Abstract
Ecosystem restoration provides unique opportunities to study community dynamics under succession and can reveal how consumer communities re-assemble and respond to successional changes. Studying community dynamics from both taxonomic and functional trait perspectives also may provide more robust assessments of restoration progress or success and allow cross-system comparisons. We studied ground beetle (Coleoptera: Carabidae) communities for three years in a restored grassland chronosequence with sites from 0 to 28 years old. We measured traditional community metrics (abundance, richness, Shannon diversity) and functional trait metrics based on species’ body length, wing morphology, activity time, phenology, and diet. Communities had high species richness and abundance in early successional stages, but these declined in later stages to low levels comparable to an adjacent grassland remnant. Species composition also shifted with time, converging with the remnant. Although functional richness, like species richness, declined as succession progressed, functional divergence quickly increased and was maintained over time, suggesting niche differentiation in established communities. Young sites were typified by small, macropterous, phytophagous species, while older sites contained larger species more likely to be flightless and carnivorous. Prescribed burns also affected traits, decreasing prevalence of larger species. This study demonstrates that functionally diverse consumer communities can self-assemble under restoration practices. In a relatively short amount of time both morphological and trophic level diversity are established. However, prescribed fire intended to control non-desirable plants may also shape beetle community functional composition, and restoration managers should consider if plant community benefits of fire outweigh potential declines in consumer function.
Similar content being viewed by others
References
Arnett RH, Thomas MC, Skelley PE, Frank JH (2002) American beetles. Polyphaga: Scarabaeoidea through Curculionoidea, vol II, 1 edn. CRC Press, Boca Raton
Barber NA, Jones HP, Duvall MR et al (2016) Phylogenetic diversity is maintained despite richness losses over time in restored tallgrass prairie plant communities. J Appl Ecol. doi:10.1111/1365-2664.12639
Bates D, Maechler M, Bolker B (2012) lme4: linear mixed-effects models using S4 classes
Bhowmik PC, Bekech MM (1993) Horseweed (Conyza canadensis) seed production, emergence, and distribution in no-tillage and conventional-tillage corn (Zea mays). Agron Trends Agric Sci 1:67–71
Blubaugh CK, Hagler JR, Machtley SA, Kaplan I (2016) Cover crops increase foraging activity of omnivorous predators in seed patches and facilitate weed biological control. Agric Ecosyst Environ 231:264–270. doi:10.1016/j.agee.2016.06.045
Bohan DA, Boursault A, Brooks DR, Petit S (2011) National-scale regulation of the weed seedbank by carabid predators. J Appl Ecol 48:888–898. doi:10.1111/j.1365-2664.2011.02008.x
Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi:10.1016/j.tree.2008.10.008
Bousquet Y (2010) Illustrated identification guide to adults and larvae of northeastern North America ground beetles. Pensoft Pub, Sofia
Cadotte MW, Cavender-Bares J, Tilman D, Oakley TH (2009) Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4:e5695
Camill P, McKone MJ, Sturges ST et al (2004) Community-and ecosystem-level changes in a species-rich tallgrass prairie restoration. Ecol Appl 14:1680–1694
Cárdenas AM, Buddle CM (2008) Introduced and native ground beetle assemblages (Coleoptera: Carabidae) along a successional gradient in an urban landscape. J Insect Conserv 13:151–163. doi:10.1007/s10841-008-9137-6
Carter DL, Blair JM (2012) Recovery of native plant community characteristics on a chronosequence of restored prairies seeded into pastures in West-Central Iowa. Restor Ecol 20:170–179
Chao A, Gotelli NJ, Hsieh TC et al (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67
Ciegler JC (2000) Ground beetles and wrinkled bark beetles of South Carolina: (Coleoptera: Geadephaga: Carabidae and Rhysodidae). Clemson University
Clements FE (1916) Plant succession: an analysis of the development of vegetation. Carnegie Institution of Washington
Dahms H, Lenoir L, Lindborg R et al (2010) Restoration of seminatural grasslands: what is the impact on ants? Restor Ecol 18:330–337
de Bello F, Lavorel S, Díaz S et al (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893. doi:10.1007/s10531-010-9850-9
Díaz S, Noy-Meir I, Cabido M (2001) Can grazing response of herbaceous plants be predicted from simple vegetative traits? J Appl Ecol 38:497–508
Díaz S, Fargione J, Chapin FS III, Tilman D (2006) Biodiversity loss threatens human well-being. PLoS Biol 4:e277
Duffy JE (2002) Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–219
Fountain-Jones NM, Baker SC, Jordan GJ (2015) Moving beyond the guild concept: developing a practical functional trait framework for terrestrial beetles. Ecol Entomol 40:1–13. doi:10.1111/een.12158
Gaines HR, Gratton C (2010) Seed predation increases with ground beetle diversity in a Wisconsin (USA) potato agroecosystem. Agric Ecosyst Environ 137:329–336
Gerisch M, Agostinelli V, Henle K, Dziock F (2012) More species, but all do the same: contrasting effects of flood disturbance on ground beetle functional and species diversity. Oikos 121:508–515
Gleason HA (1927) Further views on the succession-concept. Ecology 8:299–326
Grman E, Bassett T, Brudvig LA (2013) Confronting contingency in restoration: management and site history determine outcomes of assembling prairies, but site characteristics and landscape context have little effect. J Appl Ecol 50:1234–1243
Hance T (1987) Predation impact of carabids at different population densities on Aphis fabae development in sugar beet. Pedobiologia 30:251–262
Hansen MJ, Gibson DJ (2014) Use of multiple criteria in an ecological assessment of a prairie restoration chronosequence. Appl Veg Sci 17:63–73. doi:10.1111/avsc.12051
Hemerik L, Brussaard L (2002) Diversity of soil macro-invertebrates in grasslands under restoration succession. Eur J Soil Biol 38:145–150
Hilderbrand RH, Watts AC, Randle AM (2005) The myths of restoration ecology. Ecol Soc 10:19
Hobbs RJ, Norton DA (1996) Towards a conceptual framework for restoration ecology. Restor Ecol 4:93–110
Holliday NJ (1991) Species responses of carabid beetles (Coleoptera: Carabidae) during post-fire regeneration of boreal forest. Can Entomol 123:1369–1389. doi:10.4039/Ent1231369-6
Honek A, Martinkova Z, Saska P, Pekar S (2007) Size and taxonomic constraints determine the seed preferences of Carabidae (Coleoptera). Basic Appl Ecol 8:343–353
Kahmen S, Poschlod P (2004) Plant functional trait responses to grassland succession over 25 years. J Veg Sci 15:21–32
Kotze DJ, O’Hara RB, Lehvävirta S (2012) Dealing with varying detection probability, unequal sample sizes and clumped distributions in count data. PLoS ONE 7:e40923. doi:10.1371/journal.pone.0040923
Kromp B (1999) Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Agric Ecosyst Environ 74:187–228
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Laliberté E, Legendre P, Shipley B, Laliberté ME (2014) Package ‘FD.’ Version 1:12
Lang A (2003) Intraguild interference and biocontrol effects of generalist predators in a winter wheat field. Oecologia 134:144–153
Lang A, Filser J, Henschel JR (1999) Predation by ground beetles and wolf spiders on herbivorous insects in a maize crop. Agric Ecosyst Environ 72:189–199
Larochelle A, Larivière M-C (2003) Natural history of the ground-beetles (Coleoptera: Carabidae) of America north of Mexico
Lebrija-Trejos E, Pérez-García EA, Meave JA et al (2010) Functional traits and environmental filtering drive community assembly in a species-rich tropical system. Ecology 91:386–398
Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Springer, Dordrecht
Magura T, Tóthmérész B, Molnár T (2004) Changes in carabid beetle assemblages along an urbanisation gradient in the city of Debrecen, Hungary. Landsc Ecol 19:747–759. doi:10.1007/s10980-005-1128-4
Mason NW, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118
McAlpine C, Catterall CP, Nally RM et al (2016) Integrating plant- and animal-based perspectives for more effective restoration of biodiversity. Front Ecol Environ 14:37–45. doi:10.1002/16-0108.1
McCravy KW, Lundgren JG (2011) Carabid beetles (Coleoptera: Carabidae) of the Midwestern United States: a review and synthesis of recent research. Terr Arthropod Rev 4:63–94
McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185
Messer PW (2009) An annotated checklist of Wisconsin ground beetles (Coleoptera: Carabidae). Gt Lakes Entomol 42:30–61
Moretti M, Bello F, Ibanez S et al (2013) Linking traits between plants and invertebrate herbivores to track functional effects of land-use changes. J Veg Sci 24:949–962
Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876. doi:10.1111/j.1365-2435.2010.01695.x
Murdock JN, Gido KB, Dodds WK et al (2010) Consumer return chronology alters recovery trajectory of stream ecosystem structure and function following drought. Ecology 91:1048–1062
Oksanen J, Kindt R, Legendre P et al (2007) The vegan package
Oliver I, Beattie AJ (1996) Invertebrate morphospecies as surrogates for species: a case study. Conserv Biol 10:99–109
Packard S, Mutel CF et al (1997) The tallgrass restoration handbook: for prairies, savannas and woodlands. DC, Island Press, Washington
Pakeman RJ, Stockan JA (2014) Drivers of carabid functional diversity: abiotic environment, plant functional traits, or plant functional diversity? Ecology 95:1213–1224
Palmer MA, Ambrose RF, Poff NLR (1997) Ecological theory and community restoration ecology. Restor Ecol 5:291–300
Panzer R (2002) Compatibility of prescribed burning with the conservation of insects in small, isolated prairie reserves. Conserv Biol 16:1296–1307. doi:10.1046/j.1523-1739.2002.01077.x
Pickett STA (1989) Space-for-time substitution as an alternative to long-lerm ltudies. Long-term studies in ecology. Springer, New York, pp 110–135
Pinheiro J, Bates D, DebRoy S, et al (2014) Linear and nonlinear mixed effects models. R Package Version 3:57
Pöyry J, Lindgren S, Salminen J, Kuussaari M (2004) Restoration of Butterfly and Moth Communities in Semi-Natural Grasslands by Cattle Grazing. Ecol Appl 14:1656–1670. doi:10.1890/03-5151
Pöyry J, Luoto M, Paukkunen J et al (2006) Different responses of plants and herbivore insects to a gradient of vegetation height: an indicator of the vertebrate grazing intensity and successional age. Oikos 115:401–412
Pöyry J, Paukkunen J, Heliölä J, Kuussaari M (2009) Relative contributions of local and regional factors to species richness and total density of butterflies and moths in semi-natural grasslands. Oecologia 160:577–587. doi:10.1007/s00442-009-1328-7
Pryke JS, Samways MJ (2012) Importance of using many taxa and having adequate controls for monitoring impacts of fire for arthropod conservation. J Insect Conserv 16:177–185. doi:10.1007/s10841-011-9404-9
Retana J, Arnan X, Cerdá X (2015) A multidimensional functional trait analysis of resource exploitation in European ants. Ecology 96:2781–2793
Rowe HI (2010) Tricks of the Trade: Techniques and Opinions from 38 Experts in Tallgrass Prairie Restoration. Restor Ecol 18:253–262. doi:10.1111/j.1526-100X.2010.00663.x
Samson F, Knopf F (1994) Prairie conservation in North America. Bioscience 44:418–421
Samson FB, Knopf FL (1996) Prairie conservation: preserving North America’s most endangered ecosystem. Island Press, Washington, DC
Schirmel J, Blindow I, Buchholz S (2012) Life-history trait and functional diversity patterns of ground beetles and spiders along a coastal heathland successional gradient. Basic Appl Ecol 13:606–614
Sluis WJ (2002) Patterns of species richness and composition in re-created grassland. Restor Ecol 10:677–684. doi:10.1046/j.1526-100X.2002.01048.x
Steiner M, Öckinger E, Karrer G et al (2016) Restoration of semi-natural grasslands, a success for phytophagous beetles (Curculionidae). Biodivers Conserv 25:3005–3022. doi:10.1007/s10531-016-1217-4
Suding KN (2011) Toward an era of restoration in ecology: successes, failures, and opportunities ahead. Annu Rev Ecol Evol Syst 42:465–487
Török P, Vida E, Deák B et al (2011) Grassland restoration on former croplands in Europe: an assessment of applicability of techniques and costs. Biodivers Conserv 20:2311–2332. doi:10.1007/s10531-011-9992-4
Van Andel J, Aronson J (2012) Restoration ecology: the new frontier. Wiley, New York
van Noordwijk CGE, Baeten L, Turin H et al (2017) 17 years of grassland management leads to parallel local and regional biodiversity shifts among a wide range of taxonomic groups. Biodivers Conserv 26:717–734. doi:10.1007/s10531-016-1269-5
Vandewalle M, De Bello F, Berg MP et al (2010) Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodivers Conserv 19:2921–2947
Villéger S, Mason NW, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301
Villéger S, Miranda JR, Hernández DF, Mouillot D (2010) Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecol Appl 20:1512–1522
Violle C, Navas M-L, Vile D et al (2007) Let the concept of trait be functional! Oikos 116:882–892
WallisDeVries MF, Ens SH (2010) Effects of habitat quality and isolation on the colonization of restored heathlands by butterflies. Restor Ecol 18:390–398
WallisDeVries MF, Poschlod P, Willems JH (2002) Challenges for the conservation of calcareous grasslands in northwestern Europe: integrating the requirements of flora and fauna. Biol Conserv 104:265–273. doi:10.1016/S0006-3207(01)00191-4
Weaver SE (2001) The biology of Canadian weeds. 115. Conyza canadensis. Can J Plant Sci 81:867–875. doi:10.4141/P00-196
Willand JE, Baer SG, Gibson DJ, Klopf RP (2013) Temporal dynamics of plant community regeneration sources during tallgrass prairie restoration. Plant Ecol 214:1169–1180
Wodika BR, Baer SG (2015) If we build it, will they colonize? A test of the field of dreams paradigm with soil macroinvertebrate communities. Appl Soil Ecol 91:80–89. doi:10.1016/j.apsoil.2015.02.005
Wodika BR, Klopf RP, Baer SG (2014) Colonization and recovery of invertebrate ecosystem engineers during prairie restoration. Restor Ecol 22:456–464
Woodcock BA, Vogiatzakis IN, Westbury DB et al (2010) The role of management and landscape context in the restoration of grassland phytophagous beetles. J Appl Ecol 47:366–376
Woodcock BA, Bullock JM, Mortimer SR, Pywell RF (2012) Limiting factors in the restoration of UK grassland beetle assemblages. Biol Conserv 146:136–143
Woodcock BA, Harrower C, Redhead J et al (2014) National patterns of functional diversity and redundancy in predatory ground beetles and bees associated with key UK arable crops. J Appl Ecol 51:142–151
Young TP, Chase JM, Huddleston RT (2001) Community succession and assembly: comparing, contrasting and combining paradigms in the context of ecological restoration. Ecol Restor 19:5–18
Acknowledgements
The Nature Conservancy and the staff and volunteers at Nachusa Grasslands provided invaluable support for this research. We also thank the numerous undergraduates who provided field and laboratory assistance. This study was funded by Friends of Nachusa Grasslands, NIU Office of Student Engagement and Experiential Learning, WIU School of Graduate Studies, and Prairie Biotic Research, Inc.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Jens Wolfgang Dauber.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Barber, N.A., Lamagdeleine-Dent, K.A., Willand, J.E. et al. Species and functional trait re-assembly of ground beetle communities in restored grasslands. Biodivers Conserv 26, 3481–3498 (2017). https://doi.org/10.1007/s10531-017-1417-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-017-1417-6