... Intertidal Fish: A. Field Study, Transactions of the American Fisheries Society, 124:4, 461-476, DOI: ... TRANSACTIONS. OF THE ..... techniques after the Exxon Valdez oil spill, but the records did not ..... nical Service 3, Anchorage. Fletcher ...
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Effect of the Exxon Valdez Oil Spill on Intertidal Fish: A Field Study a
b
Willard E. Barber , Lyman L. McDonald , Wallace P. b
Erickson & Mark Vallarino
c
a
School of Fisheries and Ocean Sciences , University of Alaska , Fairbanks, Alaska, 99775, USA b
Western Ecosystems Technology , 2003 Central, Cheyenne, Wyoming, 82001, USA c
School of Fisheries and Ocean Sciences, University of Alaska , USA Published online: 09 Jan 2011.
To cite this article: Willard E. Barber , Lyman L. McDonald , Wallace P. Erickson & Mark Vallarino (1995) Effect of the Exxon Valdez Oil Spill on Intertidal Fish: A Field Study, Transactions of the American Fisheries Society, 124:4, 461-476, DOI: 10.1577/1548-8659(1995)1242.3.CO;2 To link to this article: http:// dx.doi.org/10.1577/1548-8659(1995)1242.3.CO;2
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TRANSACTIONS
OF
THE
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Volume 124
AMERICAN
FISHERIES
July 1995
SOCIETY
Number 4
Transactions of the American Fisheries Society 124:461-476, 1995 © Copyright by the American Fisheries Society 1995
Effect of the Exxon Valdez Oil Spill on Intertidal Fish: A Field Study WILLARD E. BARBER School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Alaska 99775, USA
LYMAN L. MCDONALD AND WALLACE P. ERICKSON Western Ecosystems Technology 2003 Central, Cheyenne, Wyoming 82001, USA
MARK VALLARINO School of Fisheries and Ocean Sciences, University of Alaska Abstract.—The purpose of this study was to evaluate the impact of the March 1989 Exxon Valdez oil spill and subsequent cleanup activities on density, biomass, and species diversity of intertidal fishes in Prince William Sound, Alaska. Intertidal fish were sampled in a quasi-experimental, matched-pairs (oiled-cleaned versus reference sites) design stratified by three habitat types with random selection of oiled-cleaned (O-C) sites. Site pairs were sampled twice in 1990 and in 1991. Of 21 fish taxa, 5 made up 98% and 1 made up 74% of total abundance. There were no significant differences in species diversity between reference and O-C sites. Density, however, was significantly greater at reference sites for all habitats combined for both visits in 1990. In contrast, density in 1991 was about equal at reference and O-C sites. Total biomass for all habitats combined was greater at reference than O-C sites during both visits in 1990, but differences were not statistically significant. In 1991, however, the total biomass at reference and O-C sites was about equal. Forward stepwise multiple logistic regression models indicated that presence of oil was a significant predictor of reduced density at mid-intertidal levels in 1990 but not in 1991. From the general pattern of lower density and biomass on O-C sites in 1990 followed by no significant differences in 1991 and corroborating evidence of multiple-regression modeling, we conclude that the presence of oil and subsequent cleanup activities had a negative impact on intertidal fishes in 1990 and that there was evidence that recovery was underway in 1991. On 24 March 1989, the tanker Exxon Valdez struck Bligh Reef and spilled about 46 million liters of crude oil into Prince William Sound, Alaska. This was the largest oil spill recorded in U.S. waters. By the end of August 1989, oil contaminated about 450 km of shoreline throughout western Prince William Sound, 270 km in Cook Inlet and 122 km in the Alaska Peninsula (EVOS-
DAGG 1991). Major beach cleanup activities began in May 1989 and continued throughout the summer into fall with additional cleanup in 1990 (Houghton et al. 1991). In large oil spills that occur near shore, intertidal and shallow subtidal organisms are immediately subjected to the effects of oil. Johannes (1975) and Southward (1982) reviewed the biological conse-
461
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BARBER ET AL.
quences of oil spills on invertebrates; they pointed out the congruity between experimental and field data which show invertebrate populations are negatively affected and slow to recover. Laboratory experiments of the effect of oil on fishes demonstrate histopathological changes (Khan and Kiceniuk 1984), decreased growth and reproduction (Kiceniuk and Khan 1987), changes in blood chemistry (Payne et al. 1978), morphological changes of organs (Payne et al. 1978; Kiceniuk et al. 1980; Fletcher et al. 1982), and decreased swimming activity (Berge et al. 1983). A few studies have also demonstrated these effects under field conditions. For example, after the Amoco Cadiz oil spill in 1978, Stott et al. (1983) found histopathological changes in the ovaries of the subtidal plaice Pleuronectes platessa, and Haensly et al. (1982) found hypertrophy of gill mucous cells and gastric gland degeneration in the same species. However, definitive information on the population-level effects of oil on subtidal fishes under marine field conditions is lacking (Malins and Hodgins 1981). Although Chasse (1978) observed oil spill mortality in littoral fishes of the families Ammodytidae, Labridae, and Sygnathidae, no field study has quantified a decline in density or biomass. There are also no published field studies of the effects of oil on intertidal fishes (e.g., Patten 1977; Malins and Hodgins 1981). However, information based on subtidal fishes (Patten 1977; Smith and Cameron 1979; Khan and Kiceniuk 1984; Kiceniuk and Khan 1987) suggests that intertidal fishes exposed to oil may suffer reduced growth, reproduction, and survival and increased incidences of physical abnormalities, all of which would contribute to reducing density. The influence of oil spill cleanup activities on fishes is even less well known than the influence of oil spills. The only published information (Houghton et al. 1991) indicates the effect can be substantial; samples of the lower intertidal zone of Prince William Sound before and after hot water wash cleanup of oiled beaches revealed that the saddleback gunnel Pholis ornata occurred in sample plots before but not after cleanup. In this study we examined the compound effect of the Exxon Valdez oil spill and subsequent cleanup activities on the density and biomass of intertidal fishes in Prince William Sound, Alaska. We selected these fishes because they are important in the trophic ecology of the intertidal area (Gibson 1969, 1982) and in the field are more likely than subtidal fishes to demonstrate the effects of oil; they have a relatively short life span, spawn in-
tertidally, and have restricted movements. In southern Alaska, intertidal fishes are important food for river otters Lutra canadensis (Larsen 1984), mink Mustela vison (Johnson 1985), pigeon guillemots Cepphus columba (Kuletz 1983), and subtidal fishes (Hart 1973). Although there is little published information on intertidal fishes in Alaska, studies conducted at lower latitudes of the north Pacific Ocean indicate they follow the general pattern described by Gibson (1969, 1982). Longevity is short, a maximum of about 10 years. For example, in British Columbia the maximum age of the high cockscomb Anoplarchus purpurescens was estimated as 5 years (Peppar 1965) and the crescent gunnel Pholis laeta, 6 years (Hughes 1986). Eggs are demersal, adhere to one another or to the substrate, and are guarded by either parent; the larvae are planktonic. The high cockscomb spawns beneath rocks in late January to February where it guards its eggs at low tide (Coleman 1992). Hughes (1986) found they were virtually absent in eelgrass beds from December through March, but breeding pairs were found beneath rocks in February and April. We found the high cockscomb guarding egg masses as late as May and the crescent gunnel doing so in March (unpublished data). Movements of juveniles and adults are primarily related to seasonal and tidal cycles (Gibson 1969, 1982). They move about in the intertidal zone when the tide is in but remain in wet refugia—underneath rocks or vegetation and in tide pools—when the tide is out. Horn and Riegle (1981) found that five species of intertidal stichaeids from California can survive out of water for about 20 h. Movement is restricted for planktonic larvae and adults of taxa found in this study. Marliave (1986) found that the planktonic larvae of rocky-intertidal stichaeids, cottids, and pholids were more dense within 4 m of shore than offshore; they were also more abundant along rocky shores than sandy shores. This suggests that larvae of rocky-intertidal fishes resist offshore and perhaps also alongshore dispersal. There is limited movement in both the tidepool sculpin Oligocottus maculosus and mosshead sculpin Clinocottus globiceps\ individuals of both species demonstrated fidelity to specific tide pools when displaced (Green 197la, 1973). The ability of the tidepool sculpin to return to areas previously occupied seems to increase with age (Craik 1981). Peppar (1965) concluded that movement of the high cockscomb was ordinarily restricted to 15 m in the summer but found no indication of homing. However, there was evidence of seasonal differences in movement
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OIL SPILL EFFECT ON ALASKAN INTERTIDAL FISH
FIGURE 1.—Study area and general station locations in Prince William Sound, Alaska.
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BARBER ET AL.
TABLE I.—Percentages of slope, substrate type, and cover type at reference (R) and oiled-cleaned (O) sites for three habitat types sampled in Prince William Sound. Alaska, in 1990 and 1991. Each value is the average over all tidal heights sampled during both visits in each year. Cover type 3
Substrate type
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Site
Slope
M
s
FG
CG
CB
Organic as algaeb
Ifmr-
LB
SB
BR
ganic Organic
K
MA
S
MO
BL
63 66
1 2
17 22
1 2
6 9
52 46
29 19
2 1
11 11
2 1
4 2
56 50
57 54
43 45
1 4
8 4
2 3
11 II
49 65
1990: sheltered-rocky habitat 9 22 6 35 33 6 21 5 23 33 1990: coarsc-textured habitat 15 12 8 70 28 21 1 80
R 0
19.4 17.2
0 1
0 0
1 1
9 7
R 0
7.5 6.1
1 1
4 1
3 3
23 18
26 24
R O
9.7 12.0
1 1
0 0
I 0
7 6
11 7
R 0
21.3 16.5
0 0
0
I
2 3
7 6
11 10
1991: sheltered-rocky habitat 22 12 30 35 24 11 27 37
61 61
0 0
35 37
18 5
12 11
38 43
R 0
8.2 6.1
2 1
0 0
0 2
32 26
34 35
1991: coarsc-textured habitat 10 14 1 59 13 19 1 83
40 17
2 1
36 12
10 11
3 2
45 43
R O
8.1 8.0
0 0
1 1
1 0
3 3
7 7
1991: exposed-rocky habitat 22 7 38 37 30 9 31 40
63 59
9 8
16 14
5 8
15 16
45 48
1990: exposed-rocky habitat
a b
15 34
9 5
43 38
M = mud. silt, or clay (40 cm); BR = bedrock. K = kelp; MA = mat; S = stringy; MO = mossy; BL = bulky.
(Peppar 1965; Hughes 1986). Ralston and Horn (1986) found that movement of the monkeyeface prickleback Cebidichthys violaceus during high tide was restricted to about 2 m2. Maximum age of the high cockscomb prickleback was reported as 5 years (Peppar 1965). The crescent gunnel commonly reached age 4, and one age-6 specimen was reported (Hughes 1986). Study Area Prince William Sound (Figure 1) is classified as "humid-maritime" with an annual precipitation averaging 226 cm at Cordova (Eck 1983). Although there are frequent heavy accumulations of snow during winter, precipitation at low elevations occurs primarily as rain. The topography of the islands in the sound is rugged with perennially snow-capped mountains rising to over 900 m above sea level. The area was glaciated about 10,000 years ago, and considerable tectonic activity occurs presently (Moffit 1954). The retreating glaciers and earthquakes left steep slopes that drop abruptly to rocky shorelines with many inlets and bays. Our study area was the intertidal zone, which is substantial in Prince William Sound. During
spring and summer, low tide height is 4-6 m below mean high high tide.
Methods A complete description of the study design and techniques used to select the study sites may be found in McDonald et al. (in press) and Sundberg et al. (in press). In summary, from digitized environmental sensitivity index maps contained in a geographical information system database, the shoreline of Prince William Sound was divided into computer-generated sites 100-600 m long during spring and early summer 1989. Each site was assigned to five habitat types and further classified as to three degrees of oiling (as of July 1989) from digitized oil spill impact maps. We selected potential study sites using a stratified random sampling procedure with probability proportional to arc length for each of the 15 habitat-oiling types. Those sites with slopes greater than 30° were judged unsafe and not accessible by field crews. From surveys and problems in methodology encountered during 1989, the study design was modified during winter 1989-1990 (McDonald et al., in press; Sundberg et al., in press). The five habitat
465
OIL SPILL EFFECT ON ALASKAN INTERTIDAL FISH
TABLE 2.—Numbers of intertidal fishes and their percentages of all fish captured at sampled sites in Prince William Sound during each of two visits in 1990 and 1991. 1990
Taxon
Stichaeidae High cockscomb Anoplarchus purpurescens Anoplarchus sp.
1991
Percent of total (all
Visit 1
Visit 2
Visit 1
Visit 2
Species total
1,209 9
1.223 0
1,141 0
1,094 0
4,667 9
74.2 0.1
59
42
70
63
234
3.7
2
0
1
1
4
*
9
2
5 0
17 0
24 0
55 2
0.9 *
131
221
156
153
661
10.5
2 10
1 1
0 18
0 0
3 29
* 0.5
81
100
92
13
286
4.6
0
1
7
6
14
0.2
0
0
2
0
2
*
I
0
0
0
1
*
1
2
1
1
5
*
0
0
1
0
1
*
0 2 ()
1 0 0
0 0
0 0
1 2 1
* * *
162
49
23
59
293
4.7
9
7
4
1
21
0.3
1
()
0
0
1
1.690
1,653
1,534
1.415
6.292
species^
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Black pricklcback Xiphister atropurpureus Rock prickleback X. mucosus Ribbon prickleback Phytichlhys ch irits Unidentified Pholidae Crescent gunnel Pholis laeta
Penpoint gunnel Apodichihvs flavidus Unidentified Cottidae Tidepool sculpin Oligocottus maculosus Simx)thead sculpin Anedius Uneralis Padded sculpin A. fenestralis Scalyhead sculpin A. harringtoni Sharpnose sculpin Clinocottus acuticeps
Calico sculpin C. cmbr\nm Mosshead sculpin C. globiceps Icelinus sp. Myoxttcephalus sp. Liparidae Liparis sp. Scytalinidac Graveldiver Scytalina cerdale Ammodytidae Pacific sand lance A mmodytes hexapterus
Total ;l
1
0
*
Asterisks denote
r;
^)
C)
i
i
1990
1W1
FIGURE 2.—(A) Numbers of fish species per square meter captured at reference and oiled-cleaned sites for the three habitats combined in Prince William Sound during each of two visits (1 and 2) in 1990 and 1991. (B) Mean fish species diversities (eH) for reference and oiled-cleaned sites of three habitats combined in Prince William Sound during each of two visits (1 and 2) in 1990 and 1991. Vertical bars indicate the range of species diversity.
pairs) during the first visit on 13 May-30 June and 16 site pairs during the second visit on 5 July-8 September; one coarse-textured matched pair
could not be sampled because of inclement weather. In 1991, we sampled 12 site pairs (5 shelteredrocky, 4 coarse-textured, and 3 exposed-rocky) during the first visit on 13 May-16 June and 11 site pairs (4 sheltered-rocky, 4 coarse-textured, and 3 exposed-rocky) during the second visit on 23 June-16 July. The length of shoreline at each site was measured with a surveyor's tape at the high high-water mark. During the first visit in 1990, six transects were established at each site perpendicular to the shoreline. The beginning of each transect was separated by uniform distance, 3 m to the right of
each previous transect, with a random starting point for the first transect. The length of each transect was measured at low tide with a surveyor's tape. Each transect was also divided into zones of 1-m vertical drop in elevation (MVD) from mean high high tide to the edge of the water while the tide was out. Each MVD was determined with a meter stick and surveyor's level. Within a 1-mwide area along the transect, we estimated the percentage of inorganic and organic cover before searching for fish in each MVD. The categories of inorganic cover were silt-mud-clay (particles 40 cm), and bedrock. Organic
467
OIL SPILL EFFECT ON ALASKAN INTF.RTIDAL FISH
1.5
1.2
1.3 1.0
1.1
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0.8
» 0.9
0.7
0.6
0.5 0.4 x'
Reference . Oil
0.3
0.2
0.1
1990
1991 2
1990
1991
2
FIGURE 3.—Density (number/m ) and biomass (g/m ) estimates of intertidal fish captured at reference and oiledcleaned site pairs sampled during each of two visits ( I and 2) in Prince William Sound in 1990 and 1991. Each arithmetic mean is for all three habitats and 1-m vertical drops 2-4 combined.
cover was classified by its gross features as either mat, kelp, mossy, stringy, or bulky. Fish were sampled within a collapsible frame 1 m wide by 1.5 m long that was placed lengthwise on the transect while the tide was out. We placed the frame at the head of each transect, then turned over rocks and vegetation within the frame and collected fish by hand. We sequentially moved down the transect with the frame and collected fish until we reached the edge of the water. The fish collected were recorded by quadrat, i.e., an MVD within a transect. On all visits in 1990 we sampled MVDs 1-4. However, we found few fish in MVD 1 and therefore sampled only MVDs 2-4 in 1991. Fish captured in each quadrat were killed and fixed in 10% solution of formaldehyde in freshwater. After 24 h the fish were rinsed in water and placed in 70% isopropyl alcohol. In the laboratory, fish were identified to species, measured to the nearest millimeter, and weighed to the nearest 0.01 g on an electric pan balance. Fish density (number/
m 2 ) and biomass (g/m 2 ) were computed for each quadrat, transect, and MVD. During the second visit in 1990 and both visits in 1991, transects were established 3 m to the left of each former transect, as viewed facing the water. Sampling was conducted as previously described. Species diversity at reference and O-C sites was evaluated with the Shannon-Wiener index H= -2
Pi is the proportion of species / collected at a study site and n is the number of species. Then H was rescaled (Ricklefs 1973) so it was expressed relative to the number of species: diversity = eH. A one-tailed Wilcoxon signed-ranks test was used to compare O-C and reference sites sampled during the same visit. A probability level of a = 0.05 was considered significant. Results of the Wilcoxon signed-ranks test are denoted by Pw in
the text and tables.
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BARBER ET AL.
TABLE 3.—Mean densities (number/m2) and SEs (in parentheses) for intertidal fishes captured at reference (R) and oiled-cleaned (O) sites in Prince William Sound during each of two visits (1 and 2) in 1990 and 1991. The probability value (/V) is frpm the Wilcoxon signed-ranks test; asterisks highlight P ^ 0.05*. Each value is for 1-m vertical drops 2-4 combined; /V = number of transects at reference and oiled-cleaned sites or number of site pairs in the signed-ranks test. 1990
1991
Visit 2
Visit 1
statistic
yv
Density
N
Visit 2
Visit 1
N
Density
yv
Density
0.744 (0.150) 0.399 (0.062)
49
0.868 (0.172) 0.863 (0.158)
40
0.981 (0.186) 0.981 (0.225)
0.038*
12
0.460
11
0.407
0.835 (0.261) 1.045 (0.221)
16
0.835 (0.218) 1.321 (0.375)
0.250
4
0.113
1.295 (0.377) 0.627 (0.340)
13
1.147 (0.450) 0.709 (0.418)
4
0.034*
4
0.077
Exposed-rocky habitat 0.751 12 (0.234) 0.432 10 (0.120)
0.356 (0.071) 0.852 (0.238)
11
0.997 (0.305) 0.832 (0.279)
0.142
3
Density
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Habitats combined R
90
0
89
Pw
17
0.852 (0.173) 0.295 (0.054)
82
0.028*
16
89
45
40
Sheltered-rocky habitat R
27
0
29
Pw
5
R
41
0
37
Pw
7
R
22
0
23
Pw
5
1.104 (0.379) 0.344 (0.086)
29
0.136
5
29
0.882 (0.273) 0.184 (0.075)
35
0.032*
6
0.488 (0.169) 0.410 (0.129) 0.343
38
18
22 5
0.864 (0.214) 0.622 (0.150) 0.040*
21 20 5
Coarse-textured habitat 0.641 16 (0.282) 0.209 15 (0.046) 0.199
0.343
To corroborate the Wilcoxon analyses, we used multiple stepwise logistic regression models fitted by the forward stepwise procedure in SYSTAT (Wilkinson 1990) to identify habitat variables that were significantly related to intertidal fish density. Standard errors of the coefficients were determined by bootstrap procedures (Manly 1991) because MVDs from a given transect were not independent. In the stepwise procedure, variables were included in the model if they were significant at a = 0.05. Results Habitat features differed between habitat types and varied between years (Table 1). The average slope was greatest at sheltered-rocky and least at coarse-textured sites both years. However, the slope at exposed-rocky sites declined and was more similar to coarse-textured sites in 1991. The percent organic matter was greatest at sheltered-
rocky and intermediate at exposed-rocky sites in 1990. Organic matter increased at reference
3
16
15
9
0.500
coarse-textured and at reference and oiled exposed-rocky sites in 1991. Bulky algae was most common at all three habitat types both years but declined in 1991 with a concomitant increase of matting algae. Bedrock was greatest at exposedrocky sites than other sites, undoubtedly a reflection of the greater exposure to wind and wave action. The substrate type at coarse-textured sites varied primarily between coarse gravel and large boulders. Fish in 21 species were captured during the study (Table 2). Five taxa made up 97.6% of the total number and one, the high cockscomb, made up 74.2% (Table 2). For all habitats combined, the average number of species did not differ significantly between reference and O-C sites during any visit, and the number of species increased substantially from 1990 to 1991 (Figure 2a). There were also no significant differences in the number of species between reference and O-C sites within habitat types. Diversity values for all habitats com-
OIL SPILL EFFECT ON A L A S K A N INTERTIDAL FISH
469
TABLE 4.—Mean biomasses (g/m2) and SEs (in parentheses) for intertidal fishes captured at reference (R) and oiledcleaned (O) sites in Prince William Sound during each of two visits ( I and 2) in 1990 and 1991. The probability value (/V) is from the Wilcoxon signed-ranks test; asterisks highlight P ^ 0.05*. Each value is for 1-m vertical drops 2-4 combined; N = number of transects at reference and oiled-cleaned sites or number of site pairs in the signed-ranks test. 1990
1991
Visit I
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Site
N
R
90
0
89
Visit 2 Mean
N
0.351 (0.078) 0.222 (0.050)
82 89
17
0.127
16
R
27
0.172 (0.046) 0.226 (0.065)
29
0
Pw
29 5
R
41
0
37
Pw
7
R
22
0
23
Pw
5
0.367 0.386 (0.112) 0.170 (0.056) 0.088 0.504 (0.236) 0.302 (0.155)
0.173
Mean
N
Habitats combined 0.327 49 (0.059) 0.204 45 (0.039)
Pw
29
5 35 38 6 18 22 5
Visit 2
Visit 1
0.096
12
Sheltered-rocky habitat 21 0.223 (0.060) 0.288 (0.092)
20
0.447
Mean
N
Mean
0.969 (0.239) 0.804 (0.162)
40
1.060 (0.304) 1.063 (0.251)
0.319
11
0.194
0.920 (0.416) 0.953 (0.243)
16
0.428 (0.135) 1 .354 (0.487)
40
16
5
0.343
4
0.022*
Coarse-textured habitat 0.305 16 (0.093) 0.123 15 (0.035)
1.226 (0.483) 0.478 (0.208)
13
0.771 (0.279) 0.448 (0.211)
4
0.034*
4
0.034*
Exposed-rocky habitat 0.539 12 (0.171) 10 0.234 (0.079)
0.710 (0.178) 0.993 (0.449)
11
2.321 (0.965) 1.570 (0.564)
0.500
3
0.250
0.069
bined and within habitats tended to be higher at O-C sites than at reference sites during all visits but these differences were not significant (Figure 2b). For all habitats combined, fish density and biomass were greater at reference than at O-C sites in 1990 (Figure 3). In 1991, neither density nor biomass showed consistent differences between reference and O-C sites (Figure 3). Density for all habitats combined in 1990 was significantly greater at reference sites for both the first and second visits (Table 3). Density was nearly three times greater at reference than O-C sites for the first visit and nearly twice as great at the second visit (Table 3). During 1991 for all habitats combined, there were no significant differences in density between reference and O-C sites for either the first or second visits (Table 3). Although biomass in 1990 for all habitats combined was greater at reference than O-C sites during both the first and second visits (Figure 3; Table 4), the differences
3
15
9
0.500
were not significant (Table 4). In 1991, biomass was essentially equal at reference and O-C sites for both visits (Figure 3; Table 4). Although density and biomass increased at both reference and O-C sites in 1991, the magnitude of the increases was relatively greater at O-C sites (Figure 3). The differences in density and biomass between reference and O-C sites varied among the three habitats (Figures 4, 5). In the sheltered-rocky habitat during the first visit in 1990, density at reference sites (1.10/m 2 ) was more than three times greater than at O-C sites (0.34/m3; Table 3). Although this difference was relatively large, it was not significant (Table 3). In contrast, during the second visit, density at reference sites (0.86/m2) was significantly greater than at O-C sites (0.62/ m2) but the differences in fish density were not as great on the first visit (Table 3). During 1991, density at reference sites was less than at O-C sites during the first and second visits, and there were no significant differences (Table 3). Biomass at
470
BARBER ET AL.
Sheltered Rocky
Coarse Textured
Exposed Rocky
1.6
1.4 1.2
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%
11.0 > i 0,8
0.6 0.4
Reference o—
0.2
V.--"*
0.0
1990
1991
1990
1991
1990
1991
FIGURE 4.—Density (number/m 2 ) estimates of intertidal fish captured at reference and oiled-cleaned site pairs sampled in three habitat types during each of two visits (1 and 2) in Prince William Sound in 1990 and 1991. Each arithmetic mean is for 1-m vertical drops 2-4 combined.
reference sites during both visits in 1990 and the first visit in 1991 was about the same as that of O-C sites (Table 4). Biomass at O-C sites during the second visit of 1991 was significantly greater than at reference sites (Table 4). Density and biomass in the coarse-textured habitat was consistently greater at reference sites than at O-C sites (Figures 4, 5). The differences, however, were not always significant (Tables 3, 4). During visit 1 in 1990, density at reference sites (0.9/m2) was significantly greater than at O-C sites (0.2/m2). During visit 2, density at reference sites (0.6/m2) was three times greater than at O-C sites (0.2/m2), but the difference was not significant (Table 3). Density at reference sites in 1991 during the first visit (1.3/m2) was significantly greater than at O-C sites (0.6/m2). During the second visit, density was again greater at reference than at OC sites but the difference was not significant (Table 3). Biomass at reference sites in 1990 was more than twice that at O-C sites for both the first and second visits but these differences were not sig-
nificant (Table 4). During both visits in 1991, biomass increased at both reference and O-C sites (Figure 5), reference density being about twice that of O-C sites; the differences were significant for both visits (Table 4). Within the exposed-rocky habitat, density and biomass at reference sites were greater than at OC sites during both visits in 1990 but not in 1991 (Figures 4, 5). Density at reference sites in 1990 and 1991 varied from less than half to nearly twice that of O-C sites, but these differences were not significant (Table 3). Biomass at reference sites during the first and second visits in 1990 was about twice that at O-C sites but was not significant (Table 4). In 1991, density and biomass were not consistently greater at either reference or O-C sites, and there were no significant differences (Tables 3, 4). In MVD 2 and 3 for both years, the percentage of quadrats containing fish was higher at reference sites, but these differences were not significant (Figure 6). There was an overall tendency for the
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OIL SPILL EFFECT ON ALASKAN 1NTERTIDAL FISH
2-5 r Sheltered Rocky
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2.0
Coarse Textured
Exposed Rocky
Reference o-
i 1.0
0.5
0.0
1990
1991
1990
1991
1990
1991
2
FIGURE 5.—Mean biomass (g/m ) estimates of intertidal fish captured at reference and oiled-cleaned site pairs sampled in three habitat types during each of two visits (1 and 2) in Prince William Sound in 1990 and 1991. Each arithmetic mean is for 1-m vertical drops 2-4 combined.
percentage of quadrats containing fish to increase through time in MVD 3 and 4 but not in MVD 2.
Additionally, in both reference and O-C sites, the percentage of quadrats containing fish increased from MVD 2 to MVD 4 (Figure 6). The logistic regression and bootstrapping analysis indicated that the presence of oil was a significant predictor of reduced fish density in 1990 but not in 1991 for both MVD 3 and 4, corroborating the results of the Wilcoxon signed-ranks test on density between O-C and reference sites (Tables 5, 6). Abundance of mat algae entered into the regression model as a significant predictor of increased fish density in 1990 and 1991 (MVD 3 and 4). Other habitat variables that entered the models as significant predictors of increased fish density were amount of string algae (MVD 3; 1991) and moss algae (MVD 4; 1991), whereas amount of kelp (MVD 4; 1991), bedrock (MVD 3; 1990), and cobble (MVD 2; 1991) entered the models as significant predictors of reduced fish
density. The categorical variable "visit" also entered one model as significant, indicating higher density during visit 1 than during visit 2 in 1990. Discussion For all habitat types combined, density and biomass were lower at O-C sites than at reference sites during summer 1990, 1 year after the spill. In addition, multiple logistic regression models showed that presence of oil was a significant predictor of reduced fish density in 1990 but not in 1991. In 1991, density and biomass increased at both O-C and reference sites, but the increases at O-C sites were much greater than those at reference sites. For example, biomass at reference sites during the second visit in 1991 was 324% of the biomass during the second visit of 1990, compared to a 521% increase in biomass at O-C sites for the same period. As a result, density and biomass were similar at reference and O-C sites in 1991; a similar pattern was evident within habitat types.
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40
30
MVD 2 (0.101)
(0.104)
(0.122)
(0.458)
20
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-x-
MVD3 (0.095)
(0.150)
90
60
1190
1991
FIGURE 6.—Percentages of quadrats containing intertidal fish at each 1-m vertical drop (MVD) of tidal height along transects at reference and oiled-cleaned sites sampled in Prince William Sound during each of two visits (1 and 2) in 1990 and 1991. The PW values (in parentheses) are from the Wilcoxon signed-ranks test for each visit and MVD.
Our study indicates that there was an initial negative effect on intertidal fish. In contrast, earlier field studies have generally failed to show effects of oil spills on fish (Rice 1985). Even in large, highly publicized spills, significant effects on fish stocks have not been found (Wiseman et al. 1982; Mclntyre 1982). Rice (1985) stressed that it is difficult to predict the effects of oil on fish populations from laboratory studies because fish can respond physiologically and behaviorally to oil exposure in many different ways. Additionally, there
have been no field studies that demonstrate decreased fish abundance or biomass because of oil (Malins and Hodgins 1981). That we observed statistically significant differences in density but not in biomass may be a result of differential mortality and movement between small juveniles and adults at reference and O-C sites. We might have obtained more definitive results if high sampling variability and the small sample sizes within habitat type had not limited our ability to detect statistically significant differences at the
OIL SPILL EFFECT ON A L A S K A N INTERTIDAL FISH
TABLE 5.—Coefficients and SEs (in parentheses) for forward multiple stepwise logistic regression analyses predicting fish density at 1-m vertical drops 2-4 for three habitat types sampled in Prince William Sound during two visits in 1990. Only habitat variables that entered the logistic regression analyses were included in the bootstrap procedure to determine SE and significance level. Asterisks denote significant coefficients at P ^ 0.05*.
TABLK 6.—Coefficients and SEs (in parentheses) for forward multiple stepwise logistic regression analyses predicting fish density at 1-m vertical drops 2-4 for three habitat types sampled in Prince William Sound during two visits in 1991. Only habitat variables that entered the logistic regression analyses were included in the bootstrap procedure to determine SE and significance level. Asterisks denote significant coefficients at P < 0.05*.
Meter vertical drop
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Meter vertical drop
Variable11
2
3
4
Variable3
2
3
4
Constant
0.118
0.987
1.780
Constant
0.216
0.561
1.062
-0.059 (0.058)
-0.783* (0.349)
-1.136* (0.587)
Mat
-0.016 (0.01 1)
0.019* (0.01 1)
10.060* (0.015)
-1.157* (0.623)
Moss
0.049* (0.023)
0.056* (0.03 1 )
Kelp
-0.058 (0.045)
Oil Visit
0.074 (0.068)
Mat
0.007 (0.006)
SB
0.002 (0.002)
BR
0.047* (0.026)
String -0.012* (0.005) 0.029 (0.021)
CG CT
N 11
-0.093 (0.062) 367
Cobble
-0.004* (0.002)
SR
-0.272* (0.145)
:- 0.642* (0.382)
183
166
N a
319
159
SB = small boulder, BR = bedrock, CG = coarse gravel, CT = coarsc-tcxturcd habitat.
0.047* (0.026)
104
SR = sheltered-rocky habitat.
reference sites was 3.1 times that at O-C sites but the difference was not statistically significant. There were also difficulties in locating unoiled a = 0.05 level. This variability may be due to the reference sites that could be matched with oiledpatchy distribution and abundance of intertidal fish cleaned sites and sampled in a timely manner; con(e.g., Green 197lb; Burgess 1978; Barton 1982). sequently some very lightly oiled sites were seAdditionally, unavoidable constraints imposed on lected and used as references. It is also possible the study required us to consider moderately and that some unoiled reference sites, because of their heavily oiled sites with unknown cleanup activities close proximity to oiled sites, were influenced betogether as oiled-cleaned sites. The power of the fore inspection either by undissolved oil or oil deWilcoxon signed-ranks test was relatively low be- posited on the beach and then lifted off by subcause of small sample sizes within habitats. There- sequent tides, as reported by Hayes and Gundlach fore, there was a high probability of accepting the (1979). In other spills, oil sank to near-bottom wanull hypothesis of no oil-cleanup effect within ters and moved horizontally with bottom currents habitat types when there was, indeed, an effect. into intertidal areas (Conomos 1975; Clark and As an example of the influence of small sample MacLeod 1977). If better reference sites entirely sizes on the power to detect differences, we re- free of oil effects could have been located, we calculated the significance level for 1990 density believe we would have found more significant difat reference and O-C sites, all habitats combined, ferences. Therefore, we consider our results to be at only those sites visited in 1991. The differences conservative. between reference and O-C sites were not signifThere were no significant differences or trends icant at the a = 0.05 level (first visit, Pw = 0.139; in species diversity indices. This is counter to the second visit PW = 0.059, N = 10 both visits), generally accepted observation that diversity dealthough the magnitudes of the difference between creases with decreased water quality (Morris and O-C and reference sites are similar with and with- Georges 1993). Rice et al. (1979) exposed adults out the sites that were eliminated in 1991. This of the two most common species, the high cockslack of power may have occurred at sheltered- comb and the crescent gunnel, to water-soluble rocky habitats, for example, where the density at fractions of Cook Inlet crude oil and number 2 fuel
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oil and found that none died at the highest concentrations used. This suggests that our observations of reduced density may be due more to chronic effects or behavioral responses including emigration. When reference sites are subjectively matched to the affected sites based on physical site characteristics, increased abundance and a convergence of data from the reference and affected sites over time provide strong evidence of an initial effect followed by the recovery process. They also indicate that the reference sites were properly matched to the affected sites (Skalski and Robson 1992). Therefore, the recovery we observed between 1990 and 1991 suggests that the significant differences observed in 1990 were real and a result of oil-cleanup, not simply a result of inherent precleanup differences between O-C and reference sites. Thus, we conclude that intertidal fish in Prince William Sound were adversely affected both by the March 1989 Exxon Valdez oil spill and the subsequent cleanup activities. The effect was still present in 1990, but there was strong evidence that recovery was occurring by 1991. Acknowledgments We thank W. A. Hubert, J. M. Green, and D. R. Bernard for their reviews of earlier drafts of this paper. We also thank D. R. Gibbons and M. D. Strickland for discussions throughout the project. The diligence of Julie Gillispie, Eddie Harbour, and Pam Croom is greatly appreciated. Funding for this project was provided by the Exxon Valdez Oil Spill Trustee Council. References Barton, M. G. 1982. Comparative distribution and habitat preferences of two species of stichaeoid fishes in Yaquina Bay, Oregon. Journal of Experimental Marine Biology and Ecology 59:77-87. Berge, J. A., K. I. Johannessen, and L.-O. Reiersen. 1983. Effects of the water soluble fraction of North Sea crude oil on the swimming activity of the sand goby, Pomatoschistus minutuss (Pallas). Journal of Experimental Marine Biology and Ecology 68:159167. Burgess, T. J. 1978. The comparative ecology of two sympatric polychromatic populations of Xererpes fucorum Jordan and Gilbert (Pisces: Pholididae) from the rocky intertidal zone of central California. Journal of Experimental Marine Biology and Ecology 35:43-58. Chasse, C. 1978. The ecological impact on and near shores by the Amoco Cadiz oil spill. Marine Pollution Bulletin 9:298-301.
Clark, R. C., Jr., and W. D. MacLeod, Jr. 1977. Inputs, transport mechanisms, and observed concentration of petroleum in the marine environment. Pages 91223 in D. C. Malins, editor. Effects of petroleum on arctic and subarctic marine environments and organisms, volume 1. Academic Press, New York. Coleman, R. M. 1992. Reproductive biology and female parental care in the cockscomb prickleback, Anoplarchus purpurescens (Pisces: Stichaeidae). Environmental Biology of Fishes 35:177-186. Conomos, T. J. 1975. Movement of spilled oil as predicted by estuarine nontidal drift. Limnology and Oceanography 20:159-173. Craik, G. J. S. 1981. The effects of age and length on homing performance in the intertidal cottid, Oligocottus maculosus Girard. Canadian Journal of Zoology 59:598-604. Eck, K. C. 1983. Forest characteristics and associated deer forage production on Prince William Sound islands. Master's thesis. University of Alaska Fairbanks, Fairbanks. EVOS-DAGG (Exxon Valdez Oil Spill, Damage Assessment Geoprocessing Group). 1991. The Exxon Valdez oil spill natural resource damage assessment and restoration: a report on oiling to environmentally sensitive shoreline. Alaska Department of Natural Resources, GIS Mapping and Analysis, Technical Service 3, Anchorage. Fletcher, G. L., M. J. King, J. W. Kiceniuk, and R. E Addison. 1982. Liver hypertrophy in winter flounder following exposure to experimentally oiled sediments. Comparative Biochemistry and Physiology 73C:457-462. Gibson, R. N. 1969. The biology and behavior of littoral fish. Oceanography and Marine Biology: An Annual Review 7:367-410. Gibson, R. N. 1982. Recent studies on the biology of intertidal fishes. Oceanography and Marine Biology: An Annual Review 20:363-414. Green, J. M. 197la. High tide movements and homing behaviour of the tidepool sculpin Oligocottus maculosus. Journal of the Fisheries Research Board of Canada 28:383-389. Green, J. M. 1971b. Local distribution of Oligocottus maculosus Girard and other tidepool cottids of the west coast of Vancouver Island, British Columbia. Canadian Journal of Zoology 49:1111-1128. Green, J. M. 1973. Evidence for homing in the mosshead sculpin (Clinocottus globisceps). Journal of the Fisheries Research Board of Canada 30:129-130. Haensly, W. E., J. M. Neff, J. R. Sharp, A. C. Morris, M. F. Bedgood, and P. D. Boem. 1982. Histopathology of Pleuronectes platessa L. from Aber Wrac'h and Aber Benoit, Brittany, France: longterm effects of the Amoco Cadiz crude oil spill. Journal of Fish Diseases 5:365-391. Hart, J. L. 1973. Pacific fishes of Canada. Fisheries Research Board of Canada 180. Hayes, M. O., and E. R. Gundlach. 1979. Role of dynamic coastal processes in the impact of the Amoco Cadiz oil spill (March 1978) Brittany, France. Pages 193-198 in Proceedings of the 1979 oil spill con-
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