yr-I)
N (mg v-9
P (mg v-7
40
2.40
2.19
11.2
0
Q
33
1.98
2.82
10.1
27
2.81
2.90
10.9
84;
5.73
0.53
0
0
0
46;
3.39
0.38
4.45
0.75
82t
W
Dee 79-Dee 801
21127
2:85
9.8
-
:.:9,,
5.33
17.4
4.78
2.94
0.30
82.6
9.10
0.58
0
0
* Means from two 4-month growth periods.
t Means from one 6-month growth period.
$ Means from one 12-month growth period.
5 Differences between colonies W and WO are significant
(t-test, P < 0.05).
11From Meyer et al. 1983.
ll These data are slightly different from those in Meyer et al. 1983, which are from one S-monlh
mean from two 4-month growth periods used here. The data in Meyer et al. 1983 also showed
We also assessed the effect of resident
grunt schools on P. furcata growth rate with
two grunt removal experiments. Before grunt
removal from Romney Point reef, four of
the six measures indicated significantly more
rapid growth in the colony with grunts (Table 5). Linear growth rates were higher in
the colony without grunts, where branches
were of smaller diameter than the colony
with grunts. After removal only one growth
rate measure was significantly greater in the
colony that had previously had grunts.
A more dramatic effect of grunt removal
was seen on Patch Reef 1. Before removal,
five of the seven measures of growth rate
were significantly greater in the colony with
grunts (colony W: Table 5). After grunt removal five of the seven growth rate measures were significantly greater in the colony
that never had had resident grunts (colony
WO). In other words, colony W grew significantly
faster than colony WO when
grunts were present and significantly slower
than colony WO when the resident grunt
school was removed.
Discussion
Seasonal variation in coral growth rate
and density-Growth
rates for P. furcata
have not been reported previously.
Those
After
wo
given here
rapid than
al. 1968).
branching
than rates
48.5
6.50
0.42
removal
W
wo
Jan 81-Aug
37
2.22ll
3.03
11.3
2.3
74.1
4.59
0.61
9
0
ii
0
81*
60
3.ooll
3.60
14.2
9:::
6.39
0.67
growth period on fewer branches rather than the
significantly
greater growth on colony WO.
(Tables 3, 5) are somewhat more
rates for Porites Porites (Lewis et
Growth
rates of both these
species are considerably greater
reported from St. Croix for Porites astreoides, a platelike coral, but less
than those for a branching acroporid like
Acropora cervicokis (Gladfelter et al. 1978).
The density of new skeleton produced
varied with season (Table 4). Most studies
of seasonal changes in density of coral skeleton have been done with massive species
and have used X-radiographs
to discern
patterns of density variation (references in
Highsmith
1979). In general these studies
have shown low density skeleton to be deposited at high growth rates (measured as
linear extension) and high density bands to
be associated with periods of slow growth.
Our data are somewhat different in that the
rate of linear growth did not vary with season, although skeletal density did (Table 4).
A similar lack of seasonal change in linear
extension rate has been noted for A. cervicornis in St. Croix (Gladfelter 1983a).
Current evidence (e.g. Goreau and Hayes
1977; Gladfelter 1982, 1983b) suggests that
growth of the coral skeleton is a two-step
process: formation of a scaffolding of CaCO,
crystals (“matrix production”)
and filling in
163
Efects ofjkh on coruls
variables, coral growth, and skeletal density measures over three periods
Table 6. Variation in environmental
of growth during 198 1. To facilitate comparisons, values are expressed as a percentage of the maximum observed
value for each parameter. The maximum value is included in parentheses. Sun hours were calculated as described
in the text. Infilling was measured as weight of new skeleton and matrix formation as volume of new skeleton.
Temp
(27.7”C)
Jan-Apr
May-Aug
Sep-Dee
90
97
100
Sun hours
(8.9 h)
94
100
96
-
Infilling
(0.98 g per 4 mo)
Matrix
production
(0.90 cm3 per 4 mo)
Tissue wt
(3 1.3 mg per 4 mo)
82
100
82
100
95
83
100
87
69
the crystalline scaffolding by further CaCO,
precipitation on those seed crystals (“infilling”). Highsmith (1979) has developed a
model which suggests the seasonal variation
in skeletal density seen in X-radiographs to
be a consequence of temperature-induced
variations in rates of these two processes.
Although we did not measure coral density
by X-ray analysis, the validity of this model
as a predictor of seasonal density variation
in corals from Tague Bay can be examined
if we use rate of increase in skeleton volume
as a measure of matrix production
and
weight of CaCO, deposited as a measure of
infilling.
Matrix
production
was significantly lower from September to December
than during the other periods; infilling was
significantly
greater during May-August
than during the other months; and density
was lowest during January--April
(Table 4,
Duncan’s multiple range test, P < 0.05).
Hence skeletal density was low when matrix
production was high, and density was high
when infilling was high (Table 6). Neither
density nor matrix production shows a simple relationship with temperature or light;
however, infilling appears to be directly related to light availability.
This evidence of
the importance of light rather than temperature as a determinant of density banding
in corals is in agreement with the results of
Wellington and Glynn (1983), although the
temperature variation in Tague Bay (Table
6) was slight and temperatures were always
within Highsmith’s (1979) optimum range.
The absence of a relationship
between
light and matrix production and the existence of a relationship between light and
infilling is to be expected from the results
of Barnes and Crossland (1980), who found
little diel variation in linear extension (i.e.
Skeletal density
(1.17 g cme3)
76
100
94
matrix production) but significant diel variation in calcification (i.e. infilling). The dependence of calcification on light and hence
on photosynthesis of zooxanthellae is well
known (Goreau 1959; Vandermeulen et al.
1972). We found maximum abundance of
zooxanthellae in August, when infilling is
greatest (Table 6).
The efect of resident grunts on coralsGrunts appear to have an impact on the
coral colonies over which they rest. Colonies with grunts had more tissue cm-2 and
N cme2. This may indicate a healthier coral,
since stressed corals have been observed to
have lower tissue cm-2 (Franzisket 1970;
Clayton and Lasker 1982) and well fed corals to have higher tissue cm-2 as well as
higher N cm-2 (Szmant-Froehlich
and Pilson 1980).
Density of zooxanthellae was greater on
colonies with resident grunts. Higher density of zooxanthellae has also been observed
in corals that were well fed with zooplankton (Johannes 1974). Because of the coral’s
dependence on zooxanthellae to meet its energy requirements (Porter 1980; Muscatine
et al. 198 l), a higher density of zooxanthellae could be beneficial to the coral.
These effects of fishes are comparable to
the effects observed when crustacean endosymbionts
are present in Pocillopora
damicornis, namely higher tissue nitrogen
and more rapid coral growth (Glynn 1983).
They are in marked contrast to observations
on damage done to corals by fishes, both
corallivores (Randall 1974) and damselfishes that maintain an algal turf (Vine 1974;
Kaufman
1977; Wellington
1982; Sammarco and Williams 1982).
Although the differences between colonies in tissue chemistry,
zooxanthellae
164
Meyer and Schultz
abundance, and growth rate are statistically
significant, they are not large. For P. furcata
the greatest difference was in growth rate
expressed as amount of new tissue produced, where the mean value for colonies
with grunts was 14 1% of the mean for colonies without grunts. The differences we report are subtle differences between colonies.
The effects of resident grunts were inferred from a comparison of colonies with
vs. without grunts. It could be argued that
these differences were due to factors other
than the presence of grunts. The removal
experiments (Table 5) demonstrated that fish
presence and not some other factor accelerated coral growth. The data from Patch
Reef 1 showed this most clearly: when compared to a reference colony without grunts,
the colony with grunts grew significantly
more rapidly when grunts were present and
significantly more slowly when grunts were
removed. The data from Romney Point were
less dramatic; mean growth rates after grunt
removal were still somewhat greater than
on the reference colony, but the differences
between colonies were no longer statistically
significant. The different magnitudes of response to grunt removal on these two patch
reefs are probably due to our inability to
keep the Romney Point colony free of grunts
for a long period and to the large number
of squirrclfishes
present on this colony.
Squirrelfishes also feed away from the colony at night and return to it for the day. On
the Patch Reef 1 colony there were < 10
squirrelfish. On the Romney Point reference
colony there were no squirrelfish whereas
on the colony with grunts there were 150200 squirrelfish. These fish were not removed when the grunts were removed;
hence their excretory products were still
present to fertilize the corals.
Mechanisms responsible for the efect of
grunts on corals- We have no conclusive
evidence elucidating the mechanisms responsible for the differences in tissue chemistry and the more rapid coral growth observed in the presence of resident fishes. It
is probably a complex and multifaceted relationship.
One very simple mechanism
about which we have some information
is
nutrient enrichment by the nitrogen and
perhaps also the phosphorus present in grunt
excretory and fecal material. When phosphorus is present in much higher concentrations than found here (Meyer et al. 1983),
it can decrease coral growth rate (Kinsey
and Davies 1979). However considerable
evidence exists to suggest that nutrient, espccially nitrogen, enrichment can stimulate
coral growth. Nutrient enrichment has been
implicated in more rapid coral growth in
some upwelling areas: upwelling on the
Great Barrier reef could add 20 pmol N
liter-’ annually to the reefs (Andrews and
Gcntien 1982). The grunt schools we studied add -400 pmol NH,+ liter -I annually
to water surrounding the P. furcata colonies
over which they rest (calculated from data
of Meyer et al. 1983). If additional nutrients
from upwelling can foster the luxuriant coral growth of the Great Barrier reef, grunts
could clearly be having a similar effect, although on a much smaller spatial scale.
Laboratory
experiments
have dcmonstrated increased rates of coral calcification
with NH4i enrichment
(Crossland
and
Barnes 1974; Taylor 1978) and with zooplankton supplements (Jacques and Pilson
1980), which are frequently considered to
provide a source of nutrients for corals (Johannes et al. 1970). The observed acceleration of calcification appears to be a consequence of increased photosynthesis
by
zooxanthellae (Taylor 1978). The growth
rate of zooxanthellae is higher in hosts that
experience elevated nutrient levels (Wilkerson et al. 1983). This could explain our
observation of more zooxanthellae cm-2 in
P. furcata with resident grunt schools.
Direct uptake of dissolved nitrogen and
phosphorus has been well documented in
corals (e.g. D’Elia and Webb 1977; D’Elia
1977). Corals can take up NH,+ more rapidly than other forms of dissolved nitrogen
(D’Elia and Webb 1977; D’Elia et al. 1983)
and NH,+ represents from 80 to 99% of the
dissolved nitrogen excreted by grunts (Meyer et al. 1983). Some evidence for direct
consumption of the particulate fraction also
exists (McCloskey and Chesher 197 1); however, even if corals ingest few grunt feces
directly, feces may also enrich corals indirectly via leaching of dissolved nutrients
(Meyer and Schultz 1985) and via enrichment of food resources for demersal zoo-
sh on corals
plankton. These animals are abundant bcneath coral colonies (Porter and Porter 19 7 7)
and are potentially an important component of the coral’s diet (Muscatine and Porter 1977).
Coral growth rate is influenced by a host
of physical, chemical, and biological factors
(Sheppard 1982). On the basis of the data
presented here, we suggest that localized nutrient enrichment from fish schools should
also be considered such a factor. Although
we have documented this only for grunts,
the phenomenon of resting in large aggregations over or in coral colonies and feeding
off the reef is widespread among fishes
(Hobson 1973; Helfman 1981). Hence the
enrichment of individual
coral colonies by
fish schools may be a very common phcnomenon.
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Submitted: 10 January 1984
Accepted: I9 July 1984