Abstract
Contrary to conventional agriculture, organic farming, where agrochemicals are entirely avoided, is considered more environmentally friendly. Numerous studies undertaken in agroecosystems have found that the intensification of agriculture has a negative impact on some small mammals species. In this study, we used two morphological indicators to evaluate the impact of agriculture intensification. Phenotypic variability and fluctuating asymmetry (FA- development instability proxy) have been widely used as morphological indicators of developmental stress. We implemented geometric morphometric methods to assess the influence of different agricultural farming systems on three rodent species. We hypothesize that conventional farming produces more stressful conditions than organic farming affecting species susceptible to agricultural intensification. We predicted that Akodon azarae, negatively affected by landscape simplification and more dependent on habitat quality, will show higher levels of phenotypic variation and greater FA in conventional farming. Whereas, Calomys musculinus and C. laucha, unaffected by agricultural intensification, will not show differences between farming systems. Akodon azarae exhibited higher phenotypic variability in conventional farms, while C. musculinus had no difference between farming systems. Contrarily, C. laucha exhibited higher values in conventional farms. Regarding FA, both Calomys species showed no differences between farming systems. Females of A. azarae tend to have higher FA values in conventional farming. Our results suggest that the effect of agricultural farming systems would vary according to the species, where the species most dependent on habitat quality would be more affected by intensive agriculture.
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References
Badyaev AV, Foresman KR, Fernandes MV (2000) Stress and developmental stability: vegetation removal causes increased fluctuating asymmetry in Shrews. Ecol Soc Am 81:336–345
Barros FC, Herrel A, Kohlsdorf T (2011) Head shape evolution in Gymnophthalmidae: does habitat use constrain the evolution of cranial design in fossorial lizards? J Evol Biol 24:2423–2433. https://doi.org/10.1111/j.1420-9101.2011.02372.x
Beasley DAE, Bonisoli-Alquati A, Mousseau TA (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol Indic 30:218–226. https://doi.org/10.1016/j.ecolind.2013.02.024
Benítez HA, Lemic D, Püschel TA, Viri H, Ba R, Kos T (2018) Fluctuating asymmetry indicates levels of disturbance between agricultural productions: an example in Croatian population of Pterostichus melas melas (Coleptera: Carabidae) spari c. Zool Anz 276:42–49. https://doi.org/10.1016/j.jcz.2018.07.003
Benítez HA, Lemic D, Villalobos-Leiva A, Bažok R, Órdenes-Claveria R, Živkovic IP, Mikac KM (2020) Breaking symmetry: fluctuating asymmetry and geometric morphometrics as tools for evaluating developmental instability under diverse agroecosystems. Symmetry 12(11):1–13. https://doi.org/10.3390/sym12111789
Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol. Evol 18:182–188. https://doi.org/10.1016/S0169-5347(03)00011-9
Bookstein FL (1991) Morphometric tools for landmark data: Geometry and Biology. Cambridge University Press, Cambridge
Boutin C, Baril A, Martin PA (2008) Plant diversity in crop fields and woody hedgerows of organic and conventional farms in contrasting landscapes. Agric Ecosyst Environ 123:185–193. https://doi.org/10.1016/j.agee.2007.05.010
Cassini GH, Vizcaíno SF, Bargo MS (2012) Body mass estimation in Early Miocene native South American ungulates: a predictive equation based on 3D landmarks. J Zool 287:53–64. https://doi.org/10.1111/j.1469-7998.2011.00886.x
Coda JA, Gomez MD, Steinmann AR, Priotto JW (2014) The effects of agricultural management on the reproductive activity of female rodents in Argentina. Basic Appl Ecol 15:407–415. https://doi.org/10.1016/j.baae.2014.06.005
Coda JA, Gomez MD, Steinmann AR, Priotto JW (2015) Small mammals in farmlands of Argentina: responses to organic and conventional farming. Agric Ecosyst Enviroment 211:17–23. https://doi.org/10.1016/j.agee.2015.05.007
Coda JA, Gomez MD, Martínez JJ, Steinmann AR, Priotto JW (2016) The use of fluctuating asymmetry as a measure of farming practice effects in rodents: a species-specific response. Ecol Indic 70:269–275. https://doi.org/10.1016/j.ecolind.2016.06.018
Coda JA, Martínez JJ, Steinmann AR, Priotto JW, Gomez MD (2017) Fluctuating asymmetry as an indicator of environmental stress in small mammals. Mastozoología Neotrop 24:313–321
Corti M, Aguilera M, Capanna E (2001) Size and shape changes in the skull accompanying speciation of South American spiny rats (Rodentia: Proechimys spp.). J Zool 253:537–547. https://doi.org/10.1017/S0952836901000498
de la Fuente EB, Perelman S, Ghersa CM (2010) Weed and arthropod communities in soyabean as related to crop productivity and land use in the Rolling Pampa. Argentina Weed Res 50:561–571. https://doi.org/10.1111/j.1365-3180.2010.00811.x
Delciellos AC, De Barros CS, Prevedello JA, Ferreira MS, Cerqueira R, Vieira MV (2018) Habitat fragmentation affects individual Condition: evidence from small mammals of the Brazilian Atlantic Forest. J Mammal 99:936–945. https://doi.org/10.1093/jmammal/gyy078
Domínguez A, Bedano JC (2016) Earthworm and enchytraeid co-occurrence pattern in organic and conventional farming: consequences for ecosystem engineering. Soil Sci 181:148–156. https://doi.org/10.1097/SS.0000000000000146
Dryden IL, Mardia KV (1998) Statistical shape analysis. Walter de Gruyter, Berlin / New York, Chichester, England
Ellis EC, Ramankutty N (2008) Putting people in the map: Anthropogenic biomes of the world. Front Ecol Environ 6:439–447. https://doi.org/10.1890/070062
Fordyce A, Hradsky BA, Ritchie EG, Di Stefano J (2016) Fire affects microhabitat selection, movement patterns, and body condition of an Australian rodent (Rattus fuscipes). J Mammal 97:102–111. https://doi.org/10.1093/jmammal/gyv159
Fuller RJ, Norton LR, Feber RE, Johnson PJ, Chamberlain DE, Joys AC, Mathews F, Stuart RC, Townsend MC, Manley WJ, Wolfe MS, Macdonald DW, Firbank LG (2005) Benefits of organic farming to biodiversity vary among taxa. Biol Lett 1:431–434. https://doi.org/10.1098/rsbl.2005.0357
Ghersa CM, Ferraro DO, Omacini M, Martı́nez-Ghersa, M.A., Perelman, S., Satorre, E.H., Soriano, A. (2002) Farm and landscape level variables as indicators of sustainable land-use in the Argentine Inland-Pampa. Agric Ecosyst Environ 93:279–293. https://doi.org/10.1016/S0167-8809(01)00351-6
Gomez MD, Coda JA, Simone I, Martínez JJ, Bonatto F, Steinmann AR, Priotto JW (2015) Agricultural land-use intensity and its effects on small mammals in the central region of Argentina. Mammal Res. https://doi.org/10.1007/s13364-015-0245-x
Gomez MD, Coda JA, Serafini VN, Steinmann AR, Priotto JW (2017) Small mammals in Agroecosystems: responses to land use intensity and farming management. Mastozoología Neotrop 24:289–300
Gomez MD, Goijman AP, Coda JA, Serafini VN, Priotto JW (2018) Small mammal responses to farming practices in central Argentinian agroecosystems: the use of hierarchical occupancy models. Austral Ecol 43:828–838. https://doi.org/10.1111/aec.12625
Hodara K, Busch M, Kittlein MJ, Kravetz FO (2000) Density-dependent habitat selection between maize cropfields and their borders in two rodent species (Akodon azarae and Calomys laucha) of Pampean agroecosystems. Evol Ecol 14:571–593. https://doi.org/10.1023/A:1010823128530
Hopton ME, Cameron GN, Cramer MJ, Polak M, Uetz GW (2009) Live animal radiography to measure developmental instability in populations of small mammals after a natural disaster. Ecol Indic 9:883–891. https://doi.org/10.1016/j.ecolind.2008.10.010
Imhoff C, Giri F, Siroski P, Amavet P (2018) Analysis of morphological variability and heritability in the head of the Argentine Black and White Tegu (Salvator merianae): undisturbed vs. disturbed environments. Zoology 127:47–62. https://doi.org/10.1016/j.zool.2018.02.002
Jentzsch A, Köhler G, Schumacher J (2006) Environmental stress and fluctuating asymmetry in the grasshopper Chorthippus parallelus (Acrididae: Gomphocerinae). Zoology 106:117–125
Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Klingenberg CP (2015) Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry (basel) 7:843–934. https://doi.org/10.3390/sym7020843
Klingenberg CP (2019) Phenotypic plasticity, developmental instability, and robustness: the concepts and how they are connected. Front Ecol Evol 7:1–15. https://doi.org/10.3389/fevo.2019.00056
Klingenberg CP, McIntyre GS (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution (NY). 52:1363–1375
Klingenberg CP, Barluenga M, Meyer A (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution (n. y) 56:1909–1920. https://doi.org/10.1111/j.0014-3820.2002.tb00117.x
Lazić MM, Carretero MA, Crnobrnja-Isailović J, Kaliontzopoulou A (2015) Effects of environmental disturbance on phenotypic variation: an integrated assessment of canalization, developmental stability, modularity, and allometry in lizard head shape. Am Nat 185:44–58. https://doi.org/10.1086/679011
MAGyA, 2013. Resultados campaña agrícola 2012–2013. Provincia de Córdoba.
Marchand H, Paillat G, Montuire S, Butet A (2003) Fluctuating asymmetry in bank vole populations (Rodentia, Arvicolinae) reflects stress caused by landscape fragmentation in the Mont-Saint-Michel Bay. Biol J Linn Soc 80:37–44
Martínez JJ, Millien V, Simone I, Priotto JW (2014) Ecological preference between generalist and specialist rodents: spatial and environmental correlates of phenotypic variation. Biol J Linn Soc 112:180–203. https://doi.org/10.1111/bij.12268
Medan D, Torretta JP, Hodara K, Fuente EB, Montaldo NH (2011) Effects of agriculture expansion and intensification on the vertebrate and invertebrate diversity in the Pampas of Argentina. Biodivers Conserv 20:3077–3100. https://doi.org/10.1007/s10531-011-0118-9
Nunes AC, Auffray JC, Mathias ML (2001) Instability in a riparian population of the Algerian mouse (Mus spretus) associated with a heavy metal–polluted area in central Portugal. Environ Contam Toxicol 41:515–521. https://doi.org/10.1007/s002440010279
Palmer AR (1999) Detecting publication bias in meta-analyses: a case study of fluctuating asymmetry and sexual selection. Am Nat 154:220–233. https://doi.org/10.1086/303223
Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421
Palmer, A.R., Strobeck, C., 2003. Palmer AR, Strobeck C. 2003. Fluctuating asymmetry analyses revisited. In: Polak (ed) Developmental Instability: Causes and Consequences. Oxford University Press, pp. 279–319
Quinn JE, Johnson RJ, Brandle JR (2014) Identifying opportunities for conservation embedded in cropland anthromes. Landsc Ecol 29:1811–1819. https://doi.org/10.1007/s10980-014-0098-8
R Development Core Team, 2020. R: A language and environment for statistical computing
Renaud S, Michaux JR (2003) Adaptive latitudinal trends in the mandible shape of Apodemus wood mice. J Biogeogr 30:1617–1628. https://doi.org/10.1046/j.1365-2699.2003.00932.x
Rohlf FJ (1999) Shape statistics: Procrustes superimpositions and tangent spaces. J Classif 16:197–223
Rohlf FJ (2015) The Tps Series of Software. Hystrix 26:9–12. https://doi.org/10.4404/hystrix-26.1-11264
Rohlf FJ, Corti M (2000) Use of two-block partial least-squares to study covariation in shape. Syst Biol 49:740–753. https://doi.org/10.1080/106351500750049806
Rohlf FJ, Slice D (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59
Satorre EH (2005) Cambios tecnológicos en la agricultura argentina actual. Cienc Hoy 15:24–31
Scott JM, Davis FW, McGhie RG, Gerald WR, Craig G, Estes J (2001) Nature reserves: do they capture the full range of America’s biological diversity? Ecol Appl 11:999–1007
Serafini VN, Coda JA, Contreras F, Conroy MJ, Gomez MD, Priotto JW (2019a) The landscape complexity relevance to farming effect assessment on small mammal occupancy in Argentinian farmlands. Oecologia. https://doi.org/10.1007/s00442-019-04545-3
Serafini VN, Priotto JW, Gomez MD (2019b) Effects of agroecosystem landscape complexity on small mammals: a multi-species approach at different spatial scales. Landsc Ecol 34:1117–1129. https://doi.org/10.1007/s10980-019-00825-8
Shi F, Liu S, Sun Y, An Y, Zhao S, Liu Y, Li M (2020) Ecological network construction of the heterogeneous agro-pastoral areas in the upper Yellow River basin. Agric Ecosyst Environ. https://doi.org/10.1016/j.agee.2020.107069
Teixeira CP, Hirsch A, Perini H, Young RJ (2006) Marsupials from space: fluctuating asymmetry, geographical information systems and animal conservation. Proc R Soc B 273:1007–1012. https://doi.org/10.1098/rspb.2005.3386
Tscharntke T, Klien M, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecol Lett 8:857–874. https://doi.org/10.1111/j.1461-0248.2005.00782.x
Van Valen L (1962) A study of fluctuating asymmetry. Evolution 16:125–142
Velickovic M (2004) Chromosomal aberrancy and the level of fluctuating asymmetry in black-striped mouse (Apodemus agrarius): effects of disturbed environment. Hereditas 140:112–122. https://doi.org/10.1111/j.1601-5223.2004.01827.x
Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565
Waller DM, Dole J, Bersch AJ (2008) Effects of stress and phenotypic variation on inbreeding depression in Brassica rapa. Evolution (NY) 62:917–931. https://doi.org/10.1111/j.1558-5646.2008.00325.x
Wauters LA, Dhondt AA, Knothe H, Parkin DT (1996) Fluctuating asymmetry and body size as indicators of stress in red squirrel populations in woodland fragments. J Appl Ecol 33:735–740
Willmore KE, Young NM, Richtsmeier JT (2007) Phenotypic variability: its components, measurement and underlying developmental processes. Evol Biol 34:99–120
Zakharov VM (1992) Population phenogenetics: analysis of developmental stability in natural populations. Acta Zool Fenn 191:7–30
Acknowledgements
We thank Foundation Rachel and Pamela Schiele, Las Gaviotas and Altos Verdes farms. We thank the anonymous reviewers for helpful comments on the manuscript. This research was made possible by grants of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 2015–2019 11220150100034), Agencia Nacional de Promoción Científica y Tecnológica (BID PICT 2017-1461), and Universidad Nacional de Río Cuarto (PPI 2020-2021).
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Financial support was provided by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 2015–2019 11220150100034), Agencia Nacional de Promoción Científica y Tecnológica (BID PICT 2017–1461) and Universidad Nacional de Río Cuarto (PPI 2020-2021).
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JAC, JJM, MDG and JWP: devised the study. JAC and VNS: performed data analysis and prepared the figures. All authors commented on and contributed to the draft. JAC: wrote the manuscript. All authors read and approved the final manuscript.
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Coda, J.A., Martínez, J.J., Serafini, V.N. et al. Phenotypic variability and developmental instability in rodents from different agricultural farming systems: organic vs. conventional. Mamm Biol 101, 1019–1032 (2021). https://doi.org/10.1007/s42991-021-00183-6
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DOI: https://doi.org/10.1007/s42991-021-00183-6