Commensal and wild rodents in an urban area of Argentina

International Biodeterioration & Biodegradation 52 (2003) 135 – 141

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Commensal and wild rodents in an urban area of Argentina E. Castilloa , J. Priottoa , A.M. Ambrosiob , M.C. Provensala , N. Pinib , M.A. Moralesb , A. Steinmanna , J.J. Polopa;∗ a Departamento b Instituto

de Ciencias Naturales, Universidad Nacional de Ro Cuarto, Agencia Postal No. 3, X5084ZAB Ro Cuarto, Cordoba, Argentina Nacional de Enfermedades Virales Humanas (INEVH) “Dr. Julio I. Maiztegui”, Monteagudo 2510, 2700 Pergamino, Buenos Aires, Argentina

Abstract The aim of this study was to determine the rodent species, distribution, and abundance in an urban area, in relation to epidemiology risk or damage, so as to elaborate a control program. The /rst sampling was done between May and July of 1998 on 31 vacant lots, 5 rubbish dumps, 15 stream banks, 18 railway banks and 28 vacant areas. Between August 1999 and June 2000 seasonal samples were taken in the same habitats. At each capture site 20 snap traps and 10 live traps were installed. Of 1253 animals captured, 74% were commensal rodents (Mus domesticus, Rattus rattus and Rattus norvergicus) and 26% were wild rodents (Calomys musculinus, Akodon dolores, A. azarae and C. venustus). M. domesticus was the population that numerically predominated in every sampled habitat. C. musculinus was the second most abundant species and its distribution was related to open space (vacant areas, railway banks, stream banks and rubbish dumps). The basic information found by this work will allow us to consider and measure the risk of a possible human infection in a speci/c area. Thus, human diseases can be prevented by controlling rodent reservoirs and/or by avoiding contact between rodents and humans. ? 2003 Elsevier Ltd. All rights reserved. Keywords: Rodents; Zoonoses; Urban area

1. Introduction Rodent pests in urban and rural areas have been present in di;erent situations in the world (Rowe, 1973; Davis, 1977; Fiedler et al., 1991; Frantz and Davis, 1991; Fall and Jackson, 1998; Dolbeer, 1999). In general, most of them in@ict economic losses and public health problems. However, rodents have not been paid the necessary attention considering the risk and loss that they produce. The economic losses in surveyed countries were estimated in million of dollars (Dolbeer, 1999). Surveys about food loss from rodents consumption and contamination vary considerably between countries depending on the rodent species present, packing techniques utilized, time and type of storage, as well as methods of assessing loss (Myllymaki, 1975; Brooks and Rowe, 1987; Frantz and Davis, 1991; Hone, 1994). In relation to public health, the role of rodents in the transmission of diseases, that have historically @agellated human kind is well known (Arata, 1975; Gratz, 1994). Rodents act as the infection agents of many diseases, and, in the recent years, there has been a permanent epidemiological growth in the ∗

Corresponding author. Fax: 0+54-358-4676230. E-mail address: [email protected] (J.J. Polop).

0964-8305/03/$ - see front matter ? 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0964-8305(03)00033-7

number of zoonoses bound to rodents (Mills and Childs, 1998). In many countries, and due to lack of studies to establish either control programs or reduction of rodent population and to estimate risk or losses have not been possible. Only control activities on rodents in reduced environment and times were performed. Thus, speci/c treatments were made, and many animals were eliminated by poisoning, but quickly new animals move to occupy the vacant area and exploit the resources of not treated areas. These campaigns are an expensive way of “harvesting” some rodents, and usually they are not useful for eliminating or controlling population that endanger or damage people’s economy or public health. On the other hand, most of the materials and strategies of control have been designed to be used in developed countries, and generally they are not transferable to developing countries (Fiedler et al., 1991; Singleton and Brown, 1999). Rodent control includes ecology, bionomics and distribution of the rodent species and the way in which contact among man, stored products and rodents occurs (Frantz and Davis, 1991). Consequently, base information is a priority to decide whether intervention is necessary and to value what type of intervention is more adequate, and when and where it is applicable (Drummond, 1970; Kaukeinen, 1979, 1984;

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Davies and Jackson, 1981; Jackson, 1984, 1998; Frantz and Davis, 1991). As di;erent rodent species have di;erent reactions to control methods, local studies and evaluations are necessary before producing a recommendation for any speci/c problem. In general, the rodent species reported as urban are mainly commensal: Norway rat (Rattus norvegicus), roof rat (Rattus rattus) and house mouse (Mus musculus). These species were generalized considered their habitats and food requirements. However, in Argentina, due to the characteristics of many urban areas, the possibility of cohabitation of introduced species with native species of South America has not been investigated. The aim of this study was to determine rodent species, distribution, and abundance in the urban area of RNOo Cuarto city, CNordoba Province, Argentina, in relation to epidemiology risk or damage, so as to elaborate a control program. 2. Materials and methods The city of RNOo Cuarto is situated in the southwest of the province of CNordoba, Argentina, between the 33◦ 01 and

33◦ 10 S, and the 64◦ 15 and 64◦ 22 W. It has a surface area of 4698 ha and approximately 150,000 inhabitants. Service activities are predominant with low industrial activity. In the city, sample habitats were identi/ed as: vacant lots, rubbish dumps, stream banks, railway banks and vacant areas. Lands without structures, but adjacent to them, and with an approximate surface area of 500 m2 were de/ned as vacant lots. Vacant areas were areas located in the urban area without structures, and with a minimum surface of 5000 m2 . Vacant lots and vacant areas were dominated by weedy vegetative species. The stream banks were represented by the north and south side of the RNOo Cuarto river, that crosses the city from northwest to southeast (6800 m long), and by a stream of approximate 2500 m long (Fig. 1). The rubbish dumps were areas where trash had accumulated for ¿ 3 months, located on the river borders. The railway banks were longitudinal habitats along both sides of the railway, and with weed cover. The /rst sampling was done between May and July of 1998 during 8 weeks, on 31 vacant lots, 5 rubbish dumps active, 15 stream banks, 18 railway banks and 28 vacant areas. The capture of animals at a sampling site was done during two consecutive nights in each week. The trap e;ort

Fig. 1. Site of sample distribution in the city of RNOo Cuarto between May–July 1998 and August 1999 –June 2000. Each dot shows the site of sample.

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was of 5820 trap nights (97 lines×30 traps) during the study period. Subsequently, between August 1999 and June 2000 seasonal samples (winter: 11/08–19/08/99; spring: 23/11– 10/12/99; summer: 07/03–16/03/00, and autumn: 06/06 – 12/06/00) were taken in the same habitats. During the second sampling period trapping was carried out in three consecutive nights, with 4320 traps nights. At each site, two capture lines were installed. In the /rst line 20 snap traps of two sizes (18 × 7 × 1 cm and 10 × 5 × 1 cm) were installed, two per station. In live capture lines, ten modi/ed Davis (1962) model traps (35 × 8 × 10 cm) were placed, one per station. Trap stations were situated at 5 m intervals. All traps were baited with a mixture of peanut butter and cow fat. Traps were checked in the morning, trapped animals were placed in hermetic plastic bags and carried to the laboratory. Species, sex, and body measurements (weight, lengths of body and tail) were recorded. Male and female reproductive status was also recorded. A relative density indices (RDI) was used to estimate abundance of the population in each habitat. number of capture RDI = –––––––––––––––––––––––––––––– × 100; (number of traps × number of nights) − a where a is the number of active traps that were empty. On the /rst period sampling (May–July 1998) RDI values between habitats were compared with non parametric analysis of Kruskal Wallis. Blood samples were collected by cardiac puncture following ether anesthesia. All animals were then euthanized by ether inhalation. In the serum samples from these rodents antibodies were searched for: (a) Junin virus (n=217) by inmuno@uorescence (Peters et al., 1973), and by ELISA (n = 418), as described by Morales et al. (2002); (b) Hantavirus (n = 627) by ELISA (Ksiazek et al., 1995), using a Sin Nombre recombinant antigen (Feldman et al., 1993); (c) Lymphocytic Choriomeningitis (LCM) by ELISA (n=570),

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performed as described by Riera et al. (1995). Di;erent numbers of sera studied for each virus were due to the available volume of each serum. 3. Results Out of a total of 1253 animals that were captured, 69.2% were Mus domesticus, 18.8% Calomys musculinus, 4.9% Akodon dolores, 4.3% Rattus rattus, 1.8% A. azarae, 0.8% R. norvegicus and 0.2% C. venustus. The population abundance indices of M. domesticus were not signi/cantly di;erent among habitats (P ¿ 0:05), and it was the population that numerically predominated in every sampled habitat. R. rattus were also captured in every habitat, were most abundant in rubbish dumps (P ¡ 0:05). R. norvegicus were captured in low numbers in stream banks and railway banks. For that, the abundance di;erences among habitats were not signi/cant (P ¿ 0:05) (Fig. 2). The sigmodontine rodents C. musculinus, A. azarae, A. dolores and C. venustus, are usually considered wild rodents because they inhabit extensive grasslands, forested environments, or cultivated /elds. These species represented 26% of all the captures in the urban area, where their distribution was related to open space (railway bank, stream bank, vacant area and rubbish dump) (Fig. 2). C. musculinus came to be the most abundant in vacant areas, and was also captured in railway banks, stream banks and rubbish dumps. These di;erences in abundance between habitats were statistically signi/cant (P ¡ 0:05). A. azarae was captured in low numbers in vacant areas, stream banks and rubbish dumps, di;erence between habitats was not statistically signi/cant (P ¿ 0:05). A. dolores abundance varied signi/cantly between habitats (P ¡ 0:05), it was the most abundant species in rubbish dumps. Due to a low capture of C. venustus to statistically compare its abundance between habitats was not possible.

Fig. 2. Relative abundance (RDI) of each species by sampled habitat in the city of RNOo Cuarto, between May–July of 1998.

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RDI

10 8 6 4 2 0

Winter Vacant lots

Spring

Summer

Railway banks

Stream banks

Autumn Vacant areas

Fig. 3. Seasonal variation of total rodents relative abundance (RDI) by sampled habitat in the city of RNOo Cuarto, between August 1999 –June 2000.

14

6

12

5

10

RDI

RDI

4 3

8 6 4 2

2

0

1 0 Winter

Spring Mus domesticus

Summer

Winter

Spring

Vacant lots

Railway banks

Summer Stream banks

Autumn Vacant areas

Autumn

Calomys musculinus

Fig. 4. Seasonal variation of Mus domesticus and Calomys musculinus relative abundance (RDI) in the city of RNOo Cuarto, between August 1999 – June 2000.

From the total abundance of rodents in seasonal samplings, two di;erent patterns were observed: 1—from summer to autumn, in vacant lots and stream banks, density increased; 2—in winter and summer the values of abundance were the largest, in spring an autumn they were the lowest, in railway banks and vacant areas (Fig. 3). There was considerable seasonal variation of M. domesticus andC. musculinus population abundance in all habitats (Fig. 4). This variation could not be calculated for populations of other species because abundance values were too low. RDI values for C. musculinus started with numbers similar to M. domesticus in winter, decreased in spring and increased again in autumn. M. domesticus population presented a continual growth pattern from winter to autumn. M. domesticus relative abundance seasonal variation in each sample habitat is registered in Fig. 5. In every habitat the same pattern of population growth was observed from winter to autumn. On the other hand, abrupt jumps in vacant areas and vacant lots were registered. In vacant areas the big fall of numerical value coincided with a high capture of C. musculinus in that habitat.

Fig. 5. Seasonal variation of Mus domesticus relative abundance (RDI) by sampled habitat in the city of RNOo Cuarto, between August 1999 –June 2000.

In Junin virus, the 5 antibody positive captures consisted of only Mus domesticus species. Because these 5 rodents were sera positiva to LCM virus, but to higher titer, and Arenavirus cross reacts within the group, we considered that rodents were infected with LCM virus. No antibody positive to Hantavirus rodents were collected, and antibody to LCM was found in 56 of 370 (15,1%) Mus domesticus. 4. Discussion The nature and severity of the risk would vary with the population of rodent and its localization. The presence of rodent infestation represented in many cases a high health risk. Disease transmission is most likely to occur when the focus of a rodent infestation is situated close to human dwellings. This report is the /rst rodent population study in urban areas of Argentina. The results show two perspectives: (1) the risk that di;erent rodent populations represent to public health in urban area; and (2) the necessity to break with beliefs about “obliged rurality” attributed to some murid rodent populations.

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Large numbers of M. domesticus were captured throughout the year, with lowest numbers in winter-spring and the largest in autumn (Fig. 4). Seasonal variation in abundance frequently has been documented for M. musculus in northern hemisphere (Myers, 1974; Zejda, 1975). House mice are regarded as habitat generalists (Brooks and Rowe, 1979) but the common general requirement for these mice appear to be the presence of low shrubby vegetation suitable as a source of water, food, and shelter. In /eld populations of Mus, @uctuations in number of mice are usually related to seasonal breeding cycles induced by changes in temperature, water, food supply, and shelter, and to changing densities of predators and competitors (Christian, 1963; Newsome et al., 1976, Tann et al., 1991; Pech et al., 1999). Whereas, the M. domesticus seasonal population numbers in urban areas may be in@uenced by human activities (Lund, 1996; Macdonald and Fenn, 1996). These activities have resulted generally in the creation of suitable habitats to maintain a stable rodent population during most of the year. House mice was widely distributed in the city, occurring in a variety of continuous habitats, and often occurred with or near every other species of commensal and sigmodontine rodents. All habitats were seasonal habitats and vacant lots and vacant areas were not occupied throughout the year. M. domesticus winter survival being made possible in adjoining railway banks or stream banks or in commensal situations (Fig. 5). On the other hand, M. domesticus was detected in all habitats associated with human population and with a high rate of LCM seropositive animals. Evidence of LCMv was detected in reservoir populations throughout most of the habitats during this study, but prevalence LCMv trends, and prevalence rate by areas or rodents abundance are described in (Riera et al. (unpublished paper)). Detailed studies of in@uence of physical and environmental factors on wild rodents populations have been done in rural ecosystems in Argentina (Crespo et al., 1970; de Villafa˜ne, 1970; Kravetz and de Villafa˜ne, 1981; Kravetz and Polop, 1983; Busch et al., 1984; Zuleta et al., 1988). The common rodent species in rural areas of Argentina show distinct habitat associations. A. dolores, C. venustus and A. azarae, for example, are found predominantly in stable, linear habitats (fencerows, roadsides, and railroad right-of-way) (Kravetz and Polop, 1983; Mills et al., 1991). C. musculinus and C. laucha are numerically dominant in cultivated /elds over the other sigmodontine species in the central region of Argentina (de Villafa˜ne et al., 1977; Kravetz, 1978; Kravetz and Polop, 1983; Mills et al., 1991; Polop and Sabattini, 1993). The habitat use of these rodents is in relation to vegetation cover, food and environment capacity to shelter them (de Villafa˜ne and Bonaventura, 1987; Bonaventura and Kravetz, 1989; Martinez et al., 1990; de Villafa˜ne et al., 1992; Della/ore and Polop, 1994; Castellarini et al., 1998; Castellarini, 1999). In some city sectors there are continuous vegetation between rural and urban areas and presence of “corridors” like stream banks

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and railway banks. Where vegetation is more related to rural area than to urban one could explain the presence and abundance of sigmodontine rodents near human dwellings. Human activities in vacant lots, the absence of vegetation related to rural areas and the vacant lots size could explain why the sigmodontine rodents were found in all habitats but not in vacant lots. C. musculinus seasonal abundance in the city was similar to the one, observed in rural areas (Kravetz and Polop, 1983; Mills et al., 1991; Polop and Sabattini, 1993): low values in spring that reached the highest peak in autumn. C. musculinus maintained relatively stable population for most of the year, and su;ered a drop in population numbers during winter. C. musculinus maintain and circulate the Junin virus, infectious agent of AHF, in rural areas. AHF has been considered as a major public health problem in certain agricultural areas of Argentina (Sabattini and Maiztegui, 1970; Mills et al., 1994). Although C. musculinus captured positive serum was not detected for Junin virus in the city of RNOo Cuarto, high capture numbers, and the proximity of endemic area of AHF (approximately 50 km), constitute a potential risk situation. When individuals of this species in urban areas come in contact with infected animal of rural areas, or rural rodents disperse into urban areas, the infectious agents may be transferred to urban rodent populations who live in close contact with humans. If this occurs, disease in human population may result. A. azarae was captured in low numbers and it was Hantavirus serologically negative. However, in this species the zoonoses was registered serum positive in other localities of CNordoba province (Levis et al., 1997). A. dolores and C. venustus were trapped in low numbers and we found no evidence about species being implicated as hosts of etiologic agent of human diseases. On the other hand, population number of Rattus spp was slow. However, R. rattus was captured in all sampled habitats and in almost all sampled units (Fig. 2), representing a potential damage in installations or in stored merchandise (Jackson, 1984, 1998), as well as risk in public health. Before our study, only populations from rural or environments related to rural areas have been considered at high risk. We documented basic information about the distribution and abundance of rodent reservoirs and their sanitary state allow us to consider the risk of a possible human infection in a speci/c area. Thus, probable outbreaks can be prevented by controlling rodent reservoirs and/or by avoiding contact between rodents and men. Acknowledgements A special thanks to Marcos P. Torres for his assistance in the capture of rodents. This work was supported by Municipalidad of Ciudad de RNOo Cuarto; SecretarNOa de Ciencia

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