"Studies on Ligula Intestinalis (Linnaeus, 1758)" by T.S.C.Orr, B
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"Studies on Ligula intestinalis (Linnaeus, 1758)" by T.S.C.Orr, B.Sc., A.R.C.S. A thesis submitted for the Degree of Doctor of Philosophy in the Faculty of Science of the University of London. APRIL 1967 Imperial College Field Wellcome Laboratories for Station, Experimental Parasitology, Ashurst Lodge, University of Glasgow, Sunninghill, and Beareden Road, ASCOT, Bearsden, Berks. GLASGOW. 1. ABSTRACT The pseudophyllidean cestode Ligula intestinalis (Lin. 1758) was studied in order to reach a fuller understanding of its biology and life cycle in a natural environment. The plerocercoid larva in rudd, Scardinius erythrophthalmus, was intensively studied by sampling the fish population of the reservoir. Environmental factors affecting the plerocercoid directly and also mediated through the host's physiology were studied in one generation of rudd sampled during a period of two years. The site of the plerocercoid in the fish was accurately determined by dissection and by sectioning of infected fish. Morphological changes during the development of the plerocercoid were investigated together with accompanying changes in nitrogen, glycogen and lipid content. Changes associated with senescence of the plerocercoid were observed from sections. Stunting of the rudd and changes in its behaviour were observed to result from infection with the plero- cercoid. Final hosts in the life cycle were observed on the reservoir and the size of infected fish eaten by these 2. birds* The adult phaoo of the lifo cycle use obtainod in the laboratory by in vitro culture and, by experimental infection of ducks* Eggs obtained from ip vivo culture in ducks were used to determine the effort of light on the hatching of the coracidia* Fish of various families harbour plorocercoids of Idatiajouleatialla and a hoot-lief was compiled showing the distribution and specie° of fish infected* Evolutionary dovolopment of the oestodo in several fish families le discussed* ACKITOWLEDGEMENTS 1 should like to thank Professor 0.W. Richards in whose Department the work was carried out and the Agricultural Research Council for financial support. should also like to thrink Dr. June Mahon for the helpful supervision extended during this work and Professor B.G. Peters for many useful discussions. I am indebted to Dr. P. Call for advice on the biochemical sections and to Dr. C.A. Hopkins for comments on this section. My thanks extended to all the personnel of the Mid-MorthamDton- shire Water Board, particularly those at Ravansthorpe reservoir, who gave help so willingly during the collection of fish and, lastly, to all my colleagues at Ashurst for assistance in various ways. CONJJ,NT5. Abotract Aelztawledgementa Contents . Introduction 4•Vcole of -the life ole Licitla autina •SECTION _ I: . Chapter I. Itothado of fiat or d examination 18* introduction 18 Sampling raothodo , 20 Seine netting 21 nod and 'him Eishing 24 , • Tranoport ot, live tiah to laboratory 25 Data rzlcorded in laboratory • 26 ticanurcrient of i'ioh cncliplorocerceids • 20 C41113) Or ko2.oh.. ,-,4.41,1. intectinalin 29 • - , . Introduction • 29- A. Phyoical -2eatniroa of ilavenot.l.lorpa rociervair 'end influence of climatic almageri on the zuld: 30 1. Ohara li ao and changes in water • . level 35 2.. 17a-tor zaveraento: 39 3. two action. 40 • 44, Teraporatnro 41 5 Might i'..i.tti.roct o Itavonothorpo ronertolr 43 1., '21-Jakton 43 2„ Bon-thou 45 30 Aquatio plan.tg 45 4, rich fatula of Itzwenat orp 1962-65 46 5, Birr.l. fauna ont lifo hi,ttory 50 1ho ruddy Soard±n ,orlithroyhthalmus 50.. ..2 Distributioti-'. of. rudd'vrithit t roctorvoir 51 3, Abundnitioo of tudd; • • 53 4.,Groith ofru- dd.. .55 • • 5. Braloaing.-habits tuld bo.hhiour 56 .6, ilierb.fion "Of.' 50, 7,tpngavttiy - of 58:- 8, Dioonsos ctrul..othOr Dartioltoo of mill 53 Diott oorrpotitovi anti prociatorn zttdd Itatp?nr.t-thorpo. 60 1, :Diot radd 67 2, Cormo-bi-ie*,16n 63 3. Pish prodatora of mid 64 III 'Lao greater Crested grebe • 65 5* Chapter III. IlcolOg or tho llorocorooid'in fho 69 oropipaiimmakrearrouto Intwaduction 69 noological • Tactors-irigluencing..host .. and praoito 74 • tffoct o soo:r3onal variations in • climatic and 'physical raptors. on . 75 2* Seasonal variation in food' supply or. =dd. and • °greet on ..- • . - intontinalio • - 81.: 3* Seasonal 'voliiation in distribution '• cf rudd the r000rvoir and egiloot on T.t3gt4a, ingestatiOns 87 Scazonal vztviation abtindanco or radd and effect on Mr iritOStatiOnd' H • • .93 5 i,13casouril variationo in raitgration . og rudd arid orfoot on Zif-,:tAlq • .-"infostationd „ . • • .• . 100 6a. poaconal variations' in activity Or . rudd and' orgoct on. - • • • . infontationS-- . - '103. • Ago and roproductiva condition rudd and ege.00ta_on44.0.422. • . infontations Introduction . 104 •• •14 Ohangon in footling habits. ox' mid - and ogre...ot onLiaula -311-ficstational.05 2*. Distribution of mid ai difforont 043 -mid affect .on Mauls • infestations - 108 3i- Abundance of radd at ditgoront ' agar, ond: offoct o.n I in:CO at ati Oh a 111 72,;.17.)..ing migration not ofloct on, ineo,ntationn = 112 -ahariGoa -in away/ V . ci4 =cid with : ago rma offoot,oar21..upaz InZeotationD FI~c o2 plorociorcoido =tad and ofxpo -on .clubsotraont infoutationd 114 : , • .1%ectliriet;-11abitte.:of., ingectod' and 6froot on. ' • t 1v .z?fosto:.ltd.. 011101•••••=111111111ft• .• _ Diatribution 1:rrrocimd -• and off ect on oubcoripout 'intoatatione" • /16: infooted7.i.add,and •ofroot on aubcoquent , ingoata.tiona, _ : 117 . Spawning migration' of Lru.dd and: offoo• o aubrioquent . 117 5 Activity of in..VoO bod' cfroat subaostont - inter:Ito:tam:La Charter IV. S to of do-vc-Aorimont ottto.,122.f.a.6orcold IntroductiOn 119 119 SitO of dovoloyment of tho' p1ol?ocoracid iVit.,iripatttra and adult mad ,'• 121 • hantor wr Growth era tiovaici mont 1orocorcoi1 iltbrOdUC'1032, - • 3.30, 1, Dovoictmont of tho pionnoroolil, 131 t" • 2, Sille tho plor000rocid 136 - 3. Ra• .z. grmrth of nlo.rocercolds _138 Si r,6 ploroceroniels i L ;iit1tiple infestations - / 5.1 Deformed growth 144 6. Chemical Changes associated vrith rowth rind develorrinnt cr.!: Van plerocerceid 145 a. nitrogen- content 145' b. lipid content. 149 0. Glycogen content - . 154 Charter VT, nffeot of :tai z1a 1nte6tinells ostau ens 1.......411MIP.11 •1•1011406 In 158. 1. Susceptibility of :rudd: 'infoStatien,:159 ' 2. Direct effect ofpioteocercoia on the ru.dd . 160: Grolith- 0f infrmted rudd 151. 4. Effect 'of plerocercoid infoutationo. ' on the -behaviour of the....t.iurld hoot • 170 rortaity of infested' .7.1.1dd 172 . Chapter VII .Diecussiont Section It Ileols.4=1...." the e7olt., intectineain 1..Ilost of plerOccrooici of allsal1.11tInt.....13.2.1 • . 174 2, Distribution O tho'plerodoreoid of' lica/a intestinalis in the Uorthamptonf- kaltAxo 44.4.o4 - . 176 3.Changoa in ruddta'diot and effort on Lifsla infostationa 177 - 4. Effect of infontations onriAd anc . ausceJitibxiity to furthar . teOstation vith Lictulti • .78 - • - 5, d6hriona1 variatioh- lh plorocereold - nfostationsfltnd in- dovololpontof: egg and.Droceroold 3-34 6. Water .t3vel in RavonStb.orpo:reserioir and: incidence' of 1ifialta 2 tho rrtdd . -1,S3 a , . .7. In of riew3onal changes• on:growth -, of .tho plerocercoldt its deirelomo:dtal 't3tagari and-.aqsociated hiochendoal.•.- changes,: . • . a, Inc• of seasonal. ohot -tea. tin ercrath• tInd development of, the plerocorcold 191 Staz-Hes 'in . e.ovelopment o Ll.gul ploroo:szcaidu -- • • 193. c. Bionhoiee.1 ehanseS dovolopment . of tho plerocoreoid Glycogen. content Iiitrogen content . Tripid Suriatiry o Discuss mit SY:CT./02i It 'Culturo or rldnl:t ni7laa-intectinAilA rm 1141221aJg.s.01. vivo . 206 1, not:hode a, nifeetiaa or duckd 207 ColVle.!tioli of eggs 208 2..gesults 210 . 3. Discussion 211 4. sc ary of In Vto culture 214 Che..ptozb IX. ntvitrc cultivier 216 216 Intro4uction .3 •. Methods of in vitro aultaxo 217 2a nosalts 219' Bicehenital sway 221 4, Dineussiaft 230' 5# St m 253 Chapter " The influenen of light on the hatch!.lw .2Lighgl=a1 Introduction 234 1.Uothoda 234 2.Res ulta 236 3. DIOCUD3i021 237 4. auM3 r2 OECTTOIT Int Chapter XI. Distribution of Liimln intostimlis 244 • rtraeronAlos • 251 Anpondiz 264 INTRODUCTION New field.. studies hive :been undertaken.'in Britain on the life cyclo of cootodea Whieh are ''not .of .irmediate, . economic 'importance. -In 1962 numbirs'..of =dd. =so were reMoved. froM Ravensthorim reservoir in Northamiton# . oh .Which..the • incidence of plerocereoide of . ' . was. high. It wan 'ideoided-lo, study the - parasite in •the field in an enVironment, which was not • fished ter coarse', fish and to.. °implement' field work, with laborato0_ observationa. Prequently'..; life: cyciled are. do9o2Abfad Eta • .. • • continuous proc000 which proceeds: ineVitably. ...In order • - to roach a 'real underatendind of .factore which Control the-life .oyelef observatione.Muot .be carried= out .in the field and. in the laboratory'..:. Pield 'Studien are governed by .the. availability' -of : material. fin which Several staaeo occur ,the .life eyole. from which the "tarasitelogiet obtains .his material* Habitats sr centinualli,influeneed "by' man whose-.. influence punt. teldiatinguiehed from other environmental • . :factors. The:' lilsciatinuoud' and - limited availability ;of Daiasitoo, in the field haa. stimulated the. culture of the pramoites in the laboratory under defined oenditione in Ardor to acquire valuable physiological evidenoo concernitig conditions necessary for .survival.,... The ocolcigy. of stages in the .life cyclic Shoed be. observed both in the flold..and in the labortito*7 under Controlled conditions.. - • Thore- are-.many methods of studying parasites, oh an culture.. electron stoma eoixy and•biochemical assity Methods,. all of which, contribute , informatiO4 'relelient to: the conditiOns under'.Which the parasite . Zito cycle of Xieu,/a 4itetkAinsAlls, (Ida. 1759). Until recently regarded as a monetypic speoies (Smyth,. 19474 two further species of the genus amaja 13loch, 1182 Moo, bOubinina, 1950), and Tai, 1:mm1078104 '040). 1111=4 .1950 is have been described, and Dingy anti pottiai(ocievhaNtr were grouped into a proposed new -Bally of the Steudephyllidea the ;#1,0411dae' (Dubinina, 1050.