Abstract
Fossorial rodents are recognized as diversity drivers in grassland ecosystems and are therefore considered ecosystem engineers and keystone species. However, there is a lack of evidence regarding this function for species in temperate grasslands, especially one of the most threatened, the European ground squirrel. We examined the effect of the European ground squirrel on plant species composition and diversity along the disturbance gradient mediated by their different population density and subsequently different disturbance intensity. We evaluated the effect of ground squirrel disturbance on plant diversity patterns in two plant communities with different species richness to determine whether the same pattern exists in contrasting habitats. In each plant community, we established transect of 25 × 250 m composed of 10 quadrats with different disturbance intensities of the ground squirrels. Vascular plant species were recorded in 320 plots of 1 m2. The distribution of individual species along the ground squirrel-mediated disturbance gradient was analysed using redundancy analysis. Diversity measures were calculated and modelled as a function of disturbances using generalized additive models. We observed significant compositional changes in plant communities accompanied by a reduction in dominant graminoid cover and a non-decreasing trend in forb cover along the disturbance gradient in both types of communities. We found that increasing disturbance activity leads to an increase in diversity at coarse spatial scale (625 m2) and spatial heterogeneity in species composition of both species-poor and species-rich plant community. The fine-scale (1 m2) diversity increased significantly only in species-poor community. Our results demonstrate that the European ground squirrel can be deservedly labelled as an important ecosystem engineer and keystone species promoting the diversity and heterogeneity of European temperate grasslands.
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References
Bangert RK, Slobodchikoff CN (2006) Conservation of prairie dog ecosystem engineering may support arthropod beta and gamma diversity. J Arid Environ 67(1):100–115. https://doi.org/10.1016/j.jaridenv.2006.01.015
Berke SK (2010) Functional groups of ecosystem engineers: a proposed classification with comments on current issues. Integr Comp Biol 50(2):147–157. https://doi.org/10.1093/icb/icq077
Bjornstad ON (2016) ncf: Spatial nonparametric covariance functions. R package version 1.1-7
Bjornstad ON, Falck W (2001) Nonparametric spatial covariance functions: estimation and testing. Environ Ecol Stat 8(1):53–70. https://doi.org/10.1023/A:1009601932481
Boellstorff DE, Owings DH (1995) Home range, population structure, and spatial organization of California ground squirrels. J Mamm 76(2):551–561. https://doi.org/10.2307/1382363
Brown JH, Heske EJ (1990) Control of a desert-grassland transition by a keystone rodent guild. Science 250(4988):1705–1707
Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Cadotte MW (2007) Competition–colonization trade-offs and disturbance effects at multiple scales. Ecology 88:823–829. https://doi.org/10.1890/06-1117
Case MF, Halpern CH, Levin SA (2013) Contributions of gopher mound and casting disturbances to plant community structure in a Cascade Range meadow complex. Botany 91(8):555–561. https://doi.org/10.1139/cjb-2013-0023
Caswell H, Cohen JE (1991) Communities in patchy environments: a model of disturbance, competition, and heterogeneity. In: Kolasa J, Pickett STA (eds) Ecological heterogeneity. Springer, New York, pp 97–122
Ceballos G, Pacheco J, List R (1999) Influence of prairie dogs (Cynomys ludovicianus) on habitat heterogeneity and mammalian diversity in Mexico. J Arid Environ 41(2):161–172. https://doi.org/10.1006/jare.1998.0479
Connell JH (1978) Diversity in tropical rainforests and coral reefs. Science 199(4335):1302–1310. https://doi.org/10.1126/science.199.4335.1302
Davidson AD, Detling JK, Brown JH (2012) Ecological roles and conservation challenges of social, burrowing, herbivorous mammals in the world’s grasslands. Front Ecol Environ 10(9):477–486. https://doi.org/10.1890/110054
Dietl W (2013) Weeds of pastures and meadows of European Alps. In: Holzner W, Numata M (eds) Biology and ecology of weeds. Springer, Dordrecht, pp 375–386
Dumbrell AJ, Clark EJ, Frost GA, Randell TE, Pitchford JW, Hill JK (2008) Changes in species diversity following habitat disturbance are dependent on spatial scale: theoretical and empirical evidence. J Appl Ecol 45(5):1531–1539. https://doi.org/10.1111/j.1365-2664.2008.01533.x
Ewacha MVA, Kaapehi C, Waterman JM, Roth JD (2016) Cape ground squirrels as ecosystem engineers: modifying habitat for plants, small mammals and beetles in Namib Desert grasslands. Afr J Ecol 54(1):68–75. https://doi.org/10.1111/aje.12266
Galvez-Bravo L, Lopez-Pintor A, Rebollo S, Gomez-Sal A (2011) European rabbit (Oryctolagus cuniculus) engineering effects promote plant heterogeneity in Mediterranean dehesa pastures. J Arid Environ 75(9):779–786. https://doi.org/10.1016/j.jaridenv.2011.03.015
Gibson DJ (2009) Grasses and grassland ecology. Oxford University Press, New York
Grime JP, Hodgson JG, Hunt R (2014) Comparative plant ecology: a functional approach to common British species. Springer, Dordrecht
Hastie TJ, Tibshirani RJ (1990) Generalized additive models. Chapman & Hall/CRC, Boca Raton
Hatcher PE (2017) Perenial weeds. In: Hatcher PE, Froud-Williams RJ (eds) Weed research: expanding horizons. Wiley, Chichester, pp 389–412
Hegedüšová-Vantarová K, Škodová I (eds) (2014) Plant communities of Slovakia 5. Grassland Vegetation, Veda
Huston M (1994) Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, Cambridge
James AI, Eldridge DJ, Koen TB, Moseby KE (2011) Can the invasive European rabbit (Oryctolagus cuniculus) assume the soil engineering role of locally-extinct natives? Biol Invasions 13(12):3027–3038. https://doi.org/10.1007/s10530-011-9987-9
Janišová M, Michálková D, Škodová I, Uhliarová E, Zaliberová M (2014) Cynosurion cristati. In: Hegedüšová-Vantarová K, Škodová I (eds) Plant communities of Slovakia 5. Grassl Veg, Veda, pp 110–117
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69(3):373–386. https://doi.org/10.2307/3545850
Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78(7):1946–1957. https://doi.org/10.1890/0012-9658(1997)078%5b1946:PANEOO%5d2.0.CO;2
Jones CC, Halpern Charles B, Niederer J (2008) Plant succession on gopher mounds in Western Cascade meadows: consequences for species diversity and heterogeneity. Am Midl Nat 159(2):275–286. https://doi.org/10.1674/0003-0031(2008)159%5b275:PSOGMI%5d2.0.CO;2
Kenney JJ, Detling JK, Reading RP (2016) Influence of black-tailed prairie dogs (Cynomys ludovicianus) on short-horned grasshoppers (Orthoptera: Acrididae) on the shortgrass steppe of Colorado. J Arid Environ 127:93–99. https://doi.org/10.1016/j.jaridenv.2015.11.006
Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7(1):69–80. https://doi.org/10.1046/j.1461-0248.2003.00551.x
Kolasa J, Rollo CD (1991) Introduction: the heterogeneity of heterogeneity: a glossary. In: Kolasa J, Pickett STA (eds) Ecological heterogeneity. Springer, New York, pp 1–23
Kotliar NB, Baker BW, Whicker AD, Plumb G (1999) Critical review of assumptions about the prairie dog as a keystone species. Environ Manag 24(2):177–192. https://doi.org/10.1007/s002679900225
Kühn I, Durka W, Klotz S (2004) BiolFlor: a new plant-trait database as a tool for plant invasion ecology. Divers Distrib 10(5/6):363–365. https://doi.org/10.1111/j.1366-9516.2004.00106.x
Laland K, Matthews B, Feldman MW (2016) An introduction to niche construction theory. Evol Ecol 30(2):191–202. https://doi.org/10.1007/s10682-016-9821-z
Lauenroth WK, Burke IC (2008) Ecology of the shortgrass steppe: a long-term perspective. Oxford University Press, New York
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69(1):1–24. https://doi.org/10.1890/0012-9615(1999)069%5b0001:DBRATM%5d2.0.CO;2
Levins R, Culver D (1971) Regional coexistence of species and competition between rare species. Proc Nat Acad Sci USA 68(6):1246–1248
Lindtner P, Ujházy K, Svitok M, Kubovčík V (2018) The European ground squirrel increases diversity and structural complexity of grasslands in the Western Carpathians. Mamm Res 63(2):223–229. https://doi.org/10.1007/s13364-017-0349-6
Mallen-Cooper M, Nakagawa S, Eldridge D (2019) Global meta-analysis of soil-disturbing vertebrates reveals strong effects on ecosystem patterns and processes. Glob Ecol Biogeogr 28(5):661–679. https://doi.org/10.1111/geb.12877
Matějů J, Šašek J, Vojta J, Poláková S (2011) Vegetation of Spermophilus citellus localities in the Czech Republic (Rodentia: Sciuridae). Lynx 42:133–143
Matějů J, Kratochvíl L, Pavelková Z, Pavelková-Řičánková V, Vohralík V, Němec P (2016) Absolute, not relative brain size correlates with sociality in ground squirrels. Proc R Soc B 283:20152725. https://doi.org/10.1098/rspb.2015.2725
Matthews B, De Meester L, Jones CG et al (2014) Under niche construction: an operational bridge between ecology, evolution and ecosystem science. Ecol Monogr 84(2):245–263. https://doi.org/10.1890/13-0953.1
Michener GR (1979) Spatial relationships and social organization of adult Richardson’s ground squirrels. Can J Zool 57:125–139. https://doi.org/10.1139/z79-010
Miklós L (ed) (2002) Landscape atlas of the Slovak Republic, 1st edn. Slovak Environmental Agency, Banská Bystrica
Miller B, Ceballos G, Reading R (1994) The prairie dog and biotic diversity. Conserv Biol 8(3):677–681. https://doi.org/10.1046/j.1523-1739.1994.08030677.x
Miller BJ, Reading RP, Biggins DE, Detling JK, Forrest SC, Hoogland JL, Javersak J, Miller SD, Proctor J, Truett J, Uresk DW (2007) Prairie dogs: an ecological review and current biopolitics. J Wildl Manag 71(8):2801–2810. https://doi.org/10.2193/2007-041
Mills LS, Soulé ME, Doak DF (1993) The keystone-species concept in ecology and conservation: Management and policy must explicitly consider the complexity of interactions in natural systems. Bioscience 43(4):219–224. https://doi.org/10.2307/1312122
Milton SJ, Dean WRJ, Klotz S (1997) Effects of small-scale animal disturbances on plant assemblages of set-aside land in Central Germany. J Veg Sci 8(1):45–54. https://doi.org/10.2307/3237241
Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: Community ecology package. R package version 2.4-5
Paine R (1966) Food web complexity and species diversity. Am Nat 100(910):65–75
Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 466(8):9–20. https://doi.org/10.2307/1312990
Pywell RF, Hayes MJ, Tallowin JB, Walker KJ, Meek WR, Carvell C et al (2010) Minimizing environmental impacts of grassland weed management: can Cirsium arvense be controlled without herbicides? Grass Forage Sci 65(2):159–174. https://doi.org/10.1111/j.1365-2494.2010.00735.x
Questad EJ, Foster BL (2007) Vole disturbances and plant diversity in a grassland metacommunity. Oecologia 153(2):341–351. https://doi.org/10.1007/s00442-007-0734-y
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Root-Bernstein M, Ebensperger LA (2013) Meta-analysis of the effects of small mammal disturbances on species diversity, richness and plant biomass. Austral Ecol 38(3):289–299. https://doi.org/10.1111/j.1442-9993.2012.02403.x
Rosenzweig M (1995) Species diversity in space and time. Cambridge University Press, Cambridge
Sasaki T, Yoshihara Y (2013) Local-scale disturbance by Siberian marmots has little influence on regional plant richness in a Mongolian grassland. Plant Ecol 214(1):29–34. https://doi.org/10.1007/s11258-012-0142-1
Shipley BK, Reading RP (2006) A comparison of herpetofauna and small mammal diversity on black-tailed prairie dog (Cynomys ludovicianus) colonies and non-colonized grasslands in Colorado. J Arid Environ 66(1):27–41. https://doi.org/10.1016/j.jaridenv.2005.10.013
Tamme R, Hiiesalu I, Laanisto L, Szava-Kovats R, Pärtel M (2010) Environmental heterogeneity, species diversity and co-existence at different spatial scales. J Veg Sci 21(4):796–801. https://doi.org/10.1111/j.1654-1103.2010.01185.x
Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75(1):2–16. https://doi.org/10.2307/1939377
Tuomisto H (2010) A diversity of beta diversities: straightening up a concept gone awry. Part 1. Defining beta diversity as a function of alpha and gamma diversity. Ecography 33(1):2–22. https://doi.org/10.1111/j.1600-0587.2009.05880.x
Van Staalduinen MA, Werger MJA (2007) Marmot disturbances in a Mongolian steppe vegetation. J Arid Environ 69(2):344–351. https://doi.org/10.1016/j.jaridenv.2006.08.002
Wheeler HC, Hik DS (2013) Arctic ground squirrels Urocitellus parryii as drivers and indicators of change in northern ecosystems. Mamm Rev 43(3):238–255. https://doi.org/10.1111/j.1365-2907.2012.00220.x
Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30(3):279–338. https://doi.org/10.2307/1943563
Wood SN (2013) On p-values for smooth components of an extended generalized additive model. Biometrika 100(1):221–228. https://doi.org/10.1093/biomet/ass048
Wood SN (2017) Generalized additive models: an introduction with R. Chapman & Hall/CRC, Boca Raton
Wright JP, Jones CG (2004) Predicting effects of ecosystem engineers on patch-scale species richness from primary productivity. Ecology 85(8):2071–2081. https://doi.org/10.1890/02-8018
Wright JP, Jones CG (2006) The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. BioScience 56(3):203–209. https://doi.org/10.1641/0006-3568(2006)056%5b0203:TCOOAE%5d2.0.CO
Yu DW, Wilson HB (2001) The competition–colonization trade-off is dead; long live the competition–colonization trade-off. Am Nat 158(1):49–63. https://doi.org/10.1086/320865
Zhang Y, Zhang Z, Liu J (2003) Burrowing rodents as ecosystem engineers: the ecology and management of plateau zokors Myospalax fontanierii in alpine meadow ecosystems on the Tibetan Plateau. Mamm Rev 33(3–4):284–294. https://doi.org/10.1046/j.1365-2907.2003.00020.x
Acknowledgements
The work was supported from European Regional Development Fund-Project “Mechanisms and dynamics of macromolecular complexes: from single molecules to cells” (No. CZ.02.1.01/0.0/0.0/15_003/0000441), by the Slovak Scientific Grant Agency (VEGA 2/0052/15) and by Operational Programme Research and Innovation (NFP: 313010T721).
Funding
This study was funded by European Regional Development Fund-Project “Mechanisms and dynamics of macromolecular complexes: from single molecules to cells” (No. CZ.02.1.01/0.0/0.0/15_003/0000441), by the Slovak Scientific Grant Agency (VEGA 2/0052/15) and by Operational Programme Research and Innovation (NFP: 313010T721).
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Lindtner, P., Svitok, M., Ujházy, K. et al. Disturbances by the European ground squirrel enhance diversity and spatial heterogeneity of plant communities in temperate grassland. Biodivers Conserv 29, 853–867 (2020). https://doi.org/10.1007/s10531-019-01914-5
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DOI: https://doi.org/10.1007/s10531-019-01914-5
Keywords
- European ground squirrel
- Spermophilus citellus
- Disturbance
- Diversity
- Plant communities
- Species composition