Widdicombe 2001 - The Interaction Between Physical Disturbance and Organic Enrichment

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Limnol. Oceanogr., 46(7), 2001, 17201733q 2001, by the American Society of Limnology and Oceanography, Inc.

The interaction between physical disturbance and organic enrichment: An importantelement in structuring benthic communities

Stephen Widdicombe1

Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, United KingdomPlymouth Environmental Research Centre, (Department of Biological Sciences), University of Plymouth, Drake Circus,Plymouth, PL4 8AA, United Kingdom

Melanie C. AustenPlymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, United Kingdom

Abstract

The interaction between physical disturbance and organic enrichment, with respect to its effect on the diversityand community structure of a macroinfaunal assemblage, has been examined in a benthic mesocosm experiment.The experiment was conducted at the Solbergstrand mesocosm (Norwegian Institute for Water Research) usingsubtidal sediment collected from Bjrnhordenbukta, a small sheltered bay in Oslofjrd. Ninety-eight areas of ho-mogenized sediment were subjected to one of seven levels of organic enrichment, combined with one of sevendifferent frequencies of physical disturbance, each replicated once. This structured matrix of physical disturbanceand organic enrichment treatments demonstrated the combined effects of these factors to be nonadditive. Diversitywas lower than expected when low frequencies of physical disturbance acted in conjunction with high levels oforganic enrichment or when high frequencies of physical disturbance were combined with low levels of organicenrichment. Diversity was higher than expected when both disturbance and enrichment were either high or low.The implications of this interaction between physical disturbance and organic enrichment for the application of thedynamic equilibrium model (Huston 1979) to sediment communities are discussed. Multivariate analysis alsoshowed community structure to be significantly affected by physical disturbance, organic enrichment, and interac-tions between the two. It is concluded that strong interactions between physical disturbance and organic enrichment,coupled with both small- and large-scale variability in these factors, could promote heterogeneity and diversity inbenthic infaunal assemblages. However, this remains to be tested in field conditions. Additionally, interactionsbetween physical disturbance and organic enrichment may have important implications for matters of coastal zonemanagement.

Marine benthic infaunal assemblages are subjected to avariety of physical disturbance events, and their response tosuch events has been studied extensively. These studies haveranged from the large-scale effects of trawling (e.g., Tuck etal. 1998) and storm events (e.g., Posey et al. 1996) to thesmall-scale disturbances caused by mobile bioturbating or-ganisms, both epifaunal (e.g., Hall et al. 1991; Thrush et al.1991) and infaunal (e.g., Flach 1992; Widdicombe and Aus-ten 1998). The importance of different scales of physicaldisturbance was discussed by Zajac et al. (1998) who, along

1 To whom correspondence should be addressed. Present address:Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth,PL1 3DH, U.K. ([email protected]).

AcknowledgementsThis work was enabled by a grant from the EC Large Scales

Facility Programme, was funded in part by the UK Ministry ofAgriculture, Fisheries, and Food (project No AE1113), and is acontribution to the PML Coastal Biodiversity research project. Wethank Torgeir Bakke, John Arthur Berge, Liv Berge, and JoannaMaloney of NIVA, Oslo, for helping to facilitate this work; HakonOen, Einar Johannesen, and Oddbjrn Pettersen for their technicalsupport at the Solbergstrand Marine Station; and the crew of R.V.Trygve Braarud. We are also very grateful to Mike Kendall, Mal-colm Jones, and Richard Warwick for constructive comments anddiscussions during the preparation of this manuscript. Additionally,we thank Bob Clarke for much needed statistical advice and guidance.

with others (e.g., Levin and Paine 1974; Hall 1994; Levin1994), highlighted the importance of cycles of disturbanceand recovery in maintaining heterogeneity in soft sedimentenvironments and thereby setting community structure. Theimportance of these cycles was first suggested by Johnson(1970, 1973), who concluded that the continual occurrenceof small-scale disturbances can account for part of the spatialand temporal variations of diversity within benthic com-munities.

Much of the extensive literature concerned with how ma-rine benthic communities respond to organic enrichment hasconcentrated on the effects of anthropogenic inputs associ-ated with freshwater runoff (e.g., Beukema 1991), aquacul-ture (e.g., Ritz et al. 1989), and sewage disposal (e.g., Hallet al. 1997). These studies of anthropogenic eutrophication,together with those examining naturally occurring organicenrichment events (e.g., Oug et al. 1991), have served tostrengthen the validity of the community response model ofPearson and Rosenberg (1978). Based on surveys of macro-benthic communities along gradients of organic enrichment,this model predicts a decline of suspension feeders and anincrease in deposit feeders as organic input to the sedimentincreases, irrespective of the type of organic material re-sponsible for the enrichment. Other models (e.g., Rhoads etal. 1978) predicted a community response to physical dis-turbance similar to that described for organic enrichment.

1721Diversity, disturbance, and enrichment

Such models suggest that communities along a physical dis-turbance or organic enrichment gradient display serialchanges in structure as the intensity or level of the pertur-bation changes. While these investigations into the effectsof either physical disturbance or organic enrichment are ex-tensive, they have not addressed the possibility of interac-tions between these two factors when acting on an assem-blage simultaneously. Such interactions may have substantialimplications for predictive models.

Organic enrichment has been shown to have a significanteffect on species diversity, a particular aspect of communitystructure. The relationship between productivity, or energyin the system (Wright 1983), and diversity was describedby Grime (1973a,b), who presented the intermediate pro-ductivity hypothesis (IPH). This hypothesis predicted max-imum species diversity occurred at some intermediate levelof productivity, at which competition for food is reduced andthe coexistence of potentially competing species was pro-moted. Grimes (1973a,b) definition of productivity was acombination of light availability and the level of soil nutri-ents supplied to the herbaceous plants communities he stud-ied. Using such a definition it is not unreasonable to viewthe supply of organic material to marine benthic communi-ties as a resource that could influence species diversity in amanner predicted by the IPH. A recent field study assessingthe impacts of terrestrial runoff on macrobenthic communi-ties supported the IPH as it demonstrated that maximum di-versity (species richness) corresponded to intermediate levelsof enrichment (Frouin 2000).

A relationship similar to that for diversity and organicenrichment has been observed between diversity and phys-ical disturbance, leading Connell (1978) to propose the in-termediate disturbance hypothesis (IDH). This hypothesisidentifies the severity and frequency of disturbance as keyelements in setting community diversity. Similar to the IPH,the IDH predicts maximum species diversity occurs at someintermediate level of disturbance, at which competitive ex-clusion is reduced. This hypothesis was originally erectedfrom studies of terrestrial communities, and subsequent ev-idence for it being applicable in the marine environment hascome, traditionally, from rocky intertidal (e.g., Paine 1966)and coral reefs studies (e.g., Connell and Keough 1985). Forsoft sediment communities, direct evidence for competitiveexclusion within communities of soft sediments has, to date,been scarce, which leads to a reluctance in accepting theIDH as a mechanism for diversity maintenance in this hab-itat. One study that did claim to provide such evidence wasthat of Kukert and Smith (1992), which used artificialmounds to explore macrofaunal community response to buri-al disturbance in the Santa Catalina Basin. These authorsconcluded that the changes in diversity they observed werea consequence of reduced pressure from competitive dom-inants occurring during community succession followingburial disturbance. In addition to this evidence, previousfield observations of epibenthic agglutinating formainiferans,also in the Santa Catalina Basin (Levin et al. 1991) andrecent laboratory-based experiments on the effects of bio-turbation on meiofaunal and macrofaunal communities (Aus-ten et al. 1998; Widdicombe and Austen 1999) have elicitedcommunity responses that were in agreement with the IDH.

Such studies would suggest that there is justification in con-sidering the IDH as a potential explanation of diversitymaintenance within soft sediment communities in additionto the traditionally accepted habitats of coral reefs and therocky intertidal.

It was evident to Huston (1979) that both the IPH (Grime1973a,b) and the IDH (Connell 1978) relied on competitivedisplacement. By combining these two hypotheses, Huston(1979) proposed the dynamic equilibrium model. This modelassumed diversity represented a balance between growthrates (productivity/organic enrichment) and disturbance, withmaximum diversity being observed when an assemblage re-ceived intermediate levels of both productivity and distur-bance. Empirical support for the dynamic equilibrium modelis hard to come by since the necessary, multifactorial ex-periments are intrinsically more difficult to conduct than ex-periments that manipulate only a single factor. However,much circumstantial evidence does exist from field surveysof interacting gradients of disturbance and rate of displace-ment (see Huston 1994). Additionally, several models ofplant competition and succession (e.g., Botkin et al. 1972;Caswell and Cohen 1991) have been used to conduct sim-ulation experiments, the results of which closely agreed withthe predictions of the dynamic equilibrium model.

While investigations into the effects of either physical dis-turbance or organic enrichment are extensive, they have notaddressed the possibility of interactions between disturbanceand organic enrichment acting simultaneously on an assem-blage. Such interactions may have substantial implicationsfor predictive models, such as the dynamic equilibrium mod-el (Huston 1979). Using an experimental approach, this pa-per explores the response of a benthic macrofaunal com-munity to the combined influence of both physicaldisturbance and organic enrichment. We have attempted totest the generality of the IDH, IPH, and dynamic equilibriummodels, and their application to the marine environment hasbeen discussed. We have examined the hypothesis that theeffects of organic enrichment and physical disturbance onthe structure and diversity of a macrobenthic community areadditive.

Methods

Experimental designThe experiment was carried out inthe mesocosm facility of the NIVA marine research stationSolbergstrand, Oslofjrd, Norway. The mesocosm was de-scribed in detail by Berge et al. (1986). On 10 May 1996,muddy sand was collected by Day grab from Bjrhodenbukta,a sheltered bay in the inner part of Oslofjrd. On the sameday, the sediment was placed in large (1 m2) containerswhere it was homogenized and used to fill 98 plastic buckets(26-cm diameter) to a depth of 20 cm. The buckets of sed-iment were then placed in a 5 m 3 7 m indoor, epoxy resincoated concrete basin, at a constant water depth of 100 cm.The water depth was maintained using an open circulationseawater supply drawn from 60-m depth from the fjord andallowing it to run to waste. A consequence of this continuoussupply was that a small degree of larval supply was possible.The sediment in the buckets was allowed to consolidate for

1722 Widdicombe and Austen

Table 1. Results from ANOVA (three factor mixed model) analysis of abundance data (number of individuals/treatment) for the 16numerically dominant taxa (disturbance and enrichment are fixed factors, the position of replicates in either block 1 or 2 is a random factor).Bold values indicate significant differences, p , 0.05.

Source DF SS MS F P

Heteromastus filiformisDisturbanceEnrichmentDisturbance 3 enrichment

66

36

523058231668739951

871763861120554

1.771.030.63

0.2520.4840.915

Chaetozone setosaDisturbanceEnrichmentDisturbance 3 enrichment

66

36

123532704324988

20594507

694

9.898.332.00

0.0070.0100.020

Paraonis fulgensDisturbanceEnrichmentDisturbance 3 enrichment

66

36

543946524952

906775138

8.536.550.93

0.0100.0190.589

Nuculoma tenuisDisturbanceEnrichmentDisturbance 3 enrichment

66

36

65312771673

109213

46

7.843.041.31

0.0120.1010.213

Cossura longcirrataDisturbanceEnrichmentDisturbance 3 enrichment

66

36

360133395218

600556145

16.007.790.96

0.0020.0120.547

Pseudopolydora pauchibranchiataDisturbanceEnrichmentDisturbance 3 enrichment

66

36

1865676

3077

311113

85

11.751.120.91

0.0040.4480.609

Goniada maculataDisturbanceEnrichmentDisturbance 3 enrichment

66

36

23500366

48310

0.248.201.66

0.9460.0110.066

Nemertea indet.DisturbanceEnrichmentDisturbance 3 enrichment

66

36

118158386

202611

9.255.421.08

0.0080.0290.404

9 weeks before any experimental manipulation began. Thisenabled the reestablishment of oxygen and nutrient gradientsand provided a settlement period when infaunal organismscould regain their spatial positions within the sediment be-fore the experimental manipulations began.

Buckets were held firmly within a wooden frame and ar-ranged in two 7 by 7 blocks of 49 buckets. From 12 July1996, for a 12-week period, each bucket within each blockwas subjected to one of seven levels of organic enrichment,combined with one of seven different frequencies of physicaldisturbance. Thus, there was a structured matrix of 49 treat-ment combinations that was duplicated between blocks. Gre-co-latin squares were used in the experimental design so thateach row within each block contained one of each distur-bance intensity and one of each organic enrichment level.Additionally, the arrangement of treatments within each ofthe two blocks was different.

Organic enrichment was administered at the start of theexperiment by a single application of powdered, dried As-cophyllum nodosum (L.) Le Jolis (product A120 from AlgeaProducts A/S; maximum particle diameter 120 mm). Thepowdered A. nodosum contained 31.5% carbon and 0.9%nitrogen. After the water level in the mesocosm basin hadbeen lowered to below the edge of the buckets, A. nodosum

was spread evenly across the sediment surface at seven treat-ment levels (P0 to P6) equivalent to 0, 12.5, 25, 50, 100,200, and 400 g carbon m22, respectively. In inshore waters,the rate of deposition of organic matter is generally in theregion of 2575 g cm22 yr21 (Gee et al. 1985 and referencestherein). Therefore, it was assumed the quantities of organicenrichment used in the current experiment represented arange of values from very low to gross enrichment. Thebrown alga Ascophyllum nodosum was chosen as it is a nat-urally occurring marine product and has been used success-fully as a source of labile carbon for organic enrichmentexperiments by previous authors (e.g., Gee et al. 1985;Schratzberger and Warwick 1998).

Physical disturbance of a consistent duration and intensitywas administered with a mechanical stirrer that raked thesediment surface to a depth of 2 cm. A plastic, circular disc(250-mm diameter), covered with 95 stainless steel nails (4-mm diameter), each protruding approximately 20 mm fromthe disc surface, was lowered onto the sediment surface androtated at a constant speed (68 rpm). The nails on the discwere orientated at different angles, which prevented the dis-turbance being concentrated in certain areas and ensured auniform disturbance across the entire sediment surface. Dis-turbances lasted for exactly 24 s, with a constant number of


Table 1. Continued.

Source DF SS MS F P

Diplocirrus glaucusDisturbanceEnrichmentDisturbance 3 enrichment

66

36

93162322

1627

9

4.4413.55

3.00

0.0460.0030.001

c. f. Syllis cornutaDisturbanceEnrichmentDisturbance 3 enrichment

66

36

4524

116

843

2.341.321.10

0.1620.3730.391

Pholoe minutaDisturbanceEnrichmentDisturbance 3 enrichment

66

36

8253

110

1493

9.105.561.36

0.0080.0280.178

Schistomeringos caecusDisturbanceEnrichmentDisturbance 3 enrichment

66

36

5145

139

874

3.811.520.95

0.0640.3130.565

Lumbrineris teturaDisturbanceEnrichmentDisturbance 3 enrichment

66

36

183092

353

1.841.571.18

0.2390.2980.310

Anobothrus gracilisDisturbanceEnrichmentDisturbance 3 enrichment

66

36

31152

212

5296

28.821.921.47

0.0010.2240.127

Lumbrineris fragilisDisturbanceEnrichmentDisturbance 3 enrichment

Eteone flavaDisturbance

66

36

6

247376

4

412

2

1

1.6312.03

1.69

0.47

0.2840.0040.060

0.808EnrichmentDisturbance 3 enrichment

636

840

11

1.081.46

0.1980.132

revolutions for each disturbance event. Suspension of themechanical stirrer from a fixed height-moveable gantryabove the mesocosm basin ensured that a constant pressureand depth of disturbance was applied to all treatments. Priorto the disturbance being administered, the water level in thebasin was lowered to below the edge of the buckets. Thisprevented loss of any fine material during periods of distur-bance. After allowing approximately 1 h for any resuspendedmaterial within the disturbed buckets to settle out, the waterlevel in the basin was raised. The physical disturbance fre-quencies were no disturbance (D0), once every 4 weeks(D1), once every 2 weeks (D2), once a week (D3), twice aweek (D4), three times a week (D5), and every day (D6).Although more rapidly and regularly administered than innatural situations, this disturbance of the upper sediment lay-ers may be considered as analogous to the sediment turnovercaused by the movement and feeding behavior of large in-faunal, deposit feeding species (e.g., the heart urchin Bris-sopsis lyrifera).

At the end of the 12-week experimental period, the sedi-ment in each bucket was sieved over a 500-mm mesh. Theresidue was fixed in a 10% formaldehyde solution and wassorted under a binocular microscope. All animals were ex-tracted and identified to the lowest possible taxonomic level.Environmental conditions remained constant throughout the

experiment: temperature was 7 6 18C and salinity was 34.56 0.5 psu.

Data analysisMeasures of a diversity were calculated;number of species, Margalefs species richness, Pielousevenness, and Shannon-Wiener (loge). Global treatment ef-fects and pairwise interaction values for these measures wereidentified using a three-factor mixed model ANOVA com-puted using Systat version 7.0. Visual interpretation of re-sidual plots was used to confirm that the data complied withthe assumptions of the ANOVA model, e.g., homogeneityof variance. SURFER version 5.02 was used to generate con-tour plots for number of species using standard krigging anda low level of smoothing.

Multivariate data analyses followed the methods describedby Clarke (1993) using the PRIMER version 4.0. softwarepackage (Clarke and Warwick 1994). Analysis was carriedout on both untransformed and transformed data usingthe Bray-Curtis similarity measure to determine the effectsof treatments on different components of the community.Analysis of untransformed data is sensitive to changes in theabundance of the dominant species, while analysis of transformed data detects effects on community structure gen-erally, including changes in abundance of the lower abun-dance and rare species, without being unduly influenced by


Fig. 1. Contour plots demonstrating the abundance (number of individuals/treatment) of 11 numerically dominant species at differentcombinations of disturbance intensities and organic enrichment levels.

dominant, high-abundance species. Two-way crossed AN-OSIM (analysis of similarities) was carried out to test fortreatment effects. The ANOSIM test for multivariate data isequivalent to an ANOVA test for univariate data, except thatANOSIM does not allow testing for interaction effects. Mul-tidimensional scaling (MDS) was used to visualize patternsof community change (1) in response to physical disturbanceat the seven different levels of organic enrichment and (2)in response to organic enrichment at the seven different lev-els of disturbance. The significance of differences betweenthese patterns of response was tested using RELATE (Clarkeet al. 1993) by calculation of the Spearman rank correlations(r) between two matrices and in this case between each pairof faunal similarity matrices. RELATE was then used to as-sess how closely patterns of response correlated to perfectseriation, by calculating the strength of correlation betweenthe observed rank dissimilarities for the experimental bioticdata with an artificially constructed rank distance matrix sim-ulating perfect seriation (rank 0 between replicates, rank 1between adjacent treatments etc., up to rank 6 between ex-treme treatments). The r values from this analysis (Spear-man rank correlations between the biotic dissimilarity andthe perfect seriation distance matrices) enabled the directcomparison of seriation strength between patterns producedat different disturbance frequencies or organic enrichmentlevels (Clarke, pers. comm.).

Results

Patterns in species abundanceA total of 81 taxa wererepresented within the mesocosm community, with the 16numerically dominant taxa being Heteromastus filiformis,Chaetozone setosa, Paraonis fulgens, Nuculoma tenuis, Cos-sura longocirrata, Pseudopolydora pauchibranchiata, Gon-iada maculata, Nemertea indet., Diplocirrus glaucus, c.f.Syllis cornuta, Pholoe minuta, Schistomeringos caecus,Lumbrineris tetura, Anobothrus gracilis, Lumbrineris fra-gilis, and Eteone flava (listed in order of decreasing abun-dance). Of these, the abundance of six taxa was shown tobe significantly affected by both physical disturbance andorganic enrichment (Table 1). In ANOVAs that investigatemultiple comparisons there is a possibility that, if enoughtests are performed, significant values will be encounteredeven if the null hypothesis of no effects was true throughout.To counteract this possibility it is customary to apply a cor-rection that reduces the p value at which a test is consideredsignificant in line with the number of tests performed. Un-fortunately, in tests such as that presented in this paper,which rely on a large number of multiple tests, in this case48, such corrections reduce the p value to such an extent asto make the tests worthless. However, in a total of 48 tests,assuming a model of 5% of error, the number of falselysignificant results is still quite small, with only three testspotentially appearing significant even if the null hypothesis

of no effects was true throughout. In Table 1 there were 19such significant values and the probability of seeing thismany significant values by chance, calculated on a singlebinomial model, is approximately zero. Consequently, a pvalue of 0.05 was maintained as to indicate situations wheresignificant effects were likely to be occurring, although thereader should be mindful of the possibility that a small num-ber of these significant results may have occurred by chance.For Nemertea indet. and the polychaetes Paraonis fulgens,Phole minuta, and Cossura longocirrata there was no inter-action between the effects of disturbance and enrichment onthe abundance of these taxa (Table 1). A significant inter-action term indicated the effects of disturbance and enrich-ment on the abundance of the polychaetes Diplocirrus glau-cus and Chaetozone setosa were not independent. Threespecies, the bivalve Nuculoma tenuis and the tube buildingpolychaetes Pseudopolydora pauchibranchiata and Ano-bothrus gracilis, were significantly affected by disturbancealone, whereas a further two species, the large bodied, mo-bile polychaetes Goniada maculata and Lumbrineris fragilis,were affected by enrichment but not by disturbance. Graph-ical representation of the effects of physical disturbance andorganic enrichment on the abundance of these 11 taxa isgiven in Fig. 1. Where effects were significant there was ageneral trend for abundance to be lowest where physicaldisturbance was most frequent. However, changes in abun-dance in response to different levels of organic enrichmentwere less clear. The abundance of most species was lowestat the highest levels of enrichment, but, the lowest levels ofenrichment did not always correspond to the highest levelsof abundance. For example, the abundance of Nemertea washighest in treatments receiving intermediate levels of enrich-ment. No significant effect of either disturbance or enrich-ment was demonstrated for the remaining five polychaetespecies; Heteromastus filiformis, c.f. Syllis cornuta, Schis-tomeringos caecus, Lumbrineris tetura, and Eteone flava.

At the end of the experiment, the structure and diversityof the mesocosm community from treatments that had re-ceived no enrichment and no physical disturbance was com-parable to the naturally occurring community present at thecollection site, Bjrnhordenbukta (see Valderhaug and Gray1984). Abundance in treatments ranged from seven to 1194individuals, and the number of taxa per treatment rangedfrom one to 36.

Patterns in diversityAll diversity measures were signif-icantly affected by organic enrichment, but only number ofspecies were significantly affected by physical disturbance(Table 2). Significant interaction effects between physicaldisturbance and organic enrichment for three diversity mea-sures, number of species, species richness, and Shannon-Wiener index, were demonstrated by the three-factor mixedmodel ANOVA (Table 2). This indicated that the effects ofphysical disturbance and organic enrichment, on these three


Table 2. Results from ANOVA (three factor mixed model) analysis of community structure measures (disturbance and enrichment arefixed factors, the position of replicates in either block 1 or 2 is a random factor). Bold values indicate significant differences, p , 0.05.

Source DF SS MS F P

Number of speciesDisturbanceEnrichmentDisturbance 3 enrichment

66

36

415.272701.411313.16

69.21450.2336.48

5.4535.44

2.87

0.0010.0010.001

Number of individualsDisturbanceEnrichmentDisturbance 3 enrichment

66

36

1137535803951

1113402

189589133992

30928

3.272.340.69

0.0870.1620.868

Species richness (Margalef)DisturbanceEnrichmentDisturbance 3 enrichment

66

36

4.244461.157832.2220

0.707410.1930

0.8951

1.9834.37

3.23

0.2130.0010.001

Shannon-Wiener diversityDisturbanceEnrichmentDisturbance 3 enrichment

66

36

1.016737.602626.39821

0.169461.267100.17773

1.2322.19

2.55

0.4050.0010.003

Pielous evenessDisturbanceEnrichmentDisturbance 3 enrichment

66

36

0.212730.236600.56878

0.034560.039430.01580

1.434.461.10

0.3390.0460.392

diversity measures, were nonadditive. The contour plots inFig. 2 demonstrate the response of the four diversity indices(number of species, species richness, Shannon-Wiener, andPielous evenness) to increasing levels of organic enrichmentand physical disturbance. It would appear that, as the rich-ness (number of species) becomes less important and thedistribution of individuals within each species (evenness) be-comes more important in the calculation of the indices, theeffect of increasing the frequency of physical disturbanceappears to lessen compared with the effect of increasing theamount of organic enrichment (Fig. 2, Table 2).

The rate at which diversity decreases appears to be greaterin response to changes in organic enrichment than in re-sponse to increased physical disturbance (Fig. 2). The patternobserved in Fig. 2 can be seen as a subset of the patterndescribed by Huston (1979), with the areas of Hustons mod-el corresponding to lower physical disturbance and lowerorganic enrichment not being represented in Fig. 2.

The ANOVA interaction values between the effects ofphysical disturbance and organic enrichment on the numberof species, species richness, and Shannon-Wiener (Table 3)highlight where the effects of physical disturbance and or-ganic enrichment act on a community either synergisticallyor antagonistically. In areas of no physical disturbance buthigh levels of organic enrichment, the diversity was lowerthan would be expected. However, in areas of high experi-mental disturbance and high levels of organic enrichment,diversity was higher than would be expected if these twofactors were acting independently on the community. Theinteraction values demonstrate that, when acting simulta-neously on a community, physical disturbance and organicenrichment can act either synergistically or antagonisticallydepending on the magnitudes of each factor.

An ameliorating effect, on species diversity, of physicaldisturbance in areas of high organic enrichment is identified

in Table 3 and demonstrated in Fig. 2. At high levels oforganic enrichment (P5 and P6) increasing the physical dis-turbance frequency resulted in higher diversity, while in ar-eas of low organic enrichment (P0, P1, and P2) increasingphysical disturbance caused diversity to decrease. In areasof midlevel organic enrichment (P3 and P4), diversity re-mained relatively constant over a range of low to midfre-quencies of physical disturbance (D3). In areas of low phys-ical disturbance frequency (D0 and D1) diversity is highestin treatments with little or no organic enrichment (P0 andP1). At midfrequencies of physical disturbance (D2D4),maximum diversity was observed in midlevel organic en-richment treatments (P2P4). While at high physical distur-bance frequencies, changes in the level of organic enrich-ment had little effect on diversity. The overall trend was forthe level of organic enrichment at which diversity was high-est to increase as the frequency of physical disturbance in-creased (Fig. 3). Where one type of disturbance factor waslow (physical disturbance or organic enrichment) diversitydecreased as the intensity of the other factor increased. How-ever, this decrease was greatest in the combination of lowphysical disturbance with increasing organic enrichment(Fig. 3). This suggested that the spread of treatments chosenfor organic enrichment was broader than that of the treat-ments chosen for physical disturbance.

Patterns in community structureGlobal tests using two-way crossed ANOSIM showed significant treatment effectsfor both physical disturbance (untransformed; R 5 0.174, p5 0.001: transformed; R 5 0.266, p 5 0.000) andorganic enrichment (untransformed; R 5 0.121, p 5 0.003: transformed; R 5 0.180, p 5 0.001).

Faunal composition of the test community varied in re-sponse to different intensities of physical disturbance oramounts of organic enrichment. These differences in com-


Fig. 2. Contour plots demonstrating diversity (number of species, Margalefs species richness, Shannon-Wiener, Pielous evenness) atdifferent combinations of disturbance intensities and organic enrichment levels. (P0P6 5 organic enrichment; D0D6 5 physical distur-bance).


Table 3. Interaction terms from ANOVA showing pair-wisecomparisons of disturbance and organic enrichment treatment lev-els.

D0 D1 D2 D3 D4 D5 D6

(a) Number of speciesP0P1P2P3P4P5P6

6.61.98.1

20.20.8

29.627.6

20.95.40.61.8

23.70.4

23.6

20.52.32.02.20.7

23.223.7

20.821.522.3

3.41.42.0

22.0

25.724.4

0.30.00.54.15.1

0.021.223.523.3

0.22.84.8

1.222.525.324.020.1

3.57.0

(b) Margalefs species richnessP0P1P2P3P4P5P6

0.90.21.10.20.2

21.521.1

20.10.80.00.2

20.50.1

20.5

20.10.40.60.50.0

20.620.8

20.120.320.5

0.40.30.5

20.3

21.020.6

0.220.1

0.10.60.8

0.220.420.520.620.1

0.60.7

0.020.020.920.620.0

0.41.1

(c) Shannon-Wiener (loge)P0P1P2P3P4P5P6

0.30.10.30.30.1

20.720.4

20.00.3

20.10.00.0

20.120.1

0.00.20.40.3

20.120.320.4

20.120.120.120.2

0.10.5

20.2

20.420.1

0.220.120.0

0.10.3

0.220.320.320.220.2

0.40.4

20.10.1

20.420.2

0.00.10.5

Fig. 3. Nonmetric multidimensional scaling (MDS) ordinationsof macrofaunal abundance on transformed data comparing (a)

the effect of organic enrichment on community response betweenareas subjected to different physical disturbance frequencies and (b)the effect of physical disturbance on community response betweenareas subjected to different organic enrichment levels. (Not all en-richment data are included in MDS for D1 and D2see text fordetails.) Stress values in italics. (0 5 low physical disturbance/or-ganic enrichment; 6 5 high physical disturbance/organic enrichment)

munity structure constituted a community response pat-tern to either of the two experimental variables and thesepatterns are represented two-dimensionally as MDS ordina-tions (Fig. 3). As an approach to identifying interaction be-tween the effects of physical disturbance and organic en-richment on multivariate aspects of community structure,RELATE was used to test whether the community responsepatterns to organic enrichment were influenced by chang-ing the intensity of physical disturbance (Table 4), or wheth-er the community response patterns to physical distur-bance were influenced by changing the level of organicenrichment.

When using transformed data in the RELATE anal-ysis, there were a high number of significant correlationsbetween the community response patterns of the differentphysically disturbed treatments, each subjected to the samerange of organic enrichment (Table 4). This showed that, forlower abundance and rarer species, the response to organicenrichment was generally consistent regardless of the phys-ical disturbance frequency. However, when using untrans-formed data in the RELATE analysis, fewer significant cor-


Table 4. Pairwise comparisons of the mutivariate community structure generated by a gradient of organic enrichment in single distur-bance regimes using RELATE on (a) untransformed and (b) transformed data and Bray-Curtis similarities. Bold values indicatesignificant correlations in the community structure in the treatments compared, p , 0.05. Results represented as r-values with p-values fora test of no relationship in parentheses.

D0 D1 D2 D3 D4 D5

(a) Untransformed dataD1D2D3D4D5D6

0.33 (0.06)0.62 (0.00)0.70 (0.00)0.35 (0.02)0.15 (0.22)

20.14 (0.82)

0.36 (0.05)0.32 (0.05)

20.04 (0.57)20.03 (0.49)20.05 (0.56)

0.64 (0.00)0.24 (0.09)0.24 (0.13)

20.33 (1.00)

0.23 (0.08)0.22 (0.14)

20.24 (0.97)20.06 (0.60)20.14 (0.79) 20.23 (0.94)

(b) transformed dataD1D2D3D4D5D6

0.64 (0.00)0.85 (0.00)0.60 (0.01)0.44 (0.02)0.50 (0.01)0.21 (0.15)

0.65 (0.00)0.52 (0.01)0.39 (0.03)0.09 (0.29)0.46 (0.02)

0.61 (0.00)0.45 (0.02)0.44 (0.02)0.23 (0.12)

0.16 (0.20)0.36 (0.04)

20.09 (0.62)0.02 (0.43)0.36 (0.04) 20.17 (0.83)

Table 5. R-values from RELATE test of seriation. Bold values indicate significant correlations between community responses observedin actual data and a similarity matrix observing perfect seriation, p , 0.05.

(a) Community response to changes in organic enrichment level at different frequencies of physical disturbanceDisturbance frequencyUntransformed data transformed data

D00.3770.475

D10.2570.467

D20.2150.400

D30.4030.387

D420.024

0.148

D50.0060.108

D60.0250.045

(b) Community response to changes in physical disturbance frequency at different levels of organic enrichmentOrganic enrichment levelUntransformed data transformed data

P00.3780.152

P10.1190.190

P20.3840.364

P30.3290.449

P40.1020.014

P50.3410.100

P620.018

0.230

relations were observed (Table 4). This suggested thatchanges in the relative abundance of numerically dominantspecies, in response to organic enrichment, were affected bydifferent physical disturbance frequencies.

When using both untransformed and transformeddata, very few significant correlations were observed be-tween the community response patterns of different or-ganically enriched treatments, each subjected to the samerange of physical disturbance frequencies. Pairwise compar-isons using RELATE showed only one significant correlationwhen using untransformed data (P0 vs. P5) and two signif-icant correlations when using transformed data (P2 vs.P3 and P1 vs. P4). This suggests that the response to phys-ical disturbance of both the numerically dominant speciesand of the low abundance and rare species was affected bythe amount of organic material received.

To examine the pattern of community response to eitherorganic enrichment or physical disturbance in more detail,the ordinations of community structure in Fig. 3 were com-pared with a pattern that observed perfect seriation. RE-LATE was used to test for significant correlations (Table 5).At low physical disturbance frequencies (D0D3), the com-munity response to increasing levels of organic enrichmentwas serial, with communities being most similar to each oth-er when the differences between their respective levels oforganic enrichment are small. At high physical disturbancefrequencies (D4D6), seriation breaks down (Table 5a). A

serial response to physical disturbance was shown mostly inmidorganic enrichment treatments (P2 and P3) (Table 5b).Additional serial response was observed in P0 and P5 foruntransformed data and in P6 for transformed data.

In two of the ordinations presented in Fig. 3 (D1 and D2)some of the highest organic enrichment levels were omittedfrom the ordinations. The community structure in these treat-ments was very different to that in the other treatments com-pared; consequently, the latter were tightly clustered in theMDS. By omitting the high enrichment data it was possibleto visualize the patterns contained within the remaining datamore clearly. For calculation of seriation values all data wereincluded.

Discussion

The results of this experiment were consistent with thosepredicted by the dynamic equilibrium model (Huston 1979),and, therefore, this model may serve as a basis of an expla-nation for the relationship between diversity, physical dis-turbance, and organic enrichment.

The discrepancy between the predicted surface plot of thedynamic equilibrium model (Huston 1979) and the plotsgenerated from actual data (Fig. 2a,b) may be due to a num-ber of factors, acting singularly or in combination. First, anysediment collected from the field that contains a viable faunawill have a preexisting level of organic material. Conse-


quently, it is not possible to produce treatments with no or-ganic material, and this will, therefore, truncate the responsesurface of Hustons model. Similarly, the removal of the sed-iment from the field and its collection in the treatment buck-ets will result in some physical disturbance of the sedimentand resident fauna. Therefore, the reestablished assemblagewas a nonequilibrium abstraction of the natural one and wasin a state of recovery from this disturbance at the start ofthe experiment, 9 weeks later. Physical disturbance wouldalso be introduced by the bioturbation generated by organ-isms already present within the sediment. This bioturbation,together with disturbance due to collection, meant it was notpossible to produce treatments with no physical disturbance,and this will truncate the response surface of Hustons mod-el. The response surface observed for number of species inFig. 2 may, therefore, be seen as a subset of the predictedresponse surface presented by Hustons model, with the areasof his model corresponding to zero/low disturbance and or-ganic enrichment absent from the response surface in Fig. 2.

An additional discrepancy between Hustons model andthe response surface in Fig. 2a may have resulted from thepragmatic way in which the treatment levels were chosen.Axes units were not assigned to Hustons conceptual modeland it is, therefore, difficult to determine the appropriatescale and spread for each of the two factors. The spread oftreatments chosen for both organic enrichment and physicaldisturbance represented a subset of a larger disturbance orenrichment gradient. Although their relative positions weredetermined, the exact position of experimental treatments onthe larger gradients was unknown. Therefore, when describ-ing the frequency of physical disturbance, terms such ashigh or low are relative to other treatments rather thanto field disturbances or the disturbance effects of organicenrichment. The levels used for organic enrichment werejustified in the methods and were expected to correspond tonaturally occurring high and low levels of enrichment. Ad-ditionally, diversity appeared to decrease more rapidly inresponse to increased organic enrichment than to increasedphysical disturbance. This may also have resulted from thepragmatic way in which treatment levels were selected. Priorto this experiment, it was impossible to know what frequen-cy of disturbance equated to any specified amount of organicenrichment in terms of impact on the macrobenthic com-munity. The relative rates at which changes in disturbanceand enrichment altered diversity were also unknown. There-fore, the severity of the gradient between low (P0) and high(P6) organic enrichment treatments may have been greaterthan that of the gradient between low (D0) and high (D6)physical disturbance treatments.

In addition to supporting the predictions of the dynamicequilibrium model, this paper has also shown that the effectsof physical disturbance and organic enrichment do not acton diversity independently. Diversity was lower than ex-pected assuming an additive model when low frequencies ofphysical disturbance acted in conjunction with high levelsof organic enrichment or when high frequencies of physicaldisturbance were combined with low levels of organic en-richment. Diversity was higher than expected when both dis-turbance and enrichment were either high or low.

The interaction between physical disturbance and organic

enrichment may have several causes. Physical disturbancemay increase the depth of oxygen penetration in enrichedsediments, supplying the increased oxygen demand of mi-crobial decomposers as the additional organic material isprocessed. This will reduce the impact of oxygen depletionon species of macrofauna sensitive to low oxygen levels,while also stimulating the activity of aerobic microbial de-composers and accelerating carbon processing. Hulthe et al.(1998) observed that fresh material degrades at the same ratein oxic and anoxic conditions, but old buried material de-grades 3.6 times faster in oxic conditions than in anoxicconditions. Physical disturbance may bury fresh material foranoxic degradation and expose old buried material to oxicconditions, thus enhancing organic carbon oxidation in ma-rine sediments. Alternate exposure of material to the activ-ities of both oxic and anoxic microorganisms through phys-ical disturbance will result in greater carbon degradation thanwhen material is subjected to a constant oxic or anoxic re-gime (Aller 1994). The idea that physical disturbance pre-vents oxygen depletion may be part of the reason why thepresence of Beggiatoa sp. mats were limited to treatmentswith high organic enrichment and little or no disturbance.The presence of this bacterial mat has been associated witheutrophic conditions and severe oxygen depletion (Sampouand Oviatt 1991), and its presence in grossly enriched treat-ments was expected. Consequently, the absence of Beggia-toa sp. from the high organic treatments that had receivedsome physical disturbance may have been as a result of in-creased sediment oxygenation. What is more likely, however,is that a combination of increased sediment oxygenation andthe physical disruption of these mats as a result of the dis-turbance prevented their formation in physically disturbedareas. In field conditions, it has been shown that interactionsbetween physical disturbance and organic enrichment occurwhen physical disturbance of the sediment surface causesthe resuspension of the organic material and results in theremoval of that material via lateral water movements (e.g.,Guidi-Guilvard and Buscail 1995). In the current study, thisfinal mechanism would have had minimal effect because,after disturbance had been administered, disturbed sedimentwas allowed to settle before the water level was raised andthe treatments exposed to lateral water movement. Conse-quently, the results from the current study would suggest thatlateral removal of organic material is not the only mecha-nism by which physical disturbance ameliorates the effectsof organic enrichment. Processes such as increased sedimentoxygenation are also important. Previous studies using fieldexperiments and observations have prompted authors to ad-vocate the use of both direct sediment disturbance (e.g.,ploughing) and the addition of bioturbating species as meth-ods for reconditioning organically polluted sediments(e.g., Chareonpanich et al. 1994). By showing that, in a lab-oratory experiment, sediment disturbance can offset thedamaging effects of high levels of organic material depositedon the benthos, this paper supports the conclusions of theseauthors.

Examining the combined effects of physical disturbanceand organic enrichment on the abundance of the numericallydominant species revealed differences in the way speciesrespond to physical disturbance and organic enrichment. As


was predicted by Brenchley (1981), tube building speciessuch as Anobothrus gracilis and Pseudopolydora pauchi-branchiata were shown to be extremely sensitive to increas-es in the frequency of physical disturbance. This sensitivityis assumed to be a result of either damage to individuals orthe failure of organism to regain/maintain their positionwithin the sediment during or after disturbance. Lumbrinerisfragilis and Goniada maculata are large, mobile species andshowed no such intolerance to physical disturbance. How-ever, their abundance was significantly reduced in areas re-ceiving the highest levels of organic enrichment. These re-sults concurred with the conclusions of Pearson andRosenberg (1978) in that A. gracilis and P. pauchibranchia-ta were typical of transitory or second order progres-sive species. It is likely that the low levels of oxygen, char-acteristic of extremely enriched environments, preventedlarger species, with relatively small body surface to volumeratios and no specialized respiratory apparatus, from per-sisting in these areas. A second species of Lumbrineris wasrecorded in the current study. Lumbrineris tetura was gen-erally smaller than Lumbrineris fragilis, and this size differ-ence may explain why the abundance of the former was notsignificantly reduced by increased organic enrichment. Ingeneral, it seems that an organisms tolerance to physicaldisturbance is influenced by its level of mobility, while tol-erance to the deoxygenation associated with organic enrich-ment is influenced by an organisms body surface to volumeratio. It may be assumed, therefore, that species of limitedmobility and with no specialized branchial structures wouldbe significantly affected by increases in both physical dis-turbance and organic enrichment. In the current study, theabundance of three taxa fitting these criteria was shown todo just that, with the abundance of Nemertea, Pholoe minuta,and Cossura longocirrata decreased in response to an in-crease in both disturbance and enrichment. Two species thatalso demonstrated significant changes in abundance in re-sponse to both disturbance and enrichment were the poly-chaetes Chaetozone setosa and Diplocirrus glaucus; how-ever, statistical analysis demonstrated a significantinteraction between the two factors. In treatments combininghigh levels of both enrichment and disturbance, their abun-dance was higher than would have been expected if bothfactors had been acting independently. Chaetozone setosapossess many long, thin branchial filaments, while Diplocir-rus glaucus has eight stout branchial filaments in addition toa papilated body surface. It is possible that these speciesused their breathing apparatus/adaptations to capitalize onany oxygenation resulting from increased physical distur-bance. However, no such interaction between disturbanceand enrichment was observed for the abundance of Paraonisfulgens, despite its possessing 22 pairs of small digitate gills.It may have been that P. fulgens was more susceptible todamage from physical disturbance than either C. setosa orD. glaucus. Alternatively, as the gills of P. fulgens have asmaller surface area to volume ratio than those of C. setosaor D. glaucus, the branchial apparatus of P. fulgens mayhave been insufficient to benefit fully from the possible in-crease in oxygen due to increased physical disturbance.

The effects of increasing levels of physical disturbance onthe community structure of samples treated with organic ma-

terial were also complex. When organic enrichment levelswere either high or low, increasing the frequency of distur-bance did not have a predictable, serial effect. Serial changesin community structure as an effect of increasing physicaldisturbance were only observed at intermediate (25 and 50g cm22) organic enrichment levels. In the field the supply oforganic material to coastal sediments is highly variable, bothtemporally and spatially. Additionally, there are many sourc-es of organic material, some from large-scale inputs (e.g.,algal blooms, benthic primary production, terriginous ma-terial from riverine input) and some that operate at smaller,more localized scales (e.g., fish/mammal carcasses, macroal-gal detritus). The results presented in this paper illustrate theimportance of considering this natural variability in the sup-ply of organic material when predicting or assessing the ef-fect of physical disturbance on benthic communities. Coastalzone management often requires monitoring of the effects ofboth physical disturbance, e.g., demersal fishing and dredg-ing, and organic enrichment, e.g., fish farm waste. The re-sults presented here emphasize that these monitoring effortsshould not address single disturbance types in isolation butshould consider all environmental conditions that may alle-viate or exacerbate any community response.

Localized forms of physical disturbance are common infine sediments and occur at a range of scales and frequen-cies. Large-scale disturbances (e.g., natural events such asstorms or anthropogenic impacts such as trawling or dredg-ing) cover large areas but may be relatively infrequent, al-lowing extended periods of recovery between disturbances.On a smaller scale, bioturbation by large macrofaunal or-ganisms have been shown to have a considerable effect onboth the associated macrofaunal and meiofaunal communi-ties (e.g., Austen et al. 1998; Widdicombe and Austen 1999).In areas sheltered from large-scale hydrodynamic distur-bances, the seasonal and spatial patchiness in the distributionof bioturbating macrofauna may increase the heterogeneitywithin an otherwise homogeneous area, in accordance withthe spatial-temporal mosaic theory (Grassle and Morse-Por-teous 1987). In addition, the interactive effects observed inthis study suggest that the frequency of physical disturbancecaused during bioturbation will both structure the fauna andaffect the manner in which that fauna responds to changesin organic enrichment. Consequently, such bioturbation in-duced community heterogeneity will be exacerbated by var-iability in the supply of organic material. Variable nutrientinput and hydrodynamic features, such as internal waves(Lennert-Cody and Franks 1999) may act to concentrateplanktonic organisms, resulting in a patchy supply of organicmaterial to the benthos. Additionally, physical structurescaused by macrobenthic organisms, e.g., feeding pits, tubes,expulsion mounds, can act to increase variability by furtherconcentrating or dissipating organic material (Yager et al.1993).

This study has demonstrated experimentally a relationshipbetween physical disturbance, organic enrichment, and di-versity in marine benthic communities, consistent with thedynamic equilibrium model. It has also shown that the ef-fects of physical disturbance and organic enrichment do notact independently on the abundance of some species, benthiccommunity structure, and diversity. However, in order to ful-


ly accept the generality of these conclusions, it is imperativethat further evidence demonstrating the effects of physicaldisturbance and organic enrichment on benthic infaunalcommunities is obtained from naturally occurring field sit-uations. Until such validation is available, the results pre-sented here should be used with an awareness for the poten-tial limitations of mesocosm experimental approaches,particularly when applied to community processes. In par-ticular, recovery after disturbance plays an important role insetting levels of diversity in benthic communities (e.g., Gras-sle and Morse-Porteous 1987). Owing to restricted immigra-tion, the importance of this process within mesocosm sys-tems is reduced, while the influence of an individualorganisms tolerance to a particular perturbation is increased.The main consequence of this is to increase the scale atwhich the experiment is relevant with small-scale distur-bances in mesocosm systems being analogous to much largerevents in the field (Widdicombe 2001). An additional artifactis the inability of some taxa to persist within mesocosms.The benthic assemblages maintained within the Solbergs-trand mesocosm have been shown to have higher faunal den-sities and lower species diversities than locally occurringfield communities (Widdicombe 2001) with the majority ofthe taxa missing from the mesocosm being crustaceans.However, community structure analysis has demonstratedthat the polychaete assemblage was a good approximationof that recorded in the field. With the majority of the con-clusions drawn from the current study having been concen-trated on the responses of polychaete fauna, it may be as-sumed that the results presented here are robust and haverelevance to field situations.

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Received: 20 November 2000Accepted: 19 June 2001

Amended: 6 July 2001

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Widdicombe 2001 - The Interaction Between Physical Disturbance and Organic Enrichment