Estuaries
Vol. 25, No. 5, p. 1033–1044
October 2002
Impact of Habitat Edges on Density and Secondary Production of
Seagrass-associated Fauna
PAUL A. X. BOLOGNA* and KENNETH L. HECK, JR.
University of South Alabama, Department of Marine Sciences, Dauphin Island Sea Lab, 101
Bienville Boulevard, Dauphin Island, Alabama 36528
ABSTRACT: Species richness and abundance of seagrass-associated fauna are often positively correlated with seagrass
biomass and structural complexity of the habitat. We found that while shoot density and plant biomass were greater in
interior portions of turtle grass (Thalassia testudinum) beds than at edges, mean faunal density was significantly greater
at edges than interior sites during 1994. This pattern was also observed in 1995, although differences were not significant.
The four numerically dominant taxonomic groups showed varying degrees of elevated densities at edges of T. testudinum
beds. Peracarids and polychaetes had significantly greater densities at edges of T. testudinum beds, while both decapods
and gastropods showed dramatic temporal variability in density, with reversals in density between edge and interior
occurring during the course of the study. This within-habitat variability in abundance may reflect both active accumulation
of fauna at edges and settlement shadows for species with pelagic larvae. Active accumulation of highly mobile taxa
seeking refuge in seagrass beds may explain the differences in density between edge and interior of T. testudinum patches
for peracarids in 1994 and in 1995. Active accumulation at edges may also explain differences in density for some
decapod taxa. Changes in gastropod densities between habitats may reflect larval settlement patterns. Results showed a
distinct settlement shadow for the gastropod Caecum nitidum whose densities (primarily second stage protoconch) increased by more than an order of magnitude in 1994. Settlement shadows and post-settlement processes may also explain
density differences of polychaetes between the edge and interior of T. testudinum patches. The differences in faunal
densities between edge and interior habitat resulted in habitat specific differences in secondary production among the
major taxonomic groups. On four of five dates in 1994 and in 1995, secondary production was greater at edge than
interior locations. These unexpected results suggest that differences in faunal densities and secondary production between edges and interiors of seagrass patches represent a potentially vital link in seagrass trophic dynamics. If this
elevated secondary production leads to increases in trophic transfer, then edges may serve as a significant trophic conduit
to higher-level consumers in this system.
insects (Didham et al. 1996). Proximity to an interface may determine the degree to which edge
effects affect associated organisms (Holling 1992;
Donovan et al. 1997).
In aquatic communities, macrophytes can have
dramatic effects on the physical environment (see
Koehl 1986). Seagrass structure is important in
dampening wave energy and deflecting and slowing water flow (Fonseca et al. 1982; Gambi et al.
1990). These effects have both geological and biological impacts. The reduction of flow associated
with grass beds increases particle deposition (Almasi et al. 1987) and the extensive root-rhizome
mat stabilizes the sediments (Thayer et al. 1984;
Fonseca and Fisher 1986). Seagrass beds act as sediment traps and often contain finer sediments than
unvegetated regions (Orth 1977). Initial reduction
in flow at edges allows large particles to settle while
finer particles are carried into the bed. When flow
is substantially reduced, the concentration of fine
particles will increase in the interior of grass beds
(Fonseca et al. 1982; Ackerman and Okubo 1993).
Since many marine larvae are small and possess
poor swimming capabilities ( Jonsson et al. 1991),
Introduction
Plant communities are frequently subjected to
disturbance events that alter the coverage, species
composition, biomass and functional characteristics of the community (Sousa 1979; White 1987;
Holling 1992; Kruess and Tscharntke 1994). As a
result, many plant communities are mosaics of habitat patches varying in shape and size (Forman and
Godron 1981; Holt et al. 1995). The interface between two different habitats (e.g., forest-meadow,
seagrass-sand flat) can produce dramatic impacts
on both physical and biological processes. In terrestrial systems, vegetation areal extent and interface between differing habitats have been shown
to affect the physical environment (e.g., wind, precipitation, light), faunal species composition (Nilsson 1986), predation and foraging success (Donovan et al. 1997), and reproduction of plants and
* Corresponding author; current address: Fairleigh Dickinson
University, Department of Biological and Allied Health Sciences, 285 Madison Avenue, M-EC1-01, Madison, New Jersey 07940;
tele: 973/443-8758; fax: 973/443-8766; e-mail: bologna@fdu.
edu.
Q 2002 Estuarine Research Federation
1033
1034
P. A. X. Bologna and K. L. Heck, Jr.
they may behave as passive particles (Butman 1987;
Eckman 1990), and just as grass beds are sediment
traps, they may also be traps for species whose larvae act as passive particles (see Orth 1992; Bologna
and Heck 2000).
Seagrass beds are often a mosaic of vegetation
interspersed with bare substrata (see Larkum and
den Hartog 1989; Robbins and Bell 1994; Marba
and Duarte 1995). The succession of these habitat
mosaics creates assemblages with variable shoot
density, seagrass species composition, canopy
height and biomass (Bell and Westoby 1986; Irlandi 1994). Supplemental structures associated with
seagrasses (e.g., macroalgae, corals, colonial bryozoans, bivalves) and epiphytes can also create complex and distinct habitat types (Stoner and Lewis
1985; Valentine and Heck 1993; Bell et al. 1995).
Many studies have investigated faunal distributions in seagrass beds and included comparisons
between vegetated and unvegetated habitats (Virnstein et al. 1983; Edgar and Shaw 1995; Heck et al.
1995), among seagrass species (Lewis 1984; Worthington et al. 1992), among other habitats (e.g.,
coral reefs, mangroves, macroalgae; Sheridan
1997), and with and without supplemental structure (e.g., macroalgae; Stoner and Lewis 1985).
Little information exists on within-habitat distributions of seagrass-associated fauna. Several predictions about the spatial distribution of plants and
animals within seagrass habitats can be made,
based on variation in spatial complexity (e.g., Stoner and Lewis 1985). Biomass, shoot density, and
leaf length should be greater in interior portions
of beds than near edges (Marba and Duarte 1995).
If faunal abundances are positively correlated with
plant biomass (Heck and Orth 1980) and shoot
density (Homziak et al. 1982), then faunal density
should reflect differences in seagrass habitat structural complexity. If faunal distribution is set at a
larval recruitment phase, then the distribution of
organisms that produce pelagic larvae may reflect
settling patterns and depositional forces (Bell and
Westoby 1986; Bertness et al. 1992; Minchinton
1997; Pineda and Caswell 1997). Lastly, size distribution of organisms within habitats may be independent of habitat characteristics (Virnstein et al.
1984) or may reflect competitive interactions between size classes and species (Edgar 1990b).
We examined the species composition and abundance of animals at edge and interior portions of
turtle grass beds (Thalassia testudinum), and asked
whether edges and interiors differed with respect
to plant biomass, shoot density and leaf morphology and then, after controlling for vegetation effects, examined the distributional response of associated fauna. Secondary production was also investigated between edge and interior portions of
T. testudinum patches to determine whether potential differences in faunal density lead to significant
differences in secondary production, which may in
turn impact trophic transfer in seagrass systems.
Materials and Methods
STUDY SITE
Research was conducted in St. Joseph Bay, Florida, in the Northeastern Gulf of Mexico (298N,
85.58W). Salinities in St. Joseph Bay range seasonally from 22‰ to 35‰ and temperatures from
8.58C to 328C (Bologna 1998). Extensive seagrass
meadows occupy the shallows (, 2 m). The meadows are comprised of turtle grass (Thalassia testudinum), shoal grass (Halodule wrightii), and manatee grass (Syringodium filiforme). Turtlegrass is the
dominant species and covers approximately 2,300–
2,400 hectares in St. Joseph Bay (Savastano et al.
1984; Iverson and Bittaker 1986). Research was
conducted in an extensive, shallow sand–T. testudinum habitat mosaic (depth , 1.2 m mean low
water).
WATER DEPTH AND CANOPY HEIGHT
In September, coincident with the water flow experiment described below, canopy height and water depth were measured to the nearest cm within
the T. testudinum habitat. Nine measurements were
collected at randomly located spots along the edge
at 0.5 m distance into the bed from the interior at
distances ranging from 16–22 m from the interface
(x̄ 5 18.5 m), and from adjacent unvegetated regions. Water depth varied significantly among habitats (F2,24 5 12.3, p , 0.0002). Unvegetated regions adjacent to the T. testudinum (mean water
depth 6 SD 5 1.15 m 6 0.16) were significantly
deeper than both edge (0.97 m 6 0.09) and interior (0.88 m 6 0.08) portions of the bed. Edge
water depth did not differ significantly from interior depth. In September, canopy height was greater at interior sites (mean 6 SD 5 36.3 cm 6 3.6)
than at edges (20.3 cm 6 1.6; t16 5 12.2, p ,
0.0001).
SEAGRASS STRUCTURAL HABITAT CHARACTERISTICS
Three 15.24-cm diameter cores were taken
monthly from June to September to assess plant
morphological patterns characteristic of edges and
interiors of T. testudinum habitat (n 5 24). Edges
were defined as in vegetated substrates 1 m inside
the sand-grass interface. Due to the mosaic nature
of the grass beds in the study area, interior portions of the beds were defined as locations within
continuous T. testudinum that were at least 10 m
from any sand-grass interface. Core samples were
collected to a depth of 25 cm at randomly selected
sample locations meeting the criteria of the de-
Seagrass Edge Effects
fined habitats. Individual samples were processed
in the field by separating all live T. testudinum from
the sediment. Core samples were then frozen and
returned to the laboratory.
In the laboratory, plants were divided into shoots
(i.e., aboveground), rhizomes, and roots. All
leaves, regardless of age, were separated out and
the first 25 encountered measured for leaf length
and leaf width to the nearest mm. All leaves were
measured if fewer than 25 were processed in a
core. New shoots emerging from rhizomes were
not included in leaf length and width measurements, however they were counted to determine
shoot density. Shoots, rhizomes and roots were
dried to constant weight at 808C (approximately 7
days) and ashed at 5008C for 8–10 hours (complete
rhizome burn often required 10 hours). Biomass
was then calculated as the difference between dry
weight and ashed weight (ash free dry weight;
AFDW). Data were analyzed using two-way ANOVA
with habitat (edge or interior) and month of collection as independent variables and plant biomass, leaf length, and leaf width as separate dependent variables. Significance level was set at a 5
0.05. Shoot density was analyzed in the same manner, but data were square-root transformed before
analysis because they failed the homogeneity of
variance test. Least-squares means contrasts were
used to determine significant differences among
dates.
FLOW REGIME
In September, relative water flow was estimated
by calculating the dissolution rate of plaster of Paris cylinders (cf., Komatsu and Kawai 1992). This
technique assumes that the dissolution of plaster
of paris is directly related to water velocity. Water
flow was measured because larval recruitment to
seagrass systems was assumed to be a potentially
important process dictating faunal community
structure. Cylinders were made by mixing 100 g of
plaster with 90 ml of distilled water. This combination resulted in a mixture that could be easily
poured into 2.5 3 5.3 cm numbered, cylindrical
containers. Plaster was poured into the containers,
allowed to set and dry, sanded flush with the surface of the cylinder and re-dried to constant weight
at 608C (approximately 5 weeks). These cylinders
minimized abrasion with sediments and grass
blades because the hard plastic cylinder surrounding the plaster limited contact between the dissolving plaster and the environment. This technique
also allowed us to estimate relative flow at a precise
height above the sediment-water interface. Three
replicate cylinders were transported to the field
and placed in the interior of T. testudinum beds, at
the edge of beds and in open sand (see canopy
1035
Fig. 1. Schematic representation of flow regime experiment.
A. Dimensions of the cylindrical container in which plaster of
Paris was poured. B. Height designation bars used in experiment. C. Schematic field layout of flow regime experiment. Representative dissolution height replicates depicted for each habitat.
height and water depth in site description). Individual cylinders were randomly deployed in the water column at heights of 10, 20, 40, 60, and 80 cm
above the sediment-water interface in each habitat
(Fig. 1). Cylinders were placed in 2.54 cm PVC
pipe couplings and then set on 2.54 cm PVC pipes
at the desired heights. Individual cylinder assemblages were randomly deployed in each habitat
with a minimum distance of 35 cm from any adjacent cylinder assemblage. All cylinders were
deployed in the field on 12 September between
12:33–13:11 h and deployment time was measured
to the nearest minute. Cylinders were retrieved on
13 September between 10:26–10:51 h. They were
then rinsed in distilled water, and dried at 608C
constant weight. Dissolution rates (g d21) were calculated for each cylinder and log-log regressions
of height above sediments to dissolution rate were
calculated for each habitat. A least-squares means
F-test was used to compare regression slopes
among habitats (a 5 0.05) and a Tukey-Kramer
minimum significant difference (a 5 0.05) was
used to compare differences among the y-intercepts (Sokal and Rohlf 1981).
FAUNAL SAMPLING
Faunal samples were collected from T. testudinum
grass beds on July 13, 20, 27, August 25, and September 3, 1994 and on August 30, 1995. Three replicates were taken at edge and interior locations
within the T. testudinum habitat in 1994 and four
replicates were collected in 1995. Samples were
1036
P. A. X. Bologna and K. L. Heck, Jr.
collected by randomly selecting a site which met
the criteria of edge and interior described above,
and then haphazardly placing a PVC cylinder 1.2
m high and 0.073 m2 in area (15.24 cm radius), in
each of the habitats. The cylinder was then
pumped dry using a gasoline-powered suction
dredge (cf., Orth and van Montfrans 1987). This
process removed epifauna, surficial benthic organisms (e.g., Gastropoda), and small quantities of
sediment. Samples were sieved to retain organisms
. 500 mm, preserved in 10% formalin and stored
in 70% isopropanol. Organisms were identified to
lowest possible taxa and enumerated. Only taxa determined to be either epifaunal and living surficially among the sediments (e.g., Nereidae, Phoxocephalidae, Hausteridae) were included in data
analyses. A full listing of all taxa identified and
their densities occurs in Bologna (1998).
Identified taxonomic groups (e.g., Order: Amphipoda, Family: Aoridae; Order: Gastropoda, Mitrella lunata) were grouped, dried to constant
weight at 808C (; 48–96 hours), ashed at 5008C
for 8 hours and then re-weighed to determine ash
free dry weight (AFDW). Total faunal density and
biomass, as well as identified taxonomic groups,
were analyzed using a 2-way ANOVA with habitat
(edge vs. interior) and date as independent variables for 1994 (n 5 28, two samples from July 20
were preserved improperly and were not used in
analysis) and as an unpaired t-test between habitats
for 1995 samples (n 5 8). Abundances were
square-root transformed before analysis to eliminate heteroscedacity. Significance level for all analyses was considered at a 5 0.05 and Scheffe’s Ftest was used for comparisons among means for
dates in 1994.
SECONDARY PRODUCTION
Daily production (mg m22 d21) was calculated using the regression relationships between biomass
(mg AFDW) and temperature outlined in Edgar
(1990a) for the four numerically dominant taxa in
samples: peracarids, decapods, gastropods, and
polychaetes. The following equations from Edgar
(1990a) were used to estimate daily production:
P 5 22.86 1 0.81·(log B) 1 1.32·(log T);
Crustaceans (Eq. 6)
P 5 22.18 1 0.87·(log B) 1 0.46·(log T);
Mollusca, Gastropoda (Eq. 7)
P 5 21.99 1 0.79·(log B) 1 0.69·(log T);
Polychaetes (Eq. 4, general epifauna)
where, P 5 daily production (mg AFDW d21); B 5
Fig. 2. Monthly plant biomass (g ash free dry weight
[AFDW] m22) distribution of Thalassia testudinum at edge (E)
and interior (I) portions of the bed. Open bars represent leaf
and shoot biomass (aboveground biomass), hatched bars represent rhizome biomass and solid bars represent root biomass
(n 5 6 for each month). Rhizome and root comprise belowground biomass.
mean biomass (mg AFDW); and T 5 temperature
(8C).
Regression equations for crustaceans and molluscs were used directly from Edgar (1990a), but
since a specific equation for polychaetes was not
available, we used the general epifauna equation.
Temperatures used in regression equations were
field collected values: 28.78C (7/13/94), 29.98C
(7/20/94), 29.58C (7/27/94), 28.18C (8/25/94),
28.48C (9/3/94) and 30.08C (8/30/95). Production was compared between habitats and among
dates using 2-way ANOVA in 1994 with habitat and
date as independent variables and production as
the dependent variable, and an unpaired t-test between habitats in 1995. Significance level for all
analyses was considered at a 5 0.05 and Scheffe’s
F-test was used for comparisons among means for
dates in 1994.
Results
SEAGRASS STRUCTURAL HABITAT CHARACTERISTICS
When seagrass biomass was compared between
edge (within 1 m) and interior (. 10 m) portions
of T. testudinum patches, samples from the interior
showed significantly greater leaf (F1,16 5 27.7; p ,
0.0001), rhizome (F1,16 5 6.6; p , 0.02), and root
biomass (F1,16 5 73.4; p , 0.0001; Fig. 2). Although
biomass peaked in August, no statistically significant differences in biomass occurred among dates,
nor were there any significant interactions. Comparison of shoot density data usually showed greater mean densities from interior portions of T. testudinum patches (Table 1), but high shoot density
1037
Seagrass Edge Effects
TABLE 1. Monthly differences in Thalassia testudinum shoot density and leaf morphology from samples collected from edge and
interior portions of beds. Values represent mean and one standard deviation for measured parameters. Shoot density is presented as
number m22. Leaf length and width are expressed in cm. * denotes significant differences in leaf morphology between edge and
interior habitats. (†) columns denote significant differences among dates for leaf length and width, differing letters indicate significant
differences in means.
Shoot Density
Edge
June
July
August
September
141.5
146.1
301.4
196.3
6
6
6
6
55.4
7.9
68.5
127.3
Leaf Length (***)
Interior
228.3
191.8
283.1
269.4
6
6
6
6
131.6
49.4
41.9
96.2
Edge
10.1
12.4
14.8
15.5
6
6
6
6
(†)
1.5
1.4
1.2
1.4
in August edge samples prevented significant differences (F1,16 5 2.3; p . 0.15). These August edge
results appear to represent an expanding grass bed
with numerous young shoots colonizing unvegetated substrate (Bologna personal observation). Samples from interior portions of the bed showed significantly greater leaf length (F1,16 5 22.0; p ,
0.0002) and leaf width (F1,16 5 53.1; p , 0.0001)
than samples collected at edges (Table 1). Leaf
morphology showed significant seasonal variability
in both leaf length (F3,16 5 7.5; p , 0.002) and leaf
width (F3,16 5 7.6; p , 0.002) with maxima occurring in August and September (Table 1).
FLOW REGIME
Results from regression analysis of height above
sediments to dissolution rates (Fig. 3) indicate that
basal dissolution rates for plaster cylinders did not
Fig. 3. Log-Log regression analysis of dissolution rate (g dry
weight day21) versus height above sediments (cm) for plaster of
Paris cylinders. The solid line represents data collected from
unvegetated regions and is denoted by Sand. The hatched line
represents data collected from the edge (0.5 m) of continuous
Thalassia testudinum and is denoted by Edge, while the dashed
line, Interior, refers to data collected from interior portions of
T. testudinum. Regression equations for independent lines follow
their designation.
b
b
a
ab
Leaf Width (***)
Interior
16.1
15.1
22.0
16.3
6
6
6
6
4.0
2.0
2.9
0.6
Edge
(†)
6
6
6
6
b
b
ab
a
0.67
0.64
0.84
0.89
0.08
0.11
0.06
0.02
Interior
1.02
0.92
0.94
1.10
6
6
6
6
0.10
0.06
0.05
0.12
vary among habitats (i.e., y-intercepts not different;
p . 0.05). Dissolution rates increased as height
above sediment increased, and slopes of the regressions were significantly different. Using a least
squares means F-test, the slope for the grass bed
was significantly greater than that for the sand
(F1,14 5 10.7; p , 0.02), but not different from the
edge (F 5 2.16; p . 0.15). Comparison of the
slopes for edge versus sand indicates no significant
difference (F 5 3.24; p 5 0.08), suggesting that
edges represent a transitional state between unvegetated habitats and interior T. testudinum beds.
FAUNAL COMMUNITY RESPONSE
A total of 196 taxa, representing 13 phyla, was
identified from the samples collected. A full listing
of the taxa and their densities within habitats appears in Bologna (1998). In 1994, samples collected at edges of T. testudinum patches had significantly greater total faunal density than samples collected in interior portions of the bed (Table 2; Fig.
4). A significant interaction occurred between date
and habitat due to a 27 July peak in density of
combined taxa in the interior of the seagrass bed
(Table 2; Fig. 4). A significant date response occurred in the analysis due to the recruitment of
small gastropods in September 1994 samples (Table 2; see Figs. 4 and 8). These results are important in assessing faunal temporal variability and potentially determining recruitment events. Similar
patterns were found in the August 1995 data, with
greater densities at the edge, although differences
were not significant (t6 5 1.23; p 5 0.26). Although it is apparent that total faunal density in
TABLE 2. ANOVA results for total faunal density between edge
and interior portions of T. testudinum (Habitat) and among
dates of collection for 1994.
Source
df
Sum of
Squares
Mean Square
F-test
p
Habitat (A)
Date (B)
A*B
Error
1
4
4
18
52,103,294
100,016,484
75,964,486
111,970,350
52,103,294
25,041,171
18,991,121
6,220,575
8.4
4.0
3.1
0.01
0.02
0.04
1038
P. A. X. Bologna and K. L. Heck, Jr.
Fig. 4. Total faunal density (number of individuals m22 6
one standard error (SE)) from edge (shaded bars) and interior
(open bars) portions of Thalassia testudinum for five sampling
dates in 1994 and one date in 1995. Shaded bars represent data
collected at edges and open bars for data collected from interior
portions of T. testudinum.
1994 was consistently greater at edge than in interior of T. testudinum beds, these differences in
density did not translate into significantly greater
total faunal biomass between edge and interior
sites (F1,18 5 0.5; p 5 0.47; Fig. 5). This was due to
the presence of large, but infrequent, sea urchins
(Lytechinus variegatus), which created tremendous
variability in mean biomass data. In 1995, mean
biomass was greater in interior portions than edges
(t6 5 0.67; p 5 0.53), primarily due to differences
in gastropod densities.
INDIVIDUAL TAXA
Peracarids
Fifteen amphipod families and six isopod families were identified from samples. Mysids, tanaids,
and cumaceans were identified to Order. In both
1994 and 1995, total peracarid density was greater
at edges of T. testudinum than at interior sites (Fig.
6). These differences were significant in 1994 (F1,18
5 10.3; p , 0.005), but not in 1995 (t6 5 1.04; p
. 0.33). In 1994 densities were significantly greater during the three samples gathered in July compared to those from August and September based
on Scheffe’s F-test among means (Fig. 6; F4,18 5
6.6; p , 0.002). This decrease in density corresponded with reductions in salinity in St. Joseph
Bay, Florida during 1994 created by rainfall from
Tropical Storm Alberto (see Bologna 1998).
Amphipod densities were greater at edges in
1994, resulting from significantly greater densities
of aorids (F1,18 5 7.8; p , 0.01) and Cymadusa spp.
(Amphithoidae) (F 5 11.4; p , 0.003). Just as the
peracarids showed significant date effects, so did
Fig. 5. Mean total biomass (g AFDW m22) from edge (shaded bars) and interior (open bars) portions of Thalassia testudinum for five sampling dates in 1994 and one date in 1995.
the aorids (F4,18 5 9.8; p , 0.0002), melitids (F 5
5.3; p , 0.005), pleustids (F 5 4.3; p , 0.02) and
Cymadusa (F 5 4.8; p , 0.01). All three groups
showed significant density reductions in August
and September compared to July. Cymadusa
showed a significant increase in August for edge
samples compared to other dates, but was virtually
absent from samples in September, thus creating a
significant date by habitat interaction (F4,18 5 4.2;
p , 0.02). Some amphipod families showed no significant difference in densities between edges and
interior portions of T. testudinum patches, but all
families showed higher densities at edges (see Bologna 1998). In 1995 amphipod density was greater
at edges, albeit not statistically significant (t6 5 1.19;
Fig. 6. Peracarid density (number of individuals m22 6 one
standard error (SE)) from edge (shaded bars) and interior
(open bars) portions of Thalassia testudinum for five sampling
dates in 1994 and one date in 1995.
Seagrass Edge Effects
1039
Fig. 7. Decapod density (number of individuals m22) from
edge (shaded bars) and interior (open bars) portions of Thalassia testudinum patches for five sampling dates in 1994 and one
date in 1995.
Fig. 8. Gastropod density (number of individuals m22) from
edge (shaded bars) and interior (open bars) portions of Thalassia testudinum patches for five sampling dates in 1994 and one
date in 1995.
p 5 0.28), but melitids did show significantly higher
densities at edges than interiors (t6 5 3.44; p ,
0.014).
Because size-based competitive interactions
among amphipods have been reported in the literature (Edgar 1990b), amphipod distributions
were investigated further by assessing the density
of two size classes: large (. 1 mm) and small (,
1 mm). Densities of both large and small amphipods were greater at edge than interior in 1994
(F1,18 5 11.9; p , 0.003; F 5 9.9; p , 0.006, respectively) and in 1995 (t6 5 0.65; p 5 0.54; t 5
1.12; p 5 0.3, respectively).
edge, while xanthid density was greater at interior
sites, although neither showed significant differences between habitats. Hermit crabs showed reversing density patterns within habitats in 1994
with higher densities at edges early in July and
higher densities at interior sites on other dates,
while density was greater at edges in 1995.
Decapods
Penaeids, carideans, and hermit crabs were identified to sub-Order, while the remaining decapod
groups were identified to Family. Decapods showed
no difference in density between edge and interior
for both 1994 (F1,18 5 0.29; p 5 0.6) and 1995 (t6
5 0.41; p 5 0.18; Fig. 7), but mean abundance was
greater in 1994 than 1995 (Fig. 7). In 1994, carideans, the most abundant taxa, showed no spatial
differences in density between edge and interior
(F1,18 5 0.26; p 5 0.6) but did show a significant
date effect (F4,18 5 6.3; p , 0.002). A Scheffe’s Ftest showed significantly fewer carideans in samples
from August compared to other dates in 1994, similar to the reduction in peracarid densities. Xanthid and majid crabs showed no significant density
differences between habitat (F1,18 5 0.03; p 5 0.87;
F 5 0.54; p 5 0.47, respectively) or among dates
(F4,18 5 1.9; p 5 0.15; F 5 2.3; p 5 0.1, respectively), but overall means densities were greater at
edges. In 1995, majids had greater densities at
Gastropods
Samples contained 110 identified gastropod species, 17 identified to Family or Genus and there
were three unidentified gastropods. In 1994, total
gastropod density was greater in the interior of T.
testudinum patches during July, but this pattern reversed in late summer with greater gastropod density at the edge of T. testudinum patches (Fig. 8).
As a consequence, ANOVA results showed both a
significant date effect (F4,18 5 12.7; p , 0.0001)
and a significant date by habitat interaction (F4,18
5 4.6; p , 0.01). These effects were the result of
a large recruitment event dominated by the genus
Caecum, whose densities increased by an order of
magnitude between initial sampling dates and September samples. There was a dominance of second
stage protoconch C. nitidum in September samples.
In 1995, a similar recruitment event did not occur,
and gastropod density was greater in interior portions of T. testudinum.
When the most abundant taxa were analyzed individually, Mitrella lunata and Crepidula spp. showed
significantly greater densities at edges in 1994 (F1,18
5 22.9; p , 0.0001; F1,18 5 5.9; p , 0.025, respectively). M. lunata also showed temporal variability
with significantly greater densities in August compared to other months (F4,18 5 13; p , 0.0001),
1040
P. A. X. Bologna and K. L. Heck, Jr.
Fig. 9. Polychaete density (number of individuals m22) from
edge (shaded bars) and interior (open bars) portions of Thalassia testudinum patches for five sampling dates in 1994 and one
date in 1995.
which also led to an interaction between date and
habitat (F4,18 5 4.3; p , 0.01). Other taxa either
did not have significantly different densities, or
had higher densities early in the summer in the
interior of T. testudinum patches and greater densities at edges in late summer. In 1995 samples,
only Phyllaplysia spp. had significantly greater densities at edges than interiors (t6 5 2.75; p , 0.034),
potentially relating to a July recruitment event (see
Bologna 1998). Caecum nitidum also showed higher
densities at edges, albeit not significantly (t6 5
0.78; p 5 0.463); while Marginella lavalleana, Caecum pulchellum and Crepidula spp. showed significantly greater densities from interior portions of T.
testudinum compared to edges (t6 5 2.48; p , 0.05;
t 5 3.11; p , 0.02; t 5 3.62; p , 0.01, respectively).
Polychaetes
There were 21 Families of polychaetes identified
from samples. In 1994, total polychaete density was
significantly greater at edges of T. testudinum (F1,18
5 10.4; p , 0.005; Fig. 9). Results were similar in
1995, but due to low sample size and high variability in the data, differences were not significant
(t6 5 1.04, p 5 0.34; see Fig. 9). When the three
most abundant families (Spionidae, Nereidae, and
Syllidae) were analyzed individually for 1994, results showed greater mean densities in interior portions of T. testudinum compared to edges (F1,18 5
1.4; p 5 0.25; F 5 0.1; p 5 0.74; F 5 1.2; p 5 0.29,
respectively). Combined effects of less abundant
families outweighed the distribution patterns of
the numerically dominant taxa. In 1995, only nereids showed similar results, with higher densities in
interior samples, while spionids and syllids showed
Fig. 10. Calculated secondary production (mg ash free dry
weight m22 d21) for amphipods (shaded bars), decapods (open
bars), gastropods (solid bars), and polychaetes (hatched bars).
Production values calculated using the equations of Edgar
(1990a).
greater densities from samples gathered at edges
of T. testudinum patches.
SECONDARY PRODUCTION
Estimated secondary production for each taxonomic group showed a direct correspondence with
faunal density (Fig. 10). Peracarid and polychaete
secondary production were greater at edge than
interior sites in both 1994 (F1,18 5 8.2; p , 0.01; F
5 5.3; p , 0.03, respectively) and 1995 (t6 5 0.5;
p 5 0.64; t6 5 2.2; p 5 0.07, respectively). Decapod
secondary production showed no clear patterns
(Fig. 10) although secondary production was very
high in early July 1994 at edges, but declined
throughout the summer. Secondary production
was opposite at interior sites, which showed increasing rates as the summer progressed. These
opposite secondary production patterns created a
significant interaction between habitat and date for
decapods (F4,18 5 3.05; p , 0.04). When decapod
data were analyzed for 1995, secondary production
was greater at edges (t6 5 0.83; p 5 0.44). Gastropod secondary production varied between habitats
and among dates in 1994 leading to no clear pattern in estimated secondary production (F1,18 5
0.11; p 5 0.74). Gastropod secondary production
in 1995 was significantly greater at interior sites
than at edges (t6 5 3.2; p , 0.02; Fig. 10), following density patterns (Fig. 8).
Discussion
Our results indicated that some taxa (e.g., amphipods and polychaetes) had significantly greater
densities at edges where seagrass biomass was sig-
Seagrass Edge Effects
nificantly reduced (Figs. 6 and 9). Our data were
contrary to a generalized pattern where animal
densities are higher in areas where seagrass biomass and structural complexity are greatest (Heck
and Orth 1980; Homziak et al. 1982). The reason
our results may differ from previous studies is because in these studies, samples were usually collected only from interior portions of extensive
beds (e.g., Heck and Orth 1980; Homziak et al.
1982; Stoner and Lewis 1985). Prior to our work,
few studies have assessed edge effects in seagrasses,
but research from salt marshes indicate extensive
differences in habitat use by fish and decapods between edge and interior portions of these habitats
(Baltz et al. 1993; Kneib and Wagner 1994), and
edges have been shown to be critical to trophic
transfer and food web dynamics in estuarine systems (Kneib and Wagner 1994; Minello et al.
1994).
The significantly greater peracarid secondary
production rates at edges (Fig. 10) may have significant impacts for trophic transfer in seagrass
communities. Peracarids are extremely important
food resources for both decapod and fish predators (Stoner 1982; Virnstein et al. 1983). Elevated
peracarid secondary production at edges, where
predation potential may be higher (because of
sparse vegetation relative to interior; see Orth et
al. 1984; Heck and Crowder 1991) may be an important feature of shallow water food webs.
Virnstein et al. (1984) suggested that the generalized pattern of increasing density of benthic
invertebrates with increasing plant biomass did not
hold for peracarids, and our results are consistent
with this. Virnstein et al. (1984) suggest that this
lack of positive correlation between seagrass biomass and associated fauna may indicate a complex
situation. Amphipods are known to be vulnerable
to predators in unvegetated habitats (Stoner 1982;
Virnstein et al. 1983). They also rapidly colonize
artificial seagrass substrates, often crossing expansive areas of unvegetated bottom (Virnstein and
Curran 1986; Bologna 1998; Bologna and Heck
1999). Many crustaceans show rapid turnover rates
within seagrass habitats (Howard 1985) and dramatic diel movement (Virnstein and Curran 1986;
Howard 1987; Sogard and Able 1994). When these
vulnerable organisms move among habitats, they
must seek refuge. Edges may accumulate mobile
organisms that are seeking refuge from predation
while traversing unvegetated bottoms. With the exception of sphaeromid isopods, other peracarid
taxa (principally Amphipoda) showed greater densities at edges of T. testudinum than interiors (Fig.
6). Amphipod distributions may reflect active selection of edges, as proposed by the nearest refuge
hypothesis of Virnstein and Curran (1986).
1041
Results for decapods showed a date effect for
1994, with significantly greater densities of decapods in July than in later samples. This was primarily due to the influx of small (, 1 mm) caridean shrimp that dominated samples in early July
(Bologna unpublished data). Decapod density was
greater at edges, which could reflect the arrival of
small caridean recruits (see below) and accumulation at edges as a nearest refuge. As the summer
progressed, caridean density decreased and decapod density distributions shifted toward higher
concentrations in the interior of T. testudinum, associated with higher plant biomass and shoot density. Changes over time in decapod secondary production (Fig. 10) suggest that high secondary production at edges in early July may have been transferred to larger consumers (sensu Virnstein et al.
1983), thus reducing densities. The edge may serve
as a significant avenue of trophic transfer for decapods as well as amphipods.
Larval recruitment also contributes to the differences in faunal densities we observed. Passively
transported larvae encountering structure settle or
are deposited and may become concentrated at
edges of permeable structures (Bologna and Heck
2000). As water moves into the grass bed, it becomes depleted in larvae and larval settlement is
reduced in the bed interior, relative to the edge
(see Orth 1992). Accelerated flow above the canopy may maintain larvae in the water column and
deposit them on leeward edges of grass beds, similar to solid structures (Snelgrove 1994). Passive
bedload transport of settled individuals may elevate densities of some taxa (Emerson and Grant
1991). Our results provide evidence for settlement
shadows for gastropods (Fig. 8). The presence of
high densities of second stage protoconch Caecum
nitidum clearly suggests elevated settling densities
and or differential post-settlement sur vival at
edges. Though we were unable to determine which
process caused the elevated densities at edges, a
clear settlement shadow was present. When the
mean dissolution rate of plaster cylinders was compared to height above sediments in sand and T.
testudinum, the steeper slopes associated with the
regressions for T. testudinum habitats indicate high
rates of change in flow velocity as depth decreases
in the canopy (Fig. 3). Flow rate was reduced, possibly creating favorable conditions for larval deposition at edges, and we surmise that larval deposition and passive bedload transport probably
caused accumulation at edges that may have partially determined gastropod distributions.
Differences in polychaete densities between the
edge and interior of T. testudinum patches (Fig. 9)
probably not only reflect differences in larval settlement and bedload transport, but also differen-
1042
P. A. X. Bologna and K. L. Heck, Jr.
tial survival. Summerson and Peterson (1984) suggested that predation was an organizing process
that regulated infaunal community structure. If
predation was the primary process organizing polychaete distributions, we might conclude that predation was higher at our interior sites, where polychaete density was significantly lower than elsewhere. This is unlikely, given that seagrass structure significantly reduces predation on infauna
(Summerson and Peterson 1984; Irlandi 1994) and
biomass and shoot density were greater at interior
sites (Table 1, Fig. 2). Our data showed that the
three most abundant families (Spionidae, Nereidae, and Syllidae) had greater mean densities in
interior portions of T. testudinum than edges, contrary to the overall pattern of greater polychaete
density at the edge. The distribution of individual
taxa within habitats may be a complex function of
larval delivery, differential survival and longer
term impacts of predation.
The elevated secondary production of polychaetes at edges (Fig. 10) suggests that they may
be an important trophic link in the food web of
seagrass systems, and quantifying these linkages
will substantially increase our understanding of
edges and their importance to food webs. Our data
indicate the significant role of gastropods in total
secondary production (6–54% total secondary production; Fig. 10). Gastropods were dominated by
small species which have often been overlooked in
samples from seagrass communities and ignored in
secondary production estimates (Robertson 1979;
Valentine and Heck 1993). Gastropod contributions to secondary production can be substantial
in seagrass habitat and should be studied further.
Our results clearly showed greater faunal densities , 1 m inside the T. testudinum sediment interface compared to that found at interior sites. For
some taxa (e.g., species with pelagic larval phases)
this relationship may reflect larval settlement; for
brooding species (e.g., peracarids), the greater faunal densities associated with edges must result
from different processes. We suggest that active accumulation of highly mobile taxa at edges may dictate these within habitat distributional patterns. Regardless of the process, the elevated faunal densities at edges lead to increases in secondary production there, with potentially important
implications for food web dynamics and trophic
transfer. Further research into the specific mechanisms determining these differences in density
and secondary production may elucidate the function of edges in marine environments.
ACKNOWLEDGMENTS
We would like to thank the many people that contributed to
the completion of this project including: Y. Gonzales, J. Harper,
G. Eisel, and S. Chavez. We would also like to thank John Valentine, Robert Orth, James Cowan, Robert Steneck, Pete Peterson, Mark Fonseca and an anonymous reviewer for critical evaluation of earlier drafts of this manuscript. This work was supported by grants from the Mississippi–Alabama SeaGrant Consortium (NA16RG0155) and a Lerner-Gray Fellowship from the
American Museum of Natural History and is contribution 338
of the Dauphin Island Sea Lab.
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Received for consideration, November 30, 1998
Accepted for publication, April 5, 2002