Zbl. Vet. Med. B, 21, 765--773 (1974) @ 1974 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-4294/ASTM-Coden: ZVRBA2

From the Swiss Rabies Center at the Veterinary Bacteriological Institute, University of Berne, Switzerland; the State Veterinary Serum Laboratory, Copenhagen, Denmark; and the State Veterinary Institute, FrankfurtlMain, Federal Republic of Germany

Rabies in Wild Carnivores in Central Europe*) 111. Ecology and Biology of the Fox in Relation to Control Operations

A. WANDELER, J. MULLER,G. WACHEND~RFER, W. SCHALE, U. FORSTER, and F. STECK With one figure and li tables (Received f or publication February 27, 1974)

The notion that foxes appear to play the determining r61e in the epizootiology of rabies in Central Europe was confirmed by our previous studies (WANDELER et al., 1974 a and b). In view of the very marked dependence of the rabies epizootic on the density of the fox population, efforts have been made in many countries to control the disease by reducing the susceptible population. Since other animal species appear to be only secondarily involved in the perpetuation of the rabies epizootic, the singling out of one particular seems justified. The efficiency of conspecies - in our situation the red fox trol operations depends on several factors, mainly: accessibility of foxes to different control methods under various ecological circumstances; effort and goodwill of people involved; regeneration capacity of the reduced fox population. These problems are discussed under the three headings: a) Estimation of population density to evaluate the effect of rabies and control operations. b) The rate of reproduction in foxes in view of the regeneration capacity of the populations, and c) The influence of fox ecology on the efficiency of control operations.

-

*) This investigation is part of a WHO/FAO Coordinated Research Programme on wildlife rabies in Europe. It received financial support from the World Health Organization, the Swiss Federal Veterinary Office, the Danish State Agricultural and Veterinary Research Foundation and the Bundesministerium fur Ernahrung, Landwirtschaft und Forsten, Bonn, BRD.

WANDELER, MULLER,WACHENDOWER, SCHALE, FORSTERund STECK

766

Material and Methods Epidemiological and virological methods have been described previously (WANDELER et al., 1974 a and b). Hunting records were obtained from the official hunting authorities. Distribution of litters and observations on litter size have been supplied by the cantonal game wardens in the canton of Berne and by hunters in the cantons Aargau, Basel-Land, and St. Gallen. Age determination was based on teeth abrasion, and the radiographic measurement of the width of the pulp cavity (JENSEN, in press). Wild carnivores: Large numbers of healthy and diseased animals from endemic and rabies-free areas were obtained through collaboration with the responsible veterinary and hunting administration. From carcasses all uteri and, in addition, organs with macroscopic lesions were fixed in 10 O/o formalin for further evaluation and histological examination. Brain and salivary gland were taken for virus isolation and blood from the thorax whenever possible for serology. I n mustelids a complete parasitological examination was performed; in foxes the diaphragm was checked for trichinosis (detailed results will be published later). Results and Discussion of f o x population density The effect of control operations and the influence of rabies on fox density should be measured directly. U p to now no simple method for determining absolute fox numbers per unit area is available. In the canton of Berne the population density was estimated from the observation of litters by the cantonal game wardens. Since all healthy vixens give birth to a litter and the proportion of male to female is 1.2 : 1, based on the sex ratio in several different samples (WANDELER, unpublished data), a minimal fox population can be calculated: Number of observed litters multiplied by 4,67 (the average number of puppies per litter, Table 2 ) plus one female and 1.2 males per litter. At a constant population density the calculated annual generation should equalize the number of foxes found dead or killed. Quite good agreement between annual generation and losses was found in this way under undisturbed and favourable topographical conditions (Table 1). It is difficult to judge what proportion of the fox population is evading this estimation. In mountainous o r other inaccessible areas with a complicated topography the registration of litters and dead animals becomes very unreliable.

a ) Estimation

Table I Calculation of population density at annual population peak in summer observed litters I km2

Jura Mittelland Oberland =

zi }

observed

calculated

puppies per litter

annual generation I

km2 4.67

0.16

number of foxes/kme

1.12 0.98 0.75

'

foxes I km2

whelping

1.13'

0.53

0.78

0.35

'

1.65 1.10

'

Rabies in Wild Carnivores in Central Europe / 111.

767

The only parameter available to estimate changes in the fox population density over larger areas is the official hunting records (MOGLE, KNORPP, and BOGEL,1971; WANDELER et al., 1974 a, in press), but this should not be interpreted uncritically. The number of animals killed per square kilometer is not only a function of population density but also of hunting intensity. Because of the gassing a large proportion of the dens are closed. A comparison between the number of foxes shot at their dens in the canton Berne (without gassing) and in a rabies-endemic zone with gassing (canton St. Gallen) is shown in Table 3. In addition one should take into account, as mentioned before, that hunting is taking its toll more among young animals than old ones within the fox population. This should be considered in particular when the hunting records are declining.

b) Rate of reproduction In view of the close correlation between fox density and incidence of rabies on one hand and the high toll which rabies, hunting, and gassing of fox dens are taking, the rate of reproduction becomes a prime factor in the epidemiology of rabies. Foxes have a very high rate of reproduction (Table 2). Table 2 Reproduction in foxes (observations on reproduction calculated per individual female or litter) L

normal foxes from rabiesfree areas

total implanted fetuses per pregnant female fetuses lost after implantation per pregnant female placental scars per adult female puppies per litter 1

from rabies endemic areas 5.37

(

90) 1

361'

0.27

( 90)'

1.46)'

5.10

(2L21

1399 1

'

foxes with chronic

'

?

number of uteri examined number of litters in the field from which puppies were counted by game wardens.

All individuals become sexually mature in their first year of life. All healthy females produce every year a litter with an average of 4.7 puppies. Assuming zero mortality, a fox population trebles its density annually. The three year cycle of rabies incidence in many areas of Europe (KAUKERet al., 1963; ULBRICH,1967) is explained by the capacity of fox populations to recover rapidly after rabies and/or control operations, so that a population reaches in this time the density needed for further rabies propagation. KAUKERand ZETTL(1960) assumed that vixens in a population reduced in density by gassing or rabies were more fertile. We could not find any significant difference between the number of fetuses implanted per female in animals from low density (rabies endemic) and those from high density (canton Berne) areas (Table 2). Variation in perinatal mortality seems to be a more important factor in self-control of vertebrate-population-density than the fertility of females (LACK, 1954). From the number of fetuses per female, the ratio between fertile and infertile (barren) vixens and the sex ratio, we calculate a proportion of about 70 O/O juveniles to 30 O / o adults just after the whelping season. The same proportion was still found in fall and winter, both in control Zbl. Vet. Med., Reihe B, Bd. 21, Heft 10

53

WANDELER, MULLER,WACHEND~RFER, SCHALE,FORSTER und STECK

768

,

canton St. Gallen (with gassing of dens)

canton Bern (without gassing) Mittelland

Jura

Oberland

Number of foxes killed in regular hunting

7L7

1607

763

1126

shot at den

6 *I.

37 *I.

29 '1.

10 *I.

and in rabies-endemic and gassed areas in animals killed or found dead for et al., 1974 a). Rabid animals on the other hand several reasons (WANDELER include in fall and winter only 46 O/o juveniles. Whether this reflected a reduced exposure of juveniles to rabies was discussed previously. Unsolved remains the problem as to which sample (rabid or shot foxes) best represents the population structure. Since these two samples differ greatly in age structure, it is difficult to compare the population turnover or longevity of foxes in an endemic and in a rabies-free area. c) Efficiency of control operations Hunting methods alone do not seem to reduce fox density sufficiently to prevent further expansion of rabies. In all study areas the number of foxes shot increased due to intensified hunting as rabies came close. The bag record nevertheless did not decrease but remained at the higher level in the following years. A rapid decline was seen only after gassing operations or still more distinctly after invasion by rabies. In view of the inefficiency of hunting, veterinary administrations ordered the gassing of fox dens in Hesse, Denmark and suitable areas of Switzerland. The effect of gassing operations aimed at reducing the fox population is largely dependent on timing and on the distribution of the fox litters in different kinds of shelters. Only earth holes can usually be rendered sufficiently airtight to allow the build-up of a toxic gas concentration in the burrows which kills the inhabitants.

number of dens studied Jura Mittelland Oberland

70L 1179 588

'

fox only

badger and fox simultaneously or alter natively

badgr only

LL *I. 28 .I. 41 'I.

27 91. 5L *I. 22 .I.

29 '1. 18 *I. 37 'I.

In areas with suitable ground and where no other shelter is available in sufficient numbers, foxes dig their own den. In Switzerland, in the canton of Berne, Mittelland, they use, and frequently enlarge, badger dens (Table 4), and in the Jura and Oberland they use natural caves. The shelters in which litters were observed are listed in Table 5. These figures illustrate very well the adaptability of foxes to different topographic situations. This is also seen in zones with gassing, where the disturbed dens are more and more avoided

Rabies in Wild Carnivores in Central Europe / 111.

769

Table > Distribution and location of fox litters' Canton Bern (without gassing)

I number of litters observed in burrows made by foxes or badgers in natural caves

I

in drainage pipes in or under buildings other locations (windfallen wood

, etc.)

number of litters observed in burrows made by foxes or badgers

I

Jura

Mittelland

Oberland

391 a4

01~

165 L5 "10

L1 %

a

01~

19 %

2% 1

I

010

225 65 %

2 010

1%

4 -10

35 %

2%

1 %

1

I

329 55 %

I

1

203 63 %

1

I

I 201 49 %

0%

I

1

I

562 La

81-

Data obtained through questionnaires from official game wardens, based on their observations in the field.

(Table 5, compare BL 1969 with BL 1970). Since the recording of litters in known earths is more reliable and complete than in other shelters, this trend could even be stronger than is evident from actual observations. The success of gassing depends also on weather conditions and season. Dens are used by foxes mainly during the whelping season for raising their puppies. At other times they serve only as an occasional refuge or lair, seldom as a regularly inhabited home; they are more frequented during bad than good weather. Disturbance of dens could induce foxes to avoid them over a longer period. The flair-up or persistence of rabies in some areas of Switzerland and Hesse may be due to some extent to the changing living habits of the fox which makes it less vulnerable to the gassing of dens, but gassing operations have certainly met with strong opposition from a considerable number of hunters (KERSTEN et al., 1971). It is understandable therefore that the gassing operations became less efficient after the immediate danger seemed to be over. In the long run these two factors (human factor and changing living habits of the fox) may render gassing operations ineffective (WACHEND~RFER et al., 1972). The success and partial failures of control operations in some areas of Switzerland have been discussed previously (WANDELERet al., 1974 a, Fig. 5 and 6). The efficacy of gassing operations in Hesse is shown in Fig. 1. After initial succes, the epizootic developed a considerable rebound. In the bottom line the numbers of post-exposure treatments in humans from 1964 to 1970 are shown. These figures show a close direct relationship with the numbers of rabies cases in animals. Even before the start of general gassing of dens in 1965, after the unset of rabies in 1953, the bag records of both foxes and badgers were declining. During the following years the number of killed foxes increased, while the bag records of badgers continuously decreased. At the same time the numbers of killed small mustelids, which do not share dens with foxes or badgers, had a general upward trend. Whether this is due to a real increase in population or to increased hunting pressure, is not known (see 53*

WANDELER, MULLER, WACHEND~RFER, SCHALE,FORSTER und STECK

770

Gassing - Operations

’M1-

Partial

om -

im 400 -

L

300

-

P Y

E a

z

n oIQO-

I

0“

Cases of Postexposure Treatment in Humans 135318841287/1131169 11% 1287 I

Fig. 1 . Cases of rabies in Hesse before and during gassing operations

WANDELERet al., 1974 a, Fig. 9). In the three European study areas are two regions where the invasion of rabies was successfully prevented. One is the canton Aargau in Switzerland which was able to stop the epizootic at the river Aare by means of intensive and correctly executed gassing on both sides of the river. The successful efforts of Denmark are described in more detail below (MULLER,1966,1971). In Denmark reduction of the fox population was used as a means of rabies control since the first outbreak in South Jutland in 1964. Shooting for bounty and gassing of fox dens were the methods employed. The gassing operations were carried out a t rutting time (JanuaryFebruary) and again a t breeding time (March-April) by specially trained personnel acting under the supervision of the local police. “Cymag” (I. C. I.), a powder containing 40 O/o sodium cyanide, was pumped into the dens releasing prussic acid in the presence of moisture and carbon dioxide. The owners of land were ordered to report the presence of fox dens on their land; for every occupied den a premium of 100 DKr. was paid. At the beginning of the rabies outbreak in 1964 gassing of fox dens was carried out within a 10 km. deep zone along the frontier. Very soon, however, the zone of gassing operations was extended to the north, eventually reaching 30-45 km. north of the frontier, when the outbreak died out in the autumn of 1965. Neverthless, gassing operations were continued during the following rabies-free years. In 1967 the hunting bag index was estimated at 0.2 fox per km2 in the gassing zone compared to 1.0 fox per kmz before the campaign, indicating an 80 O/o reduction in fox density. North of the gassing zone, in a 30 km. deep belt across South Jutland, shooting for bounty as the only measure of fox control had resulted only in a 25 O/o reduction and was, therefore, abandoned as too costly and inefficient. When in the beginning of 1969 a second wave of sylvatic rabies from Schleswig-Holstein crossed the frontier, the disease was not able to spread freely within the area where the fox population since 1964 had been kept a t low level by shooting and gassing of dens. In this area the hunting bag index was estimated at 0.15 fox per kmz in 1969.

Rabies in Wild Carnivores in Central Europe / 111.

771

However, in the north-west corner of the gassing zone a focus of fox rabies developed, which was not eliminated before the disease had spread across the nothern boundary of the gassing zone into an area where gassing of dens had never been carried out and where shooting for bounty had been abandoned in 1967. In this area, with a hunting bag index in 1969 of 1.0 fox et al., per km2, a major outbreak developed in 1969 and 1970 (WANDELER 1974 a, Fig. 2) and was eventually eliminated by the combined action of the disease itself and the gassing and shooting operations which were carried out in the freshly invaded and adjacent areas up to a depth of 120 km. from the frontier. It would appear that under Danish geographical and ecological conditions large-scale gassing of fox dens proved to be a n effective means for sufficiently reducing the fox density to eliminate two outbreaks of fox rabies. A “prophylactic” reduction of fox density proved of considerable protective value against an advancing wave of sylvatic rabies, even though the protective zone was too narrow to prevent the disease from leaping across into an unprotected area. In view of the difficulties encountered with proven methods in the two other study areas, additional methods for reducing the susceptible fox population should be further evaluated, in particular the possibility of active immunisation by the oral route, in respect to their efficiency and the possible hazards of the widespread dissemination of a live, attenuated rabies virus.

Summary The rate of reproduction, the turnover and the age structure of fox populations were determined by field observation and examination of a large number of normal and sick foxes obtained for autopsy. Undisturbed regions were compared to regions where the fox population was reduced by control operations and / or rabies. The reduction of the number of foxes, the essential vectors of rabies virus in Central Europe, has been shown to be a valuable approach to control wildlife rabies. Such operations should, however, be monitored by their effect on the fox population, rather than on rabies alone. Gassing of fox dens has proved to be the most effective single method. However, it is greatly influenced by ecological and biological factors. Complete eradication of foxes is not aimed at and cannot be reached mainly because of the high reproductivity of foxes and because many litters are raised in locations inaccessible to gassing, particularly after prolonged disturbance of dens. Campaigns aimed a t reducing other wild carnivores as a measure of rabies control appear in our situation not to be justified. Zusammenfassung Vorkommen und Bedeutung der Tollwut bei den Wildcarnivoren Zentraleuropas 111. Ukologie und Biologie des Fuchses in Beziehung zu den Kontrollmahahmen Reproduktionsrate und Altersstruktur der Fuchsdichte wurden vergleichend in tollwutfreien Zonen mit normaler Besatzdichte und in solchen Gebieten untersucht, in denen der Fuchsbestand durch Kontrollmaflnahmen und/ oder das Seuchengeschehen reduziert worden war. Die Dezimierung der Fiichse - in Zentraleuropa die essentiellen Tollwutvektoren - hat sich als wertvoll fur die Kontrolle der Wildtollwut erwiesen. Dabei sollte jedoch nicht

772

WANDELER, MULL,,, WACHENDORFER, SCHALE,FORSTERund STECK

iiur das Seuchengeschehen, sondern auch die Biologie des Fuchses berucksichtigt werden. Eine totale Ausrottung der Fuchse ist nicht wunschenswert. In dieser Hinsicht stellt die Baubegasung die wirksamste Einzelmahahme dar. Eine Dezimierung anderer Wildcarnivoren ist in unserer Situation zur Tollwutkontrolle ungeeignet und daher nicht gerechtfertigt.

Rksumk Apparition et signification de la rage chez les carnivores sauvages de 1’Europe centrale 111. Ecologie et biologie du renard en relation avec les mesures de surveillance On a examinit le taux de reproduction et les donnkes d’9ge de densitk en renards en comparant des zones indemnes de rage avec une population normale et des rkgions dont le nombre des animaux avait ktk diminuk soit par les mesures de contrble soit/et B cause de l’kpizootie. La destruction des renards, vecteurs principaux de la rage en Europe centrale, s’est rCv@lke trks valable pour le contrble de la rage sylvestre. O n ne doit cependant pas considkrer seulement le dkroulement de l’kpizootie, mais kgalement la biologie du renard. Une klimination totale des renards n’est pas souhaitable. A ce paint de vue, le gazage des terriers reprksente la mesure individuellc la plus efficace. Une destruction des autres carnivores sauvages est inadaptke B notre situation de contrble de la rage et ne se justifie pas. Resumen Incidencia y alcance de la rabia en 10s carnivoros salvajes de Europa Central 111. Ecologia y biologia de la zorra en relaci6n con las medidas de control Se analizaron comparativamente la tasa de reproduccibn y la estructura de edades de la densidad de zorras en zonas libres de rabia con densidad normal de guarnicibn y en aquellas comarcas en las que se redujo el efectivo de zorras mediante medidas de control y/o el devenir epizootolbgico. La decimalizaci6n de las zorras - en Europa Central son 10s vectores esenciales de la rabia - se ha confirmado como valiosa en el control antirrhbico de las alimaiias. Pero aqui no se deberia considerar solo el devenir epizootolbgico, sino tambikn la biologia de la zorra. La erradicacibn total de las zorras no es digna de encomio. A este respecto, la gaseificacibn de las madrigueras es la medida aislada mbs efectiva. La decimalizacibn de otros carnivoros salvajes es impropia en el caso de nuestra situacibn en el control antirribico y, por tanto, no se considera justificada. References KAUKER, E., and K. ZETTL,1963: Zur Epidemiologie der sylvatischen Tollwut in Mitteleuropa und zu den Moglichkeiten ihrer Bekampfung. Vet.-med. Nachr. H 2 / 3 , 181. KERSTEN, W., and E. ZINN, 1971 : Die Bekampfung der sylvatischen Tollwut durch Kombination der Begasung von Fuchsbaucn und AbschuflfGrderung von Fuchsen. Dtsch. tierarztl. Wschr. 78,175-187. LACK,E., 1954: The natural regulation of animal numbers. Oxford Univ. Press. London and

New York.

MOGLE,H., F. KNORPPand K. BOGEL,1971: EinfluQ der Begasung der Fuchsbaue auf die Fuchsdichte und die Wildtollwut in Baden-Wurttemberg. Berl. Munch. tierarztl. W s h r . 84,437-44 1.

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MULLEX,J., 1966: The reappearance of rabies in Denmark. Bull. Off. Int. Epiz. 61, 21-29. MULLER,J., 1971 : The effect of fox reduction on the occurrence of rabies. Observations from two outbreaks of rabies in Denmark. Bull. Off. Int. Epiz. 71, 763-776. PITZSCHKE, H., 1972: Untersuchungen uber die Fuchspopulationen - ein Beitrag zur Erforschung von Grundlagen fur eine wirksame Tollwutbekampfung. Mh. Vet. med. 27, 926-932. ULBRICH,F., 1967: Uber RegelmaSigkeiten beim Auftreten der Tollwut im Bezirk Dresden. Arch. exp. Vet.-Med. 20, 1073. WACHEND~RFER, G., W. SCHALEand U. FORSTER,1972: The Situation of Rabies in Hesse since 1953 - Evaluation of Epidemiological Data and Control Operations in Wildlife, presented at the Informal Discussions on the WHO/FAO Coordinated Research Programme on Wildlife Rabies in Europe, 3-5 July 1972, Nancy, France. WANDELER, A., 1968: Einige Daten iiber den bernischen Fuchsbestand. Rev. Suisse Zool. 71, 1071-1075. WANDELER, A., and F. STECK,1972: Epidemiological Studies of Wildlife Rabies in Switzerland 1967-1972, presented at the Informal Discussion on the WHO/FAO Coordinated Research Programme on Wildlife Rabies in Europe, 3-5 July 1972, Nancy, France. WANDELER, A., G . WACHENDORFER, U. FORSTER,H. KREKEL,W. SCHALE,J. MULLERand F. STECK,1974 a: Rabies in Wild Carnivores in Central Europe. I. Epidemiological studies (This journal, in press). A., G. WACHENDORFER, U. FORSTER,H. KREKEL,J. MULLERand F. STECK, WANDELER, 1974 b: Rabies in Wild Carnivores in Central Europe. 11. Virological and serological examinations (this journal, in press). Authors’ addresses: A. Wandeler, F. Steck, Veterinar-Bakteriologisches Institut der Universitat Bern, Langgass-Strai3e 122, C H 3001 Bern; J. Miiller, Statens Veterinaere Serumlaboratorium, Copenhagen; G . Wachendorfer, W. Schale, U. Forster, Staatliches VeterinarUntersuchungsamt, D 6 FrankfurtlMain.