Vegetation heterogeneity caused by an ecosystem engineer drives oviposition-site selection of a threatened grassland insect

Abstract

Soil-disturbing ecosystem engineers play an important role in plant-species diversity in grasslands as they increase vegetation heterogeneity by creating gaps due to burrowing or mound-building activities. However, knowledge of the ecological importance of these microsites for arthropods is still rare. In this study, we analyse the role of ant-nest mounds of the yellow meadow ant (Lasius flavus) for oviposition-site selection of the silver-spotted skipper (Hesperia comma). Ant mounds were searched for H. comma eggs. Microclimatic and vegetation parameters were ascertained at occupied sites and control sites within the matrix vegetation. Furthermore, we analysed the habitat requirements of L. flavus by means of nest counting and the sampling of environmental parameters within different sites. L. flavus occurred most frequently in abandoned and less steep sites with deeper soils. Mean egg occupancy rates of H. comma on ant hills were 32 %, nearly twice as high as at control sites (18 %). In contrast to the surrounding vegetation, nest mounds were characterized by a lower vegetation cover and litter and a higher proportion of bare ground. Furthermore, they had a higher cover of host plants compared with control samples. These microhabitats offered the following essential key factors for the larval development of H. comma: (1) a suitable microclimate due to open vegetation and (2) a high amount of host plants. This study highlights the importance of L. flavus as an ecosystem engineer within central European grasslands because this species increases vegetation heterogeneity.

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References

  1. Abbas F, Picot D, Merlet J, Cargnelutti B, Lourtet B, Angibault J-M, Daufresne T, Aulagnier S, Verheyden H (2012) A typical browser, the roe deer, may consume substantial quantities of grasses in open landscapes. Eur J Wildl Res 59:69–75. doi:10.1007/s10344-012-0648-9

    Article  Google Scholar 

  2. Augustine DJ, Baker BW (2013) Associations of grassland bird communities with black-tailed prairie dogs in the North American great plains. Conserv Biol 27:324–334. doi:10.1111/cobi.12013

    Article  PubMed  Google Scholar 

  3. Blomqvist MM, Olff H, Blaauw MB, Bongers T, van der Putten W-H (2000) Interactions between above-and belowground biota:importance for small-scale vegetation mosaics in a grassland ecosystem. Oikos 90:582–598

    Article  Google Scholar 

  4. Bobbink R, Hornung M, Roelofs JGM (1998) The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J Ecol 86:717–738. doi:10.1046/j.1365-2745.1998.8650717.x

    CAS  Article  Google Scholar 

  5. Börschig C, Klein AM, von Wehrden H, Krauss J (2013) Traits of butterfly communities change from specialist to generalist characteristics with increasing land-use intensity. Bas Appl Ecol 14:547–554. doi:10.1016/j.baae.2013.09.002

    Article  Google Scholar 

  6. Cousins S (2009) Landscape history and soil properties affect grassland decline and plant species richness in rural landscapes. Biol Conserv 142:2752–2758. doi:10.1016/j.biocon.2009.07.001

    Article  Google Scholar 

  7. Cousins SAO, Eriksson O (2008) After the hotspots are gone. Land use history and grassland plant species diversity in a strongly transformed agricultural landscape. Appl Veg Sci 11:365–374. doi:10.3170/2008-7-18480

    Article  Google Scholar 

  8. Critchley CNR, Burke MJW, Stevens DP (2003) Conservation of lowland semi-natural grasslands in the UK: a review of botanical monitoring results from agri-environment schemes. Biol Conserv 115:263–278. doi:10.1016/S0006-3207(03)00146-0

    Article  Google Scholar 

  9. Dauber J, Wolters V (2005) Colonization of temperate grasslands by ants. Bas Appl Ecol 6:83–91. doi:10.1016/j.baae.2004.09.011

    Article  Google Scholar 

  10. Dauber J, Rommeler A, Wolters V (2006) The ant Lasius flavus alters the viable seed bank in pastures. Eur J Soil Biol 42:S157–S163. doi:10.1016/j.ejsobi.2006.06.002

    Article  Google Scholar 

  11. Davidson AD, Lightfood DC (2008) Burrowing rodents increase landscape heterogeneity in a desert grassland. J Arid Environ 72:1133–1145. doi:10.1016/j.jaridenv.2007.12.015

    Article  Google Scholar 

  12. Davies ZG, Wilson RJ, Brereton TM, Thomas CD (2005) The re-expansion and improving status of the silver-spotted skipper butterfly (Hesperia comma) in Britain: a metapopulation success story. Biol Conserv 124:189–198. doi:10.1016/j.biocon.2005.01.029

    Article  Google Scholar 

  13. Davies ZG, Wilson RJ, Coles S, Thomas CD (2006) Changing habitat associations of a thermally constrained species, the silver-spotted skipper butterfly, in response to climate warming. J Anim Ecol 75:247–256

    Article  PubMed  Google Scholar 

  14. Dean WRJ, Milton SJ, Klotz S (1997) The role of ant nest-mounds in maintaining small-scale patchiness in dry grasslands in Central Germany. Biodivers Conserv 6:1293–1307

    Article  Google Scholar 

  15. Dlussky GM (1981) Nester von Lasius flavus. Pedobiologia 21:81–99

    Google Scholar 

  16. Drobnik J, Römermann C, Bernhardt-Römermann M, Poschlod P (2011) Adaptation of plant functional group composition to management changes in calcareous grassland. Agric Ecosyst Environ 145:29–37. doi:10.1016/j.agee.2010.12.021

    Article  Google Scholar 

  17. Ebert G, Rennwald E (1991) Die Schmetterlinge Baden-Württembergs. Bd. 2: Tagfalter II. Eugen Ulmer, Stuttgart

  18. Eilers S, Pettersson LB, Ockinger E (2013) Micro-climate determines oviposition site selection and abundance in the butterfly Pyrgus. armoricanus at its northern range margin. Ecol Entomol 38:183–192. doi:10.1111/een.12008

    Article  Google Scholar 

  19. Fagan KC, Pywell RF, Bullock JM, Marrs RH (2008) Are ants useful indicators of restoration success in temperate grasslands? Restor Ecol 18:373–379. doi:10.1111/j.1526-100X.2008.00452.x

    Article  Google Scholar 

  20. Fartmann T (2004) Die Schmetterlingsgemeinschaften der Halbtrockenrasen-Komplexe des Diemeltales. Biozönologie von Tagfaltern und Widderchen in einer alten Hudelandschaft. Abh Westf Mus Naturkde 66:1–256

    Google Scholar 

  21. Fartmann T (2006) Oviposition preferences, adjacency of old woodland and isolation explain the distribution of the Duke of Burgundy butterfly (Hamearis lucina) in calcareous grasslands in central Germany. Ann Zool Fenn 43:335–347

    Google Scholar 

  22. Fartmann T, Mattes H (2003) Störungen als ökologischer Schlüsselfaktor beim Komma-Dickkopffalter (Hesperia comma). Abh Westf Mus Naturkde 65:131–148

    Google Scholar 

  23. Feldmann R (2009) Buckelwiesen, Buckelweiden: Häufung von Nesthügeln der Gelben Wiesenameise, Lasius flavus. Ameisenschutz akt 23:1–6

    Google Scholar 

  24. García-Barros E, Fartmann T (2009) Butterfly oviposition: sites, behaviour and modes. In: Settele J, Shreeve TG, Konvicka M, van Dyck H (eds) Ecology of butterflies in Europe. Cambridge University Press, Cambridge, pp 29–42

    Google Scholar 

  25. Grime JP, Hodgson JG, Hunt R (2007) Comparative plant ecology, 2nd edn. Castlepoint Press, Dalbeattie

    Google Scholar 

  26. Hermann G, Steiner R (1997) Eiablage- und Larvalhabitat des Komma-Dickkopffalters (Hesperia comma LINNÉ 1758). Carolinea 55:35–42

    Google Scholar 

  27. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386. doi:10.2307/3545850

    Article  Google Scholar 

  28. Kamczyc J, Gwiazdowicz DJ (2013) The diversity of soil mites (Acari: Mesostigmata) in yellow ant (Lasius flavus) nests along a gradient of land use. Biologia 68:314–318. doi:10.2478/s11756-013-0154-x

    Article  Google Scholar 

  29. King TJ (1977) The plant ecology of ant-hills in calcareous grasslands. I. Patterns of species in relation to ant-hills in southern England. J Ecol 65:235–256. doi:10.2307/2259077

    Article  Google Scholar 

  30. Krämer B, Poniatowski D, Fartmann T (2012a) Effects of landscape and habitat quality on butterfly communities in pre-alpine calcareous grasslands. Biol Conserv 152:253–261. doi:10.1016/j.biocon.2012.03.038

    Article  Google Scholar 

  31. Krämer B, Kämpf I, Enderle J, Poniatowski D, Fartmann T (2012b) Microhabitat selection in a grassland butterfly: a trade-off between microclimate and food availability. J Insect Conserv 16:857–865. doi:10.1007/s10841-012-9473-4

    Article  Google Scholar 

  32. Lawson CR, Bennie JJ, Thomas CD, Hodgson JA, Wilson RJ (2012) Local and landscape management of an expanding range margin under climate change. J Appl Ecol 49:552–561. doi:10.1111/j.1365-2664.2011.02098.x

    Google Scholar 

  33. Lawson CR, Bennie J, Hodgson JA, Thomas CD, Wilson RJ (2014) Topographic microclimates drive microhabitat associations at the range margin of a butterfly. Ecography 37:732–740. doi:10.1111/ecog.00535

    Article  Google Scholar 

  34. Lenoir L (2009) Effects of ants on plant diversity in semi-natural grasslands. Arth-Plant Int 3:163–172. doi:10.1007/s11829-009-9066-7

    Article  Google Scholar 

  35. Löffler F, Stuhldreher G, Fartmann T (2013) How much care does a shrub-feeding hairstreak butterfly, Satyrium spini (Lepidoptera: Lycaenidae), need in calcareous grasslands? Eur J Entomol 110:145–152. doi:10.14411/eje.2013.020

    Article  Google Scholar 

  36. Mariotte P, Buttler A, Kohler F, Gilgen AK, Spiegelberger T (2013) How do subordinate and dominant species in semi-natural mountain grasslands relate to productivity and land-use change? Bas Appl Ecol 14:217–224. doi:10.1016/j.baae.2013.02.003

    Article  Google Scholar 

  37. Möllenbeck V, Hermann G, Fartmann T (2009) Does prescribed burning mean a threat to the rare satyrine butterfly Hipparchia fagi? Larval-habitat preferences give the answer. J Insect Conserv 13:77–87. doi:10.1007/s10841-007-9128-z

    Article  Google Scholar 

  38. Müller-Wille W (1981) Westfalen. Landschaftliche Ordnung und Bindung eines Landes. 2. Auflage. Aschendorffsche Verlagsbuchhandlung, Münster

  39. Munguira M, Garcia-Barros E, Cano JM (2009) Butterfly herbivory and larval ecology. In: Settele J, Shreeve TG, Konvička M, van Dyck H (eds) Ecology of butterflies in Europe. Cambridge University Press, Cambridge, pp 43–54

    Google Scholar 

  40. Pontin AJ (1978) The numbers and distribution of subterranean aphids and their exploitation by the ant Lasius flavus (Fabr.). Ecol Entomol 3:203–207. doi:10.1111/j.1365-2311.1978.tb00920.x

    Article  Google Scholar 

  41. R Development Core Team (2016) R: a language and environment for statistical computing http://www.R-project.org. Accessed 17 Feb 2016

  42. Reinhardt R, Bolz R (2011) Rote Liste und Gesamtartenliste der Tagfalter (Rhopalocera) (Lepidoptera: Papilionoidea et Hesperioidea) Deutschlands. Natursch Biol Vielfalt 70:167–194

    Google Scholar 

  43. Roy DB, Thomas JA (2003) Seasonal variation in the niche, habitat availability and population fluctuations of a bivoltine thermophilous insect near its range margin. Oecologia 134:439–444

    CAS  Article  PubMed  Google Scholar 

  44. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig B, Leemans R, Lodge DM, Mooney HA, Oesterheld M, LeRoy PN, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. doi:10.1126/science.287.5459.1770

    CAS  Article  PubMed  Google Scholar 

  45. Seifan M, Tielbörger K, Schloz-Murer D, Seifan T (2010) Contribution of molehill disturbances to grassland community composition along a productivity gradient. Acta Oecol 36:569–577. doi:10.1016/j.actao.2010.08.005

    Article  Google Scholar 

  46. Seifert B (1993) Die freilebenden Ameisenarten Deutschlands (Hymenoptera: Formicidae) und Angaben zu deren Taxonomie und Verbreitung. Abh Ber Naturkundemus Görlitz 67:1–44

    Google Scholar 

  47. Seifert B (2007) Die Ameisen Mittel- und Nordeuropas. Lutra Verlags- und Vertriebsgesellschaft, Boxberg

  48. Stoutjesdijk P, Barkman JJ (1992) Microclimate Vegetation and Fauna. Opulus Press, Uppsala

    Google Scholar 

  49. Streitberger M, Fartmann T (2013) Molehills as important larval habitats for the Grizzled Skipper (Pyrgus malvae) in calcareous grasslands. Eur J Entomol 110:643–648

    Article  Google Scholar 

  50. Streitberger M, Fartmann T (2015) Vegetation and climate determine ant-mound occupancy by a declining herbivorous insect in grasslands. Acta Oecol 68:43–49. doi:10.1016/j.actao.2015.07.004

    Article  Google Scholar 

  51. Streitberger M, Hermann G, Kraus W, Fartmann T (2012) Modern forest management and the decline of the woodland brown (Lopinga achine) in Central Europe. Forest Ecol Manage 269:239–248. doi:10.1016/j.foreco.2011.12.028

    Article  Google Scholar 

  52. Streitberger M, Rose S, Hermann G, Fartmann T (2014) The role of a mound-building ecosystem engineer for a grassland butterfly. J Insect Conserv 18:745–751. doi:10.1007/s10841-014-9670-4

    Article  Google Scholar 

  53. Thomas JA (1991) Rare species conservation: case studies of European butterflies. In: Spellerberg IF, Goldsmith FB, Morris MG (eds) The scientific management of temperate communities for conservation. Blackwell Scientific, Oxford, pp 149–197

    Google Scholar 

  54. Thomas JA (2005) Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups. Phil Trans R Soc Lond Ser B Biol Sci 360:339–357. doi:10.1098/rstb.2004.1585

    CAS  Article  Google Scholar 

  55. Thomas JA, Thomas CD, Simcox DJ, Clarke RT (1986) Ecology and declining status of the silver-spotted skipper butterfly (Hesperia comma) in Britain. J Appl Ecol 23:365–380. doi:10.2307/2404023

    Article  Google Scholar 

  56. Thomas JA, Telfer MG, Roy DB, Preston CD, Greenwood JJD, Asher J, Fox R, Clarke RT, Lawton JH (2004) Comparative losses of British butterflies, birds, and plants and the global extinction crisis. Science 303:1879–1881. doi:10.1126/science.1095046

    CAS  Article  PubMed  Google Scholar 

  57. Tonne F (1954) Besser Bauen mit Besonnungs- und Tageslicht-Planung. Hofmann, Schorndorf

    Google Scholar 

  58. Van Dijk G (1991) The status of semi-natural grasslands in Europe. In: Goriup PD, Batten LA, Norton JA (eds) The conservation of lowland dry grassland birds in Europe. JNCC, Peterborough, pp 15–36

    Google Scholar 

  59. van Swaay CAM (2002) The importance of calcareous grasslands for butterflies in Europe. Biol Conserv 104:315–318. doi:10.1016/S0006-3207(01)00196-3

    Article  Google Scholar 

  60. Van Swaay CAM, Warren M (eds) (2003) Prime Butterfly Areas in Europe: Priority Sites for Conservation. National Reference Centre for Agriculture, Nature and Fisheries, Ministry of Agriculture, Nature Management and Fisheries, Wageningen

    Google Scholar 

  61. Veen P, Jefferson R, de Smidt J, van der Straaten J (eds) (2009) Grasslands in Europe of high nature value. KNNV Publishing, Zeist

    Google Scholar 

  62. Veen GF, Geuverink E, Olff H (2012) Large grazers modify effects of aboveground—belowground interactions on small-scale plant community composition. Oecologia 168:511–518. doi:10.1007/s00442-011-2093-y

    Article  PubMed  Google Scholar 

  63. Vickery JA, Tallowin JR, Feber RE, Asteraki EJ, Atkinson PW, Fuller RJ, Brown VK (2001) The management of lowland neutral grasslands in Britain: effects of agricultural practices on birds and their food resources. J Appl Ecol 38:647–664. doi:10.1046/j.1365-2664.2001.00626.x

    Article  Google Scholar 

  64. Walker KJ, Preston CD, Boon CR (2009) Fifty years of change in an area of intensive agriculture: plant trait responses to habitat modification and conservation, Bedfordshire, England. Biodivers Conserv 18:3597–3613. doi:10.1007/s10531-009-9662-y

    Article  Google Scholar 

  65. Waloff N, Blackith RE (1962) The growth and distribution of the mounds of Lasius flavus (Fabricius) (Hym: Formicidae) in Silwood Park, Berkshire. J Anim Ecol 31:421–437. doi:10.2307/2044

    Article  Google Scholar 

  66. Weiss SB, Murphy DD, White RR (1988) Sun, slope, and butterflies: topographic determinants of habitat quality for Euphydryas editha. Ecology 69:1486–1496

    Article  Google Scholar 

  67. Weking S, Hermann G, Fartmann T (2013) Effects of mire type, land use and climate on a strongly declining wetland butterfly. J Insect Conserv 17:1081–1091. doi:10.1007/s10841-013-9585-5

    Article  Google Scholar 

  68. Wichink Kruit R, Schaap M, Segers A, Heslinga D, Builtjes P, Banzhaf S, Scheuschner T (2014) Modelling and mapping of atmospheric nitrogen and sulphur deposition and critical loads for ecosystem specific assessment of threats to biodiversity in Germany – PINETI (Pollutant INput and EcosysTem Impact). Substudy Report 1. Texte Umweltbundesamt 60/2014: 1–170

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Acknowledgments

We are very grateful to the Akademie für ökologische Landeserforschung e.V. for partly funding this study. Moreover, we like to thank an anonymous reviewer for valuable comments on an earlier version of the manuscript.

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The study was partly supported by the Akademie für ökologische Landeserforschung e.V.

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Correspondence to Merle Streitberger.

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Streitberger, M., Fartmann, T. Vegetation heterogeneity caused by an ecosystem engineer drives oviposition-site selection of a threatened grassland insect. Arthropod-Plant Interactions 10, 545–555 (2016). https://doi.org/10.1007/s11829-016-9460-x

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Keywords

  • Calcareous grassland
  • Disturbance
  • Egg-laying
  • Hesperia comma
  • Lasius flavus
  • Microhabitat preference