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S . Macia J. Exp. Mar. Biol. Ecol. 246 2000 53 –67
Table 3
a
Two-way ANOVA for T . testudinum biomass in the winter experiment
Source df
MS F
p Aboveground biomass
Urchin density 2
50.67 8.21
0.001 Algae
1 10.35
1.67 0.205
Urchin 3 algae 2
0.52 0.08
0.919 Error
30 6.17
– –
Belowground biomass Urchin density
2 2.41
0.54 0.590
Algae 1
9.35 2.08
0.160 Urchin 3 algae
2 1.65
0.37 0.697
Error 30
4.50 –
–
a
Cage control treatments were not included in the analysis because no cage effects were detected see Table 2. Assumptions of both normality and homoscedasticity were met.
of density, had no significant effect on seagrass biomass Fig. 3b; aboveground: df 5 23; F 5 1.34; p 5 0.289; belowground: df 5 23; F 5 0.13; p 5 0.939.
A total of 34 macroinvertebrate species were identified from the site, but the vast
22
majority were present in very small numbers 1 per m . Overall macrofaunal abundance including echinoderms, molluscs, polychaetes and sponges was 144.5615.3
22
individuals m in the summer, and 117.7612.0 in the winter. The four most common
species were the epifaunal gastropod Lithopoma americanum Turbinidae, the sponge Haliclona permollis Haliclonidae, and the infaunal polychaetes Marphysa sanguinea
Eunicidae and Asychis elongata Maldanidae. The density of H . permollis, averaged
22 22
over all treatments, was 0.24 m 60.07 in the summer and 0.31 m
60.07 in the winter. Results of the paired t-tests indicated that for no treatment, in either winter or
summer, was there a change in the density of H . permollis all p . 0.05. Similarly, no
significant differences were found in numbers of L . americanum, A. elongata, or M.
sanguinea Table 4.
4. Discussion
4.1. Effects of urchin grazing on seagrass population The seagrass bed at West Point harbors a small, but relatively stable, population of L
. variegatus. Exclusion of urchins had no effect on either the shoot density or biomass of
T . testudinum, indicating that the natural levels of grazing at West Point are not
sufficient to have a significant impact on the biomass or shoot density of the seagrass ´
population. This result agrees with the findings of Cebrian et al. 1998, who found that moderate grazing of seagrasses, as mimicked experimentally by clipping, has little, if
any, negative effect on leaf growth rate. The present study, however, took place over a
´ S
. Macia J. Exp. Mar. Biol. Ecol. 246 2000 53 –67 61
Fig. 3. Biomass of Thalassia after 6 weeks at experimental urchin densities. a Winter experiment August– September 1997: bars represent pooled 1 and 2 algae treatments. Aboveground values with different letters
are significantly different from each other. Belowground biomass did not differ among treatments. b Summer experiment January–February 1998: no significant differences were detected among any of the treatments for
either above- or below-ground biomass.
period of only 6 weeks. Further experiments are needed to determine if the pattern found ´
here holds true over longer time periods Macia, manuscript in preparation. Two seagrass population variables, biomass and shoot density, were used to assess the
effects of urchin grazing and drift algae at the study site. These two variables, however, did not necessarily react similarly to the experimental treatments. In the summer,
experimentally increased urchin grazing did not significantly affect shoot density. At 20
22
urchins m , however, the difference in shoot count was only marginally non-significant
´ 62
S . Macia J. Exp. Mar. Biol. Ecol. 246 2000 53 –67
Table 4
a
The common macroinvertebrates of West Point, Biscayne Bay, Florida
22 2
Species Season
Density [ m x
p L
. americanum Summer
0.0960.04 6.32
0.390 Winter
0.1560.04 5.68
0.770 M
. sanguinea Summer
53.765.8 7.21
0.302 Winter
67.369.7 6.41
0.698 A
. elongata Summer
33.067.6 12.38
0.054 Winter
61.9611.4 16.77
0.053
a
Lithopoma americanum is an epifaunal gastropod; Marphysa sanguinea and Asychis elongata are infaunal polychaetes. Population densities are averaged over all treatments, and given in mean6S.E. Results of the
Kruskal–Wallis test comparing final invertebrate densities among all treatments are presented.
22
p 5 0.056. This suggests that, for this time of year, 20 urchins m is the critical
urchin density above which the seagrass shoot density will be negatively affected. During the winter months, this critical density is less than that of the summer. Shoot
22
count data indicate that at 10 urchins m , in the presence of the naturally occurring
algae, shoot density is significantly decreased. Winter critical urchin density for negative
22
effects on shoot number is therefore approximately 10 urchins m , half of the
corresponding summer value. Thus, the effects of grazing on T . testudinum shoot density
are more pronounced in the winter than in the summer. Estimated critical urchin densities for negative effects on biomass were higher than
those for shoot density. Aboveground biomass was affected by urchin grazing only in
22
the winter, and then only at the highest density tested 20 urchins m . Biomass at this
urchin density, however, was not significantly different than the biomass at 10 urchins
22
m , indicating that critical urchin density for biomass effects in the winter is
22
somewhere between 10 and 20 urchins m . Biomass in the summer did not decline
22
significantly even at 20 urchins m . Therefore, critical urchin density for biomass
22
effects in the summer must be at some value higher than 20 per m . Although the
critical urchin densities for shoot number and aboveground biomass differ, both variables indicate that grazing on T
. testudinum has a more pronounced effect in the winter. This conclusion is similar to that found by Valentine and Heck 1991, who used
cages to study L . variegatus grazing effects in the northern Gulf of Mexico. Their study
indicated that approximately twice as high an urchin abundance is required to overgraze
22
aboveground T . testudinum biomass in the summer . 40 urchins m
than in the
22
winter , 20 urchins m . The results of Valentine and Heck 1991 pertain to
complete defoliation of the seagrasses, however; even their lowest urchin density 10
22
urchins m was enough to cause significant decreases in biomass at all times of the
year. At West Point, the critical urchin density required for negative effects on aboveground
22
biomass 4 20 and 10–20 urchins m in the summer and winter, respectively
22
appears to be higher than that for shoot density 20 and 10 urchins m in the summer
and winter, respectively. In other words, shoot density is affected by urchin grazing before effects on biomass become apparent. This pattern may be a result of urchin
grazing activity causing an increase in T . testudinum shoot-specific productivity.
´ S
. Macia J. Exp. Mar. Biol. Ecol. 246 2000 53 –67 63
Increased productivity could manifest itself as longer or more numerous leaves per shoot, either of which would produce greater amounts of biomass. In this way,
aboveground biomass may remain unaffected by grazing even though shoot density is decreasing. A grazing-induced increase in productivity has in fact been documented for a
T
. testudinum population in the Caribbean island of St. Croix, which exhibits increased specific growth rate when subject to moderate levels of turtle or urchin grazing Zieman
et al., 1984. Studies from terrestrial grasslands suggest several mechanisms through which grazing can increase plant productivity. These mechanisms include: increased
rates of photosynthesis stimulated by the loss of photosynthetic products; reallocation of nutrient reserves from the root system; increased light penetration resulting from
decreased self-shading effects; and nutrient input in the form of grazer feces urine McNaughton, 1979 and references therein; Milchunas and Lauenroth, 1993. Of the
mechanisms mentioned above, fertilization of seagrasses by urchin feces may be
´ particularly important to T
. testudinum Macia, manuscript in preparation. The results of this study suggest that the vulnerability of seagrasses to grazing
depends on the level of grazing pressure that the seagrass population normally experiences. Seagrass beds exposed to relatively low grazing rates, such as at West
Point, may be more resistant to short-term increases in grazing rates. Critical urchin density for negative effects on seagrass biomass estimated from this study is higher than
22
the 10 urchins m found by Valentine and Heck 1991 in the Gulf of Mexico. This
contrast may be a result of the different grazing pressures exerted naturally on these two seagrass beds. In the Gulf of Mexico site, urchin density ranged from 12 to 25 urchins
22 22
m , whereas in Biscayne Bay the urchin density is only 1.4 per m
. Field studies from Jamaica show that T
. testudinum subjected to repeated cropping every 70 days exhibits a decline in biomass after the sixth and seventh harvests Greenway, 1974. Valentine and
Heck 1991 stated that conditions for overgrazing are common at their site. Periodic overgrazing may make this T
. testudinum population more susceptible to grazing effects than the West Point population, which appears to suffer virtually no impact from the
naturally low grazing pressure. Using caging experiments, Keller 1983 investigated another Jamaican population of L
. variegatus with a relatively low population density
22
3.7 per m . On all but one of the sampling dates, experimental densities of 16 urchins
22
m had no significant effect on aboveground T
. testudinum biomass. This situation is similar to the present study, where a seagrass population with low natural urchin
abundance appears to be relatively resistant to experimentally increased grazing pressure.
4.2. Effects of drift algae and interaction with grazing Removal of algae in the urchin exclusion cages did not have a positive effect on
seagrass shoot density, indicating that drift algae alone do not appear to negatively affect this parameter. Similarly, drift algae did not affect seagrass biomass. For shoot density,
however, there was an interaction between drift algae and increased urchin density. Removal of algae had a positive effect on T
. testudinum shoot density in the 10 urchins
22
m treatment: cages without algae did not experience a significant decrease in shoot
count, while those with algae did. Although shoot density declined both with and
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S . Macia J. Exp. Mar. Biol. Ecol. 246 2000 53 –67
22
without algae in the 20 urchins m treatment, the effect was more pronounced for the
1 algae treatment, as shown by the lower p-value in the paired t-test. Hull 1987 discussed the potential effects, both positive and negative, of benthic
macroalgal mats on the surrounding community. Among these are reduced water velocity, flushing and oxygen exchange between the sediment and water column. While
these factors may not be of great importance to T . testudinum, which thrives in anoxic
sediments Zieman, 1982, competition for light can be very important Short et al., 1995. The drift algal mats at the study site are very thick and can completely obscure
large seagrass patches of many square meters in area personal observation. Neverthe- less, the results of the present study suggest that the annual algal bloom alone has no
negative effects on T
. testudinum shoot density or biomass. Other studies, however, have shown that if such patches remain in place for sufficiently long periods of time e.g. 6
months they can cause substantial loss of aboveground biomass and create bare patches Holmquist, 1997.
Although the naturally-occurring drift algal blooms do not appear to have significant effects on the T
. testudinum population, when combined with increased grazing pressure there are synergistic effects that can greatly decrease seagrass shoot density. Increased
grazing pressure exacerbates the negative effects of the drift algae or vice versa. When subject to both algal competition and increased urchin grazing, T
. testudinum shoot density experiences a greater decline than when there is only an increase in grazing
activity. Thus it appears that the non-significant impact of the naturally occurring urchin population is important to the persistence of the West Point seagrass community.
Increased grazing pressure from a larger urchin population, coupled with the negative effects of algae, could be so detrimental as to prevent full recovery of the seagrass
population from the annual algal bloom.
4.3. Effects on the invertebrate population The numbers of invertebrates found in this study are relatively low in comparison to
other seagrass bed studies, which often report invertebrate abundances in the thousands
22
per m Santos and Simon, 1974; Brook, 1978; Gore et al., 1981; Greening and
Livingston, 1982; Virnstein et al., 1983; Bauer, 1985; Virnstein and Howard, 1987; Valentine and Heck, 1993; Greenway, 1995. One factor undoubtedly contributing to the
low observed faunal numbers in the present study is sampling design. The sampling protocol used in this study could not effectively include crustaceans, which are among
the most common inhabitants of seagrass beds Orth, 1973; Gore et al., 1981; Lewis, 1984; Holmquist et al., 1989. Even with the absence of crustacean numbers taken into
account, however, the abundance of invertebrates at the study site is still considerably lower than that found in other studies. The reasons for this are unclear, and await the
results of further studies.
Four invertebrate species, other than L . variegatus, were commonly found at West
Point. None of these species showed a substantial response to increased urchin grazing, even when such grazing had significant effects on the seagrass. This result is not
surprising for the sponge Haliclona permollis, as L . variegatus does not generally feed
upon sponges. The herbivorous gastropod Lithopoma americanum, however, resides on
´ S
. Macia J. Exp. Mar. Biol. Ecol. 246 2000 53 –67 65
the seagrass blades, presumably feeding on epiphytes Emerson and Jacobson, 1976. As there was no decrease in aboveground biomass of T
. testudinum in the summer experiment, the lack of an effect on L
. americanum is not surprising. In the winter, however, there was a decrease in seagrass biomass in the high urchin density treatment.
Nevertheless, a concurrent decline in the abundance of L . americanum did not occur.
The population density of L . americanum found during the winter was very low 2
22
0.1560.04 individuals m . It is possible that such a small population could maintain
itself on what seagrass remained, despite the significant losses in aboveground biomass. The polychaetes Marphysa sanguinea and Asychis elongata feed primarily on detritus
Day, 1967; Fauchald and Jumars, 1979; Prevedelli, 1992. Neither species was affected by the experimental treatments. As part of the infauna, these animals would not
experience any direct impact from the algae or the urchins, which are primarily aboveground grazers. It is also unlikely that, over the short duration of the experiment 6
weeks, increased grazing pressure would affect the amount of detritus available below the surface of the sediment, where these species feed. Long-term exposure to increased
urchin grazing activity, however, could potentially increase the amount of organic
´ material in the sediment via deposition of feces Macia, manuscript in preparation.
These could eventually be worked into the sediment and benefit the infaunal detritivores.
5. Conclusions
