NOAA Technical Report NMFS 37

A Histopathologic Evaluation

of Gross Lesions Excised

from Commercially Important

North Atlantic Marine Fishes

Robert A. Murchelano

Linda Despres-Patanjo

John Ziskowski

March 1986

U.S. DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

National Marine Fisheries Service
NOAA TECHNICAL REPORT NMFS

The major responsibilities of the National Marine Fisheri« Service (NMFSI are to monitor and assess the abundance and geographic distribution of fishery resources, to

understand and predict fluctuations in the quantity and distribution of these resources, and to establish levels for their optimum use. NMFS is also charged with the development

and implementation of policies for managing national fishing ~rounds, development and enforcement of domestic fisheries regulations, surveillance of foreign fishing off United

States coastal waters, and the development and entarcemem of international fishery agreements and policies. NMFS also ass,st; the fishing industry through marketing service

and economic analysis programs, and mortgage insurance and vessel construction subsidie,. It collects, analyzes, and publishes statistics on various phases of the industry.

The NOAA Technical Repon NMFS series was established in 1983 to replace two subcategories of the Technical Repons series: "Special Scientific Repon-Fisheries" and

"Circular." The series contains the following types of repons' Scientific investigations that document long-term continuing programs of NMFS; intensive scientific repons on

studies of restricted scope; papers on applied fishery problems; technical reports of general interest intended to aid conservation and management; repons that review in considerable detail and at a high technical level certain broad areas of research; and technical papers originating in economics studies and from managemem investigations. Since

this is a formal series, all submitted papers receive peer review and those accepted receive professional editIng before publicatinn.

Copies of NOAA Technical Reports NMFS are available free in limited numbers to governmental agencies, both Federal and State. They are also available in exchange for

other scientific and technical publications in the marine sciences. Individual copies may be obtained from: U.S. Depanment of Commerce, National Technical Information Service,

5285 Pon Royal Road, Springfield, VA 22161.

I. Synopsis of biological data on the Blue Crab, Callineeles sapidus Rathbun, by

Mark R. Millikin and Austin B. Williams. March 1984, 39 p.

2. Development of hexagrammids (Pisces: Scorpaeniformes) in the Nonheastern

Pacific Ocean, by Anhur W. Kendall, Jr., and Beverly Vinter. March 1984, 44 p.

3. Configurations and relative efficiencies of shrimp trawls employed in southeastern

United States waters, by John W. Watson, Jr., Ian K. Workman, Charles W. Taylor,

and Anthony F. Serra. March 1984, 12 p.

4. Management of nonhern fur seals on the Pribilof Islands, Alaska, 1786-1981, by

Alton Y. Roppel. April 1984, 26 p.

5. Net phytoplankton and zooplankton in the New York Bight, January 1976 to

February 1978, with comments on the effects of wind, Gulf Stream eddies, and slope

water intrusions, by Daniel E. Smith and Jack W. Jossi. May 1984, 41 p.

6. Ichthyoplankton survey of the estuarine and inshore waters of the Florida Everglades, May 1971 to February 1972, by L. Alan Collins, and John H. Finucane. July

1984, 75 p.

7. The feeding ecology ofsome lOoplankters that are important prey items of larval

fish, by Jefferson T. Turner. July 1984, 28 p.

8. Proceedings of the International Workshop on Age Determination of Oceanic

Pelagic Fishes: Tunas, Billfishes, and Sharks, by Eric D. Prince (convener and editor),

and Lynn M. Pulos (editor). December 1983, 211 p.

9. Sampling statistics in the Atlantic menhaden fishery, by Alexander J. Chester.

August 1984, 16 p.

10. Proceedings of the Seventh U.S.-Japan Meeting on Aquaculture, Marine Finfish

Culture, Tokyo, Japan, October 3-4, 1978, by Carl 1. Sinderrnann (editor). August 1984,

31 p.

II. Taxonomy of Nonh American fish Eimeriidae, by Steve J. Upton. David W.

Reduker, William L. Current, and Donald W. Duszynski. August 1984 18 p.

12. Soviet-American Cooperative Research un Marine Mammals. Volume I-Pinnipeds, by Francis H. Fay, and Gennadii A. Fedoseev (editors). September 1984, 104 p.

13. Guidelines for reducing porpoise mortality in tuna purse seining, by James M.

Coe, David B. Holts, and Richard W. Butler. September 1984, 16 p.

14. Synopsis of biological data on shonnosc sturgeon, Acipenser breviroslrum leSueur

1818, by Michael 1. Dadswell, Bruce D. lilUbert, Thomas S. Squiers, Donald Marchette, and Jack Buckley. October 1984, 45 p.

15. Chaetognatha of the Caribbean sea and adjacent areas, by Harding B. Michel.

October 1984, 33 p.

16. Proceedings of the Ninth and Tenth U.S.-Japan Meetings on Aquaculture, by Car:

1. Sindermann (editor). November 1984, 92 p.

17. Identification and estimation of size from the beaks of 18 species of cephalopods

from the Pacific Ocean, by Gary A. Wolff. November 1984, 50 p.

18. A temporal and spatial study of invertebrate communities associated with hardbottom habitats in the South Atlantic Bight, by E. L. Wenner, P. Hinde, D. M. Knott,

and R. F. Van Dolah. November 1984, 104 p.

19. Synopsis of biological data on spottail finfish, Dip/odus ho/brooki (Pisces:

Sparidae), by George H. Darcy. January 1985, II p.

20. Ichthyoplankton of the Continental Shelf near Kodiak Island, Alaska, by Arthur

W. Kendall, Jr., and Jean R. Dunn. January 1985, 89 p.

21. ,"nnotated bibliography on hypoxia and its effects on marine life, with emphasis

on the Gulf of Mexico. by Maurice L. Renaud. February 1985, 9 p.

22. Congrid eels of the eastern Pacific and key to their Leptocephali, by Solomon

N. Raju. February 1985, 19 p.

23. Synopsis of biological data on the pinfish, wgodon rhomboides (Pisces:Sparidae),

by George H. Darcy. February 1985, 32 p.

24. Temperature conditions in the cold poel 1977-81: A comparison between southern

New England and New York transects, by Steven K. Cook. February 1985, 22 p.

25. Parasitology and pathology of marine organisms of the world ocean, by William

1. Hargis, Jr. (editor). March 1985, 135 p.

26. Synopsis of biological data on the sand perch, Dip/eelrum !ormosum (Pisces:

Serranidae), by George H. Darcy. March 1985, 21 p.

27. Proceedings of the Eleventh U.S.-Japan Meeting on Aquaculture, Salmon Enhancement, Tokyo, Japan, October 19-20, IQ82, by Carl 1. Sindertnann (editor). March 1985.

102 p.

28. Rev,ew of geographical <tocks of tropical dolphins \Slenella spp. and Delphillus

de/phis) in the eastern Pacific, by Willidm F. Perrin. Michael D. Scott. G. Jay Walker,

and Virginia L. Ca" March 1985. 28 p.

29. Prevalence. intensuy, long~vity. :.md persistence of Anisukis sp. larvae and WU5-

torhynchus lenuis metacestode' In San Francisco striped bass, by Mike Moser, Judy

A. Sakanari, Carol A Reilly, and Jeannette Whipple. April 1985, 4 p.

30. Synopsis of biological data on the pink shrimp. Panda/us borealis Kr6yer, 1~38,

by Sandra E. Shumway, Herben C Perkins, Daniel F Schick, and Alden P. Stickney.

May 1985, 57 p.

31. Shark catches from selected fisheries off the U.S. cast coast. by Emory D. Anderson. John G. Casey. John 1. H,'ey. and W. N. Witzell. July 1985, 22 p.

32. Nutrient Distributions for Georges Bank and adjacent waters in 1979. by A. F

1. Draxler, A. Mattc, R. Waldhauer. and 1. E. O'Reilly. July 1985, 34 p.

33. Marine Ilora and launa of the Northeastern Umted States. Echinodermata:

Echinoidea, by D. Keith Serafy and F. Jul'an Fell. September 1985, 27 p.

34. Additions to a revision of the shark genus Carehorhillus: Synonymy of Aprionudon and Hypopriun, and descnption of a new species of Careharhillus \Carcharhinidae),

by 1. A. F. Garrick. November 1985. 26 p.

35. Synoptic review of the literature on the Southern oyster drill Thais haemasloma

jluriJ<lna, by Philip A. Butler. November 1985. 9 p.
NOAA Technical Report NMFS 37

A Histopathologic Evaluation

of Gross Lesions Excised

from Commercially Important

North Altantic Marine Fishes

Robert A. Murchelano

Linda Despres-Patanjo

John Ziskowski

March 1986

U.S. DEPARTMENT OF COMMERCE

Malcolm Baldrige, Secretary

National Oceanic and Atmostpheric Administration

John V. Byrne, Administrator

National Marine Fisheries Service

William G. Gordon, Assistant Administrator for Fisheries
The National Marine Fisheries Service (NMFS) does not approve, recommend or endorse any proprietary product or proprietary material mentioned in this publication. No reference shall be made to NMFS, or to this

publication furnished by NMFS, in any advertising or sales promotion

which would indicate or imply that NMFS approves, recommends or

endorses any proprietary product or proprietary material mentioned herein,

or which has as its purpose an intent to cause directly or indirectly the

advertised product to be used or purchased because of this NMFS

publication.

ii
Contents

Introduction 1

Materials and Methods 1

Results 1

Lesions of Western North Atlantic Fishes 3

Integument 3

Gill 3

Gastrointestinal tract 4

Gonad 5

Heart 5

Liver 5

Spleen 6

Muscle 6

Miscellaneous 7

Lesions of Eastern North Atlantic Fishes 8

Integument 8

Gill 8

Gastrointestinal tract 8

Heart 8

Kidney 8

Liver 9

Spleen 9

Muscle 9

Miscellaneous 9

Discussion 9

Acknowledgments 14

Literature cited 14

iii

A Histopathologic

Evaluation of Gross Lesions

Excised from Commercially

Important North Atlantic

Marine Fishes

ROBERT A. MURCHELANO

Nonheast Fisheries Center,

National Marine Fisheries Service, NOAA,

Oxford, Maryland 21654

LINDA DESPRES-PATANJO

Nonheast Fisheries Center,

National Marine Fisheries Service, NOAA,

Woods Hole, Massachusetts 02543

JOHN ZISKOWSKI

Nonheast Fisheries Center,

National Marine Fisheries Service, NOAA,

Highlands, New Jersey (Jl732

ABSTRACf

Histopathologic studies of lesions found in commercially important North Atlantic marine fishes are uncommon. As part of a comprehensive Northeast Fisheries

Center program ("Ocean Pulse") to evaluate environmental and resource health

on the U.S. Continental Shelf from Cape Hatteras to Nova Scotia, grossly visible

lesions of the gills, integument, muscle, and viscera of primarily bottom-dwelling

fIShes were excised and examined using light microscopy.

Several gadid and pleuronectid fIShes accounted for most of the lesions

observed. Most pathological examinations were incidental to samples taken for

age and growth determination and evaluation of predator/prey relationships.

Several gadids, with either gill, heart, or spleen lesions, were sampled more

intensively.

Gill lesions principally affected gadids and were caused by either microsporidans or an unidentified oocyte-like cell. The majority of gastrointestinal

lesions consisted of encapsulated or encysted larval worms or mlcrosporidaninduced cysts. Few heart lesions were found. Integumentallesioos included ulcers,

Iymphocystis, and trematode metacercariae. Liver lesions almost always consisted

of encapsulated or encysted larval helminths. Necrotic granulomata were seen in

muscle and microsporidan-induced granulomata in spleen.

Although not numerous, histologically interesting lesions were noted in

integument, heart, liver, spleen, and muscle ofseveral fISh species. Histologic study

of tissues excised from a variety of demersal and pelagic fishes from the eastern

North Atlantic (France, Germany, Spain) revealed assorted integumental, renal,

hepatic, and splenic lesions.

Small sample size and non-random sampling precluded obtaining a meaningful quantitative estimate of the prevalence ofthe observed lesions in the population at risk; however, a useful census has been made of the types of lesions present

in commercially important marine fIShes.

INTRODUCTION _

Much attention has been given recently to the health status of

commercially important marine fishes. Although several pollutionassociated diseases have been identified (Sindermann 1979; Sindermann et al. 1980; Murchelano 1982), statistical analyses and

laboratory experimentation to corroborate the validity of field observations often are lacking or inconclusive. Despite these limitations, identification of the diseases present in the population at risk

is necessary before baselines can be established to assess future

changes. Surveys of fish disease prevalence, supplemented with

simultaneous environmental studies, may yield useful data. Incidental

to the conduct of seasonal stock assessment surveys in the western

North Atlantic from Cape Hatteras to Nova Scotia, grossly visible

integumental, respiratory, and visceral lesions were excised for

laboratory study. The histopathology of these lesions and of others

from fishes sampled in the eastern North Atlantic are the subject

of this report.

MATERIALS AND METHODS _

Randomly selected stations in depth-defined strata are sampled biannually (spring, fall) on the U.S. Continental Shelf between Cape

Hatteras and Nova Scotia to determine fish abundance and distribution. Research vessels (Albatross W, Delaware II) make 3Q-min tows

at each station using a standard No. 36 Yankee otter trawl. After

sorting and weighing the catch, requisite examinations are made to

provide data on species composition and abundance, age and growth,

fecundity, maturity, and food habits. From 1979 to 1982, fishes

sampled for age, growth, and food habit studies were also examined

for the presence of gross gill, integumental, muscle, and visceral

lesions. Biologists were asked to excise lesions from organs which

deviated distinctly from the norm in color, configuration, and size.

Prior to sampling they were advised to necropsy 10-15 fishes of a

given species to determine normal organ variability. Lesions were

excised as time permitted. Although this method was practically expedient, there can be little doubt that, eventually, sampling emphasized the excision of cysts, nodules, and other grossly recognizable

anatomic modifications ("lumps and bumps"). A total of 350 lesions

were excised and fixed in 10% seawater formalin in appropriate containers. At the laboratory, tissues were routinely dehydrated, embedded in paraffin, sectioned (N 6I-lm), and stained (hematoxylin

and eosin-H&E; azure eosin-AZE; periodic acid Schiff-PAS;

Ziehl-Neelsen-ZN; Feulgen; Grocott).

In 1979, 1980, and 1982, tissues with lesions were obtained from

fishes from the German Bight and North Sea, the Atlantic coasts

of France and Spain, and the English Channel. These tissues were

obtained on cruises conducted specifically to estimate fish disease

prevalence. The tissues were prepared for microscopic examination

as described above.

RESULTS _

Altogether, 416 lesions were examined microscopically-350 from

fishes of the western North Atlantic and 66 from fishes from the

eastern North Atlantic. Tables I and 2 list the fish species examined

and the number of lesions excised from particular tissues.
Table I.-Number of grossly visible lesions excised from fish of the western North Atlantic, sampled on stock assessment

cruises in 1979-82.

Fish

examined No. lesions

(N=350) Gill Gonad Gut Heart Integument Liver Muscle Spleen Misc. Total

American plaice (9) 7 2 9

(Hippoglossoides pla/essoides)

Cod (107) 23 II 19 20 10 4 31 2 121

(Gadus morhUll)

Cusk (2) 2 2

(Brosme brosme)

Goosefish (4) 2 4

(Lophius americanus)

Haddock (36) 18 5 3 3 6 36

(Melanograrnrrws aeglefinus)

Mackerel (4) 3 4

(Scomber scombrus)

Ocean pout (7) 5 2 7

(Macrozoarces americanus)

Pollack (11) 2 5 II

(Pollachius virens)

Redfish (3) 3

(Sebas/es marinus)

Red hake (28) 18 2 4 4 28

(Urophycis chuss)

Silver hake (32) 20 2 5 2 30

(Merluccius bilinearis)

White hake (26) II 7 4 2 26

(Urophycis /enuis)

Windowpane (8) 4 3 8

(Scophthalmus aquosus)

Wmter flounder (40) 15 21 40

(Pseutlapleuronec/es

americanus)

Yellowtail flounder (33) 12 8 12 33

(limanda ferruginea)

Total 94 5 61 19 76 42 20 32 13

Table 2.-Number of grossly visible lesions excised from fISh of the eastern North Atlantic, sampled on cruises in 1979,

198O, and 1982.

Fish

examined No. lesions

(N=66) Gill Gonad Gut Heart Integument Kidney Liver Muscle Spleen Misc. Total

Blue whiting (8) 6 4 10

(Gadus poutassou)

Cod (10) 4 4 2 7 21

(Micromesis/ius poutassou)

Dab (12) 10 12

(limanda limanda)

Flounder (7) 6 7

(Platich/hys flesus)

Goosefish (8) 8 8

(Lophius pisca/orius)

Mackerel (16) 6 3 4 8 23

(Scomber scombrus)

Whiting (5) 2 3 6

(Merluccius merluccius)

All 10 2 8 17 7 15 4 15 8

2
Lesions of Western North Atlantic Fishes

Integument-Integumental lesions accounted for 21 % of the gross

abnormalities observed, and ulcers and Iymphocystis for 44% and

20%, respectively, of the skin lesions. More ulcers were found in

cod (Gadus morhua) than in any other species. Ulcers were of varying size and either solitary or multiple. Histologically, their appearance was similar in all species. Epidermis contiguous to the ulcer

tended to be hyperplastic and spongiotic. In the dermis, scales were

either degenerate or not present, and scale pockets were edematous.

Areas of granulomatous inflammation extended from the dermis to

the hypodermis and at times into subjacent muscle. Inflammatory

tissues contained congested blood vessels as well as frank hemorrhage. Bacteria were sometimes present (usually topically). When

adjacent muscle was affected, the fibers were either atrophic or

necrotic, and leukocytic inftltrates were present. Ulcers with large

areas of fibrous tissue were presumed to be resolving.

Lymphocystis was found only in American plaice (Hippoglossoides

platessoides) and winter flounder (Pseudopleuronectes americanus).

Lymphocystis lesions were evident as foci of hypertrophied cells

containing Feulgen-positive (Fig. 1), fmely granular, basophilic, intracytoplasmic inclusions. Cell nuclei were either karyorrhectic or

not present. Frequently, the enlarged cells were bordered by erythrocyte cuffs. The dermis was fibrotic and contained infiltrates of

mononuclear leukocytes and areas of hemorrhage. The covering

epidermis usually was markedly hyperplastic. "X" cell lesions were

found in the dermis of two ocean pout (Macrozoarces americanus)

(Fig. 2). Histologically, they consisted of masses of "X" cells

separated by connective tissue trabeculae. The lesions' microscopic

appearance was similar to that of cod pseudobranch adenomas

(Wellings 1969; Lange 1973).

Gill-In the fishes examined from the western North Atlantic, gill

lesions were most numerous and accounted for 26% of the abnormalities noted. In 44%of the gill lesions, the causative agent could

not be identified but consisted of a large oocyte-like cell occupying

the intralamellar space (Fig. 3). The cell was clearly demarcated

by a well-defined PAS-negative wall. Proliferation of fibrous tissue

around the cell in some instances caused lamellar fusion. The fibrous

tissue contained small, well-defined blood vessels as well as large,

blood-filled lacunae. Examination of AZE, Grocott, and Feulgenstained sections was not informative. The oocyte-like cell was noted

in gill tissues of cod, haddock (Melanogrammus aeglefinus), red

hake (Urophycis chuss), silver hake (Merluccius bilinearis), and

white hake (Urophycis tenuis). The second most common gill lesion noted was caused by microsporidans (17 %) and found only in

cod and haddock (Morrison and Sprague 1981) (Fig. 4). Interlamellar

cysts were well-defined and, other than the elaboration of a connective tissue capsule, caused no appreciable host response. The

only other grossly evident gill lesions were found in cod. In six fish

(6%) with severely eroded gills, histologic changes included

epithelial hyperplasia, necrosis, and mononuclear infiltration, congestion, and hemorrhage. Denuded gill filaments were colonized

by an abundant and morphologically diverse bacterial flora. Blood

vessels in the affected areas contained numerous mononuclear

leukocytes. Macrophages were present in necrotic tissue areas. Four

of the gills were colonized by microsporidans. All eroded gills contained chitinous tissue fragments which probably were crustacean

in origin. It is likely, dlerefore, that the lesions observed were caused

by parasitic copepods. The only other lesion noted on cod was a

pseudobranch adenoma. At present, the primary constituent cell

("X" cell) of this tumorous mass is believed to be amebic (Dawe

et al. 1979; Dawe 1981). Gill lesions incidentally noted (those not

associated with an obvious gross lesion) included chronic, nonspecific, granulomatous inflammation (cod, haddock, white hake),

and ones caused by Trichodina (cod), Oodinium (cod), and encysted

trematode metacercariae (white hake). In many instances (23%),

grossly visible nodular lesions on gills (cysts, nodules), because of

their small size and solitary occurrence, did not survive the

preparative procedures required for microscopic examination.

3

Figure I.-Hypertrophic fibroblasts characteristic of

Iymphocystis containing viral inclusions in scale

pocket of American plaice (H&E, x 200).
Figure 2.-Cord containing "X" cells in dermis of

ocean pout (H&E, x 200).

Figure 3.-Unidentilied oocyte-like cell in gill of cod

(H&E, x lOll).

Gastrointestinal tract-There were 61 gastrointestinal tract lesions,

of which 25 (4 %) were caused by encysted larval cestodes. Thirtythree percent of the cestode cysts were found in yellowtail flounder

(limandaferruginea). Other fishes with larval cestode cysts included

cod (3), haddock (3), mackerel (Scomber scombrus) (2), red hake

(I), silver hake (I), white hake (2), windowpane flounder (Scophthalmus aquosus) (3), and winter flounder (I). In several instances,

sections disclosed obvious cystic structures which lacked worms.

Larval cestodes in the serosa of the digestive tract caused essentially no host response other than the elaboration of a thin capsule.

However, some cestodes in the muscularis of the gut caused extensive inflammation and muscle necrosis. Most ofthe cellular infiltrate

4

consisted of mononuclear leukocytes, macrophages, and occasionally

eosinophiles. The worms eliciting this response did not always appear to be dead. Ten lesions (16 %) of the gastrointestinal tract were

caused by microsporidans (Glugea stephani) (Fig. 5), all found in

the intestinal tract of the winter flounder. The number and size of

the cysts varied extensively. Cysts were located either in the serosa

or in the muscularis-and, when numerous, were enclosed in a fibrous,

connective tissue matrix. Intramuscular cysts caused substantial compression of the subjacent mucosa and in rare instances appeared to

cause mucosal ulceration. The submucosa frequently contained

leukocyte infiltrates.
FIgure 4.-Mlcrosporldan (Loma mom",,) cysts in gill

or cod (II&E, x 200).

Figure 5.-Microsporldan cyst (Glugea stepluuu) in intestinal wall or winter Oounder (II&E, x 100).

Gonad-Five gonadal abnormalities were noted grossly (cod, silver

and white hake, windowpane flounder); however, only one could

be substantiated microscopically. Encysted larval cestodes and

nematodes were present on the gonadal surface of a silver hake.

No conspicuous host response was apparent.

Heart-The 19 heart lesions (5%) were found exclusively in cod;

all were caused by microsporida and were located in the epicardium and/or myocardium (atrium and ventricle). Discrete granulomata composed of epithelioid cells and fibroblasts enclosed the spore

aggregates (Fig. 6). Early lesions exhibited no host response and

consisted of only a parasitic mass (either free or membrane bound).

5

Other lesions were infIltrated by mononuclear leukocytes, causing

a focal myocarditis. A diffuse epicarditis with infIltrates of mononuclear leukocytes was present in some tissues. Lesions in atrial

tissues caused hyperplasia and hypertrophy of endothelial

macrophages.

Liver-As was true with the gastrointestinal tract, lesions of the

liver were usually associated with encysted larval cestodes or nematodes. Cysts were found in cod, haddock, pollack (Pollachius virens),

red hake, silver hake, white hake, goosefish (Lophius americanus),

winter flounder, and yellowtail flounder, and accounted for 31%of

the liver lesions examined. Larval worms (cestodes, nematodes) were
Figure 6.-Granuloma containing microsporidan

(Loma morhua) in ventricle of cod heart (H&E, x

200).

found both on the surface of the liver and deep within its parenchyma. Some encysted worms caused only space-occupying lesions

with little apparent host response; others were isolated by a laminar,

fibrous capsule. In some instances, epithelioid cells were also present. Dead and degenerate worms provoked a host response involving

mononuclear and polymorphonuclear leukocytes, macrophages, and

fibroblasts. "Empty" cysts containing eosinophilic debris, red blood

cells, and occasionally bacteria in tissues with visible worms were

also presumed to be worm-induced. Hepatic lesions due to worms

rarely involved substantial amounts of liver parenchyma. Although

focal areas of necrosis and fibrosis were seen in many sections, large

necrotic and fibrotic areas were rarely seen. Liver lesions caused

by microsporidans were noted in cod, winter flounder, and yellowtail flounder. Multiple parasitic aggregates (presumably Lorna

morhua), some free and others clearly within a thin, fibrous capsule, were noted in cod. In one section, encysted parasites were also

visible in the lumen of a large hepatic vein (Fig. 7). The cysts were

bordered by a fibrous capsule which, in the winter flounder, had

distinct collagenous layers. The winter flounder lesions were extensive and caused much structural change to the parenchyma.

Hepatic cords were disorganized, separated by wide clefts, and composed of hepatocytes of varying size. Some cysts were necrotic and

infiltrated by leukocytes and macrophages.

Spleen-Almost all the splenic lesions examined were from cod,

and 68% were caused by microsporidans (presumably Lorna

morhua). Microsporidan cysts in the splenic capsule were bordered

by an inner, dense, laminar, fibrous capsule and an outer, loose,

fibrous layer infiltrated by mononuclear leukocytes. When multiple cysts were present, the splenic capsule was hyperplastic and also

infiltrated by leukocytes. The splenic parenchyma appeared laden

with melanin, especially immediately adjacent to small blood vessels;

however, melanin-macrophage centers were not numerous. Larger

blood vessels contained disproportionate numbers of leukocytes for

the number of red blood cells present. Parenchymal cysts varied in

their appearance. Small cysts were frequently bordered by splenic

6

cells that had pycnotic and karyorrhectic nuclei. Splenic parenchymal

cells adjacent to some small cysts were lysed, leaving a clear area

around the parasitic mass. In other cysts, a leukocyte infiltrate was

present adjacent to the residual necrotic area proximal to the cyst

wall. Mature granulomata with distinct fibrous and epithelioid cell

types were also present.

Muscle-The most frequently observed muscle lesion was chronic

inflammation (55 %). Affected fishes included cod, haddock,

pollack, redfish (Sebastes rnarinus), and white hake. No two lesions

were exactly the same in appearance; however, all shared some common attributes. Some of the lesions were comprised of distinct

granulomata, others were more diffuse and indistinct. Affected

muscle was atrophic and necrotic. When granulomata were present,

they consisted of epithelioid cells and fibroblasts. A central necrotic

area contained amorphous, eosinophilic cellular debris and proteinaceous material. Adjacent muscle was infJltrated by leukocytes

and had focal and diffuse areas of hemorrhage. Parasites were never

seen; however, the redfish lesions contained chitin fragments, suggesting copepod parasitism. One lesion (haddock) also contained

abundant, small, rod-shaped bacteria. Microsporidan-induced lesions were found in American plaice and ocean pout. The plaice

lesion consisted of a small cyst filled with rnicrosporidan pansporoblasts. The perimeter of the cyst had a thin, irregular, fibrous layer

infiltrated by dense accumulations of mononuclear leukocytes.

Leukocytes were also present in the interior of the cyst. Adjacent

muscle appeared normal. The ocean pout lesion consisted of innumerable cysts containing rnicrosporidan pansporoblasts and spores.

Individual cysts were bordered by a dense, laminar, fibrous capsule

and epithelioid cells. Fibrous tissue was present around some cysts

and was the connecting matrix which joined all cysts. In some areas

the connective tissue lattice contained plasmodial stages of the

parasite. No muscle tissue was present in the parasitic mass. At the

perimeter, however, necrotic muscle was infiltrated by leukocytes.

Resting spores of lchthyophonus were seen in a lesion involving dermis and muscle in a cusk (Brosme brosme) (Fig. 8). The epithelium
Figure 7.-Microsporidan cyst (Loma morhua) in

lumen of hepatic vein of cod (H&E, x 200).

Figure 8.-Granulomatous inflammation around lehthyophonus spores in dermis of cusk (H&E, x 200).

over the affected area was hyperplastic and spongiotic. Melanophores

normally present beneath the basal lamina in the dennis were absent.

The stratum spongiosum was necrotic and contained abundant mononuclear and polymorphonuclear leukocytes, pigment-laden macrophages, and fibroblasts. Blood vessels were congested and there were

areas of hemorrhage. Resting spores were located in an area of

granulomatous inflammation at the junction of the hypodermis and

muscle. Muscle fibers were atrophic, necrotic, and infiltrated by

leukocytes and fibroblasts. Congested blood vessels and hemorrhage

were also present. Two neoplasms were found in muscle-one in

a haddock and one in a silver hake (Fig. 9). Although both lesions

were conservatively identified as fibromas, their aggressive lateral

7

expansion suggested that they could be fibrosarcomas. Constituent

cells had indistinct cell membranes and were organized in whorls,

palisades, and random arrays, often interfacing abruptly. Vesicular

nuclei had one nucleolus and differed substantially in size. Mitotic

activity was not detectable.

Miscellaneous-Grossly visible lesions were noted in nerve

(goosefish), mesenteric (silver hake, yellowtail flounder), and swim

bladder (haddock) tissues. Microscopic examination of the swim

bladder tissues disclosed no obvious lesions. The nerve tissues from

the goosefish contained numerous microsporidan cysts; host response

was minimal and consisted of fibroplasia in the area adjacent to the
Figure 9.-Flbroma in silver bake demm. Tumor bas

inf"JItrated muscle (H&E, x 200).

cysts. The mesenteric nodules contained larval cestodes and nematodes and evoked essentially no host response. Thbles 3 and 4 present

the frequency of occurrence of unicellular and metazoan parasites

and nonspecific histologic lesions observed in tissues from western

North Atlantic fishes.

Lesions of Eastern North Atlantic Fishes

Integument-Integumental lesions were most numerous and accounted for 24% of the abnormalities noted; they occurred in cod

(Micromesistius poutassou) (1), dab (10), and flounder (Platichthys

flesus) (6). All the flounder lesions consisted of lymphocystis. The

dab lesions were heterogeneous and consisted of epidermal papilloma

(2), "X" cell-induced inflammation (2), and one each of chronic

inflammation, epidermal hyperplasia, hypermelanization, larval

trematodes, lymphocystis, and ulceration. The "X" cell lesions (Fig.

10) differed somewhat from those in U.S. west coast flatfishes. The

most conspicuous aspect ofthese lesions was the extensive infIltrate

of mononuclear leukocytes around clusters and cords of "X" cells.

The "X" cells themselves appeared to be similar to those seen in

other fishes with comparable tumors (cod, goby, ocean pout, and

several flatfish species). The dab lesions extended into adjacent

muscle fascia resulting in considerable myolysis. Necrotic fibers were

abundant and interfibrillar spaces were infIltrated by mononuclear

leukocytes and macrophages. The lesions appeared to be well

vascularized; many vessels were congested and many areas contained

hemorrhage. The epidermal papillomas were typical in appearance

and consisted of a hyperplastic, folded epidermis supported by a

fibrous stroma (Fig. 11). The epidermis was spongiotic in some areas

and infiltrated by eosinophilic granule cells (EGC). The EGC ranged

from the basal lamina to the mucous cell layer. Some mononuclear

leukocytes were also present. The fish exhibiting "hypermelanization" grossly exhibited a dark, green/black coloration. Microscopically, there were focal aggregates of melanin in the dermis just

8

below the basal lamina. In some areas, mononuclear leukocytes were

dispersed around the melanin; this was particularly evident in scale

pockets.

Gill-Gill lesions excised from fishes from the eastern North Atlantic

were most numerous in blue whiting (Gadus poutassou). Two of

the six lesions noted consisted of the oocyte-like cell seen in gadid

fishes from the western North Atlantic; the remaining four nodular

gill lesions were not visible subsequent to sectioning.

Gastrointestinal tract-One of the two gastrointestinal tract lesions

was microsporidan-induced (dab, Limanda limanda) and the other

a consequence of a coinfection of acid-fast bacteria and coccidia

(mackerel, Scomber scombrus). In the latter lesion, multiple granulomata were present in mesenteric tissue ofthe pyloric caeca. Most

ofthe granulomata were centrally necrotic; however, some contained

presumptive mycobacteria and coccidian oocysts.

Heart-Six of the eight heart lesions were from mackerel. In all

instances, these lesions were characterized grossly as cysts. Two

of the six contained inflammatory foci (endocarditis, epicarditis)

but no visible cysts. Another contained focal aggregates of small

microsporidans located between cardiac muscle fibers; there was

no host response. One heart contained multiple granulomata in which

there were resting and germinating spores of Ichthyophonus. No

microscopic lesions could be found in the two remaining mackerel

heart tissues.

Kidney-Seven lesions were noted in kidney tissues-four in cod

and three in mackerel; all consisted of granulomatous inflammation. No organisms were visible in the cod kidneys. Granulomata

in one of the mackerel kidneys contained acid-fast bacteria and coccidian oocysts (presumably Mycobacterium and Eimeria, respectively); in another kidney they contained resting and germinating

spores of Ichthyophonus. No organisms were visible in the

granulomata of the third kidney lesion.
Table 3.-Frequency of occurrence of unicellular and metazoan parasites observed in tissues of fishes

from the western North Atlantic.

No. parasites (N=151)

P'Jrasite Gill Gonad Gut Heart Integument Liver Muscle Spleen Misc. ------

Microbial, Protozoan

Lymphocystis 15

/chthyophonus

Trichodino

Oodinium

Glugea 10 2

Lama 16 U 21

Nosema Nerve 2

Pleistophora 3

Unicapsula

Metazoan

Cestodes 25 7

Nematodes 4 6

Trematodes 2 1 15

Unidentified

"X" cell 4 2

OLC 41

Table 4.-Frequency of occurrence of histologic lesions not associated with microscopically visible parasites observed in tissues of fishes from the western North

Atlantic.

No. lesions (N=76)

InteguType of lesion Gill Gonad Gut Hearl ment Liver Muscle Spleen

Hyperplastic

Biliary

Epidermal 2

Papilloma I

Inflammatory

Chronic 4 7 2 II

Necrotic

Focal

Ulceration 7 33

Neoplastic

Fibroma 2

Liver-Liver lesions were noted in 15 fishes-blue whiting, cod,

mackerel, and whiting (Merluccius merluccius). All five lesions in

whiting were recognized grossly as cysts and contained larval

nematodes when examined microscopically. Lesions described as

nodules in cod (4) and mackerel (4) consisted of granulomatous inflammatory tissue. No organisms were visible in any of the four

cod liver tissues. In one of the four mackerel livers, granulomata

contained both acid-fast bacteria and coccidia. Another mackerel

liver contained numerous microsporidan cysts. The cysts had a PASpositive wall and were bordered by concentric layers of fibrous tissue

which had been infiltrated by mononuclear leukocytes. Focal hemorrhage also was present in some areas.

Spleen-Fifteen splenic lesions were noted-seven in cod and eight

in mackerel; all were typified by chronic inflammation in either capsule or parenchyma. Granulomata in one cod lesion contained acidfast bacteria. Splenic granulomata in mackerel contained acid-fast

bacteria (1) and spores of lchthyophonus (3); granulomata were present in four spleen tissues but without any discernible infectious agent.

9

Muscle-Only four muscle lesions were noted grossly-two in cod

and one each in dab and flounder. The cod lesion extended from

the dermis to the muscle and appeared to be a lipoma. Constituent

cells were well differentiated and arranged randomly and in whorls.

The lesion was well vascularized and poorly defmed at its perimeter. Fat cells infiltrated the interfibrillar spaces of adjacent muscle

and the fibers were atrophic and necrotic. The dab lesion consisted

of a piece ofinflammatory tissue with a large central area of necrosis.

Branched, septate, fungal hyphae were present in the necrotic area

and distributed around its perimeter. The remaining muscle lesion

was either a fibroma or fibrosarcoma in flounder. Although some

cells were arranged in cords or palisades, the overall cell pattern

was random. Nuclei varied considerably in size and contained one

nucleolus. Few mitotic figures were noted. The tumor contained

many necrotic and hemorrhagic areas and focal aggregates ofmelanin

and ceroid.

Miscellaneous-Eight goosefish (Lophius piscatorius) had microsporidan-induced cysts in the central nervous system, and one whiting

had an apparent epitheliocystis lesion in gill epithelium (Fig. 12).

DISCUSSION _

In many instances, the sampling protocol biased the results in favor

of lesions characterized by proliferative host responses. Typically,

proliferative lesions are seen in fishes with chronic infectious diseases

such as those caused by some bacteria, fungi, and some protozoans

and metazoans (Table 3). Although they are compromising in some

way, these diseases usually are not imminently fatal; the fish is probably able to survive and reproduce, albeit at a lower level ofmetabolic

efficiency. Fishes with acute infectious diseases are unlikely to have

grossly visible lesions and rarely are sampled in trawl surveys.

Although the basis for sampling was the presence of grossly visible

lesions in the organs examined, in many instances microscopic examination of sectioned tissues failed to disclose the presence of a
Figure lO.-"X" cell lesion in dermis of dab. a) Lateral edge of lesion inf'I1trating muscle (H&E, x 100); b) Mononuclear leukocytes and several "X"

cells (H&E, x 200); c) Cords of "X" cells, several possibly binucleate (H&E, x 400); d) Typical "X" cells with foamy cytoplasm and nuclei with prominent nucleoli (H&E, x 1(00).

10
,;"

II

I

" \ ... ';'/ -"

'- 'vI/.

a

Figure n.-Epidermal papilloma of dab. a) Lateral

edge of lesion showing cootnN between height of normal epidennis and hyperplastic epidermis (X 100); b)

Hyperplastic epidermis supported by fibrous stroma

(H&E, x 100).

lesion. Of the 350 lesions excised from tissues of western North

Atlantic fishes and 66 excised from tissues of eastern North Atlantic fishes, 81 (23%) and 16 (24%), respectively, were not visible

in histologic sections. This most probably was because many were

small (2-5 mm) and solitary, and, therefore, less likely to be present

after embedding and sectioning than lesions which are larger and

more dispersed in the tissue sectioned. Microscopically nonverifiable lesions were present in integument (11 %), gill (26%), gastrointestinal tract (22%), heart (33%), kidney (14%), liver (35%),

spleen (23%), and muscle (17%).

Since biologists rarely had the time to conduct comprehensive

necropsies, the first and most obvious lesion was usually the only

one excised. Cod and mackerel, however, caused exceptions to this

practice. Since several organs were obviously abnormal in some fish

(invariably nodules in gill, kidney, liver, mesentery, or spleen), more

than one lesion was excised. One cod infected with Unicapsula (Fig.

13) had granulomata in liver, mesentery, and spleen; several cod

had granulomata in kidney, liver, and spleen (cause unknown); and

many cod infected with Loma morhua had granulomata in gill, heart,

and spleen. A mackerel with mycobacteriosis had granulomata in

kidney, liver, and mesentery (also coccidia in liver granulomata),

and one infected with lchthyophonus had granulomata in heart and

spleen. lchthyophonus and mycobacteriosis both are proliferative,

systemic diseases. When the disease is chronic, granulomata may

be found in many organs.

Although the findings of this survey are not quantitatively significant, they provide an insight to the identity and microscopic

aspects of lesions found in a variety of commercially important bottom fishes. In the western North Atlantic, American plaice were

found with lymphocystis (one fish had a microsporidan-induced

myositis); cod had systemic microsporidiosis and ulcers (one fish

had systemic myxosporidiosis); a cusk had lchthyophonus; haddock

11
Figure 12.-Epitheliocystis lesion in gill of whiting

(H&E, X 200).

had microsporidan-induced gill infections and also were infected

with an unidentified oocyte-like cell (OLC) (one fish had a muscle

fibrosarcoma); several ocean pout had dermal "X" cell infections;

many red hake had OLC gill lesions and several had ulcers; many

silver and white hake had OLC gill lesions; and many winter

flounder had Iymphocystis and microsporidan-induced gastrointestinal cysts. In the eastern North Atlantic, blue whiting had OLC

gill lesions; one cod had mycobacteriosis and several had lesions

compatible with mycobacteriosis (one fish had a dermal lipoma);

dab had a variety of integumental lesions including Iymphocystis,

epidermal papilloma, "X" cell infections and ulcers; flounder had

Iymphocystis (one fish had a muscle fibrosarcoma); mackerel had

Ichthyophonus and mycobacteriosis; and one whiting had gill

epitheliocystis.

In the western North Atlantic, specifically the U.S. Continental

Shelf between Cape Hatteras and Nova Scotia, surveys have been

conducted since 1mto determine the prevalence and spatial distribution of integumental lesions and skeletal/pigmentation anomalies

(Murchelano and Azarovitz 1979; Despres-Patanjo and Murchelano

1981; Despres-Patanjo et al. 1982). The results ofthese surveys have

disclosed low prevalences of integumental lesions such as fin erosion, Iymphocystis, and ulcers. Lymphocystis and fin erosion were

noted principally in winter flounder; ulcers primarily affected cod

and red hake (Murchelano and Ziskowski 1979). Recent intensive

trawl surveys in the eastern North Atlantic, particularly the Danish

coast, French coast, and German Bight, have revealed high prevalences of integumental lesions in bottom fishes, especially flatfishes

(Christensen 1980; Nounou et al. 1981; Dethlefsen and Watermann

1982). Dab from the German Bight were noted with epidermal

papilloma (Watermann 1982), Iymphocystis, and ulcers; dab from

the French coast were ulcerated but did not have Iymphocystis and

epidermal papilloma. Cod with ulcers have been obtained from

Danish, French, and German coastal waters. There are considerable

differences in the prevalences of integumental lesions between

western and eastern North Atlantic bottom fishes, whatever their

cause(s). Although pollution has been implicated in the high preval12

ences of these lesions in eastern North Atlantic bottom fishes, conclusive cause and effect relationships must yet be established.

To date, inadequate data have been collected to compare the prevalence and cause of visceral lesions of commercially valuable bottom

fishes from the eastern and western North Atlantic. Surveys in the

eastern North Atlantic have revealed that many cod, haddock,

mackerel, and plaice (Pleuronectes platessa) have granulomatous

visceral lesions. Granulomata in viscera of cod from the Dutch coast

and mackerel from southern England and northern Ireland contained

acid-fast bacteria which were presumed to be Mycobacterium (van

Banning, pers. commun.1

). Kidney tissues from haddock and plaice

from Scottish waters were found to be infected with spores of

lchthyophonus (McVicar 1980). Mackerel from the western English

Channel and northern North Sea were noted with nodular lesions

predominantly of kidney and spleen (Hastings et al. 1982). Acidfast rod-shaped bacteria were seen in kidney melanin-macrophage

centers and within centrally necrotic granulomata. Although the

organisms were not cultured for specific identification, they were

presumed to be mycobacteria.

Although the published literature is replete with case reports on

the presence ofspecific parasites and lesions in western North Atlantic fishes, comprehensive seasonal surveys of fish health are recent

initiatives. As noted herein, few fishes have lesions comparable in

cause or severity to those found either in the integument or viscera

of eastern North Atlantic fishes. Mycobacteriosis has not been

detected in either cod or mackerel. Although few mackerel were

examined histologically in this survey, nodular lesions of kidney,

liver, and spleen have not been noted incidentally in studies of a

hematozoan mackerel parasite (MacLean, pers. commun.2). A major deficiency of the present survey was the inability to routinely

examine kidney tissues. Procedurally, kidney examination required

more skill and time than could be allocated by biologists on stock

'Paul van Banning, Netherlands Institute for Fishery Investigations, Ijuiden, Holland,

pers. commun. October 1981.

'Sharon Maclean, Nat!. Mar. Fish. Serv., NOAA, Northeast Fish. Cent.. Oxford,

MD 21654, pers. commun. June 1982.
Figure 13.-Unicapsula in cod. a) Granuloma in

spteen (H&E, X 200). b) Unicapsula sp. (ZN, x

1000).

assessment cruises. Although epizootics of lchthyophonus in herring from the western North Atlantic have occurred in the past

(Sindermann and Scattergood 1954), no herring were sampled on

any of the stock assessment cruises conducted. As part of a mackerel

sportfishing creel census conducted in New Jersey coastal waters

in 1979, grossly normal kidney tissues were excised at random from

91 fish and fixed for microscopic examination (Murchelano, unpub!.). Although the amount of kidney tissue present on each slide

varied appreciably, the number of granulomata present was tallied.

Thirty-six of 91 (39%) fishes had from I to 3 granulomata per slide,

and 2 of 36 (5 %) fishes had granulomata containing resting or germinating spores oflchthyophonus. This observation indicates that infections may be present, yet not apparent at gross examination.

13

Attempts will be made to substantiate these preliminary findings

on future cruises.

The only other recent, broadly based studies of marine fish health

have been conducted in Alaskan Outer Continental Shelf waters

(Bering Sea, North Pacific) by Wellings et al. (1fJ77) and McCain

et al. (1979). Twenty-six species of fish were examined, but only

four species had grossly visible external lesions. Pacific cod (Gadus

macrocephalus) and walleye pollack (Theragra chalcogramma) had

"X" cell pseudobranch tumors; Pacific cod had integumental ulcers;

rock sole (Lepidopsetta bilineata) had "X" cell epidermal

papillomas; and yellowfin sole (Limanda aspera) had lymphocystis.

Although the authors reported that they necropsied fish as time permitted, no internal lesions were described.
The limitations to the study of diseases of wild marine fishes,

especially in ocean environments, are well known. Sampling is difficult, expensive, and never adequate since the populations are large,

dispersed, and migratory. Additionally, unless a major epizootic is

in progress, fish with acute diseases (and lesions) are unlikely to

be found. Despite these limitations, studies of marine fish diseases

should be encouraged. The information obtained will eventually

enhance the success of marine fish husbandry (mariculture) and may

substantiate that some fish diseases are a consequence of environmental degradation and a cause of population decline.

ACKNOWLEDGMENTS _

Many individuals made the acquisition of fish tissues possible. In

the western North Atlantic, tissues were obtained by biologists of

the Resource Assessment Division, Northeast Fisheries Center

(Bradford Brown, Chief). In the eastern North Atlantic, the authors

directly obtained all tissues. However, the gracious hospitality of

FFS Anton Dohm (Germany), NO Thalassa (France), and BO Cornide de Saavedra (Spain) was made possible by Volkert Dethlefsen,

Bundesforschungsansalt fur Fischerei, Cuxhaven, Claude Maurin,

Institut Scientifique et Technique des Peches Maritimes, Nantes,

and Raphael Robles. Instituto Espanol de Oceanografia, Vigo,

respectively.

14

LITERATURE CITED----------

CHRISTENSEN, N. 0.

1980. Diseases and anomalies in fish and invertebrates in Danish littoral regions

which might be connected with pollution. Rapp. P.-v. Reun. Comm. int. Explor. Sci. Mer Mediterr. Monaco 1979:103-109.

DAWE, C. 1.

1981. Polyoma tumors in mice and X-eelltumors in fish viewed through telescope

and microscope. In C. 1. Dawe, 1. C. Harshbarger, S. Kondo, T. Sugimura,

and S. Takayama (editors), Phyletic approaches to cancer, p. 19-49. Japan Sci.

Soc. Press, Tokyo.

DAWE, C. 1., 1. BAGSHAW, and C. M. POORE.

1979. Amebic pseudotumors in pseudobranchs of Pacific cod, Gadus macrocephalus. Proc. Am. Assoc. Cancer Res. 20:245.

DESPRES-PATANJO, L., and R. A. MURCHELANO.

1981. Results of an initial survey to evaluate fish health in the western North Atlantic. Int. Counc. Explor. Sea C.M.1981/E:39, 13 p.

DESPRES-PATANJO, L., 1. ZISKOWSKI, and R. A. MURCHELANO.

1982. Distribution of fish diseases monitored on stock assessment cruises in the

western North Atlantic. Int. Counc. Explor. Sea C.M.1982/E:30, 12 p.

DETHLEFSEN, v., and B. WATERMANN.

1982. Diseases of major fish species in western Baltic Sea. Int. Counc. Ex·

plor. Sea C.M.1982/E:19, 20 p.

HASTINGS, T. S., K. MacKENZIE, and A. E. ELLIS.

1982. Presumptive mycobacteriosis in mackerel (5comber scombrus L.). Bull

Eur. Assoc. Fish Path. 2:19-21.

LANGE, E.

,973. Carcinoid-like tumors in the pseudobranch of Gadus morhua. Compo

Biochem. Physiol. 45:477-481.

McCAIN, B. B., W. D. GRONLUND, M. S. MYERS, and S. R. WELLINGS.

1979. Tumours and microbial diseases of marine fishes in Alaskan water. 1. Fish

Dis. 2: 111-130.

McVICAR, A. H.

1980. The effects of Ichlhyophonus infection in haddock Melanogrammus

aeglefinus and plaice Pleuronecles plalessa in Scottish waters. Int. Counc. Ex-

• plor. Sea, Pap. 16.

MORRISON, C. M., and V. SPRAGUE.

1981. Electron microscopical study of a new genus and new species of microsporida in the gills of Atlantic cod Gadus morhua L. 1. Fish Dis. 4:15-32.

MURCHELANO, R. A.

1982. Some pollution-associated diseases and abnormalities of marine fishes and

shellfishes: A perspective for the New York Bight. In G. F. Mayer (editor),

Ecological stress and the New York Bight: Science and Management, p. 327-

346. Estuar. Res. Fed., Columbia, S.c.

MURCHELANO, R. A., and T. AZAROVITZ.

1979. Fish disease surveys in the western North Atlantic. Int. Counc. Explor.

Sea C.M.I979/E:24, 7 p.

MURCHELANO, R. A., and J. ZlSKOWSKI.

1979. Some observations on an ulcer disease of red hake, Urophycis chuss, from

the New York Bight. Int. Counc. Explor. Sea C.M.I979/E:23, 5 p.

NOUNOU, P., R. MARfOJA, and L. ORCEL.

1981. Ulcerations of marine fishes and mammals caught in the French coastal

waters. Cent. Natl. Exploit. Oceans, Sci. Tech. Rep. 43, 99 p.

SINDERMANN, C. 1.

1979. Pollution-associated diseases and abnormalities of fish and shellfish: A

review. Fish. Bull., U.S. 76:717-749.

SINDERMANN, C. J., and L. W. SCATTERGOOD.

1954. Diseases of fishes of western North Atlantic. II. Ichrhyosporidium disease

of the sea herring (Clupea hareilgus). Maine Dep. Sea Shore Fish., Res. Bull.

19:1-40.

SINDERMANN, C. 1., F. B. BANG, N. 0. CHRISTENSEN, V. DETHLEFSEN,

1. C. HARSHBARGER. 1. R. MITCHELL, and M. F. MULCAHY.

1980. The role and value of pathobiology in pollution effects monitoring programs.

Rapp. P.-v. Reun. Comm. into Exp10r. Sci. Mediterr. Monaco 179:135-151.

WATERMANN, B.

1982. An unidentified cell type associated with an inflammatory condition of the

subcutaneous connective tissue in dab, Limandn limanda L. 1. Fish Dis.

5:257-262.

WELLINGS, S. R.

1969. Neoplasia and primitive vertebrate phylogeny: Echinoderms, prevertebrates

and fish-a review. Natl. Cancer Inst. Monogr. 31:59-128.

WELLINGS, S. R., C. E. ALPERS, B. B. McCAIN, and M. S. MYERS.

1977. Fish disease in the Bering Sea. Ann. N.Y. Acad. Sci. 298:290-304.