Structure of natural foci of zoonotic cutaneous leishmaniasis and its relationship to regional morphology*

Bull. Org. mond. Sante| 1971, 44, 577-584Bull. Wid Hith Org. Structure of Natural Foci of Zoonotic Cutaneous Leishmaniasis and its Relationship to Regional Morphology* V. M. NERONOV I & P. D. GUNIN 2 Zoonotic cutaneous leishmaniasis is still a public health problem in Central Asia. To control the outbreaks, different control measures are required in different regions and comprehensive information is required about natural foci. The term landsaft, used by Soviet geographers to denote particular geographical regions, is defined and this concept is used in examining the natural focality of zoonotic cutaneous leishmaniasis in the south of the Turkmen SSR. The main reservoir species in this area was Rhombomys opimus, and the disease was transmitted mainly by Sergentomyia arpaklensis, Phlebotomus papatasi, and Phlebotomus caucasicus. The burrows of R. opimus were the main shelters and breeding places of the sandflies, but infection was not transmitted equally in all burrows. It was known that the distribution of sandflies within the burrows was influenced by the humidity in the different parts of the burrow and a survey showed that the highest rate of infection of gerbils occurred in the burrows in those areas with the highest subsoil moisture content. Studies of the prevalence of zoonotic cutaneous leishmaniasis among people in the settlements of the Murghab oasis showed that the years with the highest infection rate were also years with slightly higher rainfall and lower air temperatures in this area. Zoonotic cutaneous leishmaniasis is a typical obligate transmissive infection with natural focality. In a number of areas of Central Asia the disease is still a problem for the local public health services (Rodjakin et al., 1967; Serebrjakov & Ipatov, 1967). The requirements for the elimination of mass out- breaks of this disease in man include comprehensive information of natural foci and the application of different epidemic control measures in different regions. The task can be solved only if there is a clear understanding of the main idea of the " natural * This paper is based on material presented at a travelling seminar, held in the USSR in 1967, on the problems of leishmaniasis and its control: the seminar was organizedjointly by the Ministry of Health of the USSR and the World Health Organization. 'The Gamaleja Institute of Epidemiology and Micro- biology, Moscow, D-98, USSR. Present address: Ecologist, Division of Research in Epidemiology and Communications Science, World Health Organization, Geneva, Switzerland. 'The Institute of Deserts, Academy of Sciences of the Turkmenian SSR, Ashkhabad, USSR. focus ", so that natural foci can be identified in a given area. The first definition of a natural focus was given by E. N. Pavlovsky in 1939. It has undergone cer- tain improvements and is now frequently stated as follows: a natural focus is a part of a homogeneous geographical area in which characteristic relation- ships between the causal agent, the donor animal, the causal-agent recipients, and the vectors have been established in the course of evolution in an environment that is favourable or at least not inhi- bitory to the circulation of the causal agent (Pavlov- sky, 1955). Voronov (1967) described a zoonotic focus as the smallest part of an area (usually a natural or cultivated land§aft,l sometimes a group of land§aft) that incorporates a long-lasting popula- tion of the causal agent with the supporting popula- tions of vertebrate hosts and arthropod vectors or I The term landsaft is used by Soviet geographers to de- note particular geographical regions as defined on p. 578. 2670 - 577 578 V. M. NERONOV & P. D. GUNIN other xeno-organisms, while no causal agent from outside is introduced. A comparison of these defini- tions shows that certain features of the landsaft as a whole as well as certain factors of the environment are of great importance for the natural foci of disease. However, the lack of knowledge of the achievements of landsaft science on the part of medical workers and biologists has resulted in the fact that the term landsaft has been used in a general way to define a geographical complex, taking no account of its volume and taxonomic importance. Owing to this different approach, unequal sections of a territory are often considered as natural foci, ranging from a burrow or a cave to a vast desert of Middle Asia. This difference in interpretation has led to misunderstanding among investigators and to difficulties in the summarizing of data, which is necessary before preventive measures can be planned. To clarify this point, further consideration will be given to the opinions of landfaft scientists and to the features of the landsaft morphology. There are many diverse definitions of a land§aft, but the majority of geographers in the Soviet Union agree on an interpretation according to which a landsaft is first and foremost a specific territorial unit, and secondly a geographical complex that often consists of numerous elementary physical- geographical units (Solntsev, 1948, 1961; Isacenko, 1961, 1965). Isacenko (1965) defined a landsaft as a genetically isolated part of a province, zone, or any other major regional unit that is characterized by homogeneity, in terms of climate and geology, and that has an individual morphological structure. Annenskaja et al. (1962) regarded a landsaft as a genetically homogeneous complex that has the same geological foundation, one type of relief, and an identical climate and that consists of a collection of principal and secondary units that are dynamically related and regularly repeated in space, and that are peculiar only to this landsaft. The area of a single landsaft usually equals several hundred or several thousand square kilometres and most of them can be divided into simpler geogra- phical units, of which the basic ones are the facija and the uro&i§&e. A facija is the smallest physical- geographical unit that is characterized by homo- geneous conditions of situation and locality and by one biocoenosis. A uroc6is'ce is an interrelated system of several facija connected with individual convex or concave vrelief forms, or with flat interfluvial zones on a homogeneous substratum. Methods of distinguishing a landsaft and of studying its morpho- MI C4 EJ7 E:3 EM6 (D9 WMO 10054 Fig. 1. Schematic map of the expedition area and the rate of infection in Rhombomys opimus with the zoonotic type of cutaneous leishmaniasis in 1963 a 1. First and second terraces of the Murghab river 2. UroJiMe on the hills 3. Second terrace with drifted sand 4. Third terrace 5. Slope of the left parental bank 6. Slope of the right parental bank 7. Ridgy-hummocky-sand Iand§aft 8. Gently undulating sand land§aft 9. The black sectors indicate the percentage of infected animals with clear clinical manifestations a Each point of survey containeda 20 dult animals. logical structure have been described in detail by Isacenko (1961, 1965), Annenskaja et al. (1962), and Vidina (1962). This paper reviews the results of studies of land- s,aft morphology related to the natural focality of a zoonotic type of cutaneous leishmaniasis carried out by a complex expedition of the Gamaleya Institute of Epidemiology and Microbiology (Moscow) in the south of Soviet Turkmenia.1 The expedition surveyed a total area of about 50 km2 situated in the neighbourhood of Imam-Baba village straddling the middle reaches of the Murghab river. Within the surveyed area, sections of three landsaft are represented: (1) a ridgy-hummocky sand landsaft, (2) a valley landfaft of the middle reaches of the Murghab river, and (3) a gently undulating sand landsaft (Fig. 1). All three landsaft are well identified by their genesis, their relief, their soil and vegetation cover, and by their morphology. 1 Dr V. M. Saf'janova, Dr Ju. A. Dubrovsky, Dr V. N. V'jukov, Dr E. M. Belova, and students of the Moscow Uni- versity (departments of Biology and Geography) also partic- ipated in collecting the material. NATURAL FOCI OF ZOONOTIC CUTANEOUS LEISHMANIASIS AND ITS REGIONAL MORPHOLOGY At the boundary of the valley landsaft with the sand landsaft, the sands have been noticed to slide and drift on to the terrace surface and peculiar " train " urocise have been formed. They are quite narrow (not exceeding 30-40 m) and it is impossible to show them on the small-scale schematic map. In the vicinity of Imam-Baba all the species of mammal occur that have been recorded in the epizootics ofcutaneous leishmaniasis, includingRhom- bomys opimus Licht., Meriones lybicus Licht., M. meridianus Pall., Spermophilopsis leptodactylus Licht., Hemiechinus auritus Gmel., Mustela nivalis L., and Vormela peregusna Gield. However, in our surveys in 1962-65 infection was found only among Rhombomys opimus (Saf'janova et al., 1965) and this species is considered to be the main reservoir of the causal agent of the zoonotic cutaneous type of leish- maniasis in this area. The burrows of Rhombomys opimus were the main shelters and breeding places of 9 species of sandfly: Phlebotomus papatasi Sc., P. sergenti Parr, P. mon- gonlensis Sint., P. caucasicus Marz., P. andrejevi Shak., P. chinensis Neust., Sergentomyia arpaklensis Perf., S. graecovi Khod., and S. clydei Sint. The dominant species as regards the population density, was S. arpaklensis, with P. papatasi and P. caucasicus present as subdominant species. The rest of the species were present only in small numbers. An analysis of the sandfly population in the different areas of the valley landsaft showed that the dominant species were P. papatasi and S. arpaklensis, whereas P. caucasicus was dominant in the sandy desert landsaft. A marked reduction in sandfly density was noted in the sandy desert landsaft compared with the valley landsaft (Saf'janova & V'jukov, 1967). The rate of infection of the 3 dominant sandfly species, P. papatasi, S. arpaklensis and P. caucasicus, with the parasite was determined by preparing smears from the gut of female sandflies and by isolating living leptomonads in culture. In 1964 the average rates of infection with these three organisms were 4.6 %, 7.3 %, and 2.6% respectively. Examination of the households in Imam-Baba showed that about 50% of the indigenous population had had zoonotic cutaneous leishmaniasis at one time. Fresh cases occur annually among children and among new- comers to the village (Belova & Saf'janova, 1966). The above data demonstrate that in the vicinity of Imam-Baba there exists a circulation of the causal agent of zoonotic type of cutaneous leishmaniasis and that under certain conditions man becomes infected with it. Thus it is true to say that natural focality exists in this area. However, with due regard to the morphology of the landkaft within the expedi- tion area there arises the following question: What is a natural focus here? Is it an individual burrow, a urocisce or the whole territory? We shall try to throw some light on the subject. It has already been noted that the burrows of R. opimus are the main shelters and breeding places of the sandflies. Evidently here they transmit the leishmaniasis parasite from one animal to another. The burrows of R. opimus occur in all parts of the expedition areas; however, their density and their average size vary. V'jukov (1967) established that the composition of the sandfly fauna and their popula- tion density also varied greatly between neighbouring burrows and that in some cases, as in the burrows in the tugai near the Murghab river, there were no sandflies present. Studies on small plots showed that leishmaniasis-infected gerbils did notX occur in all burrows (Fig. 2). Dr Ju. A. Dubrovsky has reported that frequently the causal agent was not transmitted even when infected and noninfected animals shared the same burrow for 3-4 months. On the basis of the data obtained the burrows of R. opimus were divided into two groups: the favour- able and the unfavourable ones as regards the circula- tion of the leishmaniasis causal agent. The principal criterion of an independent natural focus is that long-term circulation of the causal agent should occur entirely within the focus (Kuce- ruk, 1959; Voronov, 1967). It is clear that an epizootic process in an individual burrow cannot last for long as the gerbils change burrows even within one season. During the periodic reductions in population density many burrows stay uninhabi- ted by warm-blooded animals for a long time. Thus it would be wrong to classify a burrow as a natural focus. It can be considered only as an elementary focus-part of the larger natural focus. It is rather difficult to establish the minimum area capable of sustaining the causative agent. Long- term studies on this point are to be conducted in various areas and these will try to assess the migra- tion abilities of the gerbils and sandflies. Observa- tions conducted for a number of years in the expedi- tion area as well as in the Tedzhen-Murghab inter- fluvial region show that the area of a landsaft is quite sufficient to retain the causal agent, whereas an individual urosisce within a landfaft may be completely free of gerbils at certain times. Thus the land.aft can be considered as the natural focus in this instance. 579 V. M. NERONOV & P. D. GUNIN Wi0 10053 Fig. 2. Morphological structure of a plot in the valley land§aft and distribution of Rhombomys opimus infected with the zoonotic type of cutaneous leish- maniasis A. B. C. D. E. F. G. H. Second terrace Slope of third terrace Depressions of the third terrace Elevated plots of the third terrace Drifted sand ridges Takir-like plots Colonies (burrows) of Rhombomys opimus Figures indicate the total number of animals shot in the given colony and the black dots show how many of them were infected. In other words, the expedition area around Imam- Baba comprises parts of 3 natural foci of the zoo- notic type of cutaneous leishmaniasis-a natural focus in the valley land&aft and two foci in the sandy desert landsaft. The range of sandfly abundance, the composition of the sandfly fauna, the different rates of gerbil infection, as well as the proportion of clinical examples of gerbil leishmaniasis (Dubrov- sky et al., 1966), the distribution of elementary foci, and the dynamics of the epizootic processes all show that these landsaft are relatively independent foci. Epidemiological investigations have also shown that the foci are different as regards the danger of infection to man: fresh cases occur continuously in the river valley whereas they do not occur over most of the interfluvial zone. The distribution of epizootics of the zoonotic type of cutaneous leishmaniasis in the central part of the Tedzhen-Murghab interfluvial zone confirms the va- lidity of the landsaft approach in establishing the natural foci of the disease. The rate of leishmaniasis infection in Rhombomys opimus has been found to vary in areas with a similar population density of gerbils and with populations of sandflies having similar composition and abundance (P. caucasicus dominant) (Fig. 3). The distribution of infected animals over the territory also varied in this zone (Dubrovsky et al., 1967; Saf'janova & V'jukov, 1967). As noted above, the burrows of Rhombomys opimus favourable to the circulation of the leishma- niasis parasite are unevenly distributed over the ter- ritory of a natural focus. We agree with Kuceruk (1959, 1960) and think it necessary to determine " plots of focality " as structural units within natural foci (mezofoci, as defined by Fenjuk, 1954) in which the causative agent occurs most frequently, as well as " plots of infection export" where the causative agents live for a short time only during mass epi- zootics. The train urocisce and certain sub-urocisce on the third terrace are good examples of " plots of focal- ity" in the valley land§aft (Fig. 1 and 2). Colonies of Rhombomys opimus on the banks of small canals on the irrigated fields on the second terrace as well as among the tugai bushes can be classified as plots of infection export. On the sandy desert landsaft, the areas that are favourable for the existence of the whole epizootic triad are concentrated in the uroci- sce of inter-ridge depressions, whereas the peaks of the ridges appear to be plots of infection export. All the data mentioned in this paper, including the schematic maps, clearly demonstrate the influ- ence of landsaft morphology on the structure of natural foci of zoonotic cutaneous leishmaniasis. It is not clear yet what the principal factors are in the distribution of infected animals within the landsaft unit. This is particularly true for the areas of the Tedjen-Murghab interfluvial zone that have similar sandfly fauna and diffuse settlements of gerbils with a high density of burrows. Professor Latysev (1947) said that the difference in gerbil infection could hardly be related only to the features of sandfly fauna. He thought it more likely that the microclimate of 580 NATURAL FOCI OF ZOONOTIC CUTANEOUS LEISHMANIASIS AND ITS REGIONAL MORPHOLOGY Fig. 3. Rate of infection of Rhombomys opimus with the zoonotic type of cutaneous leishmaniasis in different landsaft of the Tedzhen and Murghab interfluvial zone 1. 2. 3. 4. 5. 6. Land§aft of the Tedzhen ancient delta Undulating-hill-sand land5aft Ridgy-hummocky-sand landsaft Elevated undulated plain landsaft with old outliers and ancient lake depressions Hill and foothill landfaft The black sections of the circles show the percentage of animals with clear clinical manifestations of the zoonotic type of cutaneous leishmaniasis. A total of 967 adult animals was examined the burrows located on various plots is not always favourable for the development of leishmania in vector organisms. Microclimate is the most impor- tant feature of the different parts of a landsaft unit, and we conducted a number of surveys on the effect of microclimate on epizootics. Studies of the microclimate in the burrows of Rhombomys opimus are rather time-consuming. Moreover, the microclimate is very variable in the different parts of a burrow (V'jukov, 1967). P. papa- tasi prefers the deeper parts of burrows where the microclimate is more stable and humid, whereas S. arpaklensis inhabits mainly the upper parts of burrows where there is cyclic variation of the micro- climate and a lower humidity. On the other hand, the microclimate of a burrow is largely determined by the type of subsoil and its water-holding char- acteristics. Thus a general determination of micro- climate can be made by the ordinary field pro cedure of estimating subsoil moisture content by weighing. A hand auger is very useful for quick sampling of soil from different parts and precisely marked hori- zons for moisture content tests. The data on subsoil moisture content in different parts of the survey area are shown in the accom- panying table. The subsoil moisture content at a depth of 1.5 m was highest in the valley landsaft. Within this landsaft the humidity was highest in the urocisce of the second and third terraces above the flood plain. The rate of infection of gerbils was also highest in these places (Fig. 1). The moisture content of the subsoil varies greatly within a season as well as from year to year and the pattern of change is different in the different land- s§aft. According to measurements made in the autumn, high precipitation in the winter of 1963-64 brought about a noticeable increase in moisture con- tent only in the sands of the right bank and along the train of the right parental bank. In the rest of the urocisce of the valley landsaft and the ridgy- hummocky sand land§aft of the left bank the subsoil moisture content was a little lower than in 1963. With the increase of subsoil moisture content the epizootic intensity of the zoonotic type of cutaneous leishmaniasis also increased (Saf'janova et al., 1965). The natural foci of the ridgy-hummocky sands and of the elevated plain with old outliers and lacustrine troughs in the Tedjen-Murghab interfluvial zone 581 V. M. NERONOV & P. D. GUNIN Subsoil humidity, at a depth of 1.5 m, in the vicinity of Imam Baba in 1963 and 1964 a Typeof landsaft b 1963 1964 Ridgy-hummocky-sand landfaft 3 km from the parental bank 2.8 ? 1 km from the parental bank 2.9 2.7 Along the edge of the parental bank 3.1 2.9 Valley landsaft of Murghab Left bank train 4.5 2.5 Second terrace with drifted sand ? 2.9 Long-fallowed land on the second terrace 13.0 10.6 Third terrace 12.8 11.9 Right bank train 3.3 5.1 Gently undulating sand land§aft Along the edge of the parental bank 1 km from the parental bank 3 km from the parental bank a Measurements were made in both years during August, at more than four points in each area. b The term landfaft is used by Soviet geographers to denote particular geographical regions as defined on p. 578. have shown correlation between subsoil moisture content and rate of leishmaniasis infection in Rhom- bomys opimus. In the summer of 1966, during the survey of natural foci of the zoonotic type of cutane- ous leishmaniasis in the Kara-Kum Canal area, it was established that on sandy desert landsaft, within the area affected by infiltration of water from the canal, the rate of infection of gerbils was higher than in the areas beyond the limits of infiltration (Dubrovsky et al., 1969). It is thus clear that the moisture defi- ciency in the desert areas in the southern part of Soviet Turkmenia significantly affects the relation- ship between members of the epizootic triad of the zoonotic type of cutaneous leishmaniasis. Studies of the prevalence of zoonotic cutaneous leishmaniasis among the inhabitants of the settlements of the Murghab oasis (data for 1951-61) have shown that the years with the highest infection rate (1953 and 1957) were also years of slightly higher rainfall and lower air temperatures in summer and autumn in this area (Neronov & Gunin, 1966). Further investigations carried out by one of us (P. D. G.) in the other parts of Turkmenia have provided new data that show the importance of land- saft study of natural foci of leishmaniasis. It was discovered that in certain landsaft there are only urocisce with weak epizootics; others contain only urocisce with intensive epizootics; and a third group contains urocisce with both types of epizootics. Such combination of different urocisce on the terri- tory of one landsaft gives a picture of spatial distribu- tion of an epizootic that is highly characteristic. Analysis of the data for the whole of Turkmenia showed that outbreaks of zoonotic cutaneous leish- maniasis occurred only in those landsaft with loamy- clay soils that have sources of water in addition to natural rainfall, perhaps from irrigation canals or from shallow subsoil waters (Gunin, 1969). Rotgild (1969) reported studies on the relation between the landsaft of ancient valleys and deltas and the location of natural foci of plague in the territory near the Aral Sea. In these studies it should be emphasized that the difference in the distribution of R. opimus and the epizootics of plague was discovered only after the mapping of settlements of rodents and the land&aft mapping. These data show that it is useful to take into account the distribution of different landsaft when mapping the epidemiologically dangerous plots of focality and the individual natural foci, and when forecast- ing epidemic outbreaks, not only for zoonotic cuta- neous leishmaniasis but also for other diseases with natural focality. We think that for success in this field it is necessary for the work to be carried out by teams including not only medical workers and biologists but experts in geography as well. 582 NATURAL FOCI OF ZOONOTIC CUTANEOUS LEISHMANIASIS AND ITS REGIONAL MORPHOLOGY 583 RESUME LA STRUCTURE DES FOYERS NATURELS DE LEISHMANIOSE CUTANEE ZOONOTIQUE ET SES RAPPORTS AVEC LA MORPHOLOGIE DES REGIONS La leishmaniose cutan&e zoonotique represente toujours un probleme de sante publique en Asie centrale. Pour combattre les flambees epidemiques de la maladie, il est necessaire d'appliquer des methodes de lutte differentes suivant les endroits et de disposer d'un maximum d'infor- mations sur ses foyers naturels. Les auteurs definissent le concept de < landfaft)) utilise par les geographes sovietiques pour decrire une region geographique donnde et mettent cette notion a profit pour etudier les modalit6s de la repartition de la leishmaniose cutanee zoonotique dans le sud du Turkmenistan. Dans ce territoire, Rhombomys opimus apparait comme le principal r6servoir de la maladie qui est transmise essentiellement par Sergentomyia arpaklensis, Phleboto- mus papatasi et Phlebotomus caucasicus. Ce sont surtout les terriers de R. opimus qui servent d'abri et de gite aux simulies, mais la transmission de l'infection ne se fait pas avec une intensite egale dans tous les terriers. On a observe que la repartition des simulies etait influencee par le degre d'humidit6 regnant dans les diff& rentes parties du terrier; d'autre part, une enquete a montre un taux maximal d'infection chez les gerbilles occupant des terriers situes dans les regions a sous-sol particulierement humide. L'etude de la prevalence de la leishmaniose cutan6e zoonotique dans des collectivites humaines de l'oasis de Murghab a revele que les taux d'infection etaient parti- culierement eleves pendant les annees caracterisees par une pluviosite legerement plus forte et une temperature legerement plus basse. REFERENCES Annenskaja, G. N., Vidina, A. A. et al. (1962) [Morpho- logical structure of geographical landscapes], Moscow State University (in Russian) Belova, E. M. & Saf'janova, V. M. (1966) Zdravoohr. Turkmen. (Ashkhabad), 10, No. 81, pp. 22-25 (in Russian) Dubrovskij, Ju. A., Belova, E. M. & Neronov, V. M. (1966) Med. Parazit. (Mosk.), 3, 275-281 (in Russian, with English summary) Dubrovskij, Ju. A., Neronov, V. M., Saf'janova, V. M., Gunin, P. D., Belova, E. M. V'jukov, V. N. (1967) Zool. i., 46, No. 4, pp. 472-480 (in Russian, with English summary) Dubrovskij, Ju. A., Gunin, P. D., Komarova, L. V. & Neronov, V. M. (1969) Zool. 2., 48, No. 3, pp. 425-435 (in Russian, with English summary) Fenjuk, B. K. (1954) In: [Abstracts of papers presented at the Third Ecological Conference], Kiev, Part III, Kiev University, pp. 186-192 (in Russian) Gunin, P. D. (1969) [Landscape features of natural foci of cutaneous leishmaniasis of Eastern Turkmenija]. Synopsis of thesis, Moscow (in Russian) Isacenko, A. G. (1961) [Geographical mapping], Part III, Leningrad University (in Russian) Isacenko, A. G. (1965) [Principles of landscape study and geographical subdivision], Moscow, The Higher School Publishing House (in Russian) Kuceruk, V. V. (1959) Med. Parazit. (Mosk.), 6, 658-667 (in Russian, with English summary) Ku6eruk, V. V. (1960) [Mammals of Palaearctic steppes, natural foci of plague in the steppe zone and some theoretical questions ofnaturalfocality of this infection], Synopsis of thesis, Moscow (in Russian) Latysev, N. I. (1947) In: Kozevnikov, P. V., Dobro- tvorskaja, N. V. & Latysev, N. I. [Studies of cutaneous leishmaniasis], Medgiz (in Russian) Neronov, V. M. & Gunin, P. D. (1966) In: [Microbiology, immunology, epidemiology, natural focality of diseases], Proceedings of a conference in the Gamaleja Institute, Moscow, pp. 99-101 (in Russian) Pavlovsky, E. N. (1955) In: [Natural focality of human diseases and regional epidemiology], Medgiz, pp. 36-49 (in Russian) Rodjakin, N. F., Eresov, M. E., Dobrzanskaja,' R. S. (1967) In: [Proceedings of the first inter-republican conference of Republics of Middle Asia and the Kazakh SSR on the problem of the main parasitic diseases, their prevention and treatment], Tashkent, Medicine, pp. 40-41 (in Russian). Rotsild, E. V. (1969) Problemy osobo opasnyh infekcij (Saratov, USSR), 1, 48-53 (in Russian) Saf'janova, V. M., Dubrovskij, Yu. A., Neronov, V. M., Belova, E. M., V'jukov, V. N. & Gunin, P. D. (1965) In: [Methods of medical-geographical investigations], Moscow, Geographical Society of USSR, pp. 208-222 (in Russian) Saf'janova, V. M. & V'jukov, V. N. (1967) Zool. 2., 46, No. 3, pp. 375-383 (in Russian, with English summary) 584 V. M. NERONOV & P. D. GUNIN Serebrjakov, V. A. & Ipatov, V. P. (1967) In: [Proceed- ings of the first inter-republican conference on Repubrlics of Middle Asia and the Kazakh SSR on the problem of the main parasitic diseases, their prevention and treat- ment], Tashkent, Medicine, pp. 44-46 (in Russian) Solncev, N. A. (1948) In: [Transactions of the Second All-Union Geographical Congress], vol. I, pp. 258-269 (in Russian) Solncev, N. A. (1961) Vestn. Mosk. Univ., Geogr., 3, 53-57 (in Russian) Vidina, A. A. (1967) Methods for large-scale field landscape investigations, Moscow State University (in Russian) V'jukov, V. N. (1962) In: [Proceedings of the first inter- republican conference of Republics of Middle Asia and the Kazakh SSR on the problem of the main parasitic diseases, their prevention and treatment], Tashkent, Medicine, pp. 16-18 (in Russian) Voronov, A. G. (1967) Vestn. Mosk. Univ. Geogr., 2, 3-16 (in Russian)