Seasonal Incidence of Larval Hydatigera taeniaef or mis Infection of Microtus arvalis in Hungary Parasit. Hung. 6. 1973. Gábor NECHAY Central Plant Protection and Quarantine Laboratory of the Ministry of Agriculture and Food, Laboratory of Rodents, Tanakajd "Seasonal Incidence of Larval Hydatigera taeniaeformis Infection of Microtus arvalis in Hungary" - Hechay, G. - Parasit. Hung. 6. 117-130. 1973. On the basis of parasitological investigation of 3097 field mice the frequency of Hydatigera taeniaeformis infection was found to be 7.2 %. Seasonal studies revealed a peak of infection in the winter and spring, while a drop in infection rate was noted during the summer. In animals living in lucerne fields, a maximal rate of infection is reached already in the autumn months, while i t only takes place during next spring in those living in wheat fields. The frequency of strobilocercosis shows correlation with the age distribution of the investigated population. Taking the time, necessary for the development of cysts and the infection rate of mice into consideration, certain demographical conclusions can be reached. Hydatigera taeniaeformis Batsch, 1786 (syn.: Taenia taeniaeformi s Batsch) is common in small rodents. In the rodents as intermediate hosts the larval form of this "Strobilocercus fasciolaris" is to be found in the liver tissue with infective larvae in cysts of 8-10 mm diameter. The house and wild cats are the principal hosts. Other predators have not been found as principal hosts in Hungary. The parasite is endemic in Hungary and has been reported by KOTLÁN (1961), EDELÉNYI and SZABÓ (1963ï they report only the adult form in wild cats), NEMESÉRI and HOLLÓ (1972), KOTLÁN and KOBULEJ (1972), MURAI (1972), MURAI & TENORA (1973). KOTLÁN and KOBULEJ, NEMESÉRI and HOLLÓ have reported it as a common parasite of cats demanding veterinary attention and at the same time reported the host role of house mice and rats. MURAI and 117
M Pxg. 1: 03 Localities of the examined material 1. ábra: A vizsgált anyag gyűjtési helyei
Table 1 Number of infested common voles collected in various comitats in Hungary in 1971-72 Az ország különböző területein 1971-72-ben gyűjtött pockok fertőzőttsége Locality 1971 1972 Spring Autumn Spring Autumn L C L C L C L C 1. Egyházasfalu - - - - - - 156/2-2. Kimle 18/2 4/0 248/10 12/0 2/0 2/0 _ 3. Páli 13/0-57/15 4/0 - - - 4. Ujkér 3/0 7/3 105/13 6/0 -. - - 5. Izmény 3/0 25/4 40/9 - - - - - ízmény - - 26/3 4/1 - - - - 6. Decs 16/3 27/1 - - - - - - 7. Pusztaegres - - 15/2 - - - - - 8. Pusztaszabolcs _ 97/4 9. Velence 2/0 - - - 2/1 i/o - - 10. Kápolnásnyék _ 11/0 _ I 1 ' Isztimer - - - - - 5/0 12. Csanádalberti - - 16/5 i/o 13. Csorvás 7/0 5/0 - - - - 14. Kamut - 5/0 - - - - - - 15. Gyöngyöstarján 4/1 - - - - - - - 16. Sárvár - - 26/0-1/1 9/2 5/0 i/o Sárvár 22/7 18/3 9/0 5/0 i/o 2/0-17. Kenyéri 26/6 14/3 1/1 - - - - - Kenyéri - - 3/0 - i/o 7/0 26/0-18. Nőtincs - 305/14-2/1 - Nőtincs - - 47/3-3/0 - - nándor - - 50/4 - i/o - - - 19. Magyar - - Note: L = alfalfa or clover C = autumn wheat or barley Figures'before place-names refer to Fig. 1. A gyűjtőhelyek száma megegyezik a térkép számaival. 119
TENORA have shown the occurrence of larvae in numerous small mammalian species, namely in: 5 % of Apodemus flavicollis, 2 % of A. sylvaticus, 5 % of Microtus arvalis, 0 % of M. agrestis, 6 % of Mus musculus spicilegus, 1 % of albino laboratory breeds Of Mus musculus and Rattus rattus, 2 % of Clethrionomys glareolus and 1 % of Pitymys subterraneus. Since 1969, the Centr. Plant Prot, and Quarantine Lab., Rodent Laboratory Min. of Ag. Fd., has been continuing population-dynamic investigations on small rodents in agricultural fields. During this work we have also studied and estimated larval in fections (strobilocercosis) of Hydatigera taeniaeformis in the common vole, hypothesizing that i t has an effect on the vole population. Material and Methods Half the examined material representing one population"*" came from permanent collections near the village Bük (West Hungary, Com. Vas, see Pig. l ) in 1969-72. (Trapping in lines and 2 snap-traps taken in areas of 1000 m in perennial cultures - alfalfa, clover, italian meadow-grass or a mixture of these two latter and in corn - autumn wheat and barley.) The other half of our material came from collections made in other parts of the comitats (Békés, Csongrád, Győr, Fejér, Heves, Nógrád, Tolna and Vas, see Fig. 1.) in two regions of each comitat and twice in the same locality for three days consecutively in leguminous and corn cultures during spring (March-April) and autumn (October-December) in 1971-72. In these of areas the method collection was always line-trapping(independent of abundance and hole sites, with 100 snap-traps/meter). On the basis of the home range of the common voles and their migration from one culture to another increased particularly owing to human activity (e.g. rotation of crops, harvesting, ploughing and harvesting of perennial cultures, pest control etc.) and resulting in sudden changes of the environment, the specimens living in open areas (at the border territories of one agricultural cooperative) have to be considered as one population. 120
Pig. 2: Infestation by Hydatigera taeniaeformis larvae of different common voles according to sex and age 2. ábra: Pockok H. taeniaeformis fertőzöttsége nem és kor szerint t = number of observed Jf animals l = 1458 = 1454 number of animals infected with developing cysts n 0 = 60 n = 49 number of animals infected with fully developed cysts n ç = 59 nï = 52 Age groups= maximum 1 month, 1-2 months, 2-4 months, 4-6 months, older than 6 months 121
The investigations were carried out on fresh or occasionally frozen animal bodies. To estimate the infections in the liver the developing cysts (point-like on the surface, embedded small cyst in tissues) or cysts containing developed larvae were considered. The larvae were identified on the basis of samples sent to Dr. É. MURAI (Hungarian Nat. Hist. Museum, Budapest). The age of the common voles was also considered in the investigation. The body length of specimens was taken as an Indication of age. The animals were divided into five groups as follows: below 75 mm ( l ), 75.1-85 mm (2), 85.1-95 mm (3), 95-1-105 mm (4), and above 105 mm (5) (see Fig. 2). Supported by the investigations of several authors (BASENLNA, 1953; SEBEK, 1959; SYKORA, 1959) the ages of these groups were considered to be (l) younger than 1 month (2), about 1-2 months, (3) about 2-4 months, (4) about 4-6 months and (5) older than 6 months. Considering the well-known problems of ageing I would like to emphasize the possibility of overlapping between the groups, therefore the frequency of strobilocerci examined in each age group and the true age of the animals is only approximate. From a synoecological standpoint the infestation of groups 1 and 5 can be truly estimated, because specimens of these groups are surely younger than 1 month or older than 6 months. Results and Conclusions l ) Strobilocercosis was found generally in common vole populations from varied agricultural cultures; 222 (7.2 %) of 3097 Microtus arvalis specimens were infested (Tables 1 and 2). The degree of infestation in the more abundant population was greater than in the smaller populations. (It is shown in Table 1 that the abundance was directly proportional to the number of examined specimens.in Bük field the investigations were carried out during one population cycle. There would have been a peak year in 1971, but the population was decreased by controls carried out repeatedly in spring and autumn. Therefore the popula- 122
Table 2 Infestation in the Bük population according to the seasons and cultures in 1969-72 A büki populáció fertőzöttsége 1969-72-ben évszakok és kultúrák szerint leguminous c o r n t o t a l D a t e n inf. % n inf. % n inf. % 1969. VI-VIII 13 0 84 2 2.4 97 2 2.1 IX-XI 34 1 2.9 II-V 17 0 4 1 25.0 21 1 4.7 1970. VI-VIII 230 4 1.7 49 0 279 4 1.4 IX-XII 379 45 11.3 120 4 3.3-499 47 9.4 II-V 15 4 26.6 60 7 11.6 75 11 14.6 1971. VI-VIII 78 1 1.2 16 2 12.5 94 3 3.2 IX-XII 190 16 8.4 68 3 4.4 258 19 7.3 II-V 23 1 4.3 88 6 6.8 111 7 6.3 1972. VI-VIII 16 1 6.2 60 2 3,3 76 3 3.9 IX-XI I 19 0 19 0 " " Total - Összesen 961 72 7.3 568 27 4.7 1563 98 6.3
tion was moat abundant in autumn 1970, at a minimum in 1969 and small in 1972.) 2) The differences according to sex and age are shown in Fig. 2. (It is based on 2912 - or 220 infested - specimens examined of the total number of 3097 specimens collected.) We did not find a relationship between age of specimens and degree of infestation with strobilocercosis in mobile voles. We have ascertained that the cysts have no discernble effect on the l i f e of the hosts. The difference between sexes was negligible, but the degree of infestation in the varied specimens of different sexes and ages was of interest in some respects. On the basis of the presence of fully developed cysts among the weanling voles (2 cases, see males) and regarding several experiments (MLODZIMOWSKA, 1931; DOW & JARRETT, I960; OLIVIER, 1962) showing that more than 30 days are needed for this parasite to develop in albino mice, i t can be concluded that the infestation would have occurred during the early suckling age by parasite ova brought into the nest.the inversion between the number of developing and fully developed cysts in age groups 2 and 3 of females probably indicates a more equal development of females. But the males can be supposed to be more sensitive to an oncosphera invasion in the early phase of the infestation, resulting in a greater degree of mortality and a smaller number of manifested strobilocercosis. (The home range - area of activity - is much greater in males - even of juvenil age - than in females (REICHSTEIN, 1951), meaning theoretically a greater exposure to the infestation. According to DOW and JARRETT the male mice were more disposed to the infestation, OLIVIER experimented only on males. According to MLODZIATTOWSKA, the juvenil mice were much more seriously affected by the infestation. The symptoms of illness and generally the deaths following a few days after infestation were also experienced by these authors.) 3) The above conclusion is confirmed by the investigation of the intensity of infestation. According to the numbers of developing cysts, 29 males were infested by one and 20 others by
Fig. 3: Seasonal incidence of strobilocercosis in the Bük population A strobilocercosis szezonális előfordulása a Bük-i populációban Spring Summer Autumn n = number of examined specimens vizsgált állatok száma leguminous pillangós kultúrák corn gabona Infestation of voles in leguminous stands p i l langósokban élő populáció fertőzöttsége Infestation of voles in corn fields gabonában élő populáció fertőzöttsége 125
more than one cysts. These values in females were 41 and 19 respectively. Considering the fully developed larvae, 43 males and 50 females were infested by one and 9 males and 9 females by more than one larvae. We found several times some lactating and at the same time gravid females with an intensive infestation. The greatest number of larvae found was 6. 4) There were important differences in the occurrence of strobilocercosis according to the seasons (Table 2 and Pig. 3). The infestation was at a minimum during summer or the period of vegetation, and at a maximum in winter populations. This is probably connected with the vole-killing activity of predators or some other factor (during the infective phase of oncosphera, resistance of voles). Aware of the reproductive cycle in the vole population, the specimens infested by strobilocercosi can be considered indicative of the whole population and their disappearance from the population until summer time indicates a relatively quick mortality of overwintered animals next spring. These data confirm the results of the seasonal changes of the structure in Microtus arvalis populations shown by MARTINET (1967), MARTINET and SPITZ (1971). (In our experimental area we found the sexually inactive - non breading - season in 1968/69 from the middle of Oct. to the middle of April, in 1969/70 from Dec. to the end of March, in 1970/71 from Oct. to the middle of Pebr. and in 1971/ 72 from the end of Sept. to the middle of March.) In autumn, the small infestations of corn cultures (Pig. 3) are probably due to the fact that these are ploughed and sown in October-November.The majority of these populations consisted of recent immigrants from other territories. The migration is probably an explanation of the fact that strobilocercosis is more frequent even in autumn in these areas than during the summer. 5) Considering the infectious sources mentioned, only the Bük vole population is really known. The area represented by col- 126
lections is about 3 km,as the crow flies, from inhabited areas. Stray cats have not been seen on our sampling site. During the autumn and winter seasons of the four year investigations we have several times experienced, that weasels predated the common voles. In 1971,the trapped voles were also eaten by a field polecat (its hole was treated by gassing with PH^ and the body dug out). On the basis of these observations, Hydatigera taeniaef ormis can be supposed to be a common parasite in other predator species. This is confirmed by several publications: NEMESÉRI & HOLLÓ (196I) mentioned strobilocercosis to occur in rats and mice-eating dogs; HINAYDI (1971) identified this species in foxes in Austria; PALOTÁS (1969) stated, that the house cat was preceded by fox,field polecat and weasel from the point of view of vole-eating. Acnowledgement I wish to express my thanks for identification work and professional aid to Dr. É. MURAI-, and to my coworkers M. VERHÁS and Miss Zs.VITÁLYOS for providing assistance in collections and elaborating the data, and to my wife E. NIKODÉMUSZ, for the translation, and to M. REEVE for supervising the translation. JNECHAY, G. : A mezei pocok Hydatigera taeniaeformu lárvákkal való fertőzöttségének évszakos változása Magyarországon Az ország különböző részeiből származó 3097 mezei pocok 7,2%-át találta fertőzőttnek.a fertőzöttség gyakorisága a gazdák egyedsűrűségének növekedésével emelkedik. Szezonális ingadozás is észlelhető, legkisebb a fertőzöttség nyáron, a vegetációs időszakban. Szerző feltételezi, hogy a hímek gyakrabban fertőződnek, de a parazita kártétele iránti fokozott érzékenységük miatt - különösen az invázió szakaszában - nagyobb a mortalitásuk is. Ezért a fertőzött nőstények száma valamivel nagyobb, mint a fertőzött hímeké. A kifejlett cysták jelentős károsodást valószínűleg nem okoznak. Populáció-dinamikai szempontból a fertő- 127
zött gazdák "jelölt" egyedeknek tekinthetők, amelyek segítségével demográfiai következtetések vonhatók le, pl. a szaporodási időszak kezdetén az áttelelt egyedek éliminaiódásának időtartamát illetően. Megfigyelések és irodalmi adatok alapján feltételezhető, hogy a Hydatigera taeniaeformis a macskán kívül más ragadozó fajoknak is parazitája lehet. References 1. BASEHINA, H.V.: The question of determining age of the common vole (Microtus arvalis Pall.)(in Russian) - Zool. Zsurnal 32. 730-743- 1953. 2. DOW, C. - JARRETT, W.P. H.î Age, strain and sex differences in susceptibility to Cysticercus fasciolaris in the mouse. - Experimental Parasitology 10. 72-74. I960. 3. EDELÉHYI, B. - SZABÓ, I. : Parasitische Würmer in einheimischen Saugetieren. - Ann. Hist.-nat. Mus. Hat. Hung. 55. 275-283- 1963. 4. HIHAYDI, H. K.: Die Parasitenfauna des Rotfuchses, Vulpes vulpes L. in Österreich. - Zbl. Vet. Med. 18. 21-32, 1971. 5. KOTLÁN, S.: Parazitológia - Budapest, pp. 631-1961. 6. KOTLÁN, S. - KOBULEJ, T.: Parazitológia - Budapest, 1-503, 1972. 7. MARTINET, L.: Cycles saisonnaires de reproduction du Campagnol des champs, Microtus arvalis. - Ann. Biol. anim. Bioch. Biophys. 7. 245-260. 1967. 8. MARTINET, L. - SPITZ, P.: Variations saisonnaires de la croissance et de la mortalité du campagnol des champs, Microtus arvalis. - Mammalia, 35. 38-84- 1971. 9- ML OD Z IAN OW SKA*, B.: Über die jüngsten Entwicklungs stadien von Cysticercus fasciolaris Rud., die Larve von Taenia taeniaeformis Bloch, auf Grund von Experimentaluntersuchungen. - Bull, de l'acad. Polonaise des Sciences, Ser. B. 2. 475-511- 1931-128
10. MURAI, É.: A magyarországi Apodemus-faj ok galandférgeiről (Cestodes). - Parasit. Hung. 5_. 47-82. 1972. 11. MURAI, É. - TENORA, P.: Some taeniid species (Cestoidea) parasitizing vertebrates (Rodentia, Carnivora, Strigiformes) in Hungary. - Acta Zool. Acad. Hung. 19. 125-132. 1973. 12. NEMESÉRI, L. - HOLLÓ, P.: Állatorvosi parazitológiai diagnosztika. - Budapest, 1-469. 1972. 13. OLIVIER, L.: Natural resistance to Taenia taeniaeformis. I. Strain differences in susceptibility of rodents - J. of Parasitology 48. 373-378. 1962. 14. PALOTÁS, G.: Az emlősök szerepe a mezei pocok (Microtus arvalis Pali.) elleni biológiai védekezésben - Agrártudományi Főiskola Tudományos Közleményei, Debrecen, p. 159-189. 1969. 15- REICHSTEIN, H.: Untersuchungen zum Aktionsraum und zum Revierverhalten der Feldmaus Microtus arvalis (Pall.) - Zeitschrift für Saugetierkunde 25_. I5O-I69. 1951. 16. SEBEK, Z.: Problenlivost telesnych znaku hrabose polniho V podmxnkách volné prirody od stári t r i tydnu do prirozené smrti.-in Hrabos polni (edit. KRATOCHVIL, J.) Praha, 60-79. 1959. 17. SYKORA, I. : Rust a v^voj hlavních telesnych znaku hraboëe polniho od narození do prirozené v podmínkách chovu a volné prirody. - In Hrabos polní (edit.kratochvil, J.), Praha, 53-59- 1959. Received: 15. 2. 1973. NECHAY, G. MÉM KNKL Rágcsáló-Biológiai Laboratóriuma 9762 Tanakajd, Hungary