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Estuarine, Coastal and Shelf Science 85 (2009) 377–386

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Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier .com/locate/ecss

Difficulties in separating hurricane induced effects from natural benthicsuccession: Hurricane Isabel, a case study from Eastern Virginia, USA

C. Hughes a,b, C.A. Richardson a,*, M. Luckenbach b, R. Seed a

a School of Ocean Sciences, College of Natural Sciences, University of Wales Bangor, Menai Bridge, Anglesey LL59 5AB, UKb Virginia Institute of Marine Science, College of William and Mary, Eastern Shore Laboratory, Wachapreague, Virginia, USA

a r t i c l e i n f o

Article history:Received 20 May 2009Accepted 14 August 2009Available online 9 September 2009

Keywords:benthic environmentecological successionecosystem disturbancehurricaneszoobenthos

Regional index terms:USAVirginiaWachapreague Bay

* Corresponding author. Tel.: þ44 1248 382855; faxE-mail address: cara.hughes@bangor.ac.uk (C. Hug

0272-7714/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.ecss.2009.08.023

a b s t r a c t

Hurricane Isabel reached the Eastern seaboard of North America on 18 September 2003 causing esti-mated damage >3 billion US dollars and the death of w50 people. Isabel is considered to be one of themost significant tropical cyclones to affect Virginia, since the Chesapeake Potomac Hurricane of 1933 andHurricane Hazel in 1954. A study of the temporal changes in the benthic fauna pre- and post-hurricanewas conducted on an intertidal sandflat within the dynamic barrier island system near Wachapreague,Eastern Virginia. Replicate sediment cores were collected 3 weeks before Isabel made landfall and furthersamples were collected on 5 occasions over the following 20 months. An immediate effect of Isabel wasa doubling in the number of species, a significant increase in invertebrate species diversity (H0) and a risein opportunistic species and deposit feeders, but a non-significant increase in the total number oforganisms. Changes in infauna occurred such that by the end of the study there were significantlyincreased numbers of species, faunal abundances and community diversity measures, as compared withpre-hurricane samples, suggesting a potentially positive medium-term effect of this hurricane pertur-bation. The most notable direct effects of the hurricane were on the relative abundances of feeding guildswith a reduction in interface feeders from 87% pre-hurricane to 64% post-hurricane, and an increase insurface deposit feeders from 7% pre-hurricane to 20% post-hurricane. The study highlights potentialproblems in interpreting post-perturbation data when insufficient pre-perturbation data exist.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

Physical disturbance is an important factor in structuring softsediment infaunal communities (e.g. Thistle, 1981; Probert, 1984)and its effect depends on the nature, intensity and frequency of thedisturbance. Disturbance, broadly defined by Pickett and White(1985) as ‘‘any discrete event in time that disrupts ecosystem,community, or population structure and changes resources,substrate availability, or the physical environment’’, encompassesmany processes that have been extensively studied (see Hall, 1994for review). However, the effects of disturbances caused by hurri-canes and tropical storms on marine benthic communities havebeen studied to a lesser extent. This is due in part to the sporadicnature of such events, but more importantly because there is oftenno pre-hurricane community data or knowledge available, makinga comprehensive assessment of the direct impacts of such an eventdifficult; this also adds to the potential problems in separating

: þ44 1248 716367.hes).

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natural successional changes in time from real storm inducedeffects.

Previous studies that have focused on the effects of hurricanesand tropical storms have reported a wide range of responses of theresident subtidal and intertidal biota. These include: no significantdepletions of intertidal infaunal taxa in O’ahu, Hawaii after the verypowerful Hurricane Iniki in 1992 (Dreyer et al., 2005), increases infringing reef invertebrate densities post-Hurricanes David andFrederic in 1979 in St Croix (Moran and Reaka-Kudla, 1991), and theelimination of some soft-bottom species from certain salinityregime areas in the Chesapeake Bay, USA, after Tropical StormAgnes in 1972 (Boesch et al., 1976). Following landfall of HurricaneFran in 1996 and Hurricanes Dennis, Floyd and Irene in 1999 a studyconducted in a lagoonal estuary in the USA reported that toxicdinoflagellates were displaced down-estuary to habitats lessconducive for growth and that commercial landings of bivalvemolluscs or shrimp were not apparently impacted (Burkholderet al., 2004). The authors concluded that such events may serveessential functions of ecosystem renewal through the periodicflushing of sensitive areas and that shallow estuaries frequentlydisturbed by hurricane-level storms can exhibit rapid recovery.

C. Hughes et al. / Estuarine, Coastal and Shelf Science 85 (2009) 377–386378

These examples of the range of responses to an extreme distur-bance event reiterate a common theme in benthic ecology, which isthat the effect on a community depends on a suite of factors. Insituations such as severe perturbations these may include thephysical conditions and features of the biota of the impacted siteand surrounding areas a priori, season, and the characteristics of thestorm or hurricane itself.

Hurricane frequency and severity are subjects of currentinterest, not least because of the potentially devastating impacts onhuman populations of such events. There has been considerablespeculation about the possible increase in hurricane events asa result of global warming. For example between 1971 and 1994the North Atlantic experienced generally low levels of hurricaneactivity, followed by a doubling of overall activity, a 2.5-foldincrease in major hurricanes between 1995 and 2000 and a five-fold increase in Caribbean hurricanes (Goldenberg et al., 2001). Thisreported ‘increase’ in hurricane activity is, however, more likely tosimply be a return to more ‘normal’ levels of frequency and severityafter an anomalously low activity period during the 1970s and1980s caused by a more rapid warming of the atmosphere incomparison to the world’s oceans (Nyberg et al., 2007). However,what is clear is that high levels of hurricane activity between 1995and 2000 were associated with simultaneous increases in NorthAtlantic sea-surface temperatures and decreases in vertical windshear (Goldenberg et al., 2001). Since these changes are generallybelieved to exhibit a multi-decadal time scale it is predicted thatthe current high levels of hurricane activity will persist for another10–40 years (Goldenberg et al., 2001). The effects of a sustainedincrease in the frequency of severe physical disturbance on coastalecosystems cannot be foreseen with a single model, but, byexamining the response of natural communities in different habi-tats exposed to storms of differing severity and regularity, localisedpredictions may be possible.

On 1 September 2003 Hurricane Isabel formed from a tropicalwave that moved westward from the coast of Africa. Over the next17 days Isabel’s strength classification fluctuated, reaching themaximum level (Category 5 on the Saffir–Simpson Hurricane Scale)on 11 September. By the time it made landfall at North Carolina on18 September 2003 Isabel was classified as Category 2, and hadweakened to a Tropical Storm by the time it passed over SouthernVirginia later that day. Isabel caused damage worth over 3 billionUS dollars and the death of w50 people. Wind speeds ofw90 miles h�1 were recorded around Chesapeake Bay, and stormsurges w2.5 m above normal tide levels. Isabel is considered to beone of the most significant tropical cyclones to affect portions ofNorth Carolina and east-central Virginia since the ChesapeakePotomac Hurricane of 1933 and Hurricane Hazel in 1954.

Fortuitously, as part of a wider ecological study, the intertidalinfaunal community of an Eastern Virginian sandflat had beensampled w3 weeks prior to the arrival of Isabel. This presenteda unique opportunity to assess the immediate effects of the hurri-cane and to track the longer-term (w20 months) responses to sucha severe perturbation. The few limited studies that have investi-gated the impacts of storms in the Chesapeake Bay region andsurrounding States have sampled estuaries and their associatedtributaries (Boesch et al., 1976; Knott and Martore, 1991; Mallinet al., 1999, 2002; Balthis et al., 2006). As a result many of thedetrimental ecosystem responses that were reported with regardsto benthos (Boesch et al., 1976; Balthis et al., 2006), phytoplankton(Mallin et al., 2002), water quality (Mallin et al., 1999) fish anddecapods (Knott and Martore, 1991) were inferred to be mainly dueto reductions in dissolved oxygen and salinity caused by highfreshwater flow, leaching from swamp vegetation and contamina-tion from flooded sewage treatment plants and swine wastelagoons. The current study site is located on the seaward side of the

Chesapeake Bay, and due to its close proximity to an inlet linkingthe barrier island system with the Atlantic Ocean, it was notforeseen that the reductions in salinity and water quality seenelsewhere following hurricanes would be likely to occur. Thestretches of barrier islands along the coast of Virginia providea degree of protection from large storm surges. Once breached,however, the water surge resulting from a hurricane may bringwith it an influx of subtidal and pelagic species into the area whichmight be observed in faunal samples collected immediately post-hurricane.

A study carried out by Balthis et al. (2006) on the benthic faunaof the Neuse River System, North Carolina, after 3 sequentialhurricanes in the autumn of 1999 compared post-hurricane datafrom November 1999 with pre-hurricane samples taken from thesame area in July 1999. The authors inferred that storm-relatedreductions in dissolved oxygen and salinity were the most likelycauses of the reduction in the number of benthic species, abun-dances and diversity and a shift in taxonomic composition, but thatit was not possible to separate storm effects from natural succes-sion in the benthos in response to episodes of summer anoxia andhypoxia. In the current study pre- and directly post-hurricanesamples were closer temporally than in Balthis et al’s. (2006) studywhich were taken 3 weeks apart. In our study two samplingoccasions the following year were specifically chosen to temporallymirror these pre- and directly post-hurricane sampling events inan attempt to compare the differences observed in communitystructure after the hurricane, with the same time period thefollowing summer when no storm events occurred. However, withlittle information regarding natural seasonal fluctuations in thebenthic community structure at the study site specifically, andalong the Virginia sea-side barrier island systems more generally,it was envisaged that our sampling strategy might not be adequateto quantifiably separate true storm effects from the naturalsuccessional patterns that may prevail in such ecosystems.

2. Materials and methods

2.1. Study site

Fieldwork was conducted on a back-barrier sandflat withina barrier island–salt marsh–lagoon system along the mid-Atlanticcoast of the U.S. (Fig. 1, N 37�3603100, W 75�3701400). In response tosea-level rise throughout the Holocene this system has experienceda westward movement (Finkelstein and Ferland, 1987). Estimates ofsea-level rise in the region over the past 75 years range between 2.8and 4.2 mm yr�1 (Braatzb and Aubrey, 1987; Gornitz and Lebedeff,1987) and the barrier islands within this system have beenobserved to move westward and change shape in response to sea-level rise and coastal storms (Hayden et al., 1991). The study site isa flood-tidal delta that was initially formed by the deposition ofsand transported from the seaward side of the barrier island whena breach occurred and a new inlet formed in 1997 (Luckenbach,pers. obs.). The opening and closing of inlets within this barrierisland chain are frequently observed in response to coastal storms(Finkelstein, 1988).

2.2. Benthic samples

Pre-hurricane samples were collected on 26 August 2003,23 days before Hurricane Isabel made landfall. The site wasopportunistically re-sampled on 24 September 2003, 6 days afterthe event, then again on 3 April, 17 August and 15 September 2004,and on 25 March 2005. After April 2004, sampling dates werechosen to mirror the previous three sampling occasions and here-after the sampling on 26 August 2003, 24 September 2003 and

Fig. 1. Schematic map of the east coast of America, showing the location of the Eastern Shore of the Chesapeake Bay and the position of the study site within the barrier islandsystem of Wachapreague: (a) before and (b) after Hurricane Isabel.

C. Hughes et al. / Estuarine, Coastal and Shelf Science 85 (2009) 377–386 379

3 April 2004 is collectively referred to as period I, and 17 August2004, 24 September 2004 and 25 March 2005 as period II (see Fig. 2for the sampling strategy timeline). Twenty 10 cm diameter sedi-ment cores were collected on each sampling occasion from thelower mid-tidal level, to a depth of 10 cm (total sediment volume790 cm3). Samples were washed over a 0.5 mm mesh sieve andstored in a cold room for up to 48 h whilst sorting and identification(to Species level where possible) took place. Some organisms wereidentified alive whilst those that required dissection and closerinspection were preserved in 70% ethanol and identified within 1week of collection.

023002nuJyaMrpAraMbeFnaJceDvoNtcOtpeSguA

-erPenacirruh h

IdoirePgnilpmaS

1gnilpmaS

2gnilpmaS

3

Fig. 2. Timeline showing the six sampling occasions

The composition of the communities on each sampling occasionwas investigated using three diversity measures: Shannon–WienerIndex (H0), Pielou’s Evenness and Margalef Richness. Indicesbetween sampling occasions were compared using a one factorANOVA where assumptions of normality and equal variance wereupheld, and Kruskal–Wallis where they were not. A multivariateapproach was used to investigate relative similarities between theinfauna of all cores on all sampling occasions. Resemblance calcu-lations, ordination plots and SIMPER analysis were carried out onSpecies and Order level data (or lowest taxonomic level at whichidentifications were made), with the PRIMER package, version 6

500240raMbeFnaJceDvoNtcOtpeSguAluJ

-tsoPenacirru

IIdoirePgnilpmaS

4gnilpmaS

5gnilpmaS

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and their classification into 2 sampling periods.

C. Hughes et al. / Estuarine, Coastal and Shelf Science 85 (2009) 377–386380

(Clarke and Gorley, 2006). Permutational Multivariate Analysis ofVariance (PERMANOVA) was also used to test for an effect ofsampling occasion, and to perform all resulting pairwise compari-sons (Anderson, 2001). Comparisons based on feeding guildcomposition were also carried out between sampling occasions.Feeding guilds were categorised according to the main mode(s) offeeding (see Fauchald and Jumars,1979; Dauer et al., 1981; Manningand Felder, 1991; Cragg et al., 1999; Arruda, 2003): (1) surfacedeposit feeder; (2) sub-surface deposit feeder; (3) suspensionfeeder; (4) errant predator; (5) errant omnivore; (6) interface feeder(organisms that switch between deposit feeding and suspensionfeeding in response to physical conditions and competition fromother organisms); (7) mesograzer; and (8) other.

3. Results

Both number of species and total number of organisms variedsignificantly with sampling occasion (Table 1B) with three-fold andeight-fold increases, respectively, between period I and II averages(Table 1A), although measurements made directly after Isabelwere not significantly different from the pre-hurricane samples(Table 1C). Dunn’s pairwise value for number of species was close tothe critical value and there was a two-fold increase after thehurricane, but since this difference was proportionally much lowerthan comparisons with sampling occasions from period II the result

Table 1Summary of the differences between the infaunal community composition of Cara’s flaoccasion the numbers in parentheses indicate the sampling period. (A) Values shown are mand organisms are numbers per 790 cm3 core. In each case n¼ 20 except for pre-hurricwhere Margalef Species Richness n¼ 10 and Pielou’s Evenness n¼ 9. (B) The effect of samall variables. Comparisons for all variables were performed using the Dunn’s procedure, exvalues are differences between ranks/SD (column heading value in parentheses is the crmeans (first sampling occasion in column 1 subtracted from the second), minimum squardifference at p� 0.05.

Sampling occasion Number of species Number of organisms

(A)Pre (August 2003) (I) 2.0 (0.95) 7.5 (9.25)September 2003 (I) 4.0 (1.42) 10.5 (14.31)April 2004 (I) 1.0 (0.95) 1.5 (1.5)August 2004 (II) 8.0 (2.01) 60.0 (27.85)September 2004 (II) 6.5 (1.18) 43.0 (15.14)March 2005 (II) 5.5 (2.14) 54.9 (5.86)

Variable Sampling occasions Transformation

(B)Number of species All NoneNumber of organisms All minus April 2004 Square rootPielou’s Evenness All minus April 2004 Square rootShannon–Wiener Index All NoneMargalef Species Richness All None

Pairwise comparison Variable

Number ofspecies (2.94)

Numberorganism

(C)Pre (August 2003) (I) vs September 2003 (I) 2.47 1.11Pre (August 2003) (I) vs April 2004 (I) 1.18 –Pre (August 2003) (I) vs August 2004 (II) 5.92 6.06Pre (August 2003) (I) vs September 2004 (II) 5.41 5.07Pre (August 2003) (I) vs March 2005 (II) 4.30 5.59September 2003 (I) vs April 2004 (I) 3.65 –September 2003 (I) vs August 2004 (II) 3.45 4.95September 2003 (I) vs September 2004 (II) 2.94 3.96September 2003 (I) vs March 2005 (II) 1.83 4.48April 2004 (I) vs August 2004 (II) 7.10 –April 2004 (I) vs September 2004 (II) 6.59 –April 2004 (I) vs March 2005 (II) 5.48 –August 2004 (II) vs September 2004 (II) 0.51 0.99August 2004 (II) vs March 2005 (II) 1.62 0.47September 2004 (II) vs March 2005 (II) 1.11 0.52

was not statistically significant. Based on the measures used, theonly significant difference between the pre-hurricane andSeptember 2003 (directly post-hurricane) sampling occasions wasan increase in species diversity (H0) after the hurricane.

Few organisms were collected in the April 2004 samples. Thusthese samples were not considered when investigating differencesbetween sampling occasions for total number of organisms andPielou’s Evenness because the samples skewed the combined dataand limited the choice of tests. Ignoring any pairwise comparisonsinvolving the April 2004 samples, there is an obvious trendtowards significant differences prevailing between the inter-periodcomparisons; only two of all the remaining significant differenceswere between sampling occasions from the same period (Table 1C).Based on five measures of community structure, the longer-lastingeffect of Hurricane Isabel was, therefore, less apparent than thesubsequent successional changes and the resulting differencesbetween seasons.

Comparison of the fauna from samples taken directly pre- andpost-hurricane, showed a clear difference between sampling occa-sions based on community composition. However, six of the twentypost-hurricane samples contained distributions of organisms thatwere more similar to those in the pre-hurricane samples than otherpost-hurricane samples (Fig. 3). SIMPER analysis revealed thatthe average dissimilarity between these pre- and directly post-hurricane infauna was 61%, with an increase in the bivalve Tellina sp.

t at 6 sampling occasions: 1 pre-Hurricane Isabel and 5 post-storm. For samplingedians (SD) for all except Pielou’s Evenness which are means (SE). Number of species

ane where Margalef Species Richness and Pielou’s Evenness n¼ 19, and April 2004pling occasion. (C) Pairwise comparisons between all relevant sampling occasions forcept Pielou’s Evenness which employed the Bonferroni test. Dunn’s procedure outputitical value for significance). Bonferroni test output values are differences between

e-root difference required for significance¼ 0.32. Values in bold indicate a significant

Pielou’s Evenness Shannon–Wiener Index Margalef Richness

0.73 (0.06) 0.66 (0.34) 1.03 (0.54)0.77 (0.05) 1.10 (0.32) 1.78 (0.52)0.97 (0.02) 0.01 (0.45) 1.44 (0.51)0.48 (0.04) 0.97 (0.42) 1.70 (0.49)0.51 (0.02) 1.04 (0.20) 1.47 (0.31)0.63 (0.04) 1.09 (0.30) 1.21 (0.47)

Test used Test statistic DF p

Kruskal–Wallis H¼ 86.23 5 <0.001Kruskal–Wallis H¼ 62.67 4 <0.0011 Factor ANOVA F¼ 27.49 4 <0.001Kruskal–Wallis H¼ 38.27 5 <0.001Kruskal–Wallis H¼ 15.95 5 0.007

ofs (2.81)

Pielou’sEvenness

Shannon–WienerIndex (2.94)

Margalef SpeciesRichness (2.94)

0.03 3.59 2.44– 1.02 1.340.43 2.56 3.030.40 2.75 2.340.27 3.63 0.66– 4.61 1.100.39 1.03 0.590.37 0.84 0.110.24 0.04 1.77– 3.58 1.69– 3.77 0.99– 4.65 0.67�0.02 0.19 0.70L0.16 1.06 2.36�0.14 0.87 1.66

Fig. 3. Two-dimensional configurations for MDS ordinations of community species(or lowest taxonomic level possible) abundance data collected pre- (B) and post-Hurricane Isabel; September 2003 (;), April 2004 (,), August 2004 (6), September2004 (C) and March 2005 (þ). Data were fourth-root transformed, n¼ 20 for eachsampling occasion: (a) pre- and directly post-hurricane only, stress¼ 0.23; (b) allsampling occasions. A dummy species was added, stress¼ 0.21.

Fig. 4. Two-dimensional configurations for MDS ordinations of community Orderabundance data collected pre- (B) and post-Hurricane Isabel; September 2003 (;),April 2004 (,), August 2004 (6), September 2004 (C) and March 2005 (þ). Datawere fourth-root transformed and a dummy species added. n¼ 20 for each samplingoccasion. Stress¼ 0.20.

C. Hughes et al. / Estuarine, Coastal and Shelf Science 85 (2009) 377–386 381

and the addition of tubificid oligochaetes contributing most to theobserved differences. Prior to Isabel the polychaete Streblospiobenedicti had dominated the sandflat community accounting forw86% of the similarity between all pre-hurricane samples (Table 2).However directly post-hurricane the contribution of this polychaeteto intra-sampling occasion similarities was reduced to w53%, andthereafter no single species showed a contribution of more thanw40% within any particular sampling occasion. This indicates a shiftfrom a community numerically dominated by one species, to a morediverse, species rich community, as also demonstrated by a generalincrease in the number of species, the Shannon–Wiener Index andMargalef Richness values over the duration of the investigation(Table 1). Fig. 3 demonstrates no obvious increase in sample

Table 2Five most commonly occurring species at each sampling occasion. Numbers in parentheseto the overall similarity of samples from within the same sampling occasion.

Pre-hurricane Post-hurricane

Aug 2003 Sept 2003 Apr 2004 Au

Streblospio benedicti (86) Streblospio benedicti (53) Sipunculid (43) StrTellina sp. (7) Tellina sp. (28) Tellina sp. (39) CirSpio filicornis (1) Tubificidae (5) Leitoscoloplos fragilis (13) MeParanaitis speciosa (1) Sipunculid (4) Streblospio benedicti (1) GlyAmpelisca verrilli (1) Cirriformia grandis (1) Spio filicornis (1) Mic

variability post-hurricane, as is often the case following a pertur-bation (Warwick and Clarke, 1993), with levels of similarity in thisstudy between the fauna in pre- and post-hurricane samples of 48%and 45% respectively.

Due to the sparseness of organisms in the April 2004 samplesa dummy species was included in the analysis where all samplingoccasions are viewed on the same multi-dimensional configuration(see Clarke et al., 2006). Each sampling occasion demonstrates areasonable level of separation from all other sampling occasionswith the greatest degree of overlap occurring between pre- andpost-hurricane, and August and September 2004 communities(Fig. 4). PERMANOVA carried out on fourth-root transformedspecies abundance data confirmed a significant effect of samplingoccasion on species composition (F5¼17.27, p< 0.001). Subsequentmultiple comparisons revealed that each sampling occasiondiffered significantly from every other occasion (t¼ 2.28–4.26, all atp< 0.001). When the taxonomic resolution was reduced fromSpecies to Order a similar arrangement of samples on a multi-dimensional ordination was observed (Fig. 5). There was lessseparation at this taxonomic resolution, however PERMANOVA stillrevealed a significant effect of sampling occasion (F5¼15.79,p< 0.001). Significant differences were also shown between eachpair of sampling occasions (t¼ 2.54–6.47 all at p< 0.001) althoughsimilarities ranged from 13% between April 2004 and September2004, to 61% between August 2004 and September 2004.

The change in abundance over time for most Orders, could bebroadly classified into 3 response categories: (1) those with low orzero population densities before the hurricane, no measurableincrease directly post-storm, yet significantly higher densities inperiod II (Fig. 6a–d); (2) those with moderate population densitiesbefore the hurricane, a slight or measurable increase in numbers

s indicate the percentage (to the nearest integer) contribution of a particular species

g 2004 Sep 2005 Mar 2005

eblospio benedicti (40) Streblospio benedicti (42) Streblospio benedicti (38)riformia grandis (12) Spio filicornis (23) Mediomastus ambiseta (30)diomastus ambiseta (10) Capitella capitata (14) Gemma gemma (21)cera dibranchiata (9) Ampelisca verrilli (7) Tellina sp. (4)rura sp. (7) Tellina sp. (5) Sipunculid (1)

M'05S'04A'04Ap'04S'03Pre

2000

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0M'05S'04A'04Ap'04S'03Pre

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15

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0

Capitellida Spionida Littorinimorpha

Heteronemertea Phyllodocida Sipunculid

Cirratulida Amphipoda Tubificida

Eunicidae Orbiniida Veneroida

a e i

j

k

l

f

g

h

b

c

d

Fig. 5. Summary of Order (except the Phylum Sipuncula) abundances (numbers m�2) (y axis) over the 6 sampling occasions; pre- (Pre) and post-Hurricane Isabel; September 2003(S’03), April 2004 (Ap’04), August 2004 (Au’04), September 2004 (S’04) and March 2005 (M’05) (x axis). Error bars are upper side of 1 standard error of the mean.

C. Hughes et al. / Estuarine, Coastal and Shelf Science 85 (2009) 377–386382

post-storm, continuing to rise during sampling period II (Fig. 6e–h);and (3) those with low or zero population densities before thehurricane, a measurable increase in numbers post-storm, followedby a decline in period II (some then rising again in March 2005). The

Fig. 6. Two-dimensional configurations for MDS ordinations of feeding guild abun-dance data collected pre- (B) and post-Hurricane Isabel; September 2003 (;), April2004 (,), August 2004 (6), September 2004 (C) and March 2005 (þ). Data werefourth-root transformed and a dummy species added. n¼ 20 for each samplingoccasion. Stress¼ 0.18.

taxa responsible for most of the dissimilarity between the pre- andpost-hurricane samples primarily fell into category 3 whereasthose responsible for the obvious divide between communitystructures in periods I and II fell mainly into categories 1 and 2.

When the fauna were considered in relation to feeding guilds,the separation between each sampling occasion was reduced,particularly for collections within period II (Fig. 7). Samplescollected in August 2003 and September 2003, and August 2004and September 2004 respectively showed closest similarity to eachother. It is clear that the community composition of most samples ismore similar to that of other samples within the same samplingperiod, again indicating successional changes in the organismspresent on the sandflat. Samples taken in April 2004 and March2005 exhibited community compositions that appeared relativelydiscrete from all others. Although all results for April 2004 shouldbe viewed with some caution due to the low number of totalorganisms collected, it is interesting to note the high relativeabundance of suspension feeders on this sampling occasion, as wellas in March 2005 (Fig. 7).

The most notable direct effects of Hurricane Isabel on the rela-tive abundances of feeding guilds were a reduction in the numberof interface feeders (Pre¼ 87%, Post¼ 64%), an increase in surfacedeposit feeders (Pre¼ 7%, Post¼ 20%), and an increase in thenumber of feeding guilds present (Pre¼ 6, Post¼ 8) (Fig. 7). Thepercentage of interface feeders present in August 2004 was similarto that pre-hurricane in August 2003 (82%) whilst the proportional

Fig. 7. Relative percentage abundance of feeding guilds at the 6 sampling occasions;pre- (Pre) and post-Hurricane Isabel; September 2003 (S’03), April 2004 (Ap’04),August 2004 (Au’04), September 2004 (S’04) and March 2005 (M’05). Values abovebars represent the total number of organisms collected at each sampling occasion.

C. Hughes et al. / Estuarine, Coastal and Shelf Science 85 (2009) 377–386 383

representation of deposit feeders remained higher than pre-hurricane (13%). The relative similarity between the feeding guildcomposition of samples taken in August and September 2004 wasmuch greater than between the same 2 months of the previousyear, suggesting that Hurricane Isabel had a greater effect oncommunity composition than might have been expected fromnatural seasonal changes.

Although no sediment composition data were available at thestudy site, visual changes were observed in the sediment type andtidal circulation systems supplying sediment to the area throughoutthe study (Hughes and Luckenbach, pers. obs.). The study area hada surface layer of finer sediments directly post-hurricane which waslikely to have been transported from a nearby mudflat and the outerbarrier islands. These finer sediments persisted throughout thesubsequent sampling occasions, which may in part be due to thein-filling of the channel separating the flood-tidal delta from anearby (w30 m distant) mudflat adjacent to a Spartina alternifloramarsh.

Overall, the benthic infaunal community of the sandflatexhibited a doubling of species, a significant increase in diversity(H0) and a shift in feeding guild composition within a few days ofIsabel impacting the area. However, the most marked differences inthe benthic community were seen in the subsequent successionalchanges that took place over the following 20 months, such that, bythe end of the study period there was significantly increasednumber of species, faunal abundances and community diversity,suggesting a potentially positive medium-term effect of the hurri-cane perturbation.

4. Discussion

Temporal variations in the abundance of marine soft sedimentfauna have been recognized at scales which are smaller than thosegenerally studied in most field experiments (Morrisey et al., 1992;Olabarria and Chapman, 2002). Morrisey et al. (1992) foundsignificant variations in the macrofauna of sediments in Botany Bay,Australia at all temporal scales investigated, from days to months,and argued that without sufficient information regarding the vari-ations that occur at smaller scales, comparisons across longer time-scales were likely to be confounded. We fully recognize theseconcerns, and accept that a seasonally nested, hierarchical samplingdesign may have been a more effective way of accounting for

differences at temporal scales. However, since this study was purelyopportunistic in its nature there was no opportunity prior to thehurricane disturbance to initiate such an approach. Severe pertur-bations such as those produced by hurricanes are relatively infre-quent and the data obtained following disturbance by HurricaneIsabel provide a valuable insight into potential storm-initiatedeffects.

Following the hurricane there was no significant increase in thenumber of organisms but a significant increase in diversity (H0)indicating a storm-initiated change in the assemblage structure andthe appearance of rarer species. For example, several taxa that wereabsent, or present at very low densities before the hurricane, werecollected 6 days after the hurricane when there was also a doublingin the average number of species. These increases may haveoccurred via the physical import of individuals from other neigh-bouring habitats during the storm itself, or the subsequent activeimmigration of species during the post-storm period. Redistribu-tion of fauna by wave action, and the part this process can playin the formation of benthic associations has been recognized ina variety of benthic habitats (e.g. Rees et al., 1977; Barry, 1989). Theapproximately five-fold increase in tellinid bivalve abundancebetween the pre- and post-hurricane samples was likely to be theresult of the physical import of individuals during the hurricane,since these infaunal bivalves have limited mobility and were clearlytoo large to have resulted from a new settlement event. Waveimpacts of Isabel were reported in Onslow Bay, North Carolina, forw4.5 days following the hurricane (Wren and Leonard, 2005) andsimilar observations following the storm were noted in the vicinityof our study area (Luckenbach, pers. obs.). We hypothesize thatthese waves transported many subtidal and low intertidal tellinidsfurther up the shore into the intertidal zone.

Passive and active colonization of disturbed areas have beenobserved in field manipulations, occurring at different ratesdepending on the nature of the disturbance (Savidge and Taghon,1988). In treatments where sediment was manually removed andwhere new material quickly accumulated, the numbers of organ-isms increased rapidly following the initial disturbance. Savidge andTaghon (1988) concluded that the observed re-colonization was theresult of both passive advection and, in the case of the appearance ofmore opportunistic species (e.g. capitellids and oligochaetes), activeimmigration. In the present study the appearance of tubificidoligochaetes shortly after the hurricane disturbance is likely to bea response to the availability of new resources e.g. organic detritusand space, and represents an example of immigration directly post-storm. Oligochaetes are opportunistic colonizers and are consideredhighly adaptive surface-burrowers that can take advantage ofnewly disturbed sediments where there is a high organic detritalfood component (Dreyer et al., 2005). They have also been shown toemigrate from areas of depleted organic detritus and, under suchconditions, to exhibit changes in their reproductive strategy(Junkins et al., 2006). Oligochaete populations undergo seasonalcycles of population growth and may crash during the summer asfood supplies are depleted (Cheng et al., 1993). The appearance ofhigh densities of oligochaetes in the sandflat during September2003 immediately after Isabel is probably indicative of the suddenavailability of a fresh detrital food source following disturbance ofthe sediment. The low abundances which were then observed onall future sampling occasions are likely to have been caused initiallyby depletion of this detrital food supply, and then subsequentlymaintained by competition from other organisms. This kind oftemporal pattern of distribution can be explained by the tolerancemodel of ecological succession, in which bare patches of sedimentcan be colonized by any species, but the ability to tolerate reducedresource levels determines which species will exclude the otherspecies (Barradas et al., 1996).

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The anecdotal evidence suggesting a change in sediment typeon the sandflat following Hurricane Isabel is supported by otherobservations made during the same storm event. Transport ofsuspended material into the coastal waters of Onslow Bay, NorthCarolina during Hurricane Isabel was an order of magnitude greaterthan during a previous severe storm at the same site in 2000 (Wrenand Leonard, 2005). Moreover, Wren and Leonard (2005) observedreworking of the sediment to a depth of 5 cm suggesting that thesediment characteristics at our study site may have been signifi-cantly altered as a result of Isabel. In 1972, cores from the York Riverwithin Chesapeake Bay, provided evidence of river-wide mixing ofthe sediment sub-layer which was attributable to Tropical StormAgnes, and demonstrated that storms can contribute significantlyto the mixing of surface sediment layers (Dellapenna et al., 2003).Although no sediment data were collected during the currentstudy, casual observations suggest an increased abundance of finerparticulate material immediately following the hurricane distur-bance. This increase in fine particulate material may explain thew3-fold increase in the proportion of deposit feeders during the6 days post-hurricane since finer, more organically rich, sedimentsfavour the establishment of these organisms (Sanders, 1958). Thealteration of the study site since Hurricane Isabel, i.e. mergingwith a nearby muddier flat that is dominated by organically richdecaying Spartina, and personal observations of the persistence offiner sediments, are likely to account for the higher proportion ofdeposit feeders in August 2004 than at the same time the previousyear, before the hurricane. The availability of sedimentary organicmatter generally varies seasonally, with highest values in latewinter/early spring, followed by a reduction during the summermonths as supplies are depleted with little replenishment (Rossiet al., 2001). Deposit-feeder populations often display a similarlagging trend, and the proportion of deposit feeders in period IIappears to demonstrate this more typical seasonal pattern whereasperiod I, with the occurrence of Isabel in late summer, exhibited anunusual increase in deposit feeders between August and September2003. During the winter (November–April) the environmentalconditions at Wachapreague (seawater temperature w3–4 �C andair temperature around �8 �C) result in minimal biological activityand low productivity, conditions that are sub-optimal for depositfeeders that have a predilection for organic matter. The paucity oforganisms and proportionally higher numbers of suspensionfeeders in the April 2004 and March 2005 samples probably reflectthese conditions.

Although these patterns of deposit-feeder populations are ofinterest and may well be linked to detrital food availability, some ofthe organisms classified as interface feeders also obtain food bymeans of deposit feeding. Most interface feeders in this study werespionid polychaetes which are known to switch between depositfeeding, suspension feeding, and a combination of the two, in orderto eliminate potential interference interaction with other organ-isms (Dauer et al., 1981). Without field observations of the feedingbehaviour of these interface feeders it is difficult to infer the directeffect of the post-hurricane succession on the relationshipsbetween the different deposit and suspension-feeding guilds.However, it is logical to assume that under certain conditions whensolely deposit feeding organisms are abundant, spionids and otherinterface feeders may well utilize their suspension-feeding abilitiesto a greater extent.

That significant differences between all sampling occasionswere retained even when the taxonomic resolution was reducedfrom Species to Order indicates some level of taxonomic redun-dancy. Studies that have examined existing data sets have oftenfound that little information, regarding relative differencesbetween samples, is lost when the taxonomic level is reduced(Olsgard et al., 1997; Olsgard and Somerfield, 2000). Moreover,

Olsgard and Somerfield (2000) noted that identification to Familylevel may be satisfactory in many routine monitoring studies.However, in the current investigation some organisms could onlybe identified to Order level due to the inadequate keys for the localfauna, consequently analysis at the Order level was seen as themost appropriate approach to identifying taxonomic redundancy.The results from this element of the study concur with the growingconsensus that in situations where comparisons are simplyrequired with regard to inter-sample relationships, identification toa higher taxonomic level is indeed adequate. Clarke and Warwick(1998) suggest that the level of structural redundancy may, in somecases, be an indirect measure of the resilience or compensationpotential within an assemblage. If this is the case and speciesappear to respond to environmental change in a similar way toother species within the same taxonomic grouping, then thenumber of taxonomic level reductions which result in little changeto the inter-sample relationships may be regarded as a measure ofthe potential for functional compensation (Clarke and Warwick,1998). Since the relative similarity between all samples is main-tained at the Order level it would appear that the infaunalcommunity at the current study site has a high resilience to change.This may be a response to life in a highly dynamic and naturallychanging environment where the resources and competition forspace and food are constantly changing.

Connell’s (1978) Intermediate Disturbance Hypothesis suggeststhat the highest species diversity is maintained at intermediatescales of disturbance. With little information available regardingbenthic community structure at the study site prior to this inves-tigation it is difficult to say whether the low species diversity thatpersisted was simply due to the coarse nature of the sedimentwhich characteristically supports fewer species than finer sedi-ments (Little, 2005) or to the frequency of disturbance events. Thelast recorded storm to pass over Wachapreague, Virginia, wasTropical Storm Allison in June 2001. This 27-month period betweensignificant storm disturbances is likely to have allowed competitorsthat were either more efficient in exploiting limited resources,interfering with other species (or both), or the most resilient todamage or death, to survive, keeping diversity low (Connell, 1978).When Isabel then hit in September 2003 it caused a disturbancesufficient to reduce dominance within the benthic community andthrough subsequent successional changes the species abundancesand diversity were significantly increased.

Although our study has demonstrated a potential immediateeffect of Hurricane Isabel, together with subsequent successionalchanges in the intertidal infaunal community we urge caution ininferring mechanisms of change from post-perturbation datawhen insufficient pre-perturbation data exist, when data are notcollected in such a way that takes account of potential variability atdifferent scales of time and space and/or when there are inade-quate data on physical changes in the habitat. Future studiesattempting to assess the effects of storm events or any otherphysical disturbance (natural or anthropogenic) when little pre-event data are available, are likely to benefit from undertakinga beyond ‘‘Before–After-Control-Impact’’ (BACI) (e.g. Underwood,1992) approach if enough control sites can be identified andsampled post-event. Since most natural populations fluctuatetemporally in ways that are not the same at two or more locationsa sampling design that allows adequate assessment of ‘natural’temporal and spatial variability is required if any true causal effectof a perturbation can be concluded (Underwood, 1994). If a trueeffect of a disturbance event exists then there will be greatercommunity structure differences between the impacted andcontrol locations than among the control locations. Data fromcontrol sites collected post-perturbation can also in some situationsbe treated as pseudo-before-impact samples in the beyond BACI

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design, allowing opportunistic studies such as this one to morereliably attribute real storm effects (if any exist) to the changesobserved (see Underwood, 1992 for a comprehensive discussion ofsuch designs). However, in reality implementing the ‘ideal’sampling strategy may not always be practical or even possible. Insituations where perturbations such as hurricanes impact largeareas of coastline, the possibility of finding shores with similarphysical features and biological communities that were undis-turbed by the storm event, yet are close enough to the impactedsite(s) so as not to introduce significant spatial artifacts into theanalysis, are rare. Hence, anyone attempting to undertake a study todetermine the effects of natural disturbance events should have anappreciation of the ‘ideal’ sampling strategy, which may involvemultiple pre- and post-perturbation sampling events for impactedand undisturbed sites, but to accept that this approach may literallybe impossible due to the very nature of the disturbance. In suchcases where the favoured sampling strategy is not possible theresults obtained may still lead to some interesting theoriesregarding the short and longer-term effects of the perturbation onbenthic communities, but we must remind ourselves that suchtheories remain speculative without the opportunity for robuststatistical analysis.

5. Conclusions

The study has demonstrated that some of the increases in thenumber of species and species diversity (H0) that were observedpost-hurricane arose as a direct result of the physical and biologicalchanges brought about by the storm. However it was less clearwhether all of the post-hurricane community changes could beattributed to hurricane induced habitat changes as opposed to thenatural successional patterns that occurred in the dynamic barrierisland environment. The absence of long time series of pre-perturbation data could complicate an adequate assessment of theeffects of storms on benthic communities from those effects arisingfrom ‘natural’ temporal and spatial changes in communitystructure.

Acknowledgements

The authors would like to thank all staff at the Virginia Instituteof Marine Science, Eastern Shore Laboratory for all their field andlaboratory support, in particular Messers S. Fate and A. Birch.The Drapers’ Company, London, is thanked for its financial supportto C.H.

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