Skip to main content

Advertisement

SpringerLink
Log in

Ants and plants as indicators of biodiversity, ecosystem services, and conservation value in constructed grasslands

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Grasslands are constructed for soil and wildlife conservation in agricultural landscapes across Europe and North America. Constructed grasslands may mitigate habitat loss for grassland-dependent animals and enhance ecosystem services that are important to agriculture. The responses of animal species richness and abundance to grassland habitat quality are often highly variable, however, and monitoring of multiple taxa is often not feasible. We evaluated whether multiple animal taxa responded to variation in constructed grassland habitats of southwest Ohio, USA, in ways that could be predicted from indicators based on quality assessment indices, Simpson diversity, and the species richness of ants and plants. The quality assessment indices included a widely used Floristic Quality Assessment (FQA) index, and a new Ant Quality Assessment (AntQA) index, both based on habitat specificity and species traits. The ant and plant indicators were used as predictor variables in separate general linear models of four target taxa—bees, beetles, butterflies and birds—with response variables of overall species richness and abundance, and subsets of taxa that included the abundance of ecosystem-service providers and grassland-associated species. Plant Simpson diversity was the best-fitting predictor variable in models of overall bee and beetle abundance, and the abundance of bees classified as ecosystem-service (ES) providers. FQA and plant richness were the best predictors of overall butterfly species richness and abundance. Ant species richness was the best predictor of overall bird species richness and abundance as well as the abundance of ES birds, while the AntQA index was the best predictor for the abundance of grassland bird and butterfly species. Thus, plant Simpson diversity and ant species richness were the most effective indicators for complementary components of grassland animal communities, whereas quality assessment indices were less robust as indicators and require more knowledge on the habitat specificity of individual ant and plant species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersen AN (1993) Ants as indicators of restoration success at a uranium mine in tropical Australia. Restor Ecol 1(3):156–167

    Article  Google Scholar 

  • Andersen AN, Majer JD (2004) Ants show the way down under: invertebrates as bioindicators in land management. Front Ecol Environ 2:291–298

    Article  Google Scholar 

  • Andreas BK, Mack JJ, McCormac JS (2004) Floristic Quality Assessment Index (FQAI) for vascular plants and mosses for the State of Ohio. Ohio Environmental Protection Agency, Division of Surface Water, Wetland Ecology Group, Columbus

    Google Scholar 

  • Aviron S, Burel F, Baudry J, Schermann N (2005) Carabid assemblages in agricultural landscapes: impacts of habitat features, landscape context at different spatial scales and farming intensity. Agr Ecosyst Environ 108:205–217

    Article  Google Scholar 

  • Barton K (2016) Model selection and model averaging based on information criteria (AICc and alike), ver 1.15.6. Available at https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf

  • Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Grothendieck G, Green P (2015) Linear mixed-effects models using ‘Eigen’ and S4, ver 1.1-8. Available at http://lme4.r-forge.r-project.org/

  • Bennett EM, Peterson GD, Gordon LJ (2009) Understanding relationships among multiple ecosystem services. Ecol Lett 12:1–11

    Article  Google Scholar 

  • Bestelmeyer B, Wiens JA (2001) Ant biodiversity in semarid landscape mosaics: the consequences of grazing vs natural heterogeneity. Ecol Appl 11:1123–1140

    Article  Google Scholar 

  • Billeter R, Liira J, Bailey D, Bugter R, Arens P, Augenstein I, Aviron S, Baudry J, Bukacek R, Burel FG, Cerny M, De Blust G, De Cock R, Diekötter T, Dietz H, Dirksen J, Dormann C, Durka W, Frenzel M, Hamersky R, Hendrickx F, Herzog F, Klotz S, Koolstra B, Lausch A, Le Coeur D, Maelfait JP, Opdam P, Roubalova M, Schermann A, Schermann N, Schmidt T, Schweiger O, Smulders MJM, Speelmans M, Simova P, Verboom J, van Wingerden W, Zobel M, Edwards PJ (2008) Indicators for biodiversity in agricultural landscapes: a pan-European study. J Appl Ecol 45:141–150

    Article  Google Scholar 

  • Bisevac L, Majer J (2002) Cost effectiveness and data-yield of biodiversity surveys. J R Soc West Austr 85:129–132

    Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Brennan LA, Kuvlesky WP (2005) North American grassland birds: an unfolding conservation crisis? J Wildl Manage 69:1–13

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Coovert G (2005) The ants of Ohio (Hymenoptera: Formicidae). Ohio Biological Survey Inc., Columbus

    Google Scholar 

  • Crist TO (2009) Biodiversity, species interactions, and functional roles of ants (Hymenoptera: Formicidae) in fragmented landscapes: a review. Myrmecol News 12:3–13

    Google Scholar 

  • Crist TO, Peters VE (2014) Landscape and local controls of insect biodiversity in conservation grasslands: implications for the conservation of ecosystem service providers in agricultural environments. Land 3:693–718

    Article  Google Scholar 

  • Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–112

    Article  CAS  PubMed  Google Scholar 

  • Dauber J, Wolters V (2005) Colonization of temperate grassland by ants. Basic Appl Ecol 6(1):83–91

    Article  Google Scholar 

  • Dickson TL, Busby WH (2009) Forb species establishment increases with decreased grass seeding density and with increased forb seeding density in a Northeast Kansas, U.S.A., experimental prairie restoration. Restor Ecol 17:597–605

    Article  Google Scholar 

  • Diepenbrock LM, Finke DL (2013) Refuge for native lady beetles (Coccinellidae) in perennial grassland habitats. Insect Conserv Diver 6:671–679

    Article  Google Scholar 

  • Duelli P, Obrist MK, Schmatz DR (1999) Biodiversity evaluation in agricultural landscapes: above-ground insects. Agr Ecosyst Environ 74:33–64

    Article  Google Scholar 

  • Ellison AM (2012) Out of Oz: opportunities and challenges for using ants as biological indicators in north-temperate cold biomes. Myrmecol News 17:105–119

    Google Scholar 

  • Farhat YA, Janousek WM, McCarty JP, Rider N, Wolfenbarger LL (2014) Comparison of butterfly communities and abundances between marginal grasslands and conservation lands in the eastern Great Plains. J Insect Conserv 18:245–256

    Article  Google Scholar 

  • Freyman WA, Masters LA (2013) The universal floristic quality assessment (FQA) calculator. Available at http://universalFQA.org (accessed 17 Nov 2014)

  • Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carvalherio LG, Chacoff NP, Dudenhoffer JH, Greenleaf SS, Holzschuh A, Isaacs R, Krewenka K, Mandelik Y, MayfieldM M, Morandin LA, Potts SG, Ricketts TH, Szentgyorgyi H, Viana BF, Westphal C, Winfree R, Klein AM (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072

    Article  PubMed  Google Scholar 

  • Garibaldi LA, Carvalheiro LG, Leonhardt SD, Aizen MA, Blaauw BR, Isaacs R, Kuhlman M, Kleijn D, Klein AM, Kremen C, Morandin L, Scheper J, Winfree R (2014) From research to action: enhancing crop yield through wild pollinators. Front Ecol Environ 12:439–447

    Article  Google Scholar 

  • Harmon JP, Stephens EJ, Losey J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. J Insect Cons 11:85–94

    Article  Google Scholar 

  • Hayes M, Boyle P, Moran J, Gormally M (2015) Assessing the biodiversity value of wet grasslands: can selected plant and insect taxa be used as rapid indicators of species richness at a local scale? Biodivers Conserv 24:2535–2549

    Article  Google Scholar 

  • Herman KD, Masters LA, Penskar MR, Reznicek AA, Wilhelm GS, Brodovich WW, Gardiner KP (2001) Floristic quality assessment with wetland categories and examples of computer applications for the state of Michigan—Revised, 2nd edn. Michigan Department of Natural Resources, Wildlife, Natural Heritage Program, Lansing

    Google Scholar 

  • Hill JG, Brown RL (2010) The ant (Hymenoptera: Formicidae) Fauna of Black Belt prairie remnants in Alabama and Mississippi. Southeast Nat 9:73–84

    Article  Google Scholar 

  • Hodgson JA, Kunin WE, Thomas CD, Benton TG, Gabriel D (2010) Comparing organic farming and land sparing: optimizing yield and butterfly populations at a landscape scale. Ecol Lett 13:1358–1367

    Article  PubMed  Google Scholar 

  • Hoffmann BD, Andersen AN (2003) Responses of ants to disturbance in Australia, with particular reference to functional groups. Aust Ecol 28:444–464

    Article  Google Scholar 

  • Isaacs R, Tuell J, Fiedler A, Gardiner M, Landis D (2009) Maximizing arthropod-mediated ecosystem services in agricultural landscapes: the role of native plants. Front Ecol Environ 7:196–203

    Article  Google Scholar 

  • Jones GA, Sieving KE, Jacobson SK (2005) Avian diversity and functional insectivory in North-Central Florida farmlands. Conserv Biol 19:1234–1245

    Article  Google Scholar 

  • Karr JR (1991) Biological integrity: a long-neglected aspect of water resource management. Ecol Appl 1:66–84

    Article  Google Scholar 

  • Kimberling DN, Karr JR, Fore LS (2001) Measuring human disturbance using terrestrial invertebrates in the shrub-steppe of eastern Washington (USA). Ecol Indic 1:63–81

    Article  Google Scholar 

  • Kleijn D, Sutherland WJ (2003) How effective are European agri-environment schemes in conserving and promoting biodiversity? J Appl Ecol 40(6):947–969

    Article  Google Scholar 

  • Koivula MJ (2011) Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. ZooKeys 100:287–317

    Article  PubMed  Google Scholar 

  • Kutcher TE, Bried JT (2014) Adult Odonata conservatism as an indicator of freshwater wetland condition. Ecol Indic 38:31–39

    Article  Google Scholar 

  • Kwaiser KS, Hendrix SD (2008) Diversity and abundance of bees (Hymenoptera: Apiformes) in native and ruderal grasslands of agriculturally dominated landscapes. Agr Ecosyst Environ 124:200–204

    Article  Google Scholar 

  • Larochelle A, Larivière M (2003) A natural history of the ground-beetles (Coleoptera: Carabidae) of America north of Mexico. Pensoft, Sofia

    Google Scholar 

  • Larsen KJ, Work TW (2003) Differences in ground beetles (Coleoptera: Carabidae of original and reconstructed tallgrass prairies in northeastern Iowa, USA and impact of 3-year spring burn cycles. J Insect Conserv 7:153–166

    Article  Google Scholar 

  • Lotts K, Naberhaus T (2015) Butterflies and moths of North America. http://www.butterfliesandmoths.org/

  • Lövei GL, Sunderland KD (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu Rev Entomol 41:231–256

    Article  PubMed  Google Scholar 

  • Luff ML, Eyre MD, Rushton SP (1992) Classification and prediction of grassland habitats using ground beetles (Coleoptera, Carabidae). J Environ Manage 35:301–315

    Article  Google Scholar 

  • Magurran AE (2004) Measuring biological diversity. Blackwell, Oxford

    Google Scholar 

  • Maj A (2011) Goodness-of-fit measures for linear mixed models with one level of grouping, ver 1.0. Available at http://finzi.psych.upenn.edu/library/lmmfit/html/lmmR2.html

  • Mazerolle M (2015) Model selection and multimodel inference base on (Q)AIC(c), ver 2.0-2. Available at http://cran.r-project.org/web/packages/AICcmodavg/

  • McGeoch MA (1998) The selection, testing and application of terrestrial insects as bioindicators. Biol Rev 73:181–201

    Article  Google Scholar 

  • Michener CD (2007) The bees of the world, 2nd edn. The John Hopkins University Press, Baltimore

    Google Scholar 

  • Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: synthesis. Island Press, Washington, DC

    Google Scholar 

  • Morecroft MD, Masters GJ, Brown VK, Clarke IP, Taylor ME, Whitehouse AT (2004) Changing precipitation patterns alter plant community dynamics and succession in an ex-arable grassland. Funct Ecol 18:648–655

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Öckinger E, Schweiger O, Crist TO, Debinski DM, Krauss J, Kuussaari M, Petersen JD, Pöyry J, Settele J, Summerville KS, Bommarco R (2010) Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol Lett 13(8):969–979

    PubMed  Google Scholar 

  • Panzer R, Schwartz MW (1988) Effectiveness of a vegetation-based approach to insect conservation. Conserv Biol 12:693–702

    Article  Google Scholar 

  • Panzer R, Gnaedinger K, Derkovitz G (2010) The prevalence and status of conservative prairie and sand savanna insects in the Chicago Wilderness region. Nat Areas J 30:73–81

    Article  Google Scholar 

  • Pearman PB, Weber D (2007) Common species determine richness patterns in biodiversity indicator taxa. Biol Conserv 138:109–119

    Article  Google Scholar 

  • Peters VE, Greenberg R (2013) Fruit supplementation affects birds but not arthropod predation by birds in Costa Rican agroforestry systems. Biotropica 45:102–110

    Article  Google Scholar 

  • Petersen JD, Nault BA (2014) Landscape diversity moderates the effects of bee visitation frequency to flowers on crop production. J Appl Ecol 51:1347–1356

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New York

    Book  Google Scholar 

  • Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation. Chapman and Hall, London

    Google Scholar 

  • R Development Core Team (2015) The R Foundation for Statistical Computing, ver 3.2.1. Vienna, Austria: Vienna University of Technology. http://www.r-project.org/

  • Rainio J, Niemelä J (2003) Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers Conserv 12:487–506

    Article  Google Scholar 

  • Reed C (1996) List of insect species which may be tallgrass prairie specialists. Report to the US Fish and Wildlife Service and cooperating agencies. http://www.dnr.state.mn.us/pollinator_resources/

  • Ricketts TH, Daily GC, Ehrlich PR (2002) Does butterfly diversity predict moth diversity? Testing a popular indicator taxon at local scales. Biol Conserv 103:361–370

    Article  Google Scholar 

  • Rodrigues ASL, Brooks TM (2007) Shortcuts for biodiversity conservation planning: the effectiveness of surrogates. Annu Rev Ecol Evol Syst 38:713–737

    Article  Google Scholar 

  • Scheper J, Holzschuh A, Kuussaari M, Potts SG, Rundlof M, Smith HG, Kleijn D (2013) Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss—A meta-analysis. Ecol Lett 16:912–920

    Article  PubMed  Google Scholar 

  • Schlick-Steiner BC, Steiner FM, Moder K, Bruckner A, Fiedler K, Christian E (2006) Assessing ant assemblages: pitfall trapping versus nest counting (Hymenoptera, Formicidae). Insect Soc 53:274–281

    Article  Google Scholar 

  • Shuey JA, Metzler EH, Tungesvick K (2012) Moth communities correspond with plant communities in Midwestern (Indiana, USA) sand prairies and oak barrens and their degradation endpoints. A Midl Nat 167:273–284

    Article  Google Scholar 

  • Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology 79:2041–2056

    Article  Google Scholar 

  • Summerville KS, Ritter LM, Crist TO (2004) Moth taxa as indicators of lepidopteran biodiversity and habitat disturbance in eastern deciduous forests. Biol Cons 116:9–18

    Article  Google Scholar 

  • Swanson DA, Scott DP, Risley DL (1999) Wildlife benefits of the Conservation Reserve Program in Ohio. J Soil Water Conserv 54:390–394

    Google Scholar 

  • Swengel AB (1996) Effects of fire and hay management on abundance of prairie butterflies. Biol Conserv 76:73–85

    Article  Google Scholar 

  • Taft JB, Hauser C, Robertson KR (2006) Estimating floristic integrity in tallgrass prairie. Biol Conserv 131:42–51

    Article  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—Ecosystem services management. Ecol Lett 8:857–874

    Article  Google Scholar 

  • Underwood EC, Fisher BL (2006) The role of ants in conservation monitoring: If, when, and how. Biol Conserv 132:166–182

    Article  Google Scholar 

  • Wallner AM, Molano-Flores B, Dietrich CH (2013a) Evaluating hill prairie quality in the Midwestern United States using Auchenorrhyncha (Insecta: Hemiptera) and vascular plants: a case study in implementing grassland conservation planning and management. Biodivers Conserv 22:615–637

    Article  Google Scholar 

  • Wallner AM, Molano-Flores B, Dietrich CH (2013b) Using Auchenorrhyncha (Insecta: Hemiptera) to develop a new insect index in measuring North American tallgrass prairie quality. Ecol Indic 25:58–64

    Article  Google Scholar 

  • Waloff N (1980) Studies on grassland leafhoppers (Auchenorrhyncha, Homoptera) and their natural enemies. Adv Ecol Res 11:81–215

    Article  Google Scholar 

  • Werling BP, Dickson TL, Isaacs R, Gaines H, Gratton C, Gross KL, Liere H, Malmstrom CM, Meehan TD, Ruan L, Robertson BA, Robertson GP, Schmidt TM, Schrotenboer AC, Teal TK, Wilson JK, Landis DA (2014) Perennial grasslands enhance biodiversity and ecosystem services in bioenergy landscapes. Proc Nat Acad Sci 111:1652–1657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiens J, Fargione J, Hill J (2011) Biofuels and biodiversity. Ecol Appl 21:1085–1095

    Article  PubMed  Google Scholar 

  • Willand JE, Wodika BR (2011) Diversity of ground beetles (Coleoptera: Carabidae) in relation to habitat type in West-Central Illinois. Am Midl Nat 166:266–282

    Article  Google Scholar 

  • Wilsey BJ, Chalcraft DR, Bowles CM, Willig MR (2005) Relationships among indices suggest that richness is an incomplete surrogate for grassland biodiversity. Ecology 86:1178–1184

    Article  Google Scholar 

  • With KA, King AW, Jensen WE (2008) Remaining large grasslands may not be sufficient to prevent grassland bird declines. Biol Conserv 141:3152–3167

    Article  Google Scholar 

  • Yanahan AD, Taylor SJ (2014) Vegetative communities as indicators of ground beetle (Coleoptera: Carabidae) diversity. Biodivers Conserv 23:1591–1609

    Article  Google Scholar 

Download references

Acknowledgments

We thank Sam Stephenson and David Russell for field assistance, Natalie Konig, Aaron Coleman, and Anita Schaefer for lab assistance, Michael Minnick for bee identification, Jason Nelson for assistance with lab, field, and identification, and Alan Cady for mentoring of REU students. Butterfly, plant, and ant components were funded in part through the National Science Foundation REU site Ecology in Human-Dominated Landscapes at Miami University (Grants DBI-0754991 and DBI-1156703). Ant components were additionally funded by grants from the Ohio Biological Survey and Prairie Biotic Research, Inc. We thank many private landowners, MetroParks of Butler County, Talawanda high school, and Miller Coors Brewery for field site permission. Lastly, we thank two anonymous reviewers for thoughtful feedback that improved an earlier version of this manuscript.

Author information

Author notes

  1. Valerie E. Peters

    Present address: Department of Biological Sciences, Eastern Kentucky University, Richmond, KY, USA

Authors and Affiliations

  1. Department of Biology, Miami University, Oxford, OH, USA

    Valerie E. Peters, Kaitlin U. Campbell, Garrett Dienno, Mayrolin García, Emaly Leak, Christina Loyke, Bruce Steinly & Thomas O. Crist

  2. Institute for the Environment and Sustainability, Miami University, Oxford, OH, USA

    Valerie E. Peters & Megan Ogle

  3. Department of Entomology and Plant Pathology, Auburn University, Auburn, AL, USA

    Mayrolin García

  4. Department of Fisheries and Wildlife, Michigan State University, Ann Arbor, MI, USA

    Emaly Leak

Authors
  1. Valerie E. Peters
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaitlin U. Campbell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Garrett Dienno
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mayrolin García
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emaly Leak
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christina Loyke
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Megan Ogle
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bruce Steinly
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Thomas O. Crist
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valerie E. Peters.

Additional information

Communicated by David Hawksworth.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peters, V.E., Campbell, K.U., Dienno, G. et al. Ants and plants as indicators of biodiversity, ecosystem services, and conservation value in constructed grasslands. Biodivers Conserv 25, 1481–1501 (2016). https://doi.org/10.1007/s10531-016-1120-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-016-1120-z

Keywords

Search

Navigation