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The occurence of plerocercoids of Schistocephalus solidus in the Fraser Valley and their effect on the… Lester, Robert John Graham 1969

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THE OCCURRENCE OF PLEROCERCOIDS OF SCHISTOCEPHALUS SOLIDUS IN THE PRASER VALLEY AND THEIR EFFECT ON THE INTERMEDIATE HOST GASTEROSTEUS ACULEATUS by ROBERT J . G. LESTER B . S c , I m p e r i a l C o l l e g e London, 1964 A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE i n the Department o f Z o o l o g y We a c c e p t t h i s t h e s i s as c o n f o r m i n g t o the r e q u i r e d s t a n d a r d THE UNIVERSITY OF BRITISH COLUMBIA November 1969 In p r e s e n t i n g t h i s t h e s i s in p a r t i a l f u l f i l m e n t o f the requirements f o r an advanced degree at the U n i v e r s i t y of B r i t i s h Columbia, I agree that the L i b r a r y s h a l l make i t f r e e l y a v a i l a b l e f o r reference and study . I f u r t h e r agree tha permiss ion fo r e x t e n s i v e copying o f t h i s t h e s i s f o r s c h o l a r l y purposes may be granted by the Head of my Department or by h i s r e p r e s e n t a t i v e s . I t i s understood that copying o r p u b l i c a t i o n o f t h i s t h e s i s f o r f i n a n c i a l ga in s h a l l not be a l lowed without my w r i t t e n p e r m i s s i o n . Department of The U n i v e r s i t y of B r i t i s h Columbia Vancouver 8, Canada 1^ it AAV. & Date / i ABSTRACT Samples o f G a s t e r o s t e u s a c u l e a t u s from 16 a r e a s i n the F r a s e r V a l l e y and e n v i r o n s were examined f o r p l e r o c e r c o i d s o f S c h i s t o c e p h a l u s s o l i d u s . F i s h a t C o a l Harbour and A l o u e t t e Lake were sampled s e v e r a l t i m e s o v e r a t w e l v e month p e r i o d . The number and s i z e s o f worms p r e s e n t i n the A l o u e t t e Lake f i s h samples were r e c o r d e d , and i t was found t h a t i n f e c t e d f i s h l e s s t h a n 45 mm. t o t a l l e n g t h c a r r i e d on average more worms t h a n those o v e r 45 mm., and t h a t u n i n f e c t e d a d u l t f i s h were caught o n l y d u r i n g the b r e e d i n g season. I n a n o t h e r l a k e , i n f e c t e d f i s h were found i n a d i f f e r e n t a r e a from the u n i n f e c t e d ones. The f i s h i n t e r m e d i a t e h o s t was shown t o be a f f e c t e d by the i n f e c t i o n i n f o u r ways: ( i ) I n f e c t e d f i s h d i e d sooner t h a n u n i n f e c t e d f i s h , ( i i ) H e a v i l y i n f e c t e d f i s h were l i g h t e r i n w e i g h t o f f i s h t i s s u e t h a n c o n t r o l s o f the same l e n g t h , ( i i i ) The t o t a l s t a n d a r d r e s p i r a t i o n r a t e o f i n f e c t e d f i s h was h i g h e r t h a n t h a t c a l c u l a t e d by c o m b i n i n g v a l u e s o b t a i n e d from u n i n f e c t e d f i s h and p u b l i s h e d v a l u e s f o r i n v i t r o p l e r o c e r c o i d s . ( i v ) H e a v i l y i n f e c t e d f i s h r e q u i r e d up t o t w i c e as much oxygen per gram f i s h w e i g h t per hour when swimming a t the same speed as c o n t r o l f i s h . Other a s p e c t s were examined but the r e s u l t s were i n c o n c l u s i v e o r n e g a t i v e . The o b s e r v a t i o n s on n a t u r a l p o p u l a t i o n s a re d i s c u s s e d i n the l i g h t o f the e x p e r i m e n t a l f i n d i n g s . Errata p. 9 Line 7 Add 'samples' a f t e r 6th word p„10 Line 9 Add 'However' before f i r s t word p.47 F i g . 9 In caption for open c i r c l e s - pa r a s i t i s e d read open c i r c l e s - unparasitised TABLE OF CONTENTS A b s t r a c t I n t r o d u c t i o n L i t e r a t u r e r e v i e w I . Survey o f the d i s t r i b u t i o n and abundance o f S c h i s t o c e p h a l u s p l e r o c e r c o i d s i n G a s t e r o s t e u s i n the Lower F r a s e r V a l l e y and e n v i r o n s M a t e r i a l s and Methods R e s u l t s I I . C o l l e c t i o n and h o l d i n g of f i s h u s ed i n the f o l l o w i n g e x p e r i m e n t s I I I . E x p e r i m e n t s d e s i g n e d t o a s s e s s ways i n w h i c h S c h i s t o c e p h a l u s may a f f e c t the s u r v i v a l o f G a s t e r o s t e u s i n d i v i d u a l s 1. I n c r e a s e d m o r t a l i t y due t o d i r e c t e f f e c t o f S c h i s t o c e p h a l u s (a) W i t h no d e t e r m i n a t i o n o f cause Method R e s u l t (b) Death caused by the emergence o f the worm from the f i s h Methods R e s u l t s 2. P o s s i b l e i n d i r e c t e f f e c t s o f the p l e r o c e r c o i d i n f e c t i o n on the s t i c k l e b a c k (a) Assessment o f the e f f e c t o f the i n f e c t i o n on the number o f eggs produced by b r e e d i n g female f i s h Method R e s u l t i i i Page (b) S t a n d a r d r e s p i r a t i o n r a t e o f i n f e c t e d f i s h compared t o c o n t r o l s Method 19 R e s u l t 21 (c) A comparison o f the swimming r e s p i r a t i o n r a t e o f i n f e c t e d and u n i n f e c t e d f i s h Method 23 R e s u l t 25 (d) Comparison between e x h a u s t i o n t i m e s o f i n f e c t e d and u n i n f e c t e d f i s h Method 2 5 R e s u l t 26 (e) E f f e c t o f i n f e c t i o n on f i s h w e i g h t Method 26 R e s u l t 26 D i s c u s s i o n 27 R e f e r e n c e s 3 6 F i g u r e s 39 T a b l e s s 48 i v LIST OF TABLES Ta b l e Page I S c h i s t o c e p h a l u s i n f e c t i o n s i n the F r a s e r V a l l e y and e n v i r o n s 48 I I Number of worms per f i s h 50 I I I Numbers o f f i s h w i t h s p e c i f i c numbers o f worms 51 IV M o r t a l i t y o f i n f e c t e d and u n i n f e c t e d G a s t e r o s t e u s 52 V S t a n d a r d r e s p i r a t i o n r a t e o f p a i r e d f i s h 53 VI Oxygen consumptions o f p a r a s i t i s e d f i s h 54 V I I T o t a l oxygen consumption as per gram f i s h t i s s u e o n l y 55 V LIST OF FIGURES Figure Facing Page Length frequencies of G. aculeatus from Coal Harbour 39 Size frequencies of Schistocephalus and length frequencies of G. aculeatus trachurus from Alouette Lake 40 Size of plerocercoids plotted against host length 41 Size of plerocercoids plotted against number present i n host 42 Total worm burden plotted against f i s h length 43 Length frequencies of 3 f i s h samples from Haig Lake, Cortes Island 44 Apparatus for measuring the oxygen consumption of swimming sticklebacks 45 Oxygen consumptions of sticklebacks at d i f f e r e n t swimming speeds 46 Length/weight r e l a t i o n s h i p for G. aculeatus  trachurus 47 INTRODUCTION 1 The pseudophyllidian tapeworm Schistocephalus solidus (Muller, 1776) i s widespread and l o c a l l y common i n the Northern Hemisphere over Lat. 45°N. Its l i f e h i s t o r y follows the pattern; egg, free-swimming coracidium, procercoid i n copepod, plerocercoid i n f i s h , adult i n piscivorous b i r d . Plerocercoids are commonly found i n Gasterosteus aculeatus L. t and the weight of plerocercoids c a r r i e d by a f i s h sometimes exceeds the weight of the f i s h . This exceptional parasite burden, and i t s e f f e c t on the stickleback, has attracted, and continues to a t t r a c t , much attention from pa r a s i t o l o g i s t s and other research workers, although up to the present no serious detrimental e f f e c t on the f i s h has been demonstrated. The present study was i n i t i a t e d to e s t a b l i s h the course of natural l o c a l infections, and to examine aspects not yet studied i n which the parasite may e f f e c t the stickleback. I t was f e l t that the results would form part of a theory on how . a p a r a s i t i c i n f e c t i o n could influence the number of individuals in , or the structure of, a f i s h population. F i r s t , a survey was made of l o c a l populations of Gasterosteus to locate infections of Schistocephalus that could be sampled regularly. The survey was r e s t r i c t e d to Gasterosteus although plerocercoids of Schistocephalus solidus were also taken from two Cottus asper from Cranberry Lake near Powell River. The two' natural infections that were chosen were at Coal Harbour and Alouette Lake, and these were v i s i t e d several times over a twelve month period. 2 These areas also provided the infected f i s h and controls that were used i n laboratory experiments. Assessment was made of the e f f e c t of the i n f e c t i o n on the mortality of sticklebacks, the f i s h weight, the standard r e s p i r a t i o n rate and the swimming re s p i r a t i o n rate of f i s h . Other aspects were examined but gave negative or inconclusive r e s u l t s . These included the number of eggs produced by female f i s h , and time to exhaustion of exercised f i s h . 3 LITERATURE REVIEW There are several reports i n the l i t e r a t u r e on the seasonal incidence of infected sticklebacks. Hynes (19 50) found a 30% i n f e c t i o n i n fresh-water f i s h i n a brook draining into the Mersey and observed no seasonal maximum. Clark (1954) sampled from a freshwater pond near Leeds, Yorkshire, and found that i n the autumn of 1948 almost every f i s h was infected, though subsequently the percentage of infected f i s h dropped considerably. Similarly, Hopkins (1950) took f i s h from a reservoir near Dublin and found that p a r a s i t i s e d f i s h were common from March to October, rare (1%) during the winter and increased i n numbers again the following spring. Seasonal changes i n the size and number of plerocercoids i n infected f i s h have been noticed by some people. Smyth (1946) found large numbers of small worms i n f i s h during the summer months, and Clark (1954), at the same pond i n a d i f f e r e n t year, found only a few worms per f i s h i n the autumn and winter. Hopkins and Smyth (1951), sampling from an i s o l a t e d lake i n Yorkshire, found that during May and June, of the parasites of 33 f i s h examined (between 1 and 6 per fis h ) the greater proportion were over two centimetres long, whereas i n August thirteen f i s h yielded over 400 larvae less than one centimetre long. If this i n f e c t i o n i s normal, they suggest, i t would appear that there i s an elimination of a large number of i n i t i a l larvae. Arme and Owen (1967) present data on the mean number of worms per infected f i s h for various times over a four year period. In June 1962, 47 worms per f i s h were found; i n A p r i l -4 May-June 1963 only 12. In January-February-March 1963, 11, compared with 1 for the same period i n 1964. Hence annual v a r i a t i o n appears to be considerable. However, t h e i r data for the four quarters of 1963 (11, 12, 4 and 3) suggest a spring and summer increase i n number of small worms i n agreement with the three previous papers. The most complete account of the e f f e c t of the parasite on the stickleback has been given by Arme and Owen (1967). They were able to demonstrate a c o r r e l a t i o n between low l i v e r weight (expressed as a proportion of the f i s h weight) and high parasite burden (worm weight/total weight). They found some evidence of anaemia i n heavily infected f i s h and were able to correlate i t with parasite burden for the f i r s t and t h i r d quarters of 1963, though not i n the other two quarters. Using h i s t o l o g i c a l techniques, they showed that male gonads were unaffected by the parasite but ovaries were delayed i n maturation and at the end of the spawning season many corpora a t r e t i c a were present, showing some i n a b i l i t y on the part of the p a r a s i t i s e d female to shed eggs. This, they propose, may be mechanical as a distended female was observed to destroy a nest i n an attempt to spawn. They also found that whilst the male gonads were unaffected, greatly distended males were unable to construct nests. Examination of the p i t u i t a r y revealed no h i s t o l o g i c a l change associated with i n f e c t i o n . Kerr (1948) had e a r l i e r found s i m i l a r r e s u l t s . He found no evidence of e f f e c t on the p i t u i t a r y . Males taken i n May had testes that s t i l l contained r e l a t i v e l y more germ c e l l s than unparasitised f i s h but neverthless, there were many spermatozoa 5 present. The males, he observed, developed f u l l breeding colouration. The ovaries were i n the secondary growth phase of the oocytes but among the largest eggs he found a marked degree of a t r e s i a . Vik (1954) noticed that p a r a s i t i s e d f i s h had less f a t t y tissue around the gut than unparasitised f i s h . These e f f e c t s are remarkably s l i g h t for so heavy a parasite burden. However, there i s a p o s s i b i l i t y that Schistocephalus hastens the death of the f i s h . T h r e l f a l l (1968) recorded a mass di e - o f f of sticklebacks i n a lake near St. Johns, Newfoundland, i n August 1966, and he at t r i b u t e d i t to a combination of Schistocephalus (almost 100% infection) and Argulus canadensis, the f i s h louse, an external parasite. Mass die-offs of sticklebacks have been seen i n the Wood River Lakes of Alaska where Schistocephalus could be seen crawling out of the f i s h (H. Smith, pers. comm.). Vik (1954) noticed that great masses of sticklebacks died i n August, "due to plerocercoids crawling out through the wall of the abdomen". He examined f i s h trapped i n a sunken boat and found that the l i v e f i s h were "ready to burst on account of the pleroceroids" while those l y i n g dead had no worms but perforations i n the abdominal wall just i n front of the anus. Some l i v i n g f i s h had plerocercoids hanging put of the openings, and pleroceroids, both dead and a l i v e , were found on the bottom i n many parts of the lake. The temperature of the water was about 25°C., and he was working i n lakes near Trondheim, Norway. Wardle (1933) records the finding of Schistocephalus plerocercoids l y i n g free on the shore of Nanaimo Lake, B.C. 6 Clark (1954) noted that occasionally a worm was expressed when he was handling a stickleback, apparently through the rectum. These f i s h continued to l i v e with no evident signs of d i s t r e s s . Several people have noticed a change i n the behaviour of heavily infected f i s h . They tend to be nearer the surface and more e a s i l y caught (Arme and Owen, 1967, and Clark, 19 54). Smyth (1946) observed that infected f i s h had a c h a r a c t e r i s t i c swelling of the abdomen that produced unnatural swimming movements, though Clark (1954) thought that when aroused they could move as quickly as the unparasitised ones. 7 I. Survey of the d i s t r i b u t i o n and abundance of Schistocephalus plerocercoids i n Gasterosteus i n the Lower Fraser Valley and environs MATERIALS AND METHODS Gasterosteus aculeatus were c o l l e c t e d during 1968 from streams and lakes i n the Fraser Valley to locate a suitable source for regular sampling. Dip nets and a pole seine of less than 3/16 ths inch i n t e r n a l diameter stretched mesh were used i n conjunction with a 30' beach seine of nylon bobbinet of \ inch inte r n a l diameter stretched mesh. The f i s h were opened using fine scissors by a ventral cut running p o s t e r i o r l y from i n front of the pelvic g i r d l e . Large worms were removed using a blunt seeker and small ones by flushing with d i s t i l l e d water from a bulb pipette. Fish were sometimes examined further under a binocular microscope, particularly when Diphyllobothrium plerocercoids were encountered. Fish were measured to the nearest 5 mm. group below the t o t a l length and were separated into three races by running a needle over the side of the f i s h to f e e l for l a t e r a l plates; those with less than four plates were termed leiurus, those with a complete set trachurus, and the intermediates semi-armatus. This approximation was inaccurate for f i s h less than 2 5 mm. Worms were relaxed i n P e t r i dishes of d i s t i l l e d water i n a r e f r i g e r a t o r at 4°C for one week to allow for complete relaxation. The worm length was then measured to the nearest 5 mm. and the maximum width to the nearest 0.5 mm. From these figures, 'volume units' for the worms were calculated by cubing 8 the square root of 'length x 10 x width 1. The width/length r a t i o was close to 1:10. This procedure overcame errors due to unequal relaxation and the more slender shape of smaller worms. As the worms relaxed an outer tegument was cast o f f , and measurements were a l l made on the underlying surface. This technique was used so that a r e l a t i v e l y accurate estimate of the biomass of both small and large worms could be obtained. Net weights were inaccurate because of the varying amounts of coelomic f l u i d present on small worms, and dry weight was considered unsatisfactory because of the d i f f i c u l t y of obtaining r e l a t i v e weights of a range of worms less than one milligram. A s i m i l a r technique has since been published (Orr <et al_, 1969) . 9 RESULTS The f i s h samples collected, together with percent i n f e c t i o n , are l i s t e d i n Table I. I t can be seen that Schistocephalus i s a frequent but not common parasite i n many-bodies of water i n the Lower Fraser Valley. Figure 1 shows the r e l a t i v e abundance of the d i f f e r e n t sub-species of sticklebacks i n Coal Harbour for d i f f e r e n t quarters of the year, and also gives t h e i r length frequency and the occurrence of par a s i t i s e d f i s h . The f i s h were caught with the help of a seine net and, because of the seine mesh size, some f i s h less than 30 mm. long were able to escape through the meshes. The histograms, therefore, do not give the number of small f i s h present r e l a t i v e to the numbers of the larger s i z e s . Fish less than 30 mm. long were d i f f i c u l t to separate into subspecies. It can be seen that a l l sizes of f i s h over 25 mm. were present for most of the year, and that infected f i s h were scattered throughout a l l length groups and subspecies. Data on f i s h catch-rate i s not presented as i t was affected by many factors, however, the poorest catches were taken i n ear l y spring. The best catches of adult f i s h were i n June-July-August when there appeared to be a massive i n f l u x of adult trachurus into Coal Harbour. During hot weather i n late August, 1969, many thousand dead adult trachurus l i t t e r e d the bottom in. a shallow corner of Coal Harbour. Many of the dead f i s h were gravid females, no f i s h examined contained Schistocephalus. 10 Gasterosteus samples from Alouette Lake (Fig. 2) showed 100% i n f e c t i o n throughout the winter, uninfected f i s h appeared i n the late spring. Many of the uninfected f i s h caught were males i n breeding colouration. It i s possible that the uninfected f i s h were unsampled during most of the year because they were not present i n the lake at that time. They may have migrated into the lake i n the same manner that normal trachurus leave the sea and migrate up stream to breed during the summer. The only known outlets to the lake are over a high dam, or through the power turbine that operates i n a tunnel between Alouette and Stave Lakes. Through neither o u t l e t could f i s h enter the lakes. Numerous creeks flow into the lake and uninfected f i s h may have remained i n these.creeks for most of the year and only moved down to the lake at the breeding season. The two creeks flowing into areas regularly v i s i t e d were too small for most of the year to support f i s h , though infected sticklebacks were sometimes taken i n about two inches of water at the creek mouth. A larger creek, Gold Creek, yielded a few infected and no uninfected f i s h on the two occasions i t was v i s i t e d . I t i s highly unlikely, then, that uninfected f i s h moved into the lake from another body of water. Fish may have matured i n the lake, uninfected, and then, when they became a c e r t a i n size, became catchable and subsequently developed parasites. A l t e r n a t i v e l y , they may have been present i n the lake throughout the year, and only became catchable i n the breeding season. We may note i n passing that i t appears that these land-locked trachurus have retained t h e i r l a t e r spawning period compared to l e i u r u s . 11 Fish less than 45 mm. long were poorly represented i n the samples, ind i c a t i n g e i t h e r that there were few small f i s h for most of the year, or that a l l f i s h sizes were not being equally sampled. The worm size frequency charts i n F i g . 2 suggest that there was an increase during May of the proportion of small worms found, however this apparent seasonal peak i s due to the numbers of small worms found i n the samples of f i s h less than 45 mm. long. Table i i shows the average number of worms taken from f i s h of d i f f e r e n t length frequencies using data from a l l samples, and also gives the maximum numbers of worms found i n one f i s h . I t can be seen that f i s h s t a r t picking up the in f e c t i o n when about 20 mm. i n length, and continue to accumulate more worms u n t i l they were 35-40 mm. long. Larger f i s h contained fewer worms. As the samples of d i f f e r e n t f i s h lengths were uneuqal, the samples are divided by month i n Table I I I . This confirms the view that smaller f i s h were carrying more worms than the larger f i s h . In F i g . 3, the worm sizes are plotted against f i s h lengths. S o l i d symbols represent worms taken from a f i s h carrying only one worm. As the f i s h became larger t h e i r worms became larger and from the d i s t r i b u t i o n of symbols i t seems that worms from multiple infections are s l i g h t l y smaller than those from single i n f e c t i o n s . To further examine the r e l a t i o n between worm size and worm number i n any one infected f i s h , F i g . 4 was constructed. It includes only data from f i s h i n the 50 and 55 mm. length 12 groups to avoid complications of f i s h size a f f e c t i n g worm growth. F i g . 4b includes only those f i s h having worms over 32 5 v o l . units, to ensure that i f there i s any e f f e c t i t w i l l be exaggerated by considering only large worms. The means:.and standard deviations from F i g . 4b are plotted i n F i g . 4c. I t i s evident from t h i s that, of the f i s h caught, worms from a quadruple i n f e c t i o n are approximately 20% smaller than those from a single i n f e c t i o n . This difference may be due to several factors such as the e f f e c t of i n t r a - s p e c i f i c competition between the worms or an e a r l i e r mortality of the f i s h containing larger numbers of worms. However, the maximum e f f e c t each factor can have i s the t o t a l observed difference. Therefore, we can conclude that the e f f e c t of the worms on each other's growth i s small. In F i g . 5a, the t o t a l worm burden i s plotted against f i s h length group. Again s o l i d c i r c l e s represent single infections, and i t can be seen that a f i s h i n the 55 mm. length group, for example, can support up to three times the average burden imposed by a single worm. It i s also noticable that not many f i s h over 45 mm. were caught that were without a worm burden of at lea s t 300 v o l . units .except for the unparasitised f i s h that were caught during the breeding season. There was an absence of l i g h t l y infected f i s h even during the breeding season. If we go back to an e a r l i e r point about the absence of uninfected f i s h from the catches we concluded that i t was possible that these f i s h became catchable and then developed an i n f e c t i o n . This does not appear to be the case; mature f i s h 13 were eithe r uninfected or heavily infected (over 300 volume units of worm). The alternative conclusion, that uninfected f i s h were present i n the lake and only became catchable at the breeding season, may be closer to the truth. I t appears then that there were two conditions that would enable large Alouette Lake f i s h to be caught i n a beach seine, either they c a r r i e d a worm burden of over 300 volume units, or they were breeding f i s h . (Fig. 5b i s included i n order to relate volume units to dry weight. The data were taken from experimental f i s h that had been o r i g i n a l l y selected for carrying e i t h e r a heavy parasite burden or no burden, the l a t t e r group being used as controls. The f i s h were taken from the same source as those i n F i g . 5a. A comparison of the maximum burden c a r r i e d i n Figures 5a and 5b may be used as a crude estimate of the r e l a t i o n of volume units to milligrams). The proposed increased c a t c h a b i l i t y of breeding f i s h may have been due i n part to the t e r r i t o r i a l behaviour of the male. Causes of the increase i n p a r a s i t i s e d f i s h are more obscure. Uninfected f i s h may have been l y i n g beneath rocks when the seine swept the area during winter sampling, or these f i s h may not have been present i n the shallow stream outlets v i s i t e d . Evidence for the second p o s s i b i l i t y was gathered at Cortes Island. Samples of f i s h were taken from two small lakes joined by a short canal about 8' wide and 4' deep. The f i r s t sample (see F i g . 6) was taken from around some logs on a gently sloping shore i n Haig Lake. Most of these f i s h were infected with Schistocephalus and some also with Glugea. Dead f i s h were found on the bottom but 14 no free plerocercoids were seen. The second sample was from the canal and here one t h i r d had Schistocephalus. The l a s t sample came from several large shoals of f i s h that were m i l l i n g over and around submerged exposed rock, well away from shore i n Gun F l i n t Lake. Only a few of these f i s h were infected. In e s s e n t i a l l y one body of water then, two groups of sticklebacks were found, one heavily infected, the other r e l a t i v e l y free of i n f e c t i o n . It i s possible that they were separate populations. Some of the f i s h caught had abnormally short pelvic spines, and using these as a possible population c h a r a c t e r i s t i c , the samples were divided into two groups. The res u l t s are shown i n F i g . 6 . I t i s clear that the infected and uninfected f i s h were not separated by the spine character, and i t remained possible that uninfected and infected f i s h were derived from the same population but were caught i n d i f f e r e n t areas. 15 II. C o l l e c t i o n and holding of f i s h used i n the following experiments Most laboratory experiments required the use of infected f i s h and uninfected controls from the same population of sticklebacks. They were matched by taking pairs of approximately the same t o t a l length. Three methods for obtaining these were t r i e d . To produce con t r o l l e d laboratory infections of Schistocephalus i n Gasterosteus, plerocercoids were cultured, eggs collected, embryonated and the hatched coracidia fed to copepods. Cyclops  bicuspidatus and Macrocvclops fuscus containing developing procercoids died before f i s h could be infected. The second method involved the removal of plerocercoids from p a r a s i t i s e d f i s h . Two Alouette Lake f i s h were opened and the plerocercoids removed. The s l i t i n one f i s h was not sewn up and i t died i n the next twelve hours, while the other f i s h was sewn up with a small s u r g i c a l needle and suture and recovered well enough to feed. I t developed a fungal i n f e c t i o n around the stitches and eventually died on the fourth day. In May, uninfected f i s h were f i r s t taken from Alouette Lake and so pairs for most of the following experiments were taken from th i s natural source, though t h i s often meant that f i s h p r o v i s i o n a l l y assumed to be unparasitised were found to contain worms a f t e r the experiment, and vice versa. Pish that were caught i n the f i e l d were brought back to the laboratory i n two and three gallon jars aerated from an oxygen cyli n d e r . During the summer thi s method exposed the f i s h to temperatures i n excess of 20°C and losses frequently occurred the following night, so i f thi s was l i k e l y , the f i s h were transported i n an aerated polythene bag i n an ice chest with a few blocks of i c e . Large holding tanks i n the basement were continually aerated and had a small flow of water. They fluctuated between 6-15°C during the year, and for a l l of the following experiments except where indicated were at 10-13°C. Fish were fed about three times per week with frozen brine shrimp occasionally varied with small meal p e l l e t s or Tubifex worms. For the majority of experiments, f i s h were taken from Alouette Lake, and losses of these f i s h were a t t r i b u t e d to heavy i n f e c t i o n of Trichodina sp. and B a c t e r i a l G i l l Disease (Davis, 1961). Other parasites that were commonly found i n Alouette Lake included immature Proteocephalus sp., and the genera Gyrodactyius. Dactvlocrvrus, and plerocercoids of Diphvllobothrium. The Trichodina, Gyrodactyius and Dactylocrvrus were removed by placing the f i s h i n a 1:4000 solution of commercial formalin for one hour. The B a c t e r i a l G i l l Disease was encountered by immersing the f i s h f or one minute i n a 1:2000 solut i o n of copper sulphate, to which had been added three percent sodium chloride. However, i t was found that by the time the disease was diagnosed, many f i s h died from the treatment, eit h e r from the e f f e c t of the heavy metal ion on the g i l l mucus or through shock. 17 111^ Experiments designed to assess ways i n which Schistocephalus may a f f e c t the su r v i v a l of Gasterosteus individuals 1. Increased mortality due to the d i r e c t e f f e c t of Schistocephalus (a) With no determination of cause Methods A sample of f i s h from Coal Harbour was p r o v i s i o n a l l y separated into infected and controls by external examination, and equal numbers were placed i n an aquarium at 12-15°C. During the following weeks a l l deaths were noted and at the end of the experiment a l l f i s h were dissected to determine the actual numbers of p a r a s i t i s e d f i s h present. This experiment was duplicated. A plan to hold f i s h i n large underwater cages i n the i r natural habitat was cancelled because of the lack of infected f i s h . Results The two batches of infected f i s h and controls that were held i n tanks gave the data i n Table IV. Using the Fisher Exact Pr o b a b i l i t y Test, the p r o b a b i l i t y values for the results and the next two more extreme results are 0.0007, 0.00005 and 0.000002 giving a t o t a l of 0.000752 which indicated that i t i s highly u n l i k e l y that p a r a s i t i s e d f i s h and controls died at the same rate. It i s concluded that p a r a s i t i s e d f i s h were more l i a b l e to die from causes excluding predation than unparasitised f i s h . 18 (b) Death caused by the emergence of the worm from the f i s h From Vik's v i v i d description (1954), the emergence of the plerocercoid may increase the host mortality rate. Fish were stressed by starvation and by high temperatures i n an attempt to reproduce the phenomenon i n the laboratory. Methods Two heavily infected Alouette f i s h were starved i n the laboratory at 20-23°C and three f i s h at 10-12°C u n t i l death. Three p a r a s i t i s e d f i s h were slowly raised to th e i r upper l e t h a l temperature over several days. Results Both f i s h at 20 to 23°C died on the ninth day, those at 10 to 12°C died a f t e r 17, 21 and 24 days. In no instance did the worm show signs of emergence. Three f i s h were raised to 33°C i n two days and died with no emergence of the worms. The only worm that emerged during this study was from a gravid female from Queen Elizabeth Park which was i n a small tank i n which a male had a nest. One morning (3.4.68), the female was found dead on the surface s t i l l containing many mature eggs and the worm was stretched out i n front of the nest. The worm presumably emerged during egg laying attempts. 19 2. Possible i n d i r e c t e f f e c t s of the plerocercoid i n f e c t i o n on  the stickleback (a) Assessment of the e f f e c t of the i n f e c t i o n on the number of eggs produced by breeding female f i s h Method Counts of eggs were made on 14 Alouette Lake f i s h that were brought back a l i v e to the laboratory. They were between 54 and 65 mm. i n t o t a l length. The f i s h were k i l l e d by pithing and the gonads l i f t e d into a w a t e r - f i l l e d P e t r i dish. The eggs were separated using forceps and a blunt seeker. Errors and v a r i a b i l i t y i n egg counts were due to the d i f f i c u l t y of counting eggs i n unripe gonads, and the tendency of gravid females to spontaneously drop eggs. Results In 10 infected mature females egg number ranged from 26 to 78 with a mean near 55, and four unparasitised egg counts ranged from 41 to 53. With the small numbers of f i s h there was no demonstrable difference between the infected and uninfected f i s h . The egg number was low when compared to the numbers of eggs found i n Coal Harbour trachurus. Ten s i m i l a r sized f i s h were carrying between 56 and 287 eggs with a mean near 130. (b) Standard r e s p i r a t i o n rate of infected f i s h compared  to controls Method The standard r e s p i r a t i o n rate of twenty four sticklebacks was found by sealing i n d i v i d u a l f i s h i n jars for a known time 20 i n t e r v a l and measuring the decrease i n oxygen content of the water. The f i s h were paired, one infected and one control, on the basis of t h e i r length. A l l lengths were measured to the nearest mm. below the t o t a l length. The f i s h were not fed for the twenty four hours previous to the s t a r t of the experiment. Those f i s h whose oxygen consumption was measured at temperatures above t h e i r acclimation temperatures ( i . e . 17, 18, 20 and 2 1 ° c , see Table V), were raised to those temperatures from t h e i r holding temperatures during the morning preceding sealing i n the evening. At the s t a r t of the experiment, the tank to be used as the water bath was at the appropriate temperature and contained the f i s h . The f i s h were caught with as l i t t l e disturbance as possible and put into jars with a small amount of water. The tank was then aerated vigorously to ensure homogeneity of oxygen and the jars gently f i l l e d . A water sample from one of the jars, chosen at random, was then siphoned o f f , using a moistened tube, into a water sample b o t t l e of about 280 ml. This sample was considered representative of the oxygen concentration i n a l l the jars at the s t a r t of the experiment. The j a r providing the i n i t i a l sample was then r e f i l l e d and a l l the jars sealed under water to avoid bubbles. They were surrounded by black p l a s t i c to minimise any disturbance, and l e f t overnight i n the tank. A i r stones were l e f t i n the water to ensure mixing, and a maximum/minimum thermometer was placed i n the water to record the temperature. 21 The jars were kept sealed u n t i l there had been an estimated drop of a h a l f to two thirds of the o r i g i n a l oxygen content. Immediately before unsealing the jars were inverted once to avoid any s t r a t i f i c a t i o n , and the second sample siphoned out i n the manner already described. A l l oxygen determinations were made using the Winkler method as described i n E l l i s et al.., 1948, and also i n Hoar, 1956, Hoar and Hickman, 1967, and J o l l y , 1963. To f i n d the f i s h and worm weights, the f i s h were k i l l e d by pithing, the worms removed by a ventral s l i t , f i s h and worms l i g h t l y blotted, weighed separately and then placed i n a drying cabinet at 110°C for over f o r t y hours. They were then removed from the oven, allowed to cool for about a minute while covered with 'Parafilm', and re-weighed. The wet weights were recorded as a check on the dry weights. Worm dry weights were usually close to 30% of the wet weight, and f i s h dry weights around 20% of the wet weight, though f i s h values tended to fluctuate more widely. The volumes of the jars (approx. 920 ml.) were found by weighing the jars dry and again when f i l l e d with water. Result The r e s u l t s of the measurements of the standard r e s p i r a t i o n rate of infected f i s h and controls are given i n Table V. Infected and uninfected f i s h of s i m i l a r t o t a l length consume about the same amount of oxygen per hour. However, i t can be seen that the infected f i s h tend to have a lower dry weight of f i s h tissue compared with controls of the same length. Assuming that the par a s i t i s e d f i s h tissue 22 respires at the same rate as that of the controls, an estimate of the amount of oxygen i t would consume i s given i n the second column of Table VI. One would expect this to be an over-estimate as the par a s i t i s e d f i s h were thinner than the controls and hence had a higher proportion of slowly metabolising tissue such as bone. While aware of the assumption that we have made above, i t i s possible to calculate the oxygen consumption of the worm alone by subtracting the second column from the f i r s t , and these results are tabulated i n the t h i r d column. If the assumption i s v a l i d , then the worm i s consuming up to one t h i r d of the t o t a l consumption of the infected f i s h . The oxygen consumption of plerocercoids i n v i t r o , i n buffered saline solution, has been measured by Davies and Walkey (1966) using a Warburg apparatus. The oxygen consumption of the plerocercoids used i n Table V has been calculated from t h e i r findings and i s l i s t e d i n column 4 of Table VI. These values are r e l a t i v e l y small, only about one tenth of the t o t a l consumption l i s t e d i n column 1, and at the lower temperatures are lower than the values i n column 3, thus casting doubt upon the v a l i d i t y of the e a r l i e r assumption. Measurement of the standard r e s p i r a t i o n rate at the higher temperatures was more exposed to error. The f i s h were sealed for a shorter time period and hence any disturbance at the s t a r t or f i n i s h produced a r e l a t i v e l y greater e f f e c t . Also gonads were stimulated by the temperature r i s e and i n one case a male f i s h changed into f u l l breeding colours while sealed. The oxygen uptake of worms i n v i t r o , while open to errors r e s u l t i n g from the abnormal environment, does indicate that the 23 uptake when they are within the f i s h i s probably very small compared to the t o t a l uptake of a par a s i t i s e d f i s h , and hence, contrary to the e a r l i e r assumption, i t would appear that most of the oxygen uptake i s due to f i s h tissue alone. Assuming that the worm uptake i s zero, the consumption of pa r a s i t i s e d f i s h tissue per gram i s given i n Table VII, alongside values for unparasitised f i s h . The par a s i t i s e d f i s h are seen to consume more oxygen per gram of f i s h tissue than the controls. (c) A comparison of the swimming r e s p i r a t i o n rate of  infected and uninfected f i s h Method A swimming tube was constructed for i n d i v i d u a l sticklebacks s i m i l a r to that b u i l t by Brett (1965) for salmon, ' i t consisted of a 36 cm. swimming tube of 3.1 cm. in t e r n a l diameter (see F i g . 7); a ' L i t t l e Giant' 3-12N pump capable of l i f t i n g 5 metres of water and giving the apparatus a maximum flow of about 18 l i t r e s (four gallons) a minute; a 'Trident' household water meter ca l i b r a t e d i n tenths of a gallon; a thermometer and devices for introducing water and f i s h into the system and for releasing a i r bubbles. After the introduction of the f i s h , a water sample was taken at the s t a r t of the experiment and again at the end, and the two oxygen concentrations found by the Winkler method as already described. The i n t e r v a l between the f i r s t and second water samples was a maximum of three hours and was shortened i f the f i s h was exhausted e a r l i e r . The f i s h was stimulated to swim by the e l e c t r i f i e d g r i d (see diagram) which c a r r i e d two separate 24 s p i r a l s of copper wire. The g r i d was l i v e for ten milliseconds once per second, and c a r r i e d a maximum current flow of h a l f an amp and an adjustable potential difference of up to 100 v o l t s , 20 to 40 v o l t s being adequate i n most cases. The high voltages were found to be occasionally necessary because of mucus and algae that adhered to the g r i d . Fish were considered exhausted i f they were seen to f l i n c h but remain on the g r i d for twelve pulses, either consecutively or i n two groups of s i x . The equilibrium temperature of the c i r c u l a t i n g water was one degree ± 0.5 above the acclimation temperature of the f i s h . The procedure of using the apparatus was as follows. F i r s t the apparatus was f i l l e d with water from a b r i s k l y aerated aquarium at 15-20°C and close to saturation point i n oxygen. The flow through the apparatus was then adjusted using the tap, meter and stopwatch, the stimulator activated and the f i s h added. For the following twenty minutes the water was c i r c u l a t e d and at the same time water was drawn i n from the aquarium i n one place and allowed to flow out slowly into a sample bot t l e i n another. During t h i s time about six l i t r e s drained through the system and the sample bot t l e was taken as being representative of the water content of the apparatus. This time also enabled the f i s h i n i t s darkened tube to become used to the location of the g r i d . The water sample was then removed, inflow and outflow clamped closed, the stopwatch started and the meter read. After three hours, or sooner i f the f i s h was exhausted, the pump was stopped, 500 mis. drained from the apparatus and Winkler reagents immediately added to the sample. The number of gallons that had flowed through the meter divided by the time 25 gave the flow per minute, and from this and the diameter of the tube, the number of f i s h lengths per second was calculated. Errors due to laminar flow were reduced by the presence of grids i n the swimming tube. The water meter error was 3-5% lower than the true flow. The t o t a l volume of the closed apparatus was constant at 950 mis. Result F i g . 8 shows the oxygen consumption for twenty seven f i s h , of 50-63 mm. i n t o t a l length, for d i f f e r e n t swimming speeds expressed as lengths per second. The consumption per gram refers to f i s h weight only and therefore, from the standard re s p i r a t i o n r e s u l t s , one would expect infected f i s h to have a s l i g h t l y higher consumption regardless of flow. A l l f i s h are from Alouette Lake except for the square symbol which represents a leiurus from Mike Lake. The area within each symbol i s shaded i n proportion to the r a t i o : worm weight/fish weight, and i t can be seen that heavily infected f i s h are using twice as much oxygen as the controls to swim at the same speed. (d) Comparison between exhaustion times of infected and control f i s h  Me thod The apparatus described i n section 'c' was used without any water samples being taken and without the precautions necessary to remove a i r bubbles. Measurements of exhaustion times less than ten minutes were inaccurate because of the time taken for the f i s h to become accustomed to the tube and g r i d . Data was therefore c o l l e c t e d on f i s h from ten minutes to three hours. 26 Result The v a r i a b i l i t y i n the results obscured any difference between the two test groups, and the factors most important i n determining exhaustion time appeared to be d i r e c t l y r e l a t e d to the extent of g i l l infections and the general health of the f i s h . (e) E f f e c t of i n f e c t i o n on f i s h weight  Method The dry weights of infected and uninfected f i s h used i n various experiments were plotted against f i s h length (Fig. 9) and an analysis of covariance completed on f i s h whose lengths were 51 to 61 mms. Result The dry weights of 54 f i s h used i n d i f f e r e n t experiments are plotted on F i g . 9. Those f i s h having a worm/fish r a t i o equal to or greater than 0.46 are indicated by s o l i d c i r c l e s , unparasitised by open c i r c l e s . The r a t i o 0.46 was taken so that equal numbers of p a r a s i t i s e d and control f i s h from 51 to 61 millimetres long could be analysed by covariance analysis. The regression c o e f f i c i e n t s did not d i f f e r i n the two groups at the 9 5% l e v e l of probability, though through comparison of the variances of the adjusted means, i t appeared probable that parasitism affected the f i s h weight. It was concluded that infected f i s h were generally l i g h t e r i n weight of f i s h tissue than controls of the same length. 27 DISCUSSION Several aspects of the possible e f f e c t of Schistocephalus plerocercoids on the stickleback were examined and three revealed demonstrable changes. Infected sticklebacks were more l i k e l y to die than uninfected f i s h . This was not an unexpected r e s u l t but had nevertheless not been previously confirmed. This mortality was unrelated to the emergence of the worm. In only one instance did the worm emerge spontaneously and i n thi s case the f i s h died. Its death may not have been due to the emerging worm but to the opened coelomic ca v i t y since i n the instances where worms were removed s u r g i c a l l y , the f i s h that was sewn up l i v e d for four days while the other died within a few hours. Considering the amount of tissue present i n infected f i s h , the t o t a l standard r e s p i r a t i o n r a t e was higher than that found for normal f i s h tissue and iri v i t r o worm tis s u e . The low worm re s p i r a t i o n rates found by Davies and Walkey (19 66) are supported by Smyth (1946). He found that plerocercoids exposed to a i r gradually turned brown and he recommended that a l l culture work with these worms be c a r r i e d out i n semi-anaerobic conditions. Assuming then that the worm was responsible for only a very small part of the t o t a l r e s p i r a t i o n of an infected f i s h , the infected f i s h tissue was r e s p i r i n g at a greater rate than uninfected f i s h t i ssue. This may have been due to many factors. Movements of the worm may have disturbed the f i s h , keeping i t more active during the experiments, metabolic waste products of the worm may have been oxidised by the host or the host's c y t o l o g i c a l defence responses may have been using up extra energy; 28 During the observations on swimming f i s h , i t was found that p a r a s i t i s a t i o n had l i t t l e e f f e c t on the swimming a b i l i t y of f i s h . Any difference was obscured by factors unrelated to Schistocephalus. Both infected and uninfected f i s h were able to maintain a speed of 1 L/sec. (f i s h length per sec.) for several hours. At over 2 L/sec. the f i s h became greatly agitated and sought to escape from the tube. Bainbridge (1960) found that dace, trout and gold f i s h could sustain flows of 10 L/sec. f o r one second and about 4 L/sec. for twenty seconds. Brett, Hollands and Alderdice (1958) swam salmon f r y at 0°C and 20°C for one hour and found that the maximum speed sustained for a 5.4 cm. coho was 1.1 L/sec. at 0°C and 5.5 L/sec. at 2 0 O C . For sockeye at 6.9 cm. the values were 1.7 and 5.1 L/sec. The stickleback c r u i s i n g speed at 12-15°C (up to 1.8 L/ sec.) i s low compared with that of the salmonids and t h i s may be related to the method of swimming. At 1 L/sec. the salmonids swim by movements of the body and t a i l whereas the stickleback uses i t s pectoral f i n s to s c u l l through the water and the body and t a i l are kept s t i f f and straight. At flows of about 1.5 L/sec. s c u l l i n g movements are not adequate and the stickleback drops back only to regain i t s position with a f l i c k of the body and t a i l . Contrary to Smyth's observation (1946) that the swollen abdomen of infected f i s h produced unnatural swimming movements, the worms did not appear to p h y s i c a l l y a f f e c t s c u l l i n g movements or the smooth passage of the f i s h through the water. The amount of oxygen used by an unparasitised stickleback swimming at 1 L/sec. at 12-15°C i s about 1 ml/hr./gm. dry wt. (Fig. 8). From data i n Table IV on standard re s p i r a t i o n , a 29 h a l f to two thirds of this may be used i n standard r e s p i r a t i o n (0.5-0.7 ml./hr./gm..' dry wt.). The f i s h dry weights are approximately 20% of the wet weight so the t o t a l consumption at 1 L/sec. for 50 to 60 mm. f i s h can be expressed as 280 mgm. 02/hr./kgm. wet weight, of which a t h i r d to a h a l f (90-180 mgm. 0 2/hr./kg.) may be used for swimming at 1 L/sec. This compares favourably with data presented by Brett (19 63) for 180 mm. sockeye salmon which were using 63 mgm./hr./kgm. to swim 1 L/sec. at 15°C, though i t appears that the stickleback i s having to work a l i t t l e harder. Above a speed of 1 L/sec. (Fig. 8), the graph r i s e s sharply, the t o t a l consumption doubling by 1.7 L / s e c , whereas the sockeye salmon doubled i n t o t a l consumption at speeds above 2 L/sec. This r e f l e c t s the jerky, more excited swimming of the stickleback at the high flows. The heavily infected f i s h have a standard r e s p i r a t i o n rate of about 0.8-0.9 ml./hr./gm. and so the amount used f o r swimming at 1 L/sec. exceeds 1.0 ml./hr./gm. Compared with the 0.3-0.5 used by uninfected f i s h i t appears that the parasite i s having a marked e f f e c t on the stickleback. In applying these experimental findings to the observations on natural infections, l e t us f i r s t consider the mass die-offs of sticklebacks recorded by many people. The heavy mortality of mature Gasterosteus aculeatus seen i n Coal Harbour was not due to the presence of Schistocephalus. The p o s s i b i l i t y of very l o c a l p o l l u t i o n cannot be ruled out but because of the widespread reports of mass deaths another explanation may be sought. On a hot calm day i n August, the temperature of the water i n this corner of Coal Harbour i s over 30 22°C and hence i t s dissolved oxygen capacity i s greatly reduced. It i s conceivable that several large shoals passing to and f r o could deplete the oxygen content to below a l e v e l necessary to support the f i s h and anoxia would r e s u l t . Very few of the Coal Harbour f i s h were carrying Schistocephalus. However, i t i s c l e a r from the results that the f i s h that are burdened with t h i s parasite have an oxygen demand higher than normal and thus would be more susceptible to death through anoxia. The r e l a t i o n between the mass die-offs of f i s h and the emergence of plerocercoids remains unknown. The most detailed information on a natural l o c a l i n f e c t i o n was obtained from Alouette Lake. The f i s h caught were close to 100% infected throughout the year and this obscured any seasonal fluctuations i n the proportion of t o t a l population infected. Infected f i s h between 20 and 45 mm., t o t a l length, c a r r i e d more worms than those f i s h over 45 mm., and since more of the smaller f i s h were caught i n the summer, larger numbers of small worms were found i n the summer. This agrees with the summer increase i n numbers of small worms found by other authors (Smyth, 1946; Arme and Owen, 1967; etc.), though they do not indicate whether the increase i s also related to the average size of f i s h sampled. The r e s u l t s have shown that large plerocercoids have l i t t l e e f f e c t on each other's growth (Fig. 5). This has already been shown to be true for very small plerocercoids by Clark (1954). He experimentally infected eight sticklebacks with one procercoid each, and three with two. During the f i r s t 50 days there was no difference i n worm growth between the single and double i n f e c t i o n s . Orr, Hopkins and Charles (1969) exposed f i s h 31 to infected copepods three times over a period of a month and found that within the sticklebacks there were three sizes of young plerocercoids, i n d i c a t i n g that immunity was not developed by infected f i s h . i n Alouette Lake, f i s h less than 45 mm. c a r r i e d on average more worms than large f i s h , so, from the foregoing, i t i s concluded that small f i s h were more exposed to i n f e c t i o n than the larger f i s h . This agrees to some extent with Hynes;'; (1950) data on the food of Gasterosteus'aculeatus l e i u r u s . He found that f i s h up to 2 5 mm. long ate three times as many copepods as those f i s h at 55 mm. A worm burden decreases the weight of the f i s h (Fig. 9), i t a ffects the l i v e r weight and blood c e l l count (from Arme and Owen, 1967), abundance of f a t tissue (Vik, 1954), and infected f i s h are more l i a b l e to die (Table I I I ) . It i s concluded then, i n opposition to Smyth's (1946) suggestion that the worms are eliminated, that the heavily infected f i s h die sooner than those containing only one or two worms, i n other words, as the t o t a l worm burden increases, so the mortality rate increases. Though i t i s in e v i t a b l y r i s k y to b u i l d up a theory on data derived from natural populations, so fa r the facts have provided reasonable grounds for conclusions. The results of section I have already suggested that a Schistocephalus i n f e c t i o n increased the c a t c h a b i l i t y of the f i s h at Alouette Lake so the conclusions can be summarised as follows. At Alouette Lake, the f i s h s t a r t accummulating worms when the f i s h are 20 mm. long. As the f i s h grow, the weight of worms grows, each worm growing more or less independently of i t s neighbour, and the more heavily infected f i s h die. At the same time the f i s h become less 32 exposed to i n f e c t i o n and also become less catchable by beach seine. The worms continue to grow and when the t o t a l worm burden reaches a c e r t a i n size, the f i s h again become catchable. The increased c a t c h a b i l i t y of adult f i s h once the worm has attained a c e r t a i n size may also r e f l e c t a change i n the type and rate of natural predation. There i s l i t t l e information on predators at Alouette Lake. The lake has been stocked with lake trout. No large trout were ever seen i n the shallow stream outlets and i t i s possible that predation by f i s h i s lower i n the outlets than i n the deeper waters of the lake. The only b i r d predator seen at the lake was a kingfisher bufi, from the occurrence of infected f i s h i n very shallow water one could conclude that the p o s s i b i l i t y of predation by shore birds i s high at the o u t l e t s . " It i s possible then that a f t e r i n f e c t i o n f i s h become less susceptible to f i s h predation and more susceptible to b i r d predation, an example of a host/parasite i n t e r a c t i o n which increases the chances of a parasite reaching the next stage i n i t s l i f e c ycle. Incidentally, the apparent shortage of b i r d predators at Alouette Lake may account for the abundance of catchable infected f i s h compared with neighboring bodies of water such as Cultus or P i t t Lakes. A non-random d i s t r i b u t i o n of infected f i s h i n a f i s h population has been reported by Orr (1966). He found that rudd, Scardinius erythrophthalmus, infected with Ligula i n t e s t i n a l i s , a c l o s e l y related cestode that also reaches a large size r e l a t i v e to i t s host, did not gather into spawning shoals with other i n d i v i d u a l s . This he a t t r i b u t e d to the i n h i b i t i n g e f f e c t of 33 Licfula on the gonads, thereby preventing secretion of, or response to, sterohormones, important i n the behaviour of spawning f i s h . This cannot be the case i n Schistocephalus as segregation appeared to occur outside the breeding season. Fish schools usually consist of f i s h of the same size (Marshall, 1965) and i t may well be that the physical d i s t o r t i o n , and the extra physiological stresses that this imposes, prevent infected f i s h from schooling with the uninfected ones. For example, the r e s p i r a t i o n measurements have shown a marked change with i n f e c t i o n , e s p e c i a l l y i n active f i s h . This i s more dramatic than other e f f e c t s previously noted, and would be expected to a f f e c t f i s h behaviour i n several ways. Infected f i s h may seek well oxygenated water, for example at the surface or i n a creek, and these f i s h may also avoid excessive a c t i v i t y and would therefore seek a sheltered habitat. This corresponds well with the observed d i s t r i b u t i o n . The infected f i s h i n Alouette Lake were found i n shallow water around stream o u t l e t s . This study was i n i t i a t e d to examine the e f f e c t of the worm on the f i s h with a view to predict the e f f e c t oh the f i s h population. However, time scales are obscure because of the lack of information on the rate of growth of the worm and the rate of growth of the stickleback. The best data on the growth of the worm i s given by Orr and Hopkins (1969), who show that a f t e r three months at 19°C worms weighed 20 mgm. dry weight. The Alouette Lake worms from 45-65 mm. f i s h weighed 50-150 mgm. dry weight, and over the year the surface temperature of the lake varied from 6°C to 22°C, while creek water running into the lake never rose above 13°C. 34 The l i t e r a t u r e abounds with papers on the growth rate of sticklebacks. Some propose a four year growth period (Wunder, 1928 and 1930; Bock, 1928; Jones and Hynes, 1950), others a single year (van Mullem and van der Vlugt, 1964), and others through laboratory experiments f i n d that f i s h can be reared to maturity i n six to eight months (Wunder, 1930; Baggarman, 1958; Craig-Bennet, 1931). The presence of immature 30-35 mm. f i s h i n the May-June sample, i . e . immediately prior to the spawning season, may indicate that f i s h take two years to reach maturity i n Alouette Lake. However, the population was probably not randomly sampled, as has been suggested i n the r e s u l t s , and so l i t t l e information can be gleaned about growth from the length frequencies presented. Without some idea of the growth rate of the f i s h and of the plerocercoids, i t i s d i f f i c u l t to assess the course of the i n f e c t i o n i n Alouette Lake. However, th i s study has given an i n d i c a t i o n of the nature of the parameters important for an analysis of the e f f e c t of the i n f e c t i o n on a population. F i r s t , p o s s i b i l i t y of i n f e c t i o n i s high i n f i s h from 15 to 35 mm., and then decreases i n larger f i s h . Secondly, as the t o t a l weight of worms increases, so mortality increases. Thirdly, i n f i s h over 40 mm., when the worm weight/fish weight r a t i o i s about 0.3 the f i s h probably become more exposed to b i r d predation- and less to f i s h predation. Many authors have shown that i n d i v i d u a l f i s h harbouring th i s large p a r a s i t i c growth do not e x h i b i t the e f f e c t s normally associated with parasites, and Schistocephalus i n Gasterosteus i s generally considered a 'well-adapted' parasite. This study 35 has shown that the standard r e s p i r a t i o n rate of the p a r a s i t i s e d f i s h i s higher than normal considering the amount of f i s h tissue present. However, i t may well be that the main r e s u l t of the i n f e c t i o n i s to increase the energy requirement of the f i s h to enable i t to carry i t s burden through the water. 36 REFERENCES Arme, C. and Owen, R. Wynne. (1967). Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Muller, 1776), with special reference to pathological e f f e c t s . Parasitology J57: 301-314. Baggerman, B. (1958). An experimental study on the timing of breeding and migration i n the three-spined stickleback (Gasterosteus aculeatus L.) . Arch, neerl. Zool. jL2_: 109-317. Bainbridge, R. (1960). Speed and stamina i n three f i s h . J. Exp. B i o l . 37.: 129-153. Bennet, M. A. Craig-. (1931). Cited by Jones and Hynes, 1950. Bock, F. (1928). Cited by Jones and Hynes, 1950. Brett, J. R. (1963). The energy required for swimming by young sockeye salmon with a comparison of the drag force on a dead f i s h . Trans. Roy. Soc. Canada 1 (4) Section 3: 441-457. Brett, J. R. (1965). The swimming energetics of salmon. S c i . Amer. 213 (2): 80-85. Brett, J. R., Hollands, M. and Alderdice, D. F. (1958). The e f f e c t of temperature on the c r u i s i n g speed of young sockeye salmon. J. Fi s h . Res. Bd. Canada .1_5: 587-605. Clark, A. S. (1954). Studies on the l i f e cycle of the pseudophyllidian cestode Schistocephalus solidus. Proc. Zool. Soc. London 124: 257-302. Davies, P. S. and Walkey, M. (1966). The e f f e c t of body size and temperature upon the oxygen consumption of Schistocephalus  solidus. Comp. Biochem. & Phys. 18.: 415-425. Davis, H. S. (1961). Culture and diseases of game fi s h e s . University of C a l i f o r n i a Press, Berkeley and Los Angeles. 332 pp. E l l i s , M. M., Westfall, B. A. and E l l i s , M. D. (1948). Determination of water q u a l i t y . U.S. Fish and W i l d l i f e Service, Research Report 9. 122 pp. Hoar, W. S. (1956). Environmental physiology of animals. Scholar's Library, New York. 98 pp. Hoar, W. S. and Hickman, C P . (1950). A laboratory companion for general and comparative physiology. Prentice H a l l , New Jersey. 296 pp. 37 Hopkins, C. A. (1950). Studies on cestode metabolism. 1. Glycogen metabolism i n Schistocephalus solidus i n vivo. J. Parasit. 36: 384-390. Hopkins, C. A. and Smyth, J. D. (1951). Notes on the morphology and l i f e h i s t o r y of Schistocephalus solidus (Cestoda: Diphyllobothriidae). Parasitology 41: 283-291. J o l l y , S. C , ed. (1963). O f f i c i a l , standardised and recommended methods of analysis. A n a l y t i c a l Methods Committee, Society for A n a l y t i c a l Chemistry. W. Heffer and Sons Ltd., Cambridge, pp. 181-184. Jones, J. W. and Hynes, H. B. (1950). The age and growth of Gasterosteus aculeatus, Pvgosteus pungitius and Spinachia  vulgaris, as shown by t h e i r o t o l i t h s . J. An. Ecol. 19: 59-73. Kerr, T. (1948). The p i t u i t a r y i n normal and p a r a s i t i s e d roach (Leusiscus r u t i l u s Flem.). Q. J l . Microsc. Soc. 89: 129-137. Marshall, N. B. (1965). The l i f e of f i s h e s . Weidenfeld and Nicolson, London. 402 pp. Mullem, P. J. van and Vlugt, J. C. van der (1964). On the age, growth and migration of the anadromous stickleback, Gasterosteus aculeatus L. investigated i n mixed populations. Arch, neerl. Zool. 16 (1): 111-139. Orr, T. S. C. (1966). Spawning behaviour of rudd, Scardinius  erythrophthalmus infested with plerocercoids of Ligula  i n t e s t i n a l i s . Nature 212 (5063): 736. Orr, T. S. C. and Hopkins, C. A. (19 69). Maintenance of Schistocephalus solidus i n the laboratory with observations on rate of growth of, and p r o g l o t t i d formation in, the plerocercoid. J. Fish. Res. Bd. Canada 26.: 741-752. . Orr, T. S. C , Hopkins, C. A. and Charles, G. H. (1969). Host s p e c i f i c i t y and r e j e c t i o n of Schistocephalus solidus . Parasitology 59.: 683-690. Smyth, J. D. (1946). Studies on tapeworm physiology. 1. The c u l t i v a t i o n of Schistocephalus solidus i n v i t r o . J. Exp. B i o l . 23: 47-70. T h r e l f a l l , W. (1968). A mass die-of f of three-spined sticklebacks (Gasterosteus aculeatus L.) caused by parasites. Can. J. Zool. 46: 105-106. Vik, R. (1954);. Investigation on the pseudophyllidian cestodes of f i s h , birds and mammals i n the Anjzfya water system i n Tr^ndelag. Part 1. Cyathocephalus truncatus and Schistocephalus solidus. Nytt Mag. Zool. 2: 5-51. Wardle, R. A. (1933) . The p a r a s i t i c helminths of Canadian animals. Can. J. Research 8: 317-333. Wunder, W. (1928) -and (1930). Cited by Jones and Hynes, 19 39 F i g . 1. Length frequencies of Gasterosteus aculeatus from Coal Harbour. shaded - infected with Schistocephalus v . t r a c h u r u s v . s e m i - a r m a t u s v . l e i u r u s MAR-APR-MAY 20 DEC-JAN-FEB 40 F i g . 2. Size frequencies of Schistocephalus and length frequencies of Gasterosteus aculeatus trachurus from Alouette Lake. shaded st i p p l e d -infected with Schistocephalus not infected with Schistocephalus Schistocephalus G a s t e r o s t e u s 2 0 0 , . 4 O 0 vol. units 6 0 0 4 0 6 0 length mm. SEP-OCT '68 no data NOV-DEC "68 JAN-FEB '69 no data 41 F i g . 3. Size of plerocercoids plotted against host length (from Alouette Lake, 19 68-69). open c i r c l e - multiple i n f e c t i o n s o l i d c i r c l e - single i n f e c t i o n 0 1200- to o 800-w o r m v o l . u n i t s 400-0 o oo CO c © « 4 « ooafc oo c coo 8 OCOQ c8a COQ ® 08« 900809 0 038O9O9 CCCDOQ os«K»«l8§88oooo AO CD90 CCCXX^ C^ SCQCOO o oc»o 000 oo o oo o © «C4 «xx> f i s h l e n g t h m m . CCO0O0OSO3 00 o 0 oo oo o 50 — 1 — 60 42 F i g . 4. Size of plerocercoids plotted against number present i n host (from Alouette Lake, 1968-69). (a) From a l l f i s h i n 50 and 55 mm. length groups. (b) From the 50 and 55 mm. f i s h i n (a) omitting those with worms less than 32 5 volume units. (c) Means and standard deviations from (b). One standard deviation shown on ei t h e r side of mean. 800-w o r m v o l . u n i t s 400-(a) —r— 4 — i — 5 6 lb) • • I #f . . . . . • ••«• i 2 T 3 n o . w o r m s p e r f i s h 43 Fi g . 5. Total worm burden plotted against f i s h length (Alouette Lake f i s h , 1968-69). (a) Random samples. (b) Fish selected f o r use i n experiments. open c i r c l e - multiple i n f e c t i o n closed c i r c l e - single i n f e c t i o n cross - unparasitised f i s h 1 6 0 0 -1 2 0 0 -w o r m v o l . u n i t s 8 0 0 -4 0 0 -o o 2 0 O « 3 0 8 g o o o - R x -4 0 to SO *>ati» o 8 o # f i s h l e n g t h m m . 5 0 6 0 O 2 0 0 -w o r m d r y w e i g h t 1 6 0 -O 0 m g . 1 2 0 -8 0 4 0 -g O * « ° V • o » o o o o 3 o *>» a • • o * O O 4 0 5 0 6 0 2 0 3 0 f i s h l e n g t h m m . 44 F i g . 6 . Length f r e q u e n c i e s o f 3 f i s h samples f o r H a i g Lake, C o r t e s I s l a n d . Upper h i s t o g r a m : shaded - p a r a s i t i s e d Lower h i s t o g r a m : s t i p p l e d - r e d u c e d p e l v i c s p i n e s S h o r e O p e n w a f e r 45 F i g . 7. Apparatus for measuring the oxygen consumption of swimming sticklebacks. 46 F i g . 8. Oxygen consumption of sticklebacks at d i f f e r e n t swimming speeds. c i r c l e s - Alouette Lake f i s h square - Mike Lake f i s h * x . JZ - U J • • i • . worm wt. . . Amount of shading i n proportion to f ^ s ^ w t r a t i o ml. O a per hour per gram 1.0-Q O O O O o 1 . — — i . . .—•—,—-0.5 1.0 lengths per sec. 47 F i g . 9. Length/weight re l a t i o n s h i p for Gasterosteus aculeatus trachurus. open c i r c l e s - p a r a s i t i s e d closed c i r c l e s - w o r m w t - r a t i o greater than 0.46 f i s h wt. o 300H dry weight mg. 200 O O o o o c o o o o o o o o o o ® s o o o o 100 40 50 60 length mm. 48 Table I. Schistocephalus infections i n the Fraser Valley and environs % infected Number Date to nearest i n 1% sample Race Stave River L i t t l e Campbe11 Q.E. Park 28.1.68 15.8.68 5. 7.68 7.8. 68 12.9.68 Tin Can Creek (Musqueam Res.) P i t t Lake Horse Shoe Bay Burnaby Lake Cultus Lake Haig Lake, Cortes Is. Canal, Cortes Is. Gunflint Lake, Cortes Is. 4.7.68 6.7.68 9.7.68 9 .8 . 68 3.10.68 26.9.68 6.9.68 6. 9 . 68 6.9.68 Kendall Creek 13.3.69 Mike Lake 24.4.69 3 0 2 3 0 0 0 0 3 88 34 12 1 29 10 69 33 100 51 39 29 105 32 11 92 26 32 50 50 42 mixed leiurus dip net pole seine dip net pole seine dip net dip net trachurus dip net I I I I M leiurus dip net trachurus trap trachurus beach seine trachurus " trachurus pelagic seine leiurus  leiurus pole seine dip net Cont. 49 Table I. (Cont.) Coal Harbour 29.3.69 1. 5. 68 31.5.68 3 . 7 . 68 15.8.68 3.9.68 10 .ID. 68 20.10. 68 31.10.68 24.11.68 16.12.68 7.1.69 12.2.69 26.3.69 3.4.69 8.5.69 27.6.69 14.8.69 Alouette 2 5.8.68 Lake 6.10.68 24.12.68 8.3.69 20. 4.69 13.5.69 23.5.69 5.6.69 7. 7. 69 7.8. 69 7 145 mixed 13 16 36 33 20 35 3 86 4 54 6 108 0 46 1 1000+ 0 132 0 75 " 0 68 0 146 0 2 7 0 154 1 140 " 2 65 1 148 100 67 trachurus 100 18 100 18 100 27 100 35 100 41 72 67 80 35 88 17 75 52 dip net from pier I I I I I I beach seine I I M H I I seine from pier beach seine seine from pier II I I II M beach seine seine from pier n I I beach seine seine from pier beach seine 50 Table I I . Number of worms per f i s h . Alouette Lake 19 68-69 Fish length group mms. No. of f i s h sampled No. f i s h infected Total no. worms Infected f i s h Average no. worms Max. no. worms found 15 20 25 30 35 40 45 50 55 60 65 5 4 25 26 24 17 45 71 84 18 2 0 1 15 16 19 15 45 70 77 17 0 0 1 30 48 66 44 98 133 121 22 0 0 1.0 2.0 3.0 3.5 2.9 2.2 1.9 1.6 1.3 0 0 1 5 11 10 16 10 7 4 2 0 Table I I I . Numbers of f i s h with s p e c i f i c numbers of worms. (All f i s h , Alouette Lake 1968-69) No. of worms Aug. ' 68 Dec. Mar. 11 69 A p r i l May June July Aug. Totals 0 0 0 0 0 3 (18) 4 (1) 2 6 (9) 15 (28) 43 1 15 (3) 9 12 16 (1) 24 (22) 8 (2) 6 (1) 27 (3) 117 (32) 149 2 8 (2) 4 12 12 12 (10) 2 3 (1) 2 (1) 55 (14) 69 3 9 2 1 6 2 (5) 1 (1) 21 (6) 27 4 4 (1) 3 1 1 1 3 (1) 13 (2) 15 5 3 (2')' (2) 3 (4) 7 6 (2) (2) 2 7 2 (1) 2 (1) 3 8 1 1 1 9 (1) (1) (2) 2 10 1 (1) (1) 1 (2) 3 11 (1) (1) 1 16 (1) (1) 1 Total 42 (7) 18 26 (1) 35 (1) 41 (63) 15 (4) 13 (4) 38 (15) No brackets = f i s h 45 mm. and over Brackets = f i s h less than 45 mm. 52 Table IV. Mortality of infected and uninfected Gasterosteus Fish kept i n lab. aquaria at 12-15°C Coal Harbour Fish Expt. A 4th Aug.-12th Oct. 69 days (9 weeks) Died Alive Infected 5 3 Uninfected 1 16 Expt. B 20th Oct.-29th Jan.. 100 days (14 weeks) Died Aliv e infected 4 2 Uninfected 3 12 Combined A and B Died Alive Totals infected 9 5 14 Uninfected 4 28 32 Totals 13 33 46 Table V. Standard respiration rate of paired f i s h Control f i s h Date Length nun. Fish wt. gm. Worm wt. gm. °„2 ml/hr 11/12 June 56 0.2291 - 0.117 16/17 June 56 0.2291 - 0.146 18/19 June 0.1571 - 0.113 29/30 June 62 60 0.3523 0.3265 - 0.135 0.139 55 0.2073 - 0.091 61 0.3466 - 0.094 10/11 July 50 62 0.1628 0.2566 0.0444 0.0909 0.265 0.334 4/5 Aug. 51 60 0.2205 0.2916 -0.209 0.297 12/13 Aug. 59 0.2697 - 0.263 Paras i t i s e d f i s h mgth mm. Fish wt. gm. Worm wt. gm. ml / r l r . Expt. Temp. °C Ac c l i i Temp °C 58 0.2050 0.1717 0.164 10 10 58 0.2050 0.1717 0.174 11 11 0.1556 0.0832 0.131 12 11 0.1365 0.0086 0.101 12 11 62 0.3327 0.1121 0.149 10 10 59 0.2776 0.1405 0.131 10 10 56 0.2146 0.1541 0.110 10 10 60 0.3900 0.1308 0.148 10 10 46 0.1037 0.1105 0.189 21 11 59 0.2256 0.1812 0.383 20 11 51 0.1620 0.1127 0.181 18 12 58 0.2760 0.1452 0.305 18 12 59 0.2106 0.0913 0.237 17 14 U l Table VI. Oxygen consumptions of par a s i t i s e d f i s h  as observed and as calculated Total 0 o Fish tissue - ^ - j - r - Worm tissue T A 2 ,^ Difference _ , ml/hr. 0 2 ml/hr. ml/hr 2 m l/* i r-observed estimated* ' * estimated* 0.164 0.105 0.059 0.013 0.174 0.132 0.042 0.013 0.101 0.098 0.003 0.002 0.149 0.126 0.025 0.008 0J131 0.120 0.011 0.006 0.110 0.094 0.016 0.009 0.148 0.105 0.044 0.007 0.189 0.169 0.020 0.024 0.383 0.293 0.090 0.026 0.181 0.154 0.027 0.022 0.305 0.281 0.014 0.036 0.237 0.206 0.031 0.014 * Values calculated from i n v i t r o experiments of Davies and Walkey, 1966 ^ Values calculated from r e s p i r a t i o n rate of control f i s h 55 Table VII. Total oxygen consumption as per gram  f i s h tissue only Control mis .Air ./gm. 0.51 0.64 0.72 0.38 0.43 0.44 0.27 1.63 1.30 0.95 1.02 0.98 Parasitised mis ,/hr ./gra. 0.80 0.85 0.84 0.74 0.45 0.47 0.47 0.38 1.82 1.70 1.12 1.05 1.13 

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