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We tested the relative effects of nutrient loading, reduced predation, and reduced grazing on eelgrass community dynamics in Chesapeake Bay and found evidence supporting the ‘‘mutualistic mesograzer model’’ in which small invertebrate grazers control accumulation of epiphytic algae, buffer eutrophication effects, and thus facilitate seagrass dominance. Experimental reduction of crustacean grazers in the field stimulated a nearly sixfold increase in epiphytic algae, and reduced seagrass biomass by 65% compared to controls with grazers. Nutrient fertilization generally had much weaker effects, but an interaction with mesograzers was key in changing the sign of fertilization effects on the system: aboveground eelgrass biomass was reduced by fertilization under reduced grazing, but increased by fertilization under ambient grazing. When protected from predators in field cages, these mesograzers limited epiphyte blooms even with nutrient enrichment, and nutrients instead enhanced grazer secondary production. Crustacean mesograzers play a key role in maintaining macrophyte (seagrass) dominance in Chesapeake Bay, in buffering eelgrass against eutrophication, and in efficiently transferring nitrogen to higher trophic levels. Yet, these crustacean grazers are also highly sensitive to predator abundance. Reducing nutrient pollution alone is unlikely to restore seagrass meadows where alterations to food webs have reduced populations of algae-feeding mesograzers. Integration of both water quality and fishery management will be more effective in restoring and maintaining healthy coastal ecosystems.
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Field experimental evidence that grazers mediate transition between microalgal and
seagrass dominance
Pamela L. Reynolds,
J. Paul Richardson, and J. Emmett Duffy
Virginia Institute of Marine Science, College of William & Mary, Gloucester Point, Virginia
We tested the relative effects of nutrient loading, reduced predation, and reduced grazing on eelgrass
community dynamics in Chesapeake Bay and found evidence supporting the ‘‘mutualistic mesograzer model’’ in
which small invertebrate grazers control accumulation of epiphytic algae, buffer eutrophication effects, and thus
facilitate seagrass dominance. Experimental reduction of crustacean grazers in the field stimulated a nearly sixfold
increase in epiphytic algae, and reduced seagrass biomass by 65%compared to controls with grazers. Nutrient
fertilization generally had much weaker effects, but an interaction with mesograzers was key in changing the sign
of fertilization effects on the system: aboveground eelgrass biomass was reduced by fertilization under reduced
grazing, but increased by fertilization under ambient grazing. When protected from predators in field cages, these
mesograzers limited epiphyte blooms even with nutrient enrichment, and nutrients instead enhanced grazer
secondary production. Crustacean mesograzers play a key role in maintaining macrophyte (seagrass) dominance
in Chesapeake Bay, in buffering eelgrass against eutrophication, and in efficiently transferring nitrogen to higher
trophic levels. Yet, these crustacean grazers are also highly sensitive to predator abundance. Reducing nutrient
pollution alone is unlikely to restore seagrass meadows where alterations to food webs have reduced populations
of algae-feeding mesograzers. Integration of both water quality and fishery management will be more effective in
restoring and maintaining healthy coastal ecosystems.
A fundamental challenge in ecology is understanding
and predicting how changes in the abiotic and biotic
environment influence the structure and function of
ecosystem processes (Gruner et al. 2008). Understanding
the interplay of bottom-up and top-down processes,
including the supply of nutrients and consumer pressure,
is critical given ongoing perturbations to environmental
condition and food-web topology (Duffy 2003; Byrnes et
al. 2007). The importance of quantifying the synergistic
effects of bottom-up and top-down control is well
illustrated by seagrass ecosystems, which are highly
threatened by both the bottom-up effects of eutrophication
and the top-down effects of overfishing, among other
human activities. Seagrasses provide important ecologic
and economic services from provision of nursery habitat to
shoreline protection against erosion and storm events to
carbon sequestration (Costanza et al. 1997), but seagrasses
worldwide have declined dramatically over recent decades
(Orth et al. 2006b; Waycott et al. 2009).
Historically, responses to seagrass declines have focused
on eutrophication, associated high turbidity, and blooms of
epiphytic and planktonic algae (bottom-up control), which
compete with seagrasses for light and other resources
(McGlathery 1995; Hauxwell et al. 2001). Although good
water quality is clearly important for seagrass vigor (Orth
et al. 2006a), growing evidence also supports an important
role for top-down control in seagrass systems (reviewed by
Hughes et al. 2004; Baden et al. 2010; Duffy et al. 2013),
with important implications for the extensive efforts and
expense devoted to seagrass management and restoration
worldwide. In particular, the small invertebrate herbivores
that dominate many coastal and estuarine systems often
appear to play key roles in shifts between alternative
community states dominated by macrophytes (e.g., sea-
grasses) and microalgae. These small crustacean and
gastropod mesograzers are thought to function as a critical
link in coastal food webs similarly to zooplankton in
pelagic systems, and they can shift primary producer
dominance by mediating trophic cascades (Duffy and
Hay 2000; Davenport and Anderson 2007). Mesograzers
are often the dominant herbivores in temperate seagrass
systems (Cebrian 1999; Valentine and Duffy 2006) and,
while they have been observed in select cases to act as pests
and inhibit their hosts through direct consumption of
seagrass tissue (Zimmerman et al. 2010; Reynolds et al.
2012), in most instances they feed preferentially and heavily
on ephemeral macroalgae and microalgae (reviewed by
Jernakoff et al. 1996; Valentine and Duffy 2006).
Because algae are typically competitively superior to
seagrasses, especially under high-nutrient conditions, me-
sograzers may play a key role in preventing overgrowth of
seagrasses by algae and therefore act as mutualists with
their hosts, promoting seagrass growth and buffering them
against algal overgrowth resulting from nutrient pollution.
This ‘‘mutualistic mesograzer’’ model (Duffy et al. 2013)
was originally based on natural history observations and
lab experiments (Orth and Van Montfrans 1984) and is
supported by growing field evidence (Baden et al. 2010;
Cook et al. 2011; Whalen et al. 2013), although there are
exceptions (Lewis and Anderson 2012).
The important role of grazing in seagrass systems raises
the question of what factors control grazers and their algal
resources. Invertebrate grazers, particularly crustaceans,
* Corresponding author:
Present address: Department of Environmental Science and
Policy, University of California, Davis, California
Limnol. Oceanogr., 59(3), 2014, 1053–1064
E2014, by the Association for the Sciences of Limnology and Oceanography, Inc.
are important prey for fishes (Edgar and Shaw 1995) and are
highly vulnerable to predation. Thus, disturbances to upper
levels of the food web, e.g., through fishing, could have
pervasive effects that ripple through food webs and ecosys-
tems (Heck and Valentine 2007). Recent evidence from the
Swedish west coast supports this hypothesis, showing declines
in top predators and concomitant increases in mesopredator
populations coinciding with reduced grazer abundances and
dramatic seagrass declines (Baden et al. 2012).
Although many lines of evidence now support a role for
cascading top-down effects in vegetated marine communi-
ties, few if any studies have unequivocally documented the
final links in the proposed mutualism, that is, from
mesograzer reduction to algal bloom to reduced seagrass
performance and biomass. It is also unclear how general
this model of mesograzer control of alternate vegetation
states is within estuaries (Duffy et al. 2013). In many
temperate estuaries, invertebrate grazers in seagrass beds
are consumed by a diverse suite of small predators
including decapod crustaceans and demersal fishes (Orth
et al. 1984; Teixeira and Musick 1994), most of which are
generalists capable of strongly controlling grazer popula-
tions with potential consequences for algal–seagrass
dynamics in this system. These small predators may be an
important link in seagrass systems, since fluctuations in
their populations and overall predation intensity may lead
to grazer and/or algal outbreaks (Baden et al. 2010;
Svensson et al. 2012). While nutrient loading has histori-
cally been attributed as the driver for shifts in seagrass to
algal dominance (Harlin 1993; Orth et al. 2006b; Bur-
kholder et al. 2007), trophic interactions are clearly also
important (Heck et al. 2000; Hughes et al. 2004). In the
presence of small invertebrate herbivores, fertilization
alone has shown little negative effect on seagrass growth
(reviewed by Hughes et al. 2004; Burkepile and Hay 2006;
Valentine and Duffy 2006), and thus the question remains:
can small invertebrate grazers mediate eutrophication
effects in coastal food webs?
Here we investigate the interactive influence of bottom-up
and top-down forcing on seagrass systems in Chesapeake
Bay, Virginia. Using a combination of cageless and tradi-
tional caging methods in the field, we evaluate the potential
role of small crustacean grazers in buffering this system from
nutrient-mediated algal blooms and the effect of small
predators (fish, shrimp, crabs) in regulating these communi-
ties. Specifically, we examined the effects of fertilization and
grazer and predator exclusion on epiphyte accumulation,
seagrass production, and grazer biomass in the field.
We conducted two experiments to evaluate the relative
importance of top-down effects of consumers and the
bottom-up influence of fertilization on the dynamics of
eelgrass (Zostera marina) communities in the field. Histor-
ically the role of mesograzers in realistic field situations has
been very difficult to address owing to the difficulty of
caging them (Connell 1974; Virnstein 1978; Miller and
Gaylord 2007). The first experiment used a novel cageless
method to exclude grazers (Poore et al. 2009), while the
second featured cages to exclude their predators. Addi-
tionally, a predation assay was conducted in the field to
assess top-down pressure on the most abundant mesograzer
taxa and to confirm hypothesized food-web relationships.
All experiments were conducted in a dense bed of Z. marina
on the southeast side of the Goodwin Islands National
Estuarine Research Reserve on the York River estuary near
the mouth of the Chesapeake Bay in Virginia (37u139N,
76u239W) at 0.5 m mean-low-water depth.
Mesograzer exclusion—To test the role of grazers and
nutrient additions on the seagrass community, we estab-
lished experimental plots in May of 2011 using cageless
methods (modified from Whalen et al. 2013). Plots were
framed by three polyvinyl chloride (PVC) poles forming a
0.5 m sided equilateral triangle and randomly assigned to
one of four experimental treatments in a factorial design.
For the nutrient addition treatment, plots received either
0 or 300 g of the commercial, slow-release (4 month)
fertilizer (14 nitrogen, 14 phosphorus, 14
potassium) placed in fiberglass mesh (1 mm) bags attached
30 cm from the sediment to each plot pole, such that
fertilized plots received a total of 900 g and nonfertilized
plots received only empty bags (methods comparable to
Moksnes et al. 2008; Baden et al. 2010). Although the
fertilizer slowly leaches into the water column over a period
of 6–8 weeks, to ensure consistent delivery throughout the
experiment the bags were replaced with new fertilizer after
4 weeks. Prior work in the York River, Virginia, and
ongoing monitoring by the Chesapeake Bay National
Estuarine Research Reserve show pronounced fluctuations
in nutrients and phytoplankton in patterns that are not
indicative of chronic background eutrophication (Whalen
et al. 2013). Our fertilizer application increased nitrogen
content in the eelgrass leaves by over 20%(see Results),
simulating a chronic, eutrophic condition.
Experimental reduction of mesograzers was accom-
plished by fitting each pole in a plot with a plaster (Ortho
Plaster, 275-310 bar slow) block containing 10%carbaryl
(Bayer Crop Science) by weight, which reduces crustacean
grazer densities in the field (Whalen et al. 2013), attached
15 cm from the sediment. Carbaryl, a reversible acetylcho-
linesterase inhibitor widely used against arthropods in
homes, gardens, and aquaculture in the United States, has
had limited direct effects on nonarthropod taxa (such as
algae) in experimental studies (Carpenter and Lodge 1986;
Duffy and Hay 2000; Dumbauld et al. 2001). Supplemental
studies found the concentration used here effectively
reduced gammaridean amphipod densities in the field up
to 60 cm away from the block, with greatly diminished
effectiveness at greater distances, supporting the highly
localized effects of this treatment (Whalen et al. 2013).
Control plots received plaster blocks without carbaryl.
Blocks were prepared with a recipe modified from Poore
et al. (2009) and were replaced weekly throughout the
experiment. This cageless design allows experimental
exclusion of small crustacean grazers from seagrass in the
field without strong modification of flow, light, and other
parameters that can be compromised in traditional caging
experiments (Connell 1974; Virnstein 1978).
1054 Reynolds et al.
Table 1. Mesograzer exclusion experiment: Effects of experimental treatments (deterrent and nutrient additions) on mesograzer
biomass at 4 weeks, epiphyte (mg Chl aper gram of Z. marina) and epibiont load at 4 weeks, total seagrass biomass at 8 weeks, and Z.
marina production and tissue percent nitrogen at 4 weeks. Values significant at p,0.05 are listed in italic. df, degrees of freedom.
Response df Sum squares Fp
Total mesograzer biomass
Deterrent 1 2.256 7.036 0.012
Nutrients 1 0.001 0.001 0.972
Deterrent 3nutrients 1 0.016 0.050 0.824
Error 36 11.544
Deterrent 1 1.754 10.836 0.002
Nutrients 1 0.001 0.006 0.940
Deterrent 3nutrients 1 0.396 2.449 0.126
Error 36 5.827
Deterrent 1 5.682 81.829
Nutrients 1 0.025 0.366 0.549
Deterrent 3nutrients 1 0.194 2.791 0.103
Error 36 2.500
Total seagrass biomass
Deterrent 1 0.78 43.410
Nutrients 1 0.032 1.760 0.193
Deterrent 3nutrients 1 0.044 2.383 0.131
Error 36 0.663
Z. marina biomass
Deterrent 1 0.421 13.218 0.001
Nutrients 1 0.058 1.830 0.185
Deterrent 3nutrients 1 0.146 4.584 0.039
Error 36 1.147
Deterrent 1 0.789 5.059 0.031
Nutrients 1 0.000 0.001 0.973
Deterrent 3nutrients 1 0.005 0.033 0.858
Error 36 5.615
R. maritima biomass
Deterrent 1 1.447 7.172 0.011
Nutrients 1 0.081 0.340 0.531
Deterrent 3nutrients 1 0.290 1.437 0.238
Error 36 7.265
Deterrent 1 1.040 7.309 0.010
Nutrients 1 0.427 2.998 0.092
Deterrent 3nutrients 1 0.569 3.996 0.053
Error 36 5.123
Zostera production
Deterrent 1 1.676 4.663 0.038
Nutrients 1 0.214 5.952 0.020
Deterrent 3nutrients 1 0.082 2.272 0.141
Error 34 1.222
Zostera tissue %N
Deterrent 1 0.015 3.911 0.056
Nutrients 1 0.018 4.780 0.035
Deterrent 3nutrients 1 0.003 0.719 0.402
Error 36 0.137
Grazers structure eelgrass communities 1055
Four weeks after treatment application, we collected Z.
marina shoots and associated algae and epifauna to test for
treatment effects. We quantified the mesograzer communi-
ty by collecting all macrophytes in approximately a 19 cm
diameter circle in the center of each plot using a 300 mm
mesh bag. Grazers were counted and sorted by species, as
well as by size class using a stack of nested sieves. We then
estimated total biomass and secondary production from
the sieve size class abundance data using taxon-specific
empirical equations (as in Edgar 1990). We then standard-
ized mesograzers by the total biomass (grams of dry mass)
of macrophytes collected per sample.
Additional collections of one Z. marina shoot per plot
were made to quantify epiphytic algae (chlorophyll aper
dry mass [g] of the scraped leaves), and four Z. marina
shoots per plot to quantify the total mass of epibiota
(pooled dry mass of all material scraped from the four
leaves standardized by total leaf dry mass). We used whole
shoots instead of single leaves to examine epiphyte and
epibiont loading as leaf age can influence fouling accumu-
lation. These collections were repeated after 8 weeks. After
8 weeks we also harvested all remaining seagrass per plot.
This material was separated into species (Z. marina, Ruppia
maritima) and into aboveground vs. belowground tissue
and dried to assess differences in biomass across experi-
mental treatments.
We quantified treatment effects on the growth rate of the
Z. marina within the plots by punching at least five shoots
(just above their respective leaf sheaths) per plot 3 weeks
after the experiment was initiated. These shoots were
collected a week later (timepoint week 4) and taken back to
the laboratory, where we then measured the linear
extension of the leaves and calculated the rate of dry mass
accumulation (g d
; Short and Duarte 2001). Estimated
growth rates from all shoots in a plot were pooled to obtain
a plot-level mean, which we used to examine treatment
effects on eelgrass growth rate (mm new growth extension
3(Z. marina mg 3mm
). To assess
treatment effects on Z. marina leaf stoichiometry, at the
4 week time point we collected five shoots from the edge of
each plot and removed the youngest leaf from each shoot.
A 3 cm piece of each of these leaves was rinsed with
deionized water, and this tissue was then pooled by plot,
dried, ground, and processed on a carbon–hydrogen–
nitrogen (CHN) analyzer at the Virginia Institute of
Marine Science (VIMS) to assess treatment differences in
leaf tissue nitrogen content. The leaf tissue nitrogen served
as an integrated metric to assess nutrient availability for the
eelgrass (e.g., fertilization treatment effectiveness at elevat-
ing water column nitrogen) during the field experiment
(Burkholder et al. 2007). Epiphyte tissue was not available
for CHN analysis, although owing to its faster turnover
rates we do not necessarily expect to have been able to
strongly detect fertilization effects on microalgal stoichi-
We tested deterrent and nutrient treatment effects on
plant and epifaunal biomass, epiphyte load, and Z. marina
growth and leaf tissue nitrogen content using two-way
Fig. 1. Effects in mesograzer exclusion experiment of deterrent application (control, DØ;
addition, D+) and nutrient additions (N+) or control (NØ) treatments on total mesograzer,
amphipod, isopod, and gastropod biomass per gram of macrophyte and epiphyte load (mgChlaper
gram of Z. marina) after 4 weeks, and final seagrass dry mass after 8 weeks in experimental field plots.
1056 Reynolds et al.
ANOVAs in R (R Development Core Team 2013, version
2.15.2) with type III sums of squares. To graphically
examine changes in the mesograzer community across
experimental treatments, we used nonmetric multidimen-
sional scaling (NMDS) based on Bray–Curtis distance with
the metaMDS function in the vegan package in R. The
results were plotted in two dimensions, and the envfit
procedure in vegan was used to overlay species vectors.
Direct effects of chemical deterrent—To confirm whether
the experimental deterrent treatment may have had direct
effects on the seagrasses in the mesograzer exclusion
experiment, we conducted a mesocosm experiment at
VIMS factorially manipulating seagrass species (Z. marina,
R. maritima) and deterrent (none, plaster only, plaster +
carbaryl) treatments (n58). Seagrasses were collected
from Allen’s Island, York River, Virginia, in October 2011
and transported back to the lab on ice where they were
gently defaunated by hand and rinsed in freshwater and salt
water to ensure removal of all grazers. Mesocosms
(18 liters) were randomly placed in tanks (blocking factor),
assigned to one of the four treatments, and filled with
4.5 liters of prepared sediment (30%mud, 70%sand
mixture). Mesocosms then received either 12 63gZ.
marina or 13 63gR. maritima and either no block or a 50 g
block composed of plaster only or plaster prepared with
10%carbaryl (deterrent treatment). Mesocosms received
pulsed dumps approximately every 2 min of 150 mm filtered
seawater from the adjacent York River and were shaded to
approximate light conditions in the field. Three Z. marina
shoots per mesocosm were punched at the leaf sheath to
quantify growth rate. After 17 d we harvested all seagrass
and scraped off all epibionts, which were dried and weighed
to quantify epiphyte load. Barnacles were removed and
dried separately to test deterrent treatment effects on this
fouling invertebrate. After scraping, we then lightly rinsed
and weighed all seagrass shoots. Responses were analyzed
separately for the two seagrass species with one-way
blocked ANOVAs in R.
Predation assay—To assess the selectivity of predation in
the field, we employed a predation assay (Manyak et al.
2013) examining differences among mesograzer taxa in
vulnerability to predators in the field. Although gammar-
idean amphipod, isopod, and gastropod grazers are all
consumed by larger invertebrates and fishes, predator
selection and preferences may vary across taxa with
potential effects on epiphyte–seagrass interactions depend-
ing on which grazer taxa, and their relative grazing effects,
are more susceptible to predation (Best and Stachowicz
2012; Eklo¨ f et al. 2012). To test predator effects across
grazer taxa in the field, in July 2012 we used super glue to
attach one mesograzer (Ampithoid amphipod, isopod
Erichsonella attenuata, or gastropod Bittium varium), or a
standard prey type (10 mm piece of freeze-dried shrimp), or
a control prey mimic (10 mm piece of fuzzy pipe cleaner) to
Fig. 2. Effects of nutrient addition (control, NØ; addition, N+) and mesograzer deterrent application
(D+) on mesograzer community composition after 4 weeks in the mesograzer exclusion experiment,
illustrated via NMDS. Grazer taxa included amphipods Ampithoe longimana, Ampithoe valida, Caprella
equilibria, Caprella penantis, Corophium sp., Cymadusa compta, Elasmopus levis, Gammarus mucronatus,
Microprotopus raneyi, Paracaprella tenuis; isopod Edotea triloba; gastropods Bittium varium, Crepidula sp.
Grazers structure eelgrass communities 1057
a standardized location on a leaf of a shoot of Z. marina.
Individual grazers were collected within their most abun-
dant size class (5–15 mm) and represent the most common
mesograzer species at the field site. The shoot was then tied
to a clear acrylic rod for deployment in the field such that
the shoot was oriented upright in a natural orientation.
Rods were deployed at low tide and collected 24 h later. As
nearly all mimics remained attached, we inferred that
missing prey were likely eaten and not absent due to a loss
of glue adhesion. Prey presence vs. absence data were
analyzed with logistic regression in R, which took into
account baseline (control) losses.
Predator exclusion—To explore top-down effects of
predators on mesograzer and cascading effects on primary
producers, we conducted a 3 week field caging experiment
manipulating predator access and nutrient addition in plots
established in July 2012. Thirty plots were randomly
assigned in a two-way factorial design to experimental
nutrient addition (two levels: 0 or 300 g Plantacote
) and
predator exclusion (three levels: open plot, cage control, full
cage). Cages were constructed using a frame of PVC (40 3
40 345 cm length, width, height) wrapped in nylon mesh
(0.79 mm diameter holes), which allowed access to the cage
by grazers but excluded the larger predatory fishes and
invertebrates. All plots were established along a seagrass
patch edge and were marked with two PVC poles; cages were
secured to these poles with bungee cords. Cages were filled
with approximately 5 liters of coarsely defaunated mud and
Fig. 3. Effect in mesograzer exclusion experiment of deterrent application (D+) and nutrient
additions (N+)onZ. marina and R. maritima aboveground (shoots) and belowground (roots,
rhizomes) biomass after 4 weeks in the mesograzer exclusion experiment.
Fig. 4. Effects in mesograzer exclusion experiment of deter-
rent application (D+) and nutrient additions (N+) treatments on
the percentage nitrogen in new growth Z. marina leaf tissue, and
on Z. marina growth rate after 4 weeks in the field.
1058 Reynolds et al.
sand to provide substrate and assist in anchoring the cage.
Open plots received a square of PVC placed on the sediment
and secured to the marking poles. A circle of Vexar (30 cm
diameter), to which 24 shoots of live Z. marina were cable
tied at natural densities (initial wet mass of ,35 g per plot),
was attached to the bottom PVC square of each plot. Z.
marina shoots were collected with their associated rhizomes
and root hairs and were gently rinsed in seawater to remove
any fauna and debris prior to attachment. After the eelgrass
was added, all plots were then stocked with natural
assemblages of grazers (,75 amphipods and ,50
gastropods) collected by conducting two, 2 m long dipnet
(13 314.5 cm) sweeps within the center of the seagrass bed
adjacent to each plot. Nutrients were placed in mesh bags as
in the mesograzer exclusion experiment and attached to one
of the poles next to the cage. Plots were monitored and cages
cleaned weekly throughout the experiment.
After 3 weeks, we enclosed each Vexar circle with its
attached Z. marina and associated epifauna and predators
in a mesh bag and transported them to the lab where we
quantified the final dry mass of Z. marina, abundance and
biomass of associated grazers by gross taxonomic group
(gastropods, amphipods, and isopods), and identity and
abundance of predators. Epiphytic algal load was quanti-
fied from one separately collected shoot per plot as in the
mesograzer exclusion experiment. Since previous experi-
ments have demonstrated that cages can introduce unin-
tended artifacts due to reductions in light, water flow, and
other factors (Connell 1974; Virnstein 1978), our interest
Table 2. ANOVAs of treatment effect (control, plaster only,
plaster +carbaryl) on given responses in experimental mesocosms.
Response df Sum squares Fp
Z. marina growth
Treatment 2 34.738 2.050 0.158
Blocking 1 18.716 2.209 0.155
Treatment 3blocking 2 4.641 0.274 0.764
Error 18 152.498
Z. marina growth rate
Treatment 2 0.037 0.771 0.479
Blocking 1 0.005 0.194 0.666
Treatment 3blocking 2 0.059 1.221 0.321
Error 16 0.387
R. maritima growth
Treatment 2 27.69 0.352 0.708
Blocking 1 161.82 4.118 0.058
Treatment 3blocking 2 51.34 0.653 0.532
Error 18 707.39
Barnacles on Z. marina
Treatment 2 0.001 0.051 0.950
Blocking 1 0.002 0.436 0.518
Treatment 3blocking 2 0.022 2.056 0.157
Error 18 0.096
Barnacles on R. maritima
Treatment 2 0.030 2.676 0.096
Blocking 1 0.000 0.001 0.970
Treatment 3blocking 2 0.012 1.048 0.371
Error 18 0.102
Fig. 5. Effects of plaster and deterrent (10%carbaryl) on seagrass growth and barnacle accumulation in experimental mesocosms
after 17 d.
Grazers structure eelgrass communities 1059
was in contrasts specifically between the partial and full
caging treatments, and thus analyses were performed as in
Hindell et al. (2001) using a priori contrasts comparing the
partial to the full treatments. Two-way ANOVAs in R were
used to test for effects of nutrient addition (6), cage
treatment (partial, full), and their interactions on epiphyte
load and final Z. marina biomass and mesograzer wet mass
in the predator exclusion experiment.
Mesograzer exclusion—The dilute, slowly dissolving
chemical deterrent reduced invertebrate mesograzer bio-
mass by 76%, and this mesograzer reduction cascaded to
increase epiphytic algae (chlorophyll a[Chl a]) by 590%on
average after 4 weeks, which in turn reduced seagrass
biomass by 65%after 8 weeks (Table 1; Fig. 1). The total
biomass of epibiota on the eelgrass was positively
correlated with chlorophyll a(p,0.0001, R
was higher in the plots with reduced mesograzer biomass,
and was thus likely largely composed of epiphytic algae.
The chemical deterrent specifically reduced crustaceans,
with little to no effect on gastropods (Fig. 1). The
deterrent, but not the nutrient addition, substantially
shifted mesograzer community composition after 4 weeks
as a result of greatly reduced amphipod abundances
(Fig. 2). Nutrient additions had no effect on either epiphyte
load or mesograzer abundance in this experiment (Table 1;
Fig. 1).
Both eelgrass and widgeongrass (R. maritima) declined
on average in plots exposed to the deterrent (Table 1;
Fig. 3). This change was evident in both the aboveground
(leaves) and belowground (roots and rhizomes) compo-
nents of both seagrass species after 8 weeks in the field.
Deterrent (D) and nutrient (N) treatments interactively
affected Z. marina aboveground biomass, since greater leaf
biomass was observed in fertilized plots with the intact
ambient mesograzer community (DØ N+treatments).
Fig. 6. Prey survivorship by mesograzer type and seagrass
(habitat) type in predation assays.
Table 3. Predator exclusion experiment: Results of a priori contrasts of experimental treatments (caging, nutrient addition) on final mesograzer
biomass by taxa, epiphyte load (Chl amgpergramofZ. marina), and Z. marina dry mass after 3 weeks. Standard error (SE); Pr(.|t|) ,0.05 are
in italics.
Response Estimate SE tPr(.|t|)
Crustacean grazer biomass
Open plot vs. caging 21.459 0.591 22.467 0.022
Partial vs. full cage 20.887 0.348 22.546 0.018
Nutrient addition vs. no addition 20.894 0.422 22.116 0.045
Nutrients 3caging 20.177 0.348 20.508 0.616
Gastropod grazer biomass
Open plot vs. caging 1.131 0.408 2.770 0.011
Partial vs. full cage 0.911 0.241 3.786
Nutrient addition vs. no addition 0.060 0.292 0.205 0.839
Nutrients 3caging 0.163 0.241 0.678 0.505
Total mesograzer biomass
Open plot vs. caging 21.040 0.537 21.935 0.065
Partial vs. full cage 20.674 0.317 22.130 0.044
Nutrient addition vs. no addition 20.699 0.384 21.822 0.082
Nutrients 3caging 20.078 0.317 20.247 0.807
Open plot vs. caging 0.907 0.257 3.526 0.002
Partial vs. full caging 0.209 0.154 1.353 0.190
Nutrient addition vs. no addition 20.004 0.186 20.021 0.983
Nutrients 3caging 0.075 0.154 0.487 0.631
Z. marina dry mass (g)
Open plot vs. caging 1.162 0.426 2.728 0.012
Partial vs. full caging 0.141 0.251 0.562 0.579
Nutrient addition vs. no addition 0.304 0.304 0.999 0.328
Nutrients 3caging 20.012 0.251 20.047 0.963
1060 Reynolds et al.
While fertilization promoted Z. marina production, meso-
grazer exclusion had the opposite effect (Fig. 4). Nitrogen
content of new Z. marina tissue was 9%higher in fertilized
plots and correlated with the increased growth rate in those
treatments (Fig. 4).
Direct effects of chemical deterrent—Z. marina and R.
maritima seagrasses grew by 9.7 and 7.6 g in wet mass, on
average, across all mesocosms during the experimental test
of potential direct effects of the chemical deterrent
treatment. No treatment (control, plaster only, plaster +
deterrent), blocking, or blocking by treatment interaction
effects were observed on the growth of Z. marina or R.
maritima, the growth rate of Z. marina, or the accumula-
tion of barnacles on each seagrass type (Table 2; Fig. 5).
Predation assay—Prey survivorship differed strongly
among prey taxa (amphipod, isopod, gastropod) and
seagrass habitats (Z. marina,R. maritima;x
p50.010). Gammaridean amphipods were completely
removed by predators, whereas gastropods were largely
untouched (Fig. 6). Losses due to abrasion or weakened
glue adhesion in the field (measured as losses of the mimic)
were minimal in the eelgrass habitat and not observed at all
in the widgeongrass.
Predator exclusion—Few predators were recorded in the
full cages at the end of the experiment compared with
the partial cages (F
52.234, p50.018), confirming that
the experiment reduced predator pressure in the full cage
treatments. Predator exclosure increased crustacean but
reduced gastropod biomass (a priori contrast of partial vs.
full cage, Table 3; Fig. 7). Caged mesograzer communities
were dominated by gammaridean amphipods that are
known to be strong algal grazers (e.g., Ampithoe longimana,
Cymadusa compta,Gammarus mucronatus, Fig. 8). Nutri-
ent additions increased crustacean biomass but had no
effect on gastropod biomass (Table 3; Fig. 7). Neither
predator exclusion nor nutrient additions affected epiphyte
load (Chl aper gram of Z. marina) or the final mass of Z.
marina (a priori contrasts), although we did observe an
effect of caging itself (Table 3; Fig. 7).
Our results provide direct field experimental confirma-
tions of the mutualistic mesograzer hypothesis, i.e., that
mesograzers promote seagrass dominance by cropping
algal competitors that otherwise reduce seagrass perfor-
mance (Orth et al. 1984; Duffy et al. 2013). Specifically,
experimental reduction of crustacean grazers stimulated a
nearly sixfold increase in epiphytic algae in the field, which
in turn strongly reduced seagrass growth and biomass (by
65%compared with controls). In general, we found
stronger evidence of top-down than of bottom-up control
in this system, although there were important effects of
fertilization on grazer production. In particular, the two
field experiments demonstrated that that grazers substan-
tially promoted eelgrass, nutrient loading enhanced bio-
mass of crustacean grazers but not of algae, and that
crustacean grazers were highly sensitive to the abundance
of predators. These results corroborate similar evidence of
mesograzer control of algae in laboratory and mesocosm
studies (reviewed by Jernakoff et al. 1996; Hughes et al.
2004; Valentine and Duffy 2006) as well as a growing
number of field experiments in eelgrass (Moksnes et al.
2008; Baden et al. 2010; Whalen et al. 2013) and other
seagrass systems (Cook et al. 2011; Myers and Heck 2013).
But few previous studies have made the final connection
from reduced grazing to ephemeral algal blooms to reduced
seagrass fitness.
Our results also support pioneering work in the Baltic
region, where experiments and time series also showed that
Fig. 7. Effects in predator exclusion experiment of caging
(open, partial, full) and nutrient addition (N+) on crustacean and
gastropod mesograzer biomass, epiphyte load, and Z. marina dry
mass after 3 weeks.
Grazers structure eelgrass communities 1061
mesograzers are a key link in eelgrass food webs, potentially
mediating the transition between macrophyte- and algal-
dominated systems (Moksnes et al. 2008; Baden et al. 2010,
2012). Our results thus confirm the emerging generalization
that temperate seagrass beds are much more sensitive than
historically assumed to perturbations to coastal food webs.
As in the Baltic region, however, the top-down control we
documented interacts in important ways with bottom-up
forcing. Specifically, in both systems, small crustacean
grazers play an important role in buffering seagrass against
eutrophication and improving seagrass health, as evidenced
by the interaction between fertilization treatment and
mesograzer presence on eelgrass biomass. In our study,
nutrient loading increased eelgrass biomass when mesogra-
zers were present but tended to reduce eelgrass biomass
when mesograzers were excluded; fertilization enhanced
eelgrass growth in both presence and absence of grazers in
our short-term assay. Similarly, experimentally enhanced
nutrient levels on the Swedish west coast resulted in blooms
of macroalgal mats and decreased growth of eelgrass in the
absence of mesograzers but had no effect under historically
high mesograzer densities (Baden et al. 2010). Likewise,
nutrient enrichment had no effect on shoalgrass biomass in a
recent field experiment (Myers and Heck 2013), although
there was a negative effect on leaf length in protected sites
where amphipod abundances were low. These interactions
between grazing and nutrient loading mirror many previous
experiments conducted in the laboratory and mesocosms
(Hughes et al. 2004), which showed that mesograzers
controlled the growth of ephemeral algae, even under
elevated nutrient conditions.
Seagrass ecology and the management strategies based
on it have historically focused almost exclusively on water
quality (specifically turbidity and nutrient loading). How-
ever, several of the studies discussed above from temperate
seagrass beds found that experimental fertilization had
little effect on epiphytic algae, whereas experimental
mesograzer reduction had stronger effects than fertilization
(Heck et al. 2000; Hughes et al. 2004; Spivak et al. 2009).
Nutrient limitation was supported in our study, however,
by the positive effect of nutrient enrichment on mesograzer
biomass in the predator exclusion study. This finding that
fertilization effects bypassed standing stock of primary
producers to elevate secondary production is similar to that
observed in a field caging experiment in the Baltic, where
ambient densities of grazers are high (Baden et al. 2010).
The key role of invertebrate grazers raises the question of
what controls their abundance. Both our study and
experiments in the Baltic region show that ambient
predator abundances exert strong top-down control on
grazers (Moksnes et al. 2008; Baden et al. 2010) and that
this pattern is overlain on, and interacts with, a base of
bottom-up control. Our field experiment confirmed previ-
ous mesocosm findings of a bottom-up influence on grazers
as nutrient loading was transmitted efficiently up the food web
to increase mesograzer biomass in mesocosm experiments in
Fig. 8. Effects of nutrient addition and cage type (open, partial, full) on mesograzer
community composition in the predator exclusion experiment after 3 weeks in the field, illustrated
via NMDS. Grazer taxa included species listed in Fig. 2 as well as amphipods Dulichiella
appendiculata,Lembos spinicarpus,Microdeutopus anomalus; isopod Paracerceis caudata,
gastropod Mitrella lunata, and an unidentified limpet.
1062 Reynolds et al.
Chesapeake Bay (Spivak et al. 2009) and field experiments in
Sweden (Moksnes et al. 2008). This bottom-up signal is
consistent with patterns in time-series data from our site
showing that correlations across trophic levels are more often
positive than negative (Douglass et al. 2010).
Although our data suggest that patterns of trophic
control are similar in eelgrass beds on both sides of the
North Atlantic, quite different processes can occur in other
seagrass systems (see review in Duffy et al. 2013), where,
for example, algal grazing by omnivorous fishes (Heck et
al. 2000) or destructive grazing of eelgrass tissue by
invertebrates (Zimmerman et al. 2010; Reynolds et al.
2012) has variable consequences for seagrasses when food
webs are perturbed. The relative strengths of top-down and
bottom-up control and their system-level consequences are
thus mediated by species- and system-specific factors,
including palatability of primary producers, food prefer-
ence and vulnerability of mesograzers (Best and Stachowicz
2012), omnivory of mesopredators (Heck and Valentine
2006), and differences in recruitment dynamics on different
trophic levels (Svensson et al. 2012). Similar to prior work
in Sweden (Baden et al. 2010), we found strong cascading
top-down control, likely because the most abundant
epifauna were effective algal grazers (primarily ampithoid
amphipods). These taxa were in turn highly vulnerable to
the ambient predator community, as evidenced by the
intense predation upon this group in field predation assays
(Fig. 6) as well as their dominance in communities in which
their predators were excluded (full field cages, Fig. 8).
Our results add growing support for the hypothesis that
changes in both nutrient regimes and coastal food-web
structure often interact to have a fundamental effect on
seagrass ecosystems. Reducing nutrient pollution alone is
unlikely to restore seagrass meadows if there have been
pervasive alterations to food webs that have resulted in
reduced populations of algal mesograzers. In these areas,
management of water quality would best be integrated with
fishery management to restore the abundance of large
predators and improve coastal ecosystems.
We thank the many technicians, students, and volunteers who
assisted with field and lab work, including R. Blake, S. Donadi, E.
Ferer, C. Fikes, M. Gyoerkoe, K. Jenkins, A. Kuwahara, J.
Lefcheck, K. Sobocinski, and M. Whalen. We also appreciate the
contributions of two anonymous reviewers and insights from the
Zostera Experimental Network. This work was supported by the
National Science Foundation grant 1031061 in Oceanography to
JED. This paper is Contribution No. 3354 of the Virginia Institute
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Associate editor: Anthony W. D. Larkum
Received: 19 June 2013
Accepted: 02 January 2014
Amended: 12 February 2014
1064 Reynolds et al.
... Increases in nutrients from for example eutrophication, favour fast-growing macro and epiphytic algae with negative effects on seagrasses. Top-down control of algal overgrowth has emerged as a key function in the maintenance and management of seagrass habitats (Eriksson et al. 2009, Reynolds et al. 2014, Campbell et al. 2017, which requires the biomass of competing epiphytes to be stemmed by maintaining a balance of both top-down (grazing) and bottom-up (nutrients levels) processes (Duffy et al. 2015). ...
... Top-down consumer control and bottom-up effects of nutrients can be influenced by direct (predation) and indirect (presence/absence) effects of predators (Amundrud et al. 2015, Hill and Heck 2015, Beerman et al. 2018) as well as herbivore identity and feeding rates Stachowicz 2012, Svensson et al. 2012), which can differ temporally (Whalen et al. 2013) and across spatial scales (Campbell et al. 2017, Donadi et al. 2017. Mesograzers (mainly crustaceans) have been recognized to fulfill a key role in controlling ephemeral algae in several eutrophic seagrass systems (Eriksson et al. 2009, Jaschinski and Sommer 2011, Reynolds et al. 2014). ...
... Findings from this large-scale experiment corresponded with previous local-scale studies (Hughes et al. 2004, Reynolds et al. 2014, and provided global and local support for the importance of biodiversity and top-down control in influencing threatened seagrass habitats (Duffy et al. 2015). ...
... Seagrass-epiphyte interactions are central to seagrass ecosystems and can be competitive for nutrients and light (Hauxwell et al., 1998;McGlathery, 2001) or a symbiotic relationship mediated by nutrient exchange (Harlin, 1973a). In addition to their interactions with seagrass, epiphytic algae also play an important role at the base of the green food web associated with seagrass habitats in temperate systems (Duffy et al., 2015;Fry, 1984;Reynolds et al., 2014). Understanding causes of variation in epiphyte abundance, and seagrass-epiphyte interactions, is an important component of understanding energy flow and community structure of a seagrass meadow (Heck et al., 2000;McGlathery, 2001). ...
... After shoots were covered in mesh, we broke eelgrass off at the sediment-water interface and tied the bag to prevent escape by invertebrates. This method is effective at capturing epifaunal invertebrates that may be important grazers (0.5 mm -4 cm long) on eelgrass shoots, but less effective in capturing larger mobile invertebrates such as adult crabs (Duffy et al., 2015;Reynolds et al., 2014;Whippo et al., 2018). In the lab we separated Zostera shoots, epiphytes including Smithora, and invertebrates. ...
... We counted shoots and dried and weighed algae and seagrass. Following standard processing protocol (Reynolds et al., 2014), all invertebrates were removed from shoots and preserved with 95% ethanol. Invertebrates > 0.5 mm were visually classified to lowest taxonomic level possible (Appendix 1) using a stereo microscope. ...
In aquatic foundation species, composition and abundance of associated epibionts can change substantially over small spatial distances. Such spatial variation can reflect top-down control by consumers, bottom-up control by abiotic factors or facilitation, or a combination of processes. We used visual and molecular surveys to describe spatial patterns in the abundance and distribution of the epiphytic red macroalga Smithora naiadum in a meadow of the seagrass Zostera marina on the Central Coast of British Columbia. We detected Smithora using 18 S ribosomal RNA molecular marker throughout the seagrass meadow at both interior and edge sites, even in the absence of macroscopic Smithora. We used a reciprocal transplant experiment to test two hypotheses: that patterns in Smithora abundance reflect local environmental conditions, or alternately, that patterns reflect spatial variation in the host plant attributes, microbiota and grazers. Zostera shoots hosted more Smithora at meadow edges relative to meadow interior sites, and shoots with Smithora were associated with distinct invertebrate grazer and bacterial communities relative to shoots 5 m in from the meadow edge without Smithora. Macroscopic Smithora grew on shoots experimentally transplanted from the interior to the meadow edge and shoots hosting Smithora that were transplanted to the interior did not lose Smithora. Our survey and experimental results suggest that presence of macroscopic Smithora blades on Zostera shoots changes the Zostera microbiota. Altogether, we conclude that environmental variation, not host plant attributes or dispersal limitation, affects Smithora colonization on Zostera, and once established, Smithora alters the microbiota on Zostera.
... These effects indicated a response of the epifauna to indirect effects on their habitat, but not to the direct effects of predation. The important result here was the contrast between treatment effects on epifaunal abundances when these were normalized to algal cover ( habitat to abundant and diverse epifauna (Reynolds et al., 2014;Williams et al., 2013). Invertebrate grazers relying on macroalgae as food have strong direct effects on algae, including altering not only their abundance but also their structure (Cook et al., 2011;Reynolds et al., 2014). ...
... The important result here was the contrast between treatment effects on epifaunal abundances when these were normalized to algal cover ( habitat to abundant and diverse epifauna (Reynolds et al., 2014;Williams et al., 2013). Invertebrate grazers relying on macroalgae as food have strong direct effects on algae, including altering not only their abundance but also their structure (Cook et al., 2011;Reynolds et al., 2014). In our experiments, grazing had a signif- ...
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We tested the response of algal epifauna to the direct effects of predation and the indirect consequences of habitat change due to grazing and nutrient supply through upwelling using an abundant intertidal rhodophyte, Gelidium pristoides. We ran a mid-shore field experiment at four sites (two upwelling sites interspersed with two non-upwelling sites) along 450 km of the south coast of South Africa. The experiment was started in June 2014 and ran until June 2015. Four treatments (predator exclusion, grazer exclusion, control, and procedural control) set out in a block design (n = 5) were monitored monthly for algal cover for the first 6 months and every 2 months for the last 6 months. Epifaunal abundance, species composition, algal cover, and algal architectural complexity (measured using fractal geometry) were assessed after 12 months. Predation had no significant effect on epifaunal abundances, while upwelling interacted with treatment. Grazing reduced the architectural complexity of algae, with increased fractal dimensions in the absence of grazers, and also reduced algal cover at all sites, though the latter effect was only significant for upwelling sites. Epifaunal community composition was not significantly affected by the presence of herbivores or predators but differed among sites independently of upwelling; sites were more similar to nearby sites than those farther away. In contrast, total epifaunal abundance was significantly affected by grazing, when normalized to algal cover. Grazing reduced the cover of algae; thus, epifaunal abundances were not affected by the direct top-down effects of predation but did respond to the indirect effects of grazing on habitat availability and quality. Our results indicate that epifaunal communities can be strongly influenced by the indirect consequences of biotic interactions.
... Herbivores (i.e., epifauna) that partly feed on epiphytic diatoms find refuge in macrophytes, and in terms of seagrass ecosystems, small crustaceans, gastropods, and polychaetes are the predominant groups (Lewis & Hollingworth 1982, Baden 1990, Nakaoka et al. 2001, Namba & Nakaoka 2018. The factors affecting grazer-epiphyte interactions in seagrass ecosystems are complex (Jernakoff et al. 1996), and the inclusion and exclusion of predators have immediate effects on grazers and epiphyte abundance (Reynolds et al. 2014(Reynolds et al. , Östman et al. 2016. Reduced grazing by predators increased epiphyte abundance, and this effect was greater than that of fertilization (Duffy et al. 2015(Duffy et al. , Östman et al. 2016. ...
... Studies concerning allelopathic substances with extracts under artificial conditions (i.e., laboratory) showed subtle effects (Guan et al. 2017); however, shear stress related to water motion may have caused physical detachment of the epiflora, and this remains to be examined in detail (Jacobs et al. 1983). Nevertheless, topdown control of epiphytes by grazers has previously been demonstrated (Jernakoff et al. 1996, Reynolds et al. 2014, Östman et al. 2016, and additional data should provide a much more detailed insight into the population dynamics and interactions among these three states (i.e., substrate, producer, and grazer) in Z. marina ecosystems in Japan. ...
We present a descriptive account of the dynamics of epiphytic diatoms, epifauna, and the leaf surface area of Zostera marina in a shallow water ecosystem. We hypothesized that the growth stage of the host macrophyte (i.e., leaf surface area) influenced the presence of epiflora and epifauna, as well as that the leaf surface area and epifaunal population density affected the cell density and species composition of epiphytic diatoms. To evaluate this hypothesis, we quantified the leaf surface area of a host macrophyte (Zostera marina), the presence of epifauna, and the community of epiphytic diatoms that could be observed on the leaves of Z. marina during the period from May 2017 to December 2018. We conducted a descriptive analysis of the time-series observations of leaf surface area, epiphytic diatom density, and epifauna population density. Epiphytic diatom density was low and epifauna density was high during the growing season of Z. marina. Epiphytic diatom density was high and epifauna density was low during the maturation and senescence periods of Z. marina. Our analysis shows that epifauna densities lagged epiflora densities by at least four months, and that epiflora densities lagged leaf area by four months. Therefore, we hypothesized that herbivorous gastropods and amphipods could alter species composition via their preference of food items (active choice) or by ingesting more of the species that were structurally more available (passive preference).
... marine microalgae and seagrass) that vary across different levels of biological organization [11]. A marine diatom was chosen for use in this study, as they are important primary producers that form the base of many food-webs and contribute to nutrient cycling in marine waters [21,22]. Ammonium (NH 4 þ ) is a source of inorganic nitrogen that is readily available for phytoplankton uptake and assimilation [23,24]. ...
Coastal ecosystems are exposed to multiple anthropogenic stressors. Effective management actions would be better informed from generalized predictions of the individual, combined and interactive effects of multiple stressors; however, few generalities are shared across different meta-analyses. Using an experimental study, we present an approach for analysing regression-based designs with generalized additive models that allowed us to capture nonlinear effects of exposure duration and stressor intensity and access interactions among stressors. We tested the approach on a globally distributed marine diatom, using 72 h photosynthesis and growth assays to quantify the individual and combined effects of three common water quality stressors; photosystem II-inhibiting herbicide exposure, dissolved inorganic nitrogen (DIN) enrichment and reduced light (due to excess suspended sediment). Exposure to DIN and reduced light generally resulted in additivity, while exposure to diuron and reduced light resulted in additive, antagonistic or synergistic interactions, depending on the stressor intensity, exposure period and biological response. We thus find the context of experimental studies to be a primary driver of interactions. The experimental and modelling approaches used here bridge the gap between two-way designs and regression-based studies, which provides a way forward to identify generalities in multiple stressor interactions.
... However, most research testing for their topdown effects has focused on those grazer species that consume epiphytes growing on seagrass, rather than those that consume live seagrass directly. These studies have shown that epiphyte grazers often improve seagrass productivity by controlling the growth of competitively dominant algae, especially in eutrophic environments (Heck et al., 2000;Hughes et al., 2004;Reynolds et al., 2014;Campbell et al., 2018). In general, research on direct grazing (i.e., consumption of live plant tissue) of seagrass has typically highlighted the ability of vertebrates, such as fish, birds, sea turtles, and dugongs, to exert top-down control over seagrass (Valentine and Duffy, 2006;Kollars et al., 2017). ...
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In coastal wetlands and tropical reefs, snails can regulate foundation species by feeding on marsh grasses and hard corals. In many cases, their impacts are amplified because they facilitate microbial infection in grazer-induced wounds. Whether snails commonly graze live plants and facilitate microbial growth on plants in tropical seagrass systems is less explored. On a Belizean Caye, we examined patterns in snail-generated grazer scars on the abundant turtlegrass ( Thalassia testudinum ). Our initial survey showed the occurrence of snail-induced scarring on live turtlegrass blades was common, with 57% of live leaves scarred. Feeding trials demonstrated that two of five common snails ( Tegula fasciata– smooth tegula and Smaragdia viridis –emerald nerite) grazed unepiphytized turtlegrass blades and that smooth tegula abundance had a positive relationship with scarring intensity. Subsequent surveys at three Caribbean sites (separated by >150 km) also showed a high occurrence of snail-induced scars on turtlegrass blades. Finally, simulated herbivory experiments and field observations of a turtlegrass bed in Florida, United States suggests that herbivore damage could facilitate fungal growth in live seagrass tissue through mechanical opening of tissue. Combined, these findings reveal that snail grazing on live turtlegrass blades in the Caribbean can be common. Based on these results, we hypothesize that small grazers could be exerting top-down control over turtlegrass growth directly via grazing and/or indirectly by facilitating microbial infection in live seagrass tissue. Further studies are needed to determine the generality and relative importance of direct and indirect effects of gastropod grazing on turtlegrass health.
... In healthy seagrass ecosystems, algal overgrowth is controlled by mesograzers (e.g., small crustaceans, mollusks, and fishes) that preferably consume algae over seagrass (Williams and Ruckelshaus, 1993). However, impaired grazing function and increased algal dominance can negatively impact seagrass productivity and resilience (Hughes et al., 2013;Reynolds et al., 2014). ...
Global stressors are increasingly altering ecosystem resistance, resilience, and functioning by reorganizing vital species interactions. However, our predictive understanding of these changes is hindered by failures to consider species-specific functional roles and stress responses within communities. Stressor-driven loss or reduced performance of strongly interacting species may generate abrupt shifts in ecosystem states and functions. Yet, empirical support for this prediction is scarce, especially in marine climate change research. Using a marine assemblage comprising a habitat-forming seagrass (Phyllospadix torreyi), its algal competitor, and three consumer species (algal grazers) with potentially different functional roles and pH tolerance, we investigated how ocean acidification (OA) may, directly and indirectly, alter community resistance. In the field and laboratory, hermit crabs (Pagurus granosimanus and P. hirsutiusculus) and snails (Tegula funebralis) displayed distinct microhabitat use, with hermit crabs more frequently grazing in the area of high algal colonization (i.e., surfgrass canopy). In mesocosms, this behavioral difference led to hermit crabs exerting ~2 times greater per capita impact on algal epiphyte biomass than snails. Exposure to OA variably affected the grazers: snails showed reduced feeding and growth under extreme pH (7.3 and 7.5), whereas hermit crabs (P. granosimanus) maintained a similar grazing rate under all pH levels (pH 7.3, 7.5, 7.7, and 7.95). Epiphyte biomass increased more rapidly under extreme OA (pH 7.3 and 7.5), but natural densities of snails and hermit crabs prevented algal overgrowth irrespective of pH treatments. Finally, grazers and acidification additively increased surfgrass productivity and delayed the shoot senescence. Hence, although OA impaired the function of the most abundant consumers (snails), strongly interacting and pH-tolerant species (hermit crabs) largely maintained the top-down pressure to facilitate seagrass dominance. Our study highlights significant within-community variation in species functional and response traits and shows that this variation has important ecosystem consequences under anthropogenic stressors.
... Determining how factors like patch edges and habitat degradation affect faunal predation risk is important not only to better understand the consequences of habitat alteration on population dynamics and ecological interactions, but also due to increasing evidence that top-down processes directly affect the health and persistence of seagrasses (Whalen et al. 2013, Reynolds et al. 2014) and other coastal habitats such as coral reefs (Mumby et al. 2006). Strategies for restoring degraded seagrass habitat may differ depending on whether ecosystem services (nursery habitat provision, carbon and contaminant sequestration, enhanced secondary production, shoreline protection, and others) are more closely tied to edge proximity or to structural complexity, or to other factors. ...
... Higher nutritional content of leaves resulted often in increased consumption rates of herbivores and leaf palatability was observed to be greater under chronic nutrient pollution and in combination with warming and acidification (Jiménez-Ramos et al., 2017;Campbell et al., 2018;Ravaglioli et al., 2018). However, mesograzers (such as small crustaceans) were shown to buffer eutrophication effects by consuming epiphytic algae that would otherwise overgrow seagrass leaves and compete with the plants for light and nutrients Reynolds et al., 2014). We did not measure grazing pressure and/or quantify herbivore communities at SB and NB sites. ...
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Eutrophication is one of the main threats to seagrass meadows, but there is limited knowledge on the interactive effects of nutrients under a changing climate, particularly for tropical seagrass species. This study aimed to detect the onset of stress in the tropical seagrass, Halophila stipulacea, by investigating the effect of in situ nutrient addition during an unusually warm summer over a 6-month period. We measured a suite of different morphological and biochemical community metrics and individual plant traits from two different sites with contrasting levels of eutrophication history before and after in situ fertilization in the Gulf of Aqaba. Nutrient stress combined with summer temperatures that surpassed the threshold for optimal growth negatively affected seagrass plants from South Beach (SB), an oligotrophic marine protected area, while H. stipulacea populations from North Beach (NB), a eutrophic and anthropogenically impacted area, benefited from the additional nutrient input. Lower aboveground (AG) and belowground (BG) biomass, reduced Leaf Area Index (LAI), smaller internodal distances, high sexual reproductive effort and the increasing occurrence of apical shoots in seagrasses from SB sites indicated that the plants were under stress and not growing under optimal conditions. Moreover, AG and BG biomass and internodal distances decreased further with the addition of fertilizer in SB sites. Results presented here highlight the fact that H. stipulacea is one of the most tolerant and plastic seagrass species. Our study further demonstrates that the effects of fertilization differ significantly between meadows that are growing exposed to different levels of anthropogenic pressures. Thus, the meadow's "history" affects it resilience and response to further stress. Our results suggest that monitoring efforts on H. stipulacea populations in its native range should focus especially on carbohydrate reserves in leaves and rhizomes, LAI, internodal length and percentage of apical shoots as suitable warning indicators for nutrient stress in this seagrass species to minimize future impacts on these valuable ecosystems.
Coastal ecosystems such as those in the Great Barrier Reef (GBR) lagoon, are exposed to stressors in flood plumes including low light (caused by increased turbidity) and agricultural pesticides. Photosystem II (PSII)-inhibiting herbicides are the most frequently detected pesticides in the GBR lagoon, but it is not clear how their toxicity to phototrophic species depends on light availability. This study investigated the individual and combined effects of PSII-inhibiting herbicide, diuron, and reduced light intensity (as a proxy for increased turbidity) on the marine diatom, Phaeodactylum tricornutum. Effective quantum yield (EQY) and cell density were measured to calculate responses relative to the controls over 72-h, in tests with varying stressor intensities. Individually, diuron concentrations (0.1–3 μg l⁻¹) were not high enough to significantly reduce growth (cell density), but led to decreased EQY; while, low light generally led to increased EQY, but only reduced growth at the lowest tested light intensity (5 μmol photons m⁻² s⁻¹) after 48-hours. P. tricornutum was less affected by diuron when combined with low light scenarios, with increased EQY (up to 163% of the controls) that was likely due to increased electron transport per photon, despite lesser available photons at this low light intensity. In contrast, growth was completely inhibited relative to the controls when algae were simultaneously exposed to the highest stressor levels (3 μg l⁻¹ diuron and 5 μmol photons m⁻² s⁻¹). This study highlights the importance of measuring more than one biological response variable to capture the combined effects of multiple stressors. Management of water quality stressors should consider combined impacts rather than just the impacts of individual stressors alone. Reducing suspended sediment and diuron concentrations in marine waters can decrease harmful effects and bring synergistic benefits to water quality.
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Intense herbivory can alter habitat characteristics, and grazing on reproductive structures can reduce plant fitness and long-term population stability. Herbivory on seagrasses is often limited to epiphytes; however, direct grazing has been observed recently in several systems. In San Francisco Bay, California, we documented extensive damage to leaves and especially inflorescences of eelgrass Zostera marina concurrent with blooms of the non-native amphipod Ampithoe valida. Field surveys found peaks of A. valida abundance when eelgrass was flowering, and greater abundance on flowering than vegetative shoots, with particularly high abundances on reproductive structures (spathes) in late developmental stages (with ripe fruits or post seed release). Laboratory experiments showed that A. valida consumed leaf and spathe tissue (as well as whole fruits), but usually preferred spathes to leaves. Spathes are structurally complex and likely provide better habitat, increasing opportunity for consumption. Low field algal abundances do not fully explain eelgrass herbivory, as amphipods grazed eelgrass substantially even when offered algae. When presented with eelgrass from both the amphipod's native (Virginia) and invaded range (California), the latter was consumed at significantly higher rates. Neither nutrient nor phenolic content adequately explain the tissue preference. Greater size of California eelgrass may have promoted incidental feeding on spathes used as habitat, but does not explain a California bias during consumption of structurally simple leaves. Field densities and laboratory consumption rates suggest that this non-native amphipod could remove all seeds in a California eelgrass meadow in 1-3 wk, thus challenging maintenance of genetic diversity and long-term meadow persistence.
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Seagrasses provide important habitat for fishes and invertebrates but are declining around the globe, often due to overgrowth by algae. One hypothesis for this overgrowth is that overfishing of top consumers has led to greater numbers of small predatory fishes that reduce the abundance of mesograzers. This trophic cascade hypothesis requires that the same species that control algal biomass are also susceptible to fish predation. While mesograzers are known to vary in their feeding rates on algae and seagrasses, much less is known about variation in predation susceptibility and how this is related to grazing abilities. For 6 common mesograzers from Bodega Harbor, California, USA, we assessed feeding rates on macroalgae (Ulva spp.), epiphytic microalgae, and eelgrass. We then assessed predation susceptibility using juvenile cabezon Scorpaenichthys marmoratus in tanks of eelgrass habitat with and without Ulva. We found that the fastest consumers of all 3 primary producers were the least susceptible to predation. This appeared to be due to predator avoidance strategies; fish consumed visible caprellids at a higher rate than the larger consumers, which were either better camouflaged or able to avoid predation by building tubes within the macroalgae. Using our feeding and predation rates, along with relative abundances from field surveys, we calculated the expected trophic cascade effect with and without grazer species differences. Because fish predation was skewed towards the most abundant but least important (per capita) grazers, incorporating trait variation led to a 50 to 80% reduction in expected trophic cascade effects. Examining other seagrass communities for either similar grazer species or a similar mismatch between feeding rates and predation susceptibility may improve our understanding of the variation in trophic cascade effects across systems.
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Abstract Bergmann's rule-an increase in body size with latitude-correlates with latitudinal declines in ambient temperature and predation risk, but relatively few studies simultaneously explore the relative importance of these factors. Along temperate Atlantic shorelines, the isopod Idotea balthica from high latitudes are 53% longer on average than isopods from low latitudes. When reared at 6°-24°C, juveniles increased growth and development rates with temperature. Because the increase in growth rate with temperature outstripped increases in development rate, female size at maturity increased with temperature. This thermal sensitivity of growth cannot account for the latitudinal pattern in body size. Within temperature treatments, females from low latitudes reached sexual maturity at younger ages and at a smaller size than did females from higher latitudes. This shift in life-history strategy is predicted by latitudinal declines in predation pressure, which we tested using field-tethering experiments. Overall, isopods at low latitudes had a 44% greater mortality risk from daytime predators relative to isopods at higher latitudes. We conclude that a latitudinal gradient in predation risk, not temperature, is principally responsible for Bergmann's rule in I. balthica. Increases in body size during future warming of oceans may be constrained by local patterns of predation risk.
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We characterized the seasonal and interannual variation in macrophytes, epiphytes, invertebrate herbivores, small demersal predators, and physicochemical characteristics of an eelgrass (Zostera marina) bed in Chesapeake Bay, Virginia, over 10 yr, to explore the relative importance of abiotic and biotic forcing on community composition and abundance. Our hypotheses were (1) physicochemical drivers affect community structure directly, (2) bottom-up trophic control is evidenced by positive covariance among trophic levels, (3) top-down control generates inverse patterns of abundance at adjacent trophic levels, and (4) species diversity among herbivores contributes to temporal stability. Composition and abundance of eelgrass-associated species varied strongly among seasons and years. Much of this variation correlated with temperature and salinity anomalies, and multivariate analysis grouped communities roughly by season, supporting our first hypothesis. Severe seagrass loss during the hot summer of 2005 shifted the community toward a novel composition, but community structure rebounded within a year. Evidence for trophic control was mixed: selected taxa showed patterns consistent with top-down or bottom-up control, but these patterns generally disappeared at the level of whole years and entire trophic levels. Our ability to detect trophic effects may have been limited, however, by consumer movement or changing behavioral responses to resource availability and predation. There was also little evidence that diversity stabilized total herbivore abundance. Although consumer effects on lower levels were inconsistent, the strong physicochemical forcing of community structure supports suggestions that eelgrass communities are highly vulnerable to natural and anthropogenic changes in climate and hydrography.
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Recent large-scale seagrass declines have prompted experimental investigations of potential mechanisms. Although many studies have implicated eutrophication or reductions of epiphyte grazers in these declines, few experiments have simultaneously manipulated both factors to assess their relative effects. This study used meta-analyses of 35 published seagrass studies to compare the relative strength of 'top-down' grazer effects and 'bottom-up' nutrient effects on epiphyte biomass and seagrass above-ground growth rate, above-ground biomass, below-ground biomass, and shoot density. A surprising result was that seagrass growth and biomass were limited in situ by sediment nutrients; light limitation has been emphasized in the literature to date. Water column enrichments, which were correlated with increased epiphyte biomass, had strong negative effects on seagrass biomass. Grazers overall had a positive effect on shoot density, but negligible effects on seagrass biomass and growth rate. However, analyzing epiphyte grazers separately from other grazers revealed positive effects of grazing on seagrass response variables and corresponding negative impacts on epiphyte biomass. The positive effects of epiphyte grazers were comparable in magnitude to the negative impacts of water column nutrient enrichment, suggesting that the 2 factors should not be considered in isolation of each other. Until the determinants of epiphyte grazer populations are empirically examined, it will be difficult to address the contribution that overfishing and cascading trophic effects have had on seagrass decline. Because increases in water column nutrients are documented in many regions, efforts to reduce coastal eutrophication are an appropriate and necessary focus for the management and conservation of seagrass ecosystems.
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The effects of predation by fishes, in relation to habitat complexity and periodicity of sampling, on abundances of fishes and macroinvertebrates were investigated using controlled caging experiments during summer 1999/2000 at multiple locations (Blairgowrie, Grand Scenic, and Kilgour) in Port Phillip Bay, Australia. A second experiment evaluated biological and physical cage effects, Sites and habitats, but not caging treatments, could generally be differentiated by the assemblage structure of fishes. Regardless of species, small fishes were generally more abundant in seagrass than unvegetated sand, although the nature of this pattern was site- and time-specific. Depending on the site, abundances of fishes varied between cage treatments in ways that were consistent with neither cage nor predation effects (Grand Scenic), strong cage effects (Kilgour) or strong predation or cage effects (Blairgowrie). The abundance of syngnathids varied inconsistently between caging treatments and habitats within sites through time. Although they were generally more abundant in seagrass, whether or not predation or cage effects were observed depended strongly on the time of sampling. Atherinids and clupeids generally occurred more commonly over seagrass. In this habitat, atherinids varied between cage treatments in a manner consistent with strong cage effects, while clupeids varied amongst predator treatments in a way that could be explained either by cage or predation effects. Macroinvertebrates were closely associated with seagrass, palaemonid shrimps varied little with cage structure, and abundance of cephalopods appeared to be influenced by predation. Neither environmental (particle size and organic content) nor biological (abundances of meiofaunal crustaceans) attributes appeared to be altered by cage structure, but the statistical power of these experiments was sometimes low. Patterns in the abundances of fishes and macroinvertebrates are discussed in relation to predation and cage effects, habitat type, and the time of and location within which experiments were conducted.
“[F]or most of the past 50 My, Caribbean seagrass communities have had to withstand heavy, sustained grazing pressure from several sympatric lineages of large mammalian herbivores. This factor is almost totally absent both from these communities today (wherein manatees are scarce or absent in most areas) and from the thinking of the aquatic botanists and marine ecologistswho study these communities. Consequently, the long-established tenet that seagrass ecosystems are largely detritus-based … must be revised to recognize that the modern situation is anomalous, and that the ‘normal’ pattern throughout most of tropical seagrass history has been that much (probably most) of the primary productivity has been channeled through the guts of herbivores, particularly sirenians.” (Domning, 2001)
We investigated the interaction between epiphyte-grazer abundance and eutrophication to assess the relative importance of top-down and bottom-up effects in subtropical seagrass meadows. In field experiments using a cageless technique to control amphipod abundance, we measured the effects of grazing and nutrient supply on the growth and productivity of shoalgrass Halodule wrightii and its epiphytes at both protected and wave exposed sites. Amphipod removal at the protected site resulted in 70% greater epiphyte loads on shoalgrass leaves and a 36% reduction in leaf biomass after 10 wk. At the wave-exposed site, where amphipod abundance was consistently low, we found no significant effects of grazer presence or nutrients on epiphyte load or leaf biomass. Average leaf length, however, was significantly reduced in nitrogen-enriched plots. Our results indicate that natural densities of amphipods can reduce seagrass loss by controlling epiphytes.
Both natural and managed ecosystems experience large fluctuations in submersed macrophyte biomass. These fluctuations have important consequences for ecosystem processes because of the effects of macrophytes on the physical/chemical environment and littoral biota.The first part of this paper reviews the effects of submersed macrophytes on the physical environment (light extinction, temperature, hydrodynamics, substrate), chemical environment (oxygen, inorganic and organic carbon, nutrients) and the biota (epiphytes, grazers, detritivores, fishes). This extensive literature suggests that variations in macrophyte biomass could have major effects on aquatic ecosystems.The second part of this paper considers the ecosystem consequence of several common changes in submersed macrophytes: replacement of vascular macrophytes by bryophytes during lake acidification; short-term biomass changes caused by invasions of adventive species, cultural eutrophication or macrophyte management; and changes in littoral grazers. These scenarios illustrate the importance of macrophytes in ecosystems, but raise any questions which cannot be answered at present. Controlled, whole-lake macrophyte experiments are needed to resolve these open questions.