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The development of Taenia pisiformis in various definitive host species
International Journal
for Parasifology.1975.Vol.
5. pp. 633-639.Pergamon Press. Printed in Great Britain.
THE DEVELOPMENT OF TAENZA PZSZFORMZS IN VARIOUS DEFINITIVE HOST SPECIES IAN BEVERIDGE
and
MICHAEL
D. RICKARD
Department of Veterinary Paraclinical Sciences, University of Melbourne, Veterinary Clinical Centre, Werribee, Victoria, 3030, Australia (Received 20 December 1974) Abstract-BEVERIDGE
I. and RICKARD M. D. 1975. The development of Taeniff pisiformis in various definitive host species. International Journal for Parasitology 5: 633-639. In pups experimentally infected with T. pisiformis evagination and attachment of cysticerci occurred in the small intestine, proglottization was initiated 3-5 DA1 and gravid cestodes were recovered on and after 35 DAL Establishment in fox cubs (Vrdpes v&es) was similar but only a few worms had become gravid by 70 DAI. T. pisiformis developed slowly in kittens and although reaching sexual maturity 21 DAI, infections were lost before worms became gravid. Cysticerci fed to ferrets (Musteluputorius) evaginated in the small intestine but failed to attach and passed rapidly into the colon. No significant hostinduced effects on morphological features of the parasites, apart from their sizes and rates of development, were detected.
INDEX KEY WORDS: establishment.
Tuck
development; .rtisifhrmis; .
INTRODUCTION
host records of Tueniapisif~~mis indicate that it parasitizes the intestine of a relatively wide range of carnivore species belonging to the families Canidae, Felidae and Mustelidae (Abuladse, 1964; Leiby & Dyer, 1971). Records are most numerous for species of the family Canidae and include the domestic dog, wolves, foxes, coyotes, jackals and dingoes. T. pisiformis has been collected from large felids (lions and tigers) (Benoit-Bazille & Dramard, 1905; SouthwelI, 1912; Baer, 19X), from lynxes ~ollin~, 1945; Loftin, 1961; Van Zyll de Jong, 1966; Little &Hopkins, 1969) and from domestic cats (Neumann, 1896; Lewis, 1927; Skurski, 1963; Styles & Evans, 1971) though some evidence suggests that development in felids may be limited (Benoit-Bazille & Dramard, 1905; Van ZylI de Jong, 1966). Ackert & Grant (1917) experimentally infected kittens and recovered only a few cestodes; in most of these development had not proceeded beyond the appearance of a genital anlagen in the terminal proglottides, and the most advanced stage reached was sexual maturity. T. pisiformis has been reported on one occasion (Jacob, 1939) from a mustelid (Musteh putorius) though the validity of the record has been questioned (Verster, 1969). Although a common parasite of foxes, the few experimental studies carried out on development in these hosts have provided conflicting results. Dubnitskii (1946) reported a prepatent period of 82-95 days for T. pisiJbrmis in red foxes (Vulpes DEFINITIVE
dog; cat; fox (Vulpes dozes);
ferret;
vu&es) whilst in experiments reported by Matov & Yanchev (1955), T. pisiformis failed to achieve patency in this host. Dubnitskii (1946) recorded poor establishment and growth of the parasite in arctic foxes (Alopex lagopus). Apart from contradictory experimental data and the lack of reliability in certain host records, comparisons of the development of T, pisiformis in different host species are limited by the lack of knowledge of its development in the normal host, the dog. The only observation on establishment of T. pisiformis in the intestine has been made in cats (Ackert & Grant, 1917), and apart from a report (Fotselveva-Sakhno, 1958 cited by Abuladse, 1964) of a prepatent period in the dog of 35-46 days, nothing is known of the establishment, growth and development of the parasite in this host. The present study was undertaken to define various growth parameters in dogs and to compare the development of the cestode in representative members of the families Canidae, Felidae and Mustelidae. MATERIALS
AND METHODS
Cestodes. Cysticerci were derived from an inbred line of T. Disiformis of doa origin. adult cestodes of which had been *“selfed” twice prior ‘to commencement of this experiment. Rabbits, infected with eggs collected from these worms, were killed by cervical dislocation as required but not earlier than 6 weeks after infection. Mature cysticerci were collected into normal saline still within their host tissue capsule and fed to definitive hosts within 1 h of the death of the rabbit. 633
634
IAN BEVERIDGEand MICHAELD. RICKARD
Experimental animals. A total of 26 pups, 28 kittens, 9 fox cubs (Vulpes vulpes) and 3 ferrets (Mustela putorius) were used when 7-8 weeks of age; 14 ferrets approximately 1 year old were also used. Fox cubs were collected from dens when approximately 4 weeks of age and hand reared to preclude infection with taeniid cestodes. All animals were treated with bunamidine hydrochloride (Scolaban, Burroughs Wellcome Co. Ltd.) and piperazine citrate (Antoban, Burroughs Wellcome Co. Ltd.) prior to their use in experiments, to eliminate infections with Dipylidium caninum and round-worms. For 2 weeks prior to and throughout the course of the experiments, all animals were maintained on an identical diet of tinned dog food (Pets Gold Label, Processed Meats Prop. Ltd., Aust.) supplemented with calcium phosphate and biscuits (Puppy Chow, R. Harper & Co. Ltd., Victoria). Infections. Food was withdrawn from animals 12 h before force feeding with 10 cysticerci each; 4 of the kittens received 60 cysticerci each. Ferrets to be killed at 4 and 6 hours after infection (HAI) were individually caged and their faeces collected until the time of death. Two ferrets were fed a meal 30 min prior to infection to determine the effect of feeding on establishment of cestodes. Recovery of cestodes. From 1 day after infection (DAI) onwards, animals were killed, between 9 and 11 a.m. (to eliminate any effects of diurnal cestode movement in the intestine), with a barbiturate overdose. The intestines were rapidly removed, stretched out on the bench, and searched for cestodes. The distance of the point of attachment of each cestode from the pylorus was noted and the frequency of occurrence of cestodes in 10 equal sectors of the small intestine calculated for different times after infection. Following removal from the host, cestodes were relaxed in water, fixed in 10% formalin and wet weight, total length and proglottis number determined. Points on graphs (Figs. l-4) represent mean parameters for the cestodes from 2 or 3 hosts killed at each time after infection. Differences in means were tested statistically using Student’s t-test. Whole worms or terminal proglottides were then stained in Mayer’s acid haemalum for morphological comparisons. In certain instances, eggs removed from gravid proglottides prior to fixation were counted using a Spencer “Bright line” haemocytometer, and tested for their viability and infectivity in vitro, using the method of Rickard & Bell (1971) and by feeding to rabbits. Morphological comparisons. Cestodes from each host were examined for differences in internal morphology. Features examined included the size and morphology of the cirrus sac, its relationship with the longitudinal osmoregulatory canals, number and distribution of testes, position of ovaries and vitellaria and number of uterine branches.
RESULTS Recovery
of cestodes
The overall recovery rate of cestodes from 24 dogs killed between 0.5 HA1 and 42 DA1 was 84x, similar recovery rates being obtained at different killing times through the course of the experiment. High recovery rates were also obtained from fox cubs. In cats, recoveries for the first 10 days of the experiment were almost comparable with those from
I.J.P. VOL.5. 1975
dogs, however, a decline followed and between 28 DA1 and 42 DA1 1 cestode only was recovered from a total of 290 cysticerci fed to 9 kittens (Fig. 1).
In 8 ferrets killed 0.5 to 4 HAI, 92% of cestodes were recovered; none were recovered from 6 ferrets killed 6 HAI. 12 HA1 and 7 DAI.
FIG. 1. Percentage recovery of T. pisi.formis from the small intestine of experimentally infected dogs, foxes and cats during growth. Establishment
A similar pattern of establishment was observed in dogs, foxes and cats. By 0.5 HA1 cysticerci were either unevaginated in the stomach or were evaginated and attached in the small intestine. One HAI, all cestodes were evaginated in the small intestine and were lying apposed to the mucosa, grasping villi with one or two suckers. Loss of the posterior bladder had commenced 1 HA1 and was complete by 6 HAI. At 24 HA1 the scoleces of most cestodes were deeply embedded in the mucosa with only a tag of strobila protruding. In serial histological sections, the rostellum was situated near the base of the villi, adjacent villi having been displaced or grasped by suckers. A few cestodes were found on the mucosal surface. Two ferrets were killed 0.5 HA1 and 15 cestodes were found evaginated in the small intestine but unattached. In 2 of 3 ferrets killed 1 HAI, 18 evaginated, unattached cestodes, 17 of them without posterior bladders, were recovered from the terminal one-sixth of the small intestine. In the third ferret, 9 evaginated, bladderless cestodes were located in the colon. From the 2 ferrets placed in individual cages after infection, and killed 4 HAI, 19 cestodes, without posterior bladders, were found in the faeces and none in their intestines. Three 6-week old ferrets were similarly caged when infected and 6 HA1 all cestodes were recovered in their faeces. In 2 ferrets fed immediately prior to infection and killed 6 HAI, all cestodes were likewise found in the faeces. In no ferret was any sign of cestode attachment to the intestinal mucosa noted.
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VOL.
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Development of Taeniu pisiformis
Migration
635 DOGS
-
During establishment in dogs, cestodes were found in all of the 10 sectors of the small intestine. At subsequent killing times, worms were usually attached in sectors 3 to 8, but no significant change occurred in median worm position during development. In cats, worms occupied a similar position in the small intestine during the period 3-21 DA1 and no migration was detected. Growth
Changes in the mean length, mean wet weight and mean proglottis number of cestodes during growth in dogs, foxes and cats are shown in Figs. 2-4. DOGSFOXES . .........____.. CATS..-.-.-..
FIG. 4. Increases in mean wet weight of T. pisiformis developing
FIG. 2. Mean numbers of proglottides of T. pisiformis in cestodes
developing in the small intestines of experimentally infected dogs, foxes and cats.
in the small intestines of experimentally infected dogs, foxes and cats.
Proglottisation was initiated at about 3 DA1 and there was a steady increase in proglottis number in cestodes from dogs until the onset of apolysis about 35 DAI. Curves for the increase in length and weight of worms during growth in dogs were sigmoidal in form, the rate of increase of both being markedly reduced by the onset of apolysis. Considerable variability was noted between cestodes from an individual host. Not uncommonly, even as early as 14 DAI, a single worm could be found which was much smaller than its 8 or 9 coinhabitant cestodes. At 42 and 75 DAI, cestodes from foxes were much smaller in all three parameters measured than those from dogs. The differences were, in each case highly significant (P < 0.001). Growth in cats between 0 and 21 DA1 was erratic and was slower than in dogs; increase in proglottis number most closely approximated that in dogs, whilst weight increases lagged considerably. Twentyone DAI, cestodes from cats were significantly lighter and shorter than those from dogs (P < 0.001) as well as having significantly fewer proglottides (0.05 < P < 0.02). Development In dogs. Examination
FIG. 3. Increases in mean length of T. pisi’rmis ing in the small intestines of experimentally dogs, foxes and cats.
developinfected
of fresh and stained worms from dogs revealed the following developmental stages: 7 DAI: T-shaped genital anlagen present in centre of terminal proglottides; 14 DAI: genital ducts dully formed; testes present but small; ovaries and vitellaria present; 21 DAI: proglottides mature, testes, ovaries and vitellaria fully developed; filling and primary branching of the uterus under way;
636
IAN BEVERIDGE and MICHAEL D. RICKARD
28 DAI: uterus extensively branched; lateral branches reaching the margin of proglottis medulla; testes and ovaries still visible; no sign of embryophore formation in uterine content; uterine material not infective when fed to each of 2 rabbits; 35 DAI: apolysis evident; 17 of 19 cestodes gravid, uterus filled with eggs numbering 2000-16,000 per proglottis; embryophores fully developed; eggs hatched and activated in vitro, infective when fed to 2 rabbits; 1 worm of 19 was only mature, and another had eggs in the uterus with incompletely formed embryophores; eggs of the latter worm disintegrated when placed in artificial intestinal fluid (AIF); 42 and 75 DAI: all worms gravid, 9000-28,000 eggs per proglottis; eggs hatched and activated in vitro, and were infective to each of 3 rabbits. In foxes. Cestodes recovered from foxes were relatively poorly developed. Seven DAI, a genital anlagen was present in the terminal proglottides, comparable in development to cestodes from dogs collected at the same time, however, 42 DAI, when the cestodes were gravid in dogs, those from foxes showed no evidence of apolysis (no proglottides had been detected in the faeces up to that time) and the worms varied in stage of development from those just mature to others in which uterine filling was at an advanced stage, but there was never any sign of embryophore formation. Between 71 and 75 DAI, one fox passed gravid proglottides in its faeces, and, 75 DAI, large fragments of a worm including the scolex. Eggs from the fragments hatched in vitro and were infective to each of 3 rabbits. When recovered from the two foxes 75 DAI, none of the remaining worms from the intestines were fully gravid and most had branched uteri without indications of embryophore formation, whilst one had eggs with incompletely formed embryophores.
unsegmented. Cestodes recovered 10 DAI had visible testes primordia, whilst those recovered 14 DA1 had only an anlagen present. At 21 DAI, the best developed cestodes were mature and testes, ovaries and vitellaria were fully developed but uterine filling and branching had not occurred. In other cestodes from the same hosts, rudiments of the genital duct system were visible but testes, ovaries and vitellaria were not seen. anlagen or were
Taxonomic characters
A detailed examination of various morphological characters used for taxonomic purposes failed to reveal any consistent differences in cestodes developing in the various host species. Results in Table 1 suggest that the number of testes per proglottis depends on the age of the worm, and that the relatively low number in cestodes from cats 21 DA1 is a function of the state of development of the worm rather than a specific host effect. Again, minor differences in topographical anatomy of the genitalia in cestodes from cats 21 DAI, namely elongate mature proglottides, testes not reaching anterior proglottis margin, ovaries extending to the lateral osmoregulatory canals and vitellaria compact and narrower relative to their height, were attributed to changes occurring during growth of the worms.
In cuts. Development of cestodes in cats was extremely variable. At 7 DAI, a genital anlagen was present in the terminal proglottides of the most advanced cestodes, whilst others contained no TABLE I-COMPARISONS
I.J.P. VOL. 5. 1975
DISCUSSION Evagination of cysticerci of T. pisiformis occurred in the small intestine and was followed by rapid attachment to the mucosa and detachment of the posterior bladder; this is similar to observations made by others for Taenia taeniaeformis (Hutchison, 1959) and Taeniu hydatigena (Featherston, 1969, 1971). Initial attachment appeared to be by one or two suckers grasping villi but by 24 HAI, the scoleces of most cestodes were deeply embedded in the mucosa and attached by their suckers and rostellum. The pattern of distribution of T. pisiformis in dogs
OF TESTISNUMBER PER PROGLOTTIS IN
Taenia pisiformis FROM EXPERIMENTALLY
lNFECTEDDOGS,CATSANDFOXES
Host
Dog
Age of cestodes No.
testes
(days)
Cat
42
14
75
21
562 _f 43
313 t 36
526 ? 42
415 + 30
486 - 628
284 - 397
460 - 628
333 - 445
20
10
20
5
per proglottis
mean + s.d. Range testis
Fox
No.
No. proglottides
counted.
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Development of Tueniu pisiformis
during the first 4 HA1 differed from that described for T. hydutigena by Featherston (1969); the latter parasite was found in the anterior sections of the intestine only and not spread throughout the small intestine as was T. pisiformis. These differences may reflect variations in technique rather than differences between the two cestode species. Cooreman & De Rycke (1972) observed that in starved mice, Hymenolepis microstoma establish further posteriorly than in fed animals; if these results apply to taeniids also, the administration of cysticerci to dogs 5h after feeding by Featherston (1969) and 16h after the removal of food in the present experiment, may account in part for the differences in distribution. Furthermore, intestinal motility patterns influence the rate of establishment and hence possibly the position of attachment of cestodes in the gut (Larsh, 1947; Read & Voge, 1954). Because gastrointestinal motility may be influenced by time of feeding this may also help to account for differences recorded between present results and those of Featherston (1969) and for some of the individual variability encountered in the recovery of cestodes from hosts. Migration of T. pisiformis within the intestine during development was not detected, in agreement with the results of Hutchison (1959) with T. taeniaeformis in cats; Featherston (1969) reported significant migrations of T. hydatigena during its development in dogs. Although T. pisiformis established and developed in fox cubs, the slow growth rate and the small numbers of cestodes which had become gravid by 75 DA1 suggests that the fox is a less suitable host than the dog. This is in agreement with the results of Dubnitskii (1946) but differs from those of Matov & Yanchev (1955). It has been noted (unpublished observations) that it is more difficult to infect adult foxes than cubs with T. pisiformis and that the development of any cestodes establishing is like-wise slower. Matov & Yanchev (1955) used experimental animals 8-12 months of age and of unknown previous history and this may account for their different results. T. pisiformis is clearly capable of establishing and developing in kittens although never becoming gravid, as shown previously by Ackert & Grant (1917). However, the largest mature specimens recovered from kittens in the present work were 30 cm in length, considerably larger than the 2.2 cm described by Ackert & Grant (1917). In our experiments cestodes of 2-3 cm contained only a genital anlagen, but Ackert & Grant (1917) gave no details of the treatment of their specimens prior to measurement and may have measured unrelaxed worms. T. pisiformis grows more slowly in cats than in dogs; the differences are least evident in proglottis number suggesting that rate of proglottis production is not rigidly tied to length and weight increases. Possible explanations for the loss of T. pisiformis
637
burdens in cats after 21 DA1 include physiological unsuitability of the cat’s intestine as an environment for the worm, and the development of a heightened immunological response on the part of the abnormal host. A phenomenon of destrobilation during development in unusual hosts has been reported for Hymenolepis diminuta in mice (Turton, 1971; Hopkins, Subramanian & Stallard, 1972a) and for H. microstoma in rats (Goodall, 1972) and loss of cestode burdens following the completion of growth has been reported for Raillietina cesticillus in its normal host the fowl (Gray, 1972). Hopkins, Subramanian & Stallard (19726) have shown that immunosuppressants prevent the elimination of H. nana in mice and that destrobilate specimens transplanted to rats or unexposed mice continue to develop, suggesting immunological involvement. However, Goodall (1972) failed to prevent elimination of H. microstoma in rats with immunosuppressants and postulated that the phenomenon was due to the physiological unsuitability of the rat as a host. T. pisiformis failed to establish in the intestine of ferrets and this was not affected by feeding ferrets immediately prior to infection or by the age of the hosts. It might be suggested that the rate of passage of cysticerci through the intestines of ferrets was too rapid to permit attachment, since some had reached the colon 1 HAI; however they were present in the small intestine for at least 30 min and this was sufficient time in cats and dogs to allow attachment. Smyth & Smyth (1968) have suggested that host intestinal topography may be an important factor in the establishment of Echinococcus g. granulosus, those host species having smaller crypts of Lieberkuhn being less suitable for its attachment and growth. However, the pattern of establishment of T. pisiformis is different to that of E. granulosus and apparently requires only grasping of villi by the suckers. It seems unlikely, therefore, that mucosal topography should affect the initial attachment of worms. Alternatively the intestinal lumen of the ferret may be physiologically unsuitable to initiate the stimuli leading to attachment. Evagination is a relatively non-specific phenomenon as it can occur spontaneously, in response to bile salts and to detergent like substances (DeWaele, 1933; Campbell, 1963; DeRycke & Grembergen, 1966) but the stimuli which initiate attachment are quite unknown and may be more specific. Apart from the degree of development and worm size, morphological features of taxonomic importance were not affected by development in different hosts. Changes in testis number occur with proglottis age and due care should be exercised in attributing great weight to differences in testis number between taxa. Although Christiansen (1931) described differences in the morphology of Tuenia krabbei recovered from experimentally infected dogs and foxes, comparison with the present results
638
IAN BEVERIDGE and MICHAEL D. RICXARD
suggests that the differences he described are attributable mainly to the state of development of specimens from the two host species and not to specific “host-induced” effects on internal morphology. Although only four host species were examined the results suggest an approximate negative correlation between the “success” of T. pisiformis in a given host and the phylogenetic distance between that host and the dog, a result not unexpected on evolutionary grounds in the case of a moderately specialized parasite infecting members of related but diverging host groups. Data on development in other host species are not available apart from the dingo (Curtis familiaris dingo) in which development is comparable to that in the dog (unpublished observations). This is not unexpected because of the close (subspecific) relationship of dingoes with dogs. Acknowledgement-This from the Australian wish to thank Mr. collecting fox cubs.
work was supported by a grant Meat Research Committee. We B. Coman for his involvement in
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for Parasifology.1975.Vol.
5. pp. 633-639.Pergamon Press. Printed in Great Britain.
THE DEVELOPMENT OF TAENZA PZSZFORMZS IN VARIOUS DEFINITIVE HOST SPECIES IAN BEVERIDGE
and
MICHAEL
D. RICKARD
Department of Veterinary Paraclinical Sciences, University of Melbourne, Veterinary Clinical Centre, Werribee, Victoria, 3030, Australia (Received 20 December 1974) Abstract-BEVERIDGE
I. and RICKARD M. D. 1975. The development of Taeniff pisiformis in various definitive host species. International Journal for Parasitology 5: 633-639. In pups experimentally infected with T. pisiformis evagination and attachment of cysticerci occurred in the small intestine, proglottization was initiated 3-5 DA1 and gravid cestodes were recovered on and after 35 DAL Establishment in fox cubs (Vrdpes v&es) was similar but only a few worms had become gravid by 70 DAI. T. pisiformis developed slowly in kittens and although reaching sexual maturity 21 DAI, infections were lost before worms became gravid. Cysticerci fed to ferrets (Musteluputorius) evaginated in the small intestine but failed to attach and passed rapidly into the colon. No significant hostinduced effects on morphological features of the parasites, apart from their sizes and rates of development, were detected.
INDEX KEY WORDS: establishment.
Tuck
development; .rtisifhrmis; .
INTRODUCTION
host records of Tueniapisif~~mis indicate that it parasitizes the intestine of a relatively wide range of carnivore species belonging to the families Canidae, Felidae and Mustelidae (Abuladse, 1964; Leiby & Dyer, 1971). Records are most numerous for species of the family Canidae and include the domestic dog, wolves, foxes, coyotes, jackals and dingoes. T. pisiformis has been collected from large felids (lions and tigers) (Benoit-Bazille & Dramard, 1905; SouthwelI, 1912; Baer, 19X), from lynxes ~ollin~, 1945; Loftin, 1961; Van Zyll de Jong, 1966; Little &Hopkins, 1969) and from domestic cats (Neumann, 1896; Lewis, 1927; Skurski, 1963; Styles & Evans, 1971) though some evidence suggests that development in felids may be limited (Benoit-Bazille & Dramard, 1905; Van ZylI de Jong, 1966). Ackert & Grant (1917) experimentally infected kittens and recovered only a few cestodes; in most of these development had not proceeded beyond the appearance of a genital anlagen in the terminal proglottides, and the most advanced stage reached was sexual maturity. T. pisiformis has been reported on one occasion (Jacob, 1939) from a mustelid (Musteh putorius) though the validity of the record has been questioned (Verster, 1969). Although a common parasite of foxes, the few experimental studies carried out on development in these hosts have provided conflicting results. Dubnitskii (1946) reported a prepatent period of 82-95 days for T. pisiJbrmis in red foxes (Vulpes DEFINITIVE
dog; cat; fox (Vulpes dozes);
ferret;
vu&es) whilst in experiments reported by Matov & Yanchev (1955), T. pisiformis failed to achieve patency in this host. Dubnitskii (1946) recorded poor establishment and growth of the parasite in arctic foxes (Alopex lagopus). Apart from contradictory experimental data and the lack of reliability in certain host records, comparisons of the development of T, pisiformis in different host species are limited by the lack of knowledge of its development in the normal host, the dog. The only observation on establishment of T. pisiformis in the intestine has been made in cats (Ackert & Grant, 1917), and apart from a report (Fotselveva-Sakhno, 1958 cited by Abuladse, 1964) of a prepatent period in the dog of 35-46 days, nothing is known of the establishment, growth and development of the parasite in this host. The present study was undertaken to define various growth parameters in dogs and to compare the development of the cestode in representative members of the families Canidae, Felidae and Mustelidae. MATERIALS
AND METHODS
Cestodes. Cysticerci were derived from an inbred line of T. Disiformis of doa origin. adult cestodes of which had been *“selfed” twice prior ‘to commencement of this experiment. Rabbits, infected with eggs collected from these worms, were killed by cervical dislocation as required but not earlier than 6 weeks after infection. Mature cysticerci were collected into normal saline still within their host tissue capsule and fed to definitive hosts within 1 h of the death of the rabbit. 633
634
IAN BEVERIDGEand MICHAELD. RICKARD
Experimental animals. A total of 26 pups, 28 kittens, 9 fox cubs (Vulpes vulpes) and 3 ferrets (Mustela putorius) were used when 7-8 weeks of age; 14 ferrets approximately 1 year old were also used. Fox cubs were collected from dens when approximately 4 weeks of age and hand reared to preclude infection with taeniid cestodes. All animals were treated with bunamidine hydrochloride (Scolaban, Burroughs Wellcome Co. Ltd.) and piperazine citrate (Antoban, Burroughs Wellcome Co. Ltd.) prior to their use in experiments, to eliminate infections with Dipylidium caninum and round-worms. For 2 weeks prior to and throughout the course of the experiments, all animals were maintained on an identical diet of tinned dog food (Pets Gold Label, Processed Meats Prop. Ltd., Aust.) supplemented with calcium phosphate and biscuits (Puppy Chow, R. Harper & Co. Ltd., Victoria). Infections. Food was withdrawn from animals 12 h before force feeding with 10 cysticerci each; 4 of the kittens received 60 cysticerci each. Ferrets to be killed at 4 and 6 hours after infection (HAI) were individually caged and their faeces collected until the time of death. Two ferrets were fed a meal 30 min prior to infection to determine the effect of feeding on establishment of cestodes. Recovery of cestodes. From 1 day after infection (DAI) onwards, animals were killed, between 9 and 11 a.m. (to eliminate any effects of diurnal cestode movement in the intestine), with a barbiturate overdose. The intestines were rapidly removed, stretched out on the bench, and searched for cestodes. The distance of the point of attachment of each cestode from the pylorus was noted and the frequency of occurrence of cestodes in 10 equal sectors of the small intestine calculated for different times after infection. Following removal from the host, cestodes were relaxed in water, fixed in 10% formalin and wet weight, total length and proglottis number determined. Points on graphs (Figs. l-4) represent mean parameters for the cestodes from 2 or 3 hosts killed at each time after infection. Differences in means were tested statistically using Student’s t-test. Whole worms or terminal proglottides were then stained in Mayer’s acid haemalum for morphological comparisons. In certain instances, eggs removed from gravid proglottides prior to fixation were counted using a Spencer “Bright line” haemocytometer, and tested for their viability and infectivity in vitro, using the method of Rickard & Bell (1971) and by feeding to rabbits. Morphological comparisons. Cestodes from each host were examined for differences in internal morphology. Features examined included the size and morphology of the cirrus sac, its relationship with the longitudinal osmoregulatory canals, number and distribution of testes, position of ovaries and vitellaria and number of uterine branches.
RESULTS Recovery
of cestodes
The overall recovery rate of cestodes from 24 dogs killed between 0.5 HA1 and 42 DA1 was 84x, similar recovery rates being obtained at different killing times through the course of the experiment. High recovery rates were also obtained from fox cubs. In cats, recoveries for the first 10 days of the experiment were almost comparable with those from
I.J.P. VOL.5. 1975
dogs, however, a decline followed and between 28 DA1 and 42 DA1 1 cestode only was recovered from a total of 290 cysticerci fed to 9 kittens (Fig. 1).
In 8 ferrets killed 0.5 to 4 HAI, 92% of cestodes were recovered; none were recovered from 6 ferrets killed 6 HAI. 12 HA1 and 7 DAI.
FIG. 1. Percentage recovery of T. pisi.formis from the small intestine of experimentally infected dogs, foxes and cats during growth. Establishment
A similar pattern of establishment was observed in dogs, foxes and cats. By 0.5 HA1 cysticerci were either unevaginated in the stomach or were evaginated and attached in the small intestine. One HAI, all cestodes were evaginated in the small intestine and were lying apposed to the mucosa, grasping villi with one or two suckers. Loss of the posterior bladder had commenced 1 HA1 and was complete by 6 HAI. At 24 HA1 the scoleces of most cestodes were deeply embedded in the mucosa with only a tag of strobila protruding. In serial histological sections, the rostellum was situated near the base of the villi, adjacent villi having been displaced or grasped by suckers. A few cestodes were found on the mucosal surface. Two ferrets were killed 0.5 HA1 and 15 cestodes were found evaginated in the small intestine but unattached. In 2 of 3 ferrets killed 1 HAI, 18 evaginated, unattached cestodes, 17 of them without posterior bladders, were recovered from the terminal one-sixth of the small intestine. In the third ferret, 9 evaginated, bladderless cestodes were located in the colon. From the 2 ferrets placed in individual cages after infection, and killed 4 HAI, 19 cestodes, without posterior bladders, were found in the faeces and none in their intestines. Three 6-week old ferrets were similarly caged when infected and 6 HA1 all cestodes were recovered in their faeces. In 2 ferrets fed immediately prior to infection and killed 6 HAI, all cestodes were likewise found in the faeces. In no ferret was any sign of cestode attachment to the intestinal mucosa noted.
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Development of Taeniu pisiformis
Migration
635 DOGS
-
During establishment in dogs, cestodes were found in all of the 10 sectors of the small intestine. At subsequent killing times, worms were usually attached in sectors 3 to 8, but no significant change occurred in median worm position during development. In cats, worms occupied a similar position in the small intestine during the period 3-21 DA1 and no migration was detected. Growth
Changes in the mean length, mean wet weight and mean proglottis number of cestodes during growth in dogs, foxes and cats are shown in Figs. 2-4. DOGSFOXES . .........____.. CATS..-.-.-..
FIG. 4. Increases in mean wet weight of T. pisiformis developing
FIG. 2. Mean numbers of proglottides of T. pisiformis in cestodes
developing in the small intestines of experimentally infected dogs, foxes and cats.
in the small intestines of experimentally infected dogs, foxes and cats.
Proglottisation was initiated at about 3 DA1 and there was a steady increase in proglottis number in cestodes from dogs until the onset of apolysis about 35 DAI. Curves for the increase in length and weight of worms during growth in dogs were sigmoidal in form, the rate of increase of both being markedly reduced by the onset of apolysis. Considerable variability was noted between cestodes from an individual host. Not uncommonly, even as early as 14 DAI, a single worm could be found which was much smaller than its 8 or 9 coinhabitant cestodes. At 42 and 75 DAI, cestodes from foxes were much smaller in all three parameters measured than those from dogs. The differences were, in each case highly significant (P < 0.001). Growth in cats between 0 and 21 DA1 was erratic and was slower than in dogs; increase in proglottis number most closely approximated that in dogs, whilst weight increases lagged considerably. Twentyone DAI, cestodes from cats were significantly lighter and shorter than those from dogs (P < 0.001) as well as having significantly fewer proglottides (0.05 < P < 0.02). Development In dogs. Examination
FIG. 3. Increases in mean length of T. pisi’rmis ing in the small intestines of experimentally dogs, foxes and cats.
developinfected
of fresh and stained worms from dogs revealed the following developmental stages: 7 DAI: T-shaped genital anlagen present in centre of terminal proglottides; 14 DAI: genital ducts dully formed; testes present but small; ovaries and vitellaria present; 21 DAI: proglottides mature, testes, ovaries and vitellaria fully developed; filling and primary branching of the uterus under way;
636
IAN BEVERIDGE and MICHAEL D. RICKARD
28 DAI: uterus extensively branched; lateral branches reaching the margin of proglottis medulla; testes and ovaries still visible; no sign of embryophore formation in uterine content; uterine material not infective when fed to each of 2 rabbits; 35 DAI: apolysis evident; 17 of 19 cestodes gravid, uterus filled with eggs numbering 2000-16,000 per proglottis; embryophores fully developed; eggs hatched and activated in vitro, infective when fed to 2 rabbits; 1 worm of 19 was only mature, and another had eggs in the uterus with incompletely formed embryophores; eggs of the latter worm disintegrated when placed in artificial intestinal fluid (AIF); 42 and 75 DAI: all worms gravid, 9000-28,000 eggs per proglottis; eggs hatched and activated in vitro, and were infective to each of 3 rabbits. In foxes. Cestodes recovered from foxes were relatively poorly developed. Seven DAI, a genital anlagen was present in the terminal proglottides, comparable in development to cestodes from dogs collected at the same time, however, 42 DAI, when the cestodes were gravid in dogs, those from foxes showed no evidence of apolysis (no proglottides had been detected in the faeces up to that time) and the worms varied in stage of development from those just mature to others in which uterine filling was at an advanced stage, but there was never any sign of embryophore formation. Between 71 and 75 DAI, one fox passed gravid proglottides in its faeces, and, 75 DAI, large fragments of a worm including the scolex. Eggs from the fragments hatched in vitro and were infective to each of 3 rabbits. When recovered from the two foxes 75 DAI, none of the remaining worms from the intestines were fully gravid and most had branched uteri without indications of embryophore formation, whilst one had eggs with incompletely formed embryophores.
unsegmented. Cestodes recovered 10 DAI had visible testes primordia, whilst those recovered 14 DA1 had only an anlagen present. At 21 DAI, the best developed cestodes were mature and testes, ovaries and vitellaria were fully developed but uterine filling and branching had not occurred. In other cestodes from the same hosts, rudiments of the genital duct system were visible but testes, ovaries and vitellaria were not seen. anlagen or were
Taxonomic characters
A detailed examination of various morphological characters used for taxonomic purposes failed to reveal any consistent differences in cestodes developing in the various host species. Results in Table 1 suggest that the number of testes per proglottis depends on the age of the worm, and that the relatively low number in cestodes from cats 21 DA1 is a function of the state of development of the worm rather than a specific host effect. Again, minor differences in topographical anatomy of the genitalia in cestodes from cats 21 DAI, namely elongate mature proglottides, testes not reaching anterior proglottis margin, ovaries extending to the lateral osmoregulatory canals and vitellaria compact and narrower relative to their height, were attributed to changes occurring during growth of the worms.
In cuts. Development of cestodes in cats was extremely variable. At 7 DAI, a genital anlagen was present in the terminal proglottides of the most advanced cestodes, whilst others contained no TABLE I-COMPARISONS
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DISCUSSION Evagination of cysticerci of T. pisiformis occurred in the small intestine and was followed by rapid attachment to the mucosa and detachment of the posterior bladder; this is similar to observations made by others for Taenia taeniaeformis (Hutchison, 1959) and Taeniu hydatigena (Featherston, 1969, 1971). Initial attachment appeared to be by one or two suckers grasping villi but by 24 HAI, the scoleces of most cestodes were deeply embedded in the mucosa and attached by their suckers and rostellum. The pattern of distribution of T. pisiformis in dogs
OF TESTISNUMBER PER PROGLOTTIS IN
Taenia pisiformis FROM EXPERIMENTALLY
lNFECTEDDOGS,CATSANDFOXES
Host
Dog
Age of cestodes No.
testes
(days)
Cat
42
14
75
21
562 _f 43
313 t 36
526 ? 42
415 + 30
486 - 628
284 - 397
460 - 628
333 - 445
20
10
20
5
per proglottis
mean + s.d. Range testis
Fox
No.
No. proglottides
counted.
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Development of Tueniu pisiformis
during the first 4 HA1 differed from that described for T. hydutigena by Featherston (1969); the latter parasite was found in the anterior sections of the intestine only and not spread throughout the small intestine as was T. pisiformis. These differences may reflect variations in technique rather than differences between the two cestode species. Cooreman & De Rycke (1972) observed that in starved mice, Hymenolepis microstoma establish further posteriorly than in fed animals; if these results apply to taeniids also, the administration of cysticerci to dogs 5h after feeding by Featherston (1969) and 16h after the removal of food in the present experiment, may account in part for the differences in distribution. Furthermore, intestinal motility patterns influence the rate of establishment and hence possibly the position of attachment of cestodes in the gut (Larsh, 1947; Read & Voge, 1954). Because gastrointestinal motility may be influenced by time of feeding this may also help to account for differences recorded between present results and those of Featherston (1969) and for some of the individual variability encountered in the recovery of cestodes from hosts. Migration of T. pisiformis within the intestine during development was not detected, in agreement with the results of Hutchison (1959) with T. taeniaeformis in cats; Featherston (1969) reported significant migrations of T. hydatigena during its development in dogs. Although T. pisiformis established and developed in fox cubs, the slow growth rate and the small numbers of cestodes which had become gravid by 75 DA1 suggests that the fox is a less suitable host than the dog. This is in agreement with the results of Dubnitskii (1946) but differs from those of Matov & Yanchev (1955). It has been noted (unpublished observations) that it is more difficult to infect adult foxes than cubs with T. pisiformis and that the development of any cestodes establishing is like-wise slower. Matov & Yanchev (1955) used experimental animals 8-12 months of age and of unknown previous history and this may account for their different results. T. pisiformis is clearly capable of establishing and developing in kittens although never becoming gravid, as shown previously by Ackert & Grant (1917). However, the largest mature specimens recovered from kittens in the present work were 30 cm in length, considerably larger than the 2.2 cm described by Ackert & Grant (1917). In our experiments cestodes of 2-3 cm contained only a genital anlagen, but Ackert & Grant (1917) gave no details of the treatment of their specimens prior to measurement and may have measured unrelaxed worms. T. pisiformis grows more slowly in cats than in dogs; the differences are least evident in proglottis number suggesting that rate of proglottis production is not rigidly tied to length and weight increases. Possible explanations for the loss of T. pisiformis
637
burdens in cats after 21 DA1 include physiological unsuitability of the cat’s intestine as an environment for the worm, and the development of a heightened immunological response on the part of the abnormal host. A phenomenon of destrobilation during development in unusual hosts has been reported for Hymenolepis diminuta in mice (Turton, 1971; Hopkins, Subramanian & Stallard, 1972a) and for H. microstoma in rats (Goodall, 1972) and loss of cestode burdens following the completion of growth has been reported for Raillietina cesticillus in its normal host the fowl (Gray, 1972). Hopkins, Subramanian & Stallard (19726) have shown that immunosuppressants prevent the elimination of H. nana in mice and that destrobilate specimens transplanted to rats or unexposed mice continue to develop, suggesting immunological involvement. However, Goodall (1972) failed to prevent elimination of H. microstoma in rats with immunosuppressants and postulated that the phenomenon was due to the physiological unsuitability of the rat as a host. T. pisiformis failed to establish in the intestine of ferrets and this was not affected by feeding ferrets immediately prior to infection or by the age of the hosts. It might be suggested that the rate of passage of cysticerci through the intestines of ferrets was too rapid to permit attachment, since some had reached the colon 1 HAI; however they were present in the small intestine for at least 30 min and this was sufficient time in cats and dogs to allow attachment. Smyth & Smyth (1968) have suggested that host intestinal topography may be an important factor in the establishment of Echinococcus g. granulosus, those host species having smaller crypts of Lieberkuhn being less suitable for its attachment and growth. However, the pattern of establishment of T. pisiformis is different to that of E. granulosus and apparently requires only grasping of villi by the suckers. It seems unlikely, therefore, that mucosal topography should affect the initial attachment of worms. Alternatively the intestinal lumen of the ferret may be physiologically unsuitable to initiate the stimuli leading to attachment. Evagination is a relatively non-specific phenomenon as it can occur spontaneously, in response to bile salts and to detergent like substances (DeWaele, 1933; Campbell, 1963; DeRycke & Grembergen, 1966) but the stimuli which initiate attachment are quite unknown and may be more specific. Apart from the degree of development and worm size, morphological features of taxonomic importance were not affected by development in different hosts. Changes in testis number occur with proglottis age and due care should be exercised in attributing great weight to differences in testis number between taxa. Although Christiansen (1931) described differences in the morphology of Tuenia krabbei recovered from experimentally infected dogs and foxes, comparison with the present results
638
IAN BEVERIDGE and MICHAEL D. RICXARD
suggests that the differences he described are attributable mainly to the state of development of specimens from the two host species and not to specific “host-induced” effects on internal morphology. Although only four host species were examined the results suggest an approximate negative correlation between the “success” of T. pisiformis in a given host and the phylogenetic distance between that host and the dog, a result not unexpected on evolutionary grounds in the case of a moderately specialized parasite infecting members of related but diverging host groups. Data on development in other host species are not available apart from the dingo (Curtis familiaris dingo) in which development is comparable to that in the dog (unpublished observations). This is not unexpected because of the close (subspecific) relationship of dingoes with dogs. Acknowledgement-This from the Australian wish to thank Mr. collecting fox cubs.
work was supported by a grant Meat Research Committee. We B. Coman for his involvement in
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