Rabies in the Federal Republic of Germany, 1950-81: the Influence of Landscape*

Bulletin ofthe WorldHealth Organization, 62 (1): 99-106 (1984) © World Health Organization 1984

Rabies in the Federal Republic of Germany, 1950-81: the influence of landscape*

H. C. JACKSON' & L. G. SCHNEIDER2

Rabies statistics for 1950-81 were studied to investigate regional differences in the occurrence of rabies in the Federal Republic of Germany. At the level of Landkreis (administrative unit with a mean area of 1013 km ), four basicpatterns ofrabies incidence were identified: insignificant occurrence, low undulations, intermittent peaks, and high oscillations. The distribution of these four epidemiological patterns of rabies was geographically localized. Insignificant occurrence of rabies was found almost exclusively on land under 100 m abovesea level with less than 10% forest cover. High oscillations in rabies occurrence were found most often in areas over 200 m above sea level with an average of at least 35%o forest cover.

The current extended epizootic of sylvatic rabies in hunting, fox den gassing, poisoning, and trapping. Europe has affected the Federal Republic of Germany Fox den gassing, in particular, has apparently been for more than 30 years. The disease spread across successful in the short term (8, 14, 17, 18, 25, 28), but eastern Europe during the 1940s and rabies was first rabies has often reappeared within a few years. diagnosed in the Federal Republic of Germany in Indeed, since 1940, Denmark and the Netherlands are Schleswig-Holstein in December 1950. Numerous the only countries in Europe that have become free infections were observed along the eastern border of from the disease for more than a few years, once the country in 1951, and by the 1970s rabies had been rabies has been diagnosed in foxes. diagnosed in all parts of the country. The disease con- This failure to eliminate rabies can almost certainly tinues to be an intractable problem in many regions be explained by the adaptability of red fox popu- today. lations. Foxes are ubiquitous in Europe with an esti- As in the rest of central Europe, the red fox, Vulpes mated density range of 0.1-4.0 foxes per km2 (spring- vulpes, is both the reservoir of rabies infection and the time population) and are thought to be more numer- major vector species (23, 24). A knowledge of certain ous in mixed mosaic habitats than in homogeneous aspects of fox biology is central to an understanding ones (10-12). Difficulties arise in describing the of rabies epidemiology, in particular, the variations in habitat requirements and preferences of foxes fox habitat, population density, population turnover, because these are so broad (the animals being able to and behaviour. survive under the most diverse conditions), and also Rabies occurrence is strongly dependent on fox because fox-hunting and other control measures can density, but the relationship is nonlinear (1, 14, 20), disturb their behaviour. and, according to conventional theory, the frequency Foxes become sexually mature at the end of the first of rabies is also related to fox population turnover year of life and mature females can produce an and fox-to-fox contact rate (1, 2). Rabies cannot average of 4-5 cubs per year (12, 23). A fox popu- persist in areas of very low fox density and low fox-to- lation, reduced by hunting, control measures, rabies, fox contact rate. The threshold population level for or a combination of these, is capable of rapid continued transmission is thought to lie around 0.3 recovery and may even overshoot the original popu- foxes per km2 (15). lation level within 3-7 years (3, 16). The time required The aim of rabies control in central Europe is to to regain the original population level, or at least that reduce fox density to below the threshold level. The required for rabies propagation, depends on the pro- methods currently in use include intensified fox- portion by which the population has been reduced * From the WHO Collaborating Centre for Rabies Surveillance (3). Rabies alone can cause a reduction in the fox and Research, Federal Research Institute for Animal Virus Diseases, of 5007o or more Postfach 1149, D7400 Tubingen, Federal Republic of Germany. population (3, 19). Requests for reprints should be addressed to Dr Schneider. The present paper discusses the rabies statistics for Assistant. the Federal Republic of Germany from 1950 to 1981 2 Head. at the level of Landkreise (administrative units). It 4383 -99- 100 H. C. JACKSON & L. G. SCHNEIDER thus covers a large area over a long period of time. sidered only an indicator of the incidence of the Although the report is necessarily descriptive, it disease. attempts to put the problem in perspective by showing the relative degree to which different areas are Landscape characteristics affected, how the patterns of rabies occurrence vary In order to obtain a preliminary approximation of from region to region and, finally, how landscape the landscape character in regions of the Federal characteristics are associated with the different Republic of Germany with distinct patterns of rabies patterns of occurrence. These epidemiological pat- occurrence, the percentage of different types of land terns of rabies are interpreted in terms of fox popu- use and an indication of the altitude were obtained lation density and contact rate. using 1:2 500 000 maps from the Times World Atlas The many factors that can play a role in fox rabies (21) and the World Atlas ofAgriculture (26). epidemiology (such as geographic variation in fox behaviour, fox population density and population dynamics, type and degree of hunting, and type and RESULTS timing of fox population control methods) are not discussed. Mean rabiesfrequency The mean frequency of reported rabies cases in METHODS each Kreis, calculated from the year rabies was first reported, ranged from 0.0 to 9.0 cases per 100 km2 Rabies occurrence per year. The overall mean frequency for the country was 1.9 cases per 100 km2 per year (standard devi- Data on rabies for 1950-78 were extracted from the ation, 1.5). Tierseuchenbericht (record of notifiable animal dis- Fig. 1 shows the geographic distribution of low, eases) (22), and for 1979-81 from computer records intermediate and high mean rabies frequencies. held at the WHO Collaborating Centre for Rabies Kreise with a mean frequency of fewer than 1.0 Surveillance and Research in Tubingen. The country reported case per 100 km2 per year are found in west was divided into 257 units representing either one or Schleswig-Holstein, north and west Niedersachsen, several Kreise. Because of the large number of Kreis north and west Nordrhein-Westfalen, on the west boundary reforms since 1950 and because the exact bank of the river Rhine in Rheinland-Pfalz, and parts location of rabies cases is not known, rabies cases of north central Bayern and south-east Bayern. Kreise occurring before the Kreis reforms were allocated with a mean rabies frequency of 3.1 cases or more per proportionately to the appropriate present day Kreis. 100 km2 are found in eastern Nordrhein-Westfalen, The size of the Kreis unit ranged from 183 km2 to west Hessen, south Baden-Wurttemberg, and south 2860 km2 (mean, 1013 km2; standard deviation, Bayern. All other Kreise have an intermediate mean 446 kM2); the total area of the Federal Republic of frequency of 1.1-3.0 cases per 100 km2 per year. Germany is 248 144 km2. In terms of the relative importance of rabies, the south of the country plays the major role. The five Animal species southern Lander, Hessen, Rheinland-Pfalz, Saar- Species of animals diagnosed as rabid were not land, Baden-Wurttemberg and Bayern, cover 600o of named with any consistency in the Tierseuchenbericht the area of the Federal Republic of Germany but in until the second half of 1954 and the number of cases 1977-81, for example, they reported 79.3-88.30o of in unspecified species remained high for a number of all cases. years after this. For this reason total rabies cases are discussed rather than cases in foxes alone. The cases Epidemiological patterns of rabies in foxes usually accounted for 60-80% of the total The variation with time in the reported number of diagnosed cases. rabies cases per 100 km2 was plotted for each Kreis. Diagnosed cases in foxes have been estimated to Four distinct epidemiological patterns of rabies (first represent only 2-10O7o of the actual number (4). a Thus described by Jackson (7)) were identified: insignifi- the numbers of officially registered rabies cases, cant occurrence, low undulations, intermittent peaks, which furnish the data base of this study, can be con-- and high oscillations. Kreise with 15 years or less of rabies infection were difficult to classify, particularly a WACHENDORFER, G. The problem of rabies in the European those in south-east Bayern. region. WHO Conference on Surveillance and Control of Rabies, Frankfurt, 15-19 November 1977 (WHO unpublished document, Fig. 2 shows the geographical distribution of the ICP/VPH 001/6). four patterns of rabies occurrence in the Federal RABIES IN THE FEDERAL REPUBLIC OF GERMANY 101

Fig. 2. Geographic distribution of the four epidemio- Fig. 1. Geographic distribution of low, intermediate and logical patterns of rabies in the Federal Republic of high mean rabies frequencies: low mean frequency (light Germany: 1 - insignificant occurrence; 2- low undula- area), 0.01-1.0 cases per 100 km2 per year; inter- tions; 3- intermittent peaks; 4- high oscillations. mediate mean frequency (medium area), 1.-1-3.0 cases Areas with characteristics of more than one pattern are per 100 km2 per year; high mean frequency (dark area), shown, for example, as 42 or 12 where the subscript 3.1 or more cases per 100 km2 per year. indicates the secondary pattern.

Republic of Germany. Examples of the 4 patterns are per year. In the most representative Kreise of this given in Fig. 3, 4, and 5, which also show specific group, the background rabies occurrence is re- patterns with characteristics of more than one epi- peatedly interrupted by small ill-defined peaks, demiological type. though occasional peaks (not more than 2 in 20 years) The main features of each type, together with their of more than 5 cases per 100 km2 may occur. A geographic locations, are described below. number of Kreise show a more clearly defined peaking in rabies occurrence (see Fig. 3, pattern 24). 1. Insignificant occurrence: rabies is either com- The most typical examples of this pattern ofrabies are pletely absent (unrecorded), or there are a few spor- found in the east of Niedersachsen and the north of adic cases (not more than 3 reported cases per Bayern. In Schleswig-Holstein, the trend is to a 3-5 100 km2 per year), or there is one peak of not more year periodicity with clearly defined peaks and than 5 cases per 100 km2 per year over a period of 20 troughs. Well-defined peaks in rabies occurrence, at years (Fig. 3). This rabies pattern is found in the west irregular intervals, are also seen in a number of small of Niedersachsen, in north and west Nordrhein- areas in the centre of the country. Westfalen, and in south-east Bayern. 3. Intermittentpeaks in rabies occurrence are inter- 2. Low undulations: rabies is usually continuously rupted by a complete absence of the disease (Fig. 4). present at levels below 5 reported cases per 100 km2 In many Kreise, the peaks of rabies occurrence reach 102 H. C. JACKSON & L. G. SCHNEIDER

3, Bad DGr(kNim Awi ch Lbeel 20

t0 19

60 6S 70 7S 80 0 S0 0 66 70 7s Be S0 £0 s70 6 80 , irsterifeldbruc 12 1S Eceleed Cloppenburg 19 6q

I So0II ss Go 6s 70 75 8 e SS £0 6S£6 2i70 2576 ji80 .S 6e0 £6 70 76 8. Sio .Ss 0 .G6S 0 7s Be

2 Rhein-Meck,r Kreis Pei ne Meutadt1 -6lednab 3,, Restatt 16 ~~ ~~~~.. i...2 6 10

60 £65 70 7 £6 7o 7 Morthei. I ir chedreuth 10 00 6o 6S 6e £6 70 76 80 60 66 70 76 80 34 6o 6S G6 £6 70 76 80 60 £6 70 76 B0 Rheir-rTa1us Krei,

24 10, Oaru,6d Dielbug Segeberg "Of 10 15

Sso SS66 60lGO.GS66 7070 7S76 go80 £0 70

S0 60 £6 70 7S 9n Fig. 3. Patterns of insignificant occurrence and low undulations of rabies in the Federal Republic of Germany. Fig. 4. Patterns of intermittent occurrence of rabies 1 - typical insignificant occurrence: Aurich (Nieder- in the Federal Republic of Germany: 3i - typical sachsen), Wesel (Nordrhein-Westfalen), and Passau intermittent peaks: Bad Durkheim and Donnersberg- (Bayern); 12-insignificant occurrence with some kreis (Rheinland-Pfalz), Pfaffenhofen and Furstenfeld- characteristics of low undulations: Emsland and bruck (Bayern); 3i - typical intermittent occurrence Cloppenburg (Niedersachsen); 2-typical low undu- with possible change to high oscillations: Rastatt and lations: Peine and Northeim (Niedersachsen), Neustadt- Rhein-Neckar Kreis (Baden-Wuirttemberg); 34 - inter- Waldnaab and Tirschenreuth (Bayern); 24- low undula- mittent peaks with some characteristics of high oscil- tions with some characteristics of high oscillations: lations: Rheingau-Taunus-Kreis and Darmstadt Dieburg Segeberg (Schleswig-Holstein) and Hof (Bayern). (Hessen). considerably more than 5 reported cases per 100 km2 (Fig. 5). The interval between peaks in rabies occur- and are followed by an absence of recorded rabies for rence is usually 3-7 years. This pattern of rabies is 3-10 years. This pattern is found in Rheinland-Pfalz found in the central part of the country in eastern west of the river Rhine, Saarland, north-west Baden- Nordrhein-Westfalen, south-east Niedersachsen, and Wurttemberg, and a small part of central Bayern. In Hessen, excluding the southern tip. It is also found in south Hessen, two consecutive peaks are followed by a broad band across southern Baden-Wurttemberg a period of rabies absence and then a further two and Bayern. peaks (Fig. 4, pattern 34). Kreise in this group in A comparison of Fig. 1 and 2 reveals the close cor- Rheinland-Pfalz on the west bank of the Rhine and in relation between the distributions of the four epi- Schleswig-Holstein display only small peaks in rabies demiological patterns of rabies and the mean rabies occurrence (fewer than 5 cases per 100 kM2). frequency. 4. High oscillations: rabies is usually continuously Landscape characteristics present and peaks often reach more than 10 reported cases per 100 km2 per year. In a small number of In order to obtain a preliminary approximation of Kreise, there is a fairly clear periodicity in the number the landscape character in regions of the Federal of cases, though most show disturbances in regularity Republic of Germany with distinct patterns of rabies RABIES IN THE FEDERAL REPUBLIC OF GERMANY 103

4 21 7o forest, 280/o permanent grassland, and 39% Osterode arable land. Region 4, in Bayern, lies more than 15 is 200 m above sea level extending in parts over 500 m; Is there is 33070 forest, 21 0o permanent grassland, and 39% arable land.

S0 55 60 65 70 75 B0 55 6e 65 70 7S In both regions 5 and 6 of intermittent rabies there S.ew is a wide range of altitude, from under 100 m to over IS Is 500 m above sea level. There is a high percentage of 2s forest (34-38%), a low proportion of permanent grassland (about 157o), and a high percentage of arable land (33-34%7o). In comparison with the rest of "~~~~~~~'58 SS 60 65 71 7 10 55 70 75 ...... 7.... U0 a0 Lindm a.lodu , the country, there is a particularly high percentage 36 (7-8%) of land used for special purposes (vineyards 25 25 and market gardening). 23 20 1 Regions 7 and 8, with a rabies pattern of high oscillations, are topographically varied. Region 7, in 15 Hessen and Nordrhein-Westfalen, lies predominantly between 200 and 500 m above sea level. Forest covers 41%7o of the region but is concentrated in the centre So 60 65 7e 75 where much of the permanent grassland (17%7o of the whole region) is also found. This central region also nwburg-lieder6opf has the highest mean frequency of rabies. The area of Is Gosla high rabies occurrence in Bayern and Baden-Wurt- 01 temberg (region 8) is characterized by a high percentage of forest (35%7o) and of permanent grassland

60 65 (38/o). The whole area is more than 200 m above sea 1ll 55 U0 65 701 75 1N so SS 70 7S g0 level with more than three-quarters of the land lying above 500 m. Fig. 5. Patterns of high oscillations of rabies in the Federal Republic of Germany: 4-typical high oscil- There is a general tendency for a higher frequency lations: Osterode (Niedersachsen), Siegen and Mar- of rabies (patterns 3 and 4) to be found on high kischer Kreis (Nordrhein-Westfalen), Lindau-a. Bodensee ground with more than average forest cover. A lower (Bayern), Ravensburg and Waldshut(Baden-Wuirttem- frequency of rabies is found in areas with less forest berg); 42- high oscillations with some characteristics of cover, on both low and relatively high ground. There low undulations: Marburg-Biedenkopf (Hessen), Goslar is, in general, less topographical variation than in the (Niedersachsen). areas with a high frequency of rabies. occurrence, eight regions were examined (2 regions DISCUSSION for each rabies pattern) for altitude, forest, arable land, permanent grassland, special uses (vineyards and market gardening), and non-agricultural land. Many recent studies, including those by Gessler & The results'are summarized in Table 1. Spittler (5), Irmer & Schlegel (6), and Zimen (27) on Insignificant occurrence of rabies is found in two different aspects of rabies epidemiology, have been topographically distinct areas. In region 1 (north-west restricted in time, space, or both. In the present Niedersachsen and west Nordrhein-Westfalen), this survey, a more global approach has been attempted, pattern is very clearly restricted to land under 100 m rabies occurrence in a large area being looked at over above sea level. There is little forest (less than 100o) a long period of time. throughout the whole region; permanent grassland Because the Landkreis is an administrative and not predominates in the north of the region whereas in the a geographic unit, the patterns of rabies occurrence south there is more arable land and the Ruhr indus- are open to misinterpretation. It is possible, par- trial region. Region 2 in Bayern is very small (about ticularly in Landkreise with large topographical varia- 250 kM2). The whole area lies more than 200 m above tions, or with two or more types of habitat, such as sea level with 26%o forest, 3207o permanent grassland, moorland and arable land, that the observed rabies and 3507o arable land. pattern does not fully represent the situation, e.g., a The pattern of low undulations is also found in two pattern of low undulations could be the result of distinct areas of the country. Region 3 in Nieder- repeated peaks in different areas of a Kreis. Thus, sachsen is mostly under 100 m above sea level with interpretations must be made with caution. 104 H. C. JACKSON & L. G. SCHNEIDER

Table 1. Percentage distribution of land area according to altitude and land use for eight regions of the Federal Republic of Germany with four epidemiological patterns of rabies. 1 = Niedersachsen/Nordrhein-Westfalen; 2 = Bayern; 3 = Niedersachsen; 4 = Bayern; 5 = Rheinland-Pfalz, west of river Rhine; 6= Hessen/Baden-Wurt- temberg, east of Rhine; 7 = Hessen/Nordrhein-Westfalen; 8 = Baden-Wurttemberg/Bayern.

Insignificant Low Intermittent High occurrence undulations peaks oscillations Landscape 1 2 3 4 5 6 7 8

Altitude (m) 0-100 95 92 8 5 3 101-200 5 6 2 22 30 21 201-500 77 2 77 62 50 68 22 >500 23 21 8 15 8 78

Land use Forest 9 26 21 33 34 38 41 35 Permanent grassland 39 32 28 21 1 6 14 1 7 38 Arable 35 35 39 39 33 34 30 18 Special uses 5 1 4 2 8 7 3 2 Non-agricultural 12 6 8 5 9 7 9 7

Type 1, insignificant occurrence, is probably un- lation, which has thus been reduced to below the mistakable in that rabies occurrence is almost non- threshold level for continued transmission. existent. This pattern can only occur in areas where The restriction of the area of intermittent rabies rabies virus cannot easily persist, suggesting either a to Rheinland-Pfalz and the southwestern tip of low fox population density, a low fox-to-fox contact Nordrhein-Westfalen west of the river Rhine may be rate, or both. explained in terms of the river acting as a barrier to Type 2, low undulations, suggests an area of inter- fox movement. The reason for intermittent occur- mediate fox population density and fox-to-fox con- rence in Hessen and north-west Baden-Wurttemberg tact rate, where the population is never reduced below is less easy to explain in such terms. It has been the threshold for continued rabies transmission. suggested (H. Moegle, personal communication, Alternatively, it could be produced by a continuously 1982) that fox den gassing in the late 1960s and early circling pocket of rabies infection which, when 1970s reduced the fox population in this area to such averaged out over the Kreis, is seen as an undulating an extent that rabies could not persist. Indeed since curve. gassing was stopped, the pattern of rabies occurrence Type 3, intermittent peaks, appears to be the result appears to have changed (Fig. 4, pattern 3ii), strongly of a wave of rabies infection moving across an area. suggesting that control measures should be taken into In Rheinland-Pfalz west of the Rhine, the first wave account in the interpretation of all data. moved from east to west, and was followed by a Type 4, high oscillations, with repeated peaks of second, less marked, wave from west to east, and a rabies occurrence, often of 10 or more reported cases third wave from south-east to north-west. In the per 100 kM2, suggests high fox-to-fox contact rates, southern part of Hessen (with a pattern of two and high population densities with a rapid turnover. consecutive peaks or waves followed by at least 6 Since rabies is usually continuously present, there years almost complete absence and a further two must either be frequent inputs of rabies virus or con- consecutive peaks) the infection appeared to start stantly present foci of the virus. each time in the south-east. Although rabies infection At this level of descriptive study, it is difficult to occurs only at intervals, a high rabies frequency of 10 draw definite conclusions. Nevertheless it seems clear or more cases per 100 km2 is usually found during the that in the Federal Republic of Germany, little or no outbreaks. If this represents 2-l0O0o of actual cases, rabies can be expected on low-lying ground with a low true infection levels of 100-500 cases per 100 km2 or percentage of forest or high urbanization. Such areas, 1-5 cases per km2 are indicated. The absence of rabies with little surface cover and often a high water table, following these waves of infection suggests that the are probably not particularly suitable for foxes. disease has killed a large proportion of the fox popu- Heavy outbreaks of rabies seem to be confined to RABIES IN THE FEDERAL REPUBLIC OF GERMANY 105 higher altitude regions with above average forest The results are not directly comparable, however, cover. The areas of intermittent occurrence and high since low-lying land in Austria and Czechoslovakia oscillations of rabies are similar in some respects, refers mainly to land 200-500 m above sea level. having generally a wide range of altitude and a high The present study has several limitations. The percentage of forest cover. Although the barrier of rabies data base has a number of shortcomings and the Rhine may explain the intermittent rabies occur- the Kreis is an artificial geographic unit often com- rence west of the river, it is less easy to explain the prising a wide range of habitats. The habitat charac- occurrence of this pattern east of the Rhine; it may terization took into account only the most basic have been a result of fox control operations. features with many factors of possible importance to Krocza et al.b and Matouch & Polak (13) looked foxes being omitted. For example, only the per- at rabies occurrence and habitat in Austria and centage of forest was measured and not the distri- Czechoslovakia respectively. In both studies, the bution and type of forest. Finally, the study was results were similar to those obtained in the present restricted to a consideration of reported rabies cases study; in general, rabies occurrence was absent or and did not consider factors influencing these figures, sporadic on low-lying arable land while on high, such as fox den gassing and hunting. mountainous (at least 500 m above sea level), and Despite these limitations, there was clear local- more forested land, rabies occurrence was often high. ization of similar epidemiological patterns of rabies. Further, these geographically localized groups were b KROCZA, W. ET AL. Landscape and wildlife rabies in situated mainly in regions of distinct land use and Austria (1966-1979). WHO Consultation on Natural Barriers of Wildlife Rabies in Europe, Vienna, 28 April-i May 1981 (WHO topography, allowing cautious statements about unpublished report, Rab. Res./81.12). rabies occurrence and habitat.

RESUME

LA RAGE EN REPUBLIQUE FEDERALE D'ALLEMAGNE, 1950-1981: INFLUENCE DU CADRE NATUREL

On a etudie les statistiques de la rage pour la periode schemas epidemiologiques a e geographiquement loca- 1950-1981 en Republique federale d'Allemagne afin de lisee. Les regions ou la prevalence de la rage est insignifiante relever d'eventuelles differences de prevalence selon les sont presque toujours a moins de 100 m d'altitude et ne sont regions. Au niveau du Landkreis (unite administrative de recouvertes de forets que sur moins de 10% de leur super- 1013 km2 en moyenne), 1'evolution de l'incidence de la rage ficie. Les regions caracterisees par de fortes oscillations de la pour une superficie donnee suit les quatre chemas suivants: prevalence de la rage sont le plus souvent situees a plus de prevalence insignifiante, faibles ondulations, pics intermit- 200 m au-dessus du niveau de la mer et recouvertes de forets tents et fortes oscillations. La distribution de ces quatre sur en moyenne 35% au moins de leur superficie.

REFERENCES

1. ANDERSON, R. M. ET AL. Population dynamics of fox microbiology and infectious diseases, 5: 293-302 rabies in Europe. Nature (London), 289: 765-771 (1982). (1981). 6. IRMER, S. & SCHLEGEL, H. L. Fuchspopulation und 2. BAILEY, N. T. The mathematical theory of infectious Fuchstollwut in Niedersachsen unter Berucksichtigung diseases and its applications. 2nd ed., London, Griffin, der Landschaftsstruktur. Berliner und Munchener tier- 1976. airztliche Wochenschrift, 94: 359-362 (1981). 3. BOGEL, K. ET AL. Recovery of reduced fox populations 7. JACKSON, H. C. Rabies in the Federal Republic of in rabies control. Zentralblatt fur Veterinirmedizin, Germany. Comparative immunology, microbiology Reihe B, 21: 401-412 (1974). and infectious diseases, 5: 309-313 (1982). 4. BRAUNSCHWEIG, A. V. Ein Modell fOir die Fuchs- 8. KERSTEN, W. & ZINN, E. Die Bekimpfung der populationsdynamik in der Bundesrepublik Deutsch- silvatischen Tollwut durch Kombination der Begasung land. In: Zimen, E., ed., The red fox: ecology and von Fuchsbauen und der AbschuBforderung von behaviour (Proceedings of a Symposium on Fox Bi- Fuchsen. Deutsche tierdrztliche Wochenschrift, 78: ology, Saarbrucken, 1979). The Hague, Junk, 1980 175-178 (1971) pp. 97-106. 9. LLOYD, H. G. Wildlife rabies in Europe and the British 5. GESSLER, M. & SPITTLER, H. Relations entre population situation. Transactions ofthe Royal Society of Tropical de renards et limitation de la propagation de la rage Medicine and Hygiene, 70: 175-203 (1976). en Rhenaie-Westphalie. Comparative immunology, 10. LLOYD, H. G. The redfox. London, Batsford, 1980. 106 H. C. JACKSON & L. G. SCHNEIDER

11. LLOYD, H. G. ET AL. Annual turnover of fox popu- 20. STECK, F. & WANDELER, A. The epidemiology of fox lations in Europe. Zentralblatt fur Veterinarmedizin, rabies in Europe. Epidemiologic reviews, 2: 71-96 Reihe B, 23: 580-589 (1976). (1980). 12. MACDONALD, D. W. Rabies and wildlife. A biologist's 21. Times World Atlas. Edinburgh, John Bartholomew & perspective. Oxford, University Press, 1980. Son, 1968. 13. MATOUCH, 0. & POLAK, L. Rabies epizootiology and 22. Tierseuchenberichte der Bundesrepublik Deutschland. control methods in Czechoslovakia. Comparative Bonn, Amtliche Mitteilung des Bundesministers fur immunology, microbiology and infectious diseases, 5: Ernahrung, Landwirtschaft und Forsten, 1950-1981. 303-307 (1982). 23. WANDELER, A. ET AL. Rabies in wild carnivores in 14. MOEGLE, H. ET AL. EinfluB der Begasung der Fuchsbaue central Europe. I. Epidemiological studies. Zentralblatt auf die Fuchsdichte und die Wildtollwut in Baden- fur Veterindrmedizin, Reihe B, 21: 735-756 (1974). Wurttemberg. Berliner und Munchener tierdrztliche 24. WANDELER, A. ET AL. Rabies in wild carnivores in Wochenschrift, 84: 437-441 (1971). central Europe. II. Virological and serological examin- 15. MOEGLE, H. ET AL. Zur Epidemiologie der Wildtier- ations. Zentralblatt fur Veterinarmedizin, Reihe B, 21: tollwut. Untersuchungen im sudlichen Teil der Bundes- 757-764 (1974). republik Deutschland. Zentralblatt fur Veterindr- 25. WANDELER, A. ET AL. Rabies in wild carnivores in medizin, Reihe B, 21: 647-659 (1974). central Europe. III. Ecology and biology of the fox in 16. MULLER, J. The effect of fox reduction on the relation to control operations. Zentralblattfur Veterin- occurrence of rabies. Observations from two outbreaks armedizin, Reihe B, 21: 765-773 (1974). of rabies in Denmark. Office International des 26. World Atlas of Agriculture. Istituto de Agostini, Epizooties, Bulletin, 75: 763-776 (1971). Novara, Vol. I (and map volumes), 1969. 17. OSTHOFF, F. & GROTSCH, W. Zur Tollwutlage in Bayern 27. ZIMEN, E. The effect of rabies on different fox popu- nach Fuchsbaubegasung neben vermehrtem Abschu13 lations in the south west of the Federal Republic of von Fuchsen. Tierarztliche Umschau, 27: 274-276 Germany. Comparative immunology, microbiology (1972). and infectious diseases, 5: 257-264 (1982). 18. PIENING, C. & ZIMMERMANN, T. Tollwut im Lande 28. ZINN, E. Die Bekampfung der Wildtollwut unter Schleswig-Holstein. Deutsche tierarztliche Wochen- besonderer Berucksichtigung der Verdunnung der schrift, 76: 393-396 (1969). Fuchspopulation durch Begasung der Fuchsbaue. 19. STECK, F. Rabies, the European situation. Veterinary Deutsche tierarztliche Wochenschrift, 73: 193-197 record, 83 (Clinical Supplement Section): i-iv (1968). (1966).