Temporal changes in the benthos along a pollution gradient: Discriminating the effect of natural phenomena from sewage-industrial wastewater effects

Estuarine,

Coastal

and She&Science

(1991) 33,383-407

Temporal Changes in the Benthos along Pollution Gradient: Discriminating the Effects of Natural Phenomena from Sewage-Industrial Wastewater Effects

S. P. Ferraro,

R. C. Swarm,

F. A. Cole and D. W. Schults

U.S. Environmental Protection Agency, Pacific Ecosystems Branch, Hatfield Marine Science Center, 2111 S. E. Marine Science Drive, Oregon 97365, U.S.A. Received

16 October

1990

and in revisedform

a

1 April

ERL-N, Newport,

1991

Keywords: environmental impact studies; temporal variations; pollution; macrobenthos; toxicity; contaminants; California coast

marine

As pollution from the Los Angeles County Sanitation Districts (LACSD) outfalls decreased between 1980 and 1983, the macrobenthic community partially recovered and surficial(&2 cm deep) sediment contamination and toxicity decreased at 60 m water depth along a pollution gradient from the outfalls. Pollution from the LACSD outfalls continued to decrease but macrobenthic conditions and surficial sediment quality deteriorated 1 km, was unchanged 3 km, and improved 5-15 km from the LACSD outfalls between 1983 and 1986. The net effect of natural phenomena is indicated when ecosystem changes occur in the opposite direction from that expected under prevailing pollution conditions. Our data suggest that the net effect of natural phenomena (e.g. winter storms, El Nitio) on the benthos was greater than LACSD wastewater effects 1 km, about equal to LACSD wastewater effects 3 km, and less than the LACSD wastewater effects 5-15 km from the outfails at the LACSD 1983-86 mass emission rate. Surficial sediment samples collected beyond the 1 km station from the LACSD outfalls probably represented B 3 years of natural + effluent particulates accumulation, and they were, therefore, better suited for detecting longterm trends than for testing short-term temporal variability in sutlicial sediment contamination and toxicity. Nevertheless, some contaminants in the surficial sediments significantly increased between 1983 and 1986, probably primarily reflecting renewed wastewater effects near the outfalls and the effects of natural phenomena (e.g. storm-induced sediment transport or erosion) further from the outfalls. Since natural phenomena may have an effect on the benthos 2 3 years of LACSD wastewater effects, short-term benthic changes must be interpreted cautiously at the study site.

Introduction Predictable temporal and spatial changes in benthic community structure and composition occur in response to changes in pollution (sensu Clark, 1989) from sewage-industrial discharges (Pearson & Rosenberg, 1978). The typical response to moderate pollution 0272-7714/91/100383

f25

$03.00/O

@ 1991

Academic

Press

Limited

384

S. P. Ferraro et al.

increasesfrom a sewage-industrial outfall is an increase in benthic species richness, numerical abundance and biomassover background. As pollutant loads increasefurther, speciesrichness, abundance and biomassdecreaseto levels near or below background and benthic community composition shifts towards more pollution-tolerant, opportunistic species.High pollutant loadings may drive the benthos to an afaunal state. The Pearson and Rosenberg (1978) model provides a useful conceptual framework for predicting macrobenthic spatial and temporal successionin response to organic enrichment and chemical contamination. Information on the degree of sediment contamination and sediment toxicity is also often useful for assessingpollution impacts and relating potential causesand effects (Chapman & Long, 1983; Long & Chapman, 1985; Swartz et al., 198%,1986). The effectiveness of pollution control measurescan be assessedby monitoring ecosystemresponsesfollowing their implementation (Boesch et al., 1990; National Research Council, 1990). Surveys of the macrobenthos, sediment contamination, and sediment toxicity along a pollution gradient from the Los Angeles County Sanitation Districts (LACSD) outfalls showed that substantial reductions in the massemissionof suspended solids and chemical contaminants from the LACSD outfalls coincided with a partial recovery of the benthos and improved sediment quality between 1980 and 1983 (Swartz et al., 1986). A direct link between the reduction in wastes and the extent of recovery, however, was not possible. Natural phenomena, in particular, a seriesof unusually severe winter storms and El Nina southern oscillation events in 1982-83 (Dayton & Tegner, 1984; Seymour et al., 1984; Stull et al., 1986~; Stull, 1988), may have been primarily responsiblefor, or significantly contributed to, the improvements observed (Swartz et al., 1986; Stull, 1988). In 1986, we repeated the surveys conducted in 1980 and 1983 by Swartz et al. (1985a, 1986). Our purpose was to discriminate the net effect of natural phenomena (e.g. winter storms, El Nifio) from ongoing LACSD wastewater effects (i.e. organic enrichment and chemical contamination resulting from the deposition of LACSD effluent particulates). The flow from the LACSD discharge has been approximately 5 x 10” 1year i (3.6 x lo8 gal day-‘) since 1971 [Southern California Coastal Water Research Project (SCCWRP), 19891.About two-thirds of the flow is from residential sourcesand one-third from industrial and commercial sources(Tetra Tech, 1981). The massemissionof 21 or 22 of LACSD’s monitored effluent components (suspended solids, metals, chlorinated hydrocarbons, etc.) decreasedby an average of 14.2O, between 1977 and 1980, 18.6”,, between 1980 and 1983, and 39,6O,, between 1983 and 1986 (Schafer, 1978, 1982, 1984; SCCWRP, 1987a). If reduced pollution wasthe primary causefor the partial recovery of the benthos along the LACSD pollution gradient in 1983, one would expect further recovery (or at least no change) of the benthos in 1986 since LACSD’s effluent quality continued to improve after 1983. But if transient natural phenomena, such as the winter storms and/or El Nifio were primarily responsible for the partial recovery observed in 1983, one would expect a regression towards more polluted benthic conditions in 1986 sincethe influence of those events on the benthos is likely to be temporary. Our approach for distinguishing the effects of natural phenomena from wastewater effects was to inspect the direction of temporal changesin the benthos. The net effect of natural phenomena is indicated when ecosystemchangesoccur in the opposite direction from that expected under prevailing pollution conditions. Our expectations for the direction of change were based on Pearson and Rosenberg’s (1978) model of macrobenthic succession, and on the relations: sediment contamination and sediment toxicity=f

Temporal changes in the benthos

,,

Los

Angeles

City

385

outfalls

Palos

Santa

Monica

Figure

Bay

Verdes

Penlnsulc

I

--

1. Location

of sampling

stations

in the Southern

California

Bight,

U.S.A.

(LACSD massemissionof pollutants). During any given time interval natural phenomena and settleable solids from the wastewater impinge upon the bottom in the vicinity of sewageoutfalls. An observed change in a parameter over time interval t at a given location in a wastefield (d,) can be expressed asthe sum of the effects of natural phenomena over time t+lag time j (d,) and the wastewater effects over time t+lag time i (d,); i.e. d,= d, + d,,,. If we know, asin this study, d,,, is decreasing,and we observe that d, isin the opposite direction of expected changeswhen pollution is decreasing,then, logically, d, > d, and d, is a minimum estimate of d,. If d, is in the same direction as the expected change due to wastewater effects, we cannot distinguish d, from d, without a priori knowledge of the kind and magnitude of change associatedwith d, and d,. Exact quantification of d, and d, is not possible by this approach. Nevertheless, with careful analysis of sufficient time seriesdata the approach may yield useful estimatesof d, relative to d,. Materials

and methods

Sediment and macrobenthos sampleswere collected in 1986at 60 m water depth along the LACSD pollution gradient in the sameway as Swartz et al. (1985a, 1986). Collections were taken in May 1980 at stations 1,2,3,4,6,8 and 9 (Swartz et al., 1985a), and in June 1983 (Swartz et al., 1986) and June 1986 (this study) at stations 1, 3, 4, 5, 6, 7, 8 and 9 (Figure 1). Stations 1 to 8 were located 1 to 15km north-west of the LACSD outfalls in the direction of predominant benthic deposition of effluent particulates (LACSD, 1981). Station 9, which is 47 km from the LACSD outfalls, is the closest site in the study area representative of background benthic conditions (Word & Mearns, 1978). The Los Angeles City outfalls in Santa Monica Bay have little or no influence on either the pollution gradient stations (1 to 8) or the reference station (9) (Bascom, 1978; Bascom et aZ., 1978).

386

S. P. Ferraro et al.

Ten 0.1-m’ van Veen grab sampleswere taken at each station. The contents of five of the grabs were sieved through a 1.O-mm meshscreento collect macrofauna. Material retained on the screen was preserved in buffered 100,; formalin in seawater, later transferred to 700/, ethanol, sorted to major phylogenetic group, and weighed ( + 0.1 g) after blotting on absorbent paper. Specimens were counted and identified to the lowest possible taxon, usually species.When the identity of a specieswas uncertain, we assignedthe alphabetic codes of the Southern California Association of Marine Invertebrate Taxonomists (e.g. Tharyx sp. A). Taxonomic accuracy, precision, and synonymy (Ellis & Cross, 1981)were updated and other minor changeswere made to the 1980 and 1983 data in order to make the three data setsdirectly comparable. Problems with the winch used to retrieve the grab at station 9 in 1986 resulted in a loss ( - 20yb) of samplefrom the sidesof the grabs. This introduced a low bias in someof the fauna1statistics for station 9 in 1986. It did not affect our ability to detect temporal changes in the fauna at the stations (1 to 8) ofmost interest, i.e. those in the LACSD wastefield. Nor did it affect our interpretation of the direction of change from background (see below) since essentially the sameresults were obtained whether the mean of only 1980 and 1983, or the mean of 1980,1983 and 1986 station 9 fauna1data was usedto estimate background conditions. The surface of the 1986 station 9 sampleswas undisturbed so there was no effect on the geochemical and toxicological samples. Benthic community structure was analysed in terms of speciescomposition, species richness (S = number of speciesper 0.1 m’), abundance (A = number of individuals per 0.1 m’), biomass(B = g, wet weight, per 0.1 m*), a Dominance Index defined asthe minimum number, or fraction, of specieswhose combined abundance wasequal to 750, of the individuals in the sample (Swartz et al., 1985a, 1986), and the Infaunal Index (Word, 1978,198O). The Infaunal Index for the Southern California Bight is basedon the relative proportion of 53 invertebrate taxa in four groups. The Infaunal Index ranges from zero when all specimenscollected belonging to the index are representative of polluted conditions (Group IV) to 100 when all specimens collected belonging to the index are representative of background conditions (Group I). Our characterization of the pollution tolerance of species is derived from the Infaunal Index group assignments: Group I = pollution-sensitive; Group II = slightly pollution-tolerant; Group III = moderately pollution-tolerant; and Group IV = pollution-tolerant (Mearns & Word, 1982). Samples from five grabs at each station were used for geochemical and toxicological analyses.Redox potential (E,) was measured by inserting a Pt/calomel electrode (Orion model 96-78) 1 cm beneath the sediment surface immediately upon retrieval of the grab. Cores were taken from the surficial (O-2 cm deep) sediment layer in each grab for analysis of sediment toxicity, total volatile solids, total organic carbon, O,,,silt + clay, total sulphide, 5day biochemical oxygen demand (BOD), total oil and grease, hydrocarbon oil and grease,metals (Cd, Pb, Zn, Cr, Cu, Ni), bis(2-ethylhexyl) phthalate (DEHP), and 4,4’DDE. DDE and DEHP were measured in two grabs from each station in 1980. All other parameters were measuredin five replicate grab samplesfrom each station. The methods used to analyse the geochemical samplesare described in Swartz et al. (1985&z),except we report for all three surveys total organic carbon determined by high-temperature (> 1200“C) dry combustion (model WR-12, LECO Corporation, St Joseph, MI), I’(, silt + clay (> 4~) determined by the sieveand pipette method (Buchanan, 1984), and DDE and DEHP concentrations corrected for recovery. All bulk sediment chemical concentrations are expressed on a dry weight basis. Sediment toxicity was determined by mean survival in the phoxocephalid amphipod Rhepoxynius ubronius lo-day test (Swartz et al.,

Temporal changes in the benthos

387

198%). Sediment from the Yaquina Bay, Oregon collection site of R. abronius wasused as a control for the sediment toxicity tests. Temporal differences in the arithmetic mean or geometric mean (asappropriate) of all measuredbiological and geochemical parameters at each station were tested by analysisof variance followed by multiple comparisonsusing Student-Newman-Keuls test, or, when variances were heterogeneous, by an approximate test of equality of means using the Games and Howell method (Sokal & Rohlf, 1981). Dunnett’s test (Steel & Torrie, 1960) wasusedto compare mean survival of R. abronius exposed to sedimentsfrom the study site with survival in Yaquina Bay control sediment. Adjustments for possible sediment particle size effects on R. abronius survival were made using Dewitt et al.‘s (1988) equation (5). The significance level was P
Thqv

r sp. A” (PO )

(PE)

~pp.~ (OS)

pelodes (E)

Telli?za carpenteri

Euphilomedes

(OL)

(PO)

spp.”

cornuta franciscatra”

prorem

Lisrriolobus

Nereis

Oligochaeta

Nephtys

(PO)

1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986

(PO)

Capitellu

spp.”

Year

316.6 34.4 305.8 7.8 1.6 1.8 0 0.2 0 10.6 0 4.0 0 1.0 0 0.2 84.6 1.4 0.6 22.0 7.2 0.2 34.6 6.2

1

1. Mean densities of the three most abundant 0.1 -ma grabs were taken at each station

Species

TABLE replicate

172.6 0.2 0.4 0.8 1.2 0 0.2 0 0 11.4 0.8 13.4 28.6 2.0 2.0 0.2 19.6 I.0 2.4 21.8 6.0 0.2 46.8 63.4

3

species

4.2 0.8 1.8 0.2 0.2 0 101.6 7.8 0.8 5.2 2.6 12.0 6.0 0.8 0.2 0.6 35.8 0.2 2.2 8.4 0.6 42.4 24.4 221.4

4

at at feast

one

5

nd 1.0 1.0 nd 0.8 0 nd 26.2 0.6 nd 1.4 16.6 nd 1.8 0 nd 48.6 2.6 nd 16.0 1.0 nd 268.6 217.0

station

Station

in the

6

9.6 0.8 0.6 0.2 0.4 0 55.8 1.2 0.8 26.8 5.2 21.6 45.2 Il.0 0.2 10.2 54.2 26.4 3.6 11.2 1.6 1194.0 394.0 220.6

Southern

California

nd 0 0 nd 0.2 0 nd 0.2 0.8 nd 5.8 10.2 nd 5.0 0 nd 107.6 1.0 nd 8.8 3.0 nd 509.6 46.2

7

Bight

8

0.2 0 0 0.6 0.2 0 0 0 0 6.4 2.4 4.2 24.4 2.2 0 74.2 3.0 0.2 44.4 6.6 12.8 113.8 30.0 0.6

in 1980,

1983

0.2 1.0 0.2 0 2.8 0 0 0 0 0.2 0.8 0.2 0,8 0 0 2.2 1.2 2.6 3.8 4.6 8.8 0.8 1.4 0

9

or 1986.

Five

serricatab

light?

sp. M (PO)

urtica”

Axinopsida

l’rionospio

Myriochele

Amphiodin

Rhepoxynius

missionensi?

Spiophanes

(A)

(PO)

1983 1986

1983 1986

1983 1986 1980 1983 1986

1983 1986

1980 1983 1986 1980 1983 1986

1980 1983 1986 1980 1983

3.6 15.0 4.4 0 26.6 0.4 0 1.0 0 0 3.6 0 0 0.4 0 0 5.4 0 0 0 0 0 0 0 0 0 0

12.2 27.4 64.6 0.2 21.2 4.8 1.8 13.4 25.0 1.8 5.4 2.6 0 10.8 0.2 0.2 6.2 0 0 0 0 0 0 0 0 0 0

nd = no data; PO = polychaete; PE = pelecypod; E = echiuroid; ‘Infaunal Index Group I: pollution-sensitive. “Infaunal Index Group II: slightly pollution-tolerant. ‘Infaunal Index Group III: moderately pollution-tolerant. “Infaunal Index Group IV: pollution-tolerant.

bicuspidatuP

(PO)

(PEj

(PO)

(PO)

(OP)

(PO)

culiforniensisb

cal~forniensis”

tenuisculpta~

Pectinaria

Mediomastus

Parvilucinu

OS = ostracod;

335.4 98.6 96.0 83.8 52.0 18.2 22.0 7.4 3.6 2.8 15.2 4.6 0.4 2.0 0.8 0.4 0.6 0 0 0 0 0 0 0.2 0 0 0 OP = ophiuroid;

nd 384.0 350.2 nd 128.2 12.4 nd 10.4 6.4 nd 28.8 21.6 nd 3.4 6.0 nd 0.4 0.2 nd 0 0 nd 0 0 nd 0 0 A= amphipod;

1498.6 807.6 461.6 529.4 47.6 15.0 51.2 14.6 4.0 67.6 58.4 18.4 15.8 4.0 13.4 0.4 0.8 0 0 0 0 0 0.2 0.2 0 0 0

155.0 30.6 62.8 81.6 7.4 1.2 52.6 24.4 2.2 74.2 46.8 30-8 95.4 20.6 45.2 3.8 1.8 0.4 0.8 0 28.8 0.2 0 14.0 0 0 0 OL = oligochaete.

nd 270.4 502.8 nd 41.4 13.0 nd 19.2 1.8 nd 76.8 37.6 nd 13.2 16.0 nd 0.2 0.4 nd 0.2 0 nd 0 0 nd 0 0

33.4 3.2 5.0 7.6 25.2 0.6 15.2 29.4 4.6 39.2 42.2 25.0 21.0 9.6 8.4 1.0 46.6 0.8 53.0 1.6 3.8 131.0 89.4 205.6 23.0 5.4 20.8

390

S. P. Ferraro et al.

exception (Tharyx sp. A at station 4 in 1986), there was a decreasingtrend in the density of both Tharyx sp. A and M. californiensis at stations 4 to 8 between 1980 and 1986. A decreasing trend was also observed for L. pelodes, and P. californiensis at stations 4 to 8, and oligochaetes at stations 4 and 6. Euphilomedes spp. and Tellina carpenteri peaked in abundance at stations 1 to 6 in 1983. Amphiodia urtica (ophiuroid, Group I), the dominant speciesat the reference station (9) in 1980, 1983and 1986, was rare or absent from all other stations except station 8 in 1986 (Table 1). Rhepoxynius bicuspidatus (amphipod, Group I) was only collected at station 9 in 1980, 1983 and 1986. Several other pollution-sensitive speciesnot in Table 1, e.g. Marphysa sp. A, Sthenelanella uniformis, Ampelisca spp. and Phoronis sp. A, which had been rare or absent at stations 3 to 8 in 1980 and present at low densities at someof the intermediate stations in 1983, increasedin abundance and were collected at stations closer to the outfalls in 1986. Community

structure

The pattern of the macrobenthos species,abundance and biomass(SAB) curves for 1980, 1983and 1986(Figure 2) wastypical of that found along pollution gradients from sewageindustrial outfalls (Pearson & Rosenberg, 1978). In each year the SAB curves peaked at station 5, 6 or 7 (7 to 11km from the LACSD outfalls) and progressively decreased to levels near or below background at station 1. Although the general pattern of the SAB curves wassimilar, their peakednessdecreasedmarkedly between 1980and 1983,and, to a lesserextent, between 1983and 1986. Temporal changesin community structure statistics at stations 1 to 8 were interpreted relative to background [characterized asthe grand mean (i.e. the mean of all observations in 1980, 1983 and 1986) at station 91: a statistically significant change closer to the grand meanat station 9 indicating improving conditions, a statistically significant changefurther from the grand mean at station 9 indicating worsening conditions. For example, a statistically significant increase in speciesrichness between years at a given station would be considered an indication of improving conditions if the change moved speciesrichness closer to the grand mean speciesrichness at station 9, or it would be considered an indication of worsening conditions if the change moved speciesrichness further away from the grand mean speciesrichness at station 9. At station 1, speciesrichness, and the Dominance and Infaunal Indices significantly increased between 1980 and 1983 (indicating improving conditions), then returned to 1980levels in 1986(indicating worsening conditions) (Table 2). The samethree measures at station 3, after significantly increasing between 1980 and 1983 (improving conditions), did not change between 1983 and 1986. At stations 4 to 8 between 1983 and 1986, there were three significant changesindicative of worsening conditions (increasing speciesrichnessand decreasingInfaunal Index at station 7, and increasing speciesrichness at station 8), and 10 significant changesindicative of improving conditions [increasing speciesrichnessand Infaunal Index at station 4, increasing speciesrichness at station 5, decreasing abundance and increasing Dominance Index at station 7, and increasing abundance, Infaunal Index, and density of amphipods, phoxocephalids (a pollution-sensitive group of amphipods) and echinoderms at station 81 (Table 2). For the period 1980-86, there were no significant changes in eight community structure parameters at station 1, while at stations 3 to 8 there were 14 significant changes indicating improving conditions and only three significant changespossibly (seefootnote b in Table 2) indicating worsening conditions.

Temporal changes in the benthos

391

100 :b) 90

4000

80 “E T

i

70

x \ z 6 z :

0

‘;; .z rii 2

60

I”s

40

50

E 2

30

3000 A

2000

1000

20 IO

0 01

3

5

7

9

II

(l)(3)(4)(5)(6)(7)

15

47

(8)

(9)

‘:: I

(I)

3

5

(3)(4)(5)(6)(7)

7

9

II

15 (8)

80 70 1

60

g

50

(I)

(8)

(3)(4)(5)(6)(7) Distance

from outfalls (station number)

(9)

(km)

Figure 2. Number of species (a), abundance (b) and biomass (c) as a function of the distance from the Los Angeles County Sanitation Districts’ outfalls in 1980 (A), 1983 (0) and 1986 (W).

Fauna1 classification

There was a strong spatial fauna1gradient at the study site in 1980,1983 and 1986 (Figure 3). Fauna1 homogeneity within stations was consistently high relative to homogeneity among stations or years. Replicate samplesalmost always clustered together, and, with one exception [one replicate from station 6 in 1983 in the ‘ moderate degradation ’ cluster (defined below) which had an unusually high density of Tharyx sp. A], replicate grab samplesfrom the samestation and year were in the samemajor cluster. Descriptive labelswere assignedto six major clusters basedon the meansof the samples in each cluster on eight measuresof community structure (Table 3). Samplesfrom station 9 formed a cluster representing background conditions. ‘ Background ’ cluster samples were dominated by A. urtica, and had high Dominance and Infaunal Indices, high

47 (9)

Number (1) 1980 (2) 1983 (3) 1980

1 m’

rn?

of significant and 1983 and 1986 and 1986

Echinoderms/O,

Phoxocephalids/O,l

Amphipods/O.l

Index

Index

Dominance

Infaunal

g/O.1 m”

1 m’

Biomass,

Abundance/O,

differences

indicative

of improving 3/O O/3 o/o

16.4 36.0 19.2 371 320 357 6.5 14.3 6.3 1.03 7.57 0.88 4.5 52.8 3.6 0.0 9.4 1.6 0.0 0.0 0.0 0.00 0.20 0.40

1 29.2 40.7 43.8 295 292 298 9.9 17.7 13.5 4.70 9.92 9.73 18.4 59.9 52.6 2.4 4.3 4.2 0.0 0.0 0.0 0.20 0.33 0.00 A B B A B B

A B B

conditions/worsening 3/O o/o 3/O

A B A A B A

A B A

3 A A B A B B A B B A B” AB A B C

4/O

210

l/O -

between: -

nd 59 72 nd 1052 856 nd 43.6 31.4 nd 3.25 6.55 nd 51.9 53.3 nd 4.4 17.8 nd 2.6 6.6 nd 0.00 0.00

5

for five replicate

conditions 4/O

43.0 43.6 58.8 716 334 517 61.6 27.3 21.4 3.27 6.75 7.67 37.1 52.8 58.3 1.6 2.2 6.6 0.0 0.4 0.4 0.00 0.00 0.20

4

structure parameters. Data are mean values (experimentwise a = 0.05) between years

A B

6

312’ o/o 2/2”

100.0 72.8 87.4 4085 1655 1054 68.6 39.4 24.6 2.71 3.23 7.40 51.9 50.6 53.4 46.0 21.2 23.2 30.6 11.6 11.4 0.00 0.40 0.20

Station

0. l-m2 grabs.

A B B A B B

A B AB A B B A B B

Means

7

-

sometimes

when

A B A A B c A B B A B B A B c A B A A B c A A B

was within

occur

4/3b 5/l 511

74.4 61.8 83.2 1077 354 504 20.8 10.2 9.2 11.03 17.16 18.95 63.5 68.2 75.0 52.2 20.8 51.0 40.8 12.6 30.0 0.20 0.20 15.20

the difference

2/2

A B

A B

A B

A B

8

the same (or no) grouping

nd 71 89 nd 1286 921 nd 23.8 24.6 nd 4.08 9.00 nd 59.9 49.5 nd 31.4 29.6 nd 13.4 16.8 nd 0.40 0.80

with

“Counter-intuitive results (i.e. finding a significant difference for a smaller than a larger mean difference) heterogeneous and the Games and Howell method is used to make multiple comparisons. ‘Although there were statistically significant decreases in the densities of amphipods and phoxocephalids, variability at station 9. nd = no data.

m2

1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986

Species/O.1

m2

Year

Parameter

TABLE 2. Community significantly different

9

are not

the range

variances

of

are

74.6 69.8 62.0 518 489 398 14.4 11.5 16.1 13.07 A 14.98 A 8.07 B 81.0 A 79.6 AB 92.4 B 65.4 A 21.0 B 58.2 A 31.4 A 9.4 B 31.4 A 136.00 A 93.40 A 207.60 B

letter

Temporal changes in the benthos

393

2.22.01.8 I61.4 h tL z E -a 0

l-2 I.O0.8 O-60.40.2 -

Stotlon Yeor ClUSter

O-

i 1231133444 80 80 80 Mqor

degradation

66

83

133 86 Moderate

86

80

83

degradatwn

566678856 83 83E hlopr stlmulatlon

83

83

83

80

Moderate

86

86

stlmulatlon

78 66 66

339 ,a0 83

86,

BocKground

Figure 3. Numerical classification of replicate macrobenthic samples. Descriptive of major clusters are based on changes in community structure (see Table 3).

labels

abundance of amphipods and echinoderms, relatively low biomassand abundance, and intermediate species richness. Two clusters, with very similar community structure characteristics but with somewhat different species composition, were assigned the descriptive label ‘ moderate stimulation ’ (Table 3): in one cluster Tharyx sp. A was26.2”,, and P. tenuisculpta was 23,4O;, and in the other cluster P. tenuisculpta was 41.3”,, and Thuryx sp. A was 14.3OjAof the total abundance. Parvilucina tenuisculpta and Tharyx sp. A were 36.7O, and 29.2O,, respectively, of the total abundance in the ‘ major stimulation ’ cluster. The progression from ‘ background ’ to ‘ moderate stimulation ’ to ‘ major stimulation’ clusters was marked by increasing species richness, abundance and biomass, decreasing Dominance and Infaunal Indices and abundance of echinoderms, and the replacement of A. urtica with a P. tenuisculpta-Tharyx sp. A community. The change from ‘ major stimulation ’ to ‘ moderate degradation ’ to ‘ major degradation ’ clusters was marked by decreasesin speciesrichness, abundance, biomass, Infaunal Index, and the abundance of amphipods, and the replacement of a P. tenuisculpta-Tharyx sp. A community with a community dominated by Capitella spp. Abundance in both ‘ degradation ’ clusters and biomassin the ‘ major degradation ’ cluster was essentially the sameasin the ‘ background ’ cluster. Number of species, Dominance and Infaunal Indices, and the abundance of amphipods and echinoderms in both ‘ degradation’ clusters were substantially lessthan in the ‘ background ’ cluster. Temporal changesin macrobenthic community composition between 1980, 1983 and 1986 are indicated by changes in the location of stations among clusters (Figure 3). Stations 1,2 and 3 in 1980 and station 1 in 1986 formed the ‘ major degradation ’ cluster, while station 1 in 1983and station 3 in 1983and 1986 were in the ‘ moderate degradation ’ cluster. Fauna1composition at station 1in 1986was, therefore, more similar to that in 1980 than 1983, and fauna1 composition at station 3 in 1986 was more similar to that in 1983 than 1980. Fauna1composition shifted at station 5 between 1983and 1986from one typical

1980: 1,2,3 1986: 1

1980: 4 1983: 1,3,4,5 1986: 3,4

1980: 6

1980: 8 1983: 6,7,8

1986: 5,6,7,8

1980: 9 1983: 9 1986: 9

Moderate degradation

Major stimulation

Moderate stimulation

Moderate stimulation

Background

Year: stations

Major degradation

Cluster label

68.9

83.0

71.3

100.0

46.7

21.2

Species/ 0.1 rn?

TABLE 3. Structural

468

834

1046

4085

560

419

Abundance/ 0.1 m*

characteristics

14.0

22.5

21.8

68.6

29.9

8.6

Biomass, g/O.1 m*

12.06

10.48

9.30

2.71

6.52

1.87

Dominance Index

of the macrobenthos

clusters

84.3

57.8

61.8

51.9

51.3

7.3

Infaunal Index

in major

48.2

30.4

32.5

46.0

4.9

1.0

Amphipods/ 0.1 rn?

defined

classification

24.1

16.2

20.3

30.6

0.7

0.0

Phoxocephalids/ 0.1 mz

by numerical

3)

145.67

4.00

0.32

0.00

0.09

0.2

Echinoderms/ 0.1 m2

(Figure

Amphiodia urtica (30.30,,)

Parvilucinn tenuisculpta (41.30”)

Tharyx sp. A (26.2O,)

Parvilucina tenuisculpta (36.79,“)

Parvilucina tenuisculpta (35.3Ob)

Capitella spp. (82.0L’s,)

Dominant species (00 total abundance)

Temporal changes in the benthos

395

of ‘ moderate degradation ’ to one more typical of ‘ moderate stimulation ‘, and at station 6 between 1980 and 1983-86 from ‘ major stimulation ’ to ‘ moderate stimulation ‘. There were no major cluster changesamong years at stations 4,7,8 and 9. Sediment

contamination

Fifteen measuresof the surficial sediment contamination at stations 1 to 8 were either not statistically different or decreasedbetween 1980and 1983, while somemeasuresincreased and others decreased between 1983 and 1986 (Table 4). There were no significant increasesand 20 significant decreasesin sediment contamination at stations 1,3,4,6 and 8 between 1980and 1983 (seebottom of Table 4). Comparable results for 1983to 1986 were eight increasesand five decreases.Four of the eight increasesin contamination between 1983 and 1986 were at station 1, and four of the five decreasesin contamination were at station 4. The trend at all stations for the period 1980 to 1986 was towards reduced sediment contamination. There were 39 significant decreasesin sediment contamination at stations 1 to 8 between 1980 and 1986, and no significant increases(Table 4). The chemical classification dendrogram (Figure 4) wasstructurally similar to the fauna1 dendrogram (Figure 3). A strong spatial sediment contamination gradient is evident from the arrangement of clusters, from A containing the most contaminated samplesfrom stations 1, 2, 3 and 4 in 1980, stations 1, 3 and 4 in 1983 and station 1 in 1986, to D containing the least contaminated samplesfrom station 9 in 1980, 1983 and 1986. There was greater within-station heterogeneity in sediment contamination than fauna1composition, asindicated by the appearanceof several replicate samplesin different clusters (e.g. station 3, 1983 samplesin clusters A, B and C). Within-station heterogeneity reflected high variability in subsetsor all of the following: total volatile solids, total organic carbon, total oil and grease, hydrocarbon oil and grease, total sulphide, and the metals. Major temporal changesin overall sediment contamination are indicated by the complete separation of station replicate samplesinto different clusters depending on the year of collection. All replicate samples from stations 3, 4 and 6 in 1986 were placed in clusters representing lesscontaminated sediment conditions than in 1980.There wasno complete separation of station replicate samplesinto different clusters (A-D) for samplestaken in 1983 and 1986 (Figure 4). Sediment

toxicity

Mean survival of R. abronius was significantly less than that in Yaquina Bay control sediment only in samplesfrom stations 1,2 and 3 in 1980 and starion 6 in 1983 (Table 5). There was no significant difference from control survival in any of the 1986samples,and no evidence of increasing sediment toxicity between 1983 and 1986. Mean survival in the bioassayswith significant mortality was always above the 95:;) lower prediction limits for R. abronius survival in uncontaminated field sedimentswith the samesilt + clay fraction as the bioassay sediment [Dewitt et al., 1988, equation (5)]. The sediment toxicity observed in 1980 and 1983, therefore, could have been due to sediment contamination and/or sediment particle size effects. Summary

Overall, benthic conditions appeared to regressat station 1, remain constant at station 3, and improve at stations 4 to 8 between 1983and 1986. There wasa return to dominance of Capitella spp. and a reduction or exclusion of slightly and moderately pollution-tolerant speciesat station 1 between 1983and 1986(Table 1). In addition, station 1 in 1986 was in

organic

Total

BOD

oil/grease

5-day

Total

Hydrocarbon (mgkg ‘1

sulphide

oil/grease

(mg kg

(mg kg-‘)

(“,)

(“,,)

(mg kg

carbon

solids

(” ,,)

Total

silt + clay”

volatile

‘)

‘)

1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986

E, bv)

Total

Year

Parameter

44 3 17.5 12.1 12.1 5.3 4.4 5.4 84.9 92.1 89.4 2520 1838 1164 13800 3990 8170 20600 6860 13560 10800 6180 13290

-85

1

A B C A AB B A B C A B C A B A

A B B

TABLE 4. Geochemical characteristics basis. Means with the same (or no)

-29 132 229 15.0 11.4 8.4 4.9 4.0 3.2 92.8 94.3 91.0 2370 1349 439 10600 4540 5820 9950 5280 5190 7020 4500 4410

3

A AB B A B B A AB B

A AB B A AB B A AB B

of sediment. grouping letter

89 210 279 14.2 11.8 9.1 5.0 4.0 3.2 93.2 91.8 92.0 1310 1532 319 7160 3250 4510 6180 5060 3680 4920 4590 3210

4

AB A B A B B A AB B

A AB B A AB B

nd 138 356 nd 10.2 9.1 nd 3.2 3.3 nd 74.9 81.2 nd 1035 165 nd 2520 3460 nd 2210 2540 nd 1790 2190

5

A B

A B

A B

Station

219 114 215 15.2 10.6 10.1 4.3 4.2 4.1 76.0 63.9 69.1 443 572 113 4390 2100 3290 3620 1620 1790 2270 1290 1620

6

A AB B A B A A B B A AB B

A B B

nd 184 208 nd 9.4 8.6 nd 3.2 3.9 nd 72.0 80.3 nd 555 156 nd 1940 2100 nd 1410 2000 nd 1120 1730

7

A B

Data are mean values (n = 5 or 2”). Bulk sediment concentrations are not significantly different (experimentwise a = 0.05) between

9.5 6.9 5.2 3.2 1.9 2.8 81.4 83.2 84.3 121 157 101 1740 880 1140 1020 610 540 645 503 551

363 310 372

8

are expressed years

AB A B

A B B A B AB A AB B

4.0 6.6 2.4 1.8 1.9 0.8 62.0 73.1 56.8 24 226 10 660 680 540 338 516 215 144 291 248

321 251 317

on a dry

9

A AB B

A AB B

A AB B A AB B

weight

‘)

‘)

(pg kg

of sediment and 1983 and 1986 and 1986

4,4,-DDE

Number (1) 1980 (2) 1983 (3) 1980

(mg kg ‘)

Nickel

‘)

Bis(2-ethylhexyl) phthalate (pg kg

(mg kg-‘)

(mg kg

Copper

Chromium

Zinc (mg kg ‘)

‘)

(mg kg

Lead (mg kg

Cadmium

contamination

parameters

O/7 4/l O/9

32 26 23 338 193 143 853 873 701 821 664 416 691 328 258 95 76 68 19580 17670 50620 8640 9070 12520

significantly

A B B A AB B A A B A B B A B B AB B A

A AB B A AB B A AB B A AB B A AB B A B B

22 18 7.7 252 147 70 709 577 240 720 478 204 547 248 108 85 70 50 11080 11790 7980 12050 9750 6380

o/2 O/4 O/9

012 o/o o/12

increasing/decreasing

26 14 9.1 293 140 66 584 531 279 481 439 191 450 235 99 99 63 49 13540 10700 12040 9110 6450 6260 A AB B

A B B AB A B

A A B A AB B A A B

-

112

nd 6.6 5.3 nd 48 55 nd 222 184 nd 179 169 nd 87 86 nd 43 48 nd 3140 5980 nd 3390 5320

of sediment

between:

VI = 2 for bis(2-ethylhexyl) phthalate and 4,4’-DDE in 1980. “Significant changes in on silt + clay are not included in the number Table because it is not a measure of sediment contamination. nd=no data.

‘)

1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980 1983 1986 1980” 1983 1986 1980” 1983 1986

contamination

O/7 3/O O/7

A B B A B AB AB A B

A B c A B B

parameters

8.9 4.5 4.2 150 45 58 339 171 174 305 180 170 309 74 83 61 42 49 7880 2300 4730 2250 3620 5250 A B

A B

A B

A B

_

o/o o/o O/4

0.7 0.6 33 47 20 95 129 82 62 94 58 52 45 18 61 42 27 200 550 640 90 140 180

2.4

at the bottom

2.4 A 1.8 AB 1.2 B 57 31 32 130 107 115 101 152 117 96 51 42 26 29 34 1550 570 1420 1490 1360 1550

increasing/decreasing

3/l

nd 3.9 2.8 nd 50 57 nd 172 185 nd 229 210 nd 86 89 nd 40 46 nd 1910 4470 nd 3090 6230

of the

398

S. P. Ferraro et al.

the ‘ major degradation ’ cluster along with stations I,2 and 3 in 1980(Figure 3, Table 3) indicating a shift to more pollution-tolerant, opportunistic speciesat station 1 between 1983 and 1986. Further evidence of a regressionto more degraded conditions at station 1 between 1983 and 1986 was significant decreasesin speciesrichness and the Dominance and Infaunal Indices (Table 2) and significant increasesin 5-day sediment BOD, total oil and grease,hydrocarbon oil and grease,and DEHP (Table 4). Although fauna1conditions at station 1 in 1986 regressed to a state comparable to that in 1980 (Tables 1 and 2, Figure 2), most sediment contaminants at station 1 in 1986 did not return to 1980 levels (Table 4). Species composition (Table 1, Figure 3), community structure (Tables 2 and 3), and sediment contamination (Table 4, Figure 4) changed little, if at all, at station 3, while benthic conditions generally improved at stations 4 to 8 between 1983and 1986. Evidence for improving conditions at stations 4 to 8 between 1983and 1986 included: (1) decreasing abundance of many moderately pollution-tolerant speciesand increasing abundance of pollution-sensitive speciesbetween 1983 and 1986 (Table 1); (2) presence of pollutionsensitive speciesat stations closer to the outfalls in 1986; (3) less peaked SAB curves (Figure 2) and lessaltered community structure in 1986than 1983 (Table 2); (4) a shift in the fauna1composition at station 5 between 1983 and 1986 from one typical of ‘ moderate degradation ’ to one typical of ‘ moderate stimulation ’ (Figure 3, Table 3); and (5) significant decreasesin some sediment contaminants between 1983 and 1986, and a decreasing trend in sediment contamination between 1980 and 1986(Table 4). Discussion Distinguishing natural from pollution-related environmental changesis a major challenge in pollution ecology (McIntyre, 1977; Miller, 1984; Boesch et al., 1990). Three complications that may be encountered are time lags in responseto disturbances (pollution and natural) which may differ for different response parameters (Smith, 1974; Westman, 1978), the confounding of natural and pollution effects (Green, 1979), and high natural biological variability (e.g. Eagle, 1975; Buchanan et al., 1978; Nichols, 1985). Field studies to assesspollution impacts require observations at appropriate time and space intervals and of sufficient duration (Green, 1979; Gray, 1981; Stewart-Oaten et al., 1986; Walters et al., 1988). We believe the 3 years between field surveys in this study allowed sufficient time for many of the fauna1parameters measuredat 60 m water depth along the LACSD pollution gradient to improve in responseto decreasingpollutant loadings. Three years should have alsobeen sufficient time to seea deterioration in conditions if the unusual natural events of 1982-83 (i.e. the winter storms and/or El Niiio) had a temporary regenerative effect on the benthos. Other investigators have observed benthic responsesto altered sewageindustrial discharges occurring over time-scales of months to several years (Dean & Haskin, 1964; Smith, 1974; Greene, 1976a,b;Pearson& Rosenberg, 1978; Mearns, 1981). Stull et al: (19866) documented a dramatic reversal of the beneficial effects of the burrowing, respiratory and feeding activities of an echiuran, Listriolobus pelodes, on benthic community structure and sediment quality 2 years and longer after the echiuran’s population decline in our study area. The temporal sampling interval needed to detect differences in surficial sediment contamination and toxicity will depend upon the rates of the various processescontributing to the accumulation of sediments. Hendricks’ (1978) solids deposition and sediment flux

Temporal

changes

in the benthos

399

r

3.2 2.8 2.4 r =k 2.0 = E Y) 2 I 6 I.2 0.8

S+o+lo” ” Year Cluster

I2 i 80

80

3 80

II 86 83

3443463453 I3380 8383838086

n

Figure clusters

8686

5 83

83

5 86

676790 86 8693836380

B

88 9 83 86 ,86

9 83

C

4. Numerical classification are alphabetically coded.

of replicate

sediment

9 80,

0

chemistry

samples.

Major

5. Mean survival in Rhepoxynim abrouius IO-day test. Twenty amphipods were added to five replicate sediment samples from each station in each year. Means in italic are not significantly different from survival in Yaquina Bay, Oregon control sediment (P
TABLE

Station Year

1

2

3

4

5

6

7

8

9

Yaquina Bay control

1980 1983 1986

15.4 18.2 17.4

16.0 NT NT

16.0 17.2 18.2

184 19.2 16.6

NT 18.2 18.0

26.8 16.6” 15.8

NT 186 17.4

19.4 19.4 18.4

19.0 18.2 19.2

19.6 19.4 19.0

NT = not tested. =Incorrectly identified

as not significantly

different

from

control

in Swarrz

et al. (1986).

model includes four important processes occurring near the LACSD discharge: (1) deposition of natural and effluent particulates; (2) resuspension and transport of sediments; (3) redeposition of sediments; and (4) bioturbation. Hendricks (1984) suggested that ‘ the response time for sediments to changes in the [LACSD] effluent-related input should be fewer than 5 years ‘. Hendricks was, obviously, referring to changes near the LACSD outfalls since response times will be, in part, a function of the effluent particulates accumulation rate which varies with distance from the outfalls. Swartz et al. (1986) showed that surficial sediment contamination at station 1 reflected reductions in LACSD mass emissions of contaminants in the prior 3 years.

400

S.

P. Ferraro et al

Radiocarbon dating of sediments indicates a natural sediment accumulation rate of about 0.015 cm year-’ on the Pales Verdes Shelf (Emery, 1960). According to Hendricks (pers. comm.), however, more natural particulates accumulate near the LACSD outfalls possibly due to flocculation with effluent particles. Our best estimate of the natural+ effluent particulates accumulation rate at station 1 is 0.6 cm year-‘. This estimate is based on predictions of the deposition and flux of particulates to the bottom (units=g cmP2 year-‘) at station 1 using Hendricks’ (1978) model [calculations in LACSD (1981)] multiplied by Hendricks’ (1984) conversion factor of 2 cm3 g- * for the density (dry weight basis) of the surficial layer. Our estimates (as above) of the natural + effluent particulates accumulation rate are 0.2 cm year-’ at station 3, 0.1 cm year-’ at stations 4 and 5, and 0.06 cm year- ’ at stations 6 and 7. These may be slight overestimates since the model calculations are based on the mass emission of suspended solids from the LACSD discharge at the 1972 rate which was higher than that during 1980-86 (SCCWRP, 1989). The O-2 cm deep samples for sediment contamination and toxicity, therefore, probably represent about 3 years’ natural + effluent particulates accumulation at station 1 but >>3 years’ natural + effluent particulates accumulation at the outer stations. Virtually all of the benthic changes along the LACSD pollution gradient between 1980 and 1983 were consistent with the pattern of changes that would occur in response to reduced pollution (Swartz et al., 1986). Since the observed changes between 1980 and 1983 were in the same direction as expected when pollution is decreasing, it was not possible to separate the effects of natural phenomena from the wastewater effects. The net effect of natural phenomena was manifest in 1986 as fauna1 conditions regressed (Tables 1 and 2, Figures 2 and 3) and some chemical contaminants increased in the surficial sediments at station 1 (Table 4) even as LACSD wastewater pollutant loads continued to decrease. Supplemental biological data from 1985 (Ferraro & Cole, 1990) reinforces our finding of fauna1 regression over the period 1983 to 1986 at station 1. When the 1985 data are included in the time series for station 1 we find no community structure parameters significantly improved and three (abundance, Dominance Index, Infaunal Index) significantly worsened between 1983 and 1985 and one parameter (abundance) significantly improved and three (species richness, biomass, Infaunal Index) significantly worsened between 1985 and 1986. We think the fauna1 changes at station 1 between 1983 and 1986 represent a regression to a more polluted state following the cleansing action of natural events (probably primarily the winter storms) in 1982-83. Our reasoning is schematically illustrated by Path I in Figure 5. Following a significant natural cleansing event benthic conditions improve to an unsustainable level (IA in Figure 5) then subsequently tend to regress to a state more nearly approximating that sustainable under the prevailing pollution conditions (IB in Figure 5). When wastewater pollutant loads are monotonically increasing or decreasing, one can tentatively conclude that the effects of natural phenomena were 2 wastewater effects at the discharge’s mass emissions rate for the period when significant changes are in the opposite direction from that expected due to pollution. The impact of a natural phenomenon, even a widespread phenomenon such as a storm, may not be the same over the entire wastefield; consequently, the response paths may differ at different locations in the wastefield. A natural degrading event is illustrated by Path II in Figure 5 (see figure caption for explanation). The Figure 5 schemata are simplifications. One still has to contend with some or all of the complications mentioned earlier (time lags in responses, confounding effects, etc.). This, we believe, is best accomplished by a comprehensive, well planned field study which brackets important natural events and in which the sampling

Temporal

changes

401

in the benthos

La

,,’

IA

,’ .’

EE

-.

,’

.’

.’

.’

.’

.’

,:

:

,’

I’

.’

-.

‘.

-.

-.

*.

-.

-.

,*’

I6 -. *.

-.

-.

*.

‘.

*.

-. “‘0

:’

fl ,,,,,,,,,,..............,....,....,,,,,...........

*.

-..

,’

-.

.

..~........

-. **.. ‘.

*.

-.

UA

=-.. -.

*.

-.

*.

*-

-.

.-

.’

*-

.-

. . .. . .. . . . .. . . . . . . . . *.o *-’ e**-.* .UC *- .-

‘.DL’_______ ----__

t rI6 I

2

----___

-----____ 3

Time

Figure 5. Schematic illustration of a response to a natural perturbation (indicated by arrow) when pollution conditions are directional (monotonically increasing or decreasing). Solid line represents parameter X’s expected response to wastewater effects in the absence of the natural perturbation. Path I. The natural perturbation is a cleansing event. Observed response IA is in the same direction as the expected response to wastewater effects. Without a priori knowledge of the kind and magnitude of change associated with each, one can not separate the effects of natural phenomena from the wastewater effects based on observations at time 1 and 2. The net effect of natural phenomena (natural perturbation+possibly other natural phenomena) is manifest as response IB which is in the opposite direction from the expected wastewater response. The tentative conclusion is that the net effect of the natural phenomena is greater than or equal to the time 3 minus time 2 wastewater effects at the discharge mass emission rate between time 2 and 3. Path II. The natural perturbation is a degrading event. Observed response IIA is in the opposite direction from the expected wastewater response. One can tentatively conclude that the net effect of natural phenomena is greater than or equal to wastewater effects from the onset of the natural perturbation to time 2 at the discharge mass emission rate during that time period. One can further tentatively conclude that the net effect of natural phenomena was greater than or equal to the time 3 minus time 2 wastewater effects at the discharge mass emission rate between time 2 and 3 if parameter X continues to move in the opposite direction from the expected wastewater effects (IIB) but not if parameter X moves in the same direction as the expected wastewater effects (IIC).

intervals are chosen to coincide as closely as possible with the probable timing of significant changes in geochemical and ecological conditions in response to those events. Whatever the cause(s), the observed changes at station 1 between 1983 and 1986 were opposite predictions for recovery in an environment of decreasing wastewater pollutant loads. We therefore tentatively conclude that the net effect of natural phenomena at station 1 was 2 the effect of 3 years of LACSD wastewater effects at the LACSD 1983-86 mass emission rate (Table 6). Benthic conditions were essentially unchanged at station 3 and continued to improve at stations 4 to 8 between 1983 and 1986 (Tables 1,2,4, Figures 2 and 3). The relative magnitude of the effects of natural phenomena and wastewater effects is much more difficult or impossible to estimate when observed changes follow expectations of prevailing pollution conditions. But if we assume that the observed changes at

S. P. Ferraro et al.

402

TABLE 6. Changes in the macrobenthos and estimates of the net effect phenomena at stations 1,3 and 4-8 between 1983 and 1986

of natural

Station 1 Benthic

change

Natural

phenomena

3

4-8

Degraded

Constant

Improved

2 effect of 3 years’ LACSD wastewater effects at the 1983-86 mass emission rate

g effect of 3 years’ LACSD wastewater effects at the 1983-86 mass emission rate

-c effect of 3 years’ LACSD wastewater effects at the 1983-86 mass emission rate

station 1 were primarily causedby widespread natural phenomena, such as the 1982-83 winter storms, affecting all the stations (though not necessarily equally, since storm surge effects on the bottom may differ due to the different physical characteristics of the sediments), then the constant conditions at station 3 would suggestthat the net effect of the natural phenomena was g 3 years of LACSD wastewater effects at the LACSD 1983-86 massemissionrate, and the continued recovery at stations 4 to 8 would suggestthat the net effect of the natural phenomena was <3 years of LACSD wastewater effects at the LACSD 1983-86 massemissionrate (Table 6). Estimates of the relative effect of natural phenomena and wastewater effects can be made for individual population or community parameters, or for multiple parameters indicative of ecosystem responses(as in Table 6). Responsesto stressat higher levels of biological organization are generally more conservative (Pearson 81Rosenberg, 1978), and, therefore, they should provide a more reliable assessmentof relative effects. An alternative way of interpreting the results in Table 6 is that the reduction in LACSD mass emissionsresulted in improved benthic conditions 5-15 km from the discharge but effects of natural phenomena obscured detection of changesoccurring in response to reduced pollution closer to the discharge between 1983and 1986. We choseto return to the study area in 1986 becausewe thought the time series(1980, 1983, 1986) would be favourable for discriminating the effects of natural phenomena from LACSD wastewater effects. Natural events had occurred in 1982-83 which had substantial, widespread ecological impacts. The El Nifio of 1982-83 was‘ the strongest warming of the equatorial Pacific in this century ’ (Kerr, 1983, p. 940), and the force and duration of the 1982-83 storms were unprecedented (Seymour et al., 1984,1989; Dayton et al., 1989). The 1982-83 storms devastated kelp communities (Dayton & Tegner, 1984; Ebeling et al., 1985) and somemacroalgaepopulations (Gunnill, 1985) in shallow waters (G 18 m) off the southern California coast. Although the studies cited above and our data strongly suggestthey were important, we can not definitely attribute the natural effects in this study solely to the 1982-83 storms and/or El Nitio. There were severe storms in southern California in the winter of 1985-86 (Seymour et al., 1989; Dayton et al., 1989), and there may have been other important natural events that we are unaware of. Due to the multiplicity of possiblenatural factors and time lagsin responses,it will often be difficult, if not impossible, in a varying environment to irrefutably link specific natural causeswith their effects. As a practical matter, however, pollution ecologistsare usually lessinterested in identifying the effects of a specific natural perturbation than being able to discriminate the net effect of natural phenomena from source pollution effects.

Temporal

changes

in the benthos

403

The net effect of natural phenomena on the benthos appeared to be inversely related to the distance from the outfalls in this study (Table 6). This finding, if common, could have important sampling design implications. Obviously, it is best to sample at locations where pollution effects are high and natural effects are low when seeking to detect temporal changes in response to pollution. One might expect the greatest effect of increases or decreases in pollution from a point source to occur near the source. But if the effect of natural phenomena is also greatest near the source, then sampling at some other location(s) may be more desirable. High natural temporal benthic variability may be related to the type of substrate present near large sewage discharges (discussed below). There were some significant increases in surficial sediment contamination between 1983 and 1986 (Table 4). Most (three of four) of the increases at station 1 were in the concentration of the more labile contaminants (s-day BOD, total oil and grease, hydrocarbon oil and grease). Bottom currents and storm surges are capable of resuspending and transporting sediments (Hendricks, 1976), and the redeposited sediments will tend to dilute sediment contamination near the outfalls (Hendricks, 1984; SCCWRP, 19876). Resuspension also oxygenates sediments, promoting the decay of sediment-associated labile contaminants (Myers, 1974; Hendricks, 1984; Bauer & Capone, 1985; Warns, 1987). Sediment contaminant dilution and decay due to natural physical disturbances such as storms are likely to be greatest near the LACSD outfalls where sediments containing highly flocculent, organically enriched material from the LACSD discharge are more susceptible to resuspension (Hendricks, 1976). Renewed effluent particulates accumulation (about 0.6 cm year ’ at station 1) following a cleansing event could account for the increases in surficial sediment contamination at station 1 between 1983 and 1986. There were some increases in surficial sediment contamination at the outer stations (5 to 8) between 1983 and 1986 (Table 4). Our surficial sediment samples, with the exception of those from station 1, probably represented + 3 years of natural + effluent particulates accumulation (see estimated accumulation rates above), and they were, therefore, better suited for detecting long-term trends than for testing short-term temporal variability in sediment contamination and toxicity. Stull et al. (1986~) suggested that storm surges may have a winnowing effect on surficial sediments which could result in the exposure of more contaminated deeper sediment. Some of the increase in surficial sediment contamination could be due to long-shore transport (Hendricks, 1978) of more contaminated sediments from near the outfalls to the outer stations. It is unlikely that the increases in surficial sediment contamination at the outer stations between 1983 and 1986 were primarily due to LACSD 1983-86 wastewater effects since the natural + effluent particulates accumulation rates (of which direct effluent particulates deposition is only a part) are too low at the outer stations to account for the increases. The dramatic changes in macrobenthic community composition and structure at station 1 between 1983 and 1986 (Tables 1 and 2, Figure 2) were coincident with significant increases in only four of the 15 sediment contaminants measured (Table 4). The significant increases in surficial sediment contamination at station 1 between 1983 and 1986 may be explained by the settling of LACSD effluent particulates following the cleansing action (by the resuspension and oxygenation of sediments) of the 1982-83 storms. Following a cleansing event, contaminated LACSD effluent particulates would again accumulate on the bottom, sediments would become less oxic (reducing the rate of decay of labile contaminants), and the macrobenthos would tend to revert towards former conditions. The Listridobtis invasion on the Palos Verdes Shelf in the mid-1970s was a natural cleansing event which temporarily overshadowed the LACSD wastewater effects

404

S. P. Ferraro et al.

on the benthos (Stull et al., 1986b).Listriolobuspelodes wasfairly abundant at afew stations in 1980, but its low density in 1983and 1986 (Table 1) precludes it asa major causeof the changesobserved between 1983and 1986.More generally, our results and those of Stull et al. (1986b) suggestthat the oxygenation of sedimentsand reductions in the concentrations of relatively few labile contaminants can have a remarkable rejuvenating effect on polluted benthic communities. Sediment toxicity, asmeasuredby the R. abronius lo-day test, didnot help discriminate the effects of natural phenomena from LACSD wastewater effects in this study. Even when the toxicity test results were positive, R. abronius mortality was not so great as to allow a clear distinction between contamination and sediment particle size effects. It is not clear why the highly contaminated sediments from near the LACSD outfalls were not more toxic to R. abronius especially since field distributions of amphipods and phoxocephalids were sensitive indicators of pollution (Table 2). Acute laboratory toxicity tests will, generally, have only a limited ability to accurately and reliably predict complex ecological events (Buikema et al., 1982; Swartz, 1989). The purpose of acute toxicity tests is primarily to provide information on the bioavailability of contaminants and their potential for biological effects (Chapman & Long, 1983). The bioavailability of sedimentassociatedcontaminants may be a function of the concentration of organic carbon (Adams et al., 1985; Swartz et al., 1985c), acid-volatile sulphide (Di Toro et al., 1990), or possibly other constituents in sediments. Furthermore, the contaminants present may not be toxic to the test organism. Despite their limitations, sediment toxicity tests often provide insights into the effects of contaminated sediments especially when their results are considered together with information on sediment chemistry and field ecology (Long & Chapman, 1985; Long, 1989; Swartz, 1989; Chapman et al., 1991). Natural events may catalyse regenerative as well as degenerative processes(Ebeling et al., 1985) leading to an over- or underestimation of pollution effects in short-term studies. It is therefore very important to consider the duration of a sampling programme when seekingto assesspollution impacts. In this study we observed temporal changesin the benthos which were logically attributable to natural phenomena, and we tentatively concluded that the net effect of natural phenomenamay sometimesbe asgreat as3 years or more of LACSD wastewater effects. One should, therefore, be cautious about ascribing changesoccurring over similar or shorter intervals to LACSD wastewater effects (alsosee Stull et aZ., 19866,c). In general, long-term studies (2 6 years) are probably needed to reliably discriminate the effects of moderate, incremental changesin the massemissionsof sewage-industrial dischargesfrom the effects of natural phenomena.

Acknowledgements

We gratefully acknowledge the assistanceof K. Sercu, J. Lamberson and the crews of the R/V See S Dee and the R/V Marine Surveyor (fieldwork), W. DeBen (taxonomy), and A. Robinson, L. Hoselton, and M. Kammerzell (laboratory assistants). We thank B. Melzian, W. Nelson and two anonymous reviewers for their comments on an earlier draft of the manuscript. Mention of trade names or commercial products does not constitute endorsement or recommendation for use. Contribution number N-143 of the U.S. Environmental Protection Agency, Environmental Research Laboratory, Narragansett, RI.

Temporal

changes

in the benthos

405

References Adams, W. J., Kimerle, R. A. & Mosher, R. G. 1985 Aquatic safety assessment of chemicals sorbed to sediments. In Aquatic Toxicology and Hazard Assessment: Seventh Symposium, ASTM STP 854 (Cardwell, R. D., Purdy, R. & Bahner, R. C., eds). American Society for Testing Materials, Philadelphia, Pennsylvania, pp. 429453. Bascom, W. 1978 Life in the bottom. Southern California Coastal Water Research Project, Annual Report 3978, pp. 57-80. Bascom, W., Mearns, A. J. & Word, J. Q. 1978 Establishing boundaries between normal, changed, and degraded areas. Southern California Coastal Water Research Project, Annual Report 1978, pp. 81-94. Bauer, J. E. & Capone, D. G. 1985 Degradation and mineralization of the polycyclic aromatic hydrocarbons anthracene and naphthalene in intertidal marine sediments. Applied Environmental Microbiology 50, 81-90. Boesch, D. F. 1977 Application of numerical classification in ecological investigations of water pollution. Ecological Research Series 600/3-77-033, U. S. Environmental Protection Agency, Washington, D.C., pp. i-l 15. Boesch, D. F., Schubel, J. R., Bernstein, B. B., Eichbaum, W. M., Garber, W., Hirsch, A., Holland, A. F., Johnson, K. S., O’Connor, D. J., Speer, L. & Wiersma, G. B. 1990 Managing Troubled Waters. The Role of Marine Environmental Monitoring. National Academy Press, Washington, D. C., 125 pp. Buchanan, J. B. 1984 Sediment analysis. In Methodsfor the Study of Marine Benthos, 2nd edn (Holme, N. A. & McIntyre, A. A., eds). IBP Handbook No. 16, Blackwell Scientific Publications, Oxford, pp. 41-65. Buchanan, J. B., Sheader, M. &Kingston, P. F. 1978 Sources of variability in the benthic macrofauna off the South Northumberland coast, 1971-1976. Journal of the Marine Biological Association of the United Kingdom

S&191-209.

Buikema, A. L. Jr, Niederlehner, B. R. & Cairns, J. Jr 1982 Biological monitoring. Part IV-Toxicity testing. Water Research 16,239-262. Chapman, l’. M. & Long, E. R. 1983 The use of bioassays as part of a comprehensive approach to marine pollution assessment. Marine Pollution Bulletin 14,81X34. Chapman, I’. M., Long, E. R., Swartz, R. C., Dewitt, T . H. & Pastorok, R. 1991 Sediment toxicity tests, sediment chemistry and benthic ecology do provide new insights into the significance and management of contaminated sediments-a reply to Robert Spies. Environmental Toxicology and Chemiszry lO, l-4. Clark, R. B. 1989 Marine Pollution, 2nd edn. Clarendon Press, Oxford, 220 pp. Dayton, P. K. & Tegner, M. J. 1984 Catastrophic storms, El Nitio, and patch stability in a southern California kelp community. Science 224,283-285. Dayton, I’. K., Seymour, R. J., Parnell, P. E. & Tegner, M. J. 1989 Unusual marine erosion in San Diego County from a single storm. Estuarine, Coastal and Shelf Science 29, 151-160. Dean, D. & Haskin, H. H. 1964 Benthic repopulation of the Raritan River Estuary following pollution abatement. Limnology and Oceanography 9,551-563. Dewitt, T. H., Ditsworth, G. R. & Swartz, R. C. 1988 Effects of natural sediment features on survival of the phoxocephalid amphipod, Rhepoxynius abronius. Marme Environmental Research 25,99-124. Di Toro, D. M., Mahony, J. D., Hansen, D. J., Scott, K. J., Hicks, M. B., Mayr, S. M. & Redmond, M. S. 1990 Toxicity of cadmium in sediments: the role of acid volatile sulfide. Environmenral Toxicology and Chemistry 9, 1487-1502. Eagle, R. A. 1975 Natural fluctuations in a soft bottom benthic community. Journal of the Marine Biological Association

of the United

Kingdom

55,865-878.

Ebeling, A. W., Laur, D. R. & Rowley, R. J. 1985 Severe storm disturbances and reversal of community structure in a southern California kelp forest. Marine Biology 84,287-294. Emery, K. 0. 1960 The Sea off Southern California. John Wiley & Sons, New York, 366 pp. Ellis, D. V. & Cross, S. F. 1981 A protocol for inter-laboratory calibrations of biological species identifications (ring tests). Water Research 15,1107-l 108. Ferraro, S. P. & Cole, F. A. 1990 Taxonomic level and sample size sufficient for assessing pollution impacts on the Southern California Bight macrobenthos. Marine Ecology Progress Series 67,25 l-262. Gray, J. S. 1981 The Ecology of Marine Sediments. An Introduction to the Structure and Function of Benthic Communities. Cambridge University Press, Cambridge, 185 pp. Green, R. H. 1979 Sampling Design and Statistical Methodsfor Environmental Biologists. John Wiley & Sons, New York, 257 pp. Greene, C. S. 1976a Response and recovery of the benthos at Orange County. Southern California Coastal Water Research Project, Annual Report 1976, pp. 197-203. Greene, C. S. 19766 Partial recovery of the benthos at Palos Verdes. Southern California Coastal Water Research Project, Annual Report 1976, pp. 205-210. Gunnill, F. C. 1985 Population fluctuations of seven macroalgae in southern California during 1981-1983 including effects of severe storms and an El Nitio.Journalof Experimental Marine Biology and Ecology 8.5, 149-164.

406

et al.

S. P. Ferraro

Hendricks, Research

Hendricks, Water

Hendricks,

T.

1976 Current Project,

velocities

Annual

Report

T. 1978 Forecasting Research

Project,

changes

Annual

Report

Biennial

Report

sediment

to move

sediments.

Southern

Calafornia

Coastal

Water

pp. 71-76.

in sediments 1976,

pp.

near wastewater

outfalls.

Southern

California

Coastal

127-143.

quality around outfalls. Southern California Coastal Water Research 127-140. Kerr, R. A. 1983 Fading El Nirio broadening scientist’s view. Science 221,940-941. Lance, G. N. & Williams, W. T. 1966 A generalized sorting strategy for computer classifications. Nature 212,218. Long, E. R. 1989 The use of the sediment quality triad in classification of sediment contamination. Contaminated Marine Sediments-Assessment and Remediation. National Academy Press, Washington, D.C., pp. 78-99. Long, E. R. & Chapman, I’. M. 1985 A sediment quality triad: measures of sediment contamination, toxicity and infaunal community composition in Puget Sound. Marine Pollution Bulletin 16,405-415. Los Angeles County Sanitation Districts (LACSD) 1981 Ocean Monitoring and Research Annual Report 1980-81. Los Angeles County Sanitation Districts, Whittier, California, 384 pp. + Appendix. McIntyre, A. D. 1977 Effects of pollution on inshore benthos. In Ecology of Marine Benthos (Coull, B. C., ed.). University of South Carolina Press, Columbia, South Carolina, pp. 301-318. Mearns, A. J. 1981 Effects of municipal discharges on open coastal ecosystems. In Marine Environmental Pollution, 2. Dumping and Mining (Geyer, R. A., ed.). Elsevier Scientific Publishing Company, Amsterdam, pp. 25-66. Mearns, A. J. & Word, J. Q. 1982 Forecasting effects of sewage solids on marine benthic communities. In Ecological Stress and the New York Bight: Science and Management (Mayer, G. F., ed.). Estuarine Research Federation, Columbia, South Carolina, pp. 495-512. Miller, D. R. 1984 Distinguishing ecotoxic effects. In Effects of Pollutants az the Ecosystem Level (Sheehan, P. J., Miller, D. R., Butler, G. C. & Bourdeau, Ph., eds). Scientific Committee on Problems of the Environment, John Wiley & Sons, Chichester, United Kingdom, pp. 15-22. Myers, E. P. 1974 The concentration and isotopic composition of carbon in marine sediments affected by a sewage discharge. Ph.D. dissertation, California Institute of Technology, Pasadena, California, 179 pp. National Research Council 1990 Monitoritzg Southern Calzfornia’s Coastal Waters. National Academy Press. Washington, D.C., 154 pp. Nichols, F. H. 1985 Abundance fluctuations among benthic invertebrates in two Pacific estuaries. Estuaries 8, 136-144. Pearson, T. H. & Rosenberg, R. 1978 Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology Annual Review 16,228-311. Schafer, H. A. 1978 Characteristics of municipal wastewater discharges, 1977. Sourhern California Coastal Water Research Project, Annual Report 1978, pp. 97-101. Schafer, H. A. 1982 Characteristics of municipal wastewaters. Southern California Coastal Water Research Project, Biennial Report 1981-82, pp. 11-15. Schafer, H. A. 1984 Characteristics of municipal wastewater. Southern Calzfornia Coastal Water Research Project, Biennial Report 1983-84, pp. 11-19. Seymour, R. J., Strange, R. R. III, Cayan, D. R. &Nathan, R. A. 1984 Influence of El Nines on California’s wave climate. In Nineteenth Coastal Engineering Conference, Proceedings of the International Conference, September 3-7, 1984, Houston, Texas (Edge, B. L., ed.). American Society of Civil Engineers, New York, pp. 577-592. Seymour, R. J., Tegner, M. J., Dayton, P. K. & Parnell, P. E. 1989 Storm wave induced mortality of giant kelp, Macrocystispyrifera, in southern California. Estuarine, Coastal and Shelf Science 28,277-292. Smith, G. B. 1974 Some effects of sewage discharge to the marine environment. Ph.D. dissertation, University of California, San Diego, 334 pp. Sokal, R. R. & Rohlf, F. J. 1981 Biometry, 2nd edn. W. H. Freeman and Co., San Francisco, 859 pp. Southern California Coastal Water Research Project (SCCWRP) 1987~ Characteristics of municipal wastewater in 1986 and 1987. Southern California Coastal Water Research Project, Annual Report 1987, pp. 5-12. Southern California Coastal Water Research Project (SCCWRP) 19876 Seasonal and spatial variations m sediment resuspension. Southern California Coastal Water Research Project, Annual Report 1987, pp. 35-39. Southern California Coastal Water Research Project (SCCWRP) 1989 Recent changes and long term trends in the combined mass emissions discharged into the Southern California Bight. Southern California Coastal Water Research Project, Annual Report 1988-89, pp. 20-28. Steel, R. G. D. & Torrie, J. H. 1960 Principles and Procedures in Statistics. McGraw-Hill, New York, 48 1 pp. Stewart-Oaten, A., Murdoch, W. W. &Parker, K. R. 1986 Environmental impact assessment: ‘ pseudoreplication ’ in time? Ecolog-v 67,929-940. Project,

T. 1984 Predicting

required

1976,

1983-84,

pp.

Temporal

Stull,

changes

in the benthos

407

J. K. 1988 Long-term trends among benthic biota. InJoinr Water l’ollurion Control Plant 1988 Revised Applicarion for Modification of Secondary Treatment Requirements for Discharges into Marine Waters, Vol. II, Appendix F-4. Los Angeles County Sanitation Districts, Whittier, California. Stull, J. K., Baird, R. B. &Heesen, T. C. 1986a Marine sediment core profiles oftrace constituents offshore of a deep wastewater outfall. Journal of the Water Pollution Conrrol Federation .58,985-99 1. Stull, J. K., Haydock, C. I. & Montagne, D. E. 19866 Effects of Listriolobuspelodes (Echiura) on coastal shelf benthic communities and sediments modified by a major California wastewater discharge. Estuarine, Coastal and Shelf Science 22,1-17. Stull, J. K., Haydock, C. I., Smith, R. W. & Montagne, D. E. 1986~ Long-term changes in the benthic community on the coastal shelf of Palos Verdes, Southern California. Marine Biology 91,539-551. Swartz, R. C. 1989 Marine sediment toxicity tests. In Contaminated Marine Sediments-Assessmenr and Remediation. National Academy Press, Washington, D.C., pp. 115-129. Swartz, R. C., Schults, D. W., Ditsworth, G. R., DeBen, W. A. & Cole, F. A. 1985a Sediment toxicity, contamination, and macrobenthic communities near a large sewage outfall. In Validation and Predictability of Laboratory Methods for Assessing rhe Fate and Effects of Contaminants in Aquatic Ecosystems, ASTM STP 865 (Boyle, T. I’., ed.). American Society for Testing and Materials, Philadelphia, pp. 152-175. Swartz, R. C., DeBen, W. A., Jones, J. K. I’., Lamberson, J. 0. &Cole, F. A. 19856 Phoxocephalid amphipod bioassay for marine sediment toxicity. In Aquatic Toxicity and Hazard Assessmenr: Seventh Symposium, ASTM STP854 (Cardwell, R. D., Purdy, R. & Bahner, R. C., eds). American Society for Testing and Materials, Philadelphia, pp. 284-307. Swartz, R. C., Ditsworth, G. R., Schults, D. W. & Lamberson, J. 0. 1985~ Sediment toxicity to a marine infaunal amphipod: cadmium and its interaction with sewage sludge. Marine Environmental Research 18, 133-153. Swartz, R. C., Cole, F. A., Schults, D. W. & DeBen, W. A. 1986 Ecological changes in the Southern California Bight near a large sewage outfall: benthic conditions in 1980 and 1983. Marine Ecology Progress Series 31, 1-13. Tetra Tech. 1981 Technical evaluation of County Sanitation Districrs of Los Angeles County Joint Water Pollution Control Plant Section 301 (h) application for modification of secondary treatment requiremenrsfor discharge into marine wafers. Draft Report, March 2, 1981, 639 pp. (Available from Tetra Tech, Inc., 11820 Northup Way, Suite 100, Bellevue, WA 98005). Walters, C. J., Collie, J. S. & Webb, T. 1988 Experimental designs for estimating transient responses to management disturbances. CanadianJournal of Fisheries and Aquatic Sciences 45,530-538. Warns, T. J. 1987 Diethylhexylphthalate as an environmental contaminant-a review. Science of the Total Environment 66,1-16. Westman, W. E. 1978 Measuring the inertia and resilience of ecosystems. Bioscience 28,705-710. Word, J. Q. 1978 The infaunal trophic index. Southern California Coastal Waler Research Project, Annual Report 1978, pp. 19-39. Word, J. Q. 1980 Classification of benthic invertebrates into infaunal trophic index feeding groups. Southern California Coastal Water Research Project, Biennial Report 197%0, pp. 103-121. Word, J. Q. & Mearns, A. J. 1978 The 60-meter control survey. Southern California Coastal Water Research Projecr, Annual Report 1978, pp. 41-56.