NOTA

Microhabitat use by sigmodontine rodents in crop-field borders of pampean agroecosystems

 

Melina N. Muratore¹, Marina de la Reta¹, Sofía Perna¹, Antonia Oggero¹, Susana Ferrero², Jaime J. Polop¹ and María Cecilia Provensal¹

¹ Grupo de Investigaciones en Ecología Poblacional y Comportamental (GIEPCO), Instituto de Ciencias de la Tierra, Biodiversidad y Sustentabilidad Ambiental (ICBIA) (UNRC-CONICET), Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Universidad Nacional de Río Cuarto, Río Cuarto, Córdoba, Argentina. [Correspondence: Melina N. Muratore <melinamuratore@gmail.com> ]

² Departamento de Matemática, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, Río Cuarto, Córdoba, Argentina.

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ABSTRACT

The aims of this work were to assess the relevance of some variables in the use of microhabitats by two rodent species, and to contribute to models predicting their presence in agroecosystems in the south of Córdoba province, Argentina. Rodent sampling was conducted in crop-field borders seasonally from spring 2013 to winter 2014. Floristic composition, litter cover and bare soil percentage were determined at each trap site. Variables influencing the use and not-use of trapping stations by each species were identified with a logistic regression. We suggest a differential microhabitat use by both species.

RESUMEN

Uso de microhábitat de roedores sigmodontinos en bordes de cultivo de agroecosistemas pampeanos.

Los objetivos de este trabajo fueron determinar la relevancia de algunas variables en el uso del microhábitat por dos especies de roedores, y contribuir a modelos que predigan su presencia en agroecosistemas del sur de la provincia de Córdoba, Argentina. El muestreo de roedores fue realizado estacionalmente en bordes de campos desde primavera de 2013 hasta invierno 2014. En cada sitio de trampeo se determinó la composición florística y el porcentaje de mantillo y de suelo desnudo. Las influencias de las variables en el uso o no uso de los sitios de trampeo por cada especie fueron identificadas con regresión logística. Se puede sugerir un uso diferencial de los microhábitats para ambas especies.

Key words: Akodon azarae; Calomys musculinus; Vegetation cover.

Palabras claves: Akodon azarae; Calomys musculinus; Cobertura de vegetación.

Recibido 19 agosto 2018.
Aceptado 8 octubre 2018.

Editor asociado: A. Farías

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The use of a current habitat by organisms at a given time is influenced by factors including quantity, quality, and distribution of resources (Wiens 1986). Seasonal variation of resources causes some variables to have more or less importance as explanatory variables for the presence and abundance of a species (Lambert & Adler 2000). The relationships between species and habitat variables also change according to the reproductive activity and the study scale (Lima et al. 2002).

Microhabitat can be assessed from quantifying physical and chemical variables, which influence the allocation of time and energy by an individual within its home range (Morris 1987). Numerous studies on microhabitat use have established positive or negative relationships between the presence or abundance of rodent species and variables indicating microhabitat structure, such as the percentage of bare soil (Barnum et al. 1992), the exposed rock surface (Bertolino 2007), the soil organic matter (Dueser & Shugart 1978), and the vegetation cover (Lambert & Adler 2000; Bakker 2006). This affects the abundance and composition of the fauna inhabiting that site since it provides refuge, food, and opportunities for nesting, as well as protection against predators (Birney et al. 1976; Jacob & Brown 2000). In Argentina, the relationship between wild rodents and habitat variables has been studied for macro-habitats in desert environments (Corbalán 2006; Corbalán & Debandi 2006), in protected areas (Gómez-Villafañe et al. 2012, Vadell et al., 2017) and in agroecosystems (Ellis et al. 1997; Andreo et al. 2009, Cavia et al. 2005, Gomez et al. 2015; Gomez et al. 2018).

Pampean agroecosystems can be defined as mosaics, which are temporally and spatially heterogeneous at different scales (Merriam 1988). They are characterized by monoculture fields, surrounded by a network of linear habitats, which some authors have termed “borders” (Bennett 1990). Border habitats are less disturbed than fields which are subject to agricultural practices, and usually present a relatively high vegetation cover throughout the year (Simone 2010), and they may contain potential resources (food and shelter) for reproduction and survival in the long term of the rodent species which inhabit them (Ellis et al. 1997). The quality and quantity of resources vary seasonally in agroecosystems due to environmental changes, which are mainly the result of weather seasonality and agricultural practices (Crespo 1966; Kravetz & Polop 1983, Sommaro et al. 2010; Gomez et al. 2011).

Akodon azarae (Fisher 1829) and Calomys musculinus (Thomas 1894) are the two most abundant rodent species, which inhabit agroecosystems of the Córdoba province (Andreo et al. 2009; Simone et al. 2012; Gomez et al. 2015). Akodon azarae is usually found in habitats with little disturbance and with high levels of vegetation cover (Ellis et al. 1997; Hodara et al. 2000; Andreo et al. 2009; Gomez et al. 2015) such as crop field borders, roadsides and areas of native vegetation (Bilenca & Kravetz 1998; Gomez et al. 2011). Calomys musculinus is considered the most opportunistic and generalist species of the rodent assemblage that lives in agroecosystems, since it inhabits crop-field borders preferably, but it can also be found in cultivated fields (Busch et al. 2000; Sommaro et al. 2010). The relationship between rodent species and environmental variables at microhabitat scale (trap site) has only been studied for reproductive A. azarae (Bilenca & Kravetz 1998; Escudero et al. 2012).

 Our aims were to assess the relevance of some variables in the use of habitat by A.   azarae and C. musculinus at microhabitat scale, and to contribute to models predicting their presence in the field borders of agroecosystems in the rural area of Chucul, department of Río Cuarto, province of Córdoba, Argentina (32º 55¢ 06²  S and 64º 10¢ 09²  W). Phytogeographically the area belongs to the Neotropical Region, Chacoan Dominion, Pampean Province (Martinez et al. 2016), and has been characterized according to its physiognomic type as a Grass Steppe (Bianco et al. 1987).

Rodent sampling was conducted seasonally in 16 borders (crop-field borders) during four trapping sessions (December 2013, February, May and August 2014). A trap line was located in each border (separated by at least 100 m from one another). A total of 20 live traps of Sherman type (baited with a mixture of bovine fat and peanut butter) were set in each line at a distance of 6 m among them. Capture, mark and release (CMR) samplings were carried out during 4 consecutive nights. During trapping sessions, traps were checked each morning and the captured rodents were marked with caravans. Capture and manipulation of rodents were performed following the standards of the American Society of Mammalogists for the use of wild mammals in research (Sikes et al. 2011) and the Center for Disease Control and Prevention (CDC) (Mills et al. 1995).

In each border, vegetation measurements were made using a quadrant of 1 m² (modified from Dueser & Shugart 1978) centered on each trap site. A flora census was conducted and the species present were determined according to their morphological characteristics. In addition, the litter cover percentage and the bare soil percentage were determined through direct visual estimation. Each site containing a trap was considered a replica, and only those plant species covering more than 5% and which were present in at least 10% of the trap sites were taken into account.

Logistic regression analyses were applied to establish the relationship between the microhabitat variables and the occurrence of individuals in each trap site. Model selection followed a forward stepwise procedure, using the Akaike information criterion (AIC) for each model, including the null model. Models with the lowest AIC and p < 0.05 values were selected to draw inferences. All statistical analyses were performed using the R version 3.0.3 library (nlme) (R Development Core Team 2009, www.r-proyect.org).

With a capture effort of 5120 traps/nights, 144 captures were obtained, 93 corresponding to individuals of A. azarae and 81 to individuals of C. musculinus. In spring 2013, only Bidens subalternans, Bromus catharticus, Clematis montevidensis, Cynodon dactylon, and Sorghum halepense were present in at least 10% of the registered sites. The average of mulch at the trapping sites was 13.26 ± 22.61 and that of bare soil was 5.61 ± 11. In summer 2014, eight plant species were present in 10% of the census: B.  pilosa, B. catharticus, Conyza bonariensis, C. dactylon, Digitaria sanguinalis, Gomphrena perennis, S. halepense, and Verbena litoralis. The average values of mulch and bare soil were 1.76 ± 2.31 and 1.4 ± 2.73, respectively. During autumn 2014, B. subalternans, B. catharticus, C. dactylon, Sonchus asper, S. halepense, and V. litoralis were present in 10% of the vegetation censuses. In this season, an average of 6.17 ± 13.8 of mulch and 4.57 ± 10.54 of bare soil was registered. In winter 2014, only C.  dactylon and S. halepense were registered in 10% of the trap sites, and the average of mulch was 1.15 ± 0.99, while that of bare soil was 1.91 ± 6.37.

The best model for A. azarae in autumn included five variables (Table 1).The Odds ratio obtained indicated that the probability that A.  azarae is present in the trap is 3, almost 2 and 3.5 times higher when B. subalternans (ODDS =  3.19; C.I. 95% [1.72– 5.95]), B.  catahrticus (ODDS = 1.79; C.I. 95% [1.06 -3.03]) and C.  dactylon (ODDS = 3.41; C.I. 95% [1.41-8.24]) are present, respectively. For winter, the best model (Table 2) only included C. dactylon. When this plant species is present, the probability (ODDS = 2.53; C.I. 95% [1.04-6.17]) that A. azarae is also present in the trap is 2.5 times higher. In the logistic regression analysis for spring, none of the microhabitat variables included was statistically significant. In summer, the insufficient amount of available data for this season did not allow for any statistical analyzes.

Table 1
Best logistic regression model for Akodon azarae’s presence in autumn 2014 in crop-field borders of the rural area of Chucul, Córdoba province. AIC: Akaike Information Criterion.

Table 2
Best logistic regression model for Akodon azarae’s presence in winter 2014 in borders of the rural area of Chucul, Córdoba province. AIC: Akaike Information Criterion.

Regarding C. musculinus, in spring the best model (Table 3) included the S. halepense presence. According to the Odds ratio (ODDS =  17.68; C.I. 95% [2.35-132.84), when this plant species is present, the probability that C.  musculinus is also present is 17 times higher. None of the variables considered in the logistic regression analysis was statistically significant for summer, autumn and winter.

Table 3
Best logistic regression model for Calomys musculinus’ presence in spring 2013 in borders of the rural area of Chucul, Province of Córdoba. AIC: Akaike Information Criterion.

The physiognomy and vegetation composition of habitats in agroecosystems are not the same throughout the year and during the same season (Simone et al. 2012). It is from those differences that rodents would select resources. In autumn, the plant species related with A.  azarae have morphological characteristics that are very different, contributing differentially to the cover and vertical structure of the microhabitat. Cynodon dactylon provides cover in the low-intermediate stratum, whereas S. halepense, B.  subalternans, and B. catharticus would make up an intermediate-high vertical stratum. In this way, the presence of these plant species would generate high-quality microhabitats for the protection against predators. Besides, most of these species are available throughout the year, which would reinforce the “quality” of the microhabitat in terms of shelter. In other studies, A. azarae had already been identified as cover-dependent to avoid principally aerial predation (Bilenca et al. 1992; Ellis et al. 1998). In agroecosystems of the Buenos Aires province, at a macrohabitat scale, there was a relationship between A. azarae captures and Stipa cover and vertical development of vegetation (Bonaventura et al. 1989), grass cover (Ellis et al. 1997) and Baccharis cover (Busch et al. 2001). In most cases, that relationship was interpreted because of the vegetation contribution to the vertical structure and to the protection against predators (Bilenca et al. 1992; Ellis et al. 1998). At microhabitat scale, Escudero et al. (2012) and Bilenca & Kravetz (1998), have found a strong relationship between vegetation cover and the reproductive condition of A. azarae females, stating that cover could be an important resource in the reproductive performance for shelter instead of feeding. From the results obtained in this study, it can be suggested that A. azarae use the microhabitat differentially based on the vegetation that would provide structure and cover as protection against potential predators, this in relation to those plants would have no relevance for consumption (Castellarini et al. 2003). For C. musculinus, the lack of relationship between plant species and its presence could be expected, since this species is considered the most generalist and opportunistic species of agroecosystems (Busch et al. 2000; Sommaro et al. 2010). The relationship between C. musculinus and S. halepense at microhabitat scale found in this study could be because the cover offered by this grass in borders provides shelter for protection against predation and for reproduction, which is not offered by plot fields in spring, agreeing with findings by Simone (2010) at the macrohabitat scale. This author registered many vegetation variables as predictors of the presence of C.  musculinus in borders of the rural area of Chucul, and established relationships with individual plant species that varied according to season. However, C. musculinus would seek coverage regardless of the plant species providing it. The habitat structural characteristics and the vegetation cover as shelter would be more important than the limitations for food resources for this rodent species. Since, according to Castellarini et al. (2003), plant species related to the presence of rodents in this study would not constitute food resource, we could infer that they would be acting as a refuge, without being able to discriminate if they are used as protection against predators or nesting sites, or both. On the other hand, the fact that the small number of captures could be a limitation for model fitting in some seasons for both species cannot be ruled out.

Future studies that reinforce or complement this study are necessary to explain in accurate way microhabitat use by C. musculinus in order to include relevant variables in the management and control programs, given its zoonotic importance.

Acknowledgements

This research was supported by Secretaría de Ciencia y Técnica de la Universidad Nacional de Río Cuarto (SECyT-UNRC 242/16) and Fondo para la Investigación Científica y Tecnológica (PICT 1743/13).

LITERATURE CITED

1. Andreo, V., M. Lima, M. C. Provensal, J. Priotto, & J. J. Polop. 2009. Population dynamics of two rodent species in agro-ecosystems of central Argentina: intra-specific competition, land-use, and climate effects. Population Ecology 51:297-306. https://doi.org/10.1007/s10144-008-0123-3        [ Links ]

2. Bakker, V. 2006. Microhabitat features influence the movements of red squirrels (Tamiasciurus hudsonicus) on unfamiliar ground. Journal of Mammalogy 87:124-130. https://doi.org/10.1644/04-MAMM-A-050R2.1        [ Links ]

3. Barnum, S., C. Manville, J. Tester & W. Carmen. 1992. Path selection by Peromyscus leucopus in the presence and absence of vegetative cover. Journal of Mammalogy 73:797-801. https://doi.org/10.2307/1382198        [ Links ]

4. Bennett, A. F. 1990. Habitat corridors: their role in wildlife management and conservation. Department of Conservation and Environment, Melbourne.         [ Links ]

5. Bertolino, S. 2007. Microhabitat use by garden dormice during nocturnal activity. Journal of Zoology 272: 176-182. https://doi.org/10.1111/j.1469-7998.2006.00254.x        [ Links ]

6. Bianco, C. A., T. A. Kraus, D. L. Anderson & J. J. Cantero. 1987. Formaciones del suroeste de la Provincia de Córdoba (República Argentina). Revista UNRC 7:5-66.         [ Links ]

7. Bilenca, D. N., F. O. Kravetz, & G. A. Zuleta. 1992. Food habitats of Akodon azarae and Calomys laucha (Cricetidae: Rodentia) in agroecosystems of central Argentina. Mammalia 56:371-383. https://doi.org/10.1515/mamm.1992.56.3.371        [ Links ]

8. Bilenca, D. N., & F. O. Kravetz. 1998. Seasonal variation in microhabitat use and feeding habits of the pampas mouse Akodon azarae in agroecosystems of central Argentina. Acta Theriologica 43:195-203. https://doi.org/10.4098/AT.arch.98-15        [ Links ]

9. Birney, E. C., W. E. Grant, & D. D. Baird. 1976. Importance of vegetative cover to cycles of Microtus populations. Ecology 57:1043-1051. https://doi.org/10.2307/1941069        [ Links ]

10. Bonaventura, S. M., I. Bellocq, & F. O. Kravetz. 1989. Relación roedor-vegetación: importancia de la disponibilidad de cobertura verde para Akodon azarae durante el invierno. Physis (Bs.As.), Sec C 46:61-66.         [ Links ]

11. Busch, M., M. H. Miño, J. R. Dadon, & K. Hodara. 2000. Habitat selection by Calomys musculinus (Muridae, Sigmodontinae) in crop areas of the pampean region, Argentina. Ecology Austral 10:15-26.         [ Links ]

12. Busch, M., M. H. Miño, J. R. Dadon, & K. Hodara. 2001. Habitat selection by Akodon azarae and Calomys laucha (Rodentia, Muridae) in pampean agroecosystems. Mammalia 65:29-48. https://doi.org/10.1515/mamm.2001.65.1.29        [ Links ]

13. Castellarini F., C. Dellafiore, & J. J. Polop. 2003. Feeding habits of small mammals in agroecosystems of central Argentina. Mammalian Biology 68:91-101. https://doi.org/10.1078/1616-5047-00067        [ Links ]

14. Cavia R., I. Gómez Villafanña, E. A. Cittadinoa, D.  Bilenca, M. Miño, & M. Busch. 2005. Effects of cereal harvest on abundance and spatial distribution of the rodent Akodon azarae in central Argentina. Agriculture, Ecosystems and Environment 107:95-99. https://doi.org/10.1016/j.agee.2004.09.011        [ Links ]

15. Corbalán, V. 2006. Microhabitat selection by murid rodents in the Monte Desert of Argentina. Journal of Arid Environments 65:102-110. https://doi.org/10.1016/j.jaridenv.2005.07.006        [ Links ]

16. Corbalán, V., & G. Debandi. 2006. Microhabitat use by Eligmodontia typus (Rodentia: Muridae) in the Monte Desert (Argentina). Mammalian Biology 71:124-127. https://doi.org/10.1016/j.mambio.2005.11.009        [ Links ]

17. Crespo, J. A. 1966. Ecología de una comunidad de roedores silvestres en el Partido de Rojas, Provincia de Buenos Aires. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”. Instituto Nacional de Investigación en Ciencias Naturales. Serie Ecología 1:73-134.

18. Dueser, R. D., & H. H. Shugart. 1978. Microhabitat in a forest-floor small mammal fauna. Ecology 59:89-98. https://doi.org/10.2307/1936634        [ Links ]

19. Ellis, B. a. et al. 1997. Structure and floristics of habitats associated with five rodent species in an agroecosystem in Central Argentina. Journal of Zoology (London) 243:437-460. https://doi.org/10.1111/j.1469-7998.1997.tb02794.x        [ Links ]

20. Ellis, B. A., J. N. Mills, G. E. Glass, K. T. Mckee, D.  A. Enria, & J. E.Childs. 1998. Dietary habits of the common rodents in an agroecosystem in Argentina. Journal of Mammalogy 79:1203-1220. https://doi.org/10.2307/1383012        [ Links ]

21. Escudero, P., I. Simone, J. J. Polop, & M.C. Provensal. 2012. Environmental variables and reproductive activity in small rodents of pampean agroecosystems. Mammalia 78:23-33. https://doi.org/10.1515/mammalia-2012-0114        [ Links ]

22. Gomez, D., L. Sommaro, A. R. Steinmann, M. Chiappero, & J. W. Priotto. 2011. Movement distances of two species of sympatric rodents in linear habitats of central Argentine agro-ecosystems. Mammalian Biology 76:58-63. https://doi.org/10.1016/j.mambio.2010.02.001        [ Links ]

23. Gomez, M. D. et al. 2015. Agricultural land-use intensity and its effects on small mammals in the central region of Argentina. Mammal Research 60:415-423. https://doi.org/10.1007/s13364-015-0245-x        [ Links ]

24. Gomez, M. D., A. Goijman, J. A. Coda, V. Serafini, & J.  Priotto. 2018. Small mammal responses to farming practices in central Argentinian agroecosystems: The use of hierarchical occupancy models. Austral Ecology 43:828-838. https://doi.org/10.1111/aec.12625        [ Links ]

25. Gómez-Villafañe, I., Y. Expósito, A. San Martín, P.  Picca, & M. Busch. 2012. Rodent diversity and habitat use in a protected area of Buenos Aires province, Argentina. Revista Mexicana de Biodiversidad 83:762-771. https://doi.org/10.7550/rmb.25126        [ Links ]

26. Hodara, K., M. Bush, M. Kittlein, & F. O. Kravetz. 2000. Density-dependent habitat selection between maize cropfields and their borders in two rodent species (Akodon azarae and Calomys laucha) of pampean agroecosystems. Evolutionary Ecology 14: 571-593. https://doi.org/10.1023/A:1010823128530        [ Links ]

27. Jacob, J., & J. S. Brown. 2000. Microhabitat use, giving-up densities and temporal activity as short and long term antipredator behaviors in common voles. Oikos 91:131-138. https://doi.org/10.1034/j.1600-0706.2000.910112.x        [ Links ]

28. Kravetz, F. O., & J. J. Polop. 1983. Comunidades de roedores en agroecosistemas del Dpto. de Río Cuarto, Córdoba. Ecosur 1:1-10.         [ Links ]

29. Lambert, T., & G. Adler. 2000. Microhabitat use by a tropical forest rodent, Proechimys semispinosus, in central Panama. Journal of Mammalogy 81:70-76. https://doi.org/10.1644/1545-1542(2000)081<0070:MUBATF>2.0.CO;2        [ Links ]

30. Lima, M., N. C. Stenseth, & F. M. Jaksic. 2002. Population dynamics of South American rodent: Seasonal structure interacting with climate, density dependence and predator effects. Proceedings of the Royal Society of London B 269:2579-2586. https://doi.org/10.1098/rspb.2002.2142        [ Links ]

31. Martinez, G., M. D. Arana, A. J. Oggero, & E. S. Natale. 2016. Biogeographical relationships and new regionalization of high-altitude grasslands and woodlands of the central Pampean Ranges (Argentina), based on vascular plants and vertebrates. Australian Systematic Botany 29:473-488. https://doi.org/10.1071/SB16046        [ Links ]

32. Merriam, G. 1988. Landscape dynamics in farmland. Trends in Ecology and Evolution 3:16-20. https://doi.org/10.1016/0169-5347(88)90077-8        [ Links ]

33. Mills, J. N., J. E. Childs, T. G. Ksiazeñ, C. J. Peters, & W. M. Velleca. 1995. Methods for trapping and sampling small mammals for Virologic Testing. U.S. Department of Health and Human Services. Public Health Service. CDC.         [ Links ]

34. Morris, D. W. 1987. Ecological scale and habitat use. Ecology 68:362–369. https://doi.org/10.2307/1939267

35. R Development Core Team. 2009. R: a language and environment for statical computing. R Foundations for Statistical Computing, Viena, Austria. ISBN 3-900051-07-0, URL: http://www.r-project.org.         [ Links ]

36. Sikes, R. S., W. L. Gannon and the Animal Care and Use Committee of the American Society of Mammalogists. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92:235-253. https://doi.org/10.1644/10-MAMM-F-355.1        [ Links ]

37. Simone, I. 2010. Variaciones en la abundancia de Calomys musculinus (Rodentia: Muridae) y su relación con variables ambientales en bordes de cultivo. Tesis de Doctorado. Universidad Nacional de Río Cuarto, Río Cuarto.         [ Links ]

38. Simone, I., M. C. Provensal, & J. J. Polop. 2012. Habitat use by corn mice (Calomys musculinus) in crop-field borders of agricultural ecosystems in Argentina. Wildlife Research 39:112-122. https://doi.org/10.1071/WR11065        [ Links ]

39. Sommaro, L., A. R. Steinmann, M. Chiappero &, J. W. Priotto. 2010. Effect of high density on the short term Calomys musculinus spacing behaviour: A fencing experiment. Acta Oecologica 36:343-348. https://doi.org/10.1016/j.actao.2010.02.009        [ Links ]

40. Vadell, M. V., F. García Erize, & I. Gómez Villafañe. 2017. Evaluation of habitat requirements of small rodents and effectiveness of an ecologically-based management in a hantavirus-endemic natural protected area in Argentina. Integrative Zoology 12:77-94. https://doi.org/10.1111/1749-4877.12207        [ Links ]

41. Wiens, J. A. 1986. Spatial scale and temporal variation in studies of shrubsteppe birds. Community ecology (J.  Diamond & T. J. Case, eds) Harper & Row, Nueva York.         [ Links ]