[Advances in Marine Biology] Advances in Marine Biology Volume 11 Volume 11 || Parasites and Fishes in a Deep-Sea Environment

Adv. mar. Biol., Vol. 11, 1973, pp. 121-195

I. II.

111.

IV.

V.

VI. VII.

VIII.

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT

ELMER R. NOBLE University of California, Santa Barbara,

California, U.S.A.

Introduction . . .. . . .. .. .. .. .. .. Methods . . .. . . .. .. . . .. .. .. .. The Deep-sea Environment . . .. .. .. .. . . . .

A. Physical Features . . .. .. .. .. .. .. B. Plankton and the Food Supply . . .. .. . . .. C. Metabolism in the Deep Sea. . .. .. . . .. .. A. Organization and Behaviour of Deep-water Fishes . . ..

Fishes and Their Parasites . . . . . . .. .. .. ..

B. Parasites of Fishes-Introduction . . .. .. .. .. C. Inshore Fishes . . . . .. .. .. .. .. D. Selachians . . .. . . .. .. . . .. .. E. Midwater Fishes and Thei lParmites-North Atlantic . . .. F. Midwater Fishes and Their Parasites-Eastern Pacific and Indian

Ocean .. .. .. . . . . .. .. .. .. G. Fishes of the Family Macrouridae . . .. .. .. ..

Discussion . . .. .. .. .. .. .. .. .. A. Food .. .. .. .. .. .. .. .. .. B. Life Cycles of Parasites . . .. .. .. .. .. C. Parasites as Biological Tags. . .. .. .. .. .. D. The Uniqueness of Deep-sea Parasitism . . .. .. ..

Conclusions and Summary . . .. .. .. .. .. .. Acknowledgements . . .. .. .. .. .. .. .. References . . . . . . .. .. .. .. .. ..

121 124 129 129 130 131 134 135 137 138 142 147

162 160 171 171 174 179 184 186 189 189

I. INTRODUCTION A fish and its parasites constitute a community of organisma where

parasites are a part of the environment of the fish, and the host is the immediate environment of its internal parasites. Any comprehensive understanding of marine biology must include knowledge of parasites because they outnumber their hosts, and because they play a profound role in the biological economy of the sea. We know very little about the broad ecological aspects of deep-water parasite-host relationships. A list of species descriptions is necessary, but not enough. Influences of parasites upon their hosts and influences of the environment on parasites should be studied whenever possible. Deep-sea parasitology may also contribute to studies on evolution and host specificity of

121

122 ELMER R. NOBLE

parasites, geographic distribution of parasites and the use of parasites as clues to host distribution and behaviour.

Does the deep ocean environment, characterized by perpetual cold, darkness, great pressures and physical homogeneity, engender some attributes of parasitisms that are different from those in other kinds of habitats? This question has seldom been asked. Most parasitologists who have delved into the sea have confined their efforts to shallow waters and to describing new species. The paucity of information is also the result of a general interest in only one kind of parasite. A typical investigator is concerned with trematodes, or with nematodes, or other limited groups, and when he has garnered all that he can find of the one kind, he sometimes throws away other parasites with the remains of the fish. Thus he often discards an opportunity to study the fish and its parasites as a community of interacting organisms. Another problem is the difficulty of obtaining deep-sea fishes, especially benthic species, in sufficient numbers and kinds to furnish statistically significant results; and to h d the talent and time to secure their parasites and important relevant environmental data. The most difficult problem of all is the interpretation of data once they are obtained.

In 1961 H. H. Williams wrote a short paper entitled " Parasitic worms in marine fishes ; a neglected study ". During the 12 years that have elapsed since his paper was published much work has been done on marine fish parasitology, but his title is still applicable. Such a title would be particularly appropriate if it included the parasitic protozoa and emphasized fishes living in deep waters.

Since investigations of the biology of parasites in the deep sea have seldom been made, beyond descriptions of species and counts of incidences and intensities of infection, I shall describe some studies on the biology of hosts, or potential hosts, assuming that broad generalizations about the biomass of the deep sea include parasites as part of that biomass.

No attempt will be made to tabulate all of the parasite species that have been described from deep marine fishes during the past 10 or 12 years, nor would such a tabulation be of any particular interest to the general reader. There is, however, a growing body of information on which to base conclusions and speculations concerning differences in parasitism among the several ecological zones in the water columns of the oceans. Only a few samples from each zone will be presented to illustrate the " typical " parasite pattern. An exception will be made for benthic fishes, especially deep-dwelling macrourids, a larger number of which will be listed. Figure 1 illustrates the epipelagic, mesopelagic, bathypelagic and benthopelagic zones, and changes in biomass, light

ZONES DVM BIOMASS LIGHT TEMPERATURE

FIG. 1. A diagram of certain oceanic features in relation to the life of deep-sea fishes: mesopelagic (represented by a lantern-fish); bathypelagic (by an anglefish) ; benthopelagio (by a rat-tail, left, and by a hdosaur, right) ; benthic (by a e-snail, left, and Eathymicrop, right). At the right of the diagram are represented the extent of diurnal vertical migrations (DVM) in the mesopelagic zone, the biomass of zooplankton, the light regime, and the temperature profile of the warm ocean. (After Marshall, 1971.)

124 ELMER R. NOBLE

and temperature with depth. The term abyss has been variously d e k e d by different authors, but generally denotes the area between the bathypelagic and benthopelagic, or it is substituted for benthopelagic.

This review will be concerned only with animal parasites of fishes (omitting bacterial, fungal and viral infections). Since the uniqueness of parasitism in a deep-sea environment cannot be recognized unless it is compared with parasitism in a shallow-water environment, a few examples of fishes and their parasites from the inshore and offshore epipelagic zone will be presented. In the deep marine environments emphasis will be placed on the benthopelagic and benthic habitats, and on a comparison between them and the strikingly different midwater zones.

A detailed definition of parasitism in the deep ocean should include aspects of host biology as well as parasite biology, and an evaluation of environmental parameters that may play a role in establishing and maintaining parasite-host relationships. The formulation of such a defkition is an ambitious task, and many of the important details are little understood. Enough progress has been made to permit a clarifica- tion of the problems, a more meaningful selection of questions, the beginnings of answers, and an abundance of speculation. For general works on fish diseases see Sindermann, 1970 ; Reichenbach-Klinke and Elkan, 1966 ; Polyanskii, 1955 ; Pavlovskii, 1959 ; Altara, 1963 ; and Snieszko, 1970.

11. METHODS Several kinds of trawls are used successfully by biologists, especially

the otter trawl or a modification thereof. Most of my living or moribund fishes were obtained with an Isaacs-Kidd midwater trawl equipped at its cod end with a compartmentalized collecting chamber whose four compartments could be closed by the action of solenoids at any desired depth to about 1000 m, operated on deck through the conductor cable. In this manner I could be reasonably certain that the fishes and invertebrates were not mixed with others captured on the way down or up, except that the last chamber was always open while the trawl was being brought to the surface. Temperature, depth and light conditions at the time and place of capture were automatically registered by a digital computer read-out and strip recorder located on deck. Bathythermographic measurements were taken regularly.

Horizontal sampling is not suitable for quantitative determinations of the plankton mass in the entire water column because vertical distribution of plankton, especially at and just below surface layers, is stratified with sharp gradients between adjacent layers. For this

PARASITES AND FISHES IN A DEEP-SEA ENVlRONMENT 125

reason Vinogradov (1968) recommended the use of closing nets operated vertically.

A free vehicle for the collection and study of deep-sea organisms has been used for at least 35 years, but most advances have been made since 1960. The most recent description of these devices was by Phleger and Soutar in 1971. " A free vehicle is a timed and weighted device released from the ship in a free fall to the ocean bottom. It may be designed (1) to capture benthic organisms, as a baited free vehicle long-line or a baited free vehicle trap, (2) to collect water and/or bottom samples, or (3) to carry down instruments for various physical or chemical measurements in the benthic environment. The free vehicle and the weights which carry it to the ocean floor must be attached to each other by a timing device programmed to release the weights at any desired time. ''

Among the several release mechanisms that have been used (e.g. ice, bags of sugar, candy) the most practical release involves electro- deterioration of a magnesium rod. When the magnesium link dissolves, leaving the weight(s) on the bottom, the floats carry everything else to the surface. One assembly is shown in Fig. 2 and a very eficient wire-plier release is shown in Fig. 3. Many varieties of magnesium linkages and other parts of the assembly can, of course, be made. Among the advantages of a free vehicle are rapid launch and recovery, low price, and the fact that it can be operated from almost any small or large vessel.

Regardless of the collecting technique used, the problem is largely one of obtaining adequate samples of organisms, and bringing them to the surface in as natural a condition as possible. Ideally, the solution is the use of equipment that can bring the animals and some of their ambient water to the surface in a vessel that maintains the pressure and temperature of the normal habitat. Such vessels have not yet been constructed.

A careful dissection of small fish and tiny parasites on board a rolling ship is often extremely difficult, even without the frequent disastrous accompaniment of motion sickness that often attacks the investigator. Such work, nevertheless, must usually be done to obtain information on the appearance and behaviour of living parasites, particularly protozoa. Adequate examination of blood from preserved fishes is impossible, and highly unsatisfactory from unpreserved, dead fishes. For this reason the trypanosomes, haemogregarines, piroplasms, etc., of deep-water marine fishes are rarely mentioned in this report.

Living helminths of the digestive tract may be obtained as follows. Wash out the contents of the stomach and intestine with seawater,

FIQ. 2. The free vehiole vertical hookline-trap oombination. The top shows the plastio mast supported by Isopar-M oil-filled jerry jugs with radio and flags. Fifteen metres of handling line oonneot to the secondary float, below whioh are traps and hookline. The free vehiole is held on the bottom by s 27-kg weight. The release is loaated between the lower trap end the weight. (After Phlegm et d., 1970.)

PARASITES AND FISHES IN A DEEP-SEA ENVIRONMENT 127

and firmly scrape the walls. Allow the mixture to settle in a suitable container and decant all but the heavier particles. Pick out the larger parasites, then examine the sediment carefully with a dissecting binocular or good hand lens. Living helminths can be relaxed in 1.0%

FIQ, , 3. A scale diagram of the wire-plier release mechanism. The magnesium wire has a diameter of 0-16 om. When it dissolves in seawater, the spring insures that the pliers will snap open to release the weights. (After Phleger et uZ., 1970.)

ethyl carbamate (urethane) solution at room temperature, or in 0.9% NaCl solution.

Parasites, such as intestinal flagellates and nematodes, may remain alive for hours or even days in a dead fish if the fish has been frozen immediately upon removal from the net or line. However, although there is no good substitute for a living fish, most studies of parasitism in deep-sea fishes have been carried out on dead specimens, sometimes

128 ELMER R. NOBLE

on fishes that have been " pickled " for many years. Trematodes and cestodes that have been frozen are commonly so macerated that they are unsuitable for identification. The freezing and thawing processes are partly responsible, but sometimes the original onset of freezing is delayed by allowing the fish to lie on deck for some hours before placing them in the freezer.

Eagle and McCauley (1965) have recommended an excellent technique for ensuring well-fixed helminths on shipboard. While the fish is alive, or freshly dead, inject (with a large syringe) a quantity of AFA fixative (formalin-acetic acid-alcohol) into the mouth, rectum and body cavity. Then place the fish in 10% formaldehyde. If AFA is unavailable, formaldehyde made up with sea water is a satisfactory substitute.

Fluid preservation of fishes is usually accomplished by placing the tagged fish immediately in 10% formaldehyde. At a convenient time after the specimens are brought to the land laboratory, the fish are generally washed thoroughly in running tap water, then placed in 40% isopropyl alcohol for permanent storage. Much of my own material has come from museum specimens kindly furnished by various universities and fisheries laboratories. One difficulty in using museum specimens is the frequent need to destroy as little of the fish as possible so as to save it for future icthyological studies. A parasitologist usually is most satisfied when he can, with caution and prudence, demolish the entire fish, provided that it has been identified.

AFA is a good general fixative for parasites. Contraction of the specimens can be lessened by light pressure of a coverglass when the fixative is added, or if muscular species are present, a glass slide instead of a coverglass may be required. Hematoxylin and carmine stains prepared by various formulae are most commonly used.

Minimum data that should accompany each collection are: date, cruise number, name of collector, location (including longitude and latitude), depth of collection, depth of bottom. Other valuable data include salinity and temperature of water at level of catch, time of day, other animals captured in the same haul.

For permanent storage of specimens in vials, the addition of a few drops of glycerine to each vial often prevents ruinous drying if the vial cap is not airtight. Study of sectioned host tissues such as pieces of stomach, hindgut and kidney frequently reveals the presence of previously unnoticed protozoan parasites such as Myxosporida, Micro- sporida and Coccidia.

One is never satisfied that all the kinds of parasites in a large fish have been found. To do so would require minute dissections and


examinations of all organs, including sectioned material. Such a pro- cedure with a fish as large as the common mackerel or commercial cod would require so many days that the numbers of fish necessary for significant conclusions could not be completed unless a large team of workers could spend all of their time at it.

111. THE DEEP-SEA ENVIRONMENT Any ecological discussion of parasite-host relationships in marine

fishes must be based on a knowledge of the sea as an environment for the hosts. I shall, therefore, begin this discussion with a mention of environmental factors that may influence the variety of parasites and incidences of infection in deep-sea animals. The characteristics of deep ocean waters listed below are the chief factors that determine the kinds, numbers and behaviour of the organisms living in these waters.

A. Physical features 1. Absence of solar light

Below about 100m there is little or no photosynthetic activity. Between 150 and 1 200 m is the " twilight zone '' where plants, if they exist, must be heterotrophic. Sunlight can be detected and measured by sensitive equipment in the clearest parts of the ocean, e.g. Sargasso Sea in the southern North Atlantic, to depths of about 1000 m. A study of the eyes of deep-sea fishes suggests that they may see daylight at depths below 1 000 m.

2. High pressure For every 10 m of depth there is an increase of one atmosphere of

pressure. For example, at 4 000 m, the average depth of the wor1d)s oceans, the pressure is 400 atm or 6 000 lb/in2. See p. 131 for comments on metabolism and hydrostatic pressure.

3. Low temperature At 40" N Latitude in the north Atlantic the surface temperature

varies from 15" to 23°C. At 200 m depth the temperature is 12" to 15' ; at 1 000 m it is 7' to 8", and at 2 000 m it is about 4". Between 2 000 and 4 000 m the drop may be 1" or less (Menzies, 1965). The bottom depths generally remain at 1" to 3'. Comparable temperatures occur in the other large oceans.

4. Oxygen With increasing depth there appears to be little change in oxygen

content except in the '' oxygen minimum layers )', found at intermediate

130 ELMER R. NOBLE

depths, where the dissolved oxygen in some areas is considerably less than 0.4 ml/l. These layers, however, generally support large populations of animals (Longhurst, 1967).

5. General homogeneity

Compared with shallow water the deep sea is a homogeneous and stable environment. The stability of the physical environment has permitted organisms to evolve a high degree of physiological special- ization. The stability may not be as great as often envisaged. Knauss (1968) stated that " measurements to date suggest that strong currents. . . exist close to the bottom in the deep ocean in at least some areas some of the time. Details concerning the nature of the circulation are not clear, but it is possible that the deep circulation is as complex as the surface circulation. " The stable biomass does not exhibit much, if any, seasonal or annual fluctuation. For this reason it is extremely difficult to measure the age of deep benthic animals.

B. Plankton and the food supply

As a general rule there is a decrease in biomass and size of organism with depth. Benthic animals, however, are larger and more active than midwater species because of an increase in available food. The kinds, numbers and availability of food organisms determine the frequencies of ingestion of infected intermediate hosts. The metabolism of the host, related to hydrostatic pressure, temperature, oxygen and other factors, is one of the major determinants of parasite-host specificity.

The notion that there is a steady rain of food from the surface to the bottom of the ocean is not substantiated by facts. Food from the surface consists of dissolved organic matter, detritus formed from disintegration of tissues of animals and plants, heterotrophic organisms that swim or are carried by currents, and remains of terrestrial organisms carried into the sea by fresh water. As this material sinks it is largely dissolved in the water or decomposed by bacteria. Riley (1951) stated that only about one tenth of the organic matter produced in the surface euphotic zone penetrates below 200 m. A few observations from bathyscaphes indicate an increase in the amount of plankton near the bottom. Ekman (1967) found an insignificant number of nanoplankton species below about 200 m in the Atlantic. Vinogradov (1968) studied deep waters near Japan, and reported that at depths of 1 000-2 000 m the amount of plankton was a quarter that of the surface. Zenkevitch and Birstein (1956) reported that the biomass of benthos


and plankton in the ultra-abyssal zone in the Kuril Trench at a depth greater than 6 000 m is 1000 times less than in the surface zone. Vinogradov (op. cit.) stated that “ As one moves to trench waters at a depth of about 6 000 m, no marked change is seen either in the rat’e of decrease of the general planktonic biomass or with respect to trophic groups ”.

The demersal layer immediately above the bottom in deep waters is extremely difficult to sample, and little is known about its plankton. In this water that immediately overlies the mud there is a whole mam of plankton that is different from that found higher in the water column (Robert Hessler, personal communication). Until adequate samples of this layer can be obtained in large quantities, we cannot determine the nature of life cycles of parasites that are acquired through food obtained by fish living on the bottom. Some help can be gained by an examination of mud samples that often contain echinoderms, annelids, crustaceans and a few molluscs.

There is, then, a general decrease with depth of plankton and nekton (active swimmers). An increase occurs among the organisms living on the bottom and immediately above the bottom. A decrease in available food resources results in an increase in competition for food. With increase in depth there is an increase in morphological, physiological and behavioural modifications of the competing organisms. These adaptations to a food-poor environment (see p. 135) result in a reduction of energy expenditure. Studies on parasite-host relationships in terms of energy exchange and host metabolism have not been extended to deep ocean waters. A short account of some studies on the metabolism of fishes and invertebrates from the deep sea is presented below, especially as it relates to hydrostatic pressure. Some speculation on the relation of these events to parasitism will follow.

C. Metabolism in the deep sea During recent years a number of investigators have begun studies

on relationships between metabolism and the low temperature-high pressure environment of the deep sea. In answer to the question, do deep-sea fishes have special metabolic adaptations to high hydrostatic pressures?, Gordon (1972) answered, “ At the present time, few data are available which permit specific answers to this question. This is particularly true at the whole animal and other higher levels of organ- izational complexity.”

Deep-sea animals are mostly predators on plankton or nekton, but since the bathypelagic species have weakly developed skeletons, muscles, eyes and other organs, they must lie in wait for prey, thus

132 ELMER R. NOBLE

avoiding expenditures of energies in actively seeking and following their food. Those species without a swimbladder must swim much of the time to prevent sinking to the bottom. (See p. 135 for a note on neutral buoyancy.)

If mesopelagic and, especially, bathypelagic animals must conserve most of their energy for obtaining food and for reproduction, it is possible that they cannot sustain many parasites that would demand a considerable share of available energy. Apart from energy considera- tions, however, the relative scarcity of food and small size of fish in the deep sea might account for the paucity of parasites (e.g. digenetic trematodes, nematodes and acanthocephalans) that require intermediate hosts. On the other hand, perhaps the midwater fishes do have as many parasites per body weight as do the offshore benthic fishes that are much larger and that are invaded by relatively many parasites. Comparative studies that might answer this question have not been made.

Very few measurements of metabolic rates of intact, living deep- water fishes have been published. It is diflicult, therefore, to find a meaningful measurement of metabolism. One might apply the electron transport system assay (Packard et al., 1971) but we have no standards for measurement or knowledge of the fish’s caloric demands. A consideration of parasite-host relationships in deep-water animals, from a physiological point of view is, at the present time, almost impossible. Some recent studies on the effects of low temperatures and high pressures on fishes and invertebrates provide the basis for speculation on the effects of these environmental parameters on deep- sea parasites.

Most investigations on the effects of high pressures on marine organisms have involved subjection of surface-dwelling species (e.g. MptiZus, crustacea, bacteria) to increasing pressures. Conclusions from such experiments are often extended to animals that normally live in the deep sea. Such extensions are hazardous to make, and may be misleading or entirely false. Off-shore benthic fishes, for example, may live at a temperature of 2°C where the pressure is 340 atm (6 000 lb/in2). Ideally, here is where these environmental factors should be studied, but until adequate technology is developed we must make every effort to approximate natural conditions in our experimental designs.

Zobell (1970) has found that the metabolism, kinds of enzymes, and proteins of shallow-water bacteria are significantly different from those in similar species dwelling in deep water at 300-1 200 atm pressure. The most pronounced effects of pressure are on enzymes, not on DNA or RNA. The most pressure sensitive enzymes are oxidases,

PARASITES AND FISHES IN A DEEP-SEA ENVTRONMEN" 133

peroxidases, hydrogenases, etc., that are concerned with energy- yielding reactions. On the other hand, the hydrolytic enzymes in general are pressure tolerant. For example, alpha amylase can withstand 5 000 atm pressure for many days. Permeability of membranes and enzyme stability are limiting factors, however, that may operate long before the effect of pressure. Baryphylic organisms c m often be brought from the deep sea to the surface where they may live for a few hours or days, but cannot grow.

Hochachka (1971) studied enzyme mechanisms in temperature and pressure adaptation of off-shore benthic organisms. He restricted his inquiry " to immediate effects of temperature in comparison with effects of pressure upon enzymes of deep sea organisms ". He reminded the reader that " whereas temperature affects all chemical reactions in the same way (by altering the kinetic energy of the reactants), pressure activates some, retards some, and does not affect others. What is more, pressure can bring about all three of these effects on a given enzyme-catalyzed reaction depending upon the temperature, or more precisely, upon the enzyme conformation adopted at different temperatures. It is evident, therefore, that from a functional and evolutionary point of view, pressure is an entirely different kind of physical parameter than is temperature, . . The wide abundance of benthic and mesopelagic organisms which thrive under high and/or variable pressures indicate that the enzymatic problems imposed by this parameter are circumvented in nature." Hochachka emphasized that in benthic fishes, whether pressure accelerates maximum velocities, does not change them, or retards them, enzyme-substrate and enzyme- modulator af i i t ies are largely insensitive to pressure. He based his conclusions, however, on studies of isolated tissues. The same conclusions need not apply to whole animals because of the great variety of enzymatic steps that are involved in the functioning of the intact body.

Teal (1971) has provided evidence that, in predaceous mesopelagic animals (decapods) taken from off Bermuda and in the Sargasso Sea, the " metabolism is so arranged that the effects of decreasing temperature are offset by an equal and opposite effect of pressure ". Thus for some species there appears to be a constant metabolic rate over the depth range. The mesopelagic animals, unlike the epipelagic species, perhaps cannot afford to take advantage of the lower temperatures at depth to reduce their metabolism. Mesopelagic species live in water that is relatively poor in food, so they must have the energy to capture food during the entire 24-h period when they are migrating up and down in the water column. Teal and Carey (1967) suggested that it is

134 ELMER R. NOBLE

to the advantage of some midwater species to have pressure effects, and to others to be relatively free from pressure effects.

Childress (1971) compared metabolic rates of different species of deep-water animals (euphausiids, sergestid shrimps, amphipods, mysids, ostracods and the fishes Nectoliparis pelagicus Gilbert & Burke and Melanostigma pammelas (Gilbert)) collected from the California coast. He found that the mimals living at greater depths had lower metabolic rates than those living in shallower waters. At 0-400 m the mean respiratory rate was 12.6 mg 0, (kg dry wt)-l min-l ; at 400-900 m it was 4.5; and at 900-1 300 m the rate was 1.2. His data include respiratory rates (minus those of microbial contaminants) that the animals maintained between 70 and 30 mm Hg of 0, as they consumed the oxygen in a closed chamber in the laboratory. Pressure effects seem not to be great enough to explain the observed effects. Childress believes that the lower respiratory rate is related to the general reduction of body musculature and the concomitant increase in fat storage tissues. Such a relationship, he points out, may be an adaptation to increasing scarcity of food at increasing depths and the exclusively predacious habits of the animals. He concluded that “ Zooplankton may make a rather small contribution to the total oxygen consumption at greater depths in the oceans.”

Smith and Teal (1973) have provided additional evidence that the metabolic activity of deep-sea benthic communities is low. They measured the in situ oxygen uptake of sediments at 1 850m near Cape Cod, New England. There was no residual oxygen after the addition of formalin, indicating that the uptake was due to biological activity (“ community respiration ”). This uptake of oxygen was two orders of magnitude less than uptake of shallow depth sediments.

In any event, deep-water invertebrates and fishes me well adapted to high pressures and low temperatures, and any changes in metabolism would seem to be related t o the energy needs of individual animals. Deep-water crustaceans are known to be obligatory intermediate hosts for larval trematodes and nematodes that utilize fishes as definitive hosts. Many mesopelagic crustacea migrate to the surface, or to within 200 m of the surface, each night. The parasites within these animals must also be able to adjust their metabolism to meet their own metabolic needs, or be relatively insensitive to changes in pressure and temperature.

IV. FISHES AND THEIR PARASITES The foregoing presentation of major characteristics of the deep

ocean environment provides a background for discussing the state of


parasitism in these habitats, and for speculating on reasons for differences in the parasite-mix ( = parasitocoenosis) that have been observed in fishes inhabiting the several depth zones. Marshall (1971) described in detail some of the adaptive features (e.g. those relating to sensory systems, swimbladders) in these fishes, and they need not be repeated here. Some of his conclusions and generalizations that may be related to parasitism, however, will be mentioned.

After a few remarks on fishes in general, a tabulation of parasites to be found in a small sample of hosts will be presented. Examples will be selected from each of the major depth zones, and are taken from the relatively few papers that attempt to report most, or all, of the parasites infecting a given fish species. Many more collections and identifications of parasites must be made before a typical pattern of parasitism for midwater and deep benthic zones of each ocean can be assured, but sufficient records are available on which to establish provisional conclusions.

A. Organization and beltaviour of deepwater Jishes The chief morphological differences between mesopelagic and bathy-

pelagic species were tabulated by Marshall (1971) as in Table I. Bathy- pelagic species have a reduced specific weight and much of the soft tissue assumes a gelatinciis consistency. The average water content of tissues of the deeper-dwelling species is considerably higher than in shallow-water fishes.

An important behavioural difference is the habit of most mesopelagic species of migrating to the surface or near the surface each night. If the fishes feed at night upon a variety of organisms different from those available in deeper waters, the kinds of parasites that might be acquired would probably be different from those found in fishes that do not rise to the surface. If these surface parasites persist in the hosts when carried to mesopelagic or bathypelagic zones, they have to be " pre-adapted " to major changes in temperature and pressure, or able to make appropriate metabolic changes as they descend.

The bathypelagic fishes and those mesopelagic species that do not rise to the surface maintain a neutral buoyancy that is facilitated by fat in the liver and swimbladders, low water temperature, density and viscosity, as well as by the stability of these factors. Fat also functions as an energy reserve. The swimbladder is often absent, thus relieving the fish of the necessity of actively regulating its specific gravity.

A mention of reproductive behaviour is pertinent to a consideration of parasitism because larval fishes commonly live and develop in surface

A.Y.B.--II 6

136 ELXER R. NOBLE

TABLE I

Meaopelagic, plaakton- conauming species Featurea Bathypela& speciea

Colour Photophores

Jaws Eyes

Olfactory organs

Central nervous system

Myotomes Skeleton

Swimbladder

Gill system

Kidneys

Heart

Many with silvery sides Black Numerous and well developed Small or regressed in

in most species gonostomatids ; a single luminous lure on the females of most ceratioids

Relatively short Relatively long Fairly large to very large, Small or regressed, except in

with relatively large dioptric parts and seneitive pure-rod retinae

Moderately developed in both Regressed in females but large in sexes of most species

the males of some anglefishes

males of Cyclothone spp. and ceratioids (most species)

Weakly developed, except for the acousticolateralis centers and the forebrain of macrosmatic males

Well developed in all parts

Well developed Weakly developed Well ossified, including scales

Usually present, highly

Gill filrtments numerous,

Weakly ossified ; scales usually

Absent or regressed

Gill filaments relatively few with a reduced lamellar surface

Relatively small, with few numerous tubules tubules

absent

developed

bearing very many lamellae

Relatively large with

Large Small

waters before descending to deep layers. The following quotation is from Marshall (1971).

The reproductive adaptations of mesopelagic and bathypelagic fishes are correlated with their life history patterns. The eggs, which are probably shed and fertilized at depth, develop as they rise toward the surface. The larval existence is certainly passed in the euphotic zone, where the young find such suitable food as larval invertebrates and small copepods, dependent themselves on phytoplankton. During and after metamor- phosis the young move down to the adult living space. The eggs and young of bathypelagic fishes thus run a greater vertical gauntlet of physical changes and predation than those of mesopelagic species. A population of a black Cyclothune, a gulper eel, or of an anglerfish must thus have an overall fecundity to more than offset relatively great inroads

PARASITES AND FISHES IN A DEEP-SEA ENVIRONYENT 137

of mortality. But we have seen that the organization of bathypelagic fishes is pitched at a level to conform to their food-poor surroundings. How, then, do they manage to produce enough eggs? We should keep in mind that recent work on the California emdine indicates that reproduction accounts for only about 1 % of the energy consumed during its life.

B. Parasites of $shes-Introduction

At the beginning of this review the following question was asked. Does the deep ocean environment engender some attributes of parasitism that are different from those in other kinds of habitats? Since any answer to this question must be based on a knowledge of parasites in fishes living in other types of habitats, I shall list the kinds of parasites reported from a sample of fishes taken from shallow marine waters. Generous use will be made of tables from Polyanskii (1965) because his paper was one of the first to include lists of parasites compiled from a large number of different kinds of fishes, and to interpret collection data from a broad ecological point of view. These data will provide a basis for comparisons of parasitism in shallow water fishes with that in deep environments. Polyanskii mentioned several instances where fishes living in the Barents Sea had fewer kinds of parasites than in the same species of fishes in other waters. Neverthe- less, when the total picture presented by Polyanskii (he studied 46 species of fishes) is compared with the total picture shown by a group of midwater and deep benthic fishes, a different pattern of parasitism emerges for each zone in the water column. Comparisons made on the basis of this kind of broad survey reduces the importance of precise species identification, but accurate identifications will have to be made before we can establish the extent of " uniqueness " for each zone.

Most of the genera of deep-sea fishes apparently have not been examined for any of their parasites. Only a few of the thousands of species of well-known marine fishes have been systematically examined for all of their parasites. The majority of those that have been studied are commercially important species such as salmon, cod and herring. The f i s t group of fishes will represent those that live in tide pools and other inshore areas. The second group will represent offshore, far- ranging species, some of whom reach considerable depths (e.g. cod). A third group will represent midwater fishes that usually do not appear at the surface except during nocturnal vertical migrations. Finally, the benthic fishes will be represented by a larger number of species, with emphasis on the family Macrouridae.

The literature does not provide much choice of examples, and

138 ELMER R. NOBLE

certainly not an opportunity to select a random sample for each zone of the water column. Many large families of fishes, such as the bathypelagic Melamphaedidae and the deep benthic Brotulidae, Liparidae and Moridae, will not be included because little or nothing is known about their parasites.

C. Inshore $shes

The following five examples of fishes that live along the shore are selected because sufficient work has been done with them and their parasites to be statistically significant, and because they represent enough variety of species to suggest a pattern that may be considered typical of a shallow-water marine environment. The literature contains many more examples that could be included to corroborate the conclusion that inshore fishes harbour many kinds and numbers of parasites.

1. Bathygobius fuscus (Rappell), family Gobiidae

During 1961 to 1962 I collected 150 specimens of Bathygobius fuscus from tide pools along the coast of Oahu, Hawaii. This fish is also found on the western Pacific coast from southern Japan t o Australia and Indonesia, and west to India and Africa. My specimens lived in water with temperatures ranging from 22.6' to 34*8'C, and salinity from 33.68%, to 36%,. Food of the hosts in Hawaii consisted of small crustacea, insects, arachnids, snails, polychaete annelids and small fish. Parasites found, and per cent of fish infected, were :

Trichodina sp. (Ci1iata)-on gills, 21 % Coccompa sp. (Myxosporida)-in gall bladder, 8 % Nematodes (larvae)--on liver surface, 1.2% Capillaria sp. ova (Nematoda)--in liver, 1.2% Metacercarial cysts (Digenea)-in mesenteries, 2.0% Coitocaecum bathygobium (Digenea)-in intestine, 14% Plagiorchis sp. (Digenea)--in intestine, 0.62% Digenea adult unidentified-in intestine, 4.4% Metacercarial cysts (Digenea)-intestine, 12% Spirocammalanus sp. (Nematoda)-in intestine, 10% Cestode cysts, unidentified-in intestine, 10%

The variety of parasites was high but the numbers of any one species of helminth (except cestode cysts) in any one host was generally below five. There was considerable variation in both kinds and numbers of parasites in different geographic locations, due probably to differences in availability of infected intermediate hosts. These observations


emphasize the necessity of sampling a host from more than one population if any generalizations concerning the extent of parasitism are sought.

2. Myoxocephalus scorpius (L.), family Cottidae One hundred and thirty-three of these “ short horned sculpins ”

were obtained in the intertidal zone in gulfs and inlets of east Murman (Barents Sea) and sometimes “ directly from the littoral ”. The fish is a benthophagic predator, feeding chiefly on benthic crustaceans, molluscs, polychaetes and small fish. Polyanskii (1955) listed 24 different species of parasites from both fingerlings and older fish (Table 11). He stated that “parasites are so numerous that local human populations do not use the sculpin for food ”. TABLE 11. PARASITES OF 133 SPECIMENS OF TEE COMMON SCULPIN Myoxo-

cephrc2w, 8cUrpiw (L.) FROM THE BARENTS SEA (From Polyanskii, 1955)

Name of parasite Organ

1

2

3

7

8

Trichodina cottidarum Dogie1 (f. cottidarum)

Ceratomyxa longispina Petruschevskii

Myxidium inourvaturn Th6lohan

Myxoproteue &re& sp. nov.

landio2ce Levinsen Prosorhynchue

aqmmatue Odhner P . 8quamatue, meta-

cercariaa Podocotyle atomon

(Rudolphi) Helicometm plovmomini

Isaich

Qy?.ochiylua gr&-

Gills

Gall bladder

Gall bladder

Urinary bladder

Gills and fins

Stomach, intestines

Skin, musculature

Intestines

Intestines

73.7

9.8

2.3

0-75

2.3

53.4

1.5

69.9

0.75

From individuals to massive invasions

From individuals to massive invasions

Few plasmodia and spores Massive

infestation 1-14

1-142

1

1 4 4 8

1

TABLE 11-continued

Name of paraaite Organ

9

-10

11

12

13

14

16

16

17

18

19

20

21

22 23

24

Neop lwi~ oculatua (Levinsen) metacercariae

Hernium levinaeni Odhner

Brachyphllua crenatus (Rudolphi)

Derogenm p r a r b t a

(Miiller) Benarchm miilleri ' (Levinsen) Scolex polyrnorphua

Rudolphi

Bothriooephlua ecorpii (Miiller)

Pyramicocephalua p h o m m (Fabricius) larvae

Contracxxcum adurnum (Rudolphi)

C . aduncum, larvae C. adurnurn, larvae

Anieakie sp., larvae Aniaakis sp., larvae

Anieakis sp., larvae Terranova deoipiena

(Krabbe), larvae T . decipiena, larvae T . decipiena, larvae

Echinorhynchua gadi

Corynosorna etrurnosum

C. sememne Forsell Ottonia bmnnea (Johannson) Lernaeocera bramhidi.3

Zo6ga

Rudolphi

(L.), larvae

Intestines 19.6 1 4 6 1-10

Fins 20.3 Stomach 11-3

Stomach 0.76

Stomach 68.6

Stomach 3.3

Intestines 6.3

Intestines 87.9

Body cavity, 6.3 mesenteries

Stomach, intestines 76-9

Liver surface 6.0 Body cavity, 32.3

Liver surface 44.4 Body cavity, 61.7

Intestines 7.4 Muscles 70.7

mesenteries

mesenteries

Liver 42.1 Body cavity, 39.1

Intestines 2.3 mesenteries

Mesenteries 0.78

Mesenteries 1-6 Gills, operculum, body 12.8

Gills 0.7 surface

1-7 - 1-2 -

- 1

1-17 1-10

1-4 -

From . - individuals to several hundred From 1 to 28

strobilae 1-9

1-24

1-3 1-20

1-100 1-120

1-3 1-63

1-20 1-20

-7

1

1-3 1-4

6

-

-

1-10

- 1-10

1-10 1-10

- 1-10

1-6 1-6

- -

- - -


3. Rhacochilus vaca (Gard), family Embiotocidae Wares (1971) made an ecological study of parasitism in 62 specimens

of this (( pile perch ” collected in Yaquina Bay at Newport, Oregon, U.S.A. The fish are carnivorous feeders, obtaining food from the bottom or from protruding surfaces. Stomach contents indicated that the principal items of diet were : barnacles, mussels, clams, crabs, mud shrimps and tube-dwelling amphipods. A list of parasites is given below. Note that of the 11 genera and kinds, 6 are digenean trematodes belonging to 4 families. None of the hosts was heavily parasitized, and the only parasite infecting young-of-the-year fish was the copepod, Clavella sp. Cnidospora Digenea

unidentified myxosporidian cysts, on gills

Family Bucephalidae Prosorphynchw sp. metacercariae in heart, liver, I kidney

1 9 Rhipidocotyle sp. 9 ,

3 , Bucephalopsis sp. Y ,

Family Hemiuridae Family Monorchiidae Telolecithw pugetensis Lloyd and Gilbert

Family Opecoelidae

Superfam. Spiruroidea unindentified spiruroids, immature in liver Family Cucullanidae

Family Caligidae Family Lerneopodidae Clavella sp., on gills.

Derogenoides sp., 3 adults in liver

1 adult in the intestine Uenitocotyle sp., 1 adult in intestine

Nematoda

Cucullanzts sp., adults in intestine

Lepeoptheirw sp., on gil ls Copepoda

4. Tautogolabrus adspersus ( Walbaum), family Labridae Sekhar and Threlfall(l970) tabulated the parasites of 808 specimens

of this fish, called r r cunner ” collected along the shores of Newfound- land, Canada. They were caught with a rod and line or with the aid of a chemical that kills or paralyzes fish. Stomach contents were not examined. The fish yielded 10 species of digenean trematodes, 5 of cestodes, 6 of nematodes and 1 acanthocephalan ; a total of 22 species. Apparently protozoan parasites were omitted.

5 . PlatJishes (Order Pleuronectiformes) There are about 500 species of flatfishes, such as halibut, plaice,

sole, dabs, tonguefish, turbot, etc., most of which are also called flounders. These fish are almost entirely confined to coastal seas, where they live on sandy bottoms. Almost all of them are carnivorous

142 ELMER R. NOBLE

and heavily parasitized, each having from 15-25 species of parasites including Myxosporida, monogenean trematodes, digenean trematodes, larval and adult nematodes, acanthocephala, copepods and larval and adult cestodes.

These five representatives of parasitism in inshore fishes indicate a pattern of abundance of species, although not always of numbers, of parasites. The most common kinds are myxosporidan protozoa and digenetic trematodes.

Before moving to deep waters a mention should be made of parasitism in fishes inhabiting the offshore open ocean at depths above 100 m. As one might expect, salmon, mackerel and other far-ranging fishes that feed upon a great diversity of plankton and nekton of the sunlit surface waters harbour many species of parasites. About 50 species, including cestodes, digenetic trematodes of which the majority are didymozoans (at least 26 species), 10 or more species of crustaceans, acanthocephalans and nematodes have been reported from the skip- jack tuna, Euthynnw pelamys (L.).

D. Selachians

Sharks, rays, skates and chimaeras are distinguished, from a parasitological point of view, by harbouring a wide variety of cestodes or cestodarians in their intestines. These parasites are rarely found elsewhere, and little is known about their life histories. About 15 species of these benthic fishes live below 2 000 m. Only two representatives of the group will be mentioned here.

1. Raja radiata Donovan, family Rajidae

Skates of the family Rajidae live chiefly on the bottom or close to it, often partially buried in mud or sand. They are omnivorous, feeding primarily on molluscs, annelids, fish and large crustaceans such as crabs and lobsters. They lay large eggs deposited in leathery oblong cases, and are often caught in great numbers in otter trawls.

Carnivorous benthic fishes, according to several writers, especially Russian workers, are infected with relatively many parasites because of the diversity of food on the ocean floor. As expected, therefore, Raja radiata has one or more representatives of all the major groups of parasites. An early tabulation was that of Polyanskii (1955) who dissected 15 specimens and recovered 21 species of parasites.

In 1969 Laird and Bullock reported the presence of Trypanosoma rajae Laveran & Mesnil, and Haemogregarina delagei Laveran &

PAEtASlTES AND FISHES IN A DEEP-SEA ENVIRONMENT 143

Mesnil, in mixed infections from this host collected at St Andrews, Canada.

The most commonly reported cestode from the genus Raja is the tetraphyllidean, Acanthobothrius van Beneden. Williams (1969) found 12 species of the cestode in 11 of 26 elasmobranchs caught off the British Isles. The parasite was especially abundant in Raja spp. Williams reviewed the literature on the parasite and he listed 69 species which he accepted as valid. In his host list he included 22 species of Raja in addition to R. radiata. Goldstein (1967) also reviewed the genus Acanthobothrius and listed 44 species which he considered to be valid. Part of the criteria for establishing validity were differences in host and locality. He listed several hosts for many species of tapeworm, whereas Williams believed that these worms are strictly host-specific. The taxonomy of the genus is, however, still confused, and a large number of the descriptions are apparently of little value in species determination. Williams emphasized the importance of reserving judgment on the question of host specificity until complete life histories are known.

The following genera of monogenean trematodes have been reported from Raja radiata by several authors : Calicotyle, Bajonchocotyloides, Nerizocotyle, Nicrobothrium, Pseudumnthocotyla, Empruthotrema, Thau- mtocotyle, Dictyocotyle and Acanthocotyle. In a study of parasites from elasmobranchs from the coast of Newfoundland, Threlfall (1969) examined 17 specimens of Raja radiata and found: the copepod, Schistobrachia ramosus (Krayer) ; the monogenean, Pseudacanthocotyla verrilli (Goto) ; the digenean, Otodistomum cestoides (van Beneden) ; the cestodes, Trilocularia gracilis (Olsson), Phyllobothrium sp., Scypho- phyllidium giganteum (van Beneden), Anthobothrium cornucopia (van Beneden) ; and the nematodes, Contracaecum clavatum (Rudolphi), Eustoma rotundatum (Rudolphi), Anisakis type larvae, and Porro- caecum type larvae. The average number of parasites per infected fish wans no greater than three except for the cestode, A . cornucopia (7.0) and the nematode, E . rotundaturn (6.25). The highest percentage of hosts infected with any one parasite was 23.62% for E. rotundaturn. Kabata (1970) described the copepod, Schistobrachia tertia from R. radiata taken from coastal British Columbia. The benthic habitat plus a wide variety of food is again correlated with a large variety of parasites.

2. Chimaera monstrosa (L.), family Chimaeridae Chimaeras live near the bottom in coastal waters at depths of at

least 2 500 m. They range in length from about 600-1 800 mm (2-6 ft),

144 ELMER R. NOBLE

and apparently are more active by night than day, and are carnivorous, feeding on small invertebrates and fishes. The two most common and most diverse genera are Chimera and Hydrolagus. 0. ?nm..strosa occurs in the north Atlantic in relatively shallow waters (200-600 m), but most chimaeras dwell in considerably deeper waters. This genus is very old and hence is of unusual interest to parasitologists. The most characteristic feature of parasitism in chimaeras is the presence of Gyrocotyle spp. in the spiral valve attached to the mucosa. At least ten species of this genus have been described from C. monstrosa. Other parasites include the aspidogastrid, Macraspis elegans Olsson, reported by Brinkman in 1957 from the coast of Norway; the fluke Plagioporus mimtus Polyanskii often present in large numbers in the intestine; metacercarial cysts of the fluke Otodistomum veliporum Dolfuss ; and juvenile stages of the copepod, Vanbenedenia chimaerae Heegaard, from chimaerids in Australian waters. This copepod was studied in detail by Kabata (1964) who found that it appears to be limited to the claspers of its host where as many as 50 parasites may be crowded on one fish.

A similar pattern of parasitism has been reported from the related genus Hydrolagw occurring in both the Pacific and Atlantic oceans, and caught at depths to about 2 500 m. Van der Land and Templeman (1968) described two new species of Gyrocotyle from H . afinis (Brito Capelo) collected from the Canadian east coast.

From one to seven adult Gyrocotyle have been reported in one fish, but generally only two adult parasites are found. Halvorsen and Williams (1968) agree with several earlier investigators that " the establishment of two Gyrocotyle in one host follows a mass infection with larvae ',. These authors examined about 90 Chimaera molzstrosa caught in Oslo Fjord, Norway, and they observed that infection was correlated with the length (age?) of the fish. Those fish with a length of 13-19 cm had an incidence of l l .2%, while 96.4% of the fish measur- ing 30 cm or longer were infected. The explanation for this difference appears to be based on feeding habits of the host. Most Chimaera shorter than 20 cm have a prominent yolk sac on which the fish relies for food. After this size they feed actively on polychaetes, cumacean crustaceans and other invertebrates. This correlation between host size and parasite incidence suggests that Chimaera acquires the worms by ingesting larval stages. Manter (1961), however, suggested that larval Gyrocotyle rugosa (Diesing) from Callorhychus milii (Bory de St Vincent) may penetrate the gills or other surface area.

The mechanism which allows only two adult Gyrocotyle to become established on one host is unknown, but Halvorsen and Williams (op.


oit.) suggested that this phenomenon is ‘‘ the result of a regulation mechanism within the parasite population in relation to the carrying capacity of the habitat ”. Studies on population dynamics of other helminth parasites in fishes provide a basis for this suggestion. Hopkins (1959) stated that only one of 200 Proteocephalus Jiliwlli (Rudolphi), a tapeworm in the intestine of sticklebacks, reaches fd maturity, while 199 die from unknown causes. Chubb (1963) described a dynamic equilibrium between the tapeworm Triaenophorus nodulosus (Pallas) and the pike Esox lucius L. Halvorsen and Williams stated that the helminths might condition the habitat by secretions (pheromones?) that influence behaviour and development of other individuals in the population of worms.

Dienske (1968) found the following parasites in a survey of 215 specimens of Chimaera monstrosa collected in or near Trondheimsfjord, Norway.

Aspidogastrea

Digenea Taeniocotyle elegans Olsson, in gall bladder or gall duct.

Chimaerohemecus trondheimensis (van der Land), in dorsal aorta. Metacercariae encysted in gall duct walls and esophagus.

Calicotyle aflnis Scott, on walls of cloaca. Chimaericola leptogaster Leuckart, on gills.

Qyrocotyloides nybelini Furhmann, in intestine. Qyrocotyle urna Wagener, in intestine. Qyrocotyle confusa van der Land & Dienske, in intestine.

Larval ascarids ( 2 ) encysted in wall of ovary.

Vanbenedenia krayeri Malm, on anterior dorsal fin.

Monogenea

Gyrocotylida

Nematoda

Copepoda

Other parasites listed by Dienske as having been found by others in Chimaera are : the digenean Plagioporus minutus Polyanskii, a very small worm inhabiting the intestine ; the leech Calliobdella nodulifera Malm, on the skin of the head ; the copepods Caligus curtus 0. F. Miiller, and C. r q a x Milne-Edwards, both on the skin ; and the isopod, Aega monophtalma Johnston, one specimen on a pectoral fin.

Many studies of parasite size vs. host age have been made, but few of them have been concerned with deep-sea parasitism. Dienske (op. cit.) compared the weights of two species of Qyrocotyle with the weights of their hosts and he found a marked increase in parasite weight of G.

146 ELMER R. NOBLE

urna with increase in size of the host. The results “ are highly sug- gestive of the presence of a long life-cycle in Gyrocotyle.” Figure 4 depicts the incidence of each of five species of parasites in five length- classes of hosts. Note that G . urna has a relatively high incidence in all length groups, reaches almost to 100% in hosts with a length between about 35 and 48 cm, then drops to about 70% in the largest hosts. Calicotyle in the cloaca has a very low incidence in the smallest hosts, rises to about 50% in medium size hosts then drops to about 5% in the largest hosts. Taeniocotyle in the gall bladder appears to occur only in larger hosts, while the copepod, Vanbenedenia, is

I00

80

rlicotyle affinis

Chimaera monstrosa, average of length class

FIQ. 4. The most common parasites of Chimaera monetrosa L. from the Trondheimsfjord. (After Dienske, Incidence( yo) plotted against the average of each length class.

1968.)

practically restricted to small hosts. These differences are probably related to differences in life cycles of the parasites, and migratory and population densities of the hosts.

Dienske (op. cit.) stated that “We now know eight species of parasites that regularly occur in or on Chimaera monstrosa, and which do not occur in other hosts: Taeniocotyle elegans in the gall bladder, Chimuerohemecus trondheimensis in the dorsal aorta, Calicotyle afin;S in the cloaca, Chimaericola leptogaster on the gill, Cyrocotyloides nybelini, Gyrocotyle urna and C?yrocotyle confua in the intestine, and Vanbene- denia kwyeri on the anterior dorsal fin.” Since Plagioporu minutus from the intestine has been found only once, there is some question whether it is characteristic of Chimaera monstrosa. Although three


genera of chimaerid parasites are also known from hosts other than Holocephali, and three genera are also known from other Holocephali (in the Pacific), Chimaera mmstrosa has a characteristic parasite fauna of its own. A final conclusion by Dienske is that " apparently phylo- genetic or systematic host specificity plays a more important role than ecological or geographical host specificity ".

Since chimaerids are often caught in large numbers, the population densities apparently can be exceedingly high, but little work has been done on the biology of these hosts. The scarcity of reports of parasitic protozoa probably is a reflection of the interests of parasitologists making the studies.

E. Midwater $shes and their parasites-North Atlantic

1. Gadus morhua L., family Cadidue

The term " midwater " is sometimes used to designate only the mesopelagic zone, but more often it includes the bathypelagic or most of it. I shall use it to include the water column from a depth of 100 m to the benthopelagic zone.

As a representative of fishes living offshore in both the photic zone and upper mesopelagic zone, and that are carnivorous, feeding on a wide variety of animals, the cod, Gadus morhua, illustrates the great variety of parasites that fishes with these kinds of habits and habitats may acquire. There are about 70 species of deep sea cod, and most of these are confined to the northern hemisphere. The related haddock, Melanogrammus aeglejnus (L.), harbours much the same kinds and numbers of parasites. This similarity reflects the similarity of habits and habitats. The diet of these two fish is almost identical but the haddock is more exclusively a bottom feeder. More than 200 different species of benthic animals have been found in the stomachs of haddock.

Gadus morhua is widely distributed in the north Atlantic and is usually caught in depths of from 50-250 m, but it has been taken at 640 m. Maximum length is over 2 m, but the average is considerably shorter. The average weight is about 25 lb (100 kg), although a weight of 76 lb is not uncommon. The cod utilizes a great variety of food items including other fish, crustaceans, numerous kinds of molluscs and other benthic organisms. They live for 15 years or more, thereby having considerable time in which to accumulate parasites, and they have a wide-ranging habit of migration. One would expect them to have many parasites, which they do. Among the items that have been found in their stomachs are: scissors, oil cans, finger rings, rocks, corn cobs, rubber dolls, pieces of clothing and the heel of a boot.

TABLE 111. PARASITES OF 140 SPECIMENS OF THE COD (Jadua morhua morhua FROM THIE BARENTS SEA (From Polyanskii, 1966)

- 1

2

3 4 6 6

7 8 9

10 11 12 13

14

16

16

17 18

19

20

21

22 23 24 26

26 27

Name of paraaite Organ

*Octomitus inteatinalia Alexeev

Trichodina mumnanica sp.

Myxdium bergenae Auerbach *M. ov i fme Parisi *Zachokella hildae Auerbach Qyrodactylua marinua

Bykh. and Pol.

nova

Udonella caligowm Johnston Podowtyle atomon (Rudolphi) P . re@a (Creplin) Lepidapedon qadi Yamaguti Hemiurua levinaeni Odhner Derogenea varicua (Miiller) Smlex polymorphis Rudolphi

Abothrium qadi v. Bened. A . qadi, immature Pyramiwcephalus phocawm

(Fabricius)

Pseudophyllidea gen. sp.,

Ascarophia morhuae v. Bened. Aecaropka fllifomnis

Contracaecum adumwm

C. adunoum, larvae c. adumum, lmvae

hNae

Polyctnskii

(Rudolphi)

Ankakis sp., larvae Anhakia sp., larvae

Anbakie sp., larvae Terranwa decipiena

(Krabbe), larvae Echiwhynchue qadi Zoega Cd@s curtua Muller Lernaeocera branchialis (L.) Clavella uncinuta (Miiller)

*C. brevkollis M. Edwards Agga peora (L.)

Hindgut, urinary bladder

Gills Gall bladder Gall bladder Gall bladder Gills

On Cdigua curtus Intestines Intestines Intestines Stomach Stomach Intestines

Intestines Intestines Body cavity,

mesenteries, intestines

Mesenteries, intestines

Stomach Stomach.

intestines Stomach,

intestines Liver surface Body cavity,

mesenteries Liver surface Body cavity,

mesenteries Intestines Liver

Intestines Body surface Gills Gills, mouth

cavity, fins Fins, anal skin Body surface

12.1

2.1 0.7

rare 30.3 5.0

1.4 16.7 2.8 6.4

48.6 30.0 46.0

13.6 1.4

16.0

6.0

2.8 6.7

76-7

10.7 63.5

62.1 67.1

6.0 7.1

62.1 17.9 2.9

19.3

12.1 0.7

High

Low Low - -

From individuals

to several hundreds High

1-42 1-2 4-88 1-150 1-64

From individuals to several hundreds

1-3 1

1-6

1-2

1-2 1-10

1-400

1-6 1-96

1-116 1-1400

1-20 1-16

1-397 1-6 1-2 1-17

- 1

* Parasites found by workers other then Polyanskii.


Dollfus (1953) published a monograph devoted to the parasites of cod. He listed 71 species including 14 genera of digenetic trematodes. The first study of cod parasites from an ecological point of view was that of Polyanskii (1955). He recorded 27 kinds of parasites from 140 specimens taken in the Barents Sea (see Table 111). In addition to those parasites listed by Polyanskii are the following reported from other locations by several parasitologists.

Digenetic trematodes Derogenes varicw (Miiller) Genurches mulleri (Levinsen) Hemiurw communis (Odhner) and H . levinseni Odhner

Abothrium rugosum (Batsch) and A. morrhuae Cholodk Parabothrium gadi pollachii (Rudolphi) P . bulbi f erum Nybelin Bothriocephalw collariae Linstow B. ellipticw Linstow Tetrachynchw gadi-morrhuae Dies Proteocephalw simplicissimw (Leidy)

Contracaecum gadi (Miiller) Porrocaecum (probably P. decipiens Krabbe)

Haemogregarina aeglefini (Henry) Trypanosoma murmanensis (Nitkin), see Kahn, 1972 Myxobolw aeglefini (Auerbach)

Monogenetic Trematodes Pseudodactylocotyle sp.

Cestodes

Nematodes

Protozoa

2. Clupea harengus L., family Clupeidae

The herring is common on both sides of the north Atlantic and often occurs in schools numbering into the thousands. Like the cod, this fish inhabits both the photic and upper mesopelagic zones, but its maximum depth is apparently unknown. In contrast to cod, herring feed on plankton such as copepods and euphausiids. One might expect, therefore, that, although a shallow-water fish, it would harbour relatively few parasites. From 54 specimens collected in the Barents Sea Polyanskii (op. cit.) listed the coccidian, Eimeria sardinae Thdlohan from the testes (a massive invasion) ; 5 species of hemiurid trematodes from the intestine; and 4 nematodes (two each of Contracaecum and Anisakis) from the intestine and body cavity, only 1 of which wm

150 ELMER R. NOBLE

an adult. The highest incidence of infection among the helminths was 51.9% for Anisakis sp. larvae in the intestine. The second highest was 12.9% for the trematode, Derogenes varicus (Miiller) in the stomach.

A recent study of 330 specimens of herring taken from the northern part of the North Sea (Reimer and Jessen, 1972) yielded only three species of digenetic trematodes (Hemiurus luehei Odhner, Brachy- phallus crenatus (Rudolphi) Odhner, Derogenes varicus (Liihe), and the common nematode larvae, Contracaecum sp, and Anisakis sp.

A number of other parasites have been found in Clupea harengus taken in other waters. These include the myxosporidans Ceratomyxa spaerulosa Thelohan and C . auerbachi Kabata, both in the gall bladder, and Kudoa clupeidue Hahn in the body muscles; and the coccidian Eimeria clupearum Thdlohan in the liver. Compared with carnivorous fishes that feed on a much greater variety and size of organisms, the herring is invaded by a small number of metazoan parasite species.

3. Sebastes marinus (L . ) , family Scorpaenidae The rosefish, redfish or ocean perch is also common on both sides

of the Atlantic and adjacent Arctic regions. It is generally found near the bottom at depths of from 100-500 m, but in parts of its range it reaches to 1000 m. S. marinus mentella Travin is not distinguished from 8. m. marinus (L.) in the eadier literature. The parasites of the two subspecies appear to be essentially the same so I shall combine them in the comments below.

In June, 1971, I examined 23 specimens of Sebccstes marinus taken from Newfoundland coastal waters at depths of from 265-275 m. The

FIG. 6. Redtish, Sebaetea marinus, heavily parasitized by the copepod, Sphyrion lumpi. (After Sindermann, 1970.)


stomach contents were chiefly remains of fish and shrimp. I found Acanthocephala (4.3%), Digenea (8*6%), Nematoda (22%) and Myxosporida (83%). One of the trematodes was Podocotyle rejlexa (Crepl.). In 15 specimens of this fish from the Barents Sea, Polyanskii (op. cit.) reported no Myxosporida whereas 83% of mine had these

FIG. 6. Larval Trypanorhyncha (Cestoda). A. Cyst in muscle of redfish, Sebastes marinus ; B. orientation of larva within cyst : C. larva freed from cyst membrane with scolex retracted: D. details of evaginated scolex. (After Sindermann, 1970 ; redrawn from Kahl, 1937.)

protozoa ; also, Polyanskii reported 93% infection with Digenea (compared with my 8.6%), and 13% with adult cestodes (I found none). His fish had approximately the same incidence of infection with nematodes as did mine. Obviously the geographic location of the host may profoundly affect its parasite-mix. Templeman and Squires (1960) found numerous copepods (Xphyrion lumpi (Kreryer)) (Fig. 5) on the skin of redfish from the Canadian Atlantic coast. They reported a

A.H.B .-I1 7

152 ELMER R. NOBLE

definite increase in the percentage of Labrador hosts infested at about 250 m where the incidence was 0-70y0. At about 370 m it was 6.0y0. There was also an increase in numbers of parasites per 100 fish with depth. Larval Trypanorhycha (Cestoda) are also found in the muscles of this fish (Fig. 6).

4. Anarhichas lupus L., family Anarhichudidae

The wolffish is widely distributed on both sides of the north Atlantic. It is a cold-water species inhabiting bottom layers from shoal water to below 500 m. It generally feeds on molluscs, crustacea, sea urchins and starfish. In 15 specimens that I examined from Newfoundland coastal waters, most of the stomachs contained masses of brittlestars, and occasionally a few clams, snails and pieces of coral. The depth of collection of the 15 specimens ranged from 235-365 m. These fish were hosts for acanthocephala (in two fish), leeches (on eight fish), copepods (on one fish), Myxosporida (three genera in gall bladders, urinary bladders and kidneys) and digenetic trematodes in all fish. Those trematodes in the gall bladder were probably fellodistomids, and those in the urinary bladder were Lepidophyllum steenstrupi Odhner identified by Mrs M. Pritchard. A. lupus from the Barents Sea apparently are not infected with Myxosporida, at least none has been reported, but the fish have a high incidence (60-75%) of both adult and larval nematodes, mostly Contracaecum and Anisakis. These Barents Sea hosts are also infected with digenetic trematodes, acanthocephala and leeches. Haemogregarina anarchichadis (Henry) in the blood and the microsporidan, Plistophora ehrenbaumi Reichenow in body muscles, have been reported from A. lupus by several workers. The copepod, Clavellodes rugosus (Kroyer), has been abundantly recorded from A . lupus and from the other two species of this fish inhabiting the North Atlantic throughout the distribution ranges of these hosts.

F . Midwater fishes and their parasites-Eastern Paci$c and Indian Ocean

1. Fishes in general

Collard (1970) studied parasites of mesopelagic and bathypelagic coastal fishes collected primarily off California and Mexico, and he reported a marked paucity of infections as compared with other ecologically delimited groups of fishes. He examined 1 122 individuals belonging to 13 families and 44 species, and found that " Adult fishes harbour a numerically greater and more diverse parasite fauna than

TABLE IV. DISTRIBUTION OF PARASITES BY AGE AND SEX OF 1122 MESOPELAGIC FISHES (44 SPECIES) FROM THE EASTERN PACIFIC

(From Collard, 1970)

Parasites

Nematoda Anisakis sp. Contracaecurn sp. Paranisaksi sp. Terranova sp. Ascarophis ~ p . Anisakinae

Unidentifiable

Total

Cestoda Tetraphyllidea Pseudophyllidea Trypanorhyncha

Unidentifiable

Total

Trematoda Monogenea Digenea

Total Acanthocephala

Copepoda Cardiodectes Bomolochinae Chalimus Lernaeoceridae

Total

Fungi

Unknown (Lagenidiales)

Gill Cysts &Ielanized Cysts

Total

Age Sex

Adwlts Preadults Males Females Unknown

No. yo No. yo No. yo No. Yo No. yo (613) (415) (294) (319) (94)

-

81 13.2 6 1.4 30 10.2 51 15.9 37 6.0 12 2.8 13 4.4 24 7.5 3 0.4 0 - 1 0.3 2 0.6 7 1.1 2 0.4 3 1.0 4 1.2 1 0-1 2 0.4 0 - 1 0.3

16 2.6 1 0.2 4 1.3 12 3.7 39 6.3 9 2.1 20 6.8 19 5.9

184 30.0 32 7.7 71 24.1 113 35.4 . ..

26 4.2 25 6.0 9 3.0 17 5.3 20 3.2 3 0.6 13 4.4 7 2.1 1 0.1 0 - 1 0.3 0 -

14 2.2 8 1.9 6 1.8 8 2.5

1 1.0 0 - 0 - 2 2.1 0 - 1 1.0 1 1.0

5 5.3

0 - 0 - 0 - 0 -

61 9.9 36 8.6 29 9.8 32 10.0 0 -

7 3 0.4 1 0.2 1 0.3 2 0.6 0 - 7 1.1 24 5.8 1 0.3 6 1.8 3 3.1

10 1.6 25 6.0 2 0.6 8 2.5 3 3.1 5 1

_-

18 2.9 0 1.4 10 3.4 8 2.5 3 3.1 3 0.4 0 - 1 0.3 2 0.6 0 - 2 0.3 0 - 1 0.3 1 0.3 0 - 1 0.1 0 - 1 0.3 0 - 0 -

24 3.9 6 1.4 13 4.4 11 3.4 3 3.1

19 3.0 1 0.2 8 2.7 11 3.4 - -

29 4.7 5 1.2 13 4.4 16 5.0 1 1.0 38 6.1 17 4.0 16 5.4 22 6.8 0 -

67 10.9 22 5.3 29 9.8 38 11.9 1 1.0

Grand Total 365 59.5 122 29.3 153 52.0 213 66.7 12 12.7

154 ELMER R. NOBLE

pre-adult fishes. Female fishes are generally more heavily parasitized than males, and this is not caused by size differences or protandrous hermaphroditism. The parasite-mix is not significantly affected by seasonal change except when abundance of an obligatory intermediate host varies seasonally.” Table IV 1ist.s the distribution of parasites by age and sex of the hosts.

Collard (op. cit.) observed a great scarcity of metazoan parasites not requiring an intermediate host, and a higher incidence (but few numbers of parasites) of infections with larval helminths. He suggested that mesopelagic fishes serve as intermediate hosts that transport these parasites to predatory fishes in the epipelagic and bathypelagic zones. This concept envisions the mesopelagic fishes acting as a shuttle for parasites between definitive hosts at the ocean surface, and in waters below about 1 0 0 0 m. It is an intriguing idea, but with little evidence to support it. The dominant family in this study was the Myctophidae (called ‘‘ lantern fishes ”). I shall, therefore, list percentages of hosts infected with parasites for each species of myctophid numbering 35 or more individuals.

Family Myctophidae Stenobrachius leucopsarus Eigenman & Eigenman

486 specimens, 153 with parasites (31.4%). The parasite pattern of this species was typical of those encountered in the others, and consisted of : larval nematodes (Anisakis, Contracaecum, Ter- ranowa, Ascarophis) ; larval trematodes (two specimens of Lecithasterinae in one fish, “ Monilicaecum ” one in one fish, one unidentified larva in one fish) ; larval cestodes (phyllobothriid, pseudophyllid, tetrarhynch and “ cestode ”) ; and the copepod Cardiodectes medusaeus.

Triphoturus mexicanus (Garman) 120 specimens, 20 with parasites (16.6y0)

Diaphus theta (Eigenman & Eigenman) 61 specimens, 27 with parasites (44.2%)

Lampanyctus ritteri (Gilbert) 53 specimens, 34 with parasites (64.1%)

Ceratoscopelus townsendi (Eigenman & Eigenman) 39 specimens, 13 with parasites (33.3%)

Tarletonbenia crenularis (Jordan & Gilbert) 35 specimens, 6 with parasites (17.1 yo)

Symbolophorus californiensis (Eigenman & Eigenman) 35 specimens, 6 with parasites (17.1 %)

Lampanyctus australis (Thing) 35 specimens, G with parasites (17.1%).


Some of the data in the above list were taken from Collard (1968). The list emphasizes the scarcity of parasites in these midwater fishes. Only about 31% of the individuals were infected with metazoan parasites of any kind. The fishes were not examined for protozoa. Generally only one or two parasites were present, rarely adults. In order of abundance the parasites were : larval nematodes, larval cestodes, copepods, and larval hemiurid trematodes. See p. 171 for a discussion of the differences in parasitism between Xtenobrachius leucopsarus and Diaphus theta.

Myctophid fishes are also hosts t o the epizoic hydroid, Hydrichthys. McCormick et al. (1967) surveyed more than 30 000 specimens of mesopelagic fishes, representing 40 species collected from coastal Oregon, U.S.A., and they found 26 fishes from three species of myctophids (Tarletonbenia crenularis, Diaphus theta and Lampanyctus leucopsarus) to be infected with Hydrichthys sp. Six of the hydroids were located on the copepod Cardiodectes medusaeus (Wilson) living parasitically on the isthmus of the host fish with its anterior end buried in the bulbus arteriosus of the host. The incidence of infection with the hydroid was low but was highest in the fishes that migrate closest t o the surface each night. The Hydrichthys appears to be a new species but is closest to H . boycei Warren described from reef fishes living in Durban Bay, South Africa.

Noble and Collard (1970) made a study of parasites and com- mensals of midwater fishes collected from over the continental border- land of southern California and Mexico, with some comparative material from the Peru-Chile Trench, Central Pacific and the Antarctic. There were 1 0 8 7 fishes examined. In the abstract of their paper the authors stated that, Present information indicates that animal parasites of deep-water marine fishes are rarely pathogenic (as judged from macroscopic observations). Also, mesopelagic md, to a lesser extent, bathypelagic fishes harbor fewer numbers and kinds of parasites (especially adult helminths) than do other ecologically delimited groups of vertebrates. There is, in general, a decrease in numbers of parasites with depth. Those fishes that inhabit the benthic and abyssopelagic zones of the continental slopes harbor more species of parasites than do the midwater fishes. The homogeneity of the bottom and near-bottom environment fosters the diversification of species. With the exception of lern- aeocerid copepods, adult metazoan parasites rarely are found on or in midwater fishes. Monogenetic trematodes, adult digenes and acanthocephalans have occasionally been reported, but parasitic isopods and cirripeds are not known in these hosts.

The incidences, numbers and kinds of metazoan parasites were not

156 ELMER R . NOBLE

significantly different from those listed in Table IV, so they will not be detailed here. Five of the 22 host species harbouring larval nematodes responded to the infection by walling-off or depositing melanin pigment around the worms. Most of the nematodes occurred in the mesenteries and coelom, others were found in or on the liver, stomach, intestines, muscles, ceca, gonads, kidneys, heart, peritoneum and swimbladder.

Only 14 of the total fishes examined harboured digenetic trematodes, mostly unencysted mesocercariae. Monogenetic trematodes occurred on gills of three out of the 1 0 8 7 fishes, and these hosts were all Lampanyctus ritteri. In a separate study, Raphael Payne (personal communication) examined 220 mesopelagic myctophid fishes, and out of 11 genera and 12 species only seven individuals (all L. ritteri) were infected with monogeneans. He thus corroborated our conclusion that monogenean trematodes are extremely rare among midwater fishes of the eastern Pacific.

Cestodes were recovered from 77 specimens (7% of the total fish, and in 12 of 27 genera). Of these worms only three were adults (one

TABLE V. PROTOZOAN PARASITES AND MIDWATER FISHES IN

WHICH THEY WERE FOUND (EASTERN PACIFIC) (Extracted from Noble and Collard, 1971)

Protozoa

Numbers of fishes Depth Infected Examined (4

Cryptobia spp. (Mastigophora) Bathylagus wesethi Bathylagus ochotemis Leuroglosaus stilbius

Lycodopsis pacifica

Sagarnicthys abei Stomias atriventer Melanocetus johnsoni Melanostigma pammelas Antimora rostrata Anoploma fimbria Bajacalifornia burragei

Microsporida

Myxidium spp. (Myxosporida)

2 2

19

1

1 1 1

73 4 2 3

14 3

200

9

6 7 3

200 9 7 4

300 700 400

200

300 400 450 900

1700 1400 1400

Myxosporida (trophic stages) Melanostigma johnsoni 2 3 500 Triphoturus mexicanus 1 5 800 Stenobrachius leucopsarus 3 11 600 Cyclothone sp. 1 6 1100 -


in each of three species of fish) while the others were pleurocercoid larvae belonging to the orders Pseudophyllidea (21 fish), Tetraphyllidea (33 fish) and Trypanorhyncha (one fish). Numerous invertebrate species are known to be intermediate hosts for marine cestodes (e.g. copepods, euphausiids)-see Dollfus, 1964, 1967, and other papers of his series. The life cycles of midwater cestodes, however, are not known.

Protozoan parasites (Table V) reported by Noble and Collard (op. cit.) included a few flagellates (Cryptobia), Coccidia and Myxosporida from macrourid fishes. The parasites of macrourids are considered in detail on subsequent pages of this report, and are not included in the table.

2. Leuroglossus stilbius Gilbert, family Bathylagidae

The L L deep-sea smelt ”, Leuroglossus stilbius is a mesopelagic species that ranges from the Bering Sea to Columbia. It may spawn at the surface close to shore as well as offshore, and it tends to migrate to the surface each night. The mean standard length of those caught off California and Mexico is about 82 mm. They have been caught at a depth of 1 3 0 0 m but usually the range is between 200 and 700 m. These fish feed chiefly on larvaceans, salps, ostracods and copepods.

The predatory habit of Leuroglossus stilbius, and large variety of food consumed, suggests that this fish may harbour a large variety of parasites. Such is not the case. In 1968 I described the flagellate, Cryptobia stilbia, from the stomach of the fish, and in 1970 Noble and Orias described a hemiurid trematode, Aponurus californicus, also from its stomach. The only other parasites found were a few larval nematodes and larval cestodes. Out of 649 fish examined, 50% contained the trematode (an unusually high incidence of infection for midwater fishes) and 12% had the flagellate. One might assume that when half of a large population of fish is infected with a trematode, the intermediate hosts would be easy to find. We examined a great many invertebrates collected in waters inhabited by Leuroglossus, but did not find a single Apon‘urus larva. The problem of finding intermediate hosts in deep waters is discussed on p. 174.

3. Melanostigma pammelas Gilbert, family Zoarcidae

This fish ranges from southern California to Alaska, and is taken at depths from about 100-2 000 m, but usually below 500 m. Although it has been captured with bottom fishing gear it probably is a bathypelagic species rather than a benthic form. It has no swimbladder or photophores. Its habits are practically unknown. Food in the stomachs

158 ELMER R. NOBLE

of those that I examined consisted of a “ whitish mush ” containing remains of euphausiids, copepods and other small crustacea.

I have autopsied 221 specimens of Melanostigma pammelas and found the following parasites : the myxosporidan, Myxidium melan- ostigmum Noble, in 75 fish (33%), digenetic trematodes in 132 fish (60%) and larval nematodes in 24 fish (10%). The percentage of infected fish is higher than other species that I have autopsied from the bathypelagic zone. It is of interest to note that whereas the numbers of fish harbouring both Myxosporida and Trematoda (20y0), and Myxosporida plus Nematoda (2.5%) are what might be expected, the numbers with a concurrent infection of trematodes and nematodes were only 2.7% instead of the expected 13% (i.e. 10% of the 132 fish with trematodes). This observation suggests some kind of antagonism between the fluke and nematode, but perhaps some other factor is responsible.

4. Cyclothone spp., family Gonostom.atidae

The “ bristlemouth ” or “ viper fish ”, genus Cyclothone, are among the most abundant marine midwater fish in all oceans. They are small, rarely reaching more than 70 mm in length, with reduced tissues.

I mm H

FIG. 7 . The ‘‘ bristlemouth ” Cyclothone acclinidens Garman, a midwater fish from coastal California. (Drawing by Floyd DeWitt Jr.)

Cyclothone elongata (Giinther), living a t depths of from 800 to over 6 000 m almost everywhere throughout the oceans is probably the most widely distributed of all deep-sea fishes; and one of the feeblest and most fragile. Cyclothone is the smallest member of bathypelagic fish fauna and feeds on a size range of organisms from copepods to small fish.

DeWitt and Cailliet (1972) examined stomach contents of 227 Cyclothone signata Garman taken from the surface to about 600 m, and


255 specimens of C. acclinidens Garman (Fig. 7) from depth to 1 000 m, off the coast of southern California. The stomachs of C. signata contained copepods and ostracods (mostly from the upper 200 m level). Fish from 400-600 m, had significantly more empty stomachs than those from 0-400 m. C. acclinidens feeds on copepods, chaetognaths, odtracods and amphipods. The stomachs of both species of fish contained much unrecognizable material. The combination of small, weak bodies and a plankton-feeding habitat would suggest a paucity of parasites. These fish were not examined for parasitic protozoa, but not a single helminth or arthropod parasite was reported.

Collard (1968) examined 61 specimens of Cyclothone (the two species mentioned above and 15 specimens of C. pallida Garman) and he found one larval nematode in one C. acclinidens, and an unidentified “ cyst ” (probably a fungus) on the gills of each of two C. pallida. Gusev (1957) autopsied 15 specimens of C. microdon Giinther captured at depths of between 800 and 7 000 m in the western north Pacific. All of the fish were without animal parasites. I have examined 36 Cyclothone spp. for their protozoan and metazoan parasites, and found one tightly coiled nematode larva, lying on top of the brain of C. acclinidens, and myxosporidan trophic stages in the gall bladder of one Cyclothone sp. From the above brief account, it appears that one of the most abundant genera of the world’s marine fishes is probably tho least parasitized..

5. Latimeria chalumnae Smith, family Neodactylodiscidae

In December, 1966, a coelacanth was caught off Anjuan Island, one of the Comoro islands near Madagascar. Monogenetic trematodes were taken from the gills of this fish which had been preserved in concentrated formalin, and in 1971 the parasites were described by Satoru Kamegai. In 1972 he created a new family, new genus and new species for the monogenean, Neodactylodiscw latimeris. From the same fish four larval nematodes were found in washings of the body cavity, stomach and intestine. One of these worms was identified as Anisakis sp. The others were too badly damaged for identification. Four larval cestodes, Tentacularia sp. were recovered from the stomach. Kamegai suggested that the two kinds of larval helminths may have been part of the food remains (squid beaks and part of a fish) in the stomach. He noted that larval Anisakis sp. reported by Dollfus and Campana- Rduget (1956) from the stomach of a coelacanth seemed also to be accidental. Monod (1964) described a new species of isopod, Praniza milloti, family Gnathiidae, from a coelacanth.

160 ELMER R. NOBLE

G. Fishes of the Family Macrouridae 1. Macrourids as hosts

Emphasis will be placed on parasite-host relationships among the family Macrouridae because of all fishes living on the bottom of the deep oceans, this is the only family that has been studied extensively from a parasitological point of view. Of the world's marine fishes living predominately below 2 000 m, the macrourids (known as grenadiers or rattails) are the largest family in terms of numbers of species (over 300) and individuals. The Brotulidae contains the largest numbers of genera. Other large families are: Moridae, Liparidae and Zoarcidae. Benthopelagic fishes live a t depths a t least to 7 000 m. Marshall (1971) stated that, " At all events, if the success of a group is measured by its overall living space and the number of its species and individuals, then the most successful bottom dwellers in the deep sea are the macrourids, brotulids and-morids. And these fishes work, rather than wait for, their living."

Most of the macrourids are bottom feeders, but a few species are bathypelagic or mesopelagic in habitat. " Ninety per cent or more live close to the continental slopes between depths of some 200 and 2 000 m ) ) (Marshall, 1965). They are feeble swimmers and most species appear to have a limited distribution. Macrourids probably live for up to ten years, thereby having time in which to accumulate parasites. The depths at which eggs hatch are not known, but some authorities cite evidence that eggs never reach a level higher than 200 m below the surface. Few eggs have been found in plankton hauls. So far as I know, no parasites have been reported from young juveniles. Adults range in length from about 200-1 000 mm.

Macrourid fishes are carnivorous, but little or no information on food preferences of most species is available. The swimbladder often expands when they are brought t o the surface, thereby forcing the stomach to be everted out of the mouth, rendering food identification extremely difficult or impossible. Traces of food on gill rakers may help, as well as remains in the intestine. Okamura (1970b) listed the stomach contents of 25 species of macrourids caught off the Pacific coast of Japan (Table VI). Notice that the most abundant organisms are euphausiids. Prawns and fishes are common in 8 or 10 species, and polychaete annelids are almost entirely restricted to the genus Coelorhynchus. Polychaetes are known to be intermediate hosts for a few digenetic trematodes of marine fishes (see p. 178).

A gentle way of describing the difficulties and frustrations of identifying many of the macrourid species is to say that the taxonomy

TABLE VI. STOMACH CONTENTS OF 25 S P E C I E S O F MACROURID FISHES CAUGHT O F F T H E P A C I F I C COAST O F JAPAN (From Okamura, 1970)

Stomach contents (in percentage)

$shes squids euphausiids prawns crabs Gopods squillae polychaetes detritus mud sand

Number of Species specimens

examined

Squalogadus modi$catus Gadomus colletti Bathygadus antrodea Hymenocephalus striatissinaus Hymenocephalus lethonemus Hymenogadus kuronumai Hymenogadua gracilis Makimcephdus laevis Ventrifossa garmani Ventrifossa misakia Nezumia condylura Abyssicola macrochir Coryphaenoides pectoralis Coryphaenoides marginatus Coryphaenoides nmmtus Coelorh ynchus kishinou yei Coelorhynchus jordani Coelorhynchus multispinulosus Coelorhynchus kamoharai Coelorhynchus hubbsi Coelorhynchus longissinwa Coelorl6ynchu.s smithi Coelorhynchus anatirostris Coelorhynchus japonicus Coelorhynchus tokiemis

82 67 33 94 6

~ ~-

18 + + + 3

12 3

11 89 100 100 100

38 62 38 69 48

20 79 20 37 24

37 25 20 11

7 1

19

+ + + + + + + 45 +

+ 20

9 14 3

81 28 40 15 11 49

54 8 84

13 13 14 16 29 17 34 25

51 36

7 5

70 3 68

70 19

28 4 20 5

38 16

17 4 34 55

13 11 10

10 + 3 +

18 + + + + + + 5 + + + + +

20 6

15 12 9

14 19 8

14 4

16 + 10 + 12

4 24 15 21 4 + 5 + 16 5

3 5

tl M M

M !z

162 ELMER R. NOBLE

of the group is “ in a state of flux ”. McCauley (1968) described some trematodes from these fishes, and he stated that, “ The identification of the fish hosts posed some real problems . . . Almost four years were required to locate a specialist who would attempt to identify the carcases of the fishes which had been autopsied.” Figure 8 illustrates three species. For biological studies of macrourids see Marshall, 1965 and Phleger, 1971.

2. Parasites of Macrourids--general In my own laboratory and at other research centres in California,

Newfoundland, London and Norway we have autopsied about 275 macrourids comprising 17 species. Table VIII, p. 167, lists data from nine of these species. The others are not included because fewer than ten individuals per species were examined. The list, however, is suf- ficiently large to furnish a pattern of parasitism for macrourid fishes. In order to compare the macrourids with two non-benthic species I have included Melanostigma pammelas, a bathypelagic species (see p. 157), and Gadus morhua, an offshore epipelagic and mesopelagic species (see p. 147). Note that M . pammelas is infected with only three (Digenea, Nematoda and Myxosporida) of the eight groups of parasites, while only the Microsporida is missing from G. morhua. The only macrourid that is comparable to +he cod in percentages of fish infected is Macrourus berglax Lacepbde collected off the coast of Newfoundland.

The reasons for differences in incidences of infections are difficult to assess. Macrourus berglax, with heavy infections of many parasite species, was collected in relatively shallow waters (330 m). Probably the wide variety of available food items was a major factor. The fewest kinds of parasites were in M . rupestris (Gunnerus) from the coast of Norway (Noble et al., 1972), and in Coryphaenoides serrwla Bean from off California. The former fish apparently feeds almost exclusively on shrimp and small crabs. The latter lives at considerable depths (4 000 m) but only 12 specimens so far have been examined.

The most common parasites in macrourids are Myxosporida, and almost as common are larval Nematoda. The others, in order of decreasing percentages of infection are : Digenea, Cestoda, Copepoda, Monogenea and Microsporida. The scarcity of recorded Microsporida may be partly due to the difficulty in recognizing their spores in light infections without cysts. Some details on species of the parasites are presented below. 3. Protozoa

Myxosporida in macrourids generally invade the gall bladder, urinary bladder or kidney, sometimes all three at once. Every species

FIQ. 8. Three examples of the deep benthic family Macrouridae. (a) CoeZorhynchus jordani Smith & Pope ; (b) Nezumia proximus (Gilbert & Hubbs) ; (c) Coryphaenoides acrolepis (Bean). (After Okamura, 1970a.)

164 ELMER R. NOBLE

FIQ. 9. Sample genera of the Order Myxosporida (Protozoa) infecting maorourid fishes. A. Myxidium sp. from the kidney of Coelorhynchus scaphopsis. B. Ceratomyxa sp. from the gal1 bladder of Coryphaenoides acrolepis. C. Auerbachia sp. from the gall bladder of Macrourus berglax, Coryphaenoides pectoralis and Coryphaenoides acrolepis. D. Leptotheca (?) sp. from the kidney of Macrourus berglax and the urinary bladder of Coryphaenoides acrolepis. E. Leptotheca sp. from the gall bladder of Coelorhynchus scaphopsis, Coryphaenoides pectoralis and Coryphaenoides acrolepis. F. Myxidium spp. from the gall bladders of Macrourus rupestris, Nezumia stelgidolepis, Nezumia bairdi, Coryphaenoides abyssorum, and Coryphaenoides s e m l a . G . Myxoproteus sp. from the urinary bladder of Coryphaenoides acrolepis. H. Zschokkella sp. from the kidneys of Macrourus berglax, Coelorhynchus scaphopsis and Coryphaenoides acrolepis, and from the urinary bladder of Nezumia stelgidolepis, Coryphaenoides abyssorum and Coryphaenoides serrula. (Drawings by Timothy Yoshino.)

PARASITES AND FISHES I N A DEEP-SEA ENVIRONMENT 165

of host that I have examined has been infected with at least one species of this protozoan parasite. Figure 9 illustrates the genera that have been found in my laboratory. The most common genus was Myxidium, in seven species of hosts ; and the second most common was Zschokkella, in six species of hosts. No species of host had more than three species of Myxosporida, with the exception of Coryphaenoides acrolepis Bean in which five species of these cnidosporans were recovered-two from the gall bladder, and the others from the kidney and urinary bladder. More time was spent (by Timothy Yoshino) in examining C. acrolepis for protozoan parasites than was spent on the other species of hosts. Given an abundance of time, talent and fishes, many more protozoan parasites would probably be found. Two recent papers (both in press) devoted to the study of myxosporidan parasites of macrourid fishes are: Yoshino and Noble (1973a and 1973b). These authors found that of the macrourids studied to date, Cory- phaenoides acrolepis possesses the richest fauna of Myxosporida, and that Myxidium coryphaenoidium Noble has the widest geographic distribution and inhabits the most variety of hosts.

TABLE VII

Number of specimens Site of

infected infection Fish

with Eimeria

Coryphaenoidea acrolepis 2 of 51 intestine ( I ) , gall bladder (1) Chalinura Zanespu 2 of 2 intestine Cynornacrurus piriei 2 of 2 intestine Macrourus berglax 3 of 21 kidney (2), heart (1) Nezumia bairdi 1 of 6 stomach Nezumia stelgidolepis 16 of 35 intestine, 1 also in gall bladder

Other protozoan parasites of macrourids have rarely been reported. Coccidia (Eimeria spp.) were recovered from fishes in Table VII.

Lom (1970) found oocysts of Eimeria sp. in the swimbladder, kidney, blood, gut mucosa, muscles, gall bladder and urinary bladder of Macrourus berglax. The parasites appeared to be pathogenic because they formed pasty, whitish masses in the kidney. The same fish was commonly infected with a new species of the microsporidan, Nosema (Lorn, personal communication).

In 1971 Orias and Noble described Entamoeba nezumia from the stomach of Nezumia bairdi Goode and Bean collected from the coast

166 ELMER R. NOBLE

of Greenland. This species was the tenth amoeba described from any fish, and the only one that has been found in a macrourid.

The only flagellate that has been reported from a macrourid is Cryptobia coryphaenoideana Noble (1968) from the stomach of Cory- phaenoides acrolepis collected off the coast of southern California.

4. Nematoda

All species of macrourids that I have examined have been infected with nematodes, usually larvae but occasionally adults. Larvae generally were coiled in mesenteries or attached to peritoneum or surfaces of viscera. Adults were located in the stomach or intestine. All nine species of fishes listed in Table VIII were infected with larvae of the genus Anisakis. Contracaecum aduncum (Rudolphi) larvae were also present in Macrourus rupestris. Adult Capillaria sp. were recovered from the stomachs of Coryphaenoides acrolepis and C. pectoralis. An adult, unidentified nematode was found in the stomach of Nezumia stelgidolepis.

Nematodes have been reported from at least a dozen other species of macrourid fishes, especially those collected by T. H. Johnston (see Johnston and Mawson, 1945) from the Antarctic coast. They have been identified as Contracaecum aduncum (adults and larvae), C. tasmaniense Johnston & Mawson, C o n ~ r a ~ e c u m sp., C a ~ i l l a r i ~ ~ a s ~ n i c a Johnston & Mawson, Paranisakiopsis coelorynchi Yamaguti, P. lintoni (Linton) Johnston & Mawson, P. macrouri (Linstow) Johnston & Mawson, P. australiensis Johnston & Mawson, P. macruroidei (Linstow) Johnston & Mawson, Johnston-mawsonia coelorhynchus Johnston & Mawson, Rhabdochona coelorhynchi Johnston & Mawson, Anisakis marinus (L.), and Ascarophis chalinurae Johnston & Mawson. Coelo- rhynchus australis harboured six species of nematodes.

The abundance of nematodes, especially larval stages, in marine fishes has been well documented. First intermediate hosts are copepods, euphausiids (see Smith, 1971), amphipods, chaetognaths, etc. See p. 188 for comments on fishes as second intermediate hosts for nematodes.

5. Digenea

Digenetic trematodes so far reported from macrourid fishes listed in Table VIII belong to the families Fellodistomatidae (e.g. Pel- lodis€omum) in the gall bladder, Hemiuridae (e.g. Gonocerca, Genolinea and Dissosaccus) in the stomach, and Lepocreadiidae (e.g. Lepidapedon) in the intestine. See McCauley (1968) for a description of five species of Lepidapedon collected from five species of hosts living a t depths

T ~ L E VIII. A COMPSISON OF PERCENTAGES OF FISH HOSTS INFECTED WITH PARASITES (Numbers 1 to 9 are deep benthic 2 macrowids ; 10 is a bathypelagic zoarcid and 11 is the common cod that represents offshore-mesopelagic environments.) id

Geogra- Nematoda phical Myxo- Micro- Depth Acanthoce-

phula aporida aporida location (m) Number Copepoda Monogenea Digenea Ceatoda of jish

1. Macrourua berglux

2. Macrourua

3. Coryphaenoidm

4. Coryphuendea

rUpeat4.k

acrolepia

abyaaorum

aerrula 6. Coryphaenoidea

pectoralis 7. Coelorhynchua

acaphopsis 8. Coelorh yncua

carmidus 9. Nezumia

stelgidolepis

5. Corypbmidea

10. Melanostigma pammelaa

11. Gdua morhua

21 33

47 00

51 52

10 00

12 00

11 18

27 00

11 00

35 6

00

O@

00

10

00

00

4

00

6

57

00

6

90

83

27

18

9

6

10

6

25

00

00

00

48

9

9

76

00

00

00

00

00

00

18

3

48

49

94

70

91

27

52

54

26

62

57

73

90

91

73

74

9

20

221 00 00 60 140 25 5 60

00 00 11 20 70 85

33 30

62 New- 330 found- land

00 Norway 680 Mexico 900-

35 California 1900 3840-

00 California 4000

00 California 4000 620-

00 California 1600

00 California 470

00 Surinam 450

00 California 490- 3200

00 California goo+ 00 Barents 30-

Sea 540

168 ELMER R. NOBLE

Fra. 10. Digenetic trematodes from macrourid fishes. A-B. Lepidapedon camadem’s McCauley from Chalinura $Zifera Gilbert, and C. serrula Bean. C-E. L. jiliformis McCauley from C. JiZifera. (After McCauley, 1968.)

of 800-2 865 m off the coast of Oregon, U.S.A. Figure 10 illustrates two of these species. Of the macrourids that I have studied, the hosts with the largest numbers and species of trematodes were Mamourus berglax with the genera Gonocerca, Genolinea and Fellodistomum (the genera were identified by Mrs M. Pritchard); and Coryphaenoides abyssorurn (Gilbert) with Lepidqedon sp. and Genolinea sp. Host

PARASITES AXD FISHES IN A DEEP-SEA ENVEONXENT 169

species with the highest incidences of infection were C. abyssorurn (go%), C. serrula (83%), and M . berglax (57%). Numbers of individual hosts, however, were generally small.

Scattered throughout the literature are references to other digenetic trematodes living in macrourid fishes. For example, the following genera have been reported from Coelorhynchhus spp. : Derogenes, Dolichoenterum, Pseudopecoelus, Lomasoma, Pimbriatw and Distomum. Manter (1964) reported the following trematodes from Coelorhynchw australis (Richardson) : Derogenes varichus, Dolichoenterum sp. (immature) Qonocerca lphycidis Manter and Lepidupedon azcstralis Manter.

6. Copepoda

The copepods referred to in Table VIII included at least six species as listed in Table IX. Identification to the species level was made by Dr Z . Kabata. Among other macrourids we have recovered the following copepods (percentages of infection are not given because the numbers of individual hosts were fewer than ten).

TABLE IX. SPECIES OF COPEPODS RECOVERED VROM THE

MACROURXDS LISTED M TABLE V I I I

Host Per cent Site of infected co*e330de atbhment

Coryphrtenoidecl 62 Latermnthua gill chamber amolepis quadripedie

Kabata & Gusev Braehiella mouth, gill arwvdmkz chamber Markevich Lemeenicus? operculum

Coryphaenoidee 18 Brachiella mouth peotoralie anwu&a

Mmroumce 33 Clavdla gill chamber berglax adzlnooG Str0m

Chondrmthodes gill chamber tuberofuratzls Kabata & Gusev

Nezumia 06 not identified stomach, 9k2gidokpk intestine

170 ELMER R. NOBLE

Coryphaenoides pectoralis (Gilbert)

Nezumia bairdi Goode & Bean

Chalinura sp.

Branchiella annulata (Markevich) in mouth

Lernaeenicus? on skin

Branchiella annulata in mouth Lateracanthus. quadripedis (Kabata & Gusev) on skin.

On the skin of one specimen of Coryphaenoides abyssorum was a large copepod that appeared to be Lophoura sp. The life histories of these parasites are not known and can only be inferred from a knowledge of life histories of similar species or the same species from other hosts.

7. Other parasites Monogenean trematodes have seldom been found on macrourids.

Those that I recovered from Coryphaenoides abyssorum and Coelorphy- chus scaphopsis have not yet been identified. Those from Nezumia stelgidolepis were identified by Dr J. Mizelle as belonging to the genus Choricotyle. Since Table VIII was prepared, one specimen of a monogenean parasite was found on the gills of Coryphaenoides acrolepis. It appears superficially similar to Cyclocotyloides pinguis (Linton) taken by McCauley and Smoker (1969) from the mouth and gills of Chulinura pectoralis, C . Jilifera and Hemimacrurus ( = Coryphaenoides) acrolepis from depths of 800-2 860 m off Oregon.

I have found representatives of the subfamily Mazocraeoidinae on the gills of Nezumia bairdi. Three other species are: Diclidophora mucruri Brinkman from Macrourus rupestris, Diclidophoropsis tissieri Gallien from Macrourus laevis ( = M . rupestris ?), and Diclidophora coelorhynchi Robinson from Coelorhynchus australis.

Cestodes recovered from macrourids are generally immature. The highest incidences of infection in the fish that I have examined occurred in Coryphaenoides acrolepis (26%) and Coelorhynchus scaphopsis (48%). The most common kinds were trypanorhynch larvae. The larvae of Microbothriorhynchus coelorhynchi Yamaguti was reported from the body cavity of Coelorhynchus sp. collected from Maisaka, Japan. Cysts of Rynchobothrium and larval Nybelinia are also known from these fishes.

Acanthocephala from Macrourus berglax were tentatively identified by Dr W. Bullock as Echinorhynchus qadi, a species with a wide host spectrum among marine fishes. The life cycle probably involves deep-water amphipods. This species is also known from M . bairdi. Species from Nezumia stelgidolepis have not yet been identified.

PBRASITES AND FISHES IN A DEEP-SEA ENVIRONMENT 171

V. DISCUSSION

A. Food This review has placed much emphasis on food because many

parasites gain entry by way of the mouth. Russian parasitologists (see Dogie1 et al., 1958 and Polyanskii, 1955) have made some well- known generalizations relating to food and parasitism in marine fishes. A major conclusion is that plankton-feeders have relatively few kinds and numbers of parasites and incidences of infection, while carnivores have many kinds and numbers, and higher incidences of infection. This relationship is explained on the basis of differences in varieties of food consumed and presence of infective stages of parasites.

Data on Table X provide possible explanations for differences in the parasite-mix of two mesopelagic myctophid fishes living together in the same habitat. Only major differences in parasite incidences are tabulated. Notice that significantly more Stenobrachius are infected with the nematode Anisakis than with Contracuecum, and that the reverse is true for Diaphus; also notice that Diaphus has a higher incidence of infection with two kinds of cestode larvae and with the copepod Cardiodectes. Since the helminths are acquired with food I have tabulated differences in consumption of copepods and euphausiids, both known to be intermediate hosts for nematodes and cestodes.

TABLE X. DIFFERENCES IN PERCENTAGIES OB INFECTIONS OF Two MESOPELAGIC FISHES LI~INGI IN THE SAME HABITAT

(Extracted from Collard, 1970)

Dkphus theta Stenobrachius lezccopsarus

486 spechens 61 specimens

per cent With Anisakis larvae 15.4 3.2 With Contracaecum larvae 6.8 37.7 With phyllobothriid pleurocercoids 1.6 6.6 With pseudophyllid pleurocercoids 2.7 8.2 With Cardiodectes medusaeus 3.9 19-7

Stomachs with copepods Stomachs with euphausiids

14.0 33.0

13.0 3.0

172 ELMER R. NOBLE

Note that relatively many more stomachs of Diaphw contained copepods, and many fewer contained euphausiids than did stomachs of Stenobrachiw. These data suggest that a high consumption of copepods is correlated with a high incidence of Contracaecum and cestode larvae, and a relatively low incidence of Anisakis, at least for Diaphw theta. Cardiodectes medusaeus uses the pelagic bubble-snail Janthim globosa Blainville as an intermediate host. According to Pearcy and Laurs (1966) many more Stenobrachiw leucopsarus migrate to the surface each night than do Diaphus theta off the Oregon coast. If at this location the differences in parasites and food habits are the same as those living off the California coast, one might postulate that surface feeding habits at night may be partly responsible for the observed differences in parasitism.

In an earlier section of this paper (p. 167) I referred to an incidence of 50% infection by the trematode, Aponurus californicw, in the stomach of Leuroglossw stilbius living in the Santa Barbara Basin off California, and an incidence of 18% in the same species of host living in the Santa Cruz Basin separated from the former location by an island. The marked difference in incidence is probably due to several factors (e.g. densities of populations, size of biomass, etc.) but since the trematode employs an intermediate host that probably is part of the fish’s diet, I became particularly interested in the food of the fish.

A detailed study of the stomach contents of Leuroglossus stilbius and of Stenobrachius lezLcor)sarus, both abundant in the two basins under consideration, was made by Cailliet (1972). He removed the stomach contents, identified each organism to the lowest possible taxon, measured each with an ocular micrometer and tabulated the total numbers of individuals. The per cent volume contributed by each prey item was subjectively estimated. The “ index of relative importance ” was calculated using the method of Pinkus et al., 1971.

In the Santa Barbara Basin Leuroglossw ate primarily larvaceans (Oikopleura spp.) and salps (probably Thulia democratica) followed in order, by ostracods, small copepods, zoea larvae and Euphusia paci$m. In the Santa Cruz Basin the diet was much the same, but consisted of more nauplii, more large copepods, fewer ostracods, and the addition of amphipods (Hyperia galba) and shrimp (mysids and sergestids) in lesser amounts. Leuroglossus is dependent on highly productive areas of high primary standing crop as exists in the Santa Barbara Basin where it apparently feeds most intensely during the night in surface waters. Evidence for this conclusion is provided by the higher percentages of “ recently full ” stomachs in the surface night hauls compared with hauls made at other times and depths. Plankton


in offshore waters is less dense than in inshore waters, and not always immediately available to Lewog1ossu.s.

The higher incidence of trematode infection in the Santa Barbara Basin, therefore, might be related not only to differences in relative numbers of food items containing larval parasites, but to differences in length of time spent at night feeding at or near the surface. As indicated earlier on these pages, I was unable to find infected intermediate hosts.

One other difference in the characteristics of the two basins is important for this consideration. The Santa Barbara inshore basin is relatively shallow (600 m deep, with a sill at 425 m) and is partly isolated from other basins. The offshore Santa Cruz Basin is 2 000 m deep and in much closer contact with the oceanic environment, and contains more diverse but less abundant invertebrate and fish fauna. Cailliet stated that “The relatively shallow bottom of the Santa Barbara Basin restricts the vertical range of Leuroglossw and so causes the fish to go mostly upward at night into surface concentrations of food. Offshore, however, its relatively haphazard movements may take it down as well as up, so that here it is less sure of finding its surface food source.”

Such studies as that just described provide clues for answers to questions on life cycles of parasites and incidences of infection. The bottom depth of a sampling area apparently may be at least indirectly responsible for the amount of surface food eaten by a fish. More intermediate hosts may live at the surface than at greater dept,hs.

Much has been written about the establishment and maintenance of species diversity, and the general concensus of opinion is that if a physically stable condition persists for a long period of time, species diversity will gradually increase because of normal genetic variations and immigration. An unstable physical environment, however, prevents the establishment of many diverse communities. See the review of current ideas on the subject by Sanders (1968), and his Stability-Time Hypothesis. Almost all writers on this subject agree that the most important potentially limiting resource in the deep sea is food. Dayton and Hessler (1972) have recently presented the hypothesis that “ The maintenance of high species diversity in the deep sea is more a result of continued biological disturbance than of highly specialized competi- tive niche diversification.” In anticipating objections to this hypothesis on the grounds that deep-sea communities have an extremely low rate of food income and must, therefore, be food limited, these authors state that deep-sea communities differ from disturbance- limited (e.g. predation and weather) terrestrial communities only in

174 ELMER R. NOBLE

that the trophic levels in the deep sea are almost completely merged, “ so that the roles of most predators are not distinguishable from those of the decomposers ”. Larger animals will be more likely to be food- limited because they have to search more actively for food, but smaller animals have more potential predators and thus have less probability of being food limited. Dayton and Hessler have taken a rather extreme position that will certainly be attacked, but they agree with Levins (1966) “ tha t the truth is usually the intersection of independent lines ”.

Discussions of species diversity tend to be peppered with pitfalls because of their generally empirical nature, especially when they deal with the deep sea that is so little understood. If this relatively homogeneous environment produces a wide variety of hosts for parasites, one would expect that there would exist a wide variety of parasites. But just because a host fish is food limited does not necessarily mean that a parasite inside of that host is food limited. No one has made a study of the comparative homogeneities of environments for parasites within different kinds of hosts. Predator-prey relationships between two species of parasites have received little attention, certainly not those in fishes. Community organization in the deep sea and, particularly, in parasites of deep-sea animals is undoubtedly more complex than currently envisioned, and demands much more investigation.

B. Life cycles of parasites The most conspicuous and critical gap in our knowledge of para-

sitism in marine fishes is information on parasite life histories. Fifteen years ago Dogie1 et al. (1958) stated that “ The study of the life cycles must be regarded as one of the most important tasks of marine parasitology.” Life histories of parasitic helminths and arthropods and those protozoa that require intermediate hosts are practically unknown for deep-sea species. Experimental work on life cycles is difficult or impossible because fish are commonly dead or dying by the time they are brought to the surface. Detailed systematic studies of plankton and their parasites have not been made. The present state of our knowledge of parasites of plankton provides little more than a basis for research ideas and much speculation.

The search for intermediate hosts of deep-water parasites is usually a frustrating chore. Such a search should include shallow waters frequented by adult fish only at night, and water levels inhabited by deep-water fish only during their immature stages. Reshetnikova (1955) was probably the first investigator to suggest that whereas in freshwater fishes the immature stages are initially infected with


parasites that do not require a second host, in marine fishes the earliest infections are with parasites that require one or more intermediate hosts for the completion of their development. These conclusions, however, were based on studies in shallow waters. In 1966 I reported on some Myxosporida in deep-water hosts, and stated that :

At the thermocline, where there is a rapid change of temperature with depth, there may be a barrier (generally 100 to 400 m below the surface) that promotes a concentration of plankton. If a deep-water fish swims up to the thermocline and lingers there, it could acquire parasites not available at lower depths. Deep-sea hhes usually breed at depth, but their eggs float to the thermocline, or surface, where they hatch. The larvae develop mesopelagically in relatively warm waters, and feed on plankton. Here the young fishes might become infected with parasites that persist throughout the lives of the hosts. Presumably, the metabolic rates of larvae are higher than those ofadults, but we know far too little about the habits and physiology of both adult and larval fishes.

For the maintenance of parasitism that is dependent on host food, the primary criterion is food availability which is a function of the biomass. A tabulation of several taxonomic groups of plankton as percentages of the total biomass at different depths was made by Vinogradov in 1968. His work was done in the Kurile-Kamchatka area in the north-western Pacific, and it suggests the kinds of invertebrates that one might examine if parasitological studies were being made in that area (Table XI). Notice that copepods are the most abundant animals at almost all levels, and the second most abundant are chaetognaths. Curiously, euphausiids are relatively scarce except at the 2 500-3 000 m level where they constitute more than 10% of the mass. At the bottom levels only polychaetes, ostracods, copepods and amphipods were found. Also worthy of note is the scarcity of small fish at all levels, with a small increase at levels between 500 and 2 500 m.

We already have evidence from several reports, chiefly the work of Russian workers, that the main source of parasites of plankton feeders are copepods and chaetognaths. Shrimps of many kinds are probably also important. The enormous numbers and kinds of copepods that inhabit the deep oceans make the task of sifting through ponderous collections a formidable one indeed. When large numbers of adult parasites are found in a species of fish one might expect that large numbers of infected intermediate hosts must be present to maintain the populations of adult parasites. But perhaps only a few heavily infected intermediate hosts are needed, or possibly a few lightly infected invertebrate hosts are sufficient because extremely large numbers of these invertebrates are eaten by the fish. A high incidence

TABLE XI. ROLE OF m s OF VARIOUS TAXONOWC GROUPS IN THE PLANKTON OF THE KTJR~-KAMCHATKA AREA OF TIIE PACIFIC OCEAN

(In % of the total planktonic mass in each of the layers from which catches were made-average of 9 stations.) (From Vinogradov, 1968)

SmaU fib

Depth (m) Chaetognatha Polychaetab Ostracoda Copepoda Mysidacecc Amphipoh Euphausiacea Decapoh

0-50 50-100

100-200 200-300 300-500 500-750 750-1000

1000-1500 1500-2000

2500-3000 3000-4000 4000-5000 5000-6000 600@-7000 7000-8700

2000-2500

8.7 28.7 43.9 14-5 13-2 15.3 12.7 5.4

30.1 43-6 37.1 4.5 0.9 0.6 0.4 +

< 0.1 0.2 0.6 0-2 0.7 1.2 0.7 0-7 0-7 0.2 0.3 0-7 0.5 0.3 2-6 6.5

0.1 0.3 0.5 0.4 1.8 1.2 1 -4 1-3 0.8 0-8 2.1 3.1 1.0 0.8 1.2 3-6

82.8 57.7 39.8 76.8 70.3 61.1 66-1 65.6 48-9 32.3 33.6 58.0 42.9 28.4 25-1 27-6

+ + + + 0.4 3.8 5.7 6.9 1.9 7.4 0.4 3.3

28.3 20.3 6.9 0

2.2 3.5 5.2 3.1 2-4 1.0 0-5 1.0 1.2 1.3 0-6 1.4 1 -5

19-3 15.6 10.6

3.6 7.0 5-0 1.3 0.9 0.2 + 0.1 0-3 0.05

10-5 + 2.3 + 0 0

+ + 0.2 1.1 + E 1.2

7.7 0.9 H

4-3 2-6 8.0 3.0 7.5 4

11.0 0 + 0 + 0 0 0 0 0

1 -6 0.1 p


in the definitive host may also be due to a long life of the fish and prolonged feeding on the plankton.

In addition to larval digenetic trematodes, copepods are known to harbour ciliates, gregarines, Microsporida, larval tapeworms, larval nematodes, bopyrid isopods, fungi or fungi-like organisms (e.g. Ellobiopsis) and dinoflagellates. Among the common genera of trematodes that use marine copepods as second intermediate hosts are the hemiurids : Hemiurus, Derogenes, Lecithaster, etc.

About 17 species of trematodes, including both larval' and adult stages, have been reported from chaetognaths. The genera of these parasites include Hemiurw, Derogenes, Distomum, Opechona, Mono- stomum, Lecithaster, Accacladocoelium, etc. Some of these genera have frequently been reported from deep-sea fishes. In a survey of 242 chaetognaths I found 14 (5%) to contain trematodes. In another survey I found 50% of a total of 76 chaetognaths taken from coastal California to be infected with at least one species of parasite. Other than trematodes, chaetognaths may harbour ciliates (e.g. Xetaphrya), flagellates (e.g. Cryptobia, Trypanophys), amoebas (Paramoeba), gregarines (e.g. Lankesteria), larval nematodes (e.g. Contracaecum aduncum), larval tapeworms and copepods.

In a recent paper Smith (1971) studied the euphausiids' ThysanoZssa inermis (Kraryer) and T . 1ongicaWa (Krrayer) as first intermediate hosts of the nematode Anisakis sp. in the northern North Sea. He found that 18 of 1 335 specimens of T . inermis from 17 localities were infected, with an incidence ranging from 0-5-4*0% at individual localities ; and 3 of 335 specimens from two localities, with an incidence of 0.7 and 1.0%. The total number of T. inermis examined from all localities was 2 730, and the total of T. 1ongicaUrEata was 950. Only one larva was found in each infected shrimp, coiled in the haemocoel of the thorax. Smith cited some other reports of a low incidence of Anisakis larvae in invertebrates. One larva was found in 855 specimens of the amphipod Capella septentrionalis Krrayer and one in 990 specimens of the decapod Hyas aranew (L.) from the Barents Sea. Five larvae were found in 3 247 specimens of the euphausiids T. raschii (Sars) and T. longipes Brandt from the northern North Pacific and Bering Sea. In my own work I recently examined 983 euphausiids taken from California coastal waters and not one was infected with nematodes or any other metazoan parasib Such small incidences of infection actually result in very large numbers of larval Anisakis if the populations of invertebrates are extremely dense, and if they are eaten in large numbers by the fish. Smith wisely concluded that further work is necessary before any assessment can be made of the relative impor-

178 ELMER R. NOBLE

tance of Thysanoessa species, euphausiids in general and of other invertebrates in the life-cycle of Anisakis.

We have little evidence that molluscs other than cephalopods play an important role as intermediate hosts for parasites of deep-sea fishes. Few snails live on the ocean bottom in deep waters, and pelagic gastropods, so far as I am aware, are not known to harbour larval helminths. Clams may be abundant but they also are not known to be important as intermediate hosts except for a few groups of trematodes such as Fellodistomidae. Cephalopods are commonly infected with ciliates, mesozoans, copepods and larval nematodes, trematodes and cestodes. The remains of octopods and squid are frequently found in the stomachs of a great variety of fishes collected at all depths. Thus there is a high probability that cephalopods are commonly the natural intermediate hosts for some parasites of deep-dwelling marine fishes.

A recent review of polychaetes as intermediate hosts for helminth parasites of vertebrates was made by Margolis (1971). He pointed out that the only known exceptions to the general rule that molluscs are first intermediate hosts for digenetic trematodes are provided by three sedentary tube-dwelling polychaetes. One is Hydroides dianthus Verrill at Woods Hole, U.S.A., in which Cercaria l0055i Stunkard develops ; another is Lanicides vay8sierei (Gravier) at Ross Island in the Antarctic, in which C. hartmanae Martin is found; and the third is Ampkicteis gunneri jloridus Hartman living in the Apalachicola River estuary, Florida, in which C. ampkicteis Oglesby develops. Each of these polychaetes is in a different family and the cercariae are thought to belong to the Sanguinicolidae whose members live in the vascular system of fishes. It is of interest that Hydroides norvegica, which serves as a second intermediate host for the digenean, Proctoeces maculatus Looss has been found at depths up to 3 000 m (Ekman, 1967).

For a list of polychaetes and their larval helrninth parasites see Table XII. Note that a large majority of parasites are digenetic trematodes. At least a dozen trematode species in fishes are known to use polychaetes as second intermediate hosts. Most of the metacercariae in the annelids are encysted and are found in the body wall, parapodia and coelom. Occasionally such sites as pharynx, ventral nerve cord and nephridia are invaded. With few exceptions (cercariae from tubiculous polychaetes) infection of the definitive host by trematodes in polychaetes is by ingestion of the infected annelid.

A few larval cestode cyclophyllidean and trypanorhynch larvae have been reported from polychaetes, but only the trypanorhynchs, whose adults parasitize elasmobranchs, live in marine waters. The


polychaetes are Aphrodite aculeata L. and Polycirrus denticulatus Malmgren. In each of these hosts, however, only one larva was observed. Among the nematode parasites of fishes only Contracaecum aduncum has been found in the polychaetes. Five species of annelids are involved, including the pelagic genus Tomopteris. Among the helminths of vertebrates, only the Acanthocephala are not known to employ annelids as intermediate hosts.

A systematic study of deep benthic annelids for their parasites has not been made, but of particular interest is the report by Amsova (1955) of Lepidapedon gadi (Yamaguti) rnetacercariae in three genera of polychaetes living in the Barents Sea. The genus Lepidqedoon, as indicated earlier in this paper, is a common fluke in several species of macrourid fishes.

Many deep-sea fishes are, of course, intermediate hosts for helminth parasites, and these fishes must be eaten by other fishes or by marine mammals before their larval worms can become adult. Many species of trematodes are progenetic and, as Manter (1967) pointed out, “ This ability to reach precocious maturity not only eliminates the necessity for the usual fish host but it makes possible at least a temporary residence in a great variety of fishes that might eat the infected crustaceans. The result is a change from a former host specificity to a wide range of hosts and hence a wide geographical distribution.” The extent to which this phenomenon occurs in deep marine water has not been determined. A particularly puzzling question is the fate of larval trematodes, cestodes and nematodes in macrourid fishes. What kinds of animals are predators of macrourids? Only two come to mind, sharks and marine mammals. But most macrourids inhabit depths that are probably below the feeding range of .mammals, so sharks are incriminated. There is little evidence, however, that large, deep benthic sharks are definitive hosts for larval helminth that are known to inhabit macrourids. Nevertheless, we do know that elasmobranchs are definitive hosts for trypanorhynch cestodes (e.g. Nybelinia) that have been found in macrourids. Some larvae, such as Contracaecum aduncum, living in a wide variety of hosts, may occur in an animal species that is never eaten by a suitable defhitive host. Such may be the situation for some of the larval parasites in macrourids, and these large fishes might thus be considered dead-ends for some of their parasites.

C. Parasites as biological tags The selection of a parasite as an indicator of its host’s activities

should be based on the following criteria (Kabata, 1963). The parasite should be common in one population and rare or absent in another

TABLE XII. LIST OF TREMATODES Usma POLYCHAETES AS SECOND INTEI~MEDIATE HOSTS (From Margolis, 1971) cI

!2 T r e d o d e s Polychizetes LOditY References

Didymozoidae gen. et spec.

Fellodistomatidae indet . Prodoecea rnccculatus

Hemiuridae Ddrogenee varkua

Gen. et spec. indet.

DeropristiS in$& Lepocreadiidae

Deroprkttk i n w Hornalornetvon pallidurn

Lepidqedon qadi

Lepocreudiurn album Lepocreudium setiferoidea Opechona bacillar&

Monorchiidae Aqrnphylodora derndi

zoogonidae zoogonoides laewie zoogonw, lasiwr

Tornopteria ?dgolandim

Nereia muck&, Hydroidea m e g i c a

Harmothoe irnbricata

Tomopteris vitrina;

Nereis diversicolor, Pwynereia durnerili

Nerek w e m Unidentified " small

Hamnothoe irnbricatcc,

Nereia pelagica Akwpe sp.

Tomopteris helgoladiw

polychaetes ''b

Lep idmtus equmnatw,,

xpw sp.b

Alkrnaria rmi jn i , Nereis diversimlor

Nereks wirenab Nerek &emc

Baltic Sea

Mediterranean (France)

Greenland

Adriatic (Trieste)


Woods Hole, Mass. (USA) Woods Hole, Mass. (USA)

Barents Sea

? Woods Hole, Mass. (USA) Baltic Sea

Baltic Sea

Woods Hole, Mass. (USA) Woods Hole, Mass. (USA)

Reimer, personal communication

Pr6vot 1965

Levinsen 1881 ; Ditlevsen

Mrtizek 1917

CarrAre 1937 ; Timon-David

1914

Y F

B and Rebecq 1958; Rebecq 1964 k Cable and Eunninen 1942 0

E hl Stunkard 1964

Amosova 1955

Fuhrmann 1928 Martin 1938 Reimer, personal

communication

Reimer 1970, personal communication

Stunkard 1943 Shaw 1933; Stunkard 1938, 1941

Echinostomatidae Echinoatomum sp.

" Echinostome " Himaathla leptoaomumb

Himaathla rnilitariad

Gymnophallidae Gymnophallus nereicola

Parvatrema boreal&

Undetermined family Cermia p m h u d a t a Dktoma myzoatomatiS D i s h u r n sp. Unnamed metacercariae

(3 types) Unnamed metacercark Unnamed progenetic

metacercaria

Nereis diveraicolor, Nereb

Nereia diveraimlor Arenimh nuwina

m i -

Nereia diversicolor, Arenicola marina

Nereis diveraicolor

Nereh sucoinea, Nereb wirenab

Nereis &ernb

Nereis &em Nereb suocinea, Nephyta

h b e r g i Onuphis oonolylega Nereia sucoinea

Mymt#num platypus

Azov Sea

Scotland English Channel, Bay of

Mediterranean (France) Biscay (France)

Baltic Sea


Woods Hole, Mass. and San Francisco Bay (USA)

Woods Hole, Mass. (USA) ?

Atlantic coast, Canada Azov sea Barents Sea Azov Sea

Latysheva 1939 ; Nechaeva 1964

Burt 1962 Caullery and Mesnil 1900;

Cudnot 191 2 Timon-David and Rebecq

1958; Rebecq 1964; Reimer, personal communication

Timon-David and Rebecq 1958 ; Rebecq and Pr6vot 1962; Rebecq 1964

Stunkard 1962; Oglesby 1965

Stunkard 1950 Wheeler 1896 Stafford 1907 Latysheva 1939

Amosova 1955 Latysheva 1939

~ ~~ ~

a Due to inaccessibility of some early literature, a few records of unidentified metacercariae have been omitted. b Infected experimentally, natural infections unknown. c See text for comments on experimental hosts. d Some authors regard H . leptoaomum to be a synonym of H. militarb. Possibly all the echinostomatid records from poly-

chaetes are referable to a single species.

182 ELBIER R. NOBLE

population of the host species. The parasite should include in its life cycle only the host species which is the object of study. The infection produced should be of reasonably long duration, and the incidence of infection must remain relatively constant. Perhaps the most important requirement is a knowledge of the entire life cycle of the parasite.

Studies on the use of parasites as natural tags for offshore fishes have been made by several workers (e.g. Margolis, 1965, parasites of salmon ; Sindermann, 1961, parasites of herring ; Templeman and Fleming, 1963, copepods of cod). A recent study of this kind was made by Scott (1969) who investigated the Atlantic argentine, or greater Atlantic smelt, Argentina silus Ascanius, collected off the eastern Canadian coast. The fish were caught demersally in depths of 55- 730 m, most commonly 180-365 m, between November 1966 and May 1968. Twelve samples comprising 581 fish and over 28 000 trematodes were recovered. The abundance of trematodes, all belonging to the family Hemiuridae, suggests that the hosts are carnivorous, feeding near the bottom. Although stomach contents were not systematically analyzed, the fish were found to feed primarily on euphausiids, chaetognaths and amphipods. Intermediate hosts were not identified but Scott thought that amphipods were the more likely second intermediate hosts for Lecithophytlum botryophorum Olsson ( = bothrio- phoron 2 ) ; the copepod, Acartia for Hemiurw levinseni Odhner ; and the chaetognath, Sagitta, for Derogenes varicw Miiller.

Scott demonstrated that there is an obvious transition from heavy infections with Hemiurus levinseni to heavy infection with Lecitho- phyllum botryophorum. This shift " indicates that the young argentines feed heavily on planktonic copepods (and arrow worms 2 ) which occur' in the shallower water at the edge of the continental shelf ". As the fish approach maturity they move to deeper water. The parasites, therefore, provide information on the probable depth at which the younger fish feed. Figure 11 shows differences in percentages of incidence among the three flukes. Scott found that these trematodes are not suitable for use as biological tags to distinguish populations of Argentina silw in the areas surveyed. The composition of the three trematode species was fairly uniform. There was, moreover, a " strong similarity between the species compositions of the parasites of the argentine on each side of the Atlantic ".

Atlantic eels (Anguilla) are hosts to some 20 species of trematodes which, with one exception, also occur in other Atlantic fishes ; whereas Anguilla species of the South Pacific have trematodes (at least eight species) peculiar to them. In this case, the kinds of parasites indicate origin and long residence of Anguilla in the South Pacific. . . . The


trematodes support the theory, based on other evidence, that Anguilba is of Pacific origin . . . (Manter, 1967).

Llewellyn and Tully (1969) made a comparison of speciation in diclidophoran monogenean gill parasites and their hosts. TWO macrourids included in the study were Macrourzcs rupestris, parasitized by Diclidophora macruri from Norway, and Coelorhynchzcs australis

Fish standard length (cm)

FIG. 11. Percentage incidence of the digenetic trematodes LecithphyZZm bot?yophmm. Dmogenes varicua, and Hemium levinseni in different length groups of Argentina

Combined data from several samples. (After Scott, 1989.)

parasitized by D. coelorhynchi from New Zealand. This study illustrates the value in using parasite classification in elucidating taxonomic problems of their hosts.

Parasites of marine plankton can be used as indicators of host distribution (Noble, 1972) if the life cycles of the parasites are known. If a plankton animal is an indicator of certain features of its en-

184 ELMER R. NOBLE

vironment any larval parasite of that animal might be used as an indicator of the habits or distribution of the definitive host that feeds on the plankton. Among the few investigators who have been concerned with this kind of study is Elian (1960) who concluded that Sqitta euxina living along Rumania shores is the intermediate host for the nematode, Contracaecum sp. living as an adult in the fish Caspialosa. The presence of infected Sagitta, therefore, indicates the presence of the definitive host.

Little use has been made of deep-water parasites as biological tags because of insufficient information on parasite life cycles, insufficient numbers of individuals in samples, and relatively few numbers of parasitologists who have the interest in, or opportunity to work with, deep-sea animals.

D. The uniqueness of deep-sea parasitism

An examination of evidence for " uniqueness " of parasites in deep- sea fishes led me first to the tabulations of parasites from inshore and offshore hosts. I found that whenever this question arose (which was not often) the answer was either a straightforward-yes, the parasites are unique, or endemic, but with exceptions; or it was equivocal. Yamaguti (1970) made an extensive report on digenetic trematodes of Hawaiian fishes in which he listed 314 species of parasites (from 144 species of fishes) of which 227 were considered to be new. The hosts were chiefly commercial food fishes sold at the Honolulu fish markets. It is interesting to note that 86 of the trematode species were didymozoids, and 70 of these parasites were new species. Didy- mozoids have not been described from deep benthic fishes. Fifty fish species each contained only one trematode species, and at the other extreme, one fish species harboured 18 trematode species. There was no record of negative fish examined. In his introduction Yamaguti stated that " Most Hawaiian trematodes are endemic, that is, different from those of other waters, as is the fauna of the host fishes . . . this fact suggests that the endemicity of the Hawaiian trematodes is parallel with the endemicity of their hosts."

If endemicity of deep-water parasites parallels that of their hosts the way t o determine the degree of uniqueness of these parasites is to establish the distribution of both parasites and hosts. Information on geographic distribution of deep-sea fishes is spotty, and on their parasites even less is known. Manter (1967) was one of the few parasitologists who has been concerned with this problem. He examined a large number of fishes in the South Pacific, and stated that,


The great differences in endemicity of marine fishes in oceanio islands in different oceans are also shown by trematode parasites of these fishes. The trematodes of marine fishes of South Australia are remarkably distinct. Of 165 species from marine fishes of tropical (northern) Australia, 30 occur elsewhere, with greatest affinities to New Caledonia, Japan, Red Sea and the Caribbean.

Four hemiurid digeneans of Macrourids that have also been reported

Derogenes crassus Manter, in the gall bladder of Coelorhynchus sp. from Maisaka, Japan, has also been found in Callionymus qassigii from Florida, Physiculus barbatus from Tasmania, Pleuronectes sp. from the White Sea, and Sebastodes paucispinus and Ophiodon elongatus both from Oregon.

Gonocerca crassa Manter, in the stomach of Coelorhynchus carminatus from Florida, and in Coelorhynchus sp. from Maisaka, Japan, also occurs in the following fishes from Florida : Ancylopsetta dilecta, Brotula barba, Lophius piscatorius, Merluccius sp., Paralichthys oblongw, Setarches parmatus, Synodus intermedius, Saurida sp., synodontid, Urophycis cirratus, and U. regiw. Also in Mola byrkelange from Ireland.

Gonocerca phycidis Manter, in the stomach of Coelorhynchus car- minatw from Florida and in the stomach of C. australis from New Zealand, has also been reported from the following fishes from Florida : Hippoglossw hippoglossus, Merluccius sp., and Urophycis regius ; and from U. chus from Maine ; and the following fishes from New Zealand ; Merluccius gayi, Parapercis colias, Scorpaena cruenta and Macruronus novae-xelandiae.

Dissosaccus laevis (Linton) Manter, in the stomach of Macrourus bairdi from Woods Hole, Massachussetts, also occurs in the following fishes from Florida : Helicolenus madrensis, Peristedion longispathum, P. miniatum, and P. platycephalum.

These four examples suffice to demonstrate that not all trematodes of macrourids are restricted to macrourids. Information on digeneans other than hemiurids is not so readily available, nor have such tabulations been made of other macrourid helminths.

Most macrourid fishes are morphologically and physiologically highly adapted to environmental conditions found only on the bottom of deep ocean waters. Any given species that may be found in widely separated areas of the ocean presumably is codronted with much the same kind of environment everywhere it lives. Its parasites might also be considered as highly adapted to those environments, but we have

from other fishes are listed below.

186 ELMER R. NOBLE

seen that certain &genetic trematodes and other helminths of macrourids are normal parasites of a great variety of other species of fishes representing all depth zones of the ocean including the epipelagic. These species of parasites, therefore, have a much wider environmental tolerance than do their hosts. At least one nematode, Contracaecum adurnurn, living as a larva in Macrourus rupestris, is found not only in a great variety of fishes but in invertebrates and even in marine mammals. The systematics of the nematode parwites of fishes is unusually confusing and many species of dubious validity have been described, but when more precise and accurate descriptions are made, other species (e.g. of Anisakis) of macrourid nematodes may also be shown to have a wide host spectrum.

Uniqueness of parasitism in deep-sea fishes, if it exists, should be stated in terms of total parasite patterns. Present information on taxonomy of most deep-water parasites is insufficient for formulating precise conclusions.

VI. CONCLUSIONS AND SUMMB,RY In this review of parasitism in deep-sea fishes the host and its

parasites are considered as a community of organisms, and when studied as a community the study becomes one in ecology. For this reason considerable space has been given to a description of the food, behaviour and habitats of the hosts. Remembering that most parasites and their hosts have evolved together, and that deep-sea fishes and invertebrates have become adapted to high pressures, perpetual darkness, low temperatures and a general homogeneity of the physical environment, one might expect that the parasites of these animals have also become adapted to the same environment. The two chief questions asked at the start of the review were : (a) what kinds of parasites, and in what numbers and incidences of infection, occur in deep-water marine fishes, and (b) does the deep-sea environment engender some attributes of parasitism that are different from those in other kinds of habitats.

In order to provide a standard for comparison, a few examples of parasitism in inshore and offshore fishes were described. These examples, ranging from tide pool species to cod that move from offshore shallow water to the mesopelagic zone, show that fishes in these habitats harbour many kinds of parasites, often in large numbers.

Russian parasitologists have demonstrated that plankton-feeders have relatively few kinds and numbers of parasites and incidences of infection, while carnivores have many kinds and numbers and higher incidences of infection. This generalization has been confirmed in the


present paper, with evidence that predators feeding only on one or a few kinds of prey tend to have fewer parasites than those having a wider range of food preferences.

With increasing depth there is a decrease in biomass and hence a decrease in available food for fishes. Midwater fishes, ranging in depth from 100 m to the benthopelagic zone, tend to be relatively small, with much reduced tissues. Evidence has been presented for a decrease in metabolism in deep-sea animals. There is as yet no evidence that parasities of these animals also have a lower metabolism, but it is possible that midwater fishes cannot afford many parasites that draw heavily upon available energy.

Differences in parasite patterns between two groups of fishes are correlated with differences in food and migratory habits, life histories, body size, length of life, physical environmental features and energy relationships.

Only a few of the thousands of species of midwater fishes have been examined for all of their parasites, but, at least in the eastern Pacific, these fishes have far fewer kinds and numbers of parasites than do inshore and open ocean surface fishes. In order of abundance the parasites are larval nematodes, myxosporidan protozoa, larval cestodes, copepods and larval hemiurid trematodes. Very few adult helminths occur in midwater fishes of the eastern Pacific. There is a decrease of parasites with depth until the benthopelagic zone is reached.

If two populations of a species of mesopelagic fish prefer surface food during nocturnal vertical migrations, and if one population lives predominantly in a given water layer in relatively shallow water, and the other population lives at the same level but in an area where the bottom is much deeper, and if both populations tend to have a wide vertical range of migrations, those in the deeper waters may eat less of their preferred food, with a higher expenditure of energy. Such circumstances might explain an observed difference in the parasite-mix of the two populations.

Benthic fishes (e.g. chimaerids and macrourids) have access to a greater abundance of food than do midwater fishes, and tend to harbour more kinds and numbers of parmites because the food presumably includes a higher proportion of infected intermediate hosts. Emphasis in this review has been placed on the family Macrouridm because among the fishes that live on the bottom of the deep oceans this family is the only one that hm been studied extensively from ti

parasitological point of view. Most of these fish are bottom feeders and live at depths between 200 and 2 000 m. Compared with midwater

188 ELMER R. NOBLE

species they are much larger, stronger and more active. Macrourids such as Macrourus berglax that have great variety and incidences of parasites appear to feed on a wider variety of food items, as judged by stomach contents, and to live in relatively shallow waters. All species of macrourids that have been examined for all of their parasites have been infected with myxosporidan protozoa and with larval nematodes.

The most conspicuous and critical gap in our knowledge of parasitism in deep marine fishes is information on parasite life histories. The search for intermediate hosts of deep-water parasites is a dis- couraging task. The chief immediate source of parasites of plankton- feeding fishes appear to be copepods and chaetognaths. If plankton contains relatively few infected vectors for a given helminth, a high incidence of infection in the definitive host may be due to the ingestion of large quantities of the plankton over a long period of time. The only mollusks that appear to be generally important as intermediate hosts €or parasites of these fishes are cephalopods.

Deep-sea fishes may themselves be intermediate hosts for such parasites as nematodes, digenetic trematodes, cestodes and acanthocephala. Little is known about most of the animals that prey on these fishes. Some of the parasite larvae, such as Aniealcis spp., in macrourids, may find their hosts to be dead-ends in so far as the parasite life cycle is concerned.

The study of parasites as natural biological tags has not often been extended into the deep sea because of insufficient information on life cycles, insufficient knowledge of the parasite fauna in a population of hosts, and because relatively few parasitologists and ichthyologists are actively concerned with the problem.

Endemicity of inshore and offshore shallow water fishes appears to parallel the endemicity of their hosts. The uniqueness of parasitism in midvahr fishes lies in the relative paucity of parasites in both numbers and kinds. Deep benthic fishes have many more kinds and numbers of parasites than do midwater species, due partly to the greater abundance of food and partly to their large size and long life. Some of the parasites of benthic fishes, such as certain herniurid digenetic trematodes, are also found in a wide variety of other hosts.

For this large and complex field of endeavour, information is urgently needed on the following subjects.

1. Details of life cycles of parasites and life histories of their hosts. 2. Identity of the entire parasite fauna of each host examined. 3. Host feeding habits, migratory habits, geographical ranges and

densities of populations.

PARASITES AND FISHES IN A DEEP-SEA ’EXVIELOWENT 189

4. Duration of parmite recruitment, and effects of parasites on their hosts.

5. Larger samples of each fish species from all parts of its geographical range, and samples of more families of fishes.

6. Better techniques for collecting deep-sea animals and for obtaining them and their parasites alive.

The best approach to the overall problem of parasitism in the deep sea is one unclouded with preconceived ideas. Instead of beginning with broad concepts, perhaps a search among the little things will provide the answers.

VII. ACKNOWLEDGEMENTS I am particularly grateful to Mrs Judith Orias, Mr Timothy Yoshino

and Mr Mike Moser for the many hours spent is dissecting fishes, preparing parasites for study, identifying parasites, searching the literature, typing, etc. Thanks are also extended to Sir Frederick Russell for reading the final manuscript and for his sympathy and patience. Through the courtesy of the following publishers and editors I was permitted to use a number of figures and tables: Academic Press Inc. (New York), Academic Press of Japan, Allen Press Inc., American Fisheries Society, Commercial Fisheries Review, Fisheries Research Board of Canada, Harvard University Press, Israel Program for Scientific Translations, Journal of Parasitology, National Marine Fisheries Service, Netherlands Journal of Sea Research, Norwegian University Press. My own research was supported by the Oceanography Section, National Science Foundation, NSF Grant GA 34144.

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