COMMUNITY STRUCTURE AND DIVERSITY OF SIGMODONTINE (MURIDAE: ) INHABITING MAIZE AND SOYBEAN FIELDS IN PAMPEAN AGROECOSYSTEMS, ARGENTINA

Paula Courtalon and María Busch

SUMMARY

The aim of this work was to characterize and compare the were the most abundant species, the former being captured in communities of small sigmodontine rodents present in soybean the borders and the latter in the fields, regardless the type of and maize plots according to specific composition, richness, di- crop. Diversity was higher in maize than soybean plots when versity and equitativity. The study was performed over two con- crops were mature, or after harvest. Differences in diversi- secutive years (periods); a follow up was made in crop plots ty were due to both changes in richness (generally by absence from sowing (early crop stage) to post-harvest (stubble). For of C. musculinus or O. flavescens) and changes in equitativi- both crop types, analysis was conducted considering the entire ty (due to a high similarity between the densities of C. laucha plot and each of its habitats (field and border). The results in- and A. azarae). Species diversity varied according to the deve- dicate that although communities were composed in both lopmental stage of the crop cycle and differences resulted from types of plots of the same species: Akodon azarae, Calomys lau­ changes in species richness (generally by absence of C. muscu­ cha, Calomys musculinus and Oligoryzomys flavescens, these linus or O. flavescens) and equitativity (by high similarity in the were absent in some sampling months. A. azarae and C. laucha densities of C. laucha and A. azarae).

Introduction lands. The partitioning pro­ increase in species diver­ Studies performed in the re­ cess is known as landscape sity due to increased en­ gion indicated the presence Agricultural activities re­ fragmentation (Wilcove et vironmental heterogeneity, of two main types of habi­ sult in the replacement of al., 1986). In this way, the changes in the relationships tats available for wild rodent natural ecosystems by a ma­ croplands of the Pampean among the different land­ species, namely the crop trix composed of croplands agroecosystems are the main scape components, hunting fields and their weedy edges, and their fencerows, live­ landscape element present on dominant competitors, or the fence­rows. The latter stock and pastures, pests nowadays. introduction of new species. show less variability in veg­ and plagues, machinery and Agricultural practices lead Although the role played etal cover because they are facilities, and associated pro­ to changes in the complex­ by small rodents as com­ less affected by agricultural cesses. An agroecosystem is ity and heterogeneity of the munity structuring elements activities (Busch and Kra­ an ecosystem subjected by environment at different has been well documented vetz., 1992a, b, Busch et al., humans to frequent changes scales. Human disturbances for different types of natu­ 1997; 2000; 2001; Hodara, in its biotic and abiotic com­ may produce more uniform ral environments (Dueser 1997; Hodara, et al., 2000). ponents in order to produce landscapes at a regional and Shugart, 1978; Dueser The grasslands, pastures fibers and food (Soriano and scale, and more heteroge­ and Brown, 1980; August, and cultivated fields in Cen­ Aguiar, 1998). Its complexity neous landscapes at a local 1983; Iriarte et al.,, 1989; tral Europe exhibit a trend derives not only from eco­ scale, due to the inclusion Ojeda, 1989; Mares and Er­ towards a reduced number logical interactions but also of fields for agriculture and nest, 1995; Kelt and Brown, of species, with one of them from socioeconomic aspects. cattle raising. The expan­ 1996; Shanker and Suku­ dominating over the others The agricultural labors sion of agriculture that took mar, 1998). In contrast, little (Jacobs, 2003). In Pampe­ produce a disturbance, giv­ place during the last years is known of their structur­ an agroecosystems, Kravetz ing place to new kinds of in Latin America caused a ing role in agroecosystems. (1986) proposed a model of habitats (crop fields). This decrease in the number of (Ouin et al., 2000). rodent community dynamics disturbance generates the available habitats, which in In Pampean agroecosys­ as a function of land use; fragmentation of the natu­ turn resulted in loss of di­ tems, the most abundant this model describes an in­ ral landscape (grasslands) versity by species extinc­ sigmodontine rodent spe­ crease in the equitativity of into crop fields, the weed­ tion (Altieri, 1999; Solbrig, cies are Calomys laucha, C. the rodent community in cul­ ed borders (corridors) and 1999). In some systems, musculinus, Akodon azarae tivated fields, since the ap­ patches of remnant grass­ however, there has been an and Oligoryzomys flavescens. pearance of the field habitat

KEYWORDS / Agroecosystem / Akodon azarae / Calomys laucha / Maize / Soybean / Received: 11/19/2009. Modified: 09/27/2010. Accepted: 10/08/2010.

Paula Courtalon. Ph.D. in Bio­ Ecología Genética y Evolu­ llón 2. 4o piso, Laboratorio Busch María. Ph.D. in Biology, logy, Universidad de Buenos ción, Facultad de Ciencias 57. CP 1428. Buenos Aires, UBA, Argentina. Professor, Aires (UBA). Argentina. Re­ Exactas y Naturales, UBA. Argentina. e-mail: pcourt@ UBA, Argentina. Researcher, searcher, UBA, Argentina. Av. Intendente Cantilo s /n. ege.fcen.uba.ar CONICET, Argentina. Address: Departamento de Ciudad Universtaria. Pabe­

812 0378-1844/10/11/812-06 $ 3.00/0 NOV 2010, VOL. 35 Nº 11 ESTRUCTURA COMUNITARIA Y DIVERSIDAD DE ROEDORES SIGMODONTINOS (MURIDAE: SIGMODONTINAE) DE PARCELAS DE CULTIVO DE MAÍZ Y SOJA EN AGROECOSISTEMAS PAMPEANOS DE ARGENTINA Paula Courtalon y María Busch RESUMEN

El objetivo de este trabajo fue caracterizar y comparar las en todos los meses de muestreo. A. azarae y C. laucha fueron comunidades de roedores sigmodontinos en parcelas de soja y las más abundantes, la primera más capturada en los bordes maíz en cuanto a composición específica, riqueza, diversidad y la segunda en los campos, independiente del tipo de culti- (H) y equitatividad (E). El estudio fue llevado a cabo en dos vo. H fue mayor en las parcelas de maíz que en las de soja en años consecutivos (períodos) en que se siguió parcelas de culti- postcosecha. Las diferencias en H se debieron tanto a cambios vo desde su siembra (precosecha) hasta la post cosecha (rastro- en la riqueza (por ausencia de C. musculinus u O. flavescens) jos). Para cada tipo de cultivo, se consideró la parcela comple- como a cambios en E (por mayor similitud en las abundancias ta y cada uno de los hábitats que la forman (campo y bordes). entre C. laucha y A. azarae). Estos resultados permiten propo- Los resultados muestran que las comunidades de roedores estu- ner que la diversidad de roedores varió según el momento del vieron compuestas en ambos tipos de cultivo por las mismas es- ciclo del cultivo considerado y los cambios en la riqueza (por pecies: Akodon azarae, Calomys laucha, Calomys musculinus y ausencia de C. musculinus o O. flavescens) y en E (por alta Oligoryzomys flavescens, todas no estuvieron siempre presentes similitud en la abundancia de C. laucha and A. azarae).

ESTRUTURA COMUNITÁRIA E DIVERSIDADE DE ROEDORES SIGMODONTINOS (MURIDAE: SIGMODONTINAE) DE PARCELAS DE CULTIVO DE MILHO E SOJA EM AGROECOSSISTEMAS PAMPEANOS DE ARGENTINA Paula Courtalon e María Busch RESUMO

O objetivo de este trabalho foi caracterizar e comparar as meses de amostragem. A. azarae e C. laucha foram as mais comunidades de roedores sigmodontinos em parcelas de soja e abundantes, a primeira mais capturada nas bordas e a segunda milho quanto a composição específica, riqueza, diversidade (H) nos campos, independente do tipo de cultivo. H foi maior nos e equitatividade (E). O estudo foi realizado em dois anos conse- lotes de milho que nos de soja em pós colheita. As diferenças cutivos (períodos) em que foram acompanhados lotes de cultivo em H se deveram tanto a mudanças na riqueza (por ausência desde sua plantação (precolheita) até a pós colheita (restos). de C. musculinus u O. flavescens) como a mudanças em E (por Para cada tipo de cultivo, se considerou o lote completo e cada maior similitude nas abundâncias entre C. laucha e A. azarae). um dos hábitats que o formam (campo e bordas). Os resultados Estes resultados permitem propor que a diversidade de roedores mostram que as comunidades de roedores estiveram compos- variou segundo o momento do ciclo do cultivo considerado e tas em ambos tipos de cultivo pelas mesmas espécies: Akodon as mudanças na riqueza (por ausência de C. musculinus o O. azarae, Calomys laucha, Calomys musculinus e Oligoryzomys flavescens ) e em E (por alta similitude na abundância de C. flavescens, todas não estiveram sempre presentes em todos os laucha and A. azarae).

leads to habitat segregation Sigmodontine rodents have AND Cent Lec lineage that have been made involving and decreases the competi­ been historically studied due occurred in the provinces of a simultaneous follow-up tion effect of A. azarae on to their epidemiological im­ Entre Ríos and Buenos Ai­ from sowing to postharvest Calomys sp. However, the portance, since they act as res, but the rodents associ­ of maize and soybean fields, type of crop may affect the reservoirs of viruses such ated with the lineages AND or taking into account the features of rodent communi­ as the Junin virus, which is Cent Buenos Aires and AND different types of habitats in ties because of differences in the etiological agent of the Cent Plata are still to be de­ a crop field. resource availability. In par­ argentine hemorrhagic fever termined. On the other hand, The goal of this study is ticular, the temporal distribu­ (AHF), and the Hantavirus­ there are no records of hu­ to characterize and compare tion of the rodent community es, causing the hantavirus man cases of the Pergamino the communities of sigmo­ may vary according to the pulmonary syndrome (HPS). virus and the Maciel virus, dontine rodents present in different agriculture sched­ In the Pampean region, C. associated to A. azarae and soybean and maize crop­ ules. In this respect, Busch musculinus has been incrim­ benefactus (for­ lands, in terms of species et al. (1984) observed differ­ inated as the main reservoir merly Bolomys benefactus), composition, richness, diver­ ences in rodent density and of the Junin virus. The Han­ respectively. sity and equitativity. proportion of rodent species tavirus circulating in Argen­ In a previous study con­ between winter and summer tina, Chile and Uruguay is ducted in endemic areas of Material and Methods crops; these differences were the Andes virus (AND). The hemorrhagic fever in Ar­ attributed to a differential ef­ latter has been associated gentina, Busch et al. (1984) Study area fect of agricultural practices with species of the genus found lower densities of on distinct rodent species, Oligorizomys. In the central Calomys rodents in soybean This study was performed e.g. the reproductive cycle of region of Argentina (includ­ than in maize fields, and in the locality of Diego Calomys sp. is synchronized ing the Pampean region), O. suggested to replace soybean Gaynor (34°08'S-59°14'W), with the developmental cycle flavescens has been associat­ fields by mayze fields. Up Buenos Aires Province, Ar­ of maize. ed with cases of HPS by the to now, however, no studies gentina. The study area is

NOV 2010, VOL. 35 Nº 11 813 located in the Undu­ Statistical analyses lating Pampa subre­ gion within the Pam­ The non-parametric pean phytogeographi­ Mann Whitney U test cal region (Cabrera, (Siegel and Castel­ 1953). The area is lan, 1998) was used under a temperate cli­ to compare species mate with mean tem­ diversity and equita­ peratures of 22.5 and tivity over each pe­ 9.8°C in summer and riod: a) between maize winter, respectively. and soybean plots for The original vegeta­ each sampling month, tion consisted of 1m b) between maize and high native grasses soybean field habitats reduced to small relict Figure 1. Scheme of the experimental plot showing the grid of live traps set on the crop for each sampling grasslands along field field and adjacent borders. A total of 100 traps were used in each grid, with 81 traps in the month, and c) between borders and roads, field habitat and 19 traps in the border habitat. maize and soybean and several introduced border habitats for species: Avena spp., each sampling month. Brassica campestris, Cyn- Rodent sampling resulting in 100 traps per Differences were considered odon dactylon, Medicago plot. One side of the grid statistically significant at spp., and Stellaria medial In the present study, the will be referred to as the P<0.05. (Bonaventura and Cagno­ plot is taken as the habi­ internal border and another ni, 1995). Winter crops are tat composed of the field one as the external border. Results mainly wheat and linen, and and the border habitats Eighty one traps were set summer crops are maize, (Figure 1). Samplings were in the field habitat and 19 First period soybean and sunflower. performed between Janu­ along the border habitat. In the study area maize ary 1999 and July 2000 in Traps were baited with pea­ A total of 253 individu­ and soybean crops, which maize and soybean plots. nut butter and, in order to als were captured between are summer grain crops, The capture-mark-recapture protect rodents against low January and July 1999. Of have different agricultural method was used to follow temperatures, they were these, 100 were found in the schedules. In maize crop rodent populations over the provided with cotton wool soybean plots (76 A. azarae, fields, sowing takes place developmental cycles of both and wrapped in paper and 15 C. laucha, 8 C. musculi- between late September and types of crops. The study nylon bags. In each sam­ nus and 1 O. flavescens) and early October. During spring, was divided into two con­ pling, traps operated for 153 in maize plots (104 A. maize seedlings start to de­ secutive periods: a) Peri­ three consecutive nights and azarae, 32 C. laucha, 10 C. velop, providing the greatest od 1, from January to July were monitored every morn­ musculinus and 7 O. flave- amount of green cover. As 1999, when samplings were ing. The following infor­ scens), with a trapping effort summer progresses, maize performed in January (both mation was recorded from of 2700 captures trap-night matures and dries progres­ types of crops before har­ each caught : spe­ in soybean plots and 2400 sively until senescence at vest), March (maize crops cies, spatial location on the trap-night in the maize plot. the end of March, when har­ after harvest, soybean crops grid, sex, weight, total and In the plots, when all vest takes place; in autumn, before harvest) and May tail lengths, and reproduc­ samplings of the first pe­ stubble maize crop fields are (both crops after harvest); b) tive stage. were riod were considered, maize characterized by scarce vege­ Period 2, from October 1999 handled according to the and soybean crops showed tal cover and a high percent­ to July 2000, when sam­ national laws of animal care a richness of 4 species (A. age of bare ground. Soybean plings were made in October (www.sarem.org.ar). azarae, C. laucha, C. mus- has two periods of sowing, (recently sown maize and The abundance of each culinus and O. flavescens; the first one (first soybean soybeam crops), December rodent species in each habi­ Figure 2a). There were vari­ crop) in November, and the (maize and soybean crops tat was estimated based on ations in the values of diver­ second soybean crop in De­ in growth phase), February its trap success (trapped in­ sity and equitativity through­ cember; harvest also takes (senescent maize crops, soy­ dividuals/trap-nights)×100 out the first period (Table I). place earlier in the first than bean crops in growth phase), (Mills et al., 1991) In January (prior to harvest in the second period. The and May (both crops in Species diversity (H), in both crops) there were no crop matures in summer, stubble). Three maize plots richness (S), and equitativ­ significant differences in the dries progressively until the and three soybean plots were ity (E) were obtained for diversity (H) and equitativ­ beginning of autumn, and sampled simultaneously per each plot and each habitat ity (E) between maize and is senescent in mid-April period, and different plots (field and border), over each soybean plots (p>0.05 for (first soybean crop) or at the were studied in the first and sampling month and each both indices; Table I). The beginning of May (second second periods. period. According to Ma­ relative abundance showed a crop), when it is harvest­ Sherman live traps were gurran, (1988) diversity was similar pattern (Figure 2a), ed. Then, crop fields are in set in the six plots studied estimated with the Shannon- but O. flavescens, which was stubble, with less vegetal per period (Figure 1). In Wiener index, in low abundance in maize cover and a higher propor­ each plot traps were placed plots, was not captured in H= -Spi ln pi, and tion of bare soil than maize 10m apart from one an­ soybean plots. Likewise, in stubble fields. other in a 10×10 grid, thus E= H / lnS March (after maize harvest,

814 NOV 2010, VOL. 35 Nº 11 maize fields had a richness musculinus and 3 O. flave- of three species in each of scens). The trapping effort the three sampling months, was 3600 captures trap-night whereas only C. laucha was in soybean plots and 3300 present in soybean fields in trap-night in maize plots. May (Figure 2a), resulting During this period, richness in a significantly higher spe­ was 4 species for both crop cies diversity in maize than types (Figure 2b). in soybean fields for this In the plots, when all month (U= 0, P= 0.0495; samplings of the second pe­ Table I). A similar trend was riod were considered, maize observed for equitativity, but and soybean crops showed no significant differences a richness of 4 species (A. were found for any month azarae, C. laucha, C. mus- (p>0.05 for both indices). O. culinus and O. flavescens; flavescens was not captured Figure 2b). There were vari­ in any of the two crop fields ations in the values of H during this period. and E throughout the second When the maize and soy­ period (Table I). In October bean border habitats were (recently sown maize crops, compared, differences in not-sown soybean crops) all species richness among the 4 species were present in three sampling months were the soybean plots, whereas observed (Figure 2a). A. az- O. flavescens was not cap­ arae was present in maize tured in maize plots (Fig­ and soybean border habitats ure 2b). H and E values in all sampling months; C. did not differ between crop laucha was not found in the types (p>0.05 for both indi­ border habitats of any of the ces, Table I). In December two crops during January (well-developed maize crops and March, and appeared and recently sown soybean in both crop types in May; crops), A. azarae was the C. musculinus was not cap­ dominant species in soy­ tured neither in the border bean plots and C. laucha habitat of maize in March, in maize plots. C. musculi- nor in the border habitats of nus was not captured in any the two crop types in May. of the two crop types. No Finally, O. flavescens was significant differences were always present in the maize found in H and E between border habitat, whereas it types of crop (p>0.05 for was only captured in March both indices), and O. flave- in the soybean border habi­ scens was not captured in tat. In May, diversity was soybean plots. In February significantly higher in the (both crops in senescence), Figure 2. Relative abundance pattern of each rodent species in field maize than in the soybean diversity was higher in and border habitats of maize and soybean plots for the different sam­ pling months. a. first period, b: second period. Data are expressed as border habitats (U= 0, P= maize than in soybean plots trap success of each species in each habitat type and sampling month. 0.0495; Table I) whereas (U= 0, P= 0.0495). Differ­ Aa: Akodon azarae, Cl: Calomys laucha, Cm: Calomys musculinus, no significant differences ences in equitativity between Of: Oligoryzomys flavescens. were found in the two oth­ the two crop types was non- er months. The equitativ­ significant (p>0.05). The two before soybean harvest), no harvest), C. musculinus and ity showed no significant showed a similar pattern of significant differences were O. flavescens were not found differences between border relative abundance or ro­ found in H and E between in soybean plots, whereas habitats of the two crops for dents, with A. azarae as the maize and soybean plots the dominance of A. azarae any of the months (p>0.05). dominant species, followed (p>0.05 for both indices). over C. laucha was more by C. laucha, although the Although the most abun­ pronounced in maize plots. Second period abundance of these species dant species in both types of Species diversity was signifi­ was more similar in soy­ crops was A. azarae, C. lau- cantly higher in maize than A total of 190 individu­ bean than in maize plots. In cha and C. musculinus were in soybean plots (U= 0, P= als were captured between May (both crop types after the second most abundant 0.0463), and no significant October 1999 and July 2000, harvest), when maize plots species in crop and soybean difference in equitativity of which 91 were found in remained in stubble for a plots, respectively. O. f la- was found between soybean soybean plots (58 A. azarae, longer period than soybean vescens showed the least and maize crops (U= 2, P= 29 C. laucha, 2 C. muscu- plots, all 4 species were cap­ relative abundance in both 0.26). linus and 2 O. flavescens) tured in maize plots, but C. types of crops (Figure 2a). The comparison between and 99 in maize plots (28 A. musculinus was not found In May (both crops after field habitats indicated that azarae, 63 C. laucha, 5 C. in soybean plots. In maize

NOV 2010, VOL. 35 Nº 11 815 Table I by C. laucha and C. muscu- Mean H (diversity) and E (equitability) indices according to type linus; O. flavescens was not of plot (M: maize; S: Soybean) time period and type of habitat. found in any of the two crop (field and border) over each sampling month fields. These differences in First period Second period the pattern of relative abun­ dance would be related to January March May October December February May the fact that the population M S M S M S M S M S M S M S cycle of C. laucha was more Plots H 0.47 0.54 0.65 0.65 0.91 0.15* 0.33 0.38 0.36 0.16 0.60 0.3* 0.50 0.36 synchronized with the maize E 0.38 0.49 0.78 0.67 0.65 0.21 0.54 0.46 0.56 0.24 0.90 0.48 0.61 0.40 cycle than with the soybean Fields H 0.53 0.29 0.35 0.39 0.47 0* 0.36 0.10 0 0.16 0.54 0.33 0.20 0.36 cycle (Kravetz, 1978). Dif­ E 0.60 0.42 0.25 0.24 0.46 0 0.52 0.15 0 0.24 0.55 0.48 0.18 0.53 ferences in species diversity Borders H 0.16 0.22 0.17 0.33 0.4 0.05* 0.19 0.09 0.36 0 0.28 0 0.751 0.21* between fields were likely E 0.14 0.23 0.25 0.477 0.29 0.073 0.28 0.13 0.33 0 0.26 0 0.8 0.3 to be due to the response of *: differences between type of plots. species in May, on the basis that it was the only month when differences were sta­ plots, C. laucha dominated were no significant differ­ Species diversity showed tistically significant. During over the remaining species, ences in the equitativity be­ no differences between this month, in maize fields whereas A. azarae was the tween the two types of bor­ maize and soybean plots, the most abundant species most abundant species in der habitats for any of the but varied with the differ­ was C. laucha, followed by soybean plots. No signifi­ sampling months (p>0.05). ent developmental stages of C. musculinus and A. az- cant differences in H and E In October C. musculinus both crops. During the first arae, whereas C. laucha values were found for this was not captured in any of study period, species diver­ was the only rodent found month between crop types the border habitat types; A. sity was higher in maize in the soybean fields. The (p>0.05 for both indices). azarae was the most abun­ than in soybean plots af­ difference in species diver­ Differences in diversity dant species in both types of ter harvest, when both plots sity between the maize and and equitativity between border habitats, and C. lau- were in stubble (May). Dur­ soybean fields would be re­ the two types of field habi­ cha was exclusively captured ing the second study period, lated to the response of spe­ tats were not significant for in maize border habitats. species diversity was higher cies to agricultural activities any of the sampling months The pattern of relative abun­ in maize than in soybean undertaken for each type of (p>0.05 for both indices; dance for December was plots when both crops were crop. At the time of sam­ Table I). In October, A. az- similar to that for October: mature and standing up­ pling, after harvest, maize arae was not captured in O. flavescens was captured right (February). Mills et fields remained in stubble any of the two types of field in maize border habitats, A. al. (1991) suggested the oc­ for a longer period than did habitats. C. laucha was the azarae was only present in currence of a gradient of soybeans fields, since the dominant species in maize soybean border habitats, and increasing diversity from former were harvested at the and soybean field habitats C. musculinus was not found soybean, maize or wheat end of May and the latter but showed a higher abun­ in both types of border habi­ fields to “linear” habitats between late April and early dance in maize. In Decem­ tats (Figure 2b). represented by fence lines, May. This determined that ber, C. laucha retained its field borders and railroads. rodent populations in maize dominance over A. azarae, Discussion In the present study, how­ fields had more time for re­ while C. musculinus and O. ever, the fact that species covery after the disturbance flavescens were not captured The characterization and diversity differed between caused by harvest than those in any field habitat type. In comparison of the commu­ maize and soybean plots in in soybean fields, and that February, the abundance pat­ nities of small sigmodontine some months only, may in­ C. laucha individuals had tern was similar to that ob­ rodents present in soybean dicate that this variable de­ enough time to re-colonize served for December, but C. and maize plots is essen­ pends on the developmental fields from the borders. musculinus was detected in tial to generate management stages of the crop. In addi­ In the second period, the low abundance in both field guidelines, given their public tion, variations might have lack of significant differences habitat types. In May, C. health relevance as reser­ been due to particular fea­ between maize and soybean laucha dominated in the two voirs of the Junin virus and tures of each crop type and fields reinforces the idea that types of field habitats, with Hantaviruses. different climatic conditions the differences in rodent pop­ the rest of the species being The sigmodontine com­ among years. ulations strongly depend on in low abundance (Figure munities present in the stud­ Species diversity was the period analyzed. Diversity 2b).There were no signifi­ ied soybean and maize plots higher in the maize field and equitativity were signifi­ cant differences in diversity shared the same species, habitat than in the soybean cantly higher in borders of between the two types of namely A. azarae, C. lau- field habitat when data from maize than in borders of soy­ border habitats for Octo­ cha, C. musculinus and O. all samplings performed in bean crops during the second ber, December and Febru­ f lavescens, but there were the first period were pooled period. In the borders of the ary (p>0.05 for both vari­ differences in the relative together. In maize fields, C. two crop fields, A. azarae was ables; Table I). In May, the abundance pattern of these laucha was the most abun­ the most abundant species diversity in maize border species depending on the dant species, followed by A. in both the first and second habitats was higher than in type of crop, habitat, sam­ azarae and C. musculinus, periods. The differences in soybean border habitats (U= pling month and period con­ whereas in soybean fields, A. diversity between the borders 0, P=0.0495; Table I). There sidered. azarae dominated, followed of the two crops would be

816 NOV 2010, VOL. 35 Nº 11 due to the absence of C. mus- species diversity in maize Propuesta para un control Kravetz FO (1986) Distribution of culinus in the borders of soy­ field habitats was higher ecológico de la fiebre hemor­ Junin virus and its reservoirs. rágica Argentina a través del A tool for Argentine Hemor­ bean, and to variations in the than in soybean field habi­ manejo de hábitat. Medicina rhagic fever risk. Evaluation abundance of C. laucha. This tats, depending on the pe­ (Bs. As.) 44: 30-40. in non-endemic areas. Inter- species was always less abun­ riod analyzed and the devel­ Busch M, Álvarez MR, Cittadino ciencia 11: 185-188. dant than A. azarae, but it opmental stage of the crop; EA, Kravetz FO (1997) Habi­ Magurran A (1988) Ecological was more abundant in maize 3) when there were signifi­ tat selection and interespe­ Diversity and its Measure- borders than in soybean cant differences in species cific competition in rodents ment. Princeton University in pampean agroecosistems. Press. Princeton, NJ, USA. borders, which determined diversity between borders of Mammalia 61: 167-184. 178 pp. a higher diversity in maize maize and soybean borders, Busch M, Miño M, Dadon JR, Mares MA, Ernest KA (1995) than in soybean borders. values were higher in maize Hodara K (2000) Habitat se­ Population and community Similarly to that observed for borders; 4) species diver­ lection by Calomys muscu- ecology of small field habitats, differences in sity varied according to the linus (Muridae, Sigmodon­ in a Gallery forest of Cen­ diversity in border habitats developmental stage of the tinae) in crop areas of the tral Brazil. J. . 76: pampean region, Argentina. 750-768. might be due to the develop­ crop and differences result­ Ecol. Austral 10: 15-26. mental stage of the crops. In ed from changes in species Mills JN, Ellis B, Mecker KT, Busch M, Miño M, Dadon JR, Maiztegui JI, Childs JE this study, these differences richness (generally by the Hodara K (2001) Habitat se­ (1991) Habitat associations occurred when the two crop absence of C. musculinus or lection by Akodon azarae and and relative densities of ro­ types were in stubble (May), O. flavescens) and equitativ­ Calomys laucha (Rodentia: dent populations in cultivated because species diversity after ity (by a high similarity in Muridae) in pampean agro­ areas of central Argentina. J. the densities of C. laucha ecosystem. Mammalia 65: Mammal 72: 470-479. harvest was higher in maize 29-48. than in soybean borders for and A. azarae). These differ­ Mills JN, Ellis B, Mecker KT, both study periods. ences were mainly observed Cabrera A (1953) Esquema Fito­ Calderón EG, Maiztegui JI, geográfico de la República Childs JE (1992) A longitu­ The data provided by this after the harvest, in May. Argentina. Rev. Mus. La Pla- dinal study of Junin virus study support the recom­ ta, Bot 8: 87-168. activity in the rodent res­ mendation of Busch et al. ACKNOWLEDGEMENTS Dueser RD, Brown WC (1980) ervoir of Argentine Hemor­ (1984) to plant soybean in Ecology correlates of insular rhagic Fever. Am. J. Trop. areas endemic to argentine The authors are grateful rodent diversity. Ecology 61: Med. Hyg. 47: 749-763. hemorrhagic fever (AHF); to Adriana Lennon for her 50-56. Ojeda R (1989) Small mammal responses to fire in the Monte C. musculinus was more hospitality during fieldwork. Dueser RD, Shugart HJr (1978) Microhabitats in a forest floor dessert, Argentina. J. Mam- abundant in the field habitat This work was supported small mammal fauna. Ecol- mal. 70: 416-420. of the maize plots than in by the University of Buenos ogy 59: 89-98. Ouin A, Paillat G, Butet A, Burel that of the soybean plots in Aires and CONICET, Ar­ Hodara K (1997) Preferencias de F (2000) Spatial dynamics May, when both crops were gentina. Hábitat y Densodependencia of wood mouse (Apodemus in stubble, rodent abundance en dos Especies de Roedores sylvaticus) in an agricultural was high, and there is a REFERENCES (Akodon azarae y Calomys landscape under intensive use laucha) de Agroecosistemas in the Mont Saint Michael peak in the number of AHF Pampeanos. Tesis. Universi­ Bay (France). Agric. Ecosyst. cases (Mills et al., 1992). Altieri MA (1999) The ecological Env. 78: 159-165. role of biodiversity in agro­ dad de Buenos Aires. Argen­ With regard to the epide­ ecosystems. Agr. Ecosyst. tina. 154 pp. Shanker K, Sukumar R (1998) miology of the Hantavirus Env. 74: 19-31. 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Iriarte JA, Contreras LC, Jak­ Solbrig OT (1999) Biodiversi­ were planted with soybean 50: 63-71. sic FM (1989) A long-term dad, desarrollo económico y study of a small-mam mal sustentabilidad en la Pampa and no cases of HPS were Busch M, Kravetz FO (1992a) assemblage in the central Competitive interactions Argentina. In Mateucci SD, detected in humans. Howev­ Chilean matorral. J. Mammal Solbrig OT, Morello J, Halff­ among rodents (Akodon az- 70: 79-87. er, this observation should be arae, Calomys laucha, Cal- ter G (Eds.) Biodiversidad y interpreted with caution, con­ omys musculinus and Oli- Jacob J (2003) Short term ef­ Uso de la Tierra. Conceptos sidering the absolute number goryzomys flavescens) in a fects of farming practices y Ejemplos de Latinoamérica. of individuals captured of C. two habitat system. I. Spatial on populations of common Eudeba. Buenos Aires, Ar­ voles. Agric. Ecosyst. Env. gentina. pp. 107-130. musculinus and O. flavescens. and numerical relationships. Mammalia 56: 45-46. 95: 321-325. Further comparisons must be Soriano A, Aguiar MR (1998) Es­ Busch M, Kravetz FO (1992b) Kelt DA, Brown JH (1996) Com­ tructura y funcionamiento de made among years and/or Competitive interactions munity structure of desert los agroecosistemas. Cienc. regions where these species among rodents (Akodon az- small mammals: comparisons Inv. 50: 63-73. are more abundant to clarify arae, Calomys laucha, Calo- across four continents. Ecol- Wilcove DS, McLellan CH, Dob­ this issue. mys musculinus and Oligory- ogy 77: 746 -761. son A (1986) Habitat frag­ In brief, it is concluded zomys flavescens ) in a two Kravetz FO (1978) Ecología de mentation in the temperate habitat system. II. Effect of that 1) species diversity was las comunidades de roedores zone. In Soule ME (Ed.) species removal. Mammalia involucradas en la Fiebre He­ Conservation Biology: the higher in maize than in soy­ 56: 541-544. morrágica Argentina. Tesis. Science of Scarcity and Di- bean plots when crops were Busch M, Kravetz FO, Per­ Universidad de Buenos Aires. versity. Sinauer. Sunderland, mature or after harvest; 2) cich RE, Zuleta GA (1984) Argentina. 200 pp. MA, USA. pp. 237-256.

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