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An Unusual Form of Ichthyophonus Hoferi (Ichthyophonales: Ichthyophonaceae) from Yellowtail Flounder Limanda Ferruginea from the Nova Scotia Shelf

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An Unusual Form of Ichthyophonus Hoferi (Ichthyophonales: Ichthyophonaceae) from Yellowtail Flounder Limanda Ferruginea from the Nova Scotia Shelf DISEASES OF AQUATIC ORGANISMS Vol. 18: 21-28.1994 Published January 27 Dis. aquat. Org. I An unusual form of Ichthyophonus hoferi (Ichthyophonales: Ichthyophonaceae) from yellowtail flounder Limanda ferruginea from the Nova Scotia shelf Thomas G. Rand Biology Department, Saint Mary's University, Halifax, Nova Scotia, Canada B3H 3C3 ABSTRACT: An unusual form of Ichthyophonus hoferi is described from 12 of 254 (4.7 %) yellowtail flounder Limanda ferruginea Storer sampled from Brown's Bank on the Nova Scotia shelf This patho- gen was the cause of focal, circular to lobate, creamy-white lesions on the liver and kidneys of infected fishes. By virtue of its morphological and dimensional characteristics in the fish tissues, the histochem- ical profile of its thallus walls, and its development in vitro, this form was easily distinguished from I. hoferi sensu Plehn & Mulsow, 1911 from yellowtail flounder from other locations on the Nova Scotia shelf, and from other freshwater and marine fish species. However, gross signs of the infection, as well as the morphological, dimensional, andor histochemical features of this form of I. hoferi were so re- markably similar to those of an 'I. hoferi pathogen from L. ferruginea, Myxocephalus octodecemspino- sus, and Scomber scombrus described in the literature, and to an Ichthyophonus-type pathogen from Scopelogadus beanii, as to suggest that they are the same. KEY WORDS: Ichthyophonus hoferi . Yellowtail flounder. Northwest Atlantic . Limanda ferrugjnea INTRODUCTION effects and that the reported forms are a single species, namely Ichthyophonus hoferi sensu Plehn & Mulsow, Ichthyophonus hoferi Plehn & Mulsow, 1911 has 1911. However, Alderman (1976, 1982), Johnson & been reported from a wide variety of host species Sparrow (1961), MacKenzie (1979), and Neish & including crustaceans (see Reichenbach-Klinke 1957, Hughes (1980) have suggested that the genus Sindermann 1970), fishes (see Reichenbach-Klincke Ichthyophonus and especially I. hoferi has become a 1973, Wolke 1975, Neish & Hughes 1980, Lauckner convenient taxonomic wastebasket for poorly studied 1984),amphibians (Chauvier 1979, Herman 1984),rep- organisms often with only superficial resemblances to tiles (Chauvier 1979), and birds (Chauvier & Mortier- each other. Gabet 1984). Examination of the many studies on the During a study on the biology of Ichthyophonus morphology, life history, and developmental patterns hoferi from yellowtail flounder Limanda ferruginea of I. hoferi, or what is considered to be this pathogen Storer from the Nova Scotia shelf (Rand 1990), it be- from both freshwater and marine fish tissues reveals came apparent that the liver and kidneys of some of that the above-mentioned features of what is supposed the fishes recovered from Brown's Bank were infected to be the same species are highly variable. with a type of Ichthyphonus that was sufficiently dis- Reichenbach-Klinke (1973), Sindermann (1956) and similar from I. hoferi sensu Plehn & Mulsow, 1911 as to McVicar (1982) have suggested that the reported suggest that it was a different form. The present study variations in morphology, life history, and develop- describes this unusual form using light microscopy mental patterns are reflections of interspecific host- (LM),histochemistry, and cultural studies. 0 Inter-Research 1994 22 Dis. aquat. Org. 18: 21-28, 1994 MATERIALS AND METHODS sterilized inoculating loop was inserted inside tissue lesions that had been surface-sterilized by 2 applica- Sampling. Yellowtail flounder Limanda ferruginea tions of 70 % ethanol. The inoculum was placed on were collected in March 1987 during a ground- Petri dishes containing Earl's fish saline medium fish survey of the Brown's Bank (42" 501N, 6.5" (EFSM) (Rand & Cone 1990). The inoculum was 40'W) on the Canadian Fisheries research trawler then either left uncovered, or covered with a layer Alfred Needler. All fish landed during the cruise of filter-sterilized seawater (32%0), incubated at were captured in a Western IlA bottom trawl with a 12 "C, and observed at least twice weekly for up 2 cm cod end liner towed for 30 min at each fishing to 4 mo. Developmental stages of the fungus were station. periodically removed from the Petri dishes and studied The body and pericardial cavity of each fish in wet-mount preparations using phase-contrast illu- was opened and the fresh viscera inspected macro- mination. scopically for lesions considered characteristic of ich- Comparative studies. The present form of thyophoniasis in yellowtail flounder (see Powles et Ichthyophonus hoferi was identified by comparing al. 1968), as soon after capture as possible (usually morphological and dimensional features of its L -11..- ..-II -. n ..-A wiil~il~8 hj. ihauus iii CILU W..-. ad ~~Gullueitissues aild its other Microscopy. Infected-tissue samples from diseased in vitro developmental stages with the original yellowtail flounder were excised using heat-sterilized and other descriptions of Ichthyophonus (Ichthyo- scissors, placed in sterile Petri dishes, and taken to sporidium) gasterophilum and I. hoferi available in the the laboratory for further study. Wet mounts of smears literature (Caullery & Mesnil 1905, Plehn & Mulsow and tissue squashes made from infected tissues 1911, Axleieff 1914, Neresheimer & Clodi 1914, Daniel were examined microscopically. Small (0.5 cm3), in- 1933a, b, Fish 1934, Sproston 1944, Sindermann & fected tissue samples were also fixed in 10 % formal- Scattergood 1954, Dorier & Degrange 1961, Reichen- seawater (pH 7.4) immediately after their removal bach-Klinke & Elkan 1965, Hendricks 1972, Miyazaki from infected fish. These were then rinsed in tapwater, & Kubota 1977, Chein et al. 1979a, b, McVicar 1982, dehydrated, cleared, embedded in Paraplast Plusa, Herman 1984, Okamoto et al. 1985). They were also and sectioned 4 to 15 pm thick. Tissue sections compared with 10 % formalin-fixed, representative were then stained using techniques described by material identified as I. hoferi sensu Plehn & Mulsow, Culling et al. (1985),Humason (1972) or Roberts (1989) 1911 from the following naturally-infected host spe- as follows: Mayers' Haemalum and aqueous eosin; cies: Clupea harengus, provided by Dr C. Sindermann aqueous periodic-acid-Schiff (PAS); Alcian blue (National Marine Fisheries Service, Woods Hole, MA, pH 1 & pH 2.5; Alcian blue 8-GX according to the crit- USA); Pleuronectes platessa provided by Dr D. ical electrolyte concentration procedure; Best's car- Alderman (Fish Diseases Laboratory, Weymouth, UK); mine for glycogen; van Duijin's Acrolein-Schiff re- Melanogrammus aeglefinus and Micromesistius pou- action for proteins; Ninhydrin-Schiff reaction of alpha- tassou from the collection of Dr R. J. Roberts (Stirling amino-acids; Sakuguchi's reaction for arginine; Sudan University, UK); L. ferruginea from my own collection IV for bound lipids; and acid haematin for phospho- (Rand 1990); and with the Ichthyophonus-type patho- lipids. gen from Scopelogadus beanii provided by Dr J. V. Samples of the pathogen from fresh, unfixed tissues Gartner Jr (University of South Florida, St. Petersburg, were studied to determine whether the cell walls con- FL, USA). tained cellulose, chltin, or both. This was achieved Material for comparative morphological, and mor- using the 12KI and chitin deacetylation procedures out- phometric studies was dehydrated through an ethanol lined by Aronson & Bertke (1987),and 0.1 % calcofluor series, cleared briefly in xylene, and mounted in white (Sigma Chemical Co.) in deionized water. Calco- Canada Balsam. Differences in dimensions between fluor white is a nonspecific fluorochrome that binds to the form described herein and material considered to both cellulose and chitin in fungal cell walls (Dr M. be Ichthyophonus hofen sensu Plehn & Mulsow, 1911 McGinnis, Dept Pathol., Univ. of Texas Medical were tested using a single-factor analysis of variance Branch, Galveston, TX, USA, pers. comm.). Uptake of (ANOVA) test. The critical value, F, was tested at the the fluorochrome in pathogen walls was assessed by 95 % confidence level. viewing them with an epifluorescence microscope The holotype and representative slides of this new equipped with a violet block filter (380 to 425 pm form of Ichthyophonus hoferi have been deposited in excitation). the National Fungal Collection, William Saunders Measurements were obtained using an ocular micro- Building, Agriculture Canada, Ottawa, Canada as fol- meter and are in micrometers. lows: holotype no. DAOM 216137; representative slide Mycology. For cultural morphology studies, a heat- no. DAOM 216138. Rand. A form of Ichthyophonus hofen 23 RESULTS were bound by multilaminated walls (Fig. 4) 14.4 to 96.0 pm thick composed of an uni-laminate inner zone Sampling surrounded by a multilaminated layer having a rough to irregular outer surface. Some of the branches had A total of 12 of 254 (4.7 %) yellowtail flounder concentric restrictions along their length that gave Limanda ferruginea were infected by this unusual them a jointed appearance. Branch apices were swol- form of Ichthyphonus hoferi. The infected fish were len and contained either unbranched or dichotomously from the south-western region of Brown's Bank. branched cytoplasmic aggregations 259.2 to 672.0 pm Clinical signs were single or up to 3 focal lesions on the long by 134.4 to 470.4 pm wide. Branches had a cen- surface of the liver and/or kidneys of the infected fish tral, tubular lumen 15.4 to 42.4 pm wide that usually (Fig. 1). Lesions varied from circular to lobate (Fig. 2) contained spheroidal to prolate, terminal and inter- creamy-white patches, 0.9 to 2.3 cm wide. These were calary cytoplasmic aggregates 38.5 to 77.0 pm long by slightly raised above the surrounding tissue matrix, 19.3 to 61.6 pm wide. The cytoplasm was finely reticu- and were hard to the touch. There was no evidence of lated, and contained vacuoles 0.96 to 3.2 pm wide, bleeding but petechiae were associated with the larg- spheroidal lipid-like bodies 0.96 to 3.6 pm wide. Nuclei est lesions in 5 of the fish. There were no external signs had a central or acentric, condensed nucleolus bound that any of the fish were infected.
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