biodiversity and food web structure influence short-term accumulation
TRANSCRIPT
Biodiversity and food web structure influence short-term accumulation of sediment
organic matter in an experimental seagrass system
Elizabeth A. Canuel,1 Amanda C. Spivak, Elizabeth J. Waterson, and J. Emmett DuffyVirginia Institute of Marine Science, P.O. Box 1346, Gloucester Point, Virginia 23062
Abstract
We tested the effects of grazer diversity and food chain length on the quantity and quality of accumulatedsediment organic matter (SOM) in experimental eelgrass (Zostera marina) mesocosms. By use of a factorialmanipulation of crustacean grazer species richness and predator presence, we examined the effects of epibenthicconsumers on SOM composition by using stable carbon isotopes (d13C) and lipid biomarker compounds. Grazerspecies composition strongly influenced nearly all measures of SOM quantity and quality. In particular, increaseddensities of the grazing amphipod, Gammarus mucronatus, decreased accumulation of benthic microalgae(chlorophyll a) and the relative abundance of polyunsaturated fatty acids (FA, a proxy for labile algal organicmatter) and branched FA (a proxy for bacterial biomass). On average, increasing grazer species richnessdecreased SOM quantity (percentage of total organic carbon). Increasing food chain length by addition ofpredatory blue crabs (Callinectes sapidus) resulted in a trophic cascade, increasing algal biomass andaccumulation of algal organic matter in sediments, and enhancing the quality of SOM. Concomitantly, therelative proportion of bacterial branched FA increased. The identity and number of epibenthic consumersstrongly influence accumulation and composition of SOM and the pathways by which it is processed, and theseresponses are not easily predictable from bulk measurements (d13C, percentage of total organic carbon) alone.
Benthic ecosystems play an important role in the storageand cycling of organic matter and nutrients. Key variablesinfluencing these processes include animal activities (e.g.,bioturbation, bioirrigation, grazing) and structures (e.g.,burrows, tubes). Animals influence sediment environmentalconditions by controlling the availability of oxygen andother electron acceptors, reworking the sediment, andremoving metabolites (Aller 1982; Lee 1992; Aller and Aller1998). These activities promote degradation of organicmatter, thereby influencing global biogeochemical cyclesand the preservation of organic carbon in marine sediments(Hedges and Keil 1995). Several experimental studies havedemonstrated that marine benthic animal taxa can in-fluence organic matter diagenesis and sediment geochem-istry (Aller and Yingst 1985; Kristensen and Blackburn1987; Sun et al. 1999). However, although these studieshave provided many insights, it is important to recognizethat in nature, animals do not live as single species but asmembers of a community. Thus, it is important tounderstand not only the effects of individual species onsediment biogeochemistry, but also how diverse communi-
ties of interacting species influence sediment geochemicalprocesses.
Understanding the effects of diversity is critical becausehuman activities are currently shifting local and globaldistributions of organisms, and contributing to the sixthmajor extinction event in the history of life (Chapin et al.2000). Because of these drastic changes, a growing empha-sis has been placed on understanding the interactionsbetween biodiversity and ecosystem processes. For exam-ple, studies in terrestrial grasslands have shown thatchanges in species richness and the identity of plants affectecosystem processes such as plant productivity andnitrogen cycling (Hector et al. 1999). In comparison, thepotential impacts of species losses or changing functionaldiversity on biogeochemical processes in marine ecosystemsare poorly known (Covich et al. 2004; Duffy andStachowicz 2006). Marine benthic systems in particularare susceptible to human-induced stressors because speciestend to be sedentary and unable to avoid disturbance.Previous studies have shown that individual taxa oftenhave profound impacts on both the structure of ecosystemsand the rates and pathways of carbon and other importantbioelements (Chapin et al. 2000; Downing and Leibold2002). Yet our understanding of relationships betweenbiodiversity and ecosystem processes in marine systems isstill preliminary (Covich et al. 2004; Duffy and Stachowicz2006).
Recent studies have begun to address this gap. Oneapproach to addressing relationships between diversity andecosystem processes involves the use of simulation/model-ing. Solan et al. (2004), by use of simulation models ofbenthic infauna, concluded that, on average, loss of marinebenthic invertebrate species reduced bioturbation, animportant process influencing sediment oxygen concentra-tions, organic matter diagenesis, and nutrient recycling.These results were driven largely, but not entirely, by the
AcknowledgmentsWe thank J. Paul Richardson for assistance with setting up and
maintaining the mesocosm experiments. We also thank JamesDouglass and Kristin France for sampling assistance at the end ofthe experiment. We thank two anonymous reviewers and BoThamdrup for constructive comments that improved the manu-script. This research was supported by NSF grants OCE 00-99226and OCE 03-52343 to J. Emmett Duffy. Additional support wasprovided by the Virginia Institute of Marine Science anda National Center for Environmental Research (NCER) STARfellowship to Amanda Spivak (EPA grant number FP 91656901).This paper is contribution 2776 of the Virginia Institute of MarineScience, College of William and Mary.
1 Corresponding author ([email protected]).
Limnol. Oceanogr., 52(2), 2007, 590–602
E 2007, by the American Society of Limnology and Oceanography, Inc.
590
presence or absence of the large-bodied burrowing brit-tlestar, Amphiura filiformis, which had a disproportionatelylarge effect. Similarly, a laboratory experiment (Waldbus-ser et al. 2004) demonstrated that the functional diversity ofinfaunal invertebrates influenced pore-water profiles ofoxygen and pH, as well as sediment–water fluxes of oxygenand phosphate. These studies demonstrate that individualspecies often have unique impacts on ecosystem processes,that combinations of species can have complementaryeffects, and that biogeochemical processes often depend onthe identity of benthic species as much as on their aggregatebiomass. Equally importantly, responses to species extinc-tions depend on food web structure because biodiversityand trophic structure influence ecosystem properties in-teractively (Duffy et al. 2005).
Previous studies linking benthic species to sedimentbiogeochemistry have focused primarily on burrowinginfauna. Yet much of the organic matter arriving at thewater–sediment interface first passes through the epifaunalcommunity, or is influenced by its activities, before it isdeposited to sediments. Thus, it is reasonable to expect thatepifaunal and infaunal animal communities influence boththe fate of sediment organic matter (SOM), throughactivities such as bioturbation, as well as the abundanceand quality of the SOM that accumulates. The quantityand quality of SOM are important ecosystem propertiesinfluencing water quality (e.g., bottom-water dissolvedoxygen), distribution of contaminants, and nutrition ofbenthic organisms. At larger scales, degradation of SOMinfluences long-term carbon preservation and cycling(Hedges and Keil 1995). Despite the central importanceof SOM abundance and quality to benthic ecosystems, andongoing trends in changing benthic community structure(Thrush and Dayton 2002), to our knowledge, no study todate has specifically examined how marine biodiversity(which we define broadly to include species composition,richness, and relative abundance) influences SOM compo-sition and abundance.
Here we report results of an experiment examining howbenthic consumer diversity and food chain length influencethe composition of newly deposited (,6 weeks) SOM. Thisarticle complements a previous publication reportingresponses of the above-ground community in the sameexperiment (Duffy et al. 2005). Here, we first aimed tocharacterize the variance among grazer species in theirinfluence on SOM composition and lability. We alsopredicted that predators would decrease grazer effects,thereby increasing the accumulation of algal organic matterthrough a trophic cascade, indirectly enhancing SOMquality. To test these hypotheses, we factorially manipu-lated grazer diversity (species composition and richness)and food chain length (presence/absence of a predator), andmeasured abundance and quality of accumulated SOM,including total organic carbon (TOC), stable isotopes ofcarbon (d13C), and lipid biomarker compounds.
Methods
Experimental design—The experiment factorially crossedtwo food chain lengths with five grazer treatments (Duffy
et al. 2005). We compared a two-level food chain (plants,grazers) with a three-level food chain (plants, grazers,predators). The five grazer treatments included each of fourgrazer species stocked alone, and all four species together,providing two levels of grazer richness (1 and 4 species) andfour one-species treatments. All grazer treatments receivedthe same initial abundance of grazers, following a re-placement series design. Grazers included two amphipodtaxa, ampithoids (a mixture of Cymadusa compta andAmpithoe longimana) and Gammarus mucronatus; and twoisopods, Erichsonella attenuata and Idotea baltica. Thesegrazers, hereafter referred to by genus or family name, areamong the most abundant epifaunal species in localeelgrass beds (Parker et al. 2001; Duffy et al. 2001). Thetreatments with predators included three juveniles of theblue crab (Callinectes sapidus, carapace width 2.0–4.0 cm),an important generalist predator in Chesapeake Bayeelgrass beds (Hines et al. 1990). The control containedneither grazers nor predators. There were five replicatemesocosms of each of the 11 treatments.
The experiment was conducted in May–June 2002 in anarray of 113-liter outdoor mesocosm tanks supplied withflowing water from the York River estuary (Duffy et al.2003, 2005). The water was prefiltered through 150 mmmesh to minimize grazer introductions but allowed passageof microscopic propagules of algae and sessile inverte-brates. Seventy-five defaunated eelgrass shoots wereplanted in clean sand (%TOC was below detection), and80 individual grazers were added to each treatment.Although initial %TOC was low, seagrasses can grow ina wide range (coarse-grained, organic poor- to fine-grained,organic rich) of sediment types (Hemminga and Duarte2000), and the initially uniform TOC levels reduced initialsediment heterogeneity among replicates. The initial grazerdensity was below that which is typical in the field to allowgrazer assemblages to adjust through population growthand competition. Four-species treatments received 20individuals of each grazer species such that all treatments(except grazer-free controls) began with equal totaldensities of grazers. Three juvenile blue crabs were addeda few days later to each predator treatment mesocosm. Theexperiment ran for 6 weeks (one to three grazer genera-tions), long enough for grazer relative abundances to adjustto natural levels and to approach carrying capacity, at leastfor the rapidly growing amphipods (Duffy and Harvilicz2001). The experiment was terminated at 6 weeks to avoidcontamination by nontarget grazers entering via the flow-through seawater system, and because plants were entirelyconsumed in some treatments by that time.
Densities of all the organisms used in our experimentbegan the experiment within the (admittedly wide) range ofabundances found naturally in local eelgrass beds. Crabswere toward the high end of densities observed in local bedsin recent years but are well below densities recordedregularly in recent decades. Grazers began the experimentat relatively low densities and increased greatly in theabsence of crab predators, probably reflecting at leastpartial top-down control in nature. The communities thatdeveloped in treatments containing Gammarus alone orErichsonella alone were most similar to those seen in the
Biodiversity and sediment organic matter 591
field in supporting relatively healthy, unfouled and un-damaged eelgrass.
Bulk SOM—At the termination of the experiment, smallsediment cores (2.6-cm diameter) were collected from threeapproximately equally spaced positions within each meso-cosm tank. The upper 1 cm from each core was removedand these upper sections from the three cores werecombined into a single precombusted (450uC) jar. Thesediment sample was homogenized and aliquots wereremoved to precombusted glass scintillation vials forbenthic chlorophyll a and sediment total organic carbon(TOC) analyses. All samples were frozen immediately aftercollection. Benthic chlorophyll a (a measure of benthicmicroalgal biomass) was determined by the method ofNeubauer et al. (2000). TOC and total nitrogen wereanalyzed by standard methods with a Fisons CHN analyzer(Model EA1108) after removing inorganic carbon (Hedgesand Stern 1984). Acetanilide was used as the standard.d13COC was used to examine whether sources of organiccarbon varied in response to the experimental treatments.The stable carbon isotope ratios of bulk organic carbon(d13C) were determined at the stable isotope facility,University of California, Davis (Cloern et al. 2002). Valuesare reported in the ‘‘d’’ notation as the per-mil (%)difference between the sample ratio and the ratio ofa standard (PeeDee Belemnite):
dð Þ~ Rsample
�Rstandard { 1
� �| 1,000:
The analytical precision of these determinations was
typically about 0.1 per mil for carbon (Cloern et al. 2002).
Lipid biomarker analysis—Sediment samples were ex-tracted with methylene chloride : methanol (2 : 1, v : v) byusing the Bligh and Dyer (1959) method modified foraccelerated solvent extraction. After extraction, the sampleswere partitioned and the organic phase was removed.Hexane was added, the samples were partitioned a secondtime and the hexane layer added to the organic phase. Thecombined organic phases sat over anhydrous Na2SO4
overnight to remove traces of water and were concentratedto 1 mL by turboevaporation (Zymark Turbo Vap 500).
The total lipid extracts were saponified as described inCanuel and Martens (1993). After saponification, theresidue was extracted under basic conditions to yield theneutral fraction (SAP-N). The pH of the saponified residuewas subsequently reduced to 2 with HCl, and the acids wereextracted (SAP-A). The SAP-A fractions were methylatedwith BF3-CH3OH and purified by silica gel chromatogra-phy. The SAP-N fractions were separated into lipidcompound classes (Canuel and Martens 1993). The fractioncontaining the alkanols/sterols was collected and driedunder nitrogen, BSTFA (bis(trimethylsilyl) trifluoroaceta-mide) and acetonitrile were added to each vial, and sampleswere heated in a heating block for 15 min. Just before gaschromatography (GC) injection, samples were dried anda small volume of hexane (50 mL) and the internal standardwere added. Sterols (as trimethylsilyl ethers) were analyzedon a HP 5890 gas chromatograph using a DB-5 column
(30 m 3 0.20 mm inner diameter) and a flame ionizationdetector. Conditions for GC analysis followed previouslypublished methods (Zimmerman and Canuel 2001; Arzayusand Canuel 2005). Peaks corresponding to sterols werequantified by an internal standard, 5a(H)-cholestane,added before GC analysis.
The fatty acids (FA; as methyl esters) were analyzed bygas chromatography following previously published proce-dures (Zimmerman and Canuel 2001 and referencestherein). Peaks were quantified relative to an internalstandard, methyl nonadecanoate, added just before GCanalysis. Peak identities of FA and sterols were verified bycombined gas chromatography–mass spectrometry (GC-MS) with a Hewlett-Packard 6890 GC with a mass selectivedetector operated in the electron impact (EI) mode. FA aredesignated as A : BvC, where A is the total number ofcarbon atoms, B is the number of double bonds, and C isthe position of the first double bond from the aliphatic (v)end of the molecule. The prefixes ‘‘i’’ and ‘‘a’’ refer to isoand anteiso methyl branched FA (see Canuel et al. 1995and references therein).
Statistical analyses—The experiment was analyzed asa fully factorial two-way ANOVA, with fixed factors foodchain length (i.e., presence/absence of crabs, df 5 1), grazerdiversity (df 5 4), and their interaction. The grazer-freecontrol was excluded from statistical analyses becauseabsence of a corresponding control including only crabswould render this analysis nonorthogonal, and because ourprimary interest was how grazer diversity, rather than merepresence of grazers, influenced ecosystem properties. ANO-VAs were conducted on log-transformed data. From theseANOVAs we obtained both F tests of significance andestimates of effect strength (i.e., v2, percentage varianceexplained) for both factors and their interaction. Todistinguish effects of grazer species richness versus grazerspecies composition, we partitioned the grazer diversity SSfrom the ANOVA into two orthogonal components (seeDuffy et al. 2005 for details): (1) a planned contrastcomparing the four-species treatment against all single-species treatments (richness effect), and (2) a plannedcontrast among the four single-grazer treatments (composi-tion effect). When the effect of grazer species richness wassignificant, we also calculated Loreau’s (1998) statistic Dmax,a metric of ‘‘overyielding,’’ which is positive when the diversemixture has a larger value of the response variable than doesany single component species. Dmax is often considereda conservative estimate of whether a greater response ina mixture results from interactions among species (a ‘‘true’’diversity effect), or simply from dominance by a particularlyinfluential species (the ‘‘sampling effect’’).
To explore the influence on SOM of particular grazerspecies in more detail, we conducted multiple regressions ofeach SOM response variable against the log-transformedfinal abundances of each of the four grazer species. To aidin interpreting the biomarker data, we conducted multipleregressions of each SOM response variable against the finalbiomass of each primary producer group. In addition,factor analysis that used principal components analysis wasused to reduce the dimensionality of the data set. The
%
592 Canuel et al.
analysis was conducted by the FA or sterol concentrationsof individual compounds or groups of compounds normal-ized to the sum of all FA (percentage total FA orpercentage total sterols). We included TOC, sedimentchlorophyll a (Chl a), and macroalgal biomass in theanalysis to aid in the interpretation. Data were transformedby the Orthtran/Varimax method (StatView version 5.0.1).Loadings and scores that use the oblique (i.e., nonortho-gonal) solution are presented. The loadings are regressioncoefficients for predicting the relationship between vari-ables and the defined principal components. The scoresexpress relationships between each of the observations andthe identified principal components.
Results
Bulk SOM—Over the course of the 6-week experiment,measurable levels of sediment TOC accumulated in themesocosms, ranging from 0.41 to 3.04 mg g21 dry weightsediment (0.04 to 0.3 %TOC). Both grazer speciescomposition (p , 0.001) and richness (p , 0.035)influenced accumulation of sediment TOC (Fig. 1, Ta-ble 1), together explaining 30% of the variation in TOCcontent (v2 5 0.30), with the diverse grazer mixtures morestrongly reducing TOC accumulation (Fig. 1). Indeed, theoveryielding criterion Dmax (Loreau 1998) was positive forsediment TOC in both absence (Dmax 5 0.083) andpresence of crabs (Dmax 5 0.084), indicating that TOCcontent was more extreme (approximately 8% lower, in thiscase) in the diverse grazer treatment than for any singlegrazer species, a result usually interpreted as indicatinga ‘‘true’’ diversity effect, i.e., an effect of interactionsamong species rather than simply dominance by a particularspecies. Of the single-species grazer treatments, theaccumulation of TOC was lowest in the Gammarus(without crab) treatments and highest in the Idoteatreatments (with or without crab). Because of the shortduration of the experiment, total nitrogen content was low(often below detection) and unaffected by grazer speciescomposition, richness, or predator presence. d13COC valuesranged from 218.42 to 212.55 %, varying significantlyamong grazer species treatments (p , 0.0001), with themost depleted values occurring in the Gammarus treatments(6crab) (Fig. 1). Crab predators significantly enrichedsediment d13C (p , 0.001) (Fig. 1).
Changes in epibenthic food web composition alsoinfluenced the quality of organic matter that accumulated,as evidenced by differences among treatments in accumu-lation of benthic Chl a, a proxy for sediment microalgae(Duffy et al. 2005). On average, increasing grazer speciesrichness significantly reduced the accumulation of sedimentChl a in both the presence and absence of predators. Withthe exception of Erichsonella, individual grazer species eachreduced sediment microalgae in the absence of crabpredation, whereas crabs tended to reduce the impact ofgrazers on sediment microalgae (Fig. 1). Treatmentscontaining Gammarus accumulated the least Chl a (Fig. 1).
FA and sterol biomarker composition—Changes inepibenthic food web composition influenced both the total
abundance (SFA) and composition of FA biomarkers(Table 1, Fig. 2). Grazer species composition stronglyaffected accumulation of SFA (mg g21 dry sediment),explaining 29% of the variation in this variable, whereasgrazer species richness, presence of predatory crab, and thegrazer 3 crab interaction did not (Table 1). In the single-species grazer treatments with crabs, SFA (mg g21 dryweight sediment) ranged from 17.51 6 3.52 (mean 6 SE, n5 5) for ampithoids to 56.47 6 15.38 (mean 6 SE, n 5 5)for Erichsonella. In treatments without crabs, SFA ranged
Fig. 1. Influence of grazer species diversity and presence/absence of crab predator on measures of surface SOM abundance(%TOC) and composition (sediment Chl a and d13C of the organiccarbon). Mean 6 standard error (n 5 5) are presented in this andsubsequent figures. Solid symbols represent treatments with crabs,and open symbols represent treatments without crabs in this andsubsequent figures.
Biodiversity and sediment organic matter 593
from 13.35 6 3.01 (mean 6 SE, n 5 5) mg g21 dry sedimentfor Gammarus to 25.95 6 5.12 (mean 6 SE, n 5 5) mg g21
dry sediment for Erichsonella.Both species composition and richness of grazers
strongly affected relative abundance (percentage totalFA) of short-chain (C12 : 0, C14 : 0, C16 : 0) FA, explaining37% of the variation (Table 1, Fig. 2). The overyieldingstatistic for short-chained FA was negative in both absence(Dmax 5 20.155) and presence of crabs (Dmax 5 20.154),indicating that values in the diverse grazer assemblage didnot exceed those of the most extreme single grazer species,i.e. that the significant richness effect in this case wasprobably attributable to dominance by a particular speciesrather than by interactions among them. Grazer speciescomposition, but not richness, influenced the relativeabundance of branched (iso and anteiso C13, C15, andC17), polyunsaturated (PU) (C18, C20, and C22 PUFA), andlong-chain saturated (C22 : 0-C30 : 0) FA, explaining about20% of the variation in each case (Table 1, Fig. 2).Treatments with crabs had elevated levels of polyunsatu-rated and branched FA (p , 0.01; Table 1), explaining,10% of the variance in each of these variables, andindicating that predation on the mesograzers influenced thequality of carbon accumulating in surface sediments.Sedimentary PUFA appeared to represent labile microalgalmaterial as percentage PUFA was significantly andpositively related to sediment microalgal biomass (Chl a,Table 2). In contrast, percentage of long-chain FA (LCFA)was positively related to macroalgal biomass (Table 2).Percentage of branched FA was positively related tobenthic microalgal Chl a (Table 2), presumably reflectingbacterial response to labile organic matter produced bybenthic microalgae.
Total sterol abundance and sterol composition were alsoinfluenced by grazer species composition (Table 1; Fig. 3).In the single-species grazer treatments, sterol abundanceswere lowest in the Gammarus (no crab) treatment andhighest in the ampithoids (no crab) treatment. Overall, theaccumulation of total sterols (mg g21 dry sediment) waslowest in the ‘‘all species’’ treatment (p 5 0.0018). Cholest-5-en-3b-ol (cholesterol) and 24-ethylcholest-5-en-3b-olwere generally the dominant sterols. 24-Ethylcholest-5-en-3b-ol often showed a pattern opposite to that ofcholesterol. The presence of crab predators and grazerspecies richness had no effect on sterol composition(Table 1).
Principal components 1 and 2 (PC1 and PC2) explained21.5% and 16.5% of the variance, respectively (Fig. 4).Loadings on PC1 were most positive for dinosterol and 24-methylenecholesterol, whereas loadings for all other bio-markers were either near the origin or somewhat negative(e.g., 24-ethylcholesterol, cholesterol, Fig. 4a). PC1 distin-guished between sterols representing a subgroup of micro-algae (represented by dinosterol and 24-methylenecholes-terol) versus other biomarkers. Loadings on PC2 werehighly positive for PUFA and sedimentary Chl a andslightly negative for LCFA, dinosterol and cholesterol(Fig. 4a). BrFA (bacteria) had intermediate positive load-ings on PC2.
Table1.
Tes
tso
fsi
gn
ific
an
cea
nd
esti
ma
ted
ma
gn
itu
des
of
effe
ct(v
2)
of
wit
hin
-tro
ph
icle
vel
div
ersi
ty(g
raze
r),
nu
mb
ero
ftr
op
hic
lev
els
(cra
b),
an
dth
eir
inte
ract
ion
,o
no
rga
nic
bio
ma
rker
con
cen
tra
tio
ns
inse
dim
ents
.
Res
po
nse
Gra
zer
Cra
b(d
f51
)G
raze
r3
cra
b(d
f54
)E
rro
r(d
f53
8–
40
)R
ich
nes
s(d
f51
)C
om
po
siti
on
(df5
3)
MS
pv
2M
Sp
v2
MS
v2
MS
*p
MS
pv
2
Org
an
icC
(%se
dim
ent
dry
ma
ss)
0.0
08
0.0
35
0.0
39
,0
.00
10
.30
0.0
04
0.1
39
0.0
20
.00
20
.27
20
.02
0.0
02
0.6
6T
ota
lN
(%se
dim
ent
dry
ma
ss)
0.0
00
0.7
92
0.0
00
.0
.10
0.0
10
.00
00
.78
80
.00
0.0
00
0.1
67
0.0
60
.00
00
.95
To
tal
FA
s(m
gm
g2
1d
ryse
dim
ent)
72
0.4
80
0.1
64
2,5
65
.68
0,
0.0
01
0.2
93
8.5
60
0.7
45
0.0
02
17
.85
60
.66
00
.00
35
9.0
60
0.7
5%
PU
FA{
31
.03
90
.26
44
61
.23
0,
0.0
05
0.2
12
29
.15
10
.00
40
.11
46
.91
10
.12
20
.05
24
.15
50
.64
%C
20
-C2
2P
UF
A7
.13
20
.57
81
91
.40
0,
0.0
01
0.2
78
7.5
95
0.0
57
0.0
45
8.9
55
0.0
51
0.0
82
2.7
12
0.6
2%
bra
nch
edF
A1
.33
70
.13
78
.35
2,
0.0
10
.19
4.3
75
0.0
09
0.1
00
.12
20
.93
10
.00
0.5
80
0.7
6%
lon
g-c
ha
inF
A0
.06
40
.92
23
2.9
00
,0
.00
50
.20
1.0
34
0.6
82
0.0
05
.86
10
.43
90
.00
6.0
87
0.8
2%
sho
rt-c
ha
inF
A8
55
.77
90
.04
21
,68
4.2
20
,0
.00
10
.37
14
.27
90
.78
80
.00
7.8
94
0.9
97
0.0
01
94
.51
30
.70
To
tal
ster
ols
(ng
mg
21
dry
sed
imen
t)2
1,0
18
,25
20
.00
24
5,5
06
,95
4,
0.0
01
0.3
94
,41
9,7
93
0.1
32
0.0
21
,32
9,2
72
0.5
89
0.0
01
,86
6,0
86
0.6
1%
bra
ssic
ast
ero
l0
.00
80
.97
71
4.6
45
.0
.10
0.0
11
1.5
43
0.2
90
0.0
07
.47
10
.56
60
.00
10
.00
41
.00
%d
ino
ster
ol
2.9
86
0.0
34
69
.43
6,
0.0
01
0.7
10
.43
10
.40
80
.00
0.2
42
0.8
12
0.0
00
.61
60
.31
%st
igm
ast
ero
l5
.97
40
.39
22
.53
2.
0.7
50
.00
9.5
72
0.2
80
0.0
02
.57
80
.86
10
.00
7.9
80
1.0
0%
cho
lest
ero
l1
.27
70
.81
17
7.5
00
,0
.02
50
.10
72
.28
30
.07
80
.03
72
.22
40
.02
10
.13
22
.04
00
.74
%2
4-m
eth
yle
nec
ho
lest
ero
l7
.33
70
.16
52
7.1
05
,0
.00
10
.27
2.9
43
0.3
75
0.0
07
.71
00
.09
90
.06
3.6
53
0.6
7%
24
-eth
ylc
ho
lest
ero
l4
7.9
30
0.2
21
48
4.9
00
,0
.00
10
.46
44
.63
40
.23
70
.01
39
.25
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Scores on PC1 were most positive for Idotea (with crabs)and Gammarus (with crabs), and most negative for theampithoid treatments (6crabs) (Fig. 4b). PC2 providedresolution between samples with crabs versus thosewithout; treatments without crabs generally plotted in thenegative region of PC2. With the exception of Ericsonella,the treatments with crabs (Fig. 4b, solid symbols) had morepositive values than the corresponding treatments withoutcrabs (Fig. 4b, open symbols). The Control (no crab)treatment was positive for both PC1 and PC2, differingfrom all other grazer (no crab) treatments and indicatingdifferences in the composition of SOM accumulating intreatments with grazers versus those without.
Multiple regressions suggested that grazing amphipods(ampithoids and, especially, Gammarus mucronatus) wereindirectly responsible for most of the trends in SOMquantity and composition (Table 3). Across all treatments,final abundance of Gammarus was negatively correlatedwith sediment microalgal biomass (Chl a), %TOC, d13C,total FA, total sterols, percentage PUFA, and percentagebranched FA. Gammarus abundance correlated positivelywith percentage long-chain FA. Ampithoids influencedseveral of the SOM parameters but often in the oppositedirection to Gammarus. Ampithoid abundance correlatedpositively with %TOC, d13C, and %PUFA, but negativelywith total FA and several sterols. In contrast, abundancesof the isopods, Idotea and Erichsonella, were correlatedwith few of the SOM variables.
Discussion
SOM sources—Seagrass plants help internalize nutrientcycles within the seagrass ecosystem by producing andtrapping detritus and dissolved organic matter (Phillips andMenez 1988). Previous studies (e.g., Holmer and Nielsen1997; McGlathery et al. 1998; Dudley et al. 2001) haveshown that seagrasses can profoundly affect the chemicaland microbiological characteristics of sediments throughproduction and burial of detritus, altering fluxes of O2,DOM release from roots and rhizomes, and nutrientconsumption, and by supporting diverse biogeochemicallyactive benthic invertebrates (Moriarty and Boon 1989).Seagrass influence on such processes can greatly alter thequality of organic matter available to benthic organismsand rates of organic matter degradation by detritus-basedand herbivore food webs (Boschker et al. 2000).
In addition to the well-recognized influence of seagrasseson sediment biogeochemistry, there is a wealth of evidencethat epibenthic grazers and predators can have strong andfar-reaching effects on the biomass, composition, andproductivity of seagrass communities (van Montfrans etal. 1984; Hughes et al. 2004). It therefore stands to reasonthat such consumer impacts may also cascade down toaffect organic matter dynamics in seagrass ecosystems. In
Fig. 2. Influence of grazer species diversity and presence/absence of crab predator on FA composition of surface sediments.FA groupings are expressed relative to total FA abundance.Long-chain FA (C22 : 0-C30 : 0) reflect contributions from higherplants/macroalgae, short-chain FA (C12 : 0-C16 : 0) derive primarilyfrom aquatic (algal and microbial) sources, polyunsaturated FA
r
(PUFA) represent labile, algal-derived sources, and branched (isoand anteiso) FA reflect contributions from heterotrophic bacteria(see text for additional details pertaining to source assignments).
Biodiversity and sediment organic matter 595
this study, we showed experimentally that the structure ofthe epibenthic animal community strongly influenced theabundance and quality of organic matter accumulating inseagrass sediments, mirroring similarly strong impacts ofthe epibenthic community on above-ground variables in thesame experiment (Duffy et al. 2005). Specifically, speciescomposition of epibenthic grazers strongly affected nearlyall response variables measured. Changes in food chainlength (presence or absence of predators) had less pervasiveeffects on sediment geochemistry, but significantly influ-enced both lability of deposited organic matter (percentagePUFA) and contributions from heterotrophic bacteria(percentage branched FA). These latter results suggest thatthe enhanced biomass of macro- and epiphytic microalgae,shown previously to result from cascading impacts of crabpredation in this same experiment (Duffy et al. 2005), arealso reflected in short-term accumulation of labile organicmatter in the sediments and enhanced response of bacteria.
Bulk SOM measurements (benthic Chl a, d13C) and lipidbiomarker compounds indicate that the grazer communityprimarily influenced the accumulation of algal andbacterial sources of organic matter, as opposed to vascularplant sources, over the timeframe of the experiment.Accumulation of short-chain FA (C12 : 0-C16 : 0) dominatedover long-chain FA (C22 : 0-C30 : 0), consistent with micro-algal and/or bacterial sources of organic matter. Toevaluate the relative contributions of higher plant (i.e.,eelgrass) versus algal/microbial sources, we calculatedratios of long-chain FA (normally considered to beassociated with vascular plants) to short-chain FA (bacte-ria, algae) by using the terrestrial to aquatic ratio (TARFA)developed by Meyers (1997). Across all treatments, themean 6 SD TARFA was 0.09 6 0.12, supporting thedominance of microbial sources. However, unlike othervascular plants, long-chain FA are not abundant in Z.marina, the only vascular plant source in our study (Canuelet al. 1997) and accordingly were not correlated with the
final biomass of Z. marina. Interestingly, long-chain FAwere strongly positively correlated to total macroalgalbiomass, and more specifically to biomass of the red algaPolysiphonia (r2 5 0.24; p , 0.0001 and r2 5 0.27; p ,0.0001, respectively), the dominant macroalga in thisexperiment (J.E. Duffy et al. unpubl. data). This suggeststhat the dominant macroalga may be the source of thelong-chain FA accumulating in the surface sediments andthat its FA composition should be further investigated.Trace levels of long-chain FA have been found previouslyin diatoms (Volkman et al. 1980). Additionally, long-chainFA may derive from incoming estuarine water. Althoughlarge detritus and grazers were removed by prefiltrationthrough 150 mm mesh, microscopic propagules and smalldetritus from the adjacent estuary could enter themesocosms.
Even-numbered polyunsaturated FA (percentage C16-C22 PUFA) are considered proxies for ‘‘fresh’’ algalmaterial (Canuel and Martens 1993 and references therein).Supporting this generalization, the relative abundance ofPUFA (percentage PUFA) was positively correlated withsediment microalgal biomass (Chl a) (r2 5 0.10; p 5 0.011)(Table 2). These variables also had strong loadings on PC2and plotted in the same region of the PC2 versus PC1biplot, indicating that they were influenced similarly by thegrazer treatments (Fig. 4a). Because these proxies (percent-age PUFA and sediment Chl a) derive from the labilefraction of SOM, we interpret factor 2 as an index forseparating the most labile sources of organic matter fromother SOM sources. Iso and anteiso branched FA areconsidered biomarkers for some groups of bacteria (Gillanand Johns 1986; Kaneda 1991; Boschker et al. 2000).Branched FA were positively correlated with sediment algalbiomass (r2 5 0.15; p 5 0.002), suggesting that thesecompounds represent bacteria associated with the sedimentmicroalgal community or that the sediment bacterialcommunity is responding to the availability of labile (algal)
Table 2. Results of multiple regression of sediment organic matter variables against final biomass of primary producer groups.Results are from stepwise regressions with threshold for entry and removal from model at p 5 0.05. Regressions also included epiphyticmicroalgae, diatom mat biomass, and cyanobacterial biomass as independent variables but these were never significant. Responsevariables are percentage of total FA or percentage of total sterols, unless otherwise noted. Only statistically significant (p,0.05) resultsare reported.
Grazer
Sediment microalgae Macroalgae Zostera Total
Coefficient Partial r2 Coefficient Partial r2 Coefficient Partial r2 Model r2
Total organic C (% sediment dry mass) 20.003 0.075 0.075d13C (per mil) 1.539 0.160 20.057 0.105 0.265Total FA (mg mg21 TOC)% PUFA 5.871 0.115 0.115% branched FA 1.002 0.166 0.166% long-chain FA 0.181 0.259 0.259% short-chain FATotal sterols (mg mg21 TOC) 1.456 0.083 20.112 0.106 0.188% brassicasterol% dinosterol 0.127 0.155 0.155% stigmasterol% cholesterol% 24-methylenecholesterol 0.110 0.129 0.129% 24-ethylcholesterol
596 Canuel et al.
organic matter. Like PUFA and sediment Chl a, BranchedFA had positive loadings on PC2, consistent with theirassociation with labile SOM (Fig. 4a). Interestingly, con-tributions of both the sediment microalgal biomarkers(PUFA) and bacterial biomarkers (branched FA) weresignificantly enhanced by adding predatory crabs (Table 1),
Fig. 3. Influence of grazer species diversity and presence/absence of crab predator on sterol composition of surfacesediments. Sterol biomarkers are expressed relative to total sterolabundance. 24-Methylenecholesterol is derived primarily fromdiatoms, dinosterol represents contributions from dinoflagellates,
r
and cholesterol is the dominant sterol found in crustaceans. 24-Ethylcholesterol is the dominant sterol in Z. marina but is alsopresent in algae and cyanobacteria at trace levels. See text foradditional details pertaining to source assignments.
Fig. 4. Results from principal components analysis (PCA)showing loadings and scores for the two dominant principalcomponents (PC) that together explain 38% of the variance. (a)Loadings for fatty acid and sterol biomarkers. Sterols arepresented as letters: C 5 cholesterol; B 5 brassicasterol; E 524-ethylcholesterol; D 5 dinosterol; M 5 24-methylenecholes-terol. Fatty acid abbreviations are given in the text. (b) Mean 6SE of PCA scores for grazer treatments. Con 5 control; Amp 5ampithoids; Eri 5 Ericsonella; Gam 5 Gammarus; Ido 5 Idotea;All 5 all grazers. Open symbols represent grazer treatmentswithout crabs, gray symbols represent treatments with crabs, andblack hexagon represents control. Generally, the treatments withcrabs (gray symbols) have more positive scores on PC2 than thecorresponding treatments without crabs (open symbols).
Biodiversity and sediment organic matter 597
mirroring the enhancement of sediment algal biomass viathe trophic cascade described previously (Duffy et al. 2005).This is consistent with the hypothesis that crabs inhibitgrazer activities, leading to accumulation of labile SOMand is illustrated by the results from the principalcomponents analysis and our interpretation that PC2resolves between SOM components on the basis of theirlability (Fig. 4). With the exception of Erichsonella, thetreatments with crabs (solid symbols) had more positivevalues than the corresponding treatments without crabs(open symbols), which generally plotted in negative regionof PC2.
Compounds derived from microalgal, vascular plant,and crustacean sources dominated the sterol biomarkers.Dominating the sterol distribution was cholesterol (Fig. 3),the most abundant sterol in crustaceans, but which alsooccurs at low levels in many microalgae (Volkman 1986).Sterols, such as 24-methylenecholesterol and brassicasterol,are biomarkers for diatoms and other species of microalgae(Volkman 1986), and comprised 15–22% of the total steroldistribution (Fig. 3). Dinosterol, a sterol derived fromdinoflagellates (Volkman 1986), made up a smaller portionof the sterol distribution (generally ,5% total sterols).Interestingly, the diatom sterols were not correlated tosediment Chl a. This suggests that these sterols may derivefrom epiphytes or phytoplankton or that benthic micro-algal communities contained substantial densities of non-diatom microalgae, such as dinoflagellates and/or cyano-bacteria. Alternatively, the reactivity of Chl a may begreater than for sterol biomarkers; thus, Chl a may reflect‘‘fresher’’ algal material, whereas the sterols may reflecta mixture of fresh and detrital algae. This is consistent withthe results from the principal components analysis showingresolution between labile compounds such as PUFA andsediment Chl a versus most of the sterols (Fig. 4a).
Traditionally, 24-ethylcholest-5-en-3b-ol, 24-ethylchol-est-5,22-dien-3b-ol (stigmasterol), and 24-methylcholest-5-
en-3b-ol (campesterol) have been used as biomarkers forhigher plants (Volkman 1986). Previous work identified 24-ethylcholest-5-en-3b-ol as the dominant sterol in Z. marina(Canuel et al. 1997). However, these so-called plant sterolscan occur in algae as well (Volkman 1986; Volkman et al.1998). In our study, 24-ethylcholest-5-en-3b-ol was abun-dant in surface sediments but varied considerably in itsrelative abundance (12–43% total sterols). This compoundwas not correlated with final biomass of total algae, Z.marina, or sediment Chl a, suggesting that it may bederived from a mixture of sources or by a source (e.g.,cyanobacteria) not evaluated in our study.
Together, the biomarker results indicate that the SOMpool was dominated by contributions from microalgae andbacteria. This contrasts with field studies where seagrassdetritus has been shown to accumulate in the sedimentsassociated with seagrass beds (Hemminga and Duarte2000). However, this aspect of our results may reflect theshort timeframe of our experiment (6 weeks), under whichit seems reasonable to expect a dominant influence oforganisms with shorter response times (microbes). Recentwork has shown that microalgae can be a major source ofSOM in seagrass beds, often driving microbial degradationprocesses (Boschker et al. 2000; Kennedy et al. 2004).Despite the clear responses in the microbial biomarkers, wedo not believe that the accumulation of SOM reflects onlythe benthic microbial community response. In subsequentmesocosm experiments and complementary field studies wehave examined the abundance of both phospholipid-linkedFA and total FA in both natural and experimental seagrassbeds. Phospholipid-linked FA should reflect contributionsfrom viable microbial biomass (microalgae and bacteria),while total FA should reflect contributions from bothviable biomass and detritus. From this work, we find thatphospholipid-linked FA comprise approximately 10% oftotal FA in the mesocosms and 3–27% in natural seagrassbeds (Spivak, unpubl. data). These data suggest that our
Table 3. Results of multiple regression of sediment organic matter variables against log abundance of grazer species. Results arefrom stepwise regressions with threshold for entry and removal from model at p 5 0.05. Response variables are percentage of total FA orpercentage of total sterols, unless otherwise noted. Only statistically significant relationships (p , 0.05) are reported.
Grazer
Gammarus Ampithoids Idotea Erichsonella Total
Slope r2 Slope r2 Slope r2 Slope r2 r2
Sediment Chl a 20.115 0.188 0.188Total organic C (% sediment dry mass) 20.013 0.078 0.014 0.087 0.165Total N (% sediment dry mass)d13C (per mil) 20.482 0.198 0.411 0.177 0.375Total FA (mg mg21 TOC) 24.274 0.068 24.483 0.090 0.158% PUFA 22.275 0.218 1.378 0.093 0.311% branched FA 20.230 0.142 20.160 0.063 0.205% long-chain FA 0.787 0.153 0.153% short-chain FATotal sterols (mg mg21 TOC) 20.522 0.144 20.485 0.069 0.213% brassicasterol% dinosterol 20.553 0.252 0.252% stigmasterol% cholesterol 21.207 0.084 2.035 0.169 0.253% 24-methylenecholesterol 20.477 0.078 0.078% 24-ethylcholesterol 2.952 0.311 22.504 0.121 0.432
598 Canuel et al.
experiments likely influence both the accumulation ofmicrobial biomass as well as detritus. Future experimentsshould examine the influence of epibenthic food webstructure on the accumulation of SOM and sedimentbiogeochemistry at longer timescales.
Influence of the epibenthic animal community on SOM—Previous studies have shown that responses of marinebenthic ecosystems to species loss can vary considerablywith species identity because different species often exertunequal effects on benthic processes (Emmerson et al. 2001;Duffy et al. 2001; Solan et al. 2004). Furthermore,ecosystem-level responses to species extinctions also dependon the trophic level from which species are lost (Duffy et al.2005). A goal of our study was to elucidate how speciesidentity and richness of epibenthic grazers, and ofpredators, influenced accumulation of SOM. We hypoth-esized that individual grazer species would influence theaccumulation of SOM differentially as a result in knowndifferences in feeding modes, mobility, and vulnerability topredators (Duffy and Hay 2000; Duffy and Harvilicz 2001;Duffy et al. 2005). G. mucronatus is highly mobile and feedson a variety of algal sources, including epiphytes, benthicmicroalgae, and macroalgae (Duffy and Harvilicz 2001), aswell as on detritus. In contrast, C. compta is a relativelysedentary, tube-building amphipod that lives on theseagrass blades and appears to feed primarily on epiphytes.The isopod E. attenuata also feeds primarily on epiphyticmicroalgae, whereas the isopod I. balthica feeds onmicroalgae, macroalgae, seagrasses, and even on juvenilesof other grazers (Duffy et al. 2001; Bostrom and Mattila2005). Both isopods are strongly depressed by crabpredation, whereas the amphipods are much less affected(Duffy et al. 2005). Thus, grazer species composition islikely to influence biomass and species composition ofprimary producers and, by extension, quality, and quantityof organic matter delivery to sediments.
We used multiple linear regression analysis to examinerelationships between the final grazer abundance andmeasures of SOM abundance and quality (Table 3). Over-all, Gammarus and ampithoids had the largest number ofstatistically significant relationships with TOC and mea-sures of SOM composition (Table 3). In particular,Gammarus abundance was negatively related to sedimentChl a, %PUFA (a measure of labile, algal-derivedmaterial), and %BrFA (a measure of biomass of hetero-trophic bacteria). We suspect that this dominance of SOMeffects by the two amphipods (Fig. 1, Table 3) reflects theirhigh mobility and the habit, apparently unique toGammarus among the grazer species we studied, of feedingat the sediment surface. The negative effect of Gammaruson benthic microalgae also appeared to influence othercompartments of SOM, notably decreasing the abundanceof labile organic matter, including PUFA, in surfacesediments. Presumably in response to this decline in labileorganic matter availability, contributions from heterotro-phic bacteria (percentage branched FA) were also reducedby grazing amphipods. These findings are consistent withresults from freshwater aquatic systems where litter de-composition and process rates were found to vary in stream
microcosms with species identity and functional feedinggroups (Jonsson and Malmqvist 2003). At the same time,Gammarus increased abundance of the macroalga Poly-siphonia sp. in our experiment (Duffy et al. 2005), whichappears to explain the positive relationship betweenGammarus abundance and long-chain FA (Table 3).
In contrast to Gammarus, ampithoids increased TOC,%PUFA, and 24-ethylcholest-5-en-3b-ol, and negativelyaffected many of the sterol biomarkers (Table 3). Theampithoids are relatively sedentary, build tubes on theeelgrass blades, and graze on both epiphytes and macro-algae (although they also eat eelgrass when algal food is inshort supply; Duffy et al. 2003). Thus, we expected them tohave little impact on the accumulation of benthic micro-algae, consistent with higher %PUFA and TOC found inthe surface sediments. Interestingly, however, we found nosignificant relationship between ampithoids and benthicChl a. Instead, the strongest positive relationship wasbetween ampithoids and %24-ethylcholest-5-en-3b-ol, thedominant sterol in Z. marina (Canuel et al. 1997) but alsopresent in some microalgae and cyanobacteria (Volkman1986). Together, these results are congruent with previousstudies (Duffy and Harvilicz 2001) showing that subtledifferences in diet between grazer taxa can result insubstantial differences in biomass and composition of algaeand other components of the fouling assemblage onmacrophytes. These, in turn, influence the abundance andquality of SOM.
Trophic level influences on SOM—Most previous studiesexploring potential effects of diversity on ecosystemproperties have been limited to a single trophic level,precluding examination of the full range of bottom-up andtop-down effects (Duffy 2002; Covich et al. 2004). Yet theeffects of declining biodiversity surely differ depending onthe trophic level of the species lost and its influence onadjacent (horizontal) trophic levels. Moreover, the effectsof changing diversity within a trophic level can be stronglyinfluenced by food chain length and vice versa (Duffy et al.2005). Further exploration of how diversity at differenttrophic levels affects ecosystem-level properties, includingbiogeochemistry, is needed to develop a predictive frame-work for understanding consequences of species loss andfor effective environmental policies for managing coastalecosystems (Duffy 2002; Solan et al. 2004).
A primary goal of our study was to elucidate how effectsof individual grazer species on the accumulation of SOMwere influenced by the presence/absence of predators. Wefound two parameters (percentage PUFA and percentagebranched FA) for which both grazer composition and thepresence/absence of crabs significantly influenced SOMcomposition (Table 1). The presence of predatory crabsgenerally enhanced accumulation of %PUFA, a measure oflabile, algal organic matter. In these same treatments, therewas a coincident increase in percentage of branched FA,a measure of sediment heterotrophic bacterial biomass.These data suggest the presence of a trophic cascade inwhich crabs reduce the effects of grazers either throughpredation or by inhibiting their activities (Duffy et al.2005). As a result, algal material accumulates at the
Biodiversity and sediment organic matter 599
sediment surface, leading to an increase in bacterialbiomass (percentage branched FA). Previous studies haveshown that bacteria respond to the availability of labileorganic matter at the sediment surface (Canuel andMartens 1993). In this case, crabs promote algal biomassaccumulation (Duffy et al. 2005), and presumably alsoaccumulation of labile organic matter in sediments, byinhibiting the effects of grazers. These results imply thatfood web structure and diversity can influence not only theaccumulation of bulk organic matter but also the pathwaysby which the SOM is processed. In the absence of crabs,algal material is processed by epibenthic grazers, reducingthe amount deposited to the sediments; while in thepresence of crabs, grazers are inhibited, algal materialaccumulates in the surface sediments, and there appears tobe a response by sediment microbes.
Our findings present several intriguing contrasts withthose of previous studies testing effects of grazer diversityand food chain length on the epibenthic community in thissystem. First, previous research suggested complementarityamong grazers, i.e., that differences among species infeeding or other activities resulted in higher grazer biomassyield or more efficient feeding in diverse grazer mixturesthan in any single monoculture (Duffy et al. 2003, 2005).Second, grazer diversity interacted with food chain length(predator presence) to influence several components of theabove-ground community in the same experiment discussedin this paper (Duffy et al. 2005). In contrast, we found thatgrazer effects on SOM were dominated by one or bothamphipod species (Table 3) and that there were fewinteractions between the ‘‘horizontal’’ (grazer speciescomposition and richness) and ‘‘vertical’’ (food chainlength) components of diversity (Table 1). We suspect thatthe apparent inconsistency between studies stems from thefact that only a subset of these grazers interact substantiallywith the sediment. Previous work (Duffy et al. 2001, 2003,2005) showed that all of the crustacean grazers in thissystem strongly influence epiphytic algae, and most alsohave strong, but divergent, impacts on macroalgae and oreelgrass. These disparate impacts on above-ground primaryproducers and fouling invertebrates resulted in the com-plementary effects reported previously (Duffy et al. 2003).In contrast, sediment microalgal and SOM characteristicswere affected almost exclusively by the ampithoid andGammarus amphipods (Table 3). Interestingly, it is thesesame amphipods that were largely unaffected by predationin the previous experiment (Duffy et al. 2005), explainingwhy we found few significant interactions between pre-dators and grazer diversity on SOM characteristics(Table 1). The strong effects of amphipods (especiallyGammarus) on SOM characteristics highlight a previouslyunappreciated role of grazer diversity in this system,namely that a grazer with little impact on above-groundmacrophytes nevertheless strongly influences sediment-associated algae and organic matter.
There is another inconsistency between this and previousstudies that is more difficult to explain, however. Duffy etal. (2003) found that sediment organic carbon actuallyincreased with increasing grazer species richness, a curiousfinding suggested to reflect greater microalgal biomass
growing on the well-lit sediment surface where diversegrazer assemblages had denuded much of the macroalgaeand eelgrass. In direct contrast, we found that sedimentorganic carbon was lowest in the diverse grazer treatment(Fig. 1, Table 1). Although we cannot definitively resolvethe discrepancy between the experiments, we suspect thatthe lower sediment organic carbon at high grazer diversityis likely to be the more typical pattern in this system,reflecting intense grazing on sediment microalgae in thediverse grazer assemblages, in which most edible epiphyticand macroalgae had already been consumed by the end ofthe experiment.
In summary, our data indicate that benthic consumerspecies composition and food chain length stronglyinfluenced the composition of newly deposited (,6 weeks)SOM. Invertebrate grazer species influenced SOM compo-sition and lability differentially as a result of differences infeeding preferences, mobility, and microhabitat use. Inparticular, the generalist grazer-detritivore, Gammarusmucronatus, negatively affected accumulation of sedimentmicroalgae, thereby influencing the accumulation andavailability of sediment labile organic matter. Crabpredators decreased grazer impact through a trophiccascade, thereby indirectly increasing the accumulation ofalgal organic matter, indirectly enhancing SOM quality andsediment bacterial response. Results from this studyillustrate that not only bulk biomass but also speciescomposition and trophic structure of the epibenthiccommunity can strongly influence SOM accumulation,with implications for the accumulation of sediment carbonand the pathways by which carbon is processed.
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Received: 16 December 2005Accepted: 16 August 2006Amended: 6 October 2006
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