Classification and community structure of macrobenthos in the Hampton Roads area, Virginia

l~iarine Biology 21,226-244 (i973) �9 by Springer-Verlag t973

Classification and Community Structure of Macrobenthos in the Hampton Roads Area, Virginia*

D. F. Boeseh

Virginia Institute of Marine Science; Gloucester Point, Virginia, USA and

Department of Zoology, University of Queensland; Brisbane, Australia

Abstract

Benthic macrofauna was sampled by grab at 16 stations in Hampton Roads and the adjacent Elizabeth River, Virginia, USA. Samples were taken in February, May and August. Sampling sites and species were grouped by a classification strategy which basically consisted of the Canberra metric dissimilarity-measure and flexible and group average clustering. Following reallocations, 8 site groups and t6 species groups instructively classified the 47 sites and 93 species considered in the analysis. The sites were grouped into "associations" on mud, muddy-sand and sand-bottoms, and those in the Eliza- beth River. Species groupings distinguished a few species most frequent at Elizabeth River or mud and muddy-sand sites, larger numbers of species restricted to muddy-sand and sand or solely to sand sites, ubiquitous species, epifaunal species which were microhabitat-restricted, and seasonal species. An analysis of numerically dominant species in the different associations indicated the relative importance of ubiquitous species and seasonally abundant species. Community-structure statistics (species diversity, species richness and evenness) showed definite spatial and temporal patterns. Diversity was high at sand and muddy-sand sites and low at mud and Eliza- beth River sites. This spatial pattern was predominantly one of species richness. At Elizabeth River and mud stations, diversity increased from February to August because of increased evenness, while at sand and muddy-sand stations, diversity peaked in May in response to both high species richness and high evenness. The applicability of "community concepts", the causes of substrate specificity, seasonality and species diversity, and the effects of pollution on community structure are discussed.

Introduction

In marine biology, two approaches have recently been followed to simplify and extract information from the very complex patterns and events evidenced by collections of multispecies populations. The first is c l a s s i f i c a t i o n in which collections are classified on the basis of their biotic content, or species are classified on the basis of their distribution within a series of collections according to some mathematical criteria. Some examples are Jones (i969), Ebeling et al. (i970), Lie and Kelley (t970), Stephenson et al., (i970), Hughes and Thomas (1971a, b), Field (i974), and

* Contribution No. 553, Virginia Institute of Marine Science, Gloucester Point, Virginia, USA.

Thorrington-Smith (1971). The second approach is the analysis of " c o m m u n i t y s t r u c t u r e " , in which the distribution of importance (as measured by one of a number of criteria, usually abundance) among species is of pr imary interest. This includes such aspects as species diversity and its components, dominance, constancy, and periodicity. Recent marine examples include Dahlberg and Odum (i970), Lie and Kisker (1970), McCloskey (t970), Timonin (i97i), and Travers (197i).

Seldom have these two approaches been combined, even in terrestrial plant ecology, where distributional patterns and events are bet ter known. Nonetheless, their combination could prove mutual ly enhancing. This s tudy is an a t t empt at such a combination of approaches and involves the classification by "ob- ject ive" criteria of collections of maerobenthic animals from an estuarine harbor, and analysis of the composition, community structure, and seasonal dynamics of the resulting associations. Mathematical techniques are descriptively and analytically employed to aid the efficient extraction of important information and the simplification of complex structure.

Study Area The area studied was the Hampton Roads port

area, a multi-use harbor which lies between Norfolk and Newport News, Virginia, USA (Fig. t). Hamp to n Roads covers approximately 65 km 2 at the confluence of the Chesapeake Bay and the James River estuary. The James River contributes a significant portion, i4%, of the total fresh-water discharge of the Chesa- peake Bay system. The Nansemond, Elizabeth, and Hampton rivers are tidal tributaries of Hampton Roads and discharge little freshwater. The Roads has extensive shoals (less than 6 m deep} and a deep central channel (8 to 22 m). Navigation channels of i2 to i4 m are maintained into the James and Elizabeth Rivers. Tidal range in the James estuary is about

D. F. Boesch: Classification and Community Structure of Macrobenthos 227

Fig. I. Hampton Roads area, Virginia, USA, showing location of 16 benthic sampling stations. 6 m isobath indicted

30-

0 0

20-

E i~ 10"

9 6/l!~ \ 9 , ~ , . - - - ~ 8

'P-'/lo \

\ ' ,

i ', 4 \ ,

. . . . Surface --.N~.. " 7m 1

0 . . . . I . . . . I

15 20 25 Salinity (%0)

Fig. 2. Salinity-temperature polygons for location off Newport :News Point (near station D2) for 1969 (unpublished records, Virginia Institute of h[arine Science). Measurements made

monthly (numbers), at slack-water, before flood tide

0.8m, and tidal current velocities rarely exceed 2 m/sec.

Salinity and temperature at the surface and at a depth of 7 m for a location off Newport News Point

30 Marine ]~iology, Vol. 21

during i969 (including the sampling dates) are presented in Fig. 2. Deep bottoms experienced conditions similar to those at 7 m, and benthos on the shoals experienced near-surface conditions. The temperature range was more than 25 C o , but the total salinity range during i969 was only 3 to 420. Fluctuations during a tidal cycle were slight. Salinities were lower than normal from September to November, 1969, due to floods caused by excessively heavy rainfall. Reduced and more variable salinities may have occurred at some of the sampling locations in the Elizabeth River, but f ragmentary data indicate salinity did not drop below t 5 %o there.

The Hampton Roads area is heavily influenced by activities related to shipping (overboard disposal, oil pollution, dredging), municipal and industrial waste disposal, and "land reclamation".

Methods

Field and Laboratory Sixteen stations (Fig. i) were sampled in early

February, early May, and early August, 1969, except tha t Station E8 was not sampled in February. Three replicates were obtained at each station with a 0.06 m ~ Foerst-Petersen grab in February and a 0 .07m ~ modified van Veen grab in May and August. The con- tents of the grabs were sieved through a i .0 mm mesh screen and the portion retained fixed in 10 % formalin. Animals were removed from debris by examination under a dissecting mi-'croscope, identified, and counted.

Both grabs functioned well in muddy sediments and usually filled to capacity. The heavier van Veen grab proved superior in sandy sediments, and repeated a t tempts were often necessary to secure adequate samples in sand with the Foerst-Petersen grab. In all cases, only swift or deep-burrowing animals, which were numerically unimportant , could escape being sampled.

A fourth grab was taken in February (May at Station E8), and a sediment sample was removed from the relatively undisturbed sediment surface. Sediment particle-size distribution was determined by sieving, and pipette analysis following the procedures of Folk (i961), after disaggregation in 4% sodium hexametaphosphate (Calgon) solution for 24 h.

Classification Historically, the classification of marine bot tom

communities has been based on dominants or "characterizing species" (Thorson, 1957). Only a small portion of the many species present were used as attr ibutes on which to classify; the considerable information contained in the distribution of the remainder of the species was not utilized. The bias towards dominance remains in numerical classifications using the Czekanowski similarity-coefficient and its derivatives (e.g. percentage similarity, Bray-

228 D. ~. Boesch: Classification and Community Structure of Macrobenthos Mar. Biol.

Curtis) (Field, 1971), and especially with the non- standardized Euclidean distance measure (Orloci, t967).

Initial appraisals of the data indicated tha t many of the dominant species were ubiquitous; therefore, a classification strategy tha t is unbiased towards dominance, yet includes both qualitative and quanti- tat ive criteria, seemed most desirable. Stephenson (Stephenson et al., t972, and personal communication) has found the Canberra "metr ic" dissimilarity coefficient (Lance and Williams, 1967) efficacious in marine survey work, and it fulfills the above criteria. The dissimilarity of two individuals is defined as:

dl 2 = I ~ (z~, - x~,)

' ~ i

where x l / and xei are the importance values of the ith at tr ibute of the two individuals. The coefficient is constrained between 0 and I and, because it is the sum of a series of fractions, it is at tr ibute serf-standardized. This means tha t one attr ibute cannot overwhelm the index. In case of single zero matches (i.e., when one but not both of the x~ is zero), the zero can be replaced with a small eonsgent (e) smaller than the smallest data entry, so that the dissimilarity between zero and a large number becomes greater than between zero and a small number. Double zero matches usually have little meaning in ecology, and are sup- pressed. Symmetrical dissimilarity matrices can be computed with sites (collections) as individuals, and species as attributes ( n o r m a l a n a l y s i s ) ; or with species as individuals, and sites as attributes ( i n v e r s e a n a l y s i s ) .

A scale problem exists with all metric coefficients, including the common Euclidean and Manhat tan metrics (Williams, t97t) and coefficients derived from metrics, such as the Canberra "metric", in tha t so long as the x j s are very much larger than the x2~'s, a high dissimilarity will result, no mat te r what the degree of co-occurrence or correlation of attributes between t and 2. This problem can be overcome by s t a n d a r d i z a t i o n of the individuals (Noy-Mier, t97t). I t is desirable to compute both normal and inverse dissimilarity matrices from a single-data matr ix; however, standardization by site will not solve scale problems in the inverse analysis and, conversely, standardization by species will not solve site-scale differences. Therefore, a double standardization based on "rows and columns" seemed appropriate. Austin and Noy-Mier (t97t) found a simultaneous double standardization more helpful in solving problems of nonlinearity in ordination models than stepwise double standardization of the type used by Bray and Curtis (t957). Simultaneously double- standardized values in the data matrix become

y~J xi./= "(Z y~ Zyv) ~ '

where Yij is the unstandardized element of the ith row and ]th column.

From symmetrical inter-individual dissimilarity matrices, individuals may be clustered into related groups. This can be done most efficiently by one of the agglomerative hierarchical clustering strategies (Williams, 197t), in which individuals are successfully grouped and their relationships optimized in a dendrogram. Following Stephenson et al. (1972), two different clustering strategies were used - - one space-dilating and intensely clustering, and the other space-conserv- ing and weakly clustering. The intense strategy used is Lance and Williams (i967) "flexible sorting", in which the "cluster intensity coefficient"/3 was set at the now-conventional value of --0.25. The weaker strategy used is the common "group-average" sorting, als:o known as the unweighted pair-group method (Sokal and Sheath, 1963).

In summary, the classificatory analysis used for both normal and inverse analyses was a combination of simultaneous double standardization, Canberra Netric coefficient with e = 0.001, and both flexible and group-average clustering. Computations were performed by CDC 3600 computer at the CSIRO Computing Centre, Canberra, Australia, using the program CLASS (Lance and Williams, i967), with appropriate modifica- tions.

Communi ty Structure

Informational species diversity indices express the distribution of " importance" among species in a collection in an instructive manner (Boesch, i972). Theoretically, they express the uncertainty in the prediction of the identity of a randomly selected individual from the collection. Shannon's formula (Pielou, 1966) was used:

H' = - ~p~ log 2 p~,

where Pi is the proportion of individuals belonging to the ith species. Species diversityhas a "species richness" component and an "evenness" component (Lloyd and Ghelardi, 1964). Species richness was estimated b y S R = (s-- t ) / ln N, where s is the number of species and N the number of individuals in a collection (Mar- galef, 1958). Evenness was computed as J ' = H'/ log 2 s (Pielou, t966).

Results

Sediments

Percent of total sediment mass for phi particle- size classes t.0 through 8.0 r was plotted as cumulative probabili ty and median diameter (Mdr and standard deviation (a~) was computed using equations given by Inman (t952). These statistics, together with the sediment classification according to Shepard's (1954) nomenclature, are presented in Table t. The percentage of mass attr ibutable to particles larger than sand size (mainly shell fragments) was meager, but was in some

Vol. 21, Arc. 3, 1973 D.F. Boesch: Classification and Community Structure of 5[acrobenthos

Table ~l. Depth, sediment median particle-diameter, and standard deviation in phi units, sediment classification, and shell-gravel

percentage/or each station

Stat ion Depth ~Idr a~ Classification % shell- (m) gravel

A2 7.6 4.7 Sand-silt-clay 3.02 B2 7.6 5.5 Sand-silt-clay 3.55 134: 5.5 8.0 Silt clay 0.65 DI 3.3 2.5 0.8 Sand 0.4:3 D2 7.6 3.2 ~.9 Clayey sand 2.03 D3 4.5 2.7 L0 Sand t .94 D4 7.4 3.6 3.1 Clayey sand 0.06 D5 4.5 3.5 3.8 Clayey sand 0.94 E6 4.8 3.8 3.7 Clayey sand 2.85 E7 3.6 4.6 4A Sand-silt-clay 0.87 E8 5.0 4.8 Sand-silt-c!ay L92 :FI 3.0 3.0 0.6 Sand 0.29 i~2 7.0 3A 1.0 Sand 0.59 F3 i2.3 3.3 t .2 Sand 2.53 F4 3.t 2.5 0.8 Sand 0.55 I~5 3.6 3A 0.9 Sand 0.30

Clay

"B4

/ "F~ v ~/ v V v , , Sand 50 SHt

Fig. 3. Ternary diagram of sediment sand-silt-clay proportions at 16 stat ions shown in Fig. 1

cases under-estimated due to exclusion from samples of very large particles. Percentages of sand, silt, and da y of the sediments, excluding particles larger than sand size, are graphically presented in a ternary diagram (Fig. 3).

Sediments varied from sil ty-day (Mcl 8.0~) for Station B4 at the Nansemond River mouth, to medium to fine sand at Station F4, which was located on a shMlow bar. In general, coarse sediments (medium to fine sands) predominated on the shoals on the

30*

229

northern side of the harbor and at its eastern end. Finer sediments (clays, silts, and very fine sands) predominated on the shoals to the south and in the lower James and Elizabeth rivers.

Wave action is obviously important in determining sediment composition. Sediments were well sorted (i.e., low standard deviation) at the shalIow stations Ft , F4, and Dt, located in depths of 3.3 m or less.

F a u n a l Data

The Ill grab samples yielded 168 recognizable m acrofaunM taxa (Table 2); 161 of these could be identified to species. Fiigher taxa with the most species were Polyehaeta (56 species), Gastropoda (24), Amphipoda (23) and BivMvia (18).

For the classificatory analysis, results from the three replicate grabs at a station for a given sampling period (hereafter called a "site") were lumped. Re- cords of a species with a very low frequency generally lack a pattern on which to classify, and it is usual practice to eIiminate very rare species from a classificatory analysis. Species which occurred at less than 6 of the 4~7 sites were thus eliminated from the analysis, leaving 97 species. The 97 species used in the analysis are number-coded in Table 2. Those species eliminated include 35 which occurred only once, and 16 which occurred twice. Only one of the eliminated species, the cumacean Leucon americanu.s., was ever represented by more than 4 individuMs at a site. However, all species records were used in the computation of community structural measures.

N o r m a l Classif ication

IlierarchieM groupings of sites by flexible and group-average clustering are presented in Fig. 4. Truncation of the dendrograms at the 8-group level for flexible and the i0-group level for group-average clustering produced very similar groupings of sites. Sites were grossly grouped into those where sediments were > 38% silt-clay (Flexible Groups A, 13, C, D), and those with < 28% silt-day (Flexible Groups E, F, G, It). The only exceptions were the August sites at I)4 and ])5, which were grouped with the sandier sites. The fine-sediment sites were further divided into those in the Elizabeth 1giver (Groups A and B), and those in the Roads or the James River (Groups C and 1)). The sandy sites were subdivided largely on a seasonal basis.

Discrepancies between the two clustering strategies were: (t) the split of Flexible Group A into Group Aver- age Groups A 1 and A~; (2) the fusion of Group Average Group B with Groups C and D rather than with A as in the flexible classification; (3) the fusion of F3A with Group Average Group I-I and its membership in Flexible Group G. Examination of the original data matrix indicated that there was little purpose

230 D .F . Boesch: Classification and Community Structure of Macrobenthos Mar. Biol.

Table 2. Species collected in Hampton Roads area, February, 1969 to August, 1969. The 97 species included in the classificatory

analysis (pp 229--236) are numbered

Cnidaria 1 Ceriantheopsis americanus (Verrilt) 2 Diadumene leueolena (Verrill) 3 Edwardsia elegans Verrill

TurbellMra Stylochus ellipticus (Girard)

Phoronida 4 Phoronis architecta Andrews

Rhynchocoela Amphiporus bioculatus (McIntosh)

5 Carinomella laetea Coe 6 Cerebratulus lacteus (Leidy)

Cerebratulus luridus Verrill 7 Mierura leidyi (Verrill) 8 Tubulanus pellucidus (Coe)

Polychaeta Aglaophamus verrilli (McIntosh) Ancistrosyllis hartmannae I)ettibone Arabella irricolor (Montagu) Aricidea ie~reysi (McIntosh)

9 Asabellides oculata (Webster) Capitella capitata (Fabricius)

10 Clymenella torquata (Leidy) 11 Clymenella zonalis (Verrill) 12 Diopatra cuprea (Bose) 13 JDrilonereis filum (Claparede) 14 Eteone heteropoda Hartman

Eteone lactea Claparede t5 Eumida sanguinea (Oersted) 16 Glycera americana Leidy t7 Glyeera dibranchiata Ehlers 18 Glycinde solitaria (Webster)

Gyptis vittata (Webster and Benedict) 19 Harmothoe extenuata (Grube) 20 Heteromastus fili/ormis (Claparede) 21 Hydroides dianthus (Verrill) 22 Lepidonotus sublevis Verrill 23 Loimia medusa (Savigny) 24 Lumbrineris tenuis (Verrill)

.Marphysa sanguina (Montagu) Melinna maculata Webster Nephtys ineisa (Malmgren)

25 Nephtys magellanica (Augener) Nephtys picta (Ehlers)

26 ~Vereis suceinea (Frey and Leuckart) Notocirrus spini]erus (Moore) Notomastus laetericius Sars Odontosyllis /ulgurans Claparede

27 Paleanotus heteroseta Hartman 28 Paranaitis speciosa (Webster) 29 Paraprionospio pinnata (Ehlers) 30 Pectinaria gouldii (Verrill) 31 Phyllodoce arenae (Webster)

Phyllodoce mucosa Oersted 32 Podarke obseura Verrill 33 Polyeirrus eximius (Leidy) 34 Polydora ligni Webster

Polydora sp. Prionospio cirri/era Viren Prionospio heterobranchiata Moore Prionospio sp.

35 Pseudeurythoe paucibranchiata Fauvel 36 Sabella mierophthalma Verrill 37 Sabellaria vulgaris Verrill

Seolelpsis bousfieldi Pettibone 38 ScolopIos/ragilis VerriI1 39 Scoloplos robustus Verrill 40 Spio setosa (Verrill) 41 Spiochaetopterus oculatus Webster 42 Spiophanes bombyx Ciaparede 43 Streblospio benedieti Webster 44 Tharyx setigera Hartman

Oligochaeta 45 Peloscolex spp.

Bivalvia 46 Amygdalum papyria (Conrad)

Anadara ovalis (Bruguiere) 47 Anadara transversa (Say)

Anomia simplex Orbigay Barnea truncata (Say)

48 Ensis directus Conrad Gemma gemma (Torten)

49 Lucina multilineata Tuomey and Holmes 50 Lyonsia hyalina Conrad

Macoma baIthica (Linnaeus) 51 Macoma tenta Say 52 Mereenaria mereenaria (Linnaeus) 53 Mulinia lateralis (Say) 54 Mya arenaria (Linnaeus)

MyseUa bidentata (Montagu) 55 2gucula proxima Say 56 Tellina agilis Stimpson

Yoldia limulata (Say)

Gastropoda Acteon punctostriatus Adams

57 Anachis translirata Ravenei 58 Cerithiopsis greeni Adams 59 Crepidula convexa Say

Crepidula /ornicata (Linnaeus) Doridella obseura Verrill Doris verrucosa Linnaeus

60 Epitonium rupieolum (Knrtz) 61 Eupleura caudata (Say) 62 Haminoea solitaria (Say)

Mangelia cerina Kurtz and Stimpson 63 Mangelia plicosa Adams

Marginella denticulata Conrad Melanella iutermedia Contraine

64 Mitrella lunata (Say) Nassarius obsoletus (Say)

65 Nassarius vibex (Say) 66 Odostomia impressa Say 67 Pyramidella/usca Adams

Pyramidella sp. 68 Retusa canalicutata (Say) 69 Turbonilla interrupta Trotten

Turbonilla 8tricta Verrfll Urosalpinx cinerea (Say)

Pyenogonida Anoplodactylus parvus Giltay Call@arlene brevirostris (Johnston) Tanystylum obieulare Wilson

Ostracoda 70 Sarsiella zostericola Cushmaa

Cirripedia 71 Balanus improvisus Darwin

VoI. 21, No. 3, 1973 D. 1~. Boesch: Classification and Community Structure of Maerobenthos 23t

Table 2. (contimmd)

Mysidaeea Heteromysis /ormosa (Smith)

72 2Veomysis americana (Smith)

Cumacea Cyclaspis sp. Leucon americanus Zimmer Oxyurostylis smithi Calman 73

Isopoda 74

75

Cyathura burbaneki Frankenberg Cyathura polita (Stimpson) Edotea triloba (Say) Erichsonella fili/ormis (Say)

Amphipoda Acanthohaustorius intermedius Bousfield

76 Ampelisca abdita Mills 77 - Ampelisca vadorum Mills 78 Ampelisca verrilli Mills 79 Batea catharinensis Muller

Bathyporeia sp. Caprella equilibra Say

80 Caprella penantis Leach 81 Cerapus tubularis Say 82 Corophium acherusieum Costa

Corophium tuberculatum Shoemaker 83 Elasmopus laevis (Smith) 84 Eriehthonius brasiliensis Dana 85 Gammarus mueronatus Say

Jassa /alcata (1V[ontagu) 86 Listriella clymenellae Mills

Melita appendiculata (Say) Monoculodes edwardsi Holmes

87 Paraeaprella tenuis Mayer 88 Paraphoxus epistomus Shoemaker

Stenothoe minuta (Holmes) Sympleustes glaber (Boeek)

89 Uneiola irrorata Say

Decapoda Alpheus heteroehaelis Say Callineetes sapidus gathbun

90 Crangon septemspinosa (Say) 9t Euceramus praelongus Stimpson

Eurypanopeus depressus (Smith) Libinia dubia H. Milne-Edwards

92 Neopanope texana (Smith) 93 Ogyrides limicola Williams

Pagurus tongiearpus Say Panopeus herbsti H. Milne-Edwards

94 Pinnixa sayana Stimpson 95 Upogebia a/finis (Say)

Echinodermata 96 Amphiodia atra Stimpson

Cucumaria puleherrima (Ayres) Thyone briareUs (La Sueur)

tIemichordata Balanoglossus sp.

Uroehordata 97 Molgula manhattensis (Dekay)

Pisces Gobiesox strumosus Cope Gobiosoma bosei (Lacepede) Microgobius thalassinus (Jordan and Gilbert) Trinectes maeulatus (Lacepede)

served in subdividing Group A. I t was also decided that Group B, although intermediate between Groups A and C plus D, could be considered most similar ~o Group A, particularly because its sites were quite dissimilar to many Group D sites. Site F3A appeared intermediate between Group G and H sites but, because it lacked or had in reduced numbers species whose great abundance was highly characteristic

Group average Flexible

E'AE6A [:--I

I I I

O"F I1, . I A2M ~ 1 :A2A

S2M

S4A

D4F u ' - ~ D4I~

I _ [ ~ A2F F------ F4F

ErJ_J--[Z F3F F5F ~ E ,

! c::F'MF2M f

-E D%,M r L I sD'FD F-

G ~ F4MF5 M ~ _ _ _ ~ G ~ 3AF5 A

DIAF4A

F1AF2A ~ ] - - H D4AsA --] F--

0:8 ' 0:6 ' 0'.5' 0'7 ' 0:9 Dissimilarity

Fig. 4. Dendrograms resulting from normal analysis of sites by group-average and flexible clustering. First two characters of site designation refer to station no., last to sampling period: F February; M May; A August (for description of

stations see Table 1)

of the remaining August sand sites (see "Inverse Classification"), it was best grouped in G. Therefore, in all cases of discrepancies, the flexible strategy yielded the more instructive classification.

The inclusion of D4A and D5A with the sandier August sites was disconcerting, even after re-examination of the original data matrix. These two sites, together with the other Group H sites, were characterized by the absence or rarity of a number of species present in February and May, both on sand and finer sediments. Like F3A, however, D4A and D5A lacked those few characteristically abundant species of the

232 D. 1~. Boeseh: Classification and Community Structure of Maerobenthos Mar. Biol.

remainder of Group I t sites. These two sites were, therefore, reallocated to Group D, an already heterogeneous group of sites which includes the February and 3gay sites at ])4 and D5.

Fig. 5 presents the distribution of site groups by station and season for the two classification strategies and for the classification deemed "best" , i.e., the flexible classification with reallocation of DCA and D5A. The stations are divisible into 4 groups, corre- sponding to location and sediment type: Elizabeth River stations, "mud" stations ( > 70% silt-clay), "muddy-sand" stations (42 to 6 t% silt-clay), and

E8

E7

E6

B4

B2

A2

D5

D4

Di

F1

F2

F5

F4

D2

]:)3

F3

F M A F iVl A F lvl A

Flexible Group Average Real locat ion

Fig. 5. Distribution of site groups by station and sampling period given by the two clustering strategies used and the "best" elassifieation after realloeation. Dashed lines and shading indicate intergroup relationships. See Fig. 4 for

explanation of symbols

"sand" stations ( < 30 % silt-clay). Mud stations were distinguished by Group C sites in February and May, while muddy sand stations were Group I) sites in Febrnary and May. Furtb~er discussion of the charac- teristics of the site groups follows "Interpretat ion of Species Groups".

Inverse Classification

The group-average classification of species was characterized by excessive chaining (Lance and Wil- liams, i967), with species somewhat difficult to classify being individually fused to the great bulk of species at high levels. The most frequently occurring species were fused early in the clustering, and later fusions were simply gradual additions of individual species or small gronps of species that were less ubiq- nitous, producing a few large groups of common species arid many small "splinter" groups. The

54

67 16 - -

93 - - } - - 76

3O 12 1 61 l

96

23 7 0 - -

64 ] 86

53 _ _ ] 671 "

901~:

4365"

5% o 4619 33 2

~3~ 62

gs 67

83 11

27 " 34

63 48

45 I 56

17 4 2 ~

78 2 6 2 0 ~

10 t7 ) 7 7 - -

87 8 2 - -

60 3 - - ] ~ 69 5125 - } ~

7572-

3531

441 66

2 9 _ _ ~ - 83

36 8

49 91

61 - - t 28 - -

52 - 2

2~ 22-

3 7 7 9 ~ 58

74 ~ 5 5 7 - - 1 24

59 7 ~3

o14

j~-7 I I - -

_ _

I J- 15

, L o~6 t o'.s '

D i s s i m i l a r i t y 110

Fig. 6. Dendrogram resulting from flexible Clustering of species. Species are indicated by number code, left (see Table 2) and

species groups by numbers at right

inverse flexible classification was, on comparison, much more instructive and, therefore, the group- average classification was discarded.

The flexible classification of species is presented in Fig. 6. Because clustering strategies are "group-size dependent" (Williams et a/., t971), definition of a fixed stopping rule (i.e., some constant level of fusion) for selection of groups is unwise when groups vary in

Vol. 21, No. 3, 1973 D.F. Boeseh: Classification and Community Structure of Macrobenthos 233

size. The species groups numbered in Fig. 6 were selected by proceeding "down" the dendrogram in the direction of increasing diffusion, until the branches were subjectively determined to be relatively intern- ally consistent upon appeal to the original data matrix. This process was facilitated by construction of a two- way coincidence table, i.e., a sites-by-species original data matrix, rearranged according to both normal and inverse analyses (Stephcnson et al., t970).

Reallocation of species was performed by careful examination of the two-way coincidence table and removal of a species from one group and placement in another if cell density (i.e., constancy of the species group in a site group) was enhanced in the case of dense and/or reduced in the ease of sparse cells. This is functionally equivalent to what Popham and Ellis (t97t) call the "Ziirich-Montpellier procedure". Ten species were reallocated in this manner. Four species, Listriella elymenellae (86), Pinnixa sayana (94), Upogebia a/finis (95) and Amphiodia atra (96) were deemed nnclassifiable for want of any discernable pat tern in their distribution, and were removed from further consideration. Up to this point all the species tea]located or eliminated were relatively infrequently occurring and nonabundant.

Classification of species into Groups t0, i~, 12, and 13 remained "unsatisfactory" and these groups included many numerically important species. Scrutiny of the two-way coincidence table showed that the 28 species in these groups were, to various degrees, ubiquitous, and represented a near-continuum of distribution types, from those largely confined to sand to Spiochaetopterus oculatus (41), which was present at all but one site. I t was also apparent that a considerable number of reallocations were in order. To optimize reallocation, the 28 species were, therefore, ordinated by principle coordinate analysis (Gower, 1967), using the Canberra-metric coefficient (with e = 0.0~ for a single zero match) computed on log- transformed, species-norm standardized values (Austin and Noy-Nier, t97t), z~i, where

zi~-~ xi~/(~xi~2)'h ; x~j = log (Yii § 1) . i

Operationally, this is a divisive poly~hetic approach (Williams, i971) to the classification of these species.

Relative loadings on the first 3 axes are shown in Fig. 7. Although the largely continuous nature of the interspecific distribution patterns is apparent, the species were recast into 4 new groups as indicated in the figure. The new Group t0 is relatively distinct and conforms closely to the original Group 10. Groups t i and t2 are contiguous, but non-overlapping in three-dimensional space. Group t3 is heterogeneous, but distinct. Only -hrereis suecinea (26) presented a serious reallocation problem, since it is intermediate between Groups t0 and t2. I t was included in Group t2 on the basis of ]oadings on the fourth and fifth axes.

The redefined Group i i includes most of the members of the Flexible Groups i i and i2, and most of the members of the redefined Groups 12 and t3 are members of Flexible Group i3.

�9 Group 10 o Group 11 �9 Group 12 �9 Group 13

29~ I

* 30

75 *

72 *

66 e o c 41 �9 35 �9 20�9 82

"65 31 ..4 18 o

89, 9 2

"26 47*

o10 r

0069 60

87 ~73 o25

~

,64 55,

41 *

.29

20. 8 , .

92" "64

4. 682 5 o18 7~ 31" 75~ 55*

82 ~

~72 025 ~

3 0 ~

510

o69

47-

8;

073

Fig. 7. Principal coordinates-analysis of species of Groups 10, t l , t2, and 13. Relative loadings on first three axes axe shown. Species are indicated by number code (Table 2) and were

reallocated as shown (Table 3)

Interpretation o/Species Groups

The members of species groups after reallocations and exclusions are listed in Table 3. Group i consists of the only two species which were largely confined to Elizabeth River sites. Mya arenaria was strongly seasonal, being absent in August, whereas Scoloplos /ragilis was not. Group 2 species are those which were largely restricted to mud and muddy-sand stations and were not markedly seasonal. These species were the only ones characteristic of "muddy" bottoms, in tha t they had high constancy (50 to i00 %) and fidelity (60 to i00%) to Stations A2, ]32, ]34, Dd, and D5. Both Group 3 species were relatively rare and without much pattern, except tha t most of their occurrences were at muddy-sand sites.

234 D.F. Boesch: Classification and Community Structure of Macrobenthos Mar. Biol.

Table 3 Species groups, redefned after reallocations and exclusions

(see text)

Group Species

l 2

3 4

5

6 (~)

(b)

7 (a)

(b) 8

9

l0

11

12

13

I4 (~)

(b)

15

~6 (a)

(b)

Mya arenaria (54), Scoloplos /ragilis (38) Glycera americana (16), Ogyrides limicola (93), Ampelisca abdita (76) Diopatra cuprea (12), Cerapus tubularis (81) Ceriantheopsis amerieanus (1), Carinomella lactea (5), Loimia medusa (23), Sarsiella zostericola (70) Mulinia lateralis (53), Balanus improvisus (71), Cerebratulus laeteus (6) Eteone heteropoda (14), Strsblospio benedicti (43), Gammarus mucronatus (85), Lyonsia hyalina (50), Tharyx setigera (44), Asabellides oculata (9), ~rangon septemspinosa (90) Caprella penantis (80), Amygdalum papyria (46), Harmothoe extenuata (19), P odarke obseura (32), Polycirrus eximius (33), Scoloplos robustus (39), Spio setosa (40) Haminoea solitaria (62), Odostomia impressa (66), Clymenella zonalis (11) Pyramidella /usca (67), Paraphoxus epistomus (68) PaIeanotus heteroseta (27), Potydora tigni (34), Mangelia plicosa (63), Ensis direetus (48), Peloseolex spp. (45), Tellina agilis (56) Glyeera dibranchiata (17), Spiophanes bombyx (42), Ampelisca verrilli (78) Nucula proxima (55), Mitrella lunata (64), Neopanope texana (92), Unciola irrorata (89), Anadara transversa (47) Paracaprella tenuis (87), Ampelisca vadorum (77), Oxyurostylis smithi (73), Turbonilla interrupta (69), Epitonium rupieolum (60), Edwardsia elegans (3), 2Vephtys magellanica (25), Clymenella torquata (10), Macoma tenta (51), Corophium acherusicum (82), Glycinde sol#aria (18) Nereis succinea (26), Heteromastus fili/ormis (20}, _Tgassarius vibex (65), Retusa canaliculata (68), Pseudeurythoe paucibranchiata (35), Phoronis architecta (4), Phyllodoce arenae (3t), Spiochaetopterus oculatus (41), Paraprionospio pinnata (29) Edotea triloba (75), Neomysis americana (72), Pectinaria gouldii (30) EIasmopus laevis (83), Sabella microphthalma (36), Molgula manhattensis (97), Diadumene leucolena (2) Mercenaria mercenaria (52), Paranaitis speeiosa (28), Eupleura caudata (6t), Erichthonius brasiliensis (84), Hydroides dianthus (2i), Lepidonotus sublevis (22) Sabeltaria vulgaris (37), Batea catharinensis (79), Ceritheopsis greeni (58), Cyathura burbanclci (74), Eumida sanguinea (15), Anachis translirata (57), Lumbrineris tenuis (24), Crepidula convexa (59) Euceramus praelongus (91), Lueina multilineata (49), Tubulanus pellucidus (8) Mierura leidyi (7), Drilonereis fiIum 03)

Group 4 species infrequently occurred on sand and muddy-sand. T h e y were most frequent in August and virtually absent in February. Ceriantheopsi~ amerieanus and Loimia medusa were probably recruited in May or August from allochthonous sources. Sarsiella zostericola, on the other hand, probably occurred all year round but, because only very large specimens of

this ostracod are retained on a i mm screen, the

apparent increase in August may indicate growth rather than recruitment.

Group 5 species were widely distributed, but were most frequent and abundant at mud stations and rare and less abundant in Angust. 2Balanus improvisus and Mulinia lateralis were similarly grouped because the barnacle is commonly epibiontic on the bivalve.

Group 6 is a large group of markedly seasonal species. All the species were more common or more abundant, or both, in May, and were absent or extremely rare in August. Some were also rare in Febru- ary. The group is divisible into two subgroups, based on spatial distribution. Subgroup (a) species were widely distributed over the May sites; Subgroup (b) species were mostly limited to the sand stations. Most Group 6 species were recruited following spring spawning of either small over-winter populations or populations located elsewhere. Streblospio benedicti and Eteone heteropoda are locally common in lower salinity areas, Asabellides oculata and Tharyx setigera on deep mud bottoms (Boesch, t971), Lyonsia hyalina, Sco- loplos robustus and Spio setosa in the lower Chesapeake Bay (unpublished data), and Crangon septemspinosum, Gammarus mucronatus and Amygdalum papyria in shallow eelgrass beds (Wass, i965). Group 6 species largely die off or, in some cases, move away in summer; therefore they are, in varying degrees, ephemeral members of benthic assemblages in Hampton Roads.

Group 7 species were highly faithful (88 to t00%) to the sand stations. Subgroup (a) species were markedly more common and abundant, m February, but Subgroup (b) species were less season-specific. Group 8, like Group 6, consists of species not common or abundant in August, but the Group 8 species were much more common and abundant in February. Polydora ligni and Ensis direetus were very abundant and ubiquitous in February and May. Palaeonotus heteroseta, Mangelia plicosa and Peloscotex spp. were found on sand and, to a lesser degree, on muddy-sand; Tellina agilis was only taken on sand.

Group 9 species were highly faithful (95 to t00 %) to and widely distributed among the sand sites. They had greatly increased abundance and constancy at August sand-sites (except at F3), attributable to early to mid-summer recruitment, probably from populations in the lower Chesapeake Bay and on the adjacent ContinentM Shelf, where all 3 species are abundant (unpublished data).

Group t0 species were largely confined to muddy- sand and sand sites (88 to t00% fidelity). All 5 species, although present all the year round, were more abundant in February and May than in August. Populations were reinforced by fall and spring recruitment, and depleted during the summer.

Group li species were taken at sand sites and, to a lesser degree, muddy-sand sites. These species were less strikingly seasonal than Group t0 species. Group t l

VoL 21, No. 3, 1973 D.F. Boeseh: Classification and Community Structure of l~Iacrobenthos 235

species maintained relatively stable populations on sand bottoms, and less constant and less dense populations on muddy-sand.

Group 12 contains veryfrequent ly occurring species, and includes many of the numerically most important species of the H a m p t o n Roads macrobenthos, l~iost species were constant ( > 50%) constituents of each of the 4 major habi ta t types. Within the group, a var ie ty of abundance pat terns were represented. Nereis succinea and Heteromastus fili/ormis were more abundant at Elizabeth River sites and May sand-sites than elsewhere. _Retusa canaliculata was most ablmdant on mud and sand and, on sand, most abundant in February. Pseudeurythoe paucibranchiata, Phoronis architecta, and Phyllodoce arenae were most abundant on sand and muddy-sand. Pseudeurythoe paucibranchiata was more common and abundant in l~ay; Phoronis architecta was most abundant in sand in August (although of constant abundance in muddy- sand). Spiochaetoptcrus oculatus and Paraprionospio pinnata (the most ubiquitous of all the species) were slightly more abundant on mud and muddy-sand. The abundances of both species were noticeably seasonal only on sand, where S. oculatus was most abundant in August and P. pinnata in February.

Group 13 species were also widely distributed, but less frequently occurring than Group t2 species. None of the 3 species was noticeably seasonal.

With the exception of Mercenarla mercenaria, all Group 14 species are epifaunal and depend, to varying degrees, on the presence of shell or Sabellaria tubes. These conditions often existed at Stations A2, D2, D3, and F3. Subgroup (a) species were widely distributed, and were found wherever suitable substrates were sampled, i.e., at Elizabeth River, muddy-sand, and sand sites. Subgroup (b) species were mostly confined to muddy-sand and sand sites. All Group t4 species were more common and more abundant in May and August than in February, and only 5 had more than one occurrence in February. This suggests tha t recruitment took place in spring, and tha t populations survived throughout summer. Alternatively, recruitment may have been continuous over the warmer months of the year. Group i5 species, except for Lumbrineris tenuis, are also epifaunal. They were mostly restricted to sand sites (75 to t00% fidelity), were not as markedly seasonal as Group t4 species, and had high constancy (57 to 86%) in Site Group G. Group i5 species appear to have been more epifaunal- habi ta t specific than Group 14 species.

Group 16 consists of relatively rare and never abundant sand-specific species. All of these species were least frequent or absent in February. Sub- group (a) species were most common in August, and Subgroup (b) species most common in ~ a y . Recruit- ment during warmer months is again suggested.

In summary, the inverse analysis produced species groups of 4 main types: ( t )p redominan t ly habitat-

31 ~Sar ine B io logy , Vol . 21

restricted (Groups i , 2, 3, 7, 9, 16); (2) seasonally restricted (Groups 4, 5, 6, 8); (3) widespread (Groups 10, t l , t2, 13); (4) epifaunal or microhabitat-restricted (Groups t4 and t5).

I t is now possible to redeseribe the site groups in terms of species groups (Table 4). Sites in Groups A, B, and C were characterized more by lack of species than by the presence of any characteristic set. Species of Groups 4, 6(b), 7, 9, 10, t t , t5, and t6 were absent or infrequent in these three site groups. Only Group t was at all faithful to Groups A and B. Group C is

Table 4. Species group-constancy at site groups (i.e., "cell density"). Very high (VH)> 75 %, high (H) 50 to 74 %; moderate (M) 25 to 49 %; low (L) 10 to 25 %; very low (VL)

<10%

Species group Site group A B C D E F G H

i H H L 2 M 1~ VH 3 -- -- M 4 -- VL VL 5 ~ H VH 6 (a) L 1~I l~I L 6 (b) VL -- VL VL 7 ( a ) - - - - VL - -

7 (b) -- -- -- VL 8 L L L 1~ 9 -- - - - - VL

t o - - L L VH t l VL VL M H 12 ~ V H H VH 13 L H ~I H 14 (a) H 1VI L l ~ 14 (b) VL - - - - 15 - - VL - - VL 16 (a) L VL 16 (b) L VL

L M m

VH VL -- VL L ~ L L L 1~ L L L L 1V[

L H ~ L It I t VL VL 1V~ H L It L L VL It - - H i ~ H H H N[ H VH H VH VH H VH VH VH H H VH VH VH VH M H N~ H VL L ~ H VL M 1~ 1~ VL L H N[ - - - - ~ Yl -- L ~

separable from Groups A and B by its greater constancy of Groups 2 and l i and paucity of occurrences of Group i4(a) species. Groups A and ]3 differ because A lacked occurrences of some species of Groups t2 and t3, i.e., Nassarius vibex, Pseudeurythoe paucibranchiata, Phoronis architecta and Pectinaria gouldii. This could have been due to the effects of reduced salinity a t Group A sites, which were located farthest up the Elizabeth River.

Site Group D differs from the sand-site groups by its very high constancy of Group 2 species and its low constancy of Groups 6(b), 7, 9, and t6 species. Clearlythe fauna of the muddy-sand site was somewhat intermediate between those of the mud and sand sites. Site Group H (August sand-sites) differs from the other sand-site groups because of its higher constancy of Group 3 and 4 species, the much greater abundance

236 D. ~. Boesch: Classification and Community Structure of Maerobenthos Mar. Biol,

Table 5. Rank-analysis dominant species, their percentage/requency o/ occurrence, and mean abundance at stations representing 4 "associations" by sampling period

February ~ay Augus~

Elizabeth River stations (E6, E7, E8) Mya arenaria 83 ~12 Mya a~'enaria 78 210 Spiochaetopterus oculatus 78 19 Nereis succinea t00 35 Streblospio benedicti 100 71 2~ereis suecinea 78 7 Mulinia lateralis 100 57 Heteromastus fili/ormis t00 38 Heteromastus fili/ormis 56 6 Heteromastus fili/ormis t00 43 Nereis succinea 100 28 Paraprionospio pinnata 56 5 Spioehaetopterus oculatus 100 34 Spioehaetopterus oculatus 67 4 Sabella microphthalmaa 33 4 Sabella microphthalma ~ 100 50 Sabella microphthalma ~ 33 28 Molgula manhattensis~ 22 5 Paraprionospio pinnata 67 30 Mulinia lateralis 67 8

Mud stations (B2, Bd) Paraprionospio pinnata t00 66 Mulinia lateralis 100 242 Paraprionospio pinnata t00 44 Retusa canalieulata 100 23 Paraprionospio pinnata 100 80 Retusa canaliculata 100 35 Mulinia lateralis 50 697 Spioehaetopterus oeulatus 83 40 Spiochaetopterus oeulatus t00 25 Spiochaetopterus oculatus 100 ~[5 Retusa canalieulata I00 25 Phoronis architecta 83 19 Balanus improvisus ~ 50 9 Balanus improvisus~ 50 5 Ogyrides limicola 83 9 Ogyrides limicola 50 2 Ensis directus 83 8 Ampelisca abdita 83 3

~uddy-sand stations (A2, 1)4, DS) Spiochaetopterus oeulatus 100 42 Spioehaetopterus oculatus 89 38 Spiochaetopterus oculatus 100 45 Paraprionospio pinnata t00 29 Paraprionospio pinnata 100 43 lPhoronis architecta 78 32 Phoronis architeeta 67 34 Phoronis architeeta 67 40 Ampelisr vadorum !00 21 Retusa canaliculata 89 30 Pseudeurythoe pauci- Paraprionospio pinnata 89 10

branchiata 89 21 Ogyrides limicola 78 6 Retusa canaliculata 78 t4 Pectinaria gouldii 78 7 Nereis succinea 56 6 Unciola irrorata a 89 98 Pseudeurythoe

paucibranchiata 62 5 Polydora ligni ~ 67 22 lqereis sueeinea 62 10

Sand stations (DI, D2, D3, FI, F2, F3, F4 ,F5) l~etusa canaliculata 96 84 Heteromastus fili]ormis 96 79 Spiophanes bombyx 100 191 Polydora ligni �9 79 54 Polydora ligni~ 87 29 Phoronis architecta 87 62 Unciola irrorata ~ 63 50 Unoiola irrorata a 79 49 Ampelisca verrilli 79 35 Ampelisca variorum 7~ 24 Ensis directus 92 31 Heteromastus fili/ormis 96 36 Heteromaztus fili/ormis 50 9 Retusa canaliculata 87 22 Spiochaetopterus oeulatus 83 41 Ensis directus 54 i8 Ampelisca vadorum 75 26 Ampelisca vadorum 100 69 Nephtys magellanica 75 13 Nephtys magellanica 63 15 Glycera dibranchiata 100 28

Predominantly epifaunal species.

of Group 9 species, and its lower constancy of species in Groups 6, 7, 8, and 10. Site Group E (6 of the Febru- ary sand-sites) had higher constancy of Group 7 species and lower constancy of Groups 6, ~4, 15, and t6 species than Groups F and G. Site Group :F (4 of the May sand-sites) had lower constancy or abundance, or both, of Groups 6, 10, i4, ~5, and 16 species than Site Group G. Site Group G represents sites where there were large and diverse populations of epifaunal species. Suitable substrate conditions were widespread in May (4 sites), and present at only a few stations in February (D2 and D3) and August (F3).

D o m i n a n t Species

A rank analysis (Fager, 1957) was used to assess the numerically dominant species. Note that functional

dominance or importance is in no way implied. A score was assigned to the 5 species which were ranked highest numerically in each individual grab sample (3 at a site). The most numerous species scored 5 points, the next 4 points, etc. The scores were summed for each station group (i.e. Elizabeth River, mud, muddy- sand and sand) for each sampling period. The top 6 or 7 ranking species (depending on how many had high scores) are listed in Table 5, together with their percentage frequency in the grab samples and their mean density per 0.2 m 2.

The importance of the ubiquitous Group i2 species in each of the station groups is striking. Spiochaetop- terus oculatus, Paraprionospio pinnata, Retusa canaliculata and Heteromastus fili/ormis were at times abundant in all of the station groups, and occurred in ~00 or more of the i41 grab samples, l~elatively few

Vol. 21, No. 3, 1973 D.F. Boesch: Classification and Community Structure of Macrobenthos 237

" h a b i t a t specific" species were ever i m p o r t a n t : Mya arenaria in the E l i zabe th River , Ogyrides limicola on m u d and m u d d y - s a n d , and Ampelisca variorum, Nephtys magellanica, Spiophanes bombyx, Ampelisca verrilli and Glycera dibranchiata on sand. P r i m a r i l y seasonal species were somet imes a b u n d a n t : Streblospio benedicti, Mulinia lateralis, 2Balanus improvisus, Un- ciola irrorata, Potydora ligni and Ensis directus.

Mya arenaria was the overwhelming d o m i n a n t in t he E l i zabe th P~iver in F e b r u a r y and May, b u t h a d a lmos t comple te ly d ied off b y August . The size of these clams ( roughly 20 to 27 m m long in May) ind ica t ed t h a t mos t of these ind iv idua ls h a d been recru i ted dur ing the fal l of 1968. ~ i s i ng t empe ra tu r e s and p h y t o p l a n k t o n blooms dur ing the summer mon ths m a y lead to the demise of juveni le M. arenaria popula- t ions elsewhere in the Chesapeake B a y sys tem (J. Lucy, personal communica t ion) . Mulinia lateralis popu la t ions in t he E l i zabe th R i v e r decl ined from a h igh in F e b r u a r y , and were v i r t u a l l y dec ima ted b y Augus t . Streblospio benedicti was i m p o r t a n t on ly in May. Otherwise, t he re la t ive dominance of the more ub iqu i tous Nereis suecinea, Heteromastus fili/ormis, Spiochaetopterus oeulatus, and Paraprionospio pinnata changed l i t t le , a l though the i r popu la t ion densi t ies d id f luctuate . No t i ceab ly rare a t E l i zabe th Rive r sites was the elsewhere ub iqu i tous Retusa canalieulata.

A t the m u d s ta t ions , Mulinia lateralis suffered a s imilar dep le t ion f rom F e b r u a r y to Augus t as i t and Mya arenaria did in the E l i zabe th River . Huge fM1- spawned popu la t ions a t B2 decl ined f rom F e b r u a r y to N a y , and were gone b y August . Only Paraprionoapio pinnata, _Retusa canalieulata and Spiochaetopterus oeulatus were con t inuous ly a b u n d a n t .

The d o m i n a n t species a t t he m u d d y - s a n d s ta t ions were cons iderab ly more popu la t ion - s t ab le t h a n those of a n y o ther s t a t ion group. Spiochaetopterus oculatus, Paraprionospio pinnata and Phoronis architecta were the t h ree t op r ank ing species dur ing each of the sampl ing periods, a l t hough lesser dominan t s were somewhat more seasonal, tletusa canaliculata decl ined in abundance f rom F e b r u a r y to N a y , Uneiola irrorata and Polydora ligni were mos t a b u n d a n t in May, and Ampelisca vadorum was a b u n d a n t only in August .

A t t he sand s ta t ions , the dominan t s of F e b r u a r y and N a y were ident ical , a l though the i r r a n k orders were different. However , on ly 2 of these 7 dominan t s were st i l l r a n k d o m i n a n t s in August . Polydora ligni, Unciola irrorata, and Envis direetus were v i r t u a l l y absent , and tletusa canaliculata was much less abun- d a n t in Augus t . Meanwhile , Spiophanes bombyx, Phoronis architecta, Ampelisca verrilli, Spiochaetopterus oculatus, and Glycera dibranchiata popu la t ions increased d ra s t i ca l ly be tween May and August . The increase in P. architecta and S. oculatus popula t ions was in m a r k e d con t ras t to the i r seasonal s t ab i l i t y on m u d d y - s a n d bo t toms .

Community Structure

Values of t he c o m m u n i t y s t ruc tu ra l indices com- p u t e d are p resen ted in Table 6 and summar i zed in Fig . 8. These were c o m p u t e d on the full 168 "species"

Table 6. Numbers o/ individuals (N), numbers o/ species (S), species diversity (H'), species richness (SR), and evenness (J')

at each site (3 grabs covering a total o/0.2 m s)

Site N S H' SR J '

Elizabeth River stations E8M 636 26 t.82 3.87 0.39 E8A 104 20 3.03 4.09 0.70 E7F 314 2i 3.01 3.48 0.69 E7M 131 12 2.06 2.26 0.58 E7A 30 9 2.45 2.35 0.77 E6F 518 24 3.19 3.68 0.70 E6M 575 29 2.97 4.41 0.61 E6A t52 20 2.97 3.78 0.69

Mud stations B4F 104 9 t.63 1.72 0.51 B4~ 356 23 2.45 3.75 0.54 B4A 165 20 2.96 3.72 0.69 B2F 1556 22 0.83 2.86 0.t9 B2~ 563 37 2.51 5.68 0.48 B2A t66 27 3.40 5.09 0.71

5~uddy-sand stations A2F t48 34 4.42 6.60 0.86 A21V[ 572 46 3.34 7.09 0.61 A2A 2t4 35 4.07 6.38 0.79 D5F 247 31 3.16 5.45 0.64 D5)/[ 264 41 4.07 7.17 0.76 I)5A 252 46 3.67 8.14 0.66 D4F 250 34 3.70 5.96 0.73 D43~ 432 55 4.80 8.90 0.83 D4A 147 38 4.45 7.41 0.85

Sand stations DIF 374 42 4.38 6.92 0.81 DIM 526 55 4.27 8.62 0.74 DtA I011 39 3.61 5.49 0.68 :FtF 422 41 3.97 6.62 0.74 F I ~ 582 43 4.29 6.60 0.8t F IA 733 36 3.15 5.31 0.61 F2F 30t 43 4.40 7.36 0.81 F 2 ~ 524 52 4.61 8.15 0.81 F2A 559 49 3.97 7.59 0.71 F5F 452 39 3.75 6.22 0.71 F52r 790 57 4.58 9.14 0.78 :F5A_ 457 46 3.77 7.35 0.68 F4F 146 33 3.46 6.40 0.69 :F4~ 254 44 4.49 7.77 0.82 FdA 554 55 3.89 8.55 0.67 D2F 496 49 3.87 7.73 0.69 D2~ 292 43 4.58 7.40 0.84 D2A 548 55 3.88 8.56 0.67 D3F 860 51 3.48 7.40 0 61 D3~{ 845 65 4.93 9.50 0.82 D3A 556 51 4.04 7.91 0.71 :F3F 381 36 2.95 5.89 0.57 F31V[ 1t78 82 4.77 t l .45 0.75 F3A 1773 64 3.94 8.42 0.66

31"

238 D.F. Boeseh: Classification and Community Structure of ~aerobenthos Mar. Biol.

data set for each site (3 lumped replicates). Species diversity (H') was much higher at sand and muddy- sand sites than at Elizabeth River and mud sites. ~a rked seasonal patterns of diversity were apparent for all but the muddy-sand stations.

At the Elizabeth River stations, H ' dropped from February to May (2 out of 2 stations), and increased

- - I - - F

�9 "1-- F I , M El iz. R .

I ' A

+ u M u d - - - ~ " - - - - - A

F I Muddy-sand M

A

F Sand

A

H' i z 1

'1 2 3

I l

I ....... M " - ' - ~ - -

I - -

1 "3

4 5

- I - F I M

- ' - - - -F - - " F

I

Muddy-sand

S a n d

$R I L i

2 4

Eliz. R.

I M M u d A

F t - - M - - ' ; " ~

A - - 1 -

F " - - - - - - - + - - M - - I

A I

6 8 i - I i

lo

]

Muddy-sand

' I "F 1 M

" - P - ~ A

M + A

F I M - - ' + ' -

A "--------~

Eliz. R.

M u d

S a n d M " - - - ' P - A --'---P--

3" I I I i I J I t i

02- 0A 0.6 0.8 1.0

Fig. 8. Ranges and medians of species diversity (H'), species richness (SR), and evenness (J') for the 4 "associations" by sampling period. Eliz. R.: Elizabeth River. F February;

M Yfay; A August

from May to August (3 out of 3 stations). This was primarily in response to changes in evenness, as there was no noticeable seasonal pattern of species richness. Low evenness in May was due to the heavy concentra- tion of dominance between Mya arenaria and Streblos- pie benedicti. Both mud stations showed a continuous increase in diversity from May to August, again in response to increasing evenness. This was caused by the decreasing dominance by Mulinia lateralis. Species richness at both mud sites increased in May

due to an influx of Group 6 and Group 8 species, and declined by August.

Diversity at 7 of the 8 sand stations increased in May, and had decreased at all stations by August. This was coincident with similar patterns in both species richness (6 of 8 stations for both seasonal changes) and evenness (7 and 8 of 8 stations for May and August changes, respectively). Reference to the original data showed that the spring increase and summer decrease in richness was largely due to spring recruitment of species of Groups 6, t4, and i5 and their loss during summer. There was also an increase in the number of rare species, not considered in the classificatory analysis, taken at sand sites from February to May (from 18 to 29). A large number (28) of rare species was also taken at August sand sites, causing species richness to be higher in August than in February. The increase in evenness in May was due to an overall reduction in the number of Retusa canali. culata, and the fact tha t many of the May-specific Group 6 species, although subdominant, were present in moderate numbers. The fall in evenness by August was caused by the comparatively high dominance of Spiophanes bombyx and Phoronis architecta at most stations.

Seasonal patterns in diversity, richness and evenness were similar at the muddy-sand stations D4 and D5 to those at the sand stations. However, the pattern at A2 was aberrant, and evidently confused by the presence of year-round epifanna. Only a qualified interpretation can, therefore, be made that the seasonal fluctuations on muddy-sand bottoms were as on sand bottoms, except that the magnitude of the fluctuations was less.

Seasonal patterns in species diversity were attributable to changes in evenness at Elizabeth River and mud stations and to both evenness and species richness at sand and muddy-sand stations. On the other hand, the differences in diversity between the diverse sand and muddy-sand habitats and the low- diversity Elizabeth River and mad habitats were mainly differences in species richness. This disparity in species richness is also apparent in the characteriza- tion of site groups in terms of species groups. Whereas very few species were restricted to Elizabeth River or mud stations, many species, including most of those in Species Groups 4, 6(b), 7, 9, ~l, i5, and i6, were excluded from these stations. This agrees with my observation (Boesch, 1972) tha t between-habitat patterns of species diversity of macrobenthos in coastal Virginia are, for the most part, patterns of species richness.

Discussion

Classificatory Techniques

The computer classification of sites yielded results very similar to my a priori appraisal based on numerically dominant species. Insight into "community"

Vol. 21, No. 3, 1973 D.F. Boesch: Classification and Community Structure of Macrobenthos 239

patterns was not greatly deepened by the results of the normal analysis alone except, perhaps, at the infra- group level. This might have been different had spatial or temporal patterns been more subtle or the number of sites been very much greater. On the other hand, classification of species was quite instructive. I t shed light on the salient features of the site groups, and presented a relatively clear picture of the complex interaction of spatial and temporal patterns. To achieve the same results without automatic computation would have been extremely cumbersome.

Considerable reallocations, especially in the inverse analysis, were required to produce the most lucid description of the complex patterns observed. Although this approach may seem arbitrary, it need not be a cause of worry. Classificatory techniques in their ecological use are methods of simplification, and need not be adhered to as if they were firm prob- abilistic statistics. Prudent use of two-way coincidence tables to assist reallocation procedures is highly recommended. The investigator will remain the ulti- mate arbiter but, of course, justifications for reallocations should be stated. The criteria for assessing success of a classification are largely empirical.

Classifications fail and reallocation becomes necessary when: (1) "genuine misclassifieations" take place, or (2) the mathematical criteria used in computation do not adequately express intended biological criteria. Misclassifieations are recurring features of agglomerative strategies, and may take place, for example, by the early fusion of a pair of individuals and their eventual incorporation into a group whose members may bear great similarity to only one of the fused pair. This problem enhances the desirability of divisive strategies, in which all individuals are considered together and successively optimally split into in- creasingly internMly-similar groups. At present, however, divisive polythetic (i.e., considering all attributes at once) classifications are not practical (Williams, 197t).

The problem of mathematical statement of biologi- eally meaningful criteria is more amenable to solution. There exists a large number ofinterindividual similarity measures and clustering techniques (el. Sokal and Sneath, 1963; Williams, 1971). There have also been at tempts to empirically compare various teehuiques by application to "real" data (Field, t971; Stephenson et al., 1972). In addition, a number of data manipula- tory techniques are often useful. Transformations (e.g. logarithmic, square root) may solve problems caused by intraspecific contagion, an almost catholic phenomenon among temperate macrobenthos. Effects due to scalar differences between individuals may be alleviated by the use of standardizations. These are especially pertinent when using metric similarity measures computed between species. I f two species have similar habitat requirements, yet one is Mways much more abundant than the other (as is often the

case), they will appear dissimilar unless abundances are species-standardized. This problem was in fact realized in initial at tempts at classifying species in this s tudy using "raw" and log-transformed (but unstandardized) data. Again, a large number of standardization procedures exist, and many have been critically examined by Noy-Mier (t97t). The use of a double standardization in this study was a comprise solution to scalar differences among sites (i.e., some depauperate sites) and among species, and it gave generally satisfactory results.

The Community Concept

A minimum of t6 species groups was needed to describe spatial and temporal patterns over a 7 month period in the Hampton Roads area. Even then, considerable variations in abundance patterns by habitat or season were apparent within the species groups. Many species populations fluctuated in response to seasonal p h e n o m e n a - recruited to assemblages in response to seasonally programmed reproductive cycles, and lost due to physiological or interspecific biotic factors. Many of these seasonal species were probably recruited from allochthonous sources. Still other species responded primarily to the habitat factors, mainly sediments. In addition there were spatial-temporal interactive factors operating, e.g. causing the marked seasonality of Phoronis architects and Spiochaetopterus oculatus in sand,but not in muddy- sand.

These results support an interpretation of benthic assemblages as points in space and time collections of nearly individualistically distributed species, i.e., with each species responding to its owaa individual set of environmental determinants. Site groups or "assoeiatious", therefore, seem to be segments of near-continua of assemblages responding to complex environmental (including temporal) gradients (Whit- taker, 1970) ; thus, the process of classification is more properly one of dissection (Kendall, t966).

I t is difficult to conceive the macrobenthic associations of Hampton Roads as t ightly functioning units or as Petersen-Thorson type communities (Thorson, t957). However, a much more relaxed concept of what constitutes a community finds some applicability; for example Mills' (i969) definition as '% group of organisms occurring in a particular environment, presumably interacting with each other and the environment, and separable by means of ecological sm~ey from other groups." Given sediment type, location, and time of year, one could, with some accuracy, predict a posteriori what the macrobenthic fauna at a site in Hampton Roads in t969 would have been like. What is not known, is to what degree the patterns are repeatable year after year.

There is little justification for classifying these assemblages as "parallel level bottom communities"

240 D.F. :Boesch: Classification and Community Structure of ~acrobenthos Mar. Biol.

(sensu Thorson, 1957) or by any other formal global nomenclatural scheme. Ampelisca species have been often found to be dominant or characterizing species elsewhere (Thorson, t957; Sanders, i958; Jones, t969; Lie and Kelley, 1970). Other genera important in Hampton Roads have also been reported as dominants elsewhere, e.g. Spiophanes (Jones, ~969), Retusa (Sanders, t958), Mya (Thorson, i957) and Nephtys (Sanders, i958). However, considered as a whole or any appreciable fraction thereof, the macrobenthic associations of Hampton Roads have no definite parallels outside the Chesapeake Bay region. Within the Chesapeake ]Bay, most of the dominant species have also been found to be dominants in the lower bay (Wass et al., i967; Boeseh, i971) or the lower York River estuary (Boesch, 197t). The only apparent oddities were Spiochaetopterus oculatus which is not as abundant elsewhere as in Hampton Roads, and Nephtys incisa, which is widespread and abundant in mud and muddy-sand elsewhere, but scarce in Hampton Roads.

Factors l~egulating Species Distribution and Diversity

Within Hampton Roads proper, the overwhelming factors responsible for the observed spatial patterns of species distribution and diversity were those per- taining to the substrate. Habitat-specific species groups could be explained largely in terms of silt and clay content of sediments or the availability of hard substrates in the form of shell, gravel, or arenaceous biogenic concretions. Only 7 of the 93 species classified (Mya arenaria, Scoloplos /ragilis, Glyeera americana, Ogyrides limicola, Ampelisca abdita, ~alanus improvisus and Cerebratulus lacteus) did not have at least 50% of their occurrences at sand sites. Only M. arenaria, S. /ragilis and A. abdita were not found on sand at all, and the first two of these were largely restricted to the Elizabeth River. On the other hand, 42 species occurring at sand sites did not occur at the mud stations (B2 and Bd; > 70% silt-clay) and 22 did not occur at the muddy-sand stations (A2, Dd, D5; 42--61% silt-clay). Abundance patterns of individual species vary, of course, but it seems that most macrobenthic species in Hampton Roads were either not bottom-type specific or restricted in varying degrees to sand bottoms.

Suspension-feeder exclusion from mad bottoms as described by Sanders (i958) and Rhoads and Young (t970) seems an attractive explanation for the distribution patterns in Hampton Roads. Therefore, the feeding types of species found at sand sites but not found at 2 mud sites, and those not found at 3 muddy-sand sites, were determined by reference to feeding-type classification given by Sanders et al. (i962), Phelps (~964), and Young and Rhoads (1971). Those species deemed dependent on the presence of hard substrates (epifauna) were listed separately. Of the 93 species

classified (Table 3), 58 were largely excluded from the mud stations: 22 are epifauual, 27 infaunal deposit- feeders, 2 infaunal carnivores, 4 infaunal omnivores, and only 2 infaunal suspension-feeders. Likewise, of the 41 species largely excluded from muddy-sand, i4 are epifannal, 22 infaunal deposit-feeders, i infaunal carnivore, 4 infaunal omnivores, and none are infaunal suspension-feeders. Even if the 7 epifaunal suspension-feeders which were mud-excluded are classed with the infaunal suspension-feeders, it is obvious that the qualitative difference between faunas of sand and mud bottoms in Hampton Roads was not due to the wholesale exclusion of suspension-feeding animals from mud. Of course, generalizations based on such broad feeding-type categories suffer because they arc imprecise descriptions of feeding behavior and because of the considerable feeding-plasticity of many benthic animals. Young and Rheads (~97~) have recently found that their generalizations about suspension-feeding exclusion in Buzzard's Bay did not hold for similar situations in Cape Cod Bay, Massachusetts, and have greatly qualified their hy- pothesis.

1%oughly one-half of the differences in species richness between sand and mud-bottom assemblages was attributable to differences in epifaunal species richness, and most of the remainder to differences in deposit-feeding infaunal species richness. The epifauna of sand bottoms was more diverse because here are found suitable hard substrates, mainly shell and fragments of resistant tubes of Sabellaria vulgaris (see Wells, ~970). Suitable substrates are generally not found on mad bottoms, where they would be quickly silted over. I t is conceivable tha t greater living space is available to infauna in sand bottoms than in mud bottoms, where the shallow depth of the redox dis- continuity layer limits smaller infauna to the sediment's surface. Therefore, a greater diversity of deposit-feeding types, e.g. surface fioc-feeders and subsurface sediment-swallowers, and consequently more species, may occupy sand bottoms. Thus, in a somewhat vague sense, greater "spatial hetero- geneity" (Pianka, i966; Sanders, i968) allowed greater species diversity on stable sand bottoms than on mud.

Elizabeth ~iver

From sediment particle-size distribution (Table i ; Fig. 3) one would expect tha t the macrobenthic assemblages at the 3 Elizabeth River stations would have been similar to those at the muddy-sand stations in Hampton Roads. In fact, they were different in terms of species content (Table 4), dominant species (Table 3), and species diversity (Fig. 8). Salinity differences might have been a factor, but scattered measurements indicate tha t salinity did not drop below 15Yoo at any of the stations. Nonetheless, the absence of Na.ssarius vibex, Pseudeurythoe pauci.

Vol. 21, No. 3, 1973 D.F. Boesch: Classification and Community Structure of 1VIacrobenthos 241

branchiata, Phoronis architecta, and Pectinaria gouldii at Station ES, the station farthest up the Elizabeth River, parallels their similar up-estuary exclusion in the York River estuary (Boesch, i97i).

Instead, I suggest that pollution stress was responsible for the alteration in community structure. The Elizabeth River received approximately 2 x t04 m ~ day -1 of primarily treated sewage during i969, most of which entered via outfalls near Stations E6 and E7. In addition to organic loadings, the Elizabeth River has had among the highest levels of pesticides and heavy metals in shellfish and sediments (Bender et al., i972), and the greatest number of oil spills in the lower Chesapeake region (Virginia Institute of Marine Science, unpublished records). When compared with Hampton Roads, the Elizabeth River is very poorly flushed, indicating a greater tendancy for contaminants to concentrate in sediments. Abiotic conditions or severely altered benthic populations elsewhere characteristic of severe pollution (e.g. Reish, 1959), were not found. Instead, some species common on muddy-sand bottoms in Hampton Roads were largely excluded from the Elizabeth River, e.g. l~etusa canaliculata, and a few other species (Mya arenaria, Scoloplos /ragilis and .u succinea) were more common or abundant there. M. arenaria has also been reported as relatively pollution-tolerant in European waters (Tulkk], t968). The M. arenaria populations in the Elizabeth River were recruited during the fall of i968, evidentally found a temporary refuge, and survived in large numbers at least until May. S. ]ragilis is a very euryhaline and presumably eurytopie species (Boesch, i97i), which possibly benefited from relaxed biotic pressures in the Elizabeth River. N. succinea is perhaps the most euryeeious of any local maerobenthie species, and is extremely "opportunistic", often appearing as an early colonizer of "new" environments (Hanks, ~968).

others may be more fecund or more successful in one of the seasons. For example, Mya arenaria, Mulinia lateralis and Retusa canaliculata populations were predominantly recruited in fall, t968, survived over winter to be taken in February, and were depleted in summer after little or no spring enhancement. On the other hand, Streblospio benedicti and Spio setosa were primarily recruited in spring, and Ensis direetus, Polydora ligni, and Tellina agilis were successfully recruited in both fall and spring. Spiophanes bombyx, Phoronis architecta, Ampelisca verrilli, Glycera dibranchiata and Spiochaetopterus oculatus were recruited to sand bottoms in late spring or early summer, i.e., between early May and mid-August.

?

SAND , i = ~ , i i i = I i i

" . . o . �9 . . . . .

MUD

' O ' N ' D ' J ' F ' M ' A ' M ' J ' J ' A '

Fig. 9. Hypothetical model of seasonal behavior of species diversity (H'), species richness (SR), and evenness (J') of

assemblages on sand and mud bottoms in Hampton Roads

Seasonality

There were large-scale seasonal fiuctuations in macrobenthic populations in Hampton Roads. Over 60% of the 93 species classified clearly exhibited seasonality either in their frequency of occurrence or abundance. These included many of the dominant species, e.g. Mya arenaria, Streblospio benedicti, Mulinia lateralis, Retusa canaliculata, Polydora ligni, Unciola irrorata, Spiophanes bombyx, Phoronis archi. tecta, Ensis directus, and Ampelisca verrilli. These patterns were largely reflections of the markedly seasonal spawning cycles of the benthic invertebrates in the Chesapeake Bay region. Most species have reproductive peaks in spring or fall, or both, or in summer. Spring/fall spawners (e.g. Species Groups 6 and 8) comprise perhaps the largest group of species. These are mostly cool-temperate species, which may spawn in summer in New England. Many species successfully spawn during both spring and fall, and

The factors responsible for the depletion and some- times decimation of populations of seasonal species are largely unknown. Physiological tolerance may play a role in the decline of some, e.g. Mulinia lateralis and Mya arenaria. Otherwise, competition and, especially, predation are probably important (Thorson, 1966), but remain almost totally undocumented.

Seasonality of species occurrence and abundance had a great effect on the community structure of Hampton Roads macrobenthos. Fig. 9 presents a hypothetical model of seasonal behavior of species diversity and its components on sand and mud bottoms. On sand, diversity (H') was relatively stable, except for a peak in May. This was attributable to the influx of many "new" species recruited following spring spawning. I also suggest tha t the rise in H' was preceded by a slight dip, due to reduced evenness caused by the early influx of a few species in large numbers. Thus, the model implies counter-balances of rises and falls in species richness and evenness,

242 D.F. Boesch: Classification and CommunRy Structure of Macrobenthos Mar. Biol.

which keep diversity stable except in late spring when both richness and evenness peak.

Mud bottoms had widely fluctuating species diversity. Diversity was low over winter and high during the warmer months. The pattern of species richness was parallel to that of sand bottoms but, in this case, evenness changes had the overwhelming influence. This reflects the overwhelming dominance of Mulinia lateralis after recruitment in fall, and its gradual decline in spring and summer. Species diversity of assemblages on muddy-sand bottoms was more stable than on mud-bottoms, and roughly corre- sponded to the sand model. Community structure in the Elizabeth River paralleled that on mud bottoms, because diversity was primarily controlled by evenness

this time reflecting cool-temperature dominance by Mya arenaria.

Seasonal change in community structure is the common condition for assemblages of temperate marine and fresh-water organisms. Sager and Hasler (1969) attributed seasonal variability of H' for phy-to- plankton assemblages in Wisconsin Lakes to changes in the evelmess (equitability) of the t0 to ~5 most abundant species. Marsh (t970) found that spring brought low evenness and high species richness in eelgrass epifaunal assemblages in the York River estuary, Virginia. The net effect was rather seasonally stable H' values, as the changes in the two components "cancelled" each other. Dahlberg and Odum (1970) found significant seasonal fluctuations in the evenness of Georgia estuarine fish-assemblages due to the influx of juveniles into the estuary in the fall.

The degree to which the seasonal patterns in species distribution and community structure in Hampton Roads are regular yearly patterns is unknown. Similar seasonal abundance patterns for some species, e.g. Polyclora ligni (Orth, 1971), have been observed regularly in the York River estuary. For others, the yearly occurrence of seasonal abundance is sporadic. Mulinia lateralis, for example, has been abundant in winter and spring in mud bottoms of the York estuary during some years but not others (M. L. Wass, personal communication).

The gross nature of seasonal fluctuations in these macrobenthic assemblages indicates that "one-time" surveys of temperate estuarine benthos may be of limited value. The associations in the Hampton Roads area are not static entities, but are very dynamic, loosely cohesive, and variable.

E~ect8 o /Man

There seems to be a consensus of opinion that estuarine ecosystems are "valuable" and worthy of conservation, yet, because human population centers are often associated with estuaries, many estuaries are being heavily and multiply used by man. Hampton Roads, for example, is used for commercial and defense

shipping, commercial and sport fishing (flu_fish and shellfish), boating and water sports, and organic, chemical, and thermal-waste disposal.

The individual effects of these many uses to the benthic component of the Hampton Roads ecosystem is difficult to assess. Perhaps most important, but more subtle, have been the effects of alterations per- taining to shipping. Dredging has altered bottom topography and sediments, and spoil disposal problems have necessitated "reclaiming" a very large section of the Roads (the large, subrectangular projection, west of the mouth of the Elizabeth River in Fig. l). These changes have grossly altered circulation, caused new patterns of sedimentation (M. M. Nichols, personal communication), and perhaps affected flush- ing of the heavily taxed Elizabeth River.

In monitoring biotic populations for the effects of pollution, one is often limited to the perception of only gross alteration. Analysis of community structure provides a reasonably sensitive indication of low-to- moderate alteration. I t is in these cases that diversity indices or other descriptions may prove most useful rather than in drastically perturbed systems. The interpretation of community structural indices remains subjective, and must be made in perspective to "back- ground" levels. This approach has been used successfully, even in highly variable estuarine environments, with various groups of organisms (Armstrong et al., i971; Bechtel and Copeland, ~971; this study). However, even when man-induced alteration of community structure can be documented, we are all too ignorant of what this implies with respect to the economies both of the ecosystem in question, and of m a n .

S;lmrn:try

i. Classificatory analysis delimited Elizabeth River, mud, muddy-sand, and sand "associations" in Hampton Roads, Virginia, USA. Further groupings of the heterogeneous sand sites (8 stations) were by season, or some interaction between season and the presence of epifaunal species. The 93 species classified were allocated into 16 species groups, reflecting spatial and temporal distribution patterns. Many species were predominantly restricted to Elizabeth River sites (2% of the species classified), mud and muddy-sand sites (3%), muddy- sand sites (23 %), sand sites (14%), or one or two sampling periods (22%). Still others were essentially ubiquitous (16 %) or microhabitat-restricted, i.e., epifaunal (19%). Many of the species showed both habitat and seasonal restrictions.

2. Numerically dominant species were ubiquitous or markedly seasonal, except for Mya arenaria in the Elizabeth River and certain of the sand-station dominants which were habitat-specific.

3. Species diversity was higher in collections from sand and muddy-sand bottoms than in those from Elizabeth River and mud stations. These between-

Vol. 21, :go. 3, 1973 D.F. Boesch: Classification and Community Structure of Maerobenthos 243

hab i t a t diversi ty differences were pr imar i ly differences in species richness of epifaunal and deposit-feeding species. Exclusion of suspension-feeders from m u d bot toms was no t impor t an t in this respect.

4. Species divers i ty in El izabeth River collections ",gas reduced as a consequence of intense muir]source pol lut ion in t ha t area.

5. Definite seasonal pa t te rns in communi ty s t ructure existed. At El izabeth River and mud stat ions evenness progressively increased from ~'ebru- a ry to August , and at sand and muddy- sand stat ions species richness and evenness peaked in May. These pa t te rns were in response to recru i tment and deplet ion of populat ions of seasonally spawning species.

Acknowledgements. This research was initially sponsored by the Hampton Roads Sanitation District Commission, Norfolk, Virginia, USA. Further work was performed during the tenure of a U.S. Federal Water Pollution Control Admin- istration (now Environmental Protection Agency) predoctoral fellowship. Most of the analyses and the writing were carried out while the author held a Fulbright-Hays postdoctoral research fellowship at the University of Queensland. I thank M. D. Richardson for his invaluable assistance in the field, and M. L. Wass, Virginia Institute of Marine Science, for his advice during early stages of the study. Greatest thanks go to W. T. Williams, CSIRO Division of Tropical Pastures, for program- ming the computer classificatory analyses and W. Stephenson, University of Queensland, for advice on classificatory techniques. I am grateful to W. Stephenson, ]%: Bradbury; A. Jones and T. S. Hailstone for critically reading the manuscript. My wife, lVIiehaelyn, helped prepare the figures, and assisted in many other ways.

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Author's address: Dr. D. F. Boeseh Virginia Insti tute of Marine Science Gloucester Point, Virginia 23062 USA

Date of final manuscript acceptance: May t8, 1973. Communicated by J. Bunt, Miami

Documents

Classification and community structure of macrobenthos in the Hampton Roads area, Virginia