DETERMINING THE RELATIONSHIP BETWEEN WATER QUALITY AND INFECTIOUS DISEASE IN FISHERY POPULATIONS

WATER RESOURCES BULLETINVOL. 24, NO. 5 AMERICAN WATER RESOURCES ASSOCIATION OCTOBER 1988

DETERMINING THE RELATIONSHIP BETWEEN WATER QUALITY ANDINFECTIOUS DISEASE IN FISHERY POPULATIONS'

Edward J. Noga2

ABSTRACT: Diseases in wild fish populations may have multipleeconomic and social impacts. Epidemics of infectious diseases, whichare associated with the presence of some microbe or parasite, haverecently been observed in several major estuarine systems in theeastern United States. The most prevalent of these problems is ul-cerative mycosis (UM), a fungal infection. The agents responsible forUM and many of these other diseases are opportunistic pathogensthat are not believed to infect normal, immunocompetent individuals.While inroads have been made into determining the infectious agentsassociated with these diseases, we know very little of how pollutionmay influence their prevalence. Understanding the importance of pol-lution requires an awareness of all the environmental conditions thatcan affect the health of wild populations. In this paper, a multistepexamination of the interactions between the host, pathogen(s), andenvironment is outlined.(KEY TERMS: fish disease; epidemiology; environmental waterquality.)

INTRODUCTION

To protect aquatic resources, an understanding of humanimpact on ecosystem homeostasis is needed. This includesthe effect of human activity on the kinds and amounts ofdiseases present in aquatic organisms. It should be recog-nized that diseasç is a normal process in any animal popula-tion. Thus, we are concerned not so much with the presenceof disease but instead, about whether any anthropogenicfactors affect its prevalence. Studies of fish from relativelypristine environments indicate that disease is usually uncom-mon (Brown, et a!., 1977; Couch, 1985). In contrast, cer-tain diseases in the Albemarle-Pamlico estuary of North Caro-line frequently exceed 50 percent prevalence (Noga, 1986;Levine, eta!., unpublished). Does this mean that pollution isto blame? In this paper, I will outline our approach to tryingto answer that complexquestion.

SIGNIFICANCE OF DISEASE INFISHERY POPULAiIONS

Unfortunately, very little is known of the actual conse-quence of disease to natural populations of fish. However,the potential damage that disease can inflict is certainly worthconsidering. Disease problems may be important in fisheriespopulations for several reasons. First is their potential im-pact upon maximal sustainable yield (MSY), which is themaximum amount of biomass that can be harvested withoutdepleting the fishery stock. An accurate determination ofMSY is of great concern to both fishery managers andfishermen, as this value influences çlecisions about the amountof fish that can be harvested. The determination of MSY is,at best, an estimate and the influence of specific diseaseson MSY has yet to be evaluated. With he sensitivity ofpresent methods, usually only massive, catastrophic acutemortalities may be detectable, due to the wide degree of bio-logical variation (Munro, et aL, 1983). However, it is thechronic deterioration in water quality that may affect fisherystocks most significantly; such chronic effects are the mostdifficult to discern (Green, 1984; Wedemeyer, et a!., 1984).

Second, disease is also important from the standpoint ofaesthetics. This phenomenon may havesmore economic im-pact than previously thought. Visibly diseased fish are un-salable "in the round." If the fillet is affected, they maybe totally rejected, thus excluding them from the commercialfishery, regardless of their potential human health risk. Inaddition, people do not like to see sick fish or other animalsin the wild. This may reduce the attractiveness of fishingin affected areas, which could potentially have considerableimpact on a valuable recreational fishery. Such problemsoften become politicized. Political pressure placed on mana-agers is somewhat beneficial because it focuses attention onthese problems; but, it can also be disadvantageous as it tendsto emphasize short-term, stopgap solutions that fail to

Paper No. 88099 of the Water Resources Bulletin. Discussions are open until June 1, 1989.2Associate Professor of Aquatic Animal Medicine, Department of Companion Animal and Special Species Medicine; College of Veterinary Medi-

cine, North Carolina State University, 4700 Hilsborough St., Raleigh, North Carolina 27606.

967 WATER RESOURCES BULLETIN

recognize (or deal with) their complexity (Perry, et a!.,

1987).Third, the potential relationship of fish health to human

health is important. Fish exposed to contaminants, such ascarcinogens and other toxins, often respond in a mannersimilar to that of mammals. Neoplasia and other organ dys-functions have been documented in fish exposed to environ-ments contaminated with carcinogens and other toxins (Sinder-mann, 1982; Hawkins, et al., 1988). Such fish may pose apotential risk to humans if these toxins are present in edibletissues.

Finally, fish health may be an indicator of general eco-system health. In aquaculture, high levels of disease arefrequently a reflection of suboptinial environmental condi-tions that allow a pathogen to overwhelm a population'sdefenses (Plumb, 1984; Wedemeyer, et aL, 1976). It istempting to extrapolate such findings to natural aquatic popu-lations, but as will be explained later, such cause and effectrelationships are far from proven.

TYPES OF DISEASES AFFECTINGFISHERY POPULATIONS

Diseases fall into two general categories: infectious andnoninfectious. A microorganism (i.e., virus, bacterium, fun-gus, or parasite) is associated with infectious diseases, whereasnoninfectious diseases, such as those due to nutritional de-ficiencies or toxins, result from a chemical imbalance orinsult. There is overlap in these two categories, with somediseases having both infectious and noninfectious compo-nents (Sindermann, 1983). Furthermore, virtually all in-fectious disseases are probably initiated and/or facilitated bybiochemical imbalances that increase host susceptibility(Wedemeyer and Goodyear, 1984).

There is presently no strong evidence linking any infectiousdisease in wild fish populations to a specific pollutant. Inlarge measure, this is due to the fact that a myriad numberof possible variables ("contaminants") in polluted environ-ments may influence fish health. Factors that lead to thedevelopment of an infectious disease can be very complex.Exposure of fish to a pathogenic organism will not result indisease unless the proper conditions in the host (i.e., immunestatus) are met (Figure 1). The conditions responsible forthis immunosuppression may not be easily determined.

If a toxin responsible for reducing immunity accumulatesin host tissues, determining body burdens in affected indivi-duals may provide clues as to the cause of the problem.However, infectious diseases may also be initiated by environ-mental factors that may leave no detectable residues. Pollu-tants such as increased nutrient levels, alterations in salinitygradients, or changes in suspended solids may not be directlytoxic to fish. Instead, it is their second- and third-orderconsequences (e.g., changes in dissolved oxygen or carbondioxide due to eutrophication) that may stress fish (Plumb,1984). The rather ephemeral and temporally variable natureof such factors make them especially difficult to study. Thus,

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it is important to realize that infectious diseases are secondarymanifestations of physiological and/or environmental changesthat allow an infectious agent to colonize a host (Figure 1).The need to identify those primary effects that are ulti-mately responsible makes the study very complicated.

measurable morphological!biochemical lesion

POLLUTANT immunity —.. infectious disease

change in waler quality — immunity — infectious disease

Figure 1. Some Potential Steps Involved in the Developmentof Disease in an Aquatic Population. A pollutant may producea morphological or biochemical lesion that causes direct im-pairment of function (A). Alternatively, a pollutant mayspecifically depress immune function, resulting in increasedsusceptibility to disease (B). Thirdly, a pollutant may cause achange in water quality, the consequences of which suppressimmunity and result in disease (C).

Diseases can also be classified on the basis of organ sys-tems affected (e.g., liver, kidney, gill, etc.). Our studies havemainly involved dermatological diseases because of their pre-ponderance in the fisheries populations of North Carolina.Dermatopathies have several features that make them a usefulmonitoring tool for disease investigations. First, they arereadily visible and quantifiable. This is important because itallows large numbers of individuals to be screened rapidlyfor disease. The more individuals that are examined, thegreater the usefulness of the data. Second, the skin forms afirst line of both exposure to and defense from environmentalinsults. The skin and other body surfaces such as the gillsand gastrointestinal tract are usually the first organs to comeinto contact with toxicants or infectious agents. Skin lesions,especially ulcers, have often been associated with heavilypolluted environments (Sindermann, 1983). Thus, skin maybe a good sentinel tissue. Third, many systemic diseases offish can have dermatological manifestations, so skin lesionscan often reflect internal organ changes. Finally, skin lesions,being readily visible, often incite a high degree of publicawareness, facilitating public cooperation in disease investiga-tions.

INFECTIOUS DISEASE PROBLEMSIN NORTH CAROLINA

Infectious diseases are a major problem in the Albemarle-Pamuico estuary (APE). The APE, which includes Albemarleand Panilico Sounds and their tributaries, is the second largestestuary in the United States and is a major nursery ground fornumerous commercially important fishes including Atlanticmenhaden and many sciaenids and flatfishes.


Determining the Relationship Between Water Quality and Infectious Disease in Fishery Populations

Dermatological problems have plagued the APE fishes fora number of years. Epidemic disease was first reported in the1970's when a skin problem called "red-sore" disease causedmassive kills in largemouth bass (Micropterus salmoides),white perch (Morone americanus), and other species in Albe-marie Sound and the Chowan River (Esch and Hazen, 1980).At the time, this problem was thought to result from a pri-mary Aeromonas hydrophila skin infection followed bysecondary colonization of the lesions by a protozoan,Epistylis ( Heteropolaria) (Huizinga, et al., 1979); however,examination of fishes with early stages of "red-sore" severalyears later revealed numerous other infectious agents (Noga,1986, Table 1).

Recently, other types of diseases have been recognized inPamlico Sound and its tributaries. By far, the most commonis ulcerative mycosis (UM), a fungal infection primarily af-fecting Atlantic menhaden (Brevoortia tyrannus). UM wasfirst recognized as a serious problem in 1984. First seen inthe Pamlico River, it was soon also reported from the NeuseRiver, New River, and Albemarle Sound. Investigations inother regions including Delaware Bay, Chesapeake Bay, andthe St. Johns River estuary, Florida, have revealed fish withsimilar ulcers, suggesting that UM may be epidemic alongmost of the Atlantic seaboard of the United States (Ahren-holz, et a!., 1987; Grier and Quintero, 1987; Hargis, 1985).

Since 1984, UM has continued to cause repeated out-breaks in these eastern estuaries that in some instances hasresulted in up to 90 percent infection rates in randomlysampled Atlantic menhaden (Levine, et al., unpublished data).In the Pamlico River, where the disease has been best studied,the highest prevalence rates occur in low to moderate salini-ties. Many fish that inhabit this salinity zone appear sus-ceptible to UM. A similar disease has been observed onsouthern flounder (Paralichthys lethostigma), striped bass(Morone saxatiis), weakfish (Cynoscion regalis), croaker(Mic ropogonias undulatus), spot (Leiostomus xanthurus),silver perch (Bairdiella chrysura), gizzard shad (Dorosomacepedianum), hogchoker (Trinectes maculatus), pinfish(Lagodon rhomboides), and bluefish (Pomatomus saltatrix)(Noga, et a!., unpublished data).

Ulcerative mycosis has several characteristic features thathelp to distinguish it from other diseases that cause sores onfish. First and most obvious, there are very deep penetratinglesions that are so aggressive that they commonly perforatethe body wall, exposing the internal organs. When the deadtissue is sloughed off, a crater-shaped lesion is left (Figure 2).Lesions are commonly infected with many different types ofbacteria and Protozoa. Their role in causing the lesions isuncertain; however, the large numbers of microorganismspresent in advanced cases may contribute to the death of thefish.

The fungi present in UM lesions are water molds ofthe genera Aphanomyces and Saprolegnia (Noga and Dykstra,1986; Dykstra, et a!., 1986). These organisms have previouslybeen considered to be almost exclusively freshwater pathogensand have rarely been reported to cause disease in estuarine

fishes. These water, molds or Oomycetes are common fresh-water inhabitants that usually form fuzzy, cottony growthson the skin of freshwater fishes (Figure 3). In contrast withUM, such lesions usually do not penetrate deeply into thebody. The inflammatory response of fish to UM is alsounusually severe; this may reflect the fact that the fungusgrows aggressively into the tissue. While UM is by far themost common disease affecting menhaden in the PamlicoRiver, we have seen many other diseases in lower prevalence(Table 1, Figure 4). Other diseases have also been reportedfrom other estuarine areas (Grier, 1987). The only featurethat these maladies lave in common is that an infectiousagent is involved, which is often an opportunistic pathogen.

Figure 2. Atlantic Menhaden (Brevoortia tyrannus) from thePamlico River, North Carolina, Affected by Ulcerative Mycosis.

ELUCIDATION OF THE RISK FACTORS ASSOCIATEDWITH INFECTIOUS DISEASE

Determining the factors that are responsible for an epi-demic 'in a fishery population requires close examination ofthe three principal components that interact to produce di-sease: the host, the pathogen, and the environment (Snieszko,1974). This discussion is not intended to be a definitivethesis on how investigations of fishery diseases should be


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Figure 3. Channel Catfish (Ictalurus punctatus) Showing "Typical" Saprólegniasis. Note the cottonyappearance of the fungus and the relatively shallow lesion compared to that in Figure 2.

conducted, but rather it is meant to point out the most im-portant features of such studies. Although the steps are pre-sented in rough chronological order, discoveries in one stepmay require re-examination of a previous one.

TABLE 1. Pathogens Associated with Skin Diseases ("red-sore")from Fishes in the Albemarle-Pamlico Estuary.

VIRUSESLymphocystis

BACTERIA*Aeromonas hydrophilaAeromonas salmonicida

FUNGI"Typical" Saprolegniasis"Atypical" Saprolegniasis [Ulcerative mycosis]Proliferative granulomatous mycosis

PARASITESHenneguyaHeteropolariaMonogenean trematodesDigenean trematodesArgulusLernaeid copepods

NOTE: Only skin pathogens associated with grossly evident inflain-matory lesions are included. Many of these pathogens are also foundasymptomatically on healthy skin.

*Numerous other bacteria that have been identified from advancedlesions and which do not appear to be primary pathogens are notincluded.

1) Identify and Differentiate Diseases

From the above discussion, it should be obvious that manydiseases may look very similar to the naked eye and, thus,may mistakenly be lumped into one category (Table 1). Itis important to differentiate and identify the most importantproblems because distinct risk factors are associated with thedevelopment of different diseases.

Skin lesions in particular require careful evaluation, be-cause of the common colonization of open wounds by non-pathogenic opportunists. The earliest stages of skin lesionsare often most important in determining the cause of adisease problem since they are least likely to harbor con-taminants. For example, advanced stages of ulcerative myco-sis have large numbers of many different types of bacteria inaddition to fungi. But no bacterium is consistently the pre-dominant organism, whereas fungi are consistently observedin both early and advanced lesions (Noga and Dykstra, 1986).The importance of putative pathogens in large, open skinwounds must be carefully interpreted. Thus, it is importantthat lesions be thoroughly examined to ensure that the ini-tiating pathogen is correctly identified.

2) Reproduce the Disease Under Controlled Conditions

Once a putative pathogen(s) has(have) been isolated, thedisease must be successfully induced in the laboratory andthen the same organism must be reisolated. The meeting ofsuch criteria, termed Koch's Postulates, is essential becausereproducible induction of a disease provides an experimentalmodel that can be used to determine which environmentalconditions are most influential on disease development (StepNo. 6).



Figure 4. Aeromonas salmonicida Infection of American Eel (Anguilla rostrata), a Memberof the "Red-Sore" Disease Complex in the Albemarle-Pamlico Estuary.

Reproduction of the disease may be difficult as full ex-pression of disease depends not only upon the presence ofthe host and pathogen but also the proper environment. Thisincludes both factors conducive to pathogen virulence (StepNo. 3) and to host susceptibility. The latter is dependentupon host immunity, which in fishes is highly influenced bythe environment (Ellis, 1981; Plumb, 1984). This is particu-larly relevant to the APE, where many of the organisms af-fecting fish are opportunistic pathogens that only cause di-sease in debilitated hosts. Aeromonas hydrophila and oomy-cete fungi are classic examples of such agents.

3) Determine Factors That May influence the Pathogenicityof the infectious AgentMany fish pathogens, such as water molds and many bac-

teria, are capable of a free-living existence in water and donot require a fish host for survival. Temperature, dissolvedgases, salinity, pH, and various nutrients may influence theabundance and possibly the virulence of such agents. Highlevels of organic matter have been correlated with risk of in-fection by Aeromonas hydrophila (Wedemeyer, et al., 1976),one of the most common heterotrophic bacteria in freshwaterecosystems.

The growth of an Aphanomyces sp. isolated from men-haden with ulcerative mycosis was enhanced in the presenceof low concentrations of salt (Dykstra, et aL, 1986) Thisis very unusual, for this type of water mold is usually inhi-bited by salt. This finding correlates with the highest pre-valence of the disease apparently occurring in waters of lowto moderate salinity. Salinity tolerance may also explainhow these fungi can penetrate deep into fish tissue, whichhas a high salt content.

4) Identify Zones of High and Low Risk for Infection

The purpose of this step is to focus on those sites wherefish are becoming infected. Correctly identifying such sitesis critical in determining which water quality parameters maybe responsible for the disease. One approach is to narrow thesuspected region of high risk by using progressively moreprecise methods of detection.

Methods for identifying sites include local reports fromlay observers (fishermen, etc.), collection surveys, and sen-tinel studies. The usefulness of lay observations should notbe discounted; commercial fishermen, because of their frequentand intimate association with the fisheries, often have anacute sense of which areas are "good" or "bad" in terms ofhealth or disease. However, such observations must be sub-stantiated with a scientific approach.

Various collection devices have different advantages, basedupon the data required. For example, the pound net, astationary trap, is useful because it catches many fish withoutkilling them. Fish can often survive within this net enclosurefor up to several weeks. Because they are not damaged bythe net, this is one of the best methods for obtaining fish fordisease diagnosis. Conversely, in gill nets, another stationarycollecting device, fish usually die within hours of entrap-ment, requiring that nets be monitored closely. There is oftenskin damage due to entrapment in gill nets. Although poundnets and gill nets are useful, they are expensive to maintain.Thus, other collection methods, such as trawling or electro-shocking, are better suited for examining multiple sites.

While collection surveys can be useful for distinguishingsites of interest, they do have limitations. If the fish studiedare migratory, one cannot be absolutely certain that sick fishacquired their infection exactly where they were collected.


Also, the considerable degree of natural variation in manyecosystems may make it difficult to recognize trends. Thus,sentinel systems, such as cages or pens for holding susceptiblefishes, can be very useful for pinpointing high risk sites,particularly when used in concert with collection surveys(see Grizzle, this volume, concerning use of cage enclosures).

5) Correlate Specific Water Quality Factors With High andLow Risk Sites

The success of this stage depends upin the ability to pre-cisely identify high risk sites for infection (Step No. 4). Atpresent, there is very little information about the relationshipbetween water-quality and infectious disease development innatural environments. However, experience with diseaseproblems in aquaculture situations can be helpful in formu-lating a probable list of risk factors. Two major types offactors should be considered. First are those environmentalconditions universally essential to fish health: dissolved oxy-gen, salinity, temperature, nitrogenous compounds (ammonia,nitrite, nitrate), and pH. Deciding which to examine mostclosely depends upon their past variability in the particularsystem under study. Second are toxic contaminants (heavymetals, etc.) that may be above "normal" limits. With amyriad number of possible factors that may affect fish health,this list should also be based upon any historical trends ofanthropogenic inputs into the system. The time scale ofmonitoring to be performed will obviously be dependentupon the range of system variability for the water-qualitycriteria examined (Livingston, 1982). Collaboration withecologists and hydrologists who are familiar with the ecosystemin question is important.

As mentioned previously, most pollution-disease investiga-tions have focused on the possible cause and effect relation-ship between an anthropogenic substance and its effect onfish health. However, a direct causal relationship may notexist and instead, the pollutant may act indirectly on fishhealth by causing other changes in environmental quality(Figure 1).

6) Reproduce the Disease Using the Specific Water-QualityRisk FactorsIf differences in water quality have been detected between

high- and low-risk sites, one must decide which of those dif-ferences are most likely to be causing the disease. This im-plies that reliable information exists on factors influencingfish health in natural systems. Unfortunately, environmentalrequirements for fish health are based mainly on studies of afew species, primarily cultured fishes; and even in thesespecies, the relationship between specific environmental con-ditions and disease resistance is poorly understood. None-theless, one must demonstrate that specific water qualityfeatures increase the risk of disease under experimental condi-tions, to prove a cause-and-effect relationship.

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7) Determine Appropriate Controls

The ultimate goal is to present to managers the major waterquality factors that are responsible for the development ofthe disease. With this information and a knowledge of theanthropogenic contributions to that pollutant's loading, anadministrative decision can then be made concerning accept-able levels of that pollutant in the environment.

SUMMARY

Fishes in the Albemarle-Pamlico estuary have a very highprevalence of skin diseases. The only apparent similarity amongthe diseases is an infectious component (i.e., virus, bacterium,fungus, or parasite). Although diseases are very common inthis estuarine system, the data are insufficient to support orrefute pollution as their cause. One unknown but cruciallyimportant variable is the influence of natural environmentalperturbations on the expression of these diseases. Diseaseis certainly not restricted to fish populations in pollutedenvironments, and significant disease outbreaks have beendocumented in fish populations far from any pollutantsources.

One must first determine the major environmental factorsthat increase the risk of a fish population to disease beforespecific pollutants can be implicated. Thus, the question of"pollutant" or "natural stressor" is initially irrelevant; instead,the focus should be on those factors most important to fishhealth. It is important to understand how natural environ-mental Cfluctuations may affect the susceptibility of fish todisease. Only with this knowledge can we understand howanthropogenic activity can influence and accentuate thoseenvironmental stressors.

Finding those risk factors requires a multifactorial approachthat includes examining the host, the pathogen, and the en-vironment. It is obvious that this task is not easily done,but will require considerable effort with no guarantee thatanswers will be found. The decision to attempt such under-takings will ultimately depend upon the economic and in-trinsic value that we place on our fishery resources.

ACKNOWLEDGMENTS

Our research in the Albemarle-Pamilco estuary has been supportedby Grant No. 70054 from the University of North Carolina Water Re-sources Research Institute, the Office of Sea Grant, NOAA, U.S. De-partment of Commerce, under Grant No. NA 83AA-D-0012, the NorthCarolina Department of Administration, and by the North CarolinaDivision of Marine Fisheries. I thank M. J. Dykstra, J. F. Levine,J. H. Hawkins, M. J. Levy, and C. E. Bower for their helpful discus-sions.



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DETERMINING THE RELATIONSHIP BETWEEN WATER QUALITY AND INFECTIOUS DISEASE IN FISHERY POPULATIONS