top-down control of epifauna by ﬁshes enhances seagrass

Ecology, 93(12), 2012, pp. 2746–2757� 2012 by the Ecological Society of America

Top-down control of epifauna by fishes enhances seagrass production

LEVI S. LEWIS1

AND TODD W. ANDERSON

Department of Biology and Coastal and Marine Institute, San Diego State University, 5500 Campanile Drive, San Diego,California 92182-4614 USA

Abstract. Predators can influence the structure and function of ecosystems by altering thecomposition or behavior of herbivore communities. Overexploitation of predators, therefore,may lead to habitat loss by altering important top-down interactions that facilitate habitat-forming species. In seagrass beds, top-down control of algal growth by mesograzers appears tofacilitate seagrass production. The indirect consequences of higher-order trophic interactions,however, remain unclear. Although predators may limit the beneficial effects of algalmesograzers, it is also possible that they limit the abundance of invertebrates that consumeand foul seagrasses. We used experimental enclosure and exclosure cages to explore the directand indirect effects of microcarnivorous fishes on epifaunal invertebrates, epiphytic loads, andseagrass growth in a natural eelgrass (Zostera marina) bed in San Diego Bay, California, USA.Contrary to expectations, when fishes were excluded, invertebrate abundance increased by300–1000%, fouling on eelgrass leaves increased by 600%, and eelgrass production declined by50%. Despite high densities of predators in enclosures, subsequent effects did not differ fromambient conditions. When predators were excluded, however, abundances of epifauna(including tube-building crustaceans and an eelgrass-grazing limpet) increased dramatically,resulting in reduced seagrass production. Our results are supported by several studies ofeelgrass communities in the northeastern Pacific, characterized by coastal upwelling, inverseestuaries, and a voracious seagrass-consuming limpet. These strong, positive, indirect effectsof microcarnivores on seagrass production contrast with the beneficial mesograzer paradigm,highlighting the need for hypotheses to be tested across a variety of ecosystems with varyingbiophysical characteristics.

Key words: amphipods; epifauna; epiphytes; indirect effects; mesograzers; microcarnivores; predation;San Diego Bay, California, USA; seagrass; Tectura; trophic cascade; Zostera marina.

INTRODUCTION

The indirect effects of predators on the structure and

function of ecosystems has been a key focus of

ecological inquiry for over half a century (Hairston et

al. 1960, Paine 1980, Oksanen et al. 1981). Despite much

research and debate over the prevalence and strength of

trophic cascades in nature (Strong 1992, Pace et al. 1999,

Polis et al. 2000, Schmitz et al. 2000), it is clear that

strong indirect effects of predators are common features

in a variety of ecosystems, including terrestrial, aquatic,

and marine habitats (Terborgh and Estes 2010). The

indirect effects of predators on producers, however,

remain complex and difficult to predict. For example,

the indirect effects of predators on vegetation in African

savannas are complex given that only smaller herbivores

(e.g., zebras) are under strong predation pressure,

whereas megaherbivores (e.g., elephants) are controlled

by bottom-up processes (Sinclair et al. 2007). In

cordgrass-dominated salt marshes, predatory swimming

crabs exert strong, positive, density-mediated indirect

effects on cordgrass performance and persistence (Silli-

man and Bertness 2002); however, the trait-mediated

effects of other ambushing crabs on cordgrass may

actually be negative (Griffin et al. 2011). These examples

highlight the complexity of predator effects in natural

systems and the importance of experimentally reexam-

ining predictions regarding the indirect effects of

predators on dominant vegetation.

The prevalence and strength of trophic cascades in

benthic marine ecosystems (Heck and Valentine 2007)

have gained much attention given that many marine

foundation species (Dayton 1972), and the ecosystems

they construct, are in rapid global decline (Alongi 2002,

Steneck et al. 2002, Pandolfi et al. 2003, Gedan et al.

2009, Waycott et al. 2009). One likely mechanism

contributing to observed losses are the pervasive

human-induced changes in trophic dynamics. For

example, by loading ecosystems with nutrients and

removing entire trophic levels through overexploitation,

the dynamics under which these ecosystems have

evolved are being systematically altered (Jackson et al.

2001, Lotze et al. 2006).

Manuscript received 9 January 2012; revised 19 April 2012;accepted 8 May 2012; final version received 29 May 2012.Corresponding Editor: J. J. Stachowitz.

1 Present address: Center for Marine Biodiversity andConservation, Scripps Institution of Oceanography, Univer-sity of California, San Diego, 9500 Gilman Drive, MC 0208,La Jolla, California 92093-0208 USA.E-mail: [email protected]

2746

The effects of herbivores and their predators on

foundation species may vary widely in marine habitats,

depending strongly on the identity of dominant, habitat-

forming species and associated grazers. In temperate

rocky reefs, robust macroalgae (e.g., kelps) often serve

as dominant, habitat-forming species, whereas in coral

reefs and seagrass beds, fleshy algae appear to compete

with habitat-forming corals and seagrasses for light,

nutrients, and space (Sand-Jensen 1977, Hauxwell et al.

2001, McCook et al. 2001). In kelp forests, both

macrograzers (e.g., urchins) and mesograzers (e.g.,

amphipods) reduce the growth and extent of habitat-

forming kelps, and their predators indirectly benefit

kelps (Estes and Palmisano 1974, Davenport and

Anderson 2007). In contrast to kelp forests, algal

grazers in coral reefs and seagrass beds are thought to

facilitate the dominance of habitat-forming corals and

seagrasses by limiting algal growth (van Montfrans et al.

1984, Steneck 1988, McCook et al. 2001, Hughes et al.

2007), and their predators are thought to suppress this

beneficial effect (Williams and Heck 2001, Mumby et al.

2007). Fishes and urchins appear to be the most

important algal grazers on coral reefs (Steneck 1988,

Carpenter 1997), whereas small crustaceans and gastro-

pods appear to fill this role in seagrass beds (Kitting et

al. 1984, Orth and van Montfrans 1984, Jernakoff et al.

1996).

In seagrass ecosystems, the effects of mesograzers on

algal biomass appear equivalent and opposite to the

effects of nutrient enrichment, suggesting that meso-

grazers should be able to regulate algal biomass and

facilitate seagrass dominance (Hughes et al. 2004). In

many cases, however, mesograzers are unable to control

algal production, and it is thought that this could be due

to high abundances of their predators (i.e., micro-

carnivores) due to the overfishing of top predators

(Williams and Heck 2001, Heck and Valentine 2006).

For example, the loss of top predators may result in an

overabundance of their prey (microcarnivores) which, in

turn, may suppress mesograzer populations. In light of

widespread and well-documented losses of top predators

from marine ecosystems due to overfishing (Pauly et al.

1998, Jackson et al. 2001, Myers and Worm 2003), this

‘‘food web alteration hypothesis’’ has gained much

attention.

The majority of evidence supporting this hypothesis,

however, is limited to lower trophic levels (Orth and van

Montfrans 1984, Jernakoff et al. 1996), and the few

studies examining tri-trophic cascades in seagrass beds

have provided limited direct evidence for strong

cascading effects of small predators on seagrass perfor-

mance (Heck et al. 2000, Duffy et al. 2005, Heck et al.

2006, Douglass et al. 2007, Moksnes et al. 2008, Persson

et al. 2008). Furthermore, many epifaunal invertebrates

are known to graze directly on seagrasses (Fishlyn and

Philips 1980, Williams and Ruckelshaus 1993, Short et

al. 1995, Zimmerman et al. 2001, Duffy et al. 2003,

Fredriksen et al. 2004, Douglass et al. 2007, Brearley et

al. 2008, Rueda et al. 2009, Farlin et al. 2010) or grow

epiphytically and foul seagrass leaves (Sewell 1996,Colmenero and Lizaso 1999, Duffy and Harvilicz 2001,

Douglass et al. 2007), thus complicating the predictedeffects of their predators on seagrass performance. The

ultimate consequences of microcarnivores in seagrassbeds, therefore, remain unknown. For example, micro-carnivores may indeed limit algal mesograzers as

suggested by the food web alteration hypothesis, butthey may also be important in suppressing epifauna that

consume and foul seagrass leaves, thus facilitatingseagrass growth and persistence (Fig. 1A, B).

We tested the indirect effects of small predators(microcarnivorous fishes) on the growth of eelgrass

(Zostera marina) in a continuous eelgrass bed in SanDiego Bay, California, USA. We used a field-based

caging experiment consisting of predator enclosures,exclosures, and two controls. According to the beneficial

mesograzer paradigm, we would expect elevated abun-dances of microcarnivorous fishes to reduce mesograzer

abundances, subsequently leading to an increase in algalbiomass and a reduction in eelgrass production (Fig.

1A). Removal of microcarnivorous fishes would havethe opposite effect, enhancing mesograzer abundance,

reducing epiphytic loads, and increasing rates of eelgrassgrowth. Alternatively, removal of microcarnivorousfishes could result in reduced eelgrass growth due to

increases in seagrass-harming invertebrates (Fig. 1B).

METHODS

Experimental design

Field manipulations of predators were conducted in

the shallow (mean depth, 2 m) subtidal interior of a 173

100 m eelgrass bed that lies parallel to the southwest

shore of Shelter Island in San Diego Bay, California,USA (Appendix A). Twenty-four circular plots (1 m

diameter) were established 3 m apart along a transectthat bisected the eelgrass bed parallel to shore. Four

treatments (predator enclosure, P; predator exclosure,NP; cage control, C; and open plot, O; Fig. 1C) weredeployed in a complete, randomized block design

consisting of six blocks. Predator enclosures andexclosures were used to observe how invertebrate

assemblages, epiphytic loads, and eelgrass productionresponded to high and low densities of microcarnivorous

fishes, respectively, relative to ambient conditions (openplots). Cage controls (full cages with 15% of the mesh

area removed at the base to provide access to fishes)were used to evaluate any caging artifacts (Dayton and

Oliver 1980, Steele 1996). Cages were constructed of a 1m diameter cylindrical polyvinyl chloride (PVC) base

with a 0.63 0.63 1.5 m PVC pipe frame covered in clear6-mm plastic mesh (Fig. 1D) and did not appear to

significantly affect temperature, light, or flow (AppendixB: Fig. B3, Table B2). Enclosures received four dwarfperch (Micrometrus minimus) and two kelp bass (Para-

labrax clathratus) with total lengths of 97.5 6 8.3 mmand 91.7 6 11.3 mm (mean 6 SD), respectively

December 2012 2747FISHES, EPIFAUNA, AND SEAGRASS

(Appendix B). These two species were chosen to

represent two different gape sizes, and the densities used

reflected their relative abundances and were within the

upper range of microcarnivorous fishes observed in the

field (Appendix B: Fig. B1). Fishes were collected by

beach seine from a nearby seagrass bed on the same

morning that treatments were deployed.

The experiment began on 29–30 May 2007, with

subsequent eelgrass and invertebrate sample collections

on 6–8 and 9–11 July (six weeks) and 20–22 and 23–25

August (12 weeks), respectively. Prior to cage installa-

tion, the initial density and height (maximum) of

eelgrass were measured (Appendix C), initial eelgrass

and invertebrate samples collected, and all conspicuous

fishes and macroinvertebrates removed from each plot.

To assess the effectiveness of fish manipulations, 17

visual scuba surveys of all experimental plots were

conducted over the course of the experiment, and fish

density, biomass, and diversity (H0) were quantified

(Appendix B). Cages were scrubbed three times weekly

to remove any fouling organisms.

Abundance, biomass, and diversity of invertebrates

Seagrass-associated invertebrates (i.e., epifauna) were

collected from each plot using a 370-cm2 eelgrass grab

sample, strip-rinsed from the eelgrass onto a 500-lmsieve, and fixed in 10% buffered formalin (Appendix D).

Epifauna were later transferred to 70% ethanol,

identified to family according to Carlton (2007), and

measured to the nearest 1.0-mm total length. The

biomass (blotted wet mass) of major invertebrate groups

was calculated using length–mass relationships devel-

oped in the lab (Appendix E: Table E2). Prior to

analyses, invertebrate abundance and biomass were

standardized to eelgrass biomass for each sample.

Family diversity of invertebrates was calculated for each

plot using the Shannon index (H0).

Epiphytic load and chlorophyll content

The mass and characteristics of all fouling material

(plant, animal, and other) on eelgrass leaves (i.e.,

‘‘epiphytic material’’) were evaluated in each plot for

the three sampling periods (initiation, six weeks, 12

weeks). Epiphytic material was collected using a glass

microscope slide to scrape both sides of the third leaf

from each of five haphazardly selected mature eelgrass

shoots within each plot (Heck et al. 2006). Conspicuous

epifauna were removed from the leaf surface prior to

processing. Epiphytic material was scraped onto a piece

of aluminum foil, weighed to the nearest 0.01-mg wet

mass, and frozen at �208C. Samples were thawed and

extracted in 10 mL of 95% ethanol, and total chlorophyll

was calculated from absorbance measurements using a

Beckman DU640 spectrophotometer (Beckman Coulter,

Brea, California, USA; Appendix C). Remaining

epiphytic material was then isolated, dried at 608C for

48 h, and weighed to the nearest 0.01 mg. The length and

width of each scraped leaf were measured to the nearest

FIG. 1. Potential indirect effects of predators on eelgrass (Zostera marina) production at Shelter Island, San Diego Bay,California, USA, given (A) the food web alteration hypothesis (negative effect), and (B) predator regulation of harmful epifauna(positive effect). Solid arrows denote negative direct effects, dashed arrows represent indirect effects, and font size representsrelative abundance. Note that some epifauna may belong to multiple categories (foulers, algae grazers, and seagrass [SG] grazers).(C) Schematic representations of experimental treatments and (D) cage design with densities of microcarnivorous fishes(Paralabrax clathratus, Micrometrus minimus) used in predator treatments.

LEVI S. LEWIS AND TODD W. ANDERSON2748 Ecology, Vol. 93, No. 12

centimeter and millimeter, respectively, and leaf area

was calculated as twice the product of these dimensions.

Total chlorophyll was calculated as the chlorophyll

density of epiphytic material standardized to the scraped

area of each eelgrass leaf (lg/cm2), representing the per-

area microalgal biomass on seagrass leaves. Epiphytic

load was calculated as the dry mass of postextract solid

material standardized to total leaf area (mg/cm2),

representing the per-area total fouling mass on seagrass

leaves. Chlorophyll content was calculated as the

chlorophyll density of epiphytic material standardized

to the dry mass of extracted material (lg/mg), repre-

senting the proportional contribution of algae to total

epiphytic loads.

Eelgrass growth

Eelgrass growth was measured at the beginning,

middle, and end of the experiment using the hole-punch

method (Short and Duarte 2001). Fourteen days prior to

collection, five mature shoots were haphazardly selected

from a predetermined region within each plot and

loosely tagged using a cable tie with 10 cm of attached

red ribbon. The shoots were each hole-punched at the

leaf bifurcation using a 20-gauge hypodermic needle,

collected 14 days later in individual 3.8-L plastic storage

bags, and transported to the lab on ice.

At the lab, the length and width of the third leaf of

each shoot was measured and the leaf subsequently

scraped of all epiphytic material. For each leaf, both

total length and length of elongation (as determined by

the location of holes) were measured to the nearest

centimeter. Leaf elongation was calculated by summing

the lengths of new growth for all leaves within a shoot

and averaging these values for each plot. For each shoot,

all old (plus sheath) and new leaf material was dried at

608C for 48 h and weighed to the nearest 0.1 mg.

Seagrass growth (biomass) was analyzed as both leaf

production (dry mass new growth) and specific leaf

production (percent new growth) for each shoot.

Analyses

We used one-way blocked analysis of variance

(ANOVA) to evaluate differences among treatments in

measures of fishes, invertebrates, epiphytic loads, and

the structural complexity and growth of eelgrass. Prior

to analyses, Levene’s and Kolmogorov-Smirnov tests

were employed to evaluate variance homogeneity and

normality, respectively. When necessary, data were

log10(x)-transformed to meet the assumptions of

ANOVA. Tukey’s HSD multiple comparison tests were

used to explore pairwise comparisons. All parametric

statistics were conducted using SYSTAT, version

12.01.01 (SYSTAT Software, Chicago, Illinois, USA).

To evaluate differences in the composition of inver-

tebrate assemblages among treatments, Bray-Curtis

similarities were calculated using fourth-root-trans-

formed total count and biomass data for each family.

Differences in invertebrate assemblages were examined

using nonmetric multidimensional scaling (MDS) ordi-

nation, and analysis of similarity (ANOSIM) was usedto test the significance of observed differences in

community composition. Similarity percentage (SIM-PER) analysis was used to identify the most influential

taxa accounting for observed differences among treat-ments. ANOSIM, SIMPER, and MDS analyses were all

conducted using Primer, version 5.2.9 (PRIMER-E,Lutton, Ivybridge, UK).

RESULTS

Effectiveness of treatments

Scuba-based visual surveys indicated that predator

manipulations were effective (Fig. 2A, B; Appendix B).Densities of microcarnivorous fishes observed in cage

control and open plots (ambient conditions) were similarto estimates from beach seine collections, while densities

in predator enclosures were elevated by �300%, anddensities in exclosures were reduced by ;30% relative to

ambient densities. Entrance of a few small (,60 mm)juvenile giant kelpfish (Heterostichus rostratus) and

dwarf perch slightly elevated overall numerical densitiesof fishes in predator exclosures; however, these wereimmediately removed upon observation, and it is

unlikely that these small recruits had an appreciableeffect on epifauna abundances. The very low biomass of

fishes observed in predator exclosures further supportedthis assertion, indicating a 90% reduction relative to

ambient conditions (Fig. 2B). The occasional observa-tion of large (.200 cm) spotted sandbass (Paralabrax

maculatofasciatus) in cage control plots elevated fishbiomass within these treatments; however, these obser-

vations were excluded because they were rare, and thebass did not appear to affect the behavior or abundance

of microcarnivores in cages (Appendix B). Shannonindex values indicated that diversity of fishes was

greatest in open and cage control plots and lowest inboth fully caged treatments (Fig. 2C).

Abundance, biomass, and diversity of invertebrates

A total of 93 541 invertebrates belonging to 11 phylaand �70 families were collected over the course of thisstudy (Appendix D). No significant differences in

invertebrate abundance, biomass, or diversity werefound among treatments at initiation of the experiment

(Table 1). In addition, no differences in these metricswere ever observed between open plots and cage

controls, indicating that cages themselves did not affectinvertebrate assemblages. After six weeks, however, we

observed strong effects of predator manipulations on theabundance, biomass and diversity of epifauna (Table 1).

Post hoc comparisons showed that final (12-week)invertebrate abundance and biomass were 200–1000%greater in exclosure plots relative to treatments exposedto predators (Fig. 2D, E). Invertebrate diversity, how-

ever, was approximately twofold higher in treatmentswith access to ambient predators (open and cage

control) relative to both fully caged treatments (Fig.


2F). Spatial differences (block effects) in invertebrate

abundance and diversity were observed at initiation butwere no longer detected after six weeks.

Nonmetric multidimensional scaling (MDS) plots

based on abundance (Fig. 3A–C) and biomass (Fig.

3D–F) revealed substantial overlap initially but showed

strong dissimilarity between predator exclosures and all

other treatments after six weeks, which persisted to theend of the experiment. Results of ANOSIM analyses

(Appendix F) on invertebrate abundance and biomass

FIG. 2. (A) Abundance, (B) biomass, and (C) diversity of microcarnivorous fishes (60–200 mm total length) observed inexperimental plots, and final effects of predator manipulations on measures of (D–F) invertebrates, (G–I) epiphytes, and (J–L)eelgrass growth. Measures are meansþ SE. Treatments (x-axis) are predator (P; enclosure), no predator (NP; exclosure), open (O;unmanipulated), and caged control (C). Lowercase letters above bars indicate treatments separated by Tukey’s HSD post hocanalyses (P , 0.05). Pairwise comparisons for panels (D), (F), and (G) are based on 95% bootstrapped (n ¼ 100) confidenceintervals due to significant departures from parametric assumptions.


indicated no significant differences in invertebrate

community composition at the beginning of the

experiment, whereas strong differences (P , 0.001) were

detected at six weeks and at the end of the experiment.

Based on numerical abundance, ischyrocerid amphipods

accounted for much of the differences among treatments

(Appendix F: Table F1). Based on biomass, acmaeid

gastropods, columbellid gastropods, and ischyrocerid

amphipods were the most influential taxa contributing

to differences among treatments, with caridean shrimps

and ampeliscid amphipods making up the remaining

most influential groups (Appendix F: Table F2). Mean

biomass of key invertebrate groups (revealed by

SIMPER analyses) confirmed that predator release

(exclosures) resulted in high biomass of many groups,

including ischyrocerid amphipods, acmaeid gastropods,

and hippolytid shrimps (Fig. 3G–I).

Epiphytic load and chlorophyll content

No initial differences in measures of epiphytic

material were observed among treatments, and total

chlorophyll (per cm2 leaf area) of epiphytic material

never differed significantly among treatments through-

out the experiment (Table 1). After six weeks, however,

treatments differed greatly in epiphytic loads (dry mass

per cm2 leaf area) and chlorophyll content (total

chlorophyll per g extracted material), and after 12

weeks, predator exclusion resulted in ;600% greater

TABLE 1. Results of one-way blocked ANOVAs testing the effects of experimental manipulations at the beginning of theexperiments (‘‘Initial’’) and at 6 weeks and 12 weeks on measures of epifauna, epiphytic loads, and eelgrass (Zostera marina)growth in an eelgrass bed at Shelter Island, San Diego Bay, California, USA.

Taxa, metric,and factor

Initial 6 weeks 12 weeks

SS F P r2 SS F P r2 SS F P r2

Invertebrates

AbundanceTreat 0.089 0.19 0.179 0.660� 2.839 25.86 ,0.001 0.858� 3.453 15.14 ,0.001 0.764�Block 0.374 4.71 0.009 0.475 2.60 0.069 0.245 0.65 0.669Error 0.238 0.549 1.141

BiomassTreat 12.051 0.04 0.989 0.227 1.335 15.86 ,0.001 0.771� 1.124 12.99 ,0.001 0.743�Block 431.405 0.86 0.531 0.087 0.62 0.689 0.123 0.86 0.532Error 1508.922 0.422 0.432

Fam. div. (H’)Treat 0.029 0.53 0.671 0.530 7.772 57.88 ,0.001 0.924 0.899 9.32 0.001 0.673�Block 0.285 3.07 0.042 0.378 1.69 0.198 0.094 0.59 0.711Error 0.279 0.671 0.483

Epiphytes

Mass (dry)Treat 0.025 0.19 0.905 0.536� 0.436 3.53 0.041 0.541� 1.654 8.49 0.002 0.688�Block 0.757 3.36 0.031 0.293 1.42 0.272 0.490 1.51 0.245Error 0.676 0.617 0.974

Total chl.Treat 0.046 0.30 0.824 0.497� 0.040 1.20 0.344 0.660� 0.124 1.77 0.195 0.595�Block 0.707 2.78 0.057 0.282 5.12 0.006 0.390 3.34 0.032Error 0.762 0.165 0.351

Chl. contentTreat 0.110 0.77 0.530 0.251 5.830 7.23 0.003 0.637 1.430 16.51 ,0.001 0.784�Block 0.130 0.55 0.739 1.243 0.93 0.492 0.115 0.99 0.454Error 0.714 4.029 0.346

Eelgrass

Lf. elongationTreat 0.012 0.87 0.479 0.350� 5.928 0.53 0.680 0.127 44.462 5.37 0.010 0.587Block 0.024 1.09 0.404 2.226 0.12 0.986 14.400 1.00 0.428Error 0.066 55.842 41.373

Lf. productionTreat 0.028 1.29 0.315 0.637� 0.034 1.86 0.180 0.637� 21 521.011 5.31 0.011 0.587Block 0.163 4.48 0.011 0.127 4.14 0.015 7 291.126 1.08 0.411Error 0.103 0.092 20 263.669

Sp. lf. prod.Treat 0.013 1.11 0.376 0.428� 55.134 2.37 0.111 0.530 159.396 5.34 0.011 0.613Block 0.031 1.58 0.226 76.048 1.96 0.143 77.366 1.56 0.232Error 0.058 116.229 149.257

Notes: Statistics, including sums of squares (SS), and coefficient of determination (r2) values are provided. P values ,0.05 are inbold. Abbreviations are: Treat, treatment; chl, chlorophyll; Fam. div., family diversity; H0, Shannon index; Sp. lf. prod., specificleaf production.

� Data were log10(x)-transformed for analysis.


mass and 70% lower chlorophyll content of epiphytic

loads relative to all other treatments (Fig. 2G, I, Table

1). At initiation, spatial variation (block effect) in

epiphytic loads was observed but was not detectable

after six weeks. Total chlorophyll varied spatially (block

effect) at six weeks but at no other time.

Eelgrass habitat complexity and leaf production

Initial density and height of eelgrass shoots were 371.8

6 86.2 shoots/m2 and 131.1 6 14.1 cm (mean 6 SD),

respectively, and did not differ among blocks or

treatments (Appendix C). No differences among treat-

ments in any measures of eelgrass performance were

observed during the initial and six-week sample periods

(Table 1). After 12 weeks, however, mean leaf elonga-

tion, leaf production, and specific leaf production were

37.7%, 45.5%, and 22.4% lower, respectively, in predator

exclosures relative to all other treatments (Fig. 2J–L,

Table 1). Spatial variability (block effect) in leaf

production was observed initially and at six weeks;

however, this disappeared after 12 weeks.

DISCUSSION

Grazing and predation in benthic ecosystems

We found that removal of microcarnivorous fishes

increased the abundance of invertebrates that consume

and foul eelgrass leaves, resulting in reduced eelgrass

production. Thus first-order predators exerted positive

indirect effects on habitat-forming seagrasses. These

results align the trophic dynamics of seagrass beds with

those in many other ecosystems. For example, positive

effects of predators on dominant macrophytes have been

observed in a variety of ecosystems, including grassland

and shrub habitats (Schmitz et al. 2000), boreal forests

(Berger et al. 2001, Ripple and Beschta 2006, 2007), kelp

FIG. 3. Multidimensional scaling (MDS) plots based on Bray-Curtis similarity matrices of (A–C) abundance and (D–F)biomass of eelgrass-associated invertebrate taxa at initial, 6-week, and 12-week collections. (G–I) Biomass of three influential taxaat 12 weeks. For MDS plots, distances between points indicate relative dissimilarities in community composition of epifauna.Symbols represent predator (P; open triangles), no predator (NP; solid triangles), open (O; gray squares), and cage control (C; graydiamonds) treatments. (G–I) Final responses, based on mass (mean þ SE) of (G) Erichthonius brasiliensis, a tube-buildingamphipod, (H) Tectura depicta, a seagrass-grazing limpet, and (I) Hippolyte californica, a hippolytid shrimp, to experimentaltreatments, exemplifying predator release of invertebrates in exclosure plots (NP) relative to other treatments.


forests (Estes and Palmisano 1974, Sala and Graham

2002, Davenport and Anderson 2007), rocky intertidal

shorelines (Paine 1980, Menge 2000), salt marshes

(Silliman and Bertness 2002), and coral reefs (O’Leary

and McClanahan 2010). Our study is novel, however, in

challenging previous models of seagrass trophic dynam-

ics that suggest a negative indirect effect of micro-

carnivores on seagrass production.

Seagrass-damaging invertebrates

Although the majority of studies examining the effects

of mesograzers on seagrasses have focused on species

that feed on algae and therefore benefit seagrasses

(Kitting et al. 1984, van Montfrans et al. 1984, Jernakoff

et al. 1996), a number of other studies have documented

negative impacts of mesograzers on seagrasses. For

example, the isopod Limnora agrostisa is known to

burrow into seagrass shoots, feeding on meristems and

causing leaf malformation and defoliation (Brearley et

al. 2008), and damage to eelgrass leaves by other

crustacean mesograzers has been observed in the lab

and field (Williams and Ruckelshaus 1993, Short et al.

1995, Duffy and Harvilicz 2001, Duffy et al. 2003,

Douglass et al. 2007). Furthermore, large increases in

the natural abundance of seagrass-associated gastro-

pods, such as Rissoa mebranacea (Fredriksen et al. 2004)

and Tectura depicta (Zimmerman et al. 2001), have

resulted in strong negative effects on eelgrass via

destructive grazing, and several other marine gastropods

are known to graze directly on seagrass tissues (Fishlyn

and Phillips 1980, Rueda et al. 2009).

Studies in the northeast Pacific have demonstrated

that the common acmaeid limpet Tectura depicta exacts

strong negative effects on eelgrass growth and persis-

tence (see Plate 1). For example, a population explosion

of T. depicta in Monterey Bay, California, USA,

corresponded with a 50% loss of eelgrass habitat

(Zimmerman et al. 2001). Laboratory experiments

revealed that T. depicta, though removing ,10% of

total shoot biomass, reduced eelgrass growth rates,

carbon reserves, root proliferation, and net photosyn-

thesis by 50–80% (Zimmerman et al. 2001). A strong

negative relationship between the abundance of T.

depicta and eelgrass production was also observed in

Bahia San Quintin Baja California, Mexico (Jorgensen

et al. 2007), suggesting that T. depicta has strong effects

on seagrass production throughout its range.

Our experiment was conducted geographically be-

tween these two previous studies, also demonstrating a

strong negative relationship between T. depicta abun-

dance and eelgrass production, with a 50% reduction of

eelgrass growth in predator exclosures where T. depicta

biomass was 500% above ambient levels. Interestingly,

the maximum densities of limpets (350 limpets/m2) and

corresponding lowest eelgrass growth rates (3

mg�d�1�shoot�1) observed in our predator exclosure

treatments were both nearly identical to those observed

in San Quintın Bay, where limpet abundance alone

explained 42% of the variation in eelgrass growth rates

(Jorgensen et al. 2007). Although we could not directly

quantify grazing, we did observe conspicuous scars on

eelgrass leaves within predator exclosures, characteristic

of grazing by T. depicta (Zimmerman et al. 2001).

Examination of stomach contents indicated that both

predators in our study (kelp bass and dwarf perch)

consumed T. depicta. Therefore, predation by fishes on

T. depicta is a likely mechanism contributing to the

strong positive indirect effects of fishes observed in our

experiment.

In addition to direct grazing, epifauna can harm

seagrasses by fouling leaves and blocking the absorption

of light and nutrients with their bodies or tube masses.

Sessile bryozoans, tunicates, and cnidarians are known

to settle and grow on seagrass leaves (Colmenero and

Lizaso 1999, Duffy and Harvilicz 2001, Douglass et al.

2007) and may have strong negative effects on seagrass

performance (Sewell 1996). The most abundant epifau-

na (especially in predator exclosures) were amphipods of

the family Ischyroceridae (e.g., Erichthonius spp. and

Jassa spp.; see Plate 1). These amphipods are known to

foul substrates by constructing sediment tubes from

which they filter or graze (Coyer 1979, Chapman 2007).

When we excluded predators, populations of these

amphipods (and other tube-building species) increased

dramatically, resulting in extensive tube mats attached

to eelgrass leaves. The mass, appearance, and texture of

epiphytic material from predator exclosures were all

unique compared to those observed in other treatments,

indicating that sediment tube masses were likely a large

fraction of these epiphytic loads. Therefore, reduction of

eelgrass-fouling epifauna likely also contributed to the

positive effects of fishes on eelgrass production.

Predation intensity

Our experimental design was effective in manipulating

the abundance and biomass of microcarnivorous fishes.

Visual observations revealed predator biomass to be

elevated by 400% in enclosures and reduced by 90% in

exclosures relative to ambient conditions. Despite large

differences in observed predator abundance and bio-

mass, however, predator enclosures and access treat-

ments were similar in their effects on invertebrates,

epiphytic loads, and eelgrass growth. Possible explana-

tions for this include agonistic interactions between

enclosed predators, a low threshold of predation

necessary to exert positive effects, and similar predation

intensities among treatments due to either increased

predator diversity or detection avoidance by fishes in

open plots (Appendix B). Further experimentation is

needed to examine the relative effects of predator

density and diversity in this system.

Biophysical setting

The consequences of species interactions can be

strongly affected by the biophysical setting (Sanford

and Bertness 2009). In seagrass beds, for example,


elevated water temperatures in late summer may result

in physiological stress, making seagrasses more suscep-

tible to direct grazing and fouling (Neckles et al.1993,

Sewell 1996). Furthermore, summer peaks in inverte-

brate production are common (e.g., Neckles et al. 1993,

Valiela et al. 1997), and when combined with low

summer algal productivity, may lead to increased direct

grazing upon live seagrass tissues (Williams and

Ruckelshaus 1993). Field observations of increased

direct consumption of eelgrass leaves by epifauna in

regions of lower productivity support this view (Jorgen-

sen et al. 2007).

Large-scale geographic variation in biophysical con-

ditions may also influence species interactions (Sanford

and Bertness 2009). For example, high nutrient loadings

in positive estuaries like Chesapeake Bay, USA (Kemp

et al. 1997), may favor algal epiphyte production and

algivory, whereas lower nutrient loadings in inverse

estuaries such as Shark Bay, Australia (Smith and

Atkinson 1983), and San Diego Bay, USA (Delgadillo-

Hinojosa et al. 2008), may favor direct consumption of

eelgrass (because algae are less available). Furthermore,

heterotrophic estuaries in upwelling regions (e.g., San

Diego Bay) may support greater abundances of filter

feeding (i.e., fouling) epifauna relative to autotrophic

bays (e.g., Shark Bay) due to higher inputs of particulate

matter. Such strong differences among seagrass ecosys-

tems make them conducive to comparative experiments

(e.g., Menge et al. 2002) that explore how species

interactions vary across regions with different biophys-

ical characteristics.

It is possible, therefore, that peak summertime water

temperatures and epifauna densities, combined with low

water-column nutrients, all may have contributed to the

strength of the negative effects of epifauna on eelgrass

production. Our study was conducted in the outer

portion of San Diego Bay, characterized by relatively

low year-round water-column nutrients (dissolved inor-

ganic nitrogen [DIN], 0.73–2.95 lmol/L) compared to

Chesapeake Bay where DIN peaks of 5–16 lmol/L at

the mouth, and upwards of 100 lmol/L inside the bay,

are common (Delgadillo-Hinojosa et al. 2008). Although

San Diego Bay temperatures peak in August, the outer

bay remains ;228C, significantly lower than the inner

bay where thermal stress is thought to occur for

seagrasses. It is important to note, however, that our

results are supported by several other studies in cooler

and more nutrient-rich regions, indicating that our

conclusions are likely robust.

CONCLUSIONS

We found that microcarnivorous fishes promote

seagrass performance by suppressing seagrass-harming

epifauna. Although our study was limited in space and

time, given the wide-scale distribution of Tectura

depicta, fouling organisms, and their predators; our

results likely reflect key trophic interactions character-

istic of seagrass habitats throughout central, southern,

and Baja California. Given that seagrass-harming

epifauna have been described from a number of

ecosystems around the globe, it is possible that such

interactions are common, but overlooked, features of

seagrass ecosystems in general. Our findings suggest that

PLATE 1. (A) Tectura depicta and (B) grazing scars on an eelgrass leaf characteristic of feeding by T. depicta. Note that only athin central strip of chlorophyll-rich epidermis remains on the leaf. (C) Erichthonius brasiliensis (a fouling amphipod) and (D)associated sediment tubes coating an eelgrass leaf. Photo credits: L. S. Lewis.


an abundant and diverse community of microcarnivores

may provide stability to seagrass beds.

Although the importance of epifauna in seagrass beds

has been well documented, previous research on trophic

dynamics has focused on the role of predators in limiting

the effectiveness of beneficial mesograzers. Our results

are novel in demonstrating positive indirect effects of

microcarnivores on seagrass performance, challenging

the generalization that epifauna promote, and their

predators reduce, seagrass production. These unexpect-

ed results demonstrate the need for manipulative field

experiments that examine the direct and indirect effects

of predators in natural seagrass beds across a variety of

environmental conditions, thus providing a more

complete picture of how these ecosystems function.

ACKNOWLEDGMENTS

We thank K. Hovel, S. Schellenberg, J. Hobbs, andanonymous reviewers for providing helpful comments thatgreatly improved the manuscript. We also thank the manystudents and volunteers who provided extensive field andlaboratory support for this project, especially A. Deza, C.Galst, K. O’Connor, C. Jones, E. Floyd, E. Moore, R.Mothokakobo, S. Fejtek, V. Norrell, L. Foley, G. Fellman, J.Silveira, J. Farlin, L. Segui, A. del Pino, A. Rogers, A. Tregre,R. Carlton, L. Neyman, S. McGinty, and S. Strauss. K. Hovel,M. Edwards, K. Kim, R. Hughes, S. Williams, J. Zimmer, andD. Lipski provided useful input into study design, and L. Thurnassisted with chlorophyll and nutrient analyses. This projectwas supported by the San Diego State University M.S. EcologyProgram and by grants to L. S. Lewis from the Unified Port ofSan Diego, the PADI Foundation, and the Southern CaliforniaAcademy of Sciences, and to T. W. Anderson from the UnifiedPort of San Diego. This is Contribution No. 20 of the Coastaland Marine Institute Laboratory, San Diego State University.

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SUPPLEMENTAL MATERIAL

Appendix A

Description of the study site in San Diego Bay (Ecological Archives E093-255-A1).

Appendix B

Fish collections, cage design, and treatment integrity (Ecological Archives E093-255-A2).

Appendix C

Seagrass structural complexity and chlorophyll analysis of epiphytic loads (Ecological Archives E093-255-A3).

Appendix D

Invertebrate collections (Ecological Archives E093-255-A4).

Appendix E

Length–mass relationships for fishes and invertebrates (Ecological Archives E093-255-A5).

Appendix F

Tables from ANOSIM and SIMPER analyses (Ecological Archives E093-255-A6).


top-down control of epifauna by ﬁshes enhances seagrass

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