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Oecologia
Oecologia (Berlin) (1984) 63: 295-299
© Springer-Verlag 1984
An experimental investigation of enhanced harpacticoid
(Copepoda) abundances around isolated seagrass shoots
David Thistle
1
2
Department
Department
t,
Jeffrey A. Reidenauer
1,
Robert H. Findlay
2,
and Richard Waldo
1
of Oceanography, Florida State University, Tallahassee, FL 32306, USA
of Biological Science, Florida State University, Tallahassee, FL 32306, USA
Summary. At a site in the Gulf of Mexico (29° 54.6' N,
81°31.4' W) off the coast of northern Florida, harpacticoid
copepod abundance is significantly enhanced around isolated "plants" (technically short shoots) of the seagrass
Syringodium filiforme. Using inanimate mimics of seagrass
short shoots, we demonstrate, in the field, that the enhanced
abundance does not result from the presence of the plant
as a living entity. Our experiments reveal a two-fold increase
in bacterial biomass around both short shoots and mimics;
the harpacticoids appear to be responding to a local increase in their resources. We suggest that the flow field
around a short shoot improves the rate of supply of oxygen
and other materials to sedimentary bacteria, thereby driving
the effect. Given the ubiquity of structures that have similar
flow effects, localized bacterial enhancement may be common and should be considered in studies of the effects of
surface structures on soft-bottom community organization.
grass Syringodium filiforme. This sea grass has leaves (=
blades) that are roughly circular in cross section and 10's
of cm long. One or more leaves surrounded by a sheath
is termed a short shoot. Short shoots are connected by
a rhizome that lies 4 to 5 em below the sediment surface.
Harpacticoid biology suggested three likely causes of
the enhanced abundance: (1) the area immediately around
a short shoot was a predation refuge (Woodin 1978, 1981),
in particular, from bottom-feeding fishes; (2) the microbial
food of harpacticoids was unusually abundant around the
short shoot because the seagrass plant supplied nutrients;
or (3) food was abundant because the plant interacted with
the near-bottom flow in such a way that microbial growth
was stimulated. Below, we report our investigation of these
mechanisms.
Locality
Introduction
Studies of macroinfaunal communities have historically reported patterns in the distribution of species with arguments
as to their likely causes (Gray 1974). Only recently have
field experiments supplemented this correlative approach,
allowing the direct investigation of suspected underlying
mechanisms (e.g., Woodin 1974, 1978; Peterson and Andre
1980), and only a few, controversial generalizations have
appeared (e.g., Rhoads and Young 1970; Woodin 1976;
Peterson 1979).
Our understanding of the reasons for the localization
of infaunal meiofauna species in space is even more rudimentary. Zonation patterns on beaches have been described
together with their environmental correlates (e.g., Wieser
1959; Pollock 1970; Harris 1972), but for other soft-bottom
habitats, few patterns are known (e.g., Heip and Engels
1977; Bell et al. 1978; Coull et al. 1979; Osenga and Coull
1983), and few field experiments have been done (e.g., Bell
1980; Thistle 1980b; Fleeger et al. 1982; Reise 1983). We
seem far from any general explanation of meiofauna localization, and it seems likely that the study of many examples
will be required before any generalizations emerge. Below,
we present a pattern and explore its causes.
The pattern involves the increased abundance of harpacticoid copepods in the vicinity of short shoots of the seaOffprint requests to.' David Thistle
The site was at 1 m depth in St. George Sound, Florida,
about 300 m offshore (29°54.6' N, 81°31.4' W). In this region, seagrass meadows occupy the shallow-subtidal habitats (Bittaker and Iverson, submitted). On our site, Thalassia testudinum Konig (turtle grass) dominated the shallow
portion of the seagrass meadow, giving way to Syringoidum
filiforme Kuntz (manatee grass) and then to un vegetated
fine sand (graphic mean particle size = 0.155 mm) as the
water deepened. We worked at the interface between S.
flliforme and un vegetated sediment. This area is protected
by offshore islands and shoals, so waves are small in the
absence of local storms. Current velocity at 20 cm above
bottom averaged 4.3 cm/s (maximum velocity = 15.6 cm/s)
for 11 h of measurement (Sherman et al. 1983).
Materials and methods
Syringodium rhizomes that extended into otherwise unvegetated bottom bore short shoots that varied in their degree
of isolation. In this study, we used short shoots having
a single blade and located 5 em or more from the nearest
neighboring short shoot. To determine the dimensions of
such isolated short shoots, we identified 15 qualifying short
shoots, chose 10 at random, and cut them off at the sediment surface. In the laboratory, we measured their lengths
with a em rule and widths with the ocular micrometer of
a dissecting microscope. These data were used to select dimensions for the short-shoot mimics.
296
Fig. 1. A schematic representation
text for details of its construction.
cated. The scale line is 1 cm
of a seagrass mimic; see the
The sediment surface is indi-
The mimics were 28-cm-long pieces of polyethylene tubing (1.22 mm outer diameter). The top 5 em contained air
and served as a float; the balance was filled with agar that
had been dyed with food coloring to approximate the green
of short shoots. The ends of the tubes were melted closed
to seal the agar inside. All external traces of agar were
removed by ultrasonic cleaning. The lowest 3 em were
bound with monofilament line to a 4-cm-long glass-rod anchor. In the experiments, 6 em of the colored portion of
the tube were placed below ground, leaving 17 em exposed
(Fig. 1). The mimics were emplaced as if for the experiment
but in an unused part of the study area to condition for
one month before the start of each experiment.
Our experiments were deployed according to a randomized-block design. For each block, an isolated short shoot
was located. A pre-selected random arrangement was used
to determine where the mimic and control should be located
relative to the target short shoot. The three locations roughly paralleled the rhizome bearing the target short shoot.
The mimic and control sites were chosen to be 5 em away
from the nearest short shoot. The distances from the two
end locations to the center location were equal within a
block; among blocks, the inter-treatment distances were
randomly chosen to be at least 10 cm but less that 25 cm.
Blocks were at least 20 em from the body of the seagrass
bed.
In this region of the seagrass bed, new short shoots
appear frequently while existing short shoots produce additional blades or are broken off. For these reasons, the prearranged sample locations could not always be used. For
disrupted blocks where the mimic remained, new short
shoots and control sites were sought that met the above
criteria and preserved as much of the original randomization as possible (e.g., direction along the rhizome). One
could not merely start again because the mimic constrained
the location of the block. Although not strictly random,
the relative positions of the treatments varied and were
not in the experimenter's control; we treat them as if they
had been mechanically randomized.
The first experiment was designed to test the reality
of the positive association of harpacticoid copepods with
isolated short shoots that appeared in some preliminary
data (Waldo, unpublished). The experiment ran for 11 days
in August, 1981. At the time of sampling, the short shoots
and mimics were clipped at the sediment surface and allowed to float away. Cores (3.5-cm inside diameter) were
taken centered on the spot where each blade (mimic or
short shoot) had been. Control cores were each centered
on a predetermined spot. On the boat, the overlying water
and top 1-cm layer from each sample were preserved in
10% formaldehyde. In the laboratory, the samples were
sieved on a 0.062-mm aperture sieve. The harpacticoids
were concentrated using the Barnett (1968) technique,
stained with rose bengal, and sorted under a dissecting microscope; the Barnett procedure was 100% efficient (n = 6).
Adults and fifth-stage copepodites were identified to working species and counted. We have begun to describe this
largely new fauna formally (Thistle 1980a), but many species are without names.
The second experiment was designed to detect differences in bacterial biomass and metabolic status among the
three treatments. The experimental design followed that described above. It was done in August, 1983, and was sampled as follows. After a blade was clipped, a small (I-em
diameter) core was emplaced next to the stub and stoppered. A 3.5-cm inner diameter core was then emplaced
centered on the stub, stoppered, and the assembly removed
from the sediment. On the boat, 14 microliters of filtersterilized sea water containing 0.1 microcurie/ml of[1_14C]labeled sodium acetate (56 microcuries/micrornole,
ew
England
uclear Corp., Boston, MA) were injected into
the sediment in the large core through a self-sealing silicone
port 0.5 em below the sediment surface. After a 10-minute
incubation, the top l-cm layer of sediment was sampled
(omitting the piece of either mimic or short shoot that occurred in the layer). The reaction was then stopped by placement of the sample in a solution of chloroform and methanol (1: 2). In the laboratory, the samples were analyzed
for the incorporation of acetate into bacterial phospholipid
(as a measure of growth (White et al. 1979)) and into the
bacterial storage polymers beta-hydroxyalkanoates
(as a
measure of stored as opposed to anabolized carbon (Findlay and White 1983)). The top l-cm layer was taken from
the small core and placed in chloroform: methanol (1: 2)
and transported to the laboratory for the determination
of muramic acid as a measure of bacterial standing stock
(Findlay et al. 1983). Eight blocks were sampled, but because of field and laboratory losses only 5 could be analyzed
for acetate uptake.
In our use of the analysis of variance, we examined
plots of the residuals between observed and estimated
values for evidence of violations of the assumptions of the
ANOV A model. We were able to transform successfully
all data sets that were initially in violation. The a posteriori
Newman-Keuls procedure (Hicks 1973) was used. In all
tests, the 95% experiment-wise significance level was used.
Results
The results of the first experiment confirmed the pattern
that had appeared in the preliminary data. That is, we ana-
297
Table 1. The per-core abundance
treatments
of harpacticoid
copepods in the
Block
Short shoot
Mimic
Control
1
2
3
4
5
6
7
8
54
69
47
59
64
72
43
34
84
53
36
49
59
45
41
37
47
25
43
35
41
30
16
23
Mean
55.25
50.5
32.5
Table 2. The concentration of muramic acid (nanomoles per gram
dry weight of sediment) in the treatments
Block
Short shoot
Mimic
1
8
5.24
12.84
10.37
27.14
13.67
20.14
6.12
12.26
10.56
9.84
8.05
21.54
24.38
10.05
6.32
10.52
3.13
9.32
6.67
10.23
3.83
8.05
4.62
8.90
Mean
1348
12.66
6.84
2
3
4
5
6
7
Table 3. The ratio of 14C-acetate incorporation
to its incorporation into beta-hydroxyalkanoates
Block
1
·2
3
4
5
Mean
Control
into phospholipid
Short shoot
Mimic
Control
0.49
0.38
0.31
0.34
0.40
0.46
0.48
0.62
0.30
0.56
0.31
0.32
0.19
0.25
0.32
0.38
0.48
0.28
Iyzed total harpacticoid abundance in 8 blocks of three
treatments (plant, mimic, control) (Table 1) using a randomized-blocks, two-way analysis of variance (Sokal and
Rohlf 1969), with treatments fixed and blocks random.
There was a significant main effect. The a posteriori test
revealed that plant and mimic means differed significantly
from control means but did not differ significantly from
each other.
The abundances of the 21 harpacticoid species found
were sufficiently low that we used the nonparametric analog
of the randomized-block analysis of variance, the Friedman
analysis of variance by ranks, and the distribution-free multiple comparisons test based on it (Hollander and Wolfe
1973) to test for differences among treatments at the level
of harpacticoid species. The treatments could not be shown
to differ for any species even at a single-test alpha level
of 0.05. However, species abundances among treatments
tended to parallel the pattern found for total harpacticoid
abundance. To investigate this possibility, we treated species as replicates (Jumars 1975) asking if those that were
reasonably abundant (mean per-core abundance > 1.0)
tended to be more abundant in both plant and mimic sarn-
pies than in the control samples when the abundance of
each species was summed over blocks. Of the 10 species
that were abundant enough to consider, 9 showed this pattern. This result is unlikely to have occurred by chance
(exact two-tailed binomial probability=0.02).
The second experiment tested for differences in the bacterial community around isolated short shoots, mimics, and
controls. The biomass (muramic-acid) data are given in Table 2). The analysis of variance revealed a significant main
effect. The a posteriori test showed that muramic-acid levels
near short shoots and mimics differed from those around
controls but not from each other.
We also investigated bacterial metabolic status. Findlay
and White (in preparation) have shown that the metabolic
status of bacterial communities can be assessed by examining the ratio of carbon incorporated into cell membrane
(phospholipid) to carbon incorporated into storage polymers (beta-hydroxyalkanoates).
When cells have carbon
available but are stressed because other materials are in
short supply (e.g., inorganic nutrients and terminal electron
acceptors), storage polymers accumulate; this condition is
described as unbalanced growth, i.e., the accumulation of
cellular carbon without the corresponding increase in cell
numbers. When the stress is relieved, balanced growth can
resume and the population grows rapidly (Nickels et al.
.1979). In our data (Table 3), short-shoot means and mimic
means did not differ significantly from each other but did
differ significantly from the control mean. The direction
of the difference was toward the production of cell membrane and away from production of storage polymers.
Discussion
The results of the comparison of short-shoot and control
treatments in the first experiment confirmed our expectations based on the preliminary data; harpacticoids were
more abundant around isolated short shoots than in unvegetated sediment at a comparable distance from the body
of the sea grass bed. On the average, the abundances in
control samples were 59% of those in short-shoot samples
(Table 1). The response cannot be attributed to a dramatic
concentration of individuals of one or a few species about
the short shoots. Rather, it appears to be a general tendency
of all the abundant species.
The natural history of this association suggested several
potential causes. Harpacticoid copepods are small (approximately 1 mm in body length), mobile crustaceans that feed
on microbes (Hicks and Coull 1983, and contained references). In the laboratory, they move into sediments rich
in their food organisms and away from food-poor sediments (Gray 1968; Ravenel and Thistle 1981), suggesting
that local concentrations of harpacticoids could arise in
nature from patchiness in the distribution of microbes
(Gray 1968). Seagrasses excrete dissolved organic carbon
(penhale and Smith 1977) that sedimentary bacteria are
capable of utilizing (Moriarty and Pollard 1982). If sea grass
exudates enhance the local food available to harpacticoids,
the vicinity of a short shoot could be relatively attractive
to harpacticoids.
Microbial abundances could be elevated around isolated
short shoots for a different reason. Eckman and Nowell
(in press) report that structures comparable to isolated
short shoots interact with the near-bottom flow. One consequence is the local thinning of the layer of viscous fluid
298
at the sediment surface, allowing better exchange across
the interface (Jumars and Nowell 1984). The improved exchange could stimulate microbial growth (and attract harpacticoids) in a variety of ways. In particular, it could improve the rate of supply of oxygen which tends to be depleted in sediments (Revsbech et al. 1980; Revsbech et at
1983), thereby stimulating aerobic bacterial growth.
Harpacticoid dispersion patterns are not likely to arise
from interspecific competition given the size of harpacticoids and their trophic position (Dayton and Hessler 1972;
Hicks and Coull 1983) or from modest differences in granulometry (Gray 1968; Ravenel and Thistle 1981), but patterns may be caused by predators in the way that abundances of several macroinfaunal species have been shown
to be enhanced around the large, robust tubes formed by
the polychaete Diopatra cuprea (Woodin 1978, 1981). For
harpacticoids generally, juvenile fishes are potent predators
(Feller and Kaczynski 1975; Sibert et al. 1977; Sheridan
1979). In north-Florida seagrass meadows, harpacticoids
are heavily preyed upon by fishes (Stoner 1980). If fishes
were less likely to feed on sediment near a short shoot
than on unvegetated sediment, then one would expect the
enhanced abundances observed.
In our experiments, we sought to determine the relative
importance of these several potential contributors to enhanced harpacticoid abundances around short shoots. In
the first experiment, the mean number of harpacticoids did
not differ between short shoots and non-living mimics. We
take this result to mean that the effect is caused by the
short shoot as a structure, not as a living entity, and that
stimulation of microbes by plant exudates is not important
to the effect.
The remaining hypotheses are a flow-induced effect and
a predation-refuge effect. Cages cannot be used to distinguish these alternatives because cages alter near-bottom
water motion (Virnstein 1977; Eckman 1979; Dayton and
Oliver 1980; Hulberg and Oliver 1980). We have used an
asymmetry in the predictions of the two hypotheses to begin
to distinguish between them. The flow hypothesis predicts
that the microbial food resource of harpacticoids should
be more favorable around plants and mimics than in control
areas, whereas the refuge hypothesis predicts no such difference.
The results of the second experiment show that the vicinities of both plants and mimics are areas of enhanced
bacterial standing stocks and that the metabolic state of
the bacteria differs among the treatments. In the controls,
incorporation into carbon stores dominates; around short
shoots and mimics, incorporation into cell membrane is
relatively enhanced. This pattern is that expected if the enhanced fluid shear around short shoots and mimics were
thinning the viscous sublayer and improving exchange.
It seems clear from these results that bacterial growth
is enhanced around short shoots. Given the attraction of
harpacticoids to their bacterial food (Gray 1968; Ravenel
and Thistle 1981), it is plausible that their concentration
about short shoots is caused in this way. However, we
recognize that the predation-refuge hypothesis is not refuted by these data and may also participate in the effect.
Two secondary hypotheses also require discussion.
First, the above-ground portion of the mimics acquired an
organic coating during their conditioning that appeared to
be similar to that covering short shoots. Any exuded materials could have affected both short-shoot and mimic treat-
ments, in particular, causing the observed increase in bacteria abundance. Second, if predation on harpacticoids were
reduced in the immediate vicinity of a short shoot, then
the enhanced harpacticoid abundances observed would be
expected. The implied increase in harpacticoid feeding
could stimulate microbial growth as has been shown for
other predators on microbes (Hargrave 1970; Morrison and
White 1980). However, flume experiments have shown that
unfouled tubes similiar to ours caused local increases in
sedimentary microbial abundances in a system where no
metazoans were present (Eckman 1984). Apparently, neither fouling nor harpacticoid predation need be invoked
to explain the enhanced bacterial standing stocks we observed.
We conclude that the presence of a structure creates
favorable conditions for microbial growth. Given the information about fluid-dynamic effects near structures, we suspect that these phenomena, via their effects on the bacteria,
drive the localization of harpacticoid abundance around
isolated short shoots.
Finally, relatively isolated, cylindrical structures comparable to seagrass short shoots are not rare in the sea bed.
Many polychaete tubes and foraminiferan tests are in this
size range (1-2 mrn diameter) and extend into the nearbottom water (Thistle 1979; DeLaca et al. 1980; Carey
1983), and the same flow patterns can be expected to occur
around them as around short shoots. We predict that the
supply of bacteria near these structures will be enhanced
and that these locations will be favored by bacteria consumers. For example, this effect could explain the attractiveness of small tubes to macrofaunal larvae observed by
Gallagher et al. (1983). In fact, the effect may be even more
widespread. That is, modest increases in the diameter of
a structure should not greatly alter the flow pattern (Eckman and Nowell, in press), so organisms the size of the
Diopatra cuprea that Woodin (1978, 1981) studied, for example, may also have these effects associated with them.
Acknowledgements. We are grateful for the assistance of these individuals: M. Butterworth, E. Gregor, K. Sherman, M. Trexler. The
work was improved by discussions with D. Meeter and K. Sherman. The following criticized the manuscript: K. Cannan, F.
Dobbs, J. Guckert, P. Jumars, R. Iverson, A. Nowell, K. Sherman,
A. Thistle. We thank these individuals for their kind help. Florida
State University provided the computer resources. The work was
supported by Office of Naval Research contract N00014-82-C0404. This paper is contribution 1005 of the Florida State University Marine Laboratory.
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Received February 28, 1984