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Experimental studies on morphological variation in the cestode genus Hymenolepis. IV. Influence of the Host on Variation in H. nana
EXPERIMENTAL PARASITOLOGY 8, 581--590 (1959)
Experimental Studies on Morphological Variation in the Cestode Genus Hymenolepis. IV. Influence of the Host on Variation in H. nana 1 E v e r e t t L. S c h i l l e r Department of Pathobiology, School of Hygiene and Public Health, The Johns Hopkins University, Baltimore, Maryland ( S u b m i t t e d for publication, 10 N o v e m b e r 1958)
For some time parasitologists have recognized that worms presumably of the same species from different host-species may be very dissimilar, but no satisfactory means of evaluating the extent to which the host may influence intraspecific variation in parasitic flatworms has been developed. It has been shown in the foregoing studies dealing with growth and development of the adult cestode (Read, Schiller, and Phifer, 1958; Schiller, 1959b) that the definitive host and its diet plays an important role in determining the size (length, width, and thickness) attained by H y m e n o l e p i s n a n a (von Siebold, 1852). Further, it has been shown (Schiller, 1959b, c) that the frequency of occurrence of certain variant characteristics in H . n a n a is essentially constant within the environment furnished by a single host species, the mouse. No experimental studies of variation in cestodes of the same species from hosts of different species have been reported. It therefore seemed pertinent to undertake an investigation of the degree of variation occurring under the various environmental conditions afforded by rearing this worm in a variety of host species. EXPERIMENTAL ANIMALS
The specimens of H . n a n a utilized in this study were obtained by exposing a large series of mammalian species to direct and indirect infec1 This i n v e s t i g a t i o n was s u p p o r t e d in p a r t b y a research g r a n t E-1508, from t h e N a t i o n a l I n s t i t u t e s of H e a l t h , U. S. Public H e a l t h Service a n d was carried out d u r i n g t h e t e n u r e of a U. S. Public H e a l t h Service Research Fellowship.
581
582
SCHILLER
tions with nonirradiated material. A list of the experimental hosts and the results with respect to infectivity of H . nana for these species are presented in Table I. The technical names for the North American mammals are given in accordance with Miller and Kellogg (1955). The sources of a number of these species have been indicated in foregoing reports (Schiller, 1959a, b, c); other animals whose names appear on this list were obtained through the courtesy of various persons too numerous to be named individually here. Grateful acknowledgement is made to these people for their valuable contributions to this investigation. PROCEDURE
All animals were kept in the laboratory for a period of at least 2 weeks prior to being exposed to the infectious organisms. Unless otherwise indicated in Table I, approximately 200 gravid proglottids were administered in direct infections and 50 cysticercoids constituted the dose in the case of indirect infections. The interval between the time of infection and the time of autopsy was 15 days. After preparation as stained, whole-mount specimens, worms resulting from these infections were grouped according to the host-species from which they came and analyzed by determining the frequency with which certain of the six previously studied characteristics occurred (Schiller, 1959c). The two variants selected as subjects for analysis were "reduction in testes numbers" and "sterility," the former being considered a specific effect and the latter a relatively nonspecifie one. RESULTS
The frequency data resulting from these determinations are presented according to host-species in Table II. The percentage frequency of occurrence calculated in each case is shown graphically in Figs. 1 and 2. Data from the preceding irradiation experiments (Schiller, 1959c) with respect to the frequency of occurrence of these characteristics at the first three r-dose levels have been included in these graphs for comparative purposes. According to these data, the proportionate number of proglottids having only two testes appears to be about the same in the worms from albino hamsters, marmots (Marmota), kangaroo rats (Dipodomys), and rice mice (Oryzomys) as it is in worms from the albino mice. However, this number is markedly increased when these cestodes developed in the three species of squirrels (Sciurus, Tamiasciurus, and Glaucomys). It is of interest to note that the effect induced by these
MORPHOLOGICAL VARIATION IN HYMENOLEPIS. IV TABLE
583
I
List of Animals Used as Experimental Hosts N u m b e r of a n i m a l s exposed Direct Indirect
Experimental host ~
N u m b e r of a n i m a l s infected Direct Indirect
MARSUPIALIA
Didelphis
marsupialis virginiana
3
3
0
0
14 6
0 0
0 0
---
8 15
0 15
0 0
-0
4
4
0
0
sabaeus
1
1
0
0
(Rein-
0
1
1 0
Kerr CHIROPTERA
Myotis lucifugus (Le C o n t e ) Eptesicus fuscus ( P a l i s o t de B e a u vois)
Corynorhinus macrotis (Le C o n t e ) Pipistrellus subfiavus (F. C u v i e r ) PRIMATES
Ateles geoffroyi panamensis K e l l o g g and Goldman
Cercopithecus
aethiops
(Linnaeus)
Saimiri
5rstedii
5rstedii
hardt) Rhesus sp.
Homo sapiens sapiens ( L i n n a e u s )
--
0
1 2b
0 0
0 0
2
2
0
0
LAGOMORPHA
Sylvilagus
floridanus
mallurus
(Thomas) Domestic rabbit RODENTIA Marmota monax ( L i n n a e u s ) ~ Citellus tridecemlineatus (Mitchill) Citellus franklinii ( S a b i n e ) Tamias striatus ( L i n n a e u s ) c
6
3
0
0
3 6 1 5
2 6 1 5
3 0 0 0
2 0 0 1
Sciurus carolinensis pennsylvanicus
7
9
3
4
(Erxle-
0
2
--
2
Glaucomys volans querceti ( B a n g s ) ° Perognathus longimembris longimembris ( C o u e s ) c Acomys cahirinus (Geoffrey) Dipodomys merriami merriami
2
2
2
2
2 3
2 3
0 0
1 0
6
4
1
3
25 25 4 1
25 25 4 1
13 19 2 0
17 21 3 0
Ord c
Tamiasciurus hudsonicus ben)
Mearns c
Mesocricetus auratus W a t e r h o u s e M. auratus ( a l b i n o v a r i e t y ) Oryzomys palustris ( H a r l a n ) ~ Peromyscus crinitus ( M e r r i a m )
584
SCHILLER TABLE I. (Continued) Experimental host a
P. leucopus (Rafinesque) Sigmodon hispidus Say and Ord L e m m u s sibiricus trimucronatus
Number of animals exposed Direct Indirect
Number of animals exposed Direct Indirect
27 3
16 3
0 0
0 0
4
2
0
0
dawsoni
0
2
--
0
Microtus pennsylvanicus (Ord) Rattus norvegicus (Berkenhout) al-
5 22
4 25
0 6
0 3
0 0 25
5 6 25
0 0 16
0 0 19
10
10
4
5
1 8
1 8
0 0
0 0
2 3 1 2
2 3 1 2
0 0 0 0
0 0 0 0
Merriam Clethrionomys
rutilus
(Merriam)
bino variety R. rattus (Linnaeus) hooded variety Arvicanthus nilotieus (Geoffrey)
Domestic mouse (albino variety: Princeton) Domestic mouse (C3H brown variety) Erethizon dorsatum (Linnaeus) Domestic guinea pig CARNIVORA Domestic dog Domestic cat Procyon lotor (Linnaeus) Mustela ?nigripes (Audobon and Bachman)
a The sequenceof ordersis that adoptedby Simpsonin "ThePrinciplesof Classificationand a Classificationof Mammals"(Bull. Am. Museum Natl. Hist. 85, Oct. 5, 1945). b Fivecysticercoidsingested;resultsbasedon fecalexamination. c The experimentalinfectionsin these animalsconstitutenew host recordsfor H. nana. three hosts is of a b o u t the same m a g n i t u d e as t h a t produced b y 5 + k r of X - i r r a d i a t i o n . W h e r e sterility is concerned, all of these hosts, w i t h t h e exception of the rice mice, a p p e a r to elicit some increase in t h e freq u e n c y as compared w i t h t h a t observed in albino mice. A g a i n the increase is p a r t i c u l a r l y e v i d e n t in worms from the squirrels. T h e results of b o t h analyses have indicated t h a t certain host-species do have a p r o n o u n c e d effect on the f r e q u e n c y w i t h which v a r i a n t characteristics are expressed b y this worm a n d it appears t h a t the e x t e n t of this effect varies with the different hosts. I n the examples studied, the species e v o k i n g the greater increases in v a r i a t i o n are those iLL which n a t u r a l infections with H . n a n a n e v e r have been recorded. E x p e r i m e n t a l
MORPHOLOGICAL VARIATION IN HYMENOLEPIS. IV
585
TABLE II Frequency of Occurrence of Variant Characteristics in H. nana According to Host-Species in which Cestodes Developed Following Direct and Indirect Experimental Infections Variant characteristic Reduction in testes numbers
Sterility NE n-
Host-species
Number Per cent bei of Per cent Number of Number of with with ste igl.e of progproglottids proglottids two two pr, lottids examined examined testes testes lo sterile ti. ¢D
Albino mouse Albino hamster Marmota monax Seiurus carolinensis Tamiasciurus hudsonicus Glaucomys volans Dipodomys merriami Oryzomys palustris
5 7 6 6
121 216 112 305
113 221 182 334
2.8 3.1 2.7 5.0
2.2 2.9 2.8 5.3
8,129 5,773 4,223 6,282
4
--
185
--
4.6
7,264
2
104
98 4.9 4.7
3,537 36 35
1.00
24
40 2.4 2.3
2,068
0.77
3,610 12
0.28
1
3
120 109 2.8 2.8
21 25 3(] 32 88 95
0.31 0.55 0.52 1.50
60
0.83
2~ 22
--
infections of u n u s u a l host species p e r m i t little o p p o r t u n i t y for t h e p a r a site to a d a p t itself g r a d u a l l y to new conditions. I t seems p r o b a b l e t h a t the host-effect m a y be associated w i t h a n a b r u p t change in the e n v i r o n m e n t of this cestode. O b s e r v a t i o n s in the p r e s e n t s t u d y indicate t h a t H . nana exhibits fairly strict h a b i t a t specificity w i t h i n the host. W h e n this species occurs in the u s u a l m u r i n e r o d e n t hosts, the w o r m s are characteristically f o u n d a t the posterior end of the small intestine, v e r y n e a r the ileocecal j u n c tion. I n M a r m o t a monax these cestodes are more generally d i s t r i b u t e d
586
SCHILLER
'i w z
bJ Iz gE
BB
DIRECT INFECTION
[]
INDIRECT INFECTION
O
(.3 Z hl 0 bJ UFZ bJ (.> n~ Ld
1:1.
IN
ALBINO MOUSE (IRRADIATED)
--
--
DEFINITIVE
HOST (NON-IRRADIATED)
FIG. 1. Frequency of occurrence of proglottids with only two testes in H . n a n a according to host species and mode of infection.
throughout the posterior one third of the small intestine. 2 In Sciurus carolinensis the worms are found attached to the mucosa in a very limited area at about the mid-region of this organ. 3 In Glaucomys volans these cestodes are distributed throughout the small intestine, but the heaviest concentrations usually occur midway in its length. In this host, both the size of the worms and their numbers decrease in rough proportion to the distance from the middle toward either end. These observations suggest that H. nana tends to localize in the intestinal tract at a place which best satisfies its physiological requirements and that such conditions are met at different sites in different species of mammalian hosts. Biochemical studies of this habitat in the different host-species m a y reveal the nature of the physico-chemical factors responsible for the observed host-effect on the degree of variation in this worm. 2 The average length of the small intestine, as measured in six j uvenile animals, was 2,020 ram. The worms were always found in the region of the last 780 ram. 3 The average length of the small intestine, as measured in 12 adult animals was 220 mm.
MORPHOLOGICAL VARIATION IN HYMENOLEPIS. IV
587
DIRECT INFECTION hi
V/I
z
[ ]
vA
w
I N D I R E C T INFECTION
MA
0:: 2
v .~
(,.,) O LL O >O
Z
tJ,J ::) hi
o.
IN ALBINO MOUSE {=NNADIATEO ),...
~oo DEFINITIVE
':0 •
HOST
I!l! I l
(NON-IRRADIATED)
FtG. 2. F r e q u e n c y of occurrence of sterile proglottids in the gravid region of according to host species a n d mode of infection.
H. nana
DISCUSSION
The tapeworms usually exhibit a high order of host specificity. Although these worms occur in all vertebrates, they reach their highest specialization in birds. Some parasitologists interpret this specialization to mean that these organisms have evolved along with their hosts. Cameron (1956) is of the opinion that the parasite can diverge only within its host and that host specificity is a physiological attribute, the parasites having become too specialized in their requirements to be able to adapt themselves to any but closely related hosts. The greatest part of the available data regarding host specificity has been derived from statistical reports of the number of different host species in which the parasite has been found. The statistical data are based entirely on taxonomic work and in many cases specific identifications are questionable because of individual variability in some of the characters upon which the species concept has been established. Consequently, physiological specificity has often been inferred when no apparent morphologi-
588
SCHILLER
cal specificity could be found. While it is evident that related hosts tend to have related parasites, there are numerous exceptions, particularly among mammals with similar habits. Chandler (1955) emphasizes the fact that two conditions must be met in order for a parasite to live habitually in a host. These are: 1) a dependable means of transfer from individual to individual, and 2) ability to thrive when it gets there. Although host specificity may be primarily a problem of physiology, the first of these conditions will determine the species of host which will be exposed to the parasite. Therefore, the ecological relationships in the external environment probably are of considerable importance in defining host specificity. That such is the case has been confirmed on a number of occasions by experimental investigations in which laboratory animals that would not normally occur in the same ecological surroundings as the usual host have been successfully infected. The present investigation has provided another example of this kind. Infections with H. nana were successfully established in eight species of mammals which, heretofore, were not known to serve as definitive hosts for this tapeworm. Moreover, judging by the greater size attained by the worms in some of these new hosts (particularly in the marmot and three species of squirrels) the physiological conditions for growth and egg production appear to be considerably better in these animals than they are in the murine rodent species which habitually harbor this tapeworm. In this case infection of the new hosts seems to depend only upon an opportunity for ingestion of the infectious stages, since there appears to be no question of the worms' ability to thrive when a suitable means of transfer is provided. Of the 42 different kinds of mammals exposed in this study, infections were successfully established in 13 (Table I). Of the twelve in which the exposures were direct as well as indirect, only one species (Tamias striatus) failed to become infected by both routes. While it is apparent that ecological segregation of most of the species used as laboratory animals in this investigation would probably preclude an opportunity for the acquisition of the infectious stages of H. nana under natural conditions, this situation may not apply in all cases. It is known that, in some localities (e. g. Baltimore) squirrels (Sciurus carloinensis) and Norway rats are sympatric. Since the rats are commonly infected with H. nana, it is reasonable to assume that infectious eggs are available to the squirrels in these habitats and could be transferred to them through direct contamination. Yet, H. nana apparently does not occur in these animals. The reason why this infection is not
MORPHOLOGICAL VARIATION IN HYMENOLEPIS. IV
589
readily acquired under conditions which appear to be ideally suited for transfer has not been clarified, but it is suspected that differences in feeding behavior may be involved. Behavioral insusceptibility may be an important factor in determining host-specificity. Most animals tend to extend their range by gradual adaptation to slightly different conditions. But, even in naturally transferred infections, internal parasites are less apt to find as wide a range of intergrading conditions in their environment as are free-living animals. Therefore, any extension of their host range may represent a very sudden change. Whether the ability of H. nana to establish itself in these new hosts under experimental conditions is due to the selection of the fittest of random genetic types or merely to somatic adjustment has not been settled; however, the studies reported herein have shown that development in an unusual host has not been without a marked effect on the structure of this tapeworm. If selection of certain genetic types is involved, exploitation of new host species, when the opportunity arises, may be one mechanism whereby divergent forms are isolated. Since the physiological effects of isolation are often reflected in morphological changes that occur in the parasite, such a mechanism could account for the gradual appearance of new forms which, while in transition, serve to confuse the taxonomist, but subsequently may become sufficiently distinct to be described as new varieties, new subspecies, new species, etc. SUMMARY
Analyses of specimens of Hymenolepis nana from nonirradiated experimental infections in a large series of different mammals furnished evidence that certain host-species have a marked effect on the frequency with which a variant character is expressed in this cestode and that the extent of this effect varies with different hosts. The mammalian hosts which induced the higher increases in the frequency of variation were those in which infections with H. nana have not been recorded heretofore. These include: Marmota monax (Linnaeus), Tamias striatus (Linnaeus), Sciurus carolinensis pennsylvanicus 0rd*, Tamiasciurus hudsonicus (Erxleben)*, Glaucomys volans querceti (Bangs)*, Perognathus longimembris longimembris (Coues), Dipodomys merriami merriami Mearns, and Oryzomys palustris (Harlan). The most significant effects, with respect to increasing the frequency of variation in H. nana were found in specimens which had been reared in the three species of sciurids indicated by an asterisk in the preceding list.
590
SCHILLER I~EFERENCES
CAMERON, T. W. M. 1956. Parasites and Parasitism. J o h n Wiley and Sons, Inc. New York, 322 pp. CHANDLER, A. C. 1955. I n t r o d u c t i o n to Parasitology. J o h n Wiley and Sons, Inc. New York, 9th ed. 799 pp. MILLER, G. S., JR., AND KELLOG(~, R. 1955. List of N o r t h American recent mammals. U. S. Natl. Museum Bull. 205,954 pp. READ, C. P., SCHILLER, E. L., AND PreFER, K. 1958. The role of c a r b o h y d r a t e s in the biology of Cestodes. V. C o m p a r a t i v e studies on the effects of host d i e t a r y c a r b o h y d r a t e s on Hymenolepis spp. Exptl. Parasitol. 7, 198-216. SCHILLER, E. L. 1959a. E x p e r i m e n t a l studies on morphological v a r i a t i o n in the eestode genus Hymenolepis. I. Morphology and development of the cystL cercoid of H. nana in Tribolium confusum. Exptl. Parasitol. 8, 91 118. SCHIbLER, E. L. 1959b. E x p e r i m e n t a l studies on morphological v a r i a t i o n in the cestode genus Hymenolepis. II. Growth, d e v e l o p m e n t and reproduction of the strobilate phase of H. nana in different m a m m a l i a n host species. Exptl. Parasitol. 8, 215-235. SCHILLER, E. L. 1959c. E x p e r i m e n t a l studies on morphological v a r i a t i o n in the cestode genus Hymenolepis. III. I n v e s t i g a t i o n s on the use of X - i r r a d i a t i o n as a mechanism for facilitating analyses of the nature, extent and directional t r e n d s of morphological w~riations in H. nana. Exptl. Parasitol. 8, 427-470.
Experimental Studies on Morphological Variation in the Cestode Genus Hymenolepis. IV. Influence of the Host on Variation in H. nana 1 E v e r e t t L. S c h i l l e r Department of Pathobiology, School of Hygiene and Public Health, The Johns Hopkins University, Baltimore, Maryland ( S u b m i t t e d for publication, 10 N o v e m b e r 1958)
For some time parasitologists have recognized that worms presumably of the same species from different host-species may be very dissimilar, but no satisfactory means of evaluating the extent to which the host may influence intraspecific variation in parasitic flatworms has been developed. It has been shown in the foregoing studies dealing with growth and development of the adult cestode (Read, Schiller, and Phifer, 1958; Schiller, 1959b) that the definitive host and its diet plays an important role in determining the size (length, width, and thickness) attained by H y m e n o l e p i s n a n a (von Siebold, 1852). Further, it has been shown (Schiller, 1959b, c) that the frequency of occurrence of certain variant characteristics in H . n a n a is essentially constant within the environment furnished by a single host species, the mouse. No experimental studies of variation in cestodes of the same species from hosts of different species have been reported. It therefore seemed pertinent to undertake an investigation of the degree of variation occurring under the various environmental conditions afforded by rearing this worm in a variety of host species. EXPERIMENTAL ANIMALS
The specimens of H . n a n a utilized in this study were obtained by exposing a large series of mammalian species to direct and indirect infec1 This i n v e s t i g a t i o n was s u p p o r t e d in p a r t b y a research g r a n t E-1508, from t h e N a t i o n a l I n s t i t u t e s of H e a l t h , U. S. Public H e a l t h Service a n d was carried out d u r i n g t h e t e n u r e of a U. S. Public H e a l t h Service Research Fellowship.
581
582
SCHILLER
tions with nonirradiated material. A list of the experimental hosts and the results with respect to infectivity of H . nana for these species are presented in Table I. The technical names for the North American mammals are given in accordance with Miller and Kellogg (1955). The sources of a number of these species have been indicated in foregoing reports (Schiller, 1959a, b, c); other animals whose names appear on this list were obtained through the courtesy of various persons too numerous to be named individually here. Grateful acknowledgement is made to these people for their valuable contributions to this investigation. PROCEDURE
All animals were kept in the laboratory for a period of at least 2 weeks prior to being exposed to the infectious organisms. Unless otherwise indicated in Table I, approximately 200 gravid proglottids were administered in direct infections and 50 cysticercoids constituted the dose in the case of indirect infections. The interval between the time of infection and the time of autopsy was 15 days. After preparation as stained, whole-mount specimens, worms resulting from these infections were grouped according to the host-species from which they came and analyzed by determining the frequency with which certain of the six previously studied characteristics occurred (Schiller, 1959c). The two variants selected as subjects for analysis were "reduction in testes numbers" and "sterility," the former being considered a specific effect and the latter a relatively nonspecifie one. RESULTS
The frequency data resulting from these determinations are presented according to host-species in Table II. The percentage frequency of occurrence calculated in each case is shown graphically in Figs. 1 and 2. Data from the preceding irradiation experiments (Schiller, 1959c) with respect to the frequency of occurrence of these characteristics at the first three r-dose levels have been included in these graphs for comparative purposes. According to these data, the proportionate number of proglottids having only two testes appears to be about the same in the worms from albino hamsters, marmots (Marmota), kangaroo rats (Dipodomys), and rice mice (Oryzomys) as it is in worms from the albino mice. However, this number is markedly increased when these cestodes developed in the three species of squirrels (Sciurus, Tamiasciurus, and Glaucomys). It is of interest to note that the effect induced by these
MORPHOLOGICAL VARIATION IN HYMENOLEPIS. IV TABLE
583
I
List of Animals Used as Experimental Hosts N u m b e r of a n i m a l s exposed Direct Indirect
Experimental host ~
N u m b e r of a n i m a l s infected Direct Indirect
MARSUPIALIA
Didelphis
marsupialis virginiana
3
3
0
0
14 6
0 0
0 0
---
8 15
0 15
0 0
-0
4
4
0
0
sabaeus
1
1
0
0
(Rein-
0
1
1 0
Kerr CHIROPTERA
Myotis lucifugus (Le C o n t e ) Eptesicus fuscus ( P a l i s o t de B e a u vois)
Corynorhinus macrotis (Le C o n t e ) Pipistrellus subfiavus (F. C u v i e r ) PRIMATES
Ateles geoffroyi panamensis K e l l o g g and Goldman
Cercopithecus
aethiops
(Linnaeus)
Saimiri
5rstedii
5rstedii
hardt) Rhesus sp.
Homo sapiens sapiens ( L i n n a e u s )
--
0
1 2b
0 0
0 0
2
2
0
0
LAGOMORPHA
Sylvilagus
floridanus
mallurus
(Thomas) Domestic rabbit RODENTIA Marmota monax ( L i n n a e u s ) ~ Citellus tridecemlineatus (Mitchill) Citellus franklinii ( S a b i n e ) Tamias striatus ( L i n n a e u s ) c
6
3
0
0
3 6 1 5
2 6 1 5
3 0 0 0
2 0 0 1
Sciurus carolinensis pennsylvanicus
7
9
3
4
(Erxle-
0
2
--
2
Glaucomys volans querceti ( B a n g s ) ° Perognathus longimembris longimembris ( C o u e s ) c Acomys cahirinus (Geoffrey) Dipodomys merriami merriami
2
2
2
2
2 3
2 3
0 0
1 0
6
4
1
3
25 25 4 1
25 25 4 1
13 19 2 0
17 21 3 0
Ord c
Tamiasciurus hudsonicus ben)
Mearns c
Mesocricetus auratus W a t e r h o u s e M. auratus ( a l b i n o v a r i e t y ) Oryzomys palustris ( H a r l a n ) ~ Peromyscus crinitus ( M e r r i a m )
584
SCHILLER TABLE I. (Continued) Experimental host a
P. leucopus (Rafinesque) Sigmodon hispidus Say and Ord L e m m u s sibiricus trimucronatus
Number of animals exposed Direct Indirect
Number of animals exposed Direct Indirect
27 3
16 3
0 0
0 0
4
2
0
0
dawsoni
0
2
--
0
Microtus pennsylvanicus (Ord) Rattus norvegicus (Berkenhout) al-
5 22
4 25
0 6
0 3
0 0 25
5 6 25
0 0 16
0 0 19
10
10
4
5
1 8
1 8
0 0
0 0
2 3 1 2
2 3 1 2
0 0 0 0
0 0 0 0
Merriam Clethrionomys
rutilus
(Merriam)
bino variety R. rattus (Linnaeus) hooded variety Arvicanthus nilotieus (Geoffrey)
Domestic mouse (albino variety: Princeton) Domestic mouse (C3H brown variety) Erethizon dorsatum (Linnaeus) Domestic guinea pig CARNIVORA Domestic dog Domestic cat Procyon lotor (Linnaeus) Mustela ?nigripes (Audobon and Bachman)
a The sequenceof ordersis that adoptedby Simpsonin "ThePrinciplesof Classificationand a Classificationof Mammals"(Bull. Am. Museum Natl. Hist. 85, Oct. 5, 1945). b Fivecysticercoidsingested;resultsbasedon fecalexamination. c The experimentalinfectionsin these animalsconstitutenew host recordsfor H. nana. three hosts is of a b o u t the same m a g n i t u d e as t h a t produced b y 5 + k r of X - i r r a d i a t i o n . W h e r e sterility is concerned, all of these hosts, w i t h t h e exception of the rice mice, a p p e a r to elicit some increase in t h e freq u e n c y as compared w i t h t h a t observed in albino mice. A g a i n the increase is p a r t i c u l a r l y e v i d e n t in worms from the squirrels. T h e results of b o t h analyses have indicated t h a t certain host-species do have a p r o n o u n c e d effect on the f r e q u e n c y w i t h which v a r i a n t characteristics are expressed b y this worm a n d it appears t h a t the e x t e n t of this effect varies with the different hosts. I n the examples studied, the species e v o k i n g the greater increases in v a r i a t i o n are those iLL which n a t u r a l infections with H . n a n a n e v e r have been recorded. E x p e r i m e n t a l
MORPHOLOGICAL VARIATION IN HYMENOLEPIS. IV
585
TABLE II Frequency of Occurrence of Variant Characteristics in H. nana According to Host-Species in which Cestodes Developed Following Direct and Indirect Experimental Infections Variant characteristic Reduction in testes numbers
Sterility NE n-
Host-species
Number Per cent bei of Per cent Number of Number of with with ste igl.e of progproglottids proglottids two two pr, lottids examined examined testes testes lo sterile ti. ¢D
Albino mouse Albino hamster Marmota monax Seiurus carolinensis Tamiasciurus hudsonicus Glaucomys volans Dipodomys merriami Oryzomys palustris
5 7 6 6
121 216 112 305
113 221 182 334
2.8 3.1 2.7 5.0
2.2 2.9 2.8 5.3
8,129 5,773 4,223 6,282
4
--
185
--
4.6
7,264
2
104
98 4.9 4.7
3,537 36 35
1.00
24
40 2.4 2.3
2,068
0.77
3,610 12
0.28
1
3
120 109 2.8 2.8
21 25 3(] 32 88 95
0.31 0.55 0.52 1.50
60
0.83
2~ 22
--
infections of u n u s u a l host species p e r m i t little o p p o r t u n i t y for t h e p a r a site to a d a p t itself g r a d u a l l y to new conditions. I t seems p r o b a b l e t h a t the host-effect m a y be associated w i t h a n a b r u p t change in the e n v i r o n m e n t of this cestode. O b s e r v a t i o n s in the p r e s e n t s t u d y indicate t h a t H . nana exhibits fairly strict h a b i t a t specificity w i t h i n the host. W h e n this species occurs in the u s u a l m u r i n e r o d e n t hosts, the w o r m s are characteristically f o u n d a t the posterior end of the small intestine, v e r y n e a r the ileocecal j u n c tion. I n M a r m o t a monax these cestodes are more generally d i s t r i b u t e d
586
SCHILLER
'i w z
bJ Iz gE
BB
DIRECT INFECTION
[]
INDIRECT INFECTION
O
(.3 Z hl 0 bJ UFZ bJ (.> n~ Ld
1:1.
IN
ALBINO MOUSE (IRRADIATED)
--
--
DEFINITIVE
HOST (NON-IRRADIATED)
FIG. 1. Frequency of occurrence of proglottids with only two testes in H . n a n a according to host species and mode of infection.
throughout the posterior one third of the small intestine. 2 In Sciurus carolinensis the worms are found attached to the mucosa in a very limited area at about the mid-region of this organ. 3 In Glaucomys volans these cestodes are distributed throughout the small intestine, but the heaviest concentrations usually occur midway in its length. In this host, both the size of the worms and their numbers decrease in rough proportion to the distance from the middle toward either end. These observations suggest that H. nana tends to localize in the intestinal tract at a place which best satisfies its physiological requirements and that such conditions are met at different sites in different species of mammalian hosts. Biochemical studies of this habitat in the different host-species m a y reveal the nature of the physico-chemical factors responsible for the observed host-effect on the degree of variation in this worm. 2 The average length of the small intestine, as measured in six j uvenile animals, was 2,020 ram. The worms were always found in the region of the last 780 ram. 3 The average length of the small intestine, as measured in 12 adult animals was 220 mm.
MORPHOLOGICAL VARIATION IN HYMENOLEPIS. IV
587
DIRECT INFECTION hi
V/I
z
[ ]
vA
w
I N D I R E C T INFECTION
MA
0:: 2
v .~
(,.,) O LL O >O
Z
tJ,J ::) hi
o.
IN ALBINO MOUSE {=NNADIATEO ),...
~oo DEFINITIVE
':0 •
HOST
I!l! I l
(NON-IRRADIATED)
FtG. 2. F r e q u e n c y of occurrence of sterile proglottids in the gravid region of according to host species a n d mode of infection.
H. nana
DISCUSSION
The tapeworms usually exhibit a high order of host specificity. Although these worms occur in all vertebrates, they reach their highest specialization in birds. Some parasitologists interpret this specialization to mean that these organisms have evolved along with their hosts. Cameron (1956) is of the opinion that the parasite can diverge only within its host and that host specificity is a physiological attribute, the parasites having become too specialized in their requirements to be able to adapt themselves to any but closely related hosts. The greatest part of the available data regarding host specificity has been derived from statistical reports of the number of different host species in which the parasite has been found. The statistical data are based entirely on taxonomic work and in many cases specific identifications are questionable because of individual variability in some of the characters upon which the species concept has been established. Consequently, physiological specificity has often been inferred when no apparent morphologi-
588
SCHILLER
cal specificity could be found. While it is evident that related hosts tend to have related parasites, there are numerous exceptions, particularly among mammals with similar habits. Chandler (1955) emphasizes the fact that two conditions must be met in order for a parasite to live habitually in a host. These are: 1) a dependable means of transfer from individual to individual, and 2) ability to thrive when it gets there. Although host specificity may be primarily a problem of physiology, the first of these conditions will determine the species of host which will be exposed to the parasite. Therefore, the ecological relationships in the external environment probably are of considerable importance in defining host specificity. That such is the case has been confirmed on a number of occasions by experimental investigations in which laboratory animals that would not normally occur in the same ecological surroundings as the usual host have been successfully infected. The present investigation has provided another example of this kind. Infections with H. nana were successfully established in eight species of mammals which, heretofore, were not known to serve as definitive hosts for this tapeworm. Moreover, judging by the greater size attained by the worms in some of these new hosts (particularly in the marmot and three species of squirrels) the physiological conditions for growth and egg production appear to be considerably better in these animals than they are in the murine rodent species which habitually harbor this tapeworm. In this case infection of the new hosts seems to depend only upon an opportunity for ingestion of the infectious stages, since there appears to be no question of the worms' ability to thrive when a suitable means of transfer is provided. Of the 42 different kinds of mammals exposed in this study, infections were successfully established in 13 (Table I). Of the twelve in which the exposures were direct as well as indirect, only one species (Tamias striatus) failed to become infected by both routes. While it is apparent that ecological segregation of most of the species used as laboratory animals in this investigation would probably preclude an opportunity for the acquisition of the infectious stages of H. nana under natural conditions, this situation may not apply in all cases. It is known that, in some localities (e. g. Baltimore) squirrels (Sciurus carloinensis) and Norway rats are sympatric. Since the rats are commonly infected with H. nana, it is reasonable to assume that infectious eggs are available to the squirrels in these habitats and could be transferred to them through direct contamination. Yet, H. nana apparently does not occur in these animals. The reason why this infection is not
MORPHOLOGICAL VARIATION IN HYMENOLEPIS. IV
589
readily acquired under conditions which appear to be ideally suited for transfer has not been clarified, but it is suspected that differences in feeding behavior may be involved. Behavioral insusceptibility may be an important factor in determining host-specificity. Most animals tend to extend their range by gradual adaptation to slightly different conditions. But, even in naturally transferred infections, internal parasites are less apt to find as wide a range of intergrading conditions in their environment as are free-living animals. Therefore, any extension of their host range may represent a very sudden change. Whether the ability of H. nana to establish itself in these new hosts under experimental conditions is due to the selection of the fittest of random genetic types or merely to somatic adjustment has not been settled; however, the studies reported herein have shown that development in an unusual host has not been without a marked effect on the structure of this tapeworm. If selection of certain genetic types is involved, exploitation of new host species, when the opportunity arises, may be one mechanism whereby divergent forms are isolated. Since the physiological effects of isolation are often reflected in morphological changes that occur in the parasite, such a mechanism could account for the gradual appearance of new forms which, while in transition, serve to confuse the taxonomist, but subsequently may become sufficiently distinct to be described as new varieties, new subspecies, new species, etc. SUMMARY
Analyses of specimens of Hymenolepis nana from nonirradiated experimental infections in a large series of different mammals furnished evidence that certain host-species have a marked effect on the frequency with which a variant character is expressed in this cestode and that the extent of this effect varies with different hosts. The mammalian hosts which induced the higher increases in the frequency of variation were those in which infections with H. nana have not been recorded heretofore. These include: Marmota monax (Linnaeus), Tamias striatus (Linnaeus), Sciurus carolinensis pennsylvanicus 0rd*, Tamiasciurus hudsonicus (Erxleben)*, Glaucomys volans querceti (Bangs)*, Perognathus longimembris longimembris (Coues), Dipodomys merriami merriami Mearns, and Oryzomys palustris (Harlan). The most significant effects, with respect to increasing the frequency of variation in H. nana were found in specimens which had been reared in the three species of sciurids indicated by an asterisk in the preceding list.
590
SCHILLER I~EFERENCES
CAMERON, T. W. M. 1956. Parasites and Parasitism. J o h n Wiley and Sons, Inc. New York, 322 pp. CHANDLER, A. C. 1955. I n t r o d u c t i o n to Parasitology. J o h n Wiley and Sons, Inc. New York, 9th ed. 799 pp. MILLER, G. S., JR., AND KELLOG(~, R. 1955. List of N o r t h American recent mammals. U. S. Natl. Museum Bull. 205,954 pp. READ, C. P., SCHILLER, E. L., AND PreFER, K. 1958. The role of c a r b o h y d r a t e s in the biology of Cestodes. V. C o m p a r a t i v e studies on the effects of host d i e t a r y c a r b o h y d r a t e s on Hymenolepis spp. Exptl. Parasitol. 7, 198-216. SCHILLER, E. L. 1959a. E x p e r i m e n t a l studies on morphological v a r i a t i o n in the eestode genus Hymenolepis. I. Morphology and development of the cystL cercoid of H. nana in Tribolium confusum. Exptl. Parasitol. 8, 91 118. SCHIbLER, E. L. 1959b. E x p e r i m e n t a l studies on morphological v a r i a t i o n in the cestode genus Hymenolepis. II. Growth, d e v e l o p m e n t and reproduction of the strobilate phase of H. nana in different m a m m a l i a n host species. Exptl. Parasitol. 8, 215-235. SCHILLER, E. L. 1959c. E x p e r i m e n t a l studies on morphological v a r i a t i o n in the cestode genus Hymenolepis. III. I n v e s t i g a t i o n s on the use of X - i r r a d i a t i o n as a mechanism for facilitating analyses of the nature, extent and directional t r e n d s of morphological w~riations in H. nana. Exptl. Parasitol. 8, 427-470.