A Parasite of Red Grouse (Lagopus Lagopus Scoticus)

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A Parasite of Red Grouse (Lagopus Lagopus Scoticus) THE ECOLOGY AND PATHOLOGY OF TRICHOSTRONGYLUS TENUIS (NEMATODA), A PARASITE OF RED GROUSE (LAGOPUS LAGOPUS SCOTICUS) A thesis submitted to the University of Leeds in fulfilment for the requirements for the degree of Doctor of Philosophy By HAROLD WATSON (B.Sc. University of Newcastle-upon-Tyne) Department of Pure and Applied Biology, The University of Leeds FEBRUARY 198* The red grouse, Lagopus lagopus scoticus I ABSTRACT Trichostrongylus tenuis is a nematode that lives in the caeca of wild red grouse. It causes disease in red grouse and can cause fluctuations in grouse pop ulations. The aim of the work described in this thesis was to study aspects of the ecology of the infective-stage larvae of T.tenuis, and also certain aspects of the pathology and immunology of red grouse and chickens infected with this nematode. The survival of the infective-stage larvae of T.tenuis was found to decrease as temperature increased, at temperatures between 0-30 C? and larvae were susceptible to freezing and desiccation. The lipid reserves of the infective-stage larvae declined as temperature increased and this decline was correlated to a decline in infectivity in the domestic chicken. The occurrence of infective-stage larvae on heather tips at caecal dropping sites was monitored on a moor; most larvae were found during the summer months but very few larvae were recovered in the winter. The number of larvae recovered from the heather showed a good correlation with the actual worm burdens recorded in young grouse when related to food intake. Examination of the heather leaflets by scanning electron microscopy showed that each leaflet consists of a leaf roll and the infective-stage larvae of T.tenuis migrate into the humid microenvironment' provided by these leaf rolls. Scanning electron microscopy showed that the adult nematodes burrowed into the mucosa as well as lying on its surface and that the caecal mucosa of heavily infected grouse became disrupted in areas of nematode activity. The caecal mucosa of lightly infected grouse exhibited little damage and the caecal mucosa of grouse treated with an anthelmintic and shot 5-6 months later was similar to that of lightly infected birds. Some of the nematodes from these treated birds were covered in rosette-shaped cells which have been tentatively identified as adherent lymphocytes. The cuticle of adult T.tenuis was superficially annulated but did not possess cuticular ridges, as described in some other trichostrongyle nematodes. Primary and challenge infections with T.tenuis were established in the domestic chicken and these reached patency but nematodes were expelled in blood-stained balls of mucus and all adult nematodes had been expelled from the birds 30 days after dosing with infective-stage. Following trickle doses of larvae,,there was a rise and then a fall in nematode egg output but larvae administered later in the trickle infection appeared to fail to establish. Light and scanning electron microscopy showed haemorrhagic lesions and blood spots on the caecal mucosa of infected chickens and nematodes were found to burrow beneath mucus secreted on the mucosal surface. There were significant increases in the proportions of circulating leucocytes in infected chickens, but only on certain days of infection. No antibodies to T.tenuis were detected in the blood of infected chickens. There was a decrease in the length of the caeca of infected chickens during the period when the Ill nematodes were being expelled from the caeca. Nematode egg output continued to rise during an infection in young red grouse and there was no expulsion of nematodes from these infected birds. Infective-stage larvae that had been attenuated by cobalt 60 irradiation stimulated some degree of resistance to challenge infection in the domestic chicken but not in the red grouse. It was concluded that immunization with irradiated larvae would be of little use in the control of T.tenuis in red grouse. IV To the players and supporters of Aldershot Football Club V "This is not a book to be tossed aside lightly. It is to be thrown with great force...." (Dorothy Parker) VI ACKNOWLEDGEMENTS I would like to thank my supervisors, Professor D.L. Lee and Dr P.J. Hudson for their supervision, advice and guidance throughout the course of this work. I owe a special debt of thanks to Professor Lee for his patience and encouragement during the compilation of this work. I wish to thank all the technical staff in the Department of Pure and Applied Biology, especially Mr D. Pedley, Mrs S. Eaton, Miss S. Sguires and Miss D. Smith for the upkeep of laboratory animals and Mr Arthur Holliday for photographic advice and assistance. It is a pleasure to thank Mr D. Newborn for assistance and advice concerning field work and both Dave and Rachel Newborn for hospitality during my trips to the Yorkshire dales. I also thank Martin Clough and Jon Knight for advice concerning word processing. Finally, I wish to thank Colin Nicholls, Ian Sutherland, the 'Keighley Fisherman1 and Aldershot Football Club for making these past three years more bearable. This work was funded by the British taxpayer, through the Natural Environment Research Council, Grant No GT4/84/TLS/23 and the Game Conservancy. CONTENTS Abstract Acknowledgements Contents CHAPTER 1 GENERAL INTRODUCTION CHAPTER 2 THE EFFECT OF TEMPERATURE, FREEZING AND DESICCATION ON THE SURVIVAL OF THE INFECTIVE-STAGE LARVAE OF T.TENUIS SUMMARY INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CHAPTER 3 FOOD RESERVES, AGEING AND INFECTIVITY OF THE INFECTIVE-STAGE LARVAE OF T.TENUIS SUMMARY INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION VIII CHAPTER 4 THE OCCURENCE OF THE INFECTIVE-STAGE LARVAE OF T.TENUIS ON HEATHER AND A SCANNING ELECTRON MICROSCOPE STUDY OF THE INFECTIVE-STAGE LARVA SUMMARY 81 INTRODUCTION 8 2 MATERIALS AND METHODS 8 4 RESULTS 88 DISCUSSION 100 CHAPTER 5 THE EFFECT OF T.TENUIS ON THE CAECAL MUCOSA OF YOUNG, OLD AND ANTHELMINTIC-TREATED WILD RED GROUSE SUMMARY 1 1 7 INTRODUCTION 1 1 8 MATERIALS AND METHODS 1 21 RESULTS 123 DISCUSSION 144 CHAPTER 6 THE COURSE OF AN INFECTION WITH T.TENUIS IN THE DOMESTIC CHICKEN SUMMARY 153 INTRODUCTION 155 MATERIALS AND METHODS 157 RESULTS 165 DISCUSSION 216 I X CHAPTER 7 ATTEMPTS TO STIMULATE IMMUNITY TO T.TENUIS IN THE DOMESTIC CHICKEN AND IN THE RED GROUSE USING LARVAE ATTENUATED BY COBALT-60 IRRADIATION SUMMARY 2 33 INTRODUCTION 2 34 MATERIALS AND METHODS 2 37 RESULTS 2 39 DISCUSSION 248 CHAPTER 8 GENERAL DISCUSSION 253 REFERENCES 259 CHAPTER 1 GENERAL INTRODUCTION i 1.1. INTRODUCTION TO THE TETRAONIDAE The red grouse Lagopus lagopus scoticus belongs to the Tetraonidae, which is a sub-family of the Phasianidae. The Tetraonidae have similiar general features to other members of the Phasianidae but have the following distinguishing characteristics (Short, 1967); tarsi partly or fully feathered; nostrils covered by feathers; lateral pectinations on the toes; spurless feet; bill covering and nails shed yearly; and a swollen eye comb above the eye. The Tetraonidae may be further divided into 6 genera; Centrocercus Swainson 1831; Dendragapus Elliot 1864; Lagopus Brisson 1760; Tetrao Linnaeus 1758; Bonasa Stephens 1819; and Tympanuchus Gloger 1842. This classification is shown in Fig. 1.1. 1.1.1. THE GENUS LAGOPUS The genus Lagopus Brisson 1760 is divided into 3 separate species; Lagopus lagopus (Linnaeus) 1758, the willow ptarmigan; Lagopus mutus (Montin) 1776, the rock ptarmigan; and Lagopus leucurus (Richardson) 1831, the white-tailed ptarmigan. The willow ptarmigan breeds on treeless tundra, moors, bogs and heaths across northern Eurasia; south to circa 55 N latitude in the west, to 49 N latitude in the Russian Steppes, and to 47 N latitude in Mongolia (Johnsgard, 1983). In North America this species is restricted to the circumpolar tundra and mountain ranges (Cramp & Simmons, 1980). The species Lagopus lagopus may be further subdivided into a number of distinct sub-species. The red grouse, Lagopus lagopus scoticus, is a sub-species unique to the British Isles and Lagopus lagopus hibernicus is a sub-species which inhabits the heaths and moors of Ireland. The rock ptarmigan, unlike the willow ptarmigan, survives in parts of Scotland, in the northern Pyrenees, and from Scandinavia and the northern Urals, east through Siberia, to the Bering sea (Johnsgard, 1983). The white-tailed ptarmigan inhabits North America, its distribution conforming closely to that of the alpine tundra from central Alaska, south to Vancouver Island, and along the Rocky mountains from British Columbia to northern New Mexico (Johnsgard, 1983). 1.1.2. THE RED GROUSE Distribution The red grouse, Lagopus lagopus scoticus, is exclusively confined to the heather dominant uplands of the British Isles. Large tracts of heather moorland in Scotland support populations of red grouse, these populations being concentrated in 4 main areas; the Southern uplands, the moorlands between the Scottish borders and the Pentland Hills; the west coast highlands and islands; the central highlands, stretching from Loch Lomond, eastwards to Aberdeen; and the North West Highlands, from Glen Mor, northwards (Sharrock, 1976). In the north of England, the heather moors of the Pennines support most of the English population. This Pennine stronghold of the red grouse can be divided into three main regions; the peak district, Fig. 1.1. The classification of extant species of grouse and ptarmigan (from Johnsgard, 1983). 3 Family Phasianidae: pheasant like birds Subfamily Tetraonidae: grouse and ptarmigan Genus Centrocercus Swainson 1831 1. C.urophasianus (Bonaparte) 1828: sage grouse Genus Dendragapus Elliot 1864 1. D. obscurus (Say 1923): blue grouse 2. D. canadensis (Linnaeus) 1758: spruce grouse 3. D. falcipennis (Hartlaub) 1855: sharp-winged grouse Genus Lagopus Brisson 1760 1. L.lagopus (Linnaeus) 1758: willow grouse 2. L. mutus (Montin) 1776: rock ptarmigan 3.
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