A three-year study of benthos of muddy environments in Port Phillip Bay, Victoria

Estuarine

and Coastal Marine

A Three-year Environments Victoria”

Science (1979) 9, 477-497

Study of Benthos of Muddy in Port Phillip Bay,

Gary C. B. Poore and Sebastian Marine

--.

Rainer*

Studies Group, Ministry for Conservation, Melbourne, Victoria 3000, .4ustraZia

Extension,

Received 5 April

Keywords: variations

I978

benthos ; temporal

605

Flinders

Street

and in revised form 24 October 1978

; community composition variations ; bays ; Australia;

; species Victoria

diversity; coast

seasonal

Samples taken four times a year over three years (1973-1975) at three widely separate stations in muddy environments in Port Phillip Bay were used to compare species diversity and composition of the benthic community between areas, seasons and years. Analysis of variance of five community statistics: the number of individuals, the number of species, Shannon’s diversity and two evenness measures; showed that differences between the three stations and between years contributed the largest fractions of the variance in number of individuals and species but little to diversity or evenness. Seasonal differences contributed negligibly to variance in any statistic except diversity. Smallscale spatial patchiness (from replicate samples within stations) contributed a significant fraction of variance to all five statistics. The fauna at all stations was dominated by the deposit-feeding bivalve Theorafragilis and the decapod shrimp Callianassa limosa; only minor species were restricted to single stations. The density of few species varied seasonally but several were more abundant in some years than others. Hierarchical classification using the Canberra metric dissimilarity coefficient grouped samples into station groups. Use of the Bray-Curtis coefficient grouped some samples by station and some by season and it was concluded that the main differences between stations were in overall species composition, not in the densities of dominant species. Temporal changes in community structure were non-seasonal but. rather, were irregular changes occurring at singlestations. Differences in fauna between stations were related in part to small differences in sediment-type but not to physico-chemical features of the overlying water. The irregular fluctuations in density of the common species and in the identity of the minor species suggest that multiple-stable points in community structure may exist for the silty-clay community. The two major species seemed not to have alteredeach other’senvironment over the sampling period. Considerable variation in species composition may occur in soft-bottom benthos in the absence of marked environmental perturbations. “Paper Series. ‘Present Cronulla,

No.

162 in the Ministry address: N.S.W.

for Conservation,

C.S.I.R.O., Division XZ~O, Australia.

Victoria,

of Fisheries

Environmental

and Oceanography,

Studies 130s 21,

477 op-3524/79/100477

/ 2I

$02.00/o

8

1979 Academic

Press Inc.

(London)

Ltd.

478

G. C. B. Poore U S. Rainev

Introduction Mud substratesare widespreadin Port Phillip Bay (Beasley, 1966), forming a large basin in its centre and a smaller area in Corio Bay near the head of the Geelong Arm. The macrofauna1communitiesof thesesedimentsare the leastdiverse of all in the bay (Poore & Rainer, 1974; Poore et al., 1975) and lend themselvesto a study of community stability. Repeated sampling over three years (1973.-1975) at three stations enabled comparisonof community speciescomposition between areasof slightly different environmental regimesand levels of human influence. A secondobjective wasto assess the relative importance of seasonaleffects and year to year changeson the community. In spite of the necessityto provide long-term baselinedata on benthic communitiesaspart of environmental impact assessments (Stephensonet al., 1974, 1976; Boeschet nl., 1976), few studiesin the past have provided this sort of information. The researchesof Ziegelmeiel (1963)~ Frankenberg (1971), Lie & E vans (1973), Buchanan et al. (1974, 1978), Bocsch (1974), Watling (1975), Peterson (1975)~ Boeschet el. (1976), and Stephensonet al. (1974, 1976) are exceptions.

The study area The three stations chosenfor study were in similar environments in three different parts of Port Phillip Bay: stn 940 in Corio Bay, stn 948 in the centre of the bay and stn 977 off Martha Point (Figure I). Stns 940 and 948 were on predominantly silt-clay sediments,hut differed in depth; stn 977 wason a sand-silt-clay sedimentnear the large sandbanks which occupy the southern part of the bay (Table I). Water chemistry data were available from a sampling programme designedto monitor long-term changesin Port Phillip Bay hydrology and thesewere used asindicators of trends in water quality. Temperature and salinity gave information on seasonalityin the physical environment and total Kjeldahl nitrogen and total phosphorus were used to indicate the amount of food potentially availableto the benthos. Differencesbetweenstations,seasons and years were sought. Data from three water chemistry zoneswere examined (Figure 2): zone I in the centre of the bay, including stns 948, 977; zone 3 south of stn 977 and including the bay entrance region; and zone 4 which is the Geelong Arm and includesstn 940. Fortnightly meansof all data availabIe were calculated for temperature and salinity measurementsmade at 2.5 m below the surface. Data for total phosphorusand total nitrogen (which were lessfrequently measured)were averagedover 3-month periods. Temperature throughout most of Port Phillip Bay ranged from 10 “C to zz “C although in 1975 the annual maximum was about 2 “C lessthan in previous years (Figure 2). Another difference betweenyearswasin the length of the period of high summertemperatures,greater in 1973-74 than in other summers(Figure 2). Salinity varied from 33 to 36.$!& in spite of none of the three zones being influenced directly by major freshwater inputs (Figure 2). Xo consistentdifferencesbetween zones are obvious in thesedata but MMBW & FWD (1973) reported clear trends in salinity acrossthe bay, highest vaIues being in Corio Bay (stn 940). Salinity varied with time, more or lesssynchronously in all zones,but thesetrends were not obviously seasonal(Figure 2). Salinity was low for much of 1974. Data for nutrients are not completeand thoseavailableshow no obvious temporal patterns (Figure 3). Values of total phosphorusand total nitrogenwere highestin zone 4 (GeelongArm, stn 940) lessin zone I (central bay) and lowest in zone 3 (southern area).

A three-year study of Benthos

\

Figure I. Port (stippled; from

TABLE I. Depth Bay (from Poore

Phillip Bay showing the extent of silty-clay Beasley, 1966) and the three stations sampled

and sediment et al., 1975)

data for the three

stations

and clay sediments for benthos.

sampled

Station

Depth (ml

Sand (%

Silt (96)

Clay (x2)

Shepard

940 948 977

8 23 22

7’4 0.6

29’1 33’2 4o.r

63.5 66.2 31.7

silty clay silty clay sand-silt-clay

%hromic

acid oxidation.

2s.z

\,-

class

in Port

Phillip

Carbon” (“4) 1.3 2.6 0-j

480

G. C. B. hove @ S. Rainer

ZONE l-w--. LMlE 3...

9 .L(II1I-

10

11

12

1915

Figure 2. Trends in temperature and salinity over three years from three zones in Port Phillip Bay, measurements made during successive fortnightly periods have been summarised for each zone and means are plotted here. Benthic sampling cruise dates are marked.

Methods Three stations (940, 948 and 977 in Port Phillip Bay, Figure I) were sampled quarterly for three years, commencing in February 1973. Five 0.1 m2 Smith-McIntyre grab samples were taken from each station on each occasion (cruise), with the boat swinging at anchor. Samples taken at one time were thus not more than 15 m apart. Navigational errors associated with returning to the same station resulted in repeated sampling being over an area with a radius of approximately zoo m at stns 948, 977 and of 20 m at stn 940. Samples were elutriated on board ship as described by Poore et aE.(1975). All material retained on a I mm screen was preserved in so/b formalin; all animals were removed under stereomicroscopes and identified to species. Counts of individuals in each of five grabs (replicates) per sample were summed by species to give species counts for 35 samples. These were from station 940, cruises z-12, stations 948 and 977, cruises 1-12, hereafter given as 940/2-12, 948/1-12 and 977/1-12. Values of the log of the number of individuals log,,Ai’, number of species s, Shannon’s diversity H’ (natural logarithms), Pielou’s (1966) evennessr’, and Heip’s (1974) evenness I:‘, were calculated considering both replicates separately and summed for each sample. The five community statistics were treated to a mixed model, three-way analysis of variance (ANOVA) with 5 replicates to estimate differences between levels and the contribution to variance of the three factors:

--_ 481

A three-year study of Benthos

I

1973

Figure 3. Trends three zones in Port periods have been are plotted here to

1

1974

I

1975

J

in total phosphorus and total nitrogen over three years from Phillip Bay. Measurements made during successive three-month summarised for each zone and means and standard deviations correspond with benthic sampling cruise dates.

A, stations-940, 948, 977 (fixed factor, a = 3) B, years-1973, 1974, 1975 (random factor, b = 3) C, seasons-summer,autumn, winter, spring (fixed factor, c = 4). A two-way interpolation was used (station x time) to provide meanvalues for the sample set missingfrom stn 940, cruise I. Treatment of years as a random factor and stations and seasonsasfixed factors is made on the assumptionthat differences between years are more determined by random than systematic effects, with the converse holding for stations and seasons.This follows the usagerecommendedby Simpson et aE.(1960). Homogeneity of variance was examined by Bartlett’s x2 test. The data were then treated to a hierarchical classification analysis using polythetic, agglomerative methods (Lance & Williams, 1967a, b; seeClifford & Stephenson,1975, for review of these methods). Many strategies are available for the classification of benthic samples but two in particular have been widely used. The Canberra metric and the BrayCurtis dissimilarity measureswere used in this study to highlight the differences in species composition and dominancebetween the samples. Two normal classificationsof sampleswere done using: I. The Canberra metric dissimilarity coefficient,

482

G. C. B. Poore

M S. Raker

r 1 1 1 1 1 1 1 1 1 1 I 1 I SIN

Lag N 3

01

I

Cruise

1

I

Figure H’,J’, grabs)

I

I

2

3 1973

1

1

4

5 I

1

’

S 1 t974

__ --

940 949

SlN STN

-

911

1

1

8

9 I

’

’

10

II

’

1

12

1975

4. Fluctuations with time in five benthic community and E) at three stations from Port Phillip Bay. Means and standard deviations are plotted.

I

statistics (log N, S, of 5 replicates (0.1 m2

where s is the number of species occurring in the samples being compared and x1 and xa are the counts of each species in the two samples. Zero counts were set to 0.1 in order to reduce the contribution of species occurring at only one station of the pair (Clifford & Stephenson, 1975). 2. The Bray-Curtis dissimilarity coefficient, given in the same symbolism bv

A three-year study of Benthos

483

For both coefficients the sampleby sample matrix of coefficients was sorted using the flexible strategy with p = -0.~5. (Lance & Williams, 19673; Clifford & Stephenson, 1975). Group averagesorting was also attempted. The hierarchiesgeneratedby the two strategies differed little. For example, in the caseof the Canberra metric classificationof 35 samples the eight groups could be recognisedwith both strategies,only one samplebeing allocated differently. Resultsobtained from flexible sorting are used in all subsequentdiscussion. An inverse classificationof speciesusing samplesas attributes was carried out using the Canberrametric coefficient and flexible sorting. Analysis waslimited to the 60 most comtnon species.These had a mean density greater than z individuals/m2. Two two-way tables were constructed of sample-species coincidencesafter reordering the samplesinto groups (one table for each normal classification)and reordering the speciesinto groups (from the inverse analysis). Fidelity matrices (the percentageof individuals of each speciesoccurring in a given sample groups divided by the percentage of samplesin that group) and constancy matrices (the percentage of samplesin a group in which each speciesoccurred) were calculated for the two sets of sample groups generated by the Canberra metric and the Bray-Curtis analyses.The constancy definition is the sameasthat given by Stephensonet al. (1972) but the fidelity measureincludes a correction factor to eliminate the effect of differing number of samplesper group. Thus fidelity values greater than I indicate a preferenceby a speciesfor that station group and valueslessthan I avoidance of that station group. Results The fauna totalled 249 speciesof which 37% were polychaetes,30% crustaceansand 141& molluscs.More than half (131 species)were deposit-feedersand all numerically-important speciesand a major portion of the biomassbelongedto this trophic group. Changes in community statistics Homogenity of variance was found only in H’, with the other four statistics providing x2 values significant at P
484

G. C. B. Poore & S. Rainer

TABLE 2. Overall replicate means (and standard deviations) for five community statistics in all levels of the three factors used in the J-way ANOVAs. n is the number of replicates at each level

log N

H’

s

J’

l?na

Factor A (stations) 940 948 977

1.95 (0.28) I .86 (0.32) 2.25 (0.28)

19'0 (7’2) 16.4 (7.5) 25.6 (7.3)

2.08

(0.47) I .83 (0.50) 2'10 (0.51)

0.652 (0.213) 0.673 (0.173) 0.659 (0.151)

0.456 (0.185) 0’445 (0.222) 0.350 (0.181)

0.688 (0.164) 0.695 (0.184) 0.606 (0.177)

0’441 (0.221) 0.498 (0.193) 0.313 (0.143)

SS sg $8

Factor B (years) I973 I974

2'00

‘x’ (0.22)

1975

2'22

(0.28)

Factor C (seasons) Summer Autumn Winter

2.16 (0.26)

2.01

(0.52) 2'00

(0.55) 2'00

(0.46)

18.6

1.65

(7.7) 21'9

(1.58) 2.04 (0.45) 2'00

2'00

(9.1) 17'4 (6.7) 23.1

(022

(0.33)

(8.3)

(0.50)

2'02

(0.33) 1.91 (0.37)

Spring

20.4 (8.2) 15.8 (6.1) 24.8 (8.0)

“Stn 940, cruise I, is missing and stn 948, cruises I I, are missing one replicate each

2

and

3,

0,541 (0.194) 0.700 (0.142) 0.704 (0.129) 0.694 (0.194)

53 59 5’1

0.292 (0.158) 0'41s (0.178) 0.465 (0.200) 0.482 (0.215)

40 4-1 42 45

and stn 977, cruises 7 and

Many of the interaction terms were significant (Table 3). For example, the differences between stations are usually not consistent through different years (AB interaction), and differences between seasons vary with year (BC interaction). Variability in the community statistics between samples is related to both space and time. Spatial variation was considered between stations (Factor A) and between replicates. Temporal variation was considered between years (Factor B) and between seasons (Factor C). Calculation of variance components (Table 4) enabled measurement of the relative contribution of factors, interactions and replicates to variability. It must be remembered that in our ANOVAs we have treated stations and seasons as fixed factors. This means that the variance component associated with these factors is referable to those stations and those seasons specifically. That is, the variance component attributable to the difference between stns 940,948 and 977 is not necessarily that attributable to differences between another three stations in the same environment. We suspect that had the three areas represented by the three stations been sampled randomly interstation variability would have contributed a larger variance component than found in these results. Differences between the three stations and between years contributed the largest fractions (2~-36~/J of the variance in log N and s but little to H’,J’ or E. Seasonal differences, on the other hand, contributed negligibly to variance in any statistic except H’, where 12 “/bof the variance was attributable to season. Small-scale spatial patchiness and sampling err01

--

A three-year study of Benthos

3. F-ratios in five three-way also given

and levels ANOVAs.

TABLE

Factors and Interactions A (stations) B (years)

2,4 2,135 3,6

C (seasons)

AB AC BC ABC

4,135 6,12

x2

*Sign&ant **Significant

replicates

of significance associated Bartlett’s x2 values for

with factors within-sample

Community __----.-_----__----~----.. log N s 9.07* 90.30* 2.40

*

11'2j**

12,135

0.56 9.22* 7.88**

34

58.7**

6,135

Bartlett’s

TABLE

d.f.

4%

*

71.13** 64.96* 4.44* 1’22 r.14 2.95**

statistic H’

I.53

3.98 0.38 2.78 3.0x* 0.61 10.70** 6.92*

65.6**

46.8

*

component statistics

associated

with

*

0.94 19.72** 1.96 3.82** 0.50 13.96** 9.27**

98.9**

factors,

Community

A (stations) B (years) C (seasons) AB AC BC ABC Replicates

I:,

Y’

I.73 43.64** 2’22

7.81*” 0.46 13.16** ().16**

T~.~**

at 0.05 level. at 0.01 level.

4. Percentage variance for five community

Source of variance

and interactions variances arc

log N 22.6 22.3 4’3 7’7 8.; 20.X 14'0

statistic

s

H

136.2

4’3

--

27.1 5’7 0’4 3’4 3 ‘4 3’0 23.8

interactions

and

-Y

B

0 7’4 7’0 3 ‘4 0

IS.8

20’s

I “) 14’5 ‘7 .i ‘7. J 0 J6.h

34.6 27.1

39’4 22’2

33’5 If)'1

0 I2.2 3’0 0

within stations (replicates) contributed 14~qojo of variance of all statistics. The proportion of the variance contributed by the interactions and within-sample variability together was about 50!<, for log IV and 350; for s, contrasting with about 75-85’;; for H’, J’ and E. Variation in abundance of species At stn 940 the numerically-dominant species mere the bivalave Theora fragilis, the decapod Callianassa limosa, the bivalve Electroma georgiana, and the polychaetes Nephtys inornatn and Eupolymnia nebulosa; at stn 948, T. fragilis, C. limosa, the amphipod Byblis sp. I, the phoronid Phoronis pallida, N. inornata and the ophiuroicl Amphiura elandtformis; and at stn 977, T. fragilis, C. limosa, P. pallida, the bivalve Leionucula obliqua and the polychactc Myriochele sp. I (See Table 5 for species authorities). Few species showed clear scasonality in abundance. Most of those that did were less dense in 1974 than in other years. Theora frugilis [Figure s(a)] was most abundant in February at most stations and least in November but in 1974 the population at stn 977 failed to reach a high summer density. The abundance of two common echinoderms, Echinocardium cordatum [Figure j(b)] and Amphiura elundiformis [Figure s(c)] remained relatively constant throughout the period. PhoronispaZlida [Figure s(d)], L eionucula obliqua [Figure s(e)] and Myriochele sp. I [Figure 6(a)] showed little evidence of seasonality but had low densities at stn 977 in

486

G. C. B. Poore & S. Rainer

(a) 20(

Theora

-

frogills

stn 940 stn 94% Stn 977

I

---

IOC

IC

PCb )

Amphiuro

elondiformis

e

N E is % c x E 1

IC

(C)

Echinocardium

cordalum

I 5

30

‘Cd)

I Phoronis

le)

I

polfido

20

IO

15

Leionucula

obliqua

IO

5 , C

I se I I

I 2 1973

I. 3

I 4

b 5 I

I/ 6

1 7 I 974

I 8

1 9

I IO 1975

I II

I 12 I

Figure 5. Fluctuations in population density of species showing some seasonality (a), relatively constant densities (b, c), or reduced densities in 1974 (d, e). Data (number of individuals/o.1 m”) are means and standard deviations of 5 replicates.

1974. Myriochele sp. I, By&is sp. I [Figure 6(b)] and Nephtys inornata [Figure 6(c)] increased in density in 1975 at one or all stations. The reverse trend was shown at stns 940 and 977 by the dominant shrimp Callianussa Zimosa [Figure 6(d)]. Except for Leionuculu obliqua, Myriochele sp. I (both virtually confined to stn 977) and Byblis sp. I (stn 948), there were only small differences between stations in densities of the common species. Classification of samples The two normal hierarchies generated by the strategies outlined (Figure 7) were truncated at the level of eight groups, this being the level at which groups could be interpreted as being ecologically meaningful.

A three-year study of Benthos

487

The eight groups derived using the Canberra metric strategy were labelled CI through to C8, those using the Bray-Curtis strategy were labelled BI through to B8. The major division of samplesby the Canberra metric strategy wasinto the three stations. Only two samples,977/5 and 940/2, which fused with samplesfrom stn 948 were classified with another station. At a lower level in the hierarchy samplestended to group into temporally continuous blocks, e.g., 940/3-7 (group CS), 940/8-12 (group C7), and 977/10-12 (group c-1).

I a)

Myriochde

I I ,I _

Stn 940 Stn 949 --St” 977

sp.1

300

200 loo :

i ( b)

rp. I

Byblis

I-

I I

50 4 I’\

,’ -,A-----

Nephtys

Cl

_-I

I

v

/’

li

inornoto

! _I..I “i

,I

j’

?

d) SO

40

30

2( ICI-

Cru IIs@ I

I

2

3 1973

4

5 I

6

7 1974

6

9 I

IO 11 12 1975

I

Figure 6. Fluctuations in population density of species which either increased in density throughout the study period (a-c), or decreased (d). Data (numbers of individuals/o.1 m”) are means and standard deviations of 5 replicates.

G. C. B. Poole &f S. Rainer

488

cfuisos cruises

UN STN STN

crwts

station graupr

STN STN

948 977

12119 12 11 IO 9 7 4

8 6 3

ct

c2

2

10 a 4

1

8

1 c3

cfuisnl Ut~isaS 12 11 10 3 5

3

5 5 &c4

1

c5cLii

1 9 6 821

2

4

21211109 ---_

*roupr

El

62

B3

Figure 7. Dendrograms illustrating resulting from classification using (a) and the Bray-Curtis dissimilarity at the level of eight sample-groups.

Interpretation of the Bray-Curtis classification metric. Samples grouped in two ways : I.

2.

04

7

3 5

12 11 10 5

8 7

I 85

98

4

L-.--.. --~-~-C8

2 3

994 -

station

8 6

I-L87

the relationships between the the Canberra metric dissimilarity coefficient (b). Both dendrograms

69

35 samples coefficient are marked

was not as clear as that for the Canberra

By station. Group BI contained only samples from stn 977, group Bz only samples from stn 940, and the linked groups B7 and B8 mostly samples from stn 948 ; By season. Group B3 contained only May samples, group B4 mostly February samples, group Bg only November samples, and group B6 May and August samples.

Samples from stn 948 and stn 977 did not group particularly well by station or season while those from stn 940 tended to form a compact station group, Samples collected in different years classified differently. In 1973 the samples showed greater seasonal variability, while those from 1975 tended to group within station. No one season drew samples together across station boundaries more strongly than any other.

-

A three-year study of Benthos

Classification

489

of commonest species

Eight coherent speciesgroups were differentiated among the 60 commonestspecies(Table 5). The hierarchy linking the groups is shown in Figure 8. The characterization of sample groups by these speciesgroups (I to VIII) was determined by examination of the two-way tablesof speciesby samplegroups, and of tables of mean samplefidelity (Table 6) and constancy. 1. Four polychaetes and one bivalve largely confined to station group C6 (940/2). One species,Trichobranchus sp. I, has misclassifiedand doesnot belong to this group. II. Seven polychaeteswith highest fidelity in station groups CI, C6, BI, B3 and B7, that is, samplesfrom stn 977, especially the last cruise. Barantolla Zepte and Exogone sp. 2 were alsocommon in sample940/2. Most were rare at stn 948. III. Six speciesconfined largely to groups C7 and B2 (later cruisesfrom stn 940). These specieswere usually present at other times at stn 940 but were absentfrom stn 948 and rare at stn 977. IV. Six specieswhich were distributed much like those in group III to which this group is linked. Some of these species,Ascidiella aspersa, its commensalParaleucothoe noaaehollandiae, Electroma geovgiana and the anthozoan are epizoic. V. A large group of 13 widespread speciesfrom several taxa, with highest fidelities in groups CI, BI and B7. This group was most common at stn 977 during the last three cruises. VI. Nine specieswith affinities to station groups CI, Cz and BI. Like those in group V, most common at stn 977, especially the last cruisesbut they differed from the previous group in being lesswidespreadat other stations. Several taxa were represented. VII. Eleven speciesfrom diverse taxa, with moderateto low densitieswhich were neither highly faithful nor constant but widespreadacrossall stations. VIII.

The three most abundant specieswhich form a widespreadgroup.

1.4,.

I-----I E 2

1.3.

f

1-e -

g

I.1 -

% ‘ii .E 0

I-0 O-9

.

I

IImm

‘p:xImIxnI Spcciee

groups

Figure 8. Truncated hierarchy of eight using the Canberra metric dissimilarity species group are listed in Table 5.

species-groups derived by inverse analysis coeffkient. The names of species in each

490

G. C. B. Poore

TABLE

duals/m’)

&

S. Raker

5. The sixty most common species (average density greater than 2 indiviarranged in the eight groups derived by inverse hierarchical analysis

Group

I Anisodonta subulatu (Gatliff & Gabriel, 1910) (Bivalvia, Sportellidae) Caulleriella sp. 3, Cirmtulus sp. 2 (Polychaeta, Cirratulidae) Polydora sp. z (Polychaeta, Spionidae) Trichobranchus sp. I (Polychaeta, Trichobranchidae)

Group

II Barantolla lepte Hutchings, 1974, Chaetozone sp. I (Polychaeta, Tharvx sp. I. (Polychaeta, Cirratulidae) Oweka fkifoimishelle Chiaje, 1844 (Polychaeta, Oweniidae) Aricideafauoeli Hartman, 1957 (Polychaeta, Paraonidae) Boccurdiu sp. 3 (Polychaeta, Spionidae) Exogone sp. 2 (Polychaeta, Syllidae)

Capitellidae)

Group

III anthozoan sp. 7 (Anthozoa) Electromu georgiana (Quoy & Gaimard, 1835) (Bivalvia, Pteridae) Domilleo australiensis (McIntosh, 1885) (Polychaeta, Dorvilleidae) Harm&hoe spinosu Kinberg, 1855 (Polychaeta, Polynoidae) Eupo~ymnia nebulosu (Montagu, 1818 )(Polychaeta, Terebellidae) Paraleucothoe nowaehollundiae (Haswell, 1880) (Amphipoda, Leucothoidae)

Group

IV Carinoma sp. I (Nemertina, Palaeonemertea) Cirriformiu$ligeru (delle Chiaje, 1828), Thuryx sp. 2 (Polychaeta, Mugelona sp. 2 (Polychaeta, Magelonidae) Gyptis sp. I (Polychaeta, Phyllodocidae) Ascidiellu aspersa (Muller, 1776) (Ascidiacea, Ascidiidae)

Cirratulidae)

Group

V enoplid sp. 2 (Nematoda, Enoplidae) Leionuculu obliquu (Lamarck, 1819) (Bivalvia, Nuculidae) Capitellethus dispar (Ehlers, 1907) (Polychaeta, Capitellidae) Goniada sp. I (Polychaeta, Glyceridae) Nephtys imrmta Hutchings & Rainer, 1977 (Polychaeta, Nephtyidae) Myriochele sp. I (Polychaeta, Oweniidae) Puraonides sp. I (Polychaeta, Paraonidae) Eunoe sp. I, Purulepidonotus ampullifera (Grube, 1878) (Polychaeta, Polynoidae) Terebellides stroemi Sars, 1835 (Polychaeta, Terebellidae) Byblis sp. 1 (Amphipoda, Ampeliscidae) Echinocurdium cordatum Pennant, 1777 (Echinoidea, Loveniidae) Amphiura elandiformis Clark, 1966 (Ophiuroidea, Amphiuridae)

Group

VI Edwurdsia sp. I (Anthozoa, Edwardsiidae) Montacuta semiradiatu (Tate. 1889) (Bivalvia. Montacutidae) Lumbrineris latreilli A;douin &-‘iilne-Edwards, 1834 (Polychaeta, brineridae) Scolopolis cylindrifer Ehlers 1904 (Polychaeta, Orbiniidae) Afromysis uustruliensis Tattersall, 1940 (Mysidacea) cirolana corpulenta Hale, 1924 (Isopoda, Cirolanidae) Liljeborgiu sp. I (Amphipoda, Liljeborgiidae) Hulicarcinus rostrutus Haswell, 1882 (Brachyura, Hymenosomatidae) Trochodota allani Joshua, 1912 (Holothuria, Chiridotidae)

Group

VII Nozeba sp. I (Gastropoda, Rissoidae) Glyceru unzericanu Leidy, 1855 (Polychaeta, Glyceridae) Chaetopterus sariopedatus Renier, 1854 (Polychaeta, Chaetopteridae) Prionospio sp. 2 (Polychaeta, Spionidae) Dimorphostylis cottoni Hale, 1936 (Cumacea, Diastylidae)

Lum-

A three-year study of Benthos

491

Table 5 continued Heteromysis sp. I (Mysidacea)

oedicerotidsp. I (Amphipoda,Oedicerotidae) Paraphoxus sp. 3 (Amphipoda,Phoxocephalidae) Lucifer hanseni Nobili (Penaeidea, Sergestidae) Polyonyx trunntersus (Haswell,1882) (Anomura,Porcellanidae) Cullianassa arenosa Poore,1975(Macrura,Callianassidae)

Group VIII Phoronis pallida (Schneider,1862)(Phoronidea) Theora,fragilis (A. Adams,1855)(Bivalvia, Semelidae) Callianassa limosa Poore, 1975 (Macrura, Callianassidae)

Discussion Patterns

in community

statistics

Differences between stationswere found in the meannumbers of individuals and speciesbut not in diversity or evennessmeasures.These differencesare discussedfurther in the classification analysiswhere the patterns in distribution of speciesare explained by the nature of the sediment (more sandy at stn 977) and depth (shallower and closerto shore at stn 940). The variation of community statistics with time is a more significant result. Seasonal variation was relatively unimportant but year to year differenceswere much more marked. The available data on physico-chemicalvariables do not explain this phenomenon; no one station appearedto be physically or chemically more variable than any other. These results differ from somepreviously reported seasonalchangesin benthos in temperate climates. For example, Lie & Evans (1973) working in Puget Sound found little seasonalvariability in the number of speciesbut considerablechangesin the total number of individuals. Mean abundancevaried little from year to year, a finding quite different from that reported here for Port Phillip Bay. In a two-year study of shallow benthos in Rehoboth Bay, Delaware, where the annual temperature range is extreme, Watling (1975) found very marked repeatedseasonalchangesin the numbers of individuals and speciesand in evenness measuresbut not in Shannon’sdiversity. The Delaware fauna was much lessdiverse than that in Port Phillip Bay and dominant specieschangedduring the year. In contrast, Levings (1975) could find no seasonalityin N, s, H’ or J’ in a benthic community on soft mud in Nova Scotia. Diversity is more seasonallyvariable in areaswith greatest seasonalityin physical parameters, for example in Watling’s (1975) study, as is predicted from Sanders’(1968, p. 257) comparisons.But in fact rigid seasonalityin community structure is not a common phenomenon in shallow-water benthos and differences between years are often quite marked. Small scalepatchinessof the benthosat the specieslevel hasbeenwidely acknowledgedand investigated quantitatively. The effect of patchiness on community measureshas been examined lessfrequently. In our study differences between replicates contributed 14% of total variance in the numbers of individuals, but contribution to total variance in the number of species,diversity and evennesswas 19 to 27% (Table 4). Johnson(1970) attributed similar variability in intertidal benthos to small-scaledisturbancesor environmental heterogeneity and this may alsobe the casein our samplesbut we cannot suggesttheir form. The relative importance of small-scalepatchinessand seasonalitymust be consideredcarefully in designof benthic samplingprogrammesaimedto definebenthic communitiesin areassuchas Port Phillip Bay.

Number in group

Species

I

of samples

IV V VI VII VIII

III

II

group

3

3’9 I’2 1.7

2'2

0’2

0.8

0.8 3.5

CI

I’1

8

8

0.7

1.6

2'1

0’1 0.8 0.3 1.5

0‘0

0’2 1.1

c3

0’1 1.6

0'2

1’0 0.8

cz

0.6

1‘0

3

0’0 0.6 0.4

0'0

0’1 0.1

C4

Canberra

--

1'0

1'3

2

I

1.9

0.4 0’7

0'4

0’0 0.6

0’0

I.5

18.3 4.2

C6

set

0’0

0'0

0.8 0.6

C5

metric

5

0.4 o-8 0.6

O’j

0’1 0.6 4‘5 4’4

C7

j

0‘1 0’4 0.5

0'4

2'1

1’1 0.1 1‘3

C8

SAMPLE

5

1.6

1.2

2.7

2'1

~6” I’1

0’0

BI

7

0.3 0.6 0.6

0.5

0.5 3’7 4’2

0.2

B2

GROUPS

3

1.8

0.4

0.8

1'3

,5’;* ,i.6 0’0

B3

5

3

2.2

0’5

I.9

1.7

1'1

2.3 1.4 0.0 0’3

Bg

1.3

1.6

1'2

0.4 0.6 0.1 0’0

B4

set

j

0.3 0’3 0.6 1’3 0.5 0’3 0.4 0’5

B6

I

o-o 3’1 0.0 0.9 1.9 0’5 1.4 0’4

B7

6

0.6

I'2

0.6 0.3

0'2

0.1

0.2

0.7

B8

11

3

ii 6 13 9

5

Number of species in group

samples from Port Phillip Bay. The data given are all species in each species group. Values greater than

Bray-Curtis

6. Mean sample fidelities for two classifications of benthic means of fidelities over all samples in each sample group and over I indicate more individuals per sample than expected by chance

TABLE

-_

A three-year study of Benthos

403

The presence of significant heteroscedasticity in community statistics obtained from samplescollected from similar and relatively homogeneousareasis a factor that complicates their analysis.In the present study, the relative size of significant main effects in the analysis of variance suggeststhat the relationshipsfound were not spurious. However, the contributions of interaction and replicate terms to the total variance in H’, J’ and E considerably outweighed the contribution of the main effects. This fact and the presenceof heteroscedasticity suggeststhat particular care must be taken if these statistics are to be used in assessing the effects of environmental changes,whether in spaceor over time.

The fauna

In terms of the dominant species,the three stationsare essentiallysimilar. The two numerically most abundant species,Theora fragilis and Callianassa limosa, and many other common speciesare deposit-feeders with a strong preference for silty-clay sediments. Most are widespreadin Port Phillip Bay (Poore & Rainer, 1974; Poore, 1975; Poore& Kudenov, 1978; Emig et al., 1977). Port Phillip Bay resemblesthe Inland Sea of Japanwhich is also a deep embayment where Theora lubrica dominateson muddy sediments(Mukai, 1974). A second parallel between these two areasis the abundanceof nuculid bivalves (Leionucula obZipua at stn 977 in Port Phillip Bay and Nucula paulula in the Sea of Japan) on sandy mud sediments. Mukai (1974) mentioned few speciesother than bivalves although crustaceansand ophiuroids were common in someareas.Other embaymentswith muddy sedimentsdiffer from these two in being characterised by polychaetes or small crustaceans.St Margarets Bay, Canada, 17 m deep, has a soft mud sediment dominated numerically by an amphipod species,a polychaete and an ostracod (Levings, 1975). A very shallow area in Delaware, U.S.A., with silty sedimentswas inhabited by two different assemblages at different times, one dominated by an amphipod, the other by a polychaete (Watling, 1975). Within the Port Phillip Bay muddy bottom community, the three stationssampleddiffered only in the numbersand identity of non-dominant species.Many of thesedifferencescan be attributed to differences in substrate. The higher percentageof sand in the sedimentat stn 977 was probably largely responsible for high densities of deposit-feeding polychaetes: Myriochele sp. I, Terebellides stroemi, Eunoe sp. I and Capitellethus dispar. The depositfeeding bivalve, Leionucula oblipua, was alsocommon here. Some of the common speciescharacteristic of stn 940 indicate a more stable substrate than found elsewhere:the ascidianAscidiella aspersa, its commensalamphipod Paraleucothoe novaehollandiae, and anthozoan sp. 7. Stn 940 is much shallower than the other two, a feature which allowsgrowth of epibenthic algae.The greenalga, Caulerpa sp. wasoften taken in samplesfrom this station and provided a suitable substrate for the bivalve, Electroma georgiana, which wasoccasionallycommon.In contrast the brittle star, Amphiura elandiformis, was noticeably absentfrom this station. Only eight specieswere confined to stn 948; none was common. Sediment differencesmust have contributed to differences in absolutedensitiesof species. In particular, the shrimp, Callianassa Zimosa, wasmore abundant at stn 977 than elsewhere. Poore (1975) found that the density of this specieswashigher in muddy sedimentscontaining an appreciableproportion of silt. This study’s resultssuggestthat the presenceof somesand also favours C. Zimosa. Differences between the three areas in salinity, temperature and nutrients were slight and were of little help in explaining fauna1differences.Nutrient levels, especially phosphorus, were higher in Corio Bay than elsewhereand may indicate higher productivity. The link between this fact and benthic fauna1composition is a tenuous one.

494

G. C. B. Poore &? S. Rainer

Temporal

patterns in species composition

The classificationapproach to data analysisfailed to reveal any seasonalpatterns in species composition at any station. Instead, changesin the fauna with time were suggestedat stn 940 between cruises2 and 3 and between cruises7 and 8, and at stn 977 between cruises9 and IO. Specieswere identified which were virtually confined to samplesfrom stn 940 taken during cruise 2 and others, common on this occasion, became markedly less dense on subsequentcruises.At the samestation several speciesbecamemore abundant during later samplingoccasions(cruise 8 onwards). An increasein density of severalspecieswasapparent at stn 977 after cruise 9. These data indicate a rather unstable community structure except perhaps at stn 948. Changesin structure are not seasonalbut occur irregularly and persist over several seasons. Explanations for this behaviour may be sought in fluctuations in abiotic variables and in biological interactions. Although temperature showed a fairly regular seasonalcycle there were differences between years, notably in the longer summer period in 1973374. This period precededa year in which severalspecieshad unusually low densitiesbut it is impossible to speculateon the mechanismswhich may have operated to bring this about. Salinity was lower in late 1974than in other years and although this factor itself may have had little effect on the fauna it may indicate other changesin water quality associatedwith greater freshwater inflow into the bay in that year. Only one of the abrupt changesin fauna, that at stn 940betweencruise2 and 3, is associated with changesin hydrological factors. Between these two cruisesthere was a sharp rise in nutrient levelsnot seenat other stations(Figure 3). But a correlation between abiotic variables and fauna1changessuch asthese doeslittle to explain the phenomenon.The specieswhich were lost between the two cruises(speciesgroup I) are more normally found on sandy-silt sediments(Poore et al., 1975)and they may not have been able to maintain their populations at muddy stn 940 in the face of competition from other species. Biological interactions between species,predation, competition for space or food and trophic group amensalism(Rhoads& Young, 1970) must alsoplay a significant role in explaining many of the observed irregular population fluctuations. However, without experimental data it is fruitless to hypothesiseon these. In fact, many speciesfluctuate more or less synchronously and no caseof exclusion of one speciesby another is obvious. This is in contrast to the findings of Buchanan et al. (1974) who concluded that one species,of the genusAmmotrypane, had played a crucial role in the balanceof production of the community as a whole. Seasonalityin muddy-bottom benthic community composition is a commonphenomenon only in cool-temperate latitudes (Boesch et al., 1976). Highly seasonalfluctuations in the abundanceof dominant specieshave beenshown, for example, in Rehoboth Bay but a switch between separatedeposit-feeding assemblages also occurred (Watling, 1975). In the Dutch Wadden Sea seasonalchangesin biomasswere recorded over a s-year period (Beukema, 1974). Buchanan et al. (1978) also found several changesin biomassand in the density of dominant speciesin a benthic community of the Northumberland coastover a 6-year period. However, many workers have failed to demonstrate strong seasonalityand, as in our study, have shown benthos to fluctuate rather aperiodically. Buchanan et a/. (1974, 1978) found that the broad featuresof their deepbenthic community remainedstablefor somewhat more than a decadebut that the relative numbersof individuals of dominant specieschanged progressively over the period. They suspectedthat these changeswere leading towards a more stabilized equilibrium condition with the passageof time and may be related to variability in winter temperatures from year to year (Buchanan et al., 1978). Lie & Evans

-.-

A three-year

study

of Benthos

495

found that the relative abundanceof the commonspeciesin Puget Sound macrofauna varied but lacked seasonality. Speciesdensitiesin benthos of two Californian lagoonsalso showedlittle seasonality(Peterson, 1975) and Levings (1975) was able to find annual cycles only in the numbers of common speciesin St Margarets Bay. Strong aperiodic fluctuations similar to those found in Port Phillip Bay have been found by Ziegelmeier (1963) in the German Bight and by Boesch(1974) and Boeschet al. (1976) in ChesapeakeBay. Stephensonet aZ. (1974), working in southern Moreton Bay, Queensland,found annual changesin speciescomposition more important than seasonalones. They too had trouble explaining thesechangesbut suggestedsalinity changes(floods and drought) may have been an influencing factor. Stephensonet al. (1976) again found marked fluctuations in populations of many species in Moreton Bay and pointed out how readily one biotic assemblage may replace another if environmental conditions were not too greatly disturbed. They argued that the use of dominant speciesto characterise benthic communities (Petersen, 1914) is not always a suitable approach to the complex and confusing community concept. Mills (1967, 1969), who worked with a benthic community in which speciescomposition was not persistent throughout the year, was also led to argue against the rigid definition of communities in terms of speciescomposition. Though this appliesto highly diverse communities (Poore & Kudenov, 1978), there is stability in the dominant speciesof some muddy bottom communities. Over the j-year sampling period the benthos of silty-clay sedimentsin Port Phillip Bay showedirregular fluctuations in the density of the common speciesand in the identity of the minor species.Two species,Theora fragilis and Callianassa Zimosa, remained dominant over the period. These two specieswere alsodominant in silty-clay sedimentswhen quantitative samplingwasinitiated in the areain 1969(MMBW & FWD, 197-j) so that the major species in the community remainedunchangedover a period of six years. The concept of multiplcstable points hasbeen applied to soft-bottom benthic communitiesby Gray (1977)using the published work of Mills, Boesch,Pearsonand others. In our study the irregular changesin subdominant speciessuggestthat multiple-stable points may exist for the silty-clay community. The persistenceof Theora and Callianassa as co-dominantscan be taken to indicate that these two speciesdid not unfavourably alter each other’s environment over a period of six years. The samplingsites chosenwere selectedbecausethey possessed the most environmental stability available to us. Stations 948 and 977 in particular were remote from inputs of fresh water or nutrients. The extent of changesthat did occur in speciescomposition lend weight to the suggestionthat considerablevariation may occur in soft-bottom benthic communitiesin the absenceof marked environmental perturbations. It is also indicative of a community in which the speciesare only loosely interrelated, as seemsto be true of many soft-bottom communities. (1973)

Assessment of classification

methods

The properties of the Canberra metric and Bray-Curtis dissimilarity coefficients are wellknown (Clifford & Stephenson, 1975). In theory, all speciescontribute equally to the Canberrametric over the range zero to one and contributions are averaged.The Bray-Curtis coefficient, in contrast is dominated by abundant species;rare onescontribute little and for this reasonthe Bray-Curtis is now rarely usedwithout data transformation. In this study we were interested in comparing samplerelationships in terms of species composition (Canberra metric) with relationships in terms of dominance (Bray-Curtis),

496

G. C. B. Pool-e & S. Raker

Accordingly, data transformation wasnot performed for the Bray-Curtis measure.Using the two contrasting measureswe have found that the main differences between stationswere in overall speciescomposition, not in densities of dominant species.Regular seasonalcycles in density of the commonestspecieswere weak and accordingly neither coefficient link4 samplesfrom the sameseasontogether. Hailstone (1976) used the Canberra metric coefficient to measurerelationships between dredge samplesfrom Moreton Bay, Queensland.He found that neither samplesfrom the samestation nor from the sametime grouped strongly together. Although his result for space differed from ours, his findings emphasisethe difficulty in showing seasonalpatterns by these methods. The changesin community structure which were noted were not simultaneousat all stations. This phenomenon argues against use of currently available three-dimensional classificationmethodswhich look for patterns in both spaceand time (Williams & Stephenson, These methodsanalysefor time related changesby summing 1973 ; Stephensonet al., 1974). data from a single time acrossall stations. This approach would not have revealedthe only significant temporal fauna1changesfound in this study. Acknowledgements We wish to thank our field and laboratory assistants,in particular Merryn Dawes, for help in collecting and sorting the material. We acknowledgeuseful advice from Dennis Reid (CSIRO) and Mike Mobley (MSG) on designand interpretation of the analysisof variance. We also thank Professor W. Stephenson, University of Queensland, and Dr D. Boesch. Virginia Institute of Marine Science, for their valuable criticism.

References Beasley, A. W. 1966 Port Phillip Survey 1957-63. Bottom sediments. Memoirs of the National Muserrm of Victoria 27, 69-106. Beukema, J. J. 1974 Seasonal changes in the biomass of the macrobenthos of a tidal Aat area in the Dutch Wadden Sea. NetherlandsJournal of Sea Research 8, 94-107. Boesch, D. F. 1974 Diversity, stability and response to human disturbance in estuarine ecosystems. Proceedings of the First International Congress of Ecology pp. 109-114. Boesch, D. F., Wass, M. L. & Virstein, R. W. 1976 The dynamics of estuarine benthic communities. In Estuarine Processes. Vol. I. Uses, Stresses and Adaptation to the Estuary. Academic Press, New York, pp. 177-196. Buchanan, J. B., Kingston, P. F. & Sheader, M. 1974 Long-term population trends of the hcnthic macrofauna in the offshore mud of the Northumberland coast. Journal of the Marine Biological Association of the United Kingdom 54, 758-795. Buchanan, J. B., Sheader, M. & Kingston, P. F. 1978 Sources of variability in the benthic macrofuna off the south Northumberland coast, 1971-1976. Journal of the Marine Biological Association of the United Kingdom 58, 191-210. Clifford, H. T. & Stephenson, W. 1975 An Introduction to IVumerical Classification. Academic Press, New York, xii, 229 pp. Emig. C. C., Boesch, D. 17. s( Rainer, S. 1977 Phoronida from Australia. Records of the ifustrcdi(m Museum.30,455-474. Frankenberg, D. 1971 The dynamics of benthic communities off Georgia, USA. ThLiZassiar7rgoslavicci 7949-55. Gray, J. S. 1977 The stability of benthic ecosystems. Helgolander Wissenschaftliche Meeresunterstlchu~tgett 3% 427-444. Hailstone, T. S. 1976 Delimitation of subtidal macrobenthos associations at the mouth of the Brisbane River. Australialt Jownal of Marine and Freshwater Research 27, 217-238. Johnson, R. G. 1970 Variations in diversity within benthic marine communities. Anzerican Nutrrrdist x04,285-300.

A three-year

-.---

study

of Benthos

497

Lance, G. N. 8i Williams, W. T. 1967~ A general theory of classificatory sorting strategies. I. Hierarchical systems. Computer Journal 9, 373-380. I,ance, G. N. & Williams, W. T. r967b Mixed data classificatory programs I. Agglomerative systems. Australian ComputerJournal I, 15-20. Levings, C. D. 1975 Analyses of temporal variation in the structure of a shallow water henthic community in Nova Scotia. Internationale Revue der Gesanten Hydrobiologie 60, 449-493. I,ie, I;. & Evans, R. A. 1973 Long-term variability in the structure of suhtidal benthic communities in Puget Sound, Washington, USA. Marine Biology 21, 122-126. hIills, E. L. 1967 The biology of an ampeliscid amphipod crustacean sibling species pair. Jotrrnnl oj the Fisheries Research Board of Canada 24, 305-355. Mills, E. I,. 1969 The community concept in marine zoology, with comments on continua and instability in some marine communities: a review. Journal of the Fisheries Research Board of Canada 26, 1415-1428.

MMBW & FWD 1973 Environmental Study of Port Phillip Bay. Report on Phase One, I@--1971. Melbourne and Metronolitan Board of Works, and Fisheries and Wildlife Department of Victoria, Melbourne, 372 pp. . Rlukai, H. 1974 Ecological studies on distribution and production of some benthic animals in the coastal waters of central Inland Sea of Japan.Journal of Science of the Hiroshima University Ser. B. Div. I (Zoology) 25, 1-82. Petersen, C. G. J. 1914 Valuation of the sea. II. The animal communities of the sea bottom and their importance for marine zoogeography. Report of the Danish Biological Station 21, 1-68. Peterson, C. H. 1975 Stability of species and of community for the henthos of two lagoons. Ecology 56, 958-965. Poore, G. C. B. 1975 Systematics and distribution of Callianassa (Crustacea, Decapoda, Macrura) from Port Phillip Bay, Australia, with descriptions of two new species. Pacific Science 29, 197-209. Poore, G. C. B. & Kudenov, J. D. 1978 Benthos of the port of Melbourne: the Yarra River and Hohsons Bay. AustralianJournal of Marine and Freshwater Research 29, 141-155. I’oore, G. C. B. & Rainer, S. 1974 Distribution and abundance of soft-bottom molluscs in Port Phillip Bay, Victoria, Australia. AustralianJournal of Marine and Freshwater Research 25, 371-41 I. I’oore, G. C. B., Rainer, S. F., Spies, R. B. & Ward, E. 1975 The zoohenthos program in Port Phillip Bay, 1969-73. Fisheries and Wildlife Paper, Victoria 7, 1-78. Rhoads, D. C. Sr Young, D. K. 1970 The influence of deposit-feeding organisms on sediment stability and community trophic structure. Journal of Marine Research 28, 150-178. Sanders, H. L. 1968 Marine henthic diversity: a comparative study. American Naturalist 102, 243-282. Simpson, G. G., Roe, A. & Lewontin, R. C. 1960 Quantitative Zoology (Revised Edition). Harcourt Brace & Co., New York, 440 pp. Stephenson, W., Raphael, Y. I. & Cook, S. D. 1976 The macrohenthos of Bramble Bay, Moreton Bay, Queensland. Memoirs of the Queenstand Museum 17, q-447. Stephenson, W., Williams, W. T. & Cook, S. D. 1972 Computer analyses of Petersen’s original data 011 bottom communities. Ecological Monographs 42, 387-415. Stephenson, W., Williams, W. T. & Cook, S. D. 1974 The henthic fauna of soft bottoms, southern Moreton Bay. Memoirs of the Queensland Museum 17, 73-123. \Vatling, L. 1975 Analysis of structural variations in a shallow estuarine deposit-feeding community. ~olrrnal of Experimental Marine Biology and Ecology 19, 275-313. \Yilliams, W. T. 8r. Stephenson, W. 1973 The analysis of three-dimensional data (sites x species p: times) in marine ecology. Journal of Experimental Marine Biology and Ecology II, 207-227. Ziegelmeier, E. 1963 Das Makrohenthos im Ostteil der Deutschen Bucht nach qualitativen und quantitativen Bodengreifenmtersuchungen in der Zeit von 1949-1960. Ver~ffentlichungen des Institnts fiir Meeresforschung in Bremerhaven, Sonderband I (3. Meereshiologie Symposium), IOI--II.+.