Prog. expo Tumor Res., vol. 20, pp. 75-85 (Karger, Basel 1976)
Ocean Wastewater Discharge and Tumors in a Southern California Flatfishl A. J. MEARNS and M. J. SHERWOOD Southern California Coastal Water Research Project, EI Segundo, Calif.
Introduction
2
Contribution 26 of the Coastal Water Research Project.
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Traditionally, one of the important uses of the coastal waters for man has been as a repository for his wastes. The waters within a few kilometers of shore are perhaps the most directly influenced. Considering the absence of generally accepted criteria for environmental quality control, it is not surprising that there is concern over the adequacy of present-day marine wastewater discharge practices. In southern California, much concern has been generated by the presence of tumor-bearing fishes in coastal waters. In 1957, RUSSELL and KOTIN described lip papillomas from several white croaker (Genyonemus lineatus) taken from coastal waters in the Los Angeles area and postulated that this condition might be a response to an environmental irritant or pollutant. Later, YOUNG [1964] described a number of diseased and deformed fishes from other southern California trawl collections; the occurrence of skin tumors in Dover sole (Microstomus paci.ficus) was among the conditions described in this widely cited paper. By 1970, these reports and other (unpublished) data led the US Congress to call a Federal hearing in Santa Ana, California [US Congress, 1971] on water pollution, fish disease, and human health. The possibility that wastes discharged into the coastal waters are damaging marine resources has contributed to more extensive monitoring requirements for waste discharge agencies and more stringent State and Federal water pollution control legislation and enforcement. A major goal of the Coastal Water Research Project is to provide scientific information on the
MEARNS/SHERWOOD
76
ecological effects of wastes discharged into the sea and to identify the ecological benefits that might accrue from improved treatment of the wastewaters or reduction of discharge. More specifically, can the incidence of diseased fishes be reduced by improving waste treatment and, if so, what constituents need to be controlled? Our approach has been: (1) to identify the diseases that occur in significant frequencies; (2) to obtain the data necessary for understanding the life history of affected populations, and (3) to identify any correlations that exist between the locations of pollutant sources, the concentration of contaminants in the coastal biota, and the distribution and prevalence of diseased populations. Based on the data we have collected, we do not believe that the incidence of skin tumors in Dover sole is enhanced by southern California municipal wastewater discharges.
Our primary study area is located within the Southern California Bight, a natural oceanographic system that extends from Point Conception, California in the north to Cabo Colnett, Baja California, Mexico in the south, and is defined on the west by the eastern edge of the California Current; 94% of the total municipal wastewaters currently entering the Bight from southern California derive from five major dischargers (fig. 1). They are the County Sanitation Districts of Los Angeles County, which discharge 37l million gallons daily (mgd) on the Palos Verdes shelf; the city of Los Angeles, which discharges 335 mgd through a 60-m (5-mi.) outfall and 5 mgd through a lOO-m (7-mi.) outfall in Santa Monica Bay; the County Sanitation Districts of Orange County, which discharge 130 mgd in San Pedro Bay; the City of San Diego, which discharges 90 mgd off Point Lorna; and Ventura County, which discharges 12 mgd off Oxnard. Most of the treatment facilities of these agencies receive a substantial amount of the industrial wastes generated within their service areas. At present, less than 20% of the discharged waste receives secondary (biological) treatment; the remainder receives only primary treatment. Located adjacent to the Palos Verdes Peninsula is the Los Angeles/Long Beach Harbor, one of the three major harbors in California - also a potential source of pollutants to the coastal waters. Our studies of diseased fishes were focused on a lOO-km section of the southern California coastline from Oxnard in Ventura County to Dana Point in Orange County. Most of the nearly 700 trawls made to date were conducted in association with other local agencies, whose cooperation is greatly appreciated. All collections were taken with small otter trawls with headropes ranging in length from 4.9 to 12.2 m (16-40 feet) and cod-end stretch mesh netting of 1.3-3.5 cm (1'2-1'/, inches). Average on-bottom trawl time ranged from 10 to 20 min; most agencies conducted 10-min trawls. Trawling speeds ranged from 2.8 to 5.6 km/h, but were constant for each vessel. Tows were taken along constant depth contours. The data have been placed on computer cards, and summaries of fish abundance and disease frequencies by size, location, and season have been prepared [MEARNS and GREENE, 1974].
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Methods
Ocean Wastewater Discharge
77
LOS ANGELES
b.Rn...~"
~~
.
• •
SAN PEDRO
SANTA ~BAY • CATALINA '.: ISLAND
N
•
MAJOR MUNICIPAL WASTEWATER DISCHARGE
'. u.s.
.
~.-M80~O
Fig. 1. Otter trawl survey area, 1969-74.
Histological observations on diseased specimens have been made by Dr. R. BENDELE (Texas A & M University), Dr. J. HARSHBARGER (Smithsonian Institution), Dr. W. KLONTZ (University of Idaho), Dr. H. STICH (University of British Columbia), and Dr. S. R. WELLINGS (University of California, Davis). In addition, a series of regional studies on the sources, mass emission rates, distributions, and fates of two major groups of pollutants - chlorinated hydrocarbons and trace elements - have been coordinated by Dr. D. YOUNG of our Project. These data have proven extremely useful in understanding the ways in which pollutants are distributed in our coastal zone and have provided information for comparison with distributions of biological anomalies.
Tumors are one of several categories of diseases found in southern California fishes. Others include structural deformities and asymmetry of meristic features [VALENTINE and BRIDGES, 1969 ; VALENTINE et al., 1973 ; VALENTINE and SouLE, 1973] and fin and tail erosion diseases [MEARNS and SHERWOOD, 1974; SHERWOOD and MEARNS, in press; Southern California Coastal Water Research Project, 1973]. Among the southern California demersal, trawl-caught fishes, the Dover sole is the only species consistently affected with epidermal tumors. The tumors, which are noninvasive, vary in size and shape, ranging from round
Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
Characteristics of Tumors in Dover Sole
MEARNS/SHERWOOD
78
nodules 1 mm in diameter to irregularly shaped patches 40 mm in length. They consist primarily of the size-related structural types, i. e., angioepithelial nodules, epidermal papillomas, and angioepithelial polyps (fig. 2), previously described in flathead sole, English sole, and other pleuronectids [WELLINGS et at., 1965]. However, some affected specimens have highly pigmented (almost black) papillomas, and one tumor was described by WELLINGS [Southern California Coastal Water Research Project, 1973] as an invasive squamous cell carcinoma.
Where sampling has been sufficiently frequent, it is possible to see distinct patterns in the occurrence of tumor-bearing Dover sole. The species has an unusually long larval existence; the juveniles settle out of the plankton after approximately 1 year, and are seen primarily in February and May quarterly trawl samples, at depths greater than 80 m. Prevalence of tumorbearing individuals may reach 9% in the August and November catches. By the following February, overall prevalence in this group will have declined to about 2 %. As the fish continue to grow, the prevalence of tumor-bearing individuals drops considerably. The average number of tumors per tumorbearing fish is 1.8, and there is a positive correlation between tumor size and fish size, suggesting that tumors grow with the fish [MEARNS and SHERWOOD, 1974]. One of the most interesting aspects of our studies to date has been a comparison of the distributions of diseased fish populations with the location of pollutant sources and the distribution of contaminants in the marine environment. It seems clear that the discharge of trace metals and chlorinated hydrocarbons in municipal wastewaters has been reflected in increased concentrations of the constituents in the sediments around the wastewater outfalls. This is particularly evident in the Palos Verdes area. Prior to 1971, the Los Angeles County discharge on the Palos Verdes shelf was a major point source of DDT and its breakdown products to the southern California coastal waters. Although the mass emission rate of total DDT from this source decreased by approximately 80% from 1971 to 1973, we estimate that there are still 200 metric tons of total DDT in the Palos Verdes sediments [McDERMOTT et at., 1974]. The concentration of total DDT in the sediment decreases in all directions from the Palos Verdes shelf, and these gradients are reflected in the muscle tissue of Dover sole (table I). Since the Palos
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Distribution of Tumor-Bearing Specimens
Ocean Wastewater Discharge
79
a
b
c
o
I
I
10 20
mm
Verdes effluent includes the greatest amount of industrial waste of any of the southern California municipal wastewater discharges, it is also high in trace elements, and these are distributed in the sediments in a similar pattern along the coast. However, even in areas of extreme sediment contamination, the metals are not concentrated in animal tissues by more than a factor of two over noncontaminated areas (table I) [DE GOEIJ et ai., 1974; Southern California Coastal Water Research Project, 1973]. In addition, much of the surface sediment immediately surrounding the Palos Verdes submarine outfalls is anaerobic, as indicated by the distribution of hydrogen sulfide in the surface layer [KALIL, 1973].
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Fig. 2. Typical tumor-bearing Dover sole: (a) specimen with angioepithelial nodule (arrow); (b) specimen with epidermal papilloma, and (c) specimen with highly pigmented tumor with poorly defined edges, characteristic of angioepithelial polyp.
5
0.66 (0.22-4.0) 17 110 (18-500) 11
2.2 (1.2-3.5) 4
0.91 (0.42-4.3) 6
12
0.04 (0.02-0.10) 9
15 (13-30) 4
2.6 (1.6--3.6) 2
0.21 (0.12-0.42) 9
100-m pipe
30.5 (14--72) 24
0.24 (0.05-0.56) 21
335
60-m pipe
Los Angeles City
12.0 (1.67-69.8) 22
1.9 (1.1-3.1) 12
145 (19-550) 22
26 (2.8-230) 19
371
Los Angeles County
19 (16--36) 5
21 (12-55) 34
0.43 (0.06-0.49) 11
2.0 (1.9-2.5) 4
0.008 (0.002-0.016) 11
90
San Diego City
0.07 (0.03-0.11) 13
130
Orange County
0.08 (0.05---0.12) 6
2.0 (1.4--3.0) 6
Santa Catalina Island (control)
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a
Data from Southern California Coastal Water Research Project [1973] (reorganized and, in some cases, updated), and McDERMOTT et al. [1974].
Flow, mgd Sediments Total DDT, mg/dry kg Median Range Number of samples Copper, mg/dry kg Median Range Number of samples Dover sole liver Copper, mg/wet kg Median Range Number of samples Dover sole muscle Total DDT, mg/wet kg Median Range Number of samples
Ventura County
Table I. Distribution of total DDT and copper in sediments around five major outfall systems, and in Dover sole collected near these systems, and from a control areaa
0
00
0 0 0
~
~
en
;J:
en
Sf!..
z
en
> ~
~
Ocean Wastewater Discharge
81
Table II. Prevalence of epidermal tumors in Dover sole collected off the Palos Verdes Peninsula (135 samples) and in San Pedro Bay (64 samples), 1972-73 Fish size a , mmSL
Palos Verdes Peninsula
San Pedro Bay
number of fish
number of fish
tumor-bearing fish number
25 35 45 55 65 75 85 95 105 115 125 135 145 155 165 175 185 195 205 215 225 235 245 255 265 275 285 295 305 315 >315 Total
%
2
3 I 6 15 44 35 18 8 4 1 5
6.8 1.7
9.0 6.9 8.3 4.0 1.8 0.78 0.40 0.10 0.39
2
0.20
2
0.22
2 2 13,626
number
%
143
1.0
3 116 160 55 37 32 68 89 139 141 151 216 283 312 281 288 288 217 203 182 114 81 61 34 18 5 3 4 I 3 3,586
3 4 5 4 I 6
5.4 10.8 15.6 5.9 1.1 4.3
3 2
0.66 1.4 0.71
2
0.36
30
0.84
2
Midpoint of 10-mm size class. Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
a
2 4 20 44 58 67 217 532 873 1,021 1,025 990 1,034 1,284 1,293 1,237 1,137 1,023 796 449 303 142 46 18 7 2
tumor-bearing fish
82
MEARNS/SHERWOOD
Table III. Prevalence of epidermal tumors in Dover sole collected off southern California, 1972-73 Palos Verdes Shelf
San Pedro Bay
Dana Point
Santa Catalina Island
Number of samples Number of samples containing Dover sole
60 39
144 106
73 44
42 25
18 11
Number of Dover sole Number with tumors Percent with tumors
516 9
14,277 147 1.0
3,842 33 0.86
593 0 0
89 0 0
Number of Dover sole 60-120 mm SL Number with tumors Percent with tumors
96
1,829
443
29
8
0 0
0 0
1.7
5 5.2
106 5.8
26 5.9
The overall incidence of tumor-bearing Dover sole in southern California trawl catches is low, approximately 1 %, and the species is most abundant on the Palos Verdes shelf. However, when sufficient numbers of individuals have been collected to allow comparison of prevalences in different areas, there appear to be no gradients in the distributions of tumor-bearing specimens. Of 13,626 Dover sole collected in 135 samples off Palos Verdes, l.O% were tumor bearing; of 3,586 Dover sole collected in 64 samples in San Pedro Bay, to the south, 0.84% had epidermal tumors (table II). Specimens in the 60- to l20-mm standard length (SL) size range, which corresponds to the size of individuals taken in the fall and winter months following metamorphosis and settling, appeared to be the most frequently affected in both areas. Prevalences of tumor-bearing Dover sole in this size range were similar in Santa Monica Bay (5.2%), off Palos Verdes (5.8%), and in San Pedro Bay (5.9%; table III). Since Dover sole and sampling effort are not evenly distributed along the coast, catches off Dana Point and Santa Catalina Island have produced too few small individuals to adequately compare prevalences in these areas. The distribution of tumor-bearing individuals differs distinctly from that seen for Dover sole with eroded fins, in which affected specimens are strongly concentrated on the Palos Verdes shelf [MEARNS and SHERWOOD, 1974]. In the vicinity of the Orange County outfall system, quarterly trawl sampling at a standard set of stations began in November 1969 (although
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Santa Monica Bay
Ocean Wastewater Discharge
83
1,200
'"
0
III
Ii;
>
0
0
4-
0
Ii;
.0
E :J z
I
1- Change
1,000 800
1 1
600
1 1
400
in discharge
site
1
200 0 16 ---120mm SL
0III
'"
14
Ii;
12
0
10
I
8
1
> 0
01 C
.~
'"
.0
.!.
6
E .2
4
0
--Total I 1 1 .,
1
1
1/
c
'" '"
I 'a
II I' I'
~
i:'
a.
I
0
NFMADFMADFMANFMSN 1970
1971
1972
1973
Fig. 3. Prevalence of tumor-bearing Dover sole captured in the vicinity of the Orange County outfall system, 1969-73. The change from a 20- to 60-meter outfall occurred in April 1971. Data on length frequencies were not taken prior to December 1970.
size frequency data were not taken until December 1970). In April 1971, discharge through a short (20-meter) outfall was terminated, and a new outfall that discharges at 60 m - within the natural range of the Dover sole - was put into operation. The overall percentage of tumor-bearing Dover sole in the catches does not appear to be related to the change in discharge location (fig. 3).
Based on the data we have collected, we believe that the Dover sole skin tumor disease is not enhanced by the discharge of municipal waste in southern California and would not be reduced in overall incidence by projected improvements in waste treatment unless such changes affected the survival or recruitment of juvenile Dover sole. However, the disease may be associated
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Conclusions
MEARNS/SHERWOOD
84
with a very specific yet widely distributed agent that mayor may not be related to wastes produced by industrial development. We do believe that changes in waste treatment will affect the distribution of Dover sole with fin erosion, and that this disease, on a local scale, may be a most important sign of environmental damage. A comprehensive field program is an important part of any disease study, and sampling programs should be designed with the population characteristics of the affected species in mind: Sampling method, net mesh size, season, and depth range are important considerations in providing data for comparing different areas and for discovering correlations with potential causative agents.
Acknowledgments This work was supported in part by the Environmental Protection Agency under Grant R-801152. We are particularly indebted to Dr. B. MILLER, College of Fisheries, University of Washington, for a number of stimulating exchanges and for his assistance in formulating our research program. Special thanks are given to the Project staff, including M. J. ALLEN, J. WORD, and R. VOGLIN for their patient examination of several hundred thousand fishes.
GOEIJ, J.J.M. DE; GUINN, V.P.; YOUNG, D.R., and MEARNS, A.J.: Neutron activation analysis trace element studies of Dover sole liver and marine sediments; in Comparative studies of food and environmental contamination, pp. 189-200 (International Atomic Energy Agency, Vienna 1974). KALIL, E. K.: Rapid pore water analysis for sediments adjacent to reactor discharges. IAEA Symp. on Environmental Surveillance around Nuclear Installations, Warsaw 1973, lAEA-SM-180/37. McDERMOTT, D.J.; HEESEN, T.C., and YOUNG, D.R.: DDT in bottom sediments around five southern California outfall systems, Rept. TM 217 (So. Calif. Coastal Water Research Proj., EI Segundo 1974). MEARNS, A. J. and GREENE, C. S. (eds): A comparative trawl survey of three areas of heavy waste discharge, Rept. TM 215 (So. Calif. Coastal Water Research Proj., EI Segundo 1974). MEARNS, A. J. and SHERWOOD, M. J.: Environmental aspects of fin erosion and tumors in southern California Dover sole. Trans. Am. fish. Soc. 103: 799-810 (1974). RUSSELL, F.E. and KOTIN, P.: Squamous papilloma in the white croaker. J. natn. Cancer lnst. 18: 857-61 (1957).
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References
Ocean Wastewater Discharge
85
Dr. A.J. MEARNS, Senior Environmental Specialist, Southern California Coastal Water Research Project, 1500 East Imperial Highway, El Segundo, CA 90245 (USA)
Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
SHERWOOD, M. J. and MEARNS, A. J.: Disease responses in southern California coastal fishes. Naval Undersea Center Conf., San Clemente (in press). Southern California Coastal Water Research Project: The ecology of the Southern California Bight: Implications for water quality management. Rept. TR 104 (So. Calif. Coastal Water Research Proj., El Segundo 1973). US Congress, House Subcommittee on Fisheries and Wildlife Conservation: Water pollution, fish disease, and human health, hearing of 30 April 1970; in Fish and wildlife legislation, part 3, Rept. 91-42, 91st Congr., pp. 351-409 (US Govt. Printing Office, Washington 1971). VALENTINE, D. W. and BRIDGES, K. W.: High incidence of deformities in the serranid fish Paralabrax nebulifer from southern California. Copeia iii: 637-8 (1969). VALENTINE, D. W. and SouLE, M. E.: Effect of p,p' -DDT on developmental stability of pectoral fin rays in the grunion, Leuresthes tenuis. Fishery Bull. 71: 921-6 (1973). VALENTINE, D. W.; SouLE, M. E., and SAMOLLOW, P.: Asymmetry analysis in fishes: A possible statistical indicator of environmental stress. Fishery Bull. 71: 357-70 (1973). WELLINGS, S. R.; CHUINARD, R. G., and BENS, M.: A comparative study of skin neoplasms in four species of pleuronectid fishes. Ann. N. Y. Acad. Sci. 126: 479-501 (1965). YOUNG, P. H.: Some effects of sewer effluent on marine life. Calif. Fish Game 50: 33-41 (1964).
Ocean Wastewater Discharge and Tumors in a Southern California Flatfishl A. J. MEARNS and M. J. SHERWOOD Southern California Coastal Water Research Project, EI Segundo, Calif.
Introduction
2
Contribution 26 of the Coastal Water Research Project.
Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
Traditionally, one of the important uses of the coastal waters for man has been as a repository for his wastes. The waters within a few kilometers of shore are perhaps the most directly influenced. Considering the absence of generally accepted criteria for environmental quality control, it is not surprising that there is concern over the adequacy of present-day marine wastewater discharge practices. In southern California, much concern has been generated by the presence of tumor-bearing fishes in coastal waters. In 1957, RUSSELL and KOTIN described lip papillomas from several white croaker (Genyonemus lineatus) taken from coastal waters in the Los Angeles area and postulated that this condition might be a response to an environmental irritant or pollutant. Later, YOUNG [1964] described a number of diseased and deformed fishes from other southern California trawl collections; the occurrence of skin tumors in Dover sole (Microstomus paci.ficus) was among the conditions described in this widely cited paper. By 1970, these reports and other (unpublished) data led the US Congress to call a Federal hearing in Santa Ana, California [US Congress, 1971] on water pollution, fish disease, and human health. The possibility that wastes discharged into the coastal waters are damaging marine resources has contributed to more extensive monitoring requirements for waste discharge agencies and more stringent State and Federal water pollution control legislation and enforcement. A major goal of the Coastal Water Research Project is to provide scientific information on the
MEARNS/SHERWOOD
76
ecological effects of wastes discharged into the sea and to identify the ecological benefits that might accrue from improved treatment of the wastewaters or reduction of discharge. More specifically, can the incidence of diseased fishes be reduced by improving waste treatment and, if so, what constituents need to be controlled? Our approach has been: (1) to identify the diseases that occur in significant frequencies; (2) to obtain the data necessary for understanding the life history of affected populations, and (3) to identify any correlations that exist between the locations of pollutant sources, the concentration of contaminants in the coastal biota, and the distribution and prevalence of diseased populations. Based on the data we have collected, we do not believe that the incidence of skin tumors in Dover sole is enhanced by southern California municipal wastewater discharges.
Our primary study area is located within the Southern California Bight, a natural oceanographic system that extends from Point Conception, California in the north to Cabo Colnett, Baja California, Mexico in the south, and is defined on the west by the eastern edge of the California Current; 94% of the total municipal wastewaters currently entering the Bight from southern California derive from five major dischargers (fig. 1). They are the County Sanitation Districts of Los Angeles County, which discharge 37l million gallons daily (mgd) on the Palos Verdes shelf; the city of Los Angeles, which discharges 335 mgd through a 60-m (5-mi.) outfall and 5 mgd through a lOO-m (7-mi.) outfall in Santa Monica Bay; the County Sanitation Districts of Orange County, which discharge 130 mgd in San Pedro Bay; the City of San Diego, which discharges 90 mgd off Point Lorna; and Ventura County, which discharges 12 mgd off Oxnard. Most of the treatment facilities of these agencies receive a substantial amount of the industrial wastes generated within their service areas. At present, less than 20% of the discharged waste receives secondary (biological) treatment; the remainder receives only primary treatment. Located adjacent to the Palos Verdes Peninsula is the Los Angeles/Long Beach Harbor, one of the three major harbors in California - also a potential source of pollutants to the coastal waters. Our studies of diseased fishes were focused on a lOO-km section of the southern California coastline from Oxnard in Ventura County to Dana Point in Orange County. Most of the nearly 700 trawls made to date were conducted in association with other local agencies, whose cooperation is greatly appreciated. All collections were taken with small otter trawls with headropes ranging in length from 4.9 to 12.2 m (16-40 feet) and cod-end stretch mesh netting of 1.3-3.5 cm (1'2-1'/, inches). Average on-bottom trawl time ranged from 10 to 20 min; most agencies conducted 10-min trawls. Trawling speeds ranged from 2.8 to 5.6 km/h, but were constant for each vessel. Tows were taken along constant depth contours. The data have been placed on computer cards, and summaries of fish abundance and disease frequencies by size, location, and season have been prepared [MEARNS and GREENE, 1974].
Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
Methods
Ocean Wastewater Discharge
77
LOS ANGELES
b.Rn...~"
~~
.
• •
SAN PEDRO
SANTA ~BAY • CATALINA '.: ISLAND
N
•
MAJOR MUNICIPAL WASTEWATER DISCHARGE
'. u.s.
.
~.-M80~O
Fig. 1. Otter trawl survey area, 1969-74.
Histological observations on diseased specimens have been made by Dr. R. BENDELE (Texas A & M University), Dr. J. HARSHBARGER (Smithsonian Institution), Dr. W. KLONTZ (University of Idaho), Dr. H. STICH (University of British Columbia), and Dr. S. R. WELLINGS (University of California, Davis). In addition, a series of regional studies on the sources, mass emission rates, distributions, and fates of two major groups of pollutants - chlorinated hydrocarbons and trace elements - have been coordinated by Dr. D. YOUNG of our Project. These data have proven extremely useful in understanding the ways in which pollutants are distributed in our coastal zone and have provided information for comparison with distributions of biological anomalies.
Tumors are one of several categories of diseases found in southern California fishes. Others include structural deformities and asymmetry of meristic features [VALENTINE and BRIDGES, 1969 ; VALENTINE et al., 1973 ; VALENTINE and SouLE, 1973] and fin and tail erosion diseases [MEARNS and SHERWOOD, 1974; SHERWOOD and MEARNS, in press; Southern California Coastal Water Research Project, 1973]. Among the southern California demersal, trawl-caught fishes, the Dover sole is the only species consistently affected with epidermal tumors. The tumors, which are noninvasive, vary in size and shape, ranging from round
Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
Characteristics of Tumors in Dover Sole
MEARNS/SHERWOOD
78
nodules 1 mm in diameter to irregularly shaped patches 40 mm in length. They consist primarily of the size-related structural types, i. e., angioepithelial nodules, epidermal papillomas, and angioepithelial polyps (fig. 2), previously described in flathead sole, English sole, and other pleuronectids [WELLINGS et at., 1965]. However, some affected specimens have highly pigmented (almost black) papillomas, and one tumor was described by WELLINGS [Southern California Coastal Water Research Project, 1973] as an invasive squamous cell carcinoma.
Where sampling has been sufficiently frequent, it is possible to see distinct patterns in the occurrence of tumor-bearing Dover sole. The species has an unusually long larval existence; the juveniles settle out of the plankton after approximately 1 year, and are seen primarily in February and May quarterly trawl samples, at depths greater than 80 m. Prevalence of tumorbearing individuals may reach 9% in the August and November catches. By the following February, overall prevalence in this group will have declined to about 2 %. As the fish continue to grow, the prevalence of tumor-bearing individuals drops considerably. The average number of tumors per tumorbearing fish is 1.8, and there is a positive correlation between tumor size and fish size, suggesting that tumors grow with the fish [MEARNS and SHERWOOD, 1974]. One of the most interesting aspects of our studies to date has been a comparison of the distributions of diseased fish populations with the location of pollutant sources and the distribution of contaminants in the marine environment. It seems clear that the discharge of trace metals and chlorinated hydrocarbons in municipal wastewaters has been reflected in increased concentrations of the constituents in the sediments around the wastewater outfalls. This is particularly evident in the Palos Verdes area. Prior to 1971, the Los Angeles County discharge on the Palos Verdes shelf was a major point source of DDT and its breakdown products to the southern California coastal waters. Although the mass emission rate of total DDT from this source decreased by approximately 80% from 1971 to 1973, we estimate that there are still 200 metric tons of total DDT in the Palos Verdes sediments [McDERMOTT et at., 1974]. The concentration of total DDT in the sediment decreases in all directions from the Palos Verdes shelf, and these gradients are reflected in the muscle tissue of Dover sole (table I). Since the Palos
Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
Distribution of Tumor-Bearing Specimens
Ocean Wastewater Discharge
79
a
b
c
o
I
I
10 20
mm
Verdes effluent includes the greatest amount of industrial waste of any of the southern California municipal wastewater discharges, it is also high in trace elements, and these are distributed in the sediments in a similar pattern along the coast. However, even in areas of extreme sediment contamination, the metals are not concentrated in animal tissues by more than a factor of two over noncontaminated areas (table I) [DE GOEIJ et ai., 1974; Southern California Coastal Water Research Project, 1973]. In addition, much of the surface sediment immediately surrounding the Palos Verdes submarine outfalls is anaerobic, as indicated by the distribution of hydrogen sulfide in the surface layer [KALIL, 1973].
Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
Fig. 2. Typical tumor-bearing Dover sole: (a) specimen with angioepithelial nodule (arrow); (b) specimen with epidermal papilloma, and (c) specimen with highly pigmented tumor with poorly defined edges, characteristic of angioepithelial polyp.
5
0.66 (0.22-4.0) 17 110 (18-500) 11
2.2 (1.2-3.5) 4
0.91 (0.42-4.3) 6
12
0.04 (0.02-0.10) 9
15 (13-30) 4
2.6 (1.6--3.6) 2
0.21 (0.12-0.42) 9
100-m pipe
30.5 (14--72) 24
0.24 (0.05-0.56) 21
335
60-m pipe
Los Angeles City
12.0 (1.67-69.8) 22
1.9 (1.1-3.1) 12
145 (19-550) 22
26 (2.8-230) 19
371
Los Angeles County
19 (16--36) 5
21 (12-55) 34
0.43 (0.06-0.49) 11
2.0 (1.9-2.5) 4
0.008 (0.002-0.016) 11
90
San Diego City
0.07 (0.03-0.11) 13
130
Orange County
0.08 (0.05---0.12) 6
2.0 (1.4--3.0) 6
Santa Catalina Island (control)
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a
Data from Southern California Coastal Water Research Project [1973] (reorganized and, in some cases, updated), and McDERMOTT et al. [1974].
Flow, mgd Sediments Total DDT, mg/dry kg Median Range Number of samples Copper, mg/dry kg Median Range Number of samples Dover sole liver Copper, mg/wet kg Median Range Number of samples Dover sole muscle Total DDT, mg/wet kg Median Range Number of samples
Ventura County
Table I. Distribution of total DDT and copper in sediments around five major outfall systems, and in Dover sole collected near these systems, and from a control areaa
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Ocean Wastewater Discharge
81
Table II. Prevalence of epidermal tumors in Dover sole collected off the Palos Verdes Peninsula (135 samples) and in San Pedro Bay (64 samples), 1972-73 Fish size a , mmSL
Palos Verdes Peninsula
San Pedro Bay
number of fish
number of fish
tumor-bearing fish number
25 35 45 55 65 75 85 95 105 115 125 135 145 155 165 175 185 195 205 215 225 235 245 255 265 275 285 295 305 315 >315 Total
%
2
3 I 6 15 44 35 18 8 4 1 5
6.8 1.7
9.0 6.9 8.3 4.0 1.8 0.78 0.40 0.10 0.39
2
0.20
2
0.22
2 2 13,626
number
%
143
1.0
3 116 160 55 37 32 68 89 139 141 151 216 283 312 281 288 288 217 203 182 114 81 61 34 18 5 3 4 I 3 3,586
3 4 5 4 I 6
5.4 10.8 15.6 5.9 1.1 4.3
3 2
0.66 1.4 0.71
2
0.36
30
0.84
2
Midpoint of 10-mm size class. Downloaded by: Université de Paris 193.51.85.197 - 1/10/2020 1:58:11 AM
a
2 4 20 44 58 67 217 532 873 1,021 1,025 990 1,034 1,284 1,293 1,237 1,137 1,023 796 449 303 142 46 18 7 2
tumor-bearing fish
82
MEARNS/SHERWOOD
Table III. Prevalence of epidermal tumors in Dover sole collected off southern California, 1972-73 Palos Verdes Shelf
San Pedro Bay
Dana Point
Santa Catalina Island
Number of samples Number of samples containing Dover sole
60 39
144 106
73 44
42 25
18 11
Number of Dover sole Number with tumors Percent with tumors
516 9
14,277 147 1.0
3,842 33 0.86
593 0 0
89 0 0
Number of Dover sole 60-120 mm SL Number with tumors Percent with tumors
96
1,829
443
29
8
0 0
0 0
1.7
5 5.2
106 5.8
26 5.9
The overall incidence of tumor-bearing Dover sole in southern California trawl catches is low, approximately 1 %, and the species is most abundant on the Palos Verdes shelf. However, when sufficient numbers of individuals have been collected to allow comparison of prevalences in different areas, there appear to be no gradients in the distributions of tumor-bearing specimens. Of 13,626 Dover sole collected in 135 samples off Palos Verdes, l.O% were tumor bearing; of 3,586 Dover sole collected in 64 samples in San Pedro Bay, to the south, 0.84% had epidermal tumors (table II). Specimens in the 60- to l20-mm standard length (SL) size range, which corresponds to the size of individuals taken in the fall and winter months following metamorphosis and settling, appeared to be the most frequently affected in both areas. Prevalences of tumor-bearing Dover sole in this size range were similar in Santa Monica Bay (5.2%), off Palos Verdes (5.8%), and in San Pedro Bay (5.9%; table III). Since Dover sole and sampling effort are not evenly distributed along the coast, catches off Dana Point and Santa Catalina Island have produced too few small individuals to adequately compare prevalences in these areas. The distribution of tumor-bearing individuals differs distinctly from that seen for Dover sole with eroded fins, in which affected specimens are strongly concentrated on the Palos Verdes shelf [MEARNS and SHERWOOD, 1974]. In the vicinity of the Orange County outfall system, quarterly trawl sampling at a standard set of stations began in November 1969 (although
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Santa Monica Bay
Ocean Wastewater Discharge
83
1,200
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III
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0
0
4-
0
Ii;
.0
E :J z
I
1- Change
1,000 800
1 1
600
1 1
400
in discharge
site
1
200 0 16 ---120mm SL
0III
'"
14
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12
0
10
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01 C
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NFMADFMADFMANFMSN 1970
1971
1972
1973
Fig. 3. Prevalence of tumor-bearing Dover sole captured in the vicinity of the Orange County outfall system, 1969-73. The change from a 20- to 60-meter outfall occurred in April 1971. Data on length frequencies were not taken prior to December 1970.
size frequency data were not taken until December 1970). In April 1971, discharge through a short (20-meter) outfall was terminated, and a new outfall that discharges at 60 m - within the natural range of the Dover sole - was put into operation. The overall percentage of tumor-bearing Dover sole in the catches does not appear to be related to the change in discharge location (fig. 3).
Based on the data we have collected, we believe that the Dover sole skin tumor disease is not enhanced by the discharge of municipal waste in southern California and would not be reduced in overall incidence by projected improvements in waste treatment unless such changes affected the survival or recruitment of juvenile Dover sole. However, the disease may be associated
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Conclusions
MEARNS/SHERWOOD
84
with a very specific yet widely distributed agent that mayor may not be related to wastes produced by industrial development. We do believe that changes in waste treatment will affect the distribution of Dover sole with fin erosion, and that this disease, on a local scale, may be a most important sign of environmental damage. A comprehensive field program is an important part of any disease study, and sampling programs should be designed with the population characteristics of the affected species in mind: Sampling method, net mesh size, season, and depth range are important considerations in providing data for comparing different areas and for discovering correlations with potential causative agents.
Acknowledgments This work was supported in part by the Environmental Protection Agency under Grant R-801152. We are particularly indebted to Dr. B. MILLER, College of Fisheries, University of Washington, for a number of stimulating exchanges and for his assistance in formulating our research program. Special thanks are given to the Project staff, including M. J. ALLEN, J. WORD, and R. VOGLIN for their patient examination of several hundred thousand fishes.
GOEIJ, J.J.M. DE; GUINN, V.P.; YOUNG, D.R., and MEARNS, A.J.: Neutron activation analysis trace element studies of Dover sole liver and marine sediments; in Comparative studies of food and environmental contamination, pp. 189-200 (International Atomic Energy Agency, Vienna 1974). KALIL, E. K.: Rapid pore water analysis for sediments adjacent to reactor discharges. IAEA Symp. on Environmental Surveillance around Nuclear Installations, Warsaw 1973, lAEA-SM-180/37. McDERMOTT, D.J.; HEESEN, T.C., and YOUNG, D.R.: DDT in bottom sediments around five southern California outfall systems, Rept. TM 217 (So. Calif. Coastal Water Research Proj., EI Segundo 1974). MEARNS, A. J. and GREENE, C. S. (eds): A comparative trawl survey of three areas of heavy waste discharge, Rept. TM 215 (So. Calif. Coastal Water Research Proj., EI Segundo 1974). MEARNS, A. J. and SHERWOOD, M. J.: Environmental aspects of fin erosion and tumors in southern California Dover sole. Trans. Am. fish. Soc. 103: 799-810 (1974). RUSSELL, F.E. and KOTIN, P.: Squamous papilloma in the white croaker. J. natn. Cancer lnst. 18: 857-61 (1957).
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References
Ocean Wastewater Discharge
85
Dr. A.J. MEARNS, Senior Environmental Specialist, Southern California Coastal Water Research Project, 1500 East Imperial Highway, El Segundo, CA 90245 (USA)
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SHERWOOD, M. J. and MEARNS, A. J.: Disease responses in southern California coastal fishes. Naval Undersea Center Conf., San Clemente (in press). Southern California Coastal Water Research Project: The ecology of the Southern California Bight: Implications for water quality management. Rept. TR 104 (So. Calif. Coastal Water Research Proj., El Segundo 1973). US Congress, House Subcommittee on Fisheries and Wildlife Conservation: Water pollution, fish disease, and human health, hearing of 30 April 1970; in Fish and wildlife legislation, part 3, Rept. 91-42, 91st Congr., pp. 351-409 (US Govt. Printing Office, Washington 1971). VALENTINE, D. W. and BRIDGES, K. W.: High incidence of deformities in the serranid fish Paralabrax nebulifer from southern California. Copeia iii: 637-8 (1969). VALENTINE, D. W. and SouLE, M. E.: Effect of p,p' -DDT on developmental stability of pectoral fin rays in the grunion, Leuresthes tenuis. Fishery Bull. 71: 921-6 (1973). VALENTINE, D. W.; SouLE, M. E., and SAMOLLOW, P.: Asymmetry analysis in fishes: A possible statistical indicator of environmental stress. Fishery Bull. 71: 357-70 (1973). WELLINGS, S. R.; CHUINARD, R. G., and BENS, M.: A comparative study of skin neoplasms in four species of pleuronectid fishes. Ann. N. Y. Acad. Sci. 126: 479-501 (1965). YOUNG, P. H.: Some effects of sewer effluent on marine life. Calif. Fish Game 50: 33-41 (1964).
