Abstract
Grasslands are endangered habitats through the world. Among its threats, land-use change has been recognized as one of the most important drivers of biodiversity decline. Sustainable livestock farming can be important conserving grasslands and preserving their biodiversity, and particularly in Uruguay are extensive and are carried out based on natural grasslands with little external management. However, in recent years there has been an increasing in land-use change, replacing natural grasslands with cultivated pastures, leading to a homogenization of the environments. Spiders are a model group for ecological studies, because they are good indicators of environmental change. Our goals were to evaluate the effect of land-use change (natural grasslands by annual pastures) in livestock systems of Uruguay on the spider community; and describe this community identifying conservation priority species and potential environmental indicators. We collected spiders seasonally during 1 year in three farms in Uruguay with a cattle and sheep full cycle production system. We found that substitution of natural grasslands by pastures in livestock systems implied a reduction in spider abundance and species richness. We found species considered of priority conservation for the country according to a local list and added new species to that list.
Implications for insect conservation
Our results highlight the importance of conservation of natural grasslands, even in productive systems, to reduce spider diversity loss, and contribute to preserve one of the most threatened environments in the region.
This is a preview of subscription content, access via your institution.
Data availability
All data request will be made available by the authors.
References
Baldi G, Paruelo JM (2008) Land-use and land cover dynamics in South American temperate grasslands. Ecol Soc 13(2):6. https://doi.org/10.5751/ES-02481-130206
Batáry P, Báldi A, Samu F, Szuts T, Erdos S (2008) Are spiders reacting to local or landscape scale effects in Hungarian. pastures? Biol Conserv 141:2062–2070. https://doi.org/10.1016/j.biocon.2008.06.002
Birkhofer K, Smith HG, Weisser WW, Wolters V, Gossner MM (2015a) Land-use effects on the functional distinctness of arthropod communities. Ecography 38:889–900. https://doi.org/10.1111/ecog.01141
Birkhofer K, Diekotter T, Meub C, Stotzel K, Wolters V (2015b) Optimizing arthropod predator conservation in permanent grasslands by considering components beyond species richness. Agric Ecosyst Environ 211:65–72. https://doi.org/10.1016/j.agee.2015.05.014
Birkhofer K, Rusch A, Andersson GKS, Bonmarco R, Danhardt J, Ekbom B, Jonsson A, Lindborg R, Olsson O, Rader R, Stjemman M, Williams A, Hedlund K, Smith HG (2018) A framework to identify indicator species for ecosystem services in agricultural landscapes. Ecol Indic 91:278–286. https://doi.org/10.1016/j.ecolind.2018.04.0148
Blake RJ, Woodcock BA, Westbury DB, Sutton P, Potts SG (2013) Novel management to enhance spider biodiversity in existing grass buffer strips. Agric For Entomol 15:77–85. https://doi.org/10.1111/j.1461-9563.2012.00593.x
Bomfim LS, Bitencourt JAG, Rodrigues ENL, Podgaiski LR (2021) The role of a rosette-shaped plant (Eryngium horridum, Apiaceae) on grasslands spiders along a grazing intensity gradient. Insect Conserv Div 2021:1–12. https://doi.org/10.1111/icad.12475
Brazeiro A, Achkar M, Toranza C, Bartesaghi L (2020) Agricultural expansion in Uruguayan grasslands and priority areas for vertebrate and woody plant conservation. Ecol Soc 25(1):15. https://doi.org/10.5751/ES-11360-250115
Bucher R, Andres C, Wedel MF, Entling MH, Nickel H (2016) Biodiversity in low-intensity pastures, straw meadows, and fallows of a fen area: a multitrophic comparison. Agric Ecosyst Environ 219:190–196. https://doi.org/10.1016/j.agee.2015.12.019
Cardoso P, Silva I, de Oliveira NG, Serrano AR (2004) Indicator taxa of spider (Araneae) diversity and their efficiency in conservation. Biol Conserv 120(4):517–524. https://doi.org/10.1016/j.biocon.2004.03.024
Ceccarelli FS, Koch NM, Soto EM, Barone ML, Arnedo MA, Ramírez MJ (2019) The grass was greener: Repeated evolution of specialized morphologies and habitat shifts in ghost spiders following grassland expansion in South America. Syst Biol 68(1):63–77. https://doi.org/10.1093/sysbio/syy028.PMID:29669028
Clough Y, Kruess A, Kleijn D, Tscharntke T (2005) Spider diversity in cereal fields: comparing factors at local, landscape and regional scales. J Biogeogr 32:2007–2014. https://doi.org/10.1111/j.1365-2699.2005.01367.x
Colwell RK (2013) Estimates, version 9.1: statistical estimation of species richness and shared species from samples. Available at http://viceroy.eeb.uconn.edu/estimates. Accessed on 21 Feb 2021
Cravino A, Brazeiro A (2021) Grassland afforestation in South America: Local scale impacts of eucalyptus plantations on Uruguayan mammals. For Ecol Manag 484:118937. https://doi.org/10.1016/j.foreco.2021.118937
da Silva GO, Ott R (2017) Short-term spider community monitoring after cattle removal in grazed grassland. Iheringia 107:e2017033. https://doi.org/10.1590/1678-4766e2017033
Dennis P, Skartveit J, Kunaver A, McCracken DI (2015) The response of spider (Araneae) assemblages to structural heterogeneity and prey abundance in sub-montane vegetation modified by conservation grazing. Glob Ecol Conserv 3:715–728
Downie IS, Wilson WL, Abernethy VJ, McCracken DJ, Foster GN, Ribera I, Murphy KJ, Waterhouse A (1999) The impact of different agricultural land-uses on epigeal spider diversity in Scotland. J Insect Conserv 3:273–286
Ellis EC, Goldewijk KK, Siebert S, Lightman D, Ramankutty N (2010) Anthropogenic transformation of the biomes, 1700 to 2000. Glob Ecol Biogeogr 19:589–606. https://doi.org/10.1111/j.1466-8238.2010.00540.x
Ferreira PM, Andrade BO, Podgaiski LR, Dias AC, Pillar VD, Overbeck GE, Mendonca M Jr., Boldrini II (2020) Long-term ecological research in southern Brazil grasslands: Effects of grazing exclusion and deferred grazing on plant and arthropod communities. PLoS ONE 15(1):e0227706. https://doi.org/10.1371/journal.pone.0227706
Freiberg JA, de Sales Dambros C, Rodrigues ENL, Teixeira RA, Vieira ÂDHN, de Almeida HS, Carvahlo PCF, Jacques RJS (2020) Increased grazing intensity in pastures reduces the abundance and richness of ground spiders in an integrated crop-livestock system. Agron Sustain Dev 40(1):1–10. https://doi.org/10.1007/s13593-019-0604-0
Gallé R, Vesztergom N, Somogyi T (2011) Environmental conditions affecting spiders in grasslands at the lower reach of the River Tisza in Hungary. Entomol Fenn 22:29–38. https://doi.org/https://journal.fi/entomolfennica/article/view/4241/3955
Gallé R, Urák I, Nikolett G, Hartel T (2017) Sparse trees and shrubs confers a high biodiversity to pastures: case study on spiders from Transylvania. PLoS ONE 12(9):e0184465. https://doi.org/10.1371/journal.pone.0183465
García LF, Laborda A, Villareal O, Burlas J, Castiglioni E (2020) The spider Losdolobus nelsoni Pompozzi, 2015—the first report of the family Orsolobidae in Uruguay (Araneae: Synspermiata). Turk J Zool 44(5):472–476. https://doi.org/10.3906/zoo-2005-32
Gerlach J, Samways M, Pryke J (2013) Terrestrial invertebrates as bioindicators: an overview of available taxonomic groups. J Insect Conserv 17(4):831–850
Ghione S, Coelho L, Costa FG, Garcia LF, Gonzalez M, Jorge C, Laborda A, Montes de Oca L, Perez-Miles F, Postiglioni R, Simo M, Toscano-Gadea C, Viera C, Aisenberg A (2017) Aracnidos prioritarios para la conservación en Uruguay. Bol Soc Zool Urug 26(1):1–8
Goosey HB, Smith JT, O’Neill KM, Naugle DE (2019) Ground-dwelling arthropod community response to livestock grazing: implications for avian conservation. Environ Entomol 48(4):856–866. https://doi.org/10.1093/ee/nvz074
Gossner MM, Lewinsohn TM, Kahl T et al (2016) Land-use intensification causes multitrophic homogenization of grassland communities. Nature 540:266. https://doi.org/10.1038/nature20575
Hammer Ø, Harper DA, Ryan PD (2020) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9
Henwood WD (2010) Toward a strategy for the conservation and protection of the world´s temperate grasslands. Gt Plains Res 20:121–134
Horvath R, Magura T, Szinetar C, Tothmeresz B (2009) Spiders are not less diverse in small and isolated grasslands, but less diverse in overgrazed grasslands: a field study (East Hungary, Nyírség). Agric Ecosyst Environ 130(1–2):16–22. https://doi.org/10.1016/j.agee.2008.11.011
INUMET (2020) Instituto Uruguayo de Meteorología. Características climáticas. Available at https://www.inumet.gub.uy. Accessed on 5 Feb 2021
Laborda A, Montes de Oca L, Pérez-Miles F, Useta G, Simó M (2018) The spider fauna from Uruguay River islands: understanding its role in a biological corridor. Biodiver Data J 6:e27319. https://doi.org/10.3897/BDJ.6.e27319
Laborda A, Hagopián D, Teijón S, Ginella J, Guerrero JC, Simó M (2020) The spider assemblage in a dendrofloristic hotspot from eastern Uruguay. Bol Soc Zool Urug 29(2):73–85. https://doi.org/10.26462/29.2.4
Lafage D, Djoudi EA, Perrin G, Gallet S, Pétillon J (2019) Responses of ground-dwelling spider assemblages to changes in vegetation from oligotrophic habitats of Western France. Arthropod-Plant Interact 13:653–662. https://doi.org/10.1007/s11829-019-09685-0
Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta analytical synthesis. Oecologia 139:1–10
Lemaire G, Franzluebbers A, de Faccio Carvalho PC, Dedieu B (2014) Integrated crop–livestock systems: Strategies to achieve synergy between agricultural production and environmental quality. Agric Ecosyst Environ 190:4–8. https://doi.org/10.1016/j.agee.2013.08.009
Machado EO, Laborda A, Simó M, Brescovit AD (2013) Contributions to the taxonomy and distribution of the genus Mesabolivar in southern South America (Araneae: Pholcidae). Zootaxa 3682:401–411. https://doi.org/10.11646/zootaxa.3682.3.1
Malumbres-Olarte J, Vink CJ, Ross JG, Cruickshank RH, Paterson AM (2013) The role of habitat complexity on spider communities in native alpine grasslands of New Zealand. Insect Conserv Diver 6(2):124–134. https://doi.org/10.1111/j.1752-4598.2012.00195.x
Maxwell S, Fuller R, Brooks T, Watson J (2016) Biodiversity: the ravages of guns, nets and bulldozers. Nature 536:143–145. https://doi.org/10.1038/536143a
Meyer ST, Heuss L, Feldhaar H, Weisser WW, Gossner MM (2019) Land-use components, abundance of predatory arthropods, and vegetation height affect predation rates in grasslands. Agric Ecosyst Environ 270–271:84–92. https://doi.org/10.1016/j.agee.2018.10.015
MGAP (2020) Anuario Estadístico Agropecuario 2020. In: Freiría G (ed) Ministerio de Ganadería, Agricultura y Pesca. Montevideo, Uruguay. (in Spanish)
Milano F, Blick T, Cardoso P et al (2021) Spider conservation in Europe: a review. Biol Conserv 256:109020. https://doi.org/10.1016/j.biocon.2021.109020
Morrone JJ (2014) Biogeographical regionalisation of the Neotropical region. Zootaxa 3782(1):1–110. https://doi.org/10.11646/zootaxa.3782.1.1
Nagy RK, Bell LW, Schellhorn NA, Zalucki MP (2020) Role of grasslands in pest suppressive landscapes: how green are my pastures? Austral Entomol 59(2):227–237. https://doi.org/10.1111/aen.12464
Olfert O, Johnson D, Brandt AS, Thomas G (2002) Use of arthropod diversity and abundance to evaluate cropping systems. Agron J 94:210–216
Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265
Opatovsky I, Weintraub PG, Musli I, Lubin Y (2017) Use of alternative habitats by spiders in a desert agroecosystem. J Arachnol 45:129–138. https://doi.org/10.1636/JoA-S-16-008.1
Paruelo JM, Jobbágy EG, Oesterheld M, Golluscio R, Aguiar M (2007) Grasslands and steppes of Patagonia and the Río de la Plata plains. In: Veblen TT, Young KR, Orme AR (eds) The physical geography of South America. Oxford University Press, Oxford, pp 232–248
Picasso VD, Modernel PD, Becoña G, Salvo L, Gutiérrez L, Astigarraga L (2014) Sustainability of meat production beyond carbon footprint: a synthesis of case studies from grazing systems in Uruguay. Meat Sci 98(3):346–354. https://doi.org/10.1016/j.meatsci.2014.07.005
Podgaiski LR, Joner F, Lavorel S, Moretti M, Ibanez S, Mendonça MDS Jr., Pillar VD (2013) Spider trait assembly patterns and resilience under fire-induced vegetation change in South Brazilian grasslands. PLoS ONE 8(3):e60207. https://doi.org/10.1371/journal.pone.0060207
Pompozzi G, Marrero HJ, Haedo J, Fritz L, Torretta JP (2019) Non-cropped fragments as important spider reservoirs in a Pampean agro-ecosystem. Ann App Biol 175:326–335. https://doi.org/10.1111/aab.12537
Pompozzi G, Copperi S, Fernández Campón F, Lagos Silnick S, García S, Peralta A, Albretch E (2021) The use of artificial habitats increases spider abundance and richness in a vineyard of Argentina. Biocontrol 66:217–226. https://doi.org/10.1007/s10526-020-10056-5
Prieto-Benítez S, Méndez M (2011) Effects of land management on the abundance and richness of spiders (Araneae): a meta-analysis. Biol Conserv 144(2):683–691. https://doi.org/10.1016/j.biocon.2010.11.024
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ríos-Tamayo D (2019) Four new species of Actinopus (Mygalomorphae: Actinopodidae) from Uruguay. Zootaxa 4624(4):523–538. https://doi.org/10.11646/zootaxa.4624.4.5
Rubio GD, Lo-Ma-Hung NF, Iuri HA (2014) A revision of the Neotropical genus Austrohahnia Mello-Leitao (Araneae, Hahniidae). Zootaxa 3894(1):106–116. https://doi.org/10.11646/zootaxa.3894.1.8
Sala O, Chapin SF, Armesto JJ et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. https://doi.org/10.1126/science.287.5459
Simó M, Guerrero JC, Giuliani L, Castellano I, Acosta LE (2014) A predictive modeling approach to test distributional uniformity of Uruguayan harvestmen (Arachnida: Opiliones). Zool Stud 53(1):1–13. https://doi.org/10.1186/s40555-014-0050-2
Simó M, Núñez M, Ojeda L, Laborda A, Queirolo D (2015) Knowing the biological linkage: spider composition and guilds in a hill range of northern Uruguay. Bol Soc Zool Urug 24:117–129
Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31(1):79–92. https://doi.org/10.1046/j.0305-0270.2003.00994.x
Titeux N, Henle K, Mihoub JB, Regos A, Geijzendorffer IR, Cramer W, Verburg PH, Brotons L (2016) Biodiversity scenarios neglect future land-use changes. Glob Change Biol 22(7):2505–2515. https://doi.org/10.1111/gcb.13272
Woodcock BA, Pywell RF, Macgregor NA, Edwards ME, Redhead J, Ridding LE, Batáry P, Czerwinski M, Duffield S (2021) Historical, local and landscape factors determine the success of grassland restoration for arthropods. Agric Ecosyst Environ 308:107271. https://doi.org/10.1016/j.agee.2020.107271
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effect models and extensions in ecology with. Springer, New York
Acknowledgements
We thank the editor and an anonymous reviewer for their helpful comments that improved the manuscript. Thanks to Alvaro Laborda and Damián Hagopián for helping us with spider identification of some specimens. Thanks also due to Sofía Copperi for help with statistical analysis and graphics. We would like to thank the farmers’ member of CREA groups (families Bialade, Bremermann and Urioste) for allowing access to their fields for data collection. GP allowed ANII (Agencia Nacional de Investigación e Innovación, Uruguay) for his postdoctoral scholarship (code PD_NAC_2018_1_150034). MS acknowledge financial support by PEDECIBA (Programa de Desarrollo de Ciencias Básicas), and Sistema Nacional de Investigadores (SIN, ANII).
Funding
The study work was supported by Instituto Nacional de Investigación Agropecuaria (INIA) and Instituto Nacional de Carnes (INAC) from Uruguay.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pompozzi, G., de Santiago, F., Blumetto, O. et al. Livestock systems preserving natural grasslands are biodiversity reservoirs that promote spiders’ conservation. J Insect Conserv 26, 453–462 (2022). https://doi.org/10.1007/s10841-022-00399-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10841-022-00399-y
Keywords
- Species richness
- Abundance
- Cultivated pastures
- Land-use change
- Priority conservation
- Uruguay