Restoration increases bee abundance and richness but not pollination in remnant and post-agricultural woodlands

Breland, Sabrie; Turley, Nash E.; Gibbs, Jason; Isaacs, Rufus; Brudvig, Lars A.

doi:10.1002/ecs2.2435

Title: Restoration increases bee abundance and richness but not pollination in remnant and post-agricultural woodlands

Journal Article · Wed Sep 19 00:00:00 EDT 2018 · Ecosphere

DOI:https://doi.org/10.1002/ecs2.2435· OSTI ID:1471549

^[1]; Turley, Nash E. ^[1]; Gibbs, Jason ^[1]; Isaacs, Rufus ^[1]; Brudvig, Lars A. ^[1]

Michigan State University, East Lansing, MI (United States)

Human land use, including agriculture, is a leading contributor to declining biodiversity worldwide and can leave long-lasting legacies on ecosystems after cessation. Ecological restoration is an approach to mitigate these impacts. However, little is known about how animal communities and plant–animal interactions respond to the combined effects of land-use legacies and restoration. We investigated how restoration and agricultural history affect bee (Hymenoptera: Apoidea: Anthophila) communities and pollination function. In 27 paired remnant (no history of agriculture) and post-agricultural longleaf pine (Pinus palustris Mill.) woodlands, we established 4–10 1-ha plots (126 total) and experimentally restored half of them, while the other half were left as unrestored controls. Restoration was accomplished through canopy thinning which reinstates open savanna-like conditions. We collected bees in each plot using a combination of bowl trapping and standardized netting transects. Thinning increased bee abundance by 169% and bee richness by 110%, but agricultural land use had no effect on these variables. Bee community composition was affected by restoration and was marginally affected by agricultural history. To measure pollination function, we conducted a sentinel plant experiment in which potted black mustard (Brassica nigra L.) plants were placed out in a subset of these sites (n = 10) and either bagged to exclude pollinators or left open for pollinator access. Then, we measured fruit and seed set of sentinel plants to compare pollination function among the restoration and land-use history treatments. Seed set and fruit set of sentinel plants were higher in open than bagged plants, indicating that this model system effectively measured pollination, but we found no differences in pollination based on restoration or agricultural history. These results indicate that although pollinator communities may show clear responses to restoration that are largely independent of prior land-use impacts, this does not necessarily translate into differences in pollination function after restoration.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Environmental Management (EM); United States Forest Service (USFS)

Grant/Contract Number:: AI09-00SR22188; EM0003622

OSTI ID:: 1471549

Alternate ID(s):: OSTI ID: 1483358

Report Number(s):: 18-04-P; 18-04-P

Journal Information:: Ecosphere, Vol. 9, Issue 9; ISSN 2150-8925

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 20 works

Citation information provided by
Web of Science

References (63)

A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems Kennedy, Christina M.; Lonsdorf, Eric; Neel, Maile C. Ecology Letters, Vol. 16, Issue 5 https://doi.org/10.1111/ele.12082	journal	March 2013
The restoration of ecological interactions: plant-pollinator networks on ancient and restored heathlands: Plant-pollinator networks on heathlands Forup, Mikael Lytzau; Henson, Kate S. E.; Craze, Paul G. Journal of Applied Ecology, Vol. 45, Issue 3 https://doi.org/10.1111/j.1365-2664.2007.01390.x	journal	November 2007
Associations between species and groups of sites: indices and statistical inference Cáceres, Miquel De; Legendre, Pierre Ecology, Vol. 90, Issue 12 https://doi.org/10.1890/08-1823.1	journal	December 2009
The ecology of solitary bees Linsley, E. Gorton Hilgardia, Vol. 27, Issue 19 https://doi.org/10.3733/hilg.v27n19p543	journal	October 1958
How many flowering plants are pollinated by animals? Ollerton, Jeff; Winfree, Rachael; Tarrant, Sam Oikos, Vol. 120, Issue 3 https://doi.org/10.1111/j.1600-0706.2010.18644.x	journal	February 2011
Restoring the Ground Layer of Longleaf Pine Ecosystems Walker, Joan L.; Silletti, Andrea M. Springer Series on Environmental Management https://doi.org/10.1007/978-0-387-30687-2_10	book	January 2007
Vegetation changes and land-use legacies of depression wetlands of the western coastal plain of South Carolina: 1951–1992 Kirkman, L. Katherine; Lide, Robert F.; Wein, Gary Wetlands, Vol. 16, Issue 4 https://doi.org/10.1007/BF03161347	journal	December 1996
Morphological and molecular delineation of a new species in the Ceratina dupla species-group (Hymenoptera: Apidae: Xylocopinae) of eastern North America Rehan, Sandra M.; Sheffield, Cory S. Zootaxa, Vol. 2873, Issue 1 https://doi.org/10.11646/zootaxa.2873.1.3	journal	May 2011
Elevated pan traps to monitor bees in flowering crop canopies Tuell, Julianna K.; Isaacs, Rufus Entomologia Experimentalis et Applicata, Vol. 131, Issue 1 https://doi.org/10.1111/j.1570-7458.2009.00826.x	journal	April 2009
Landscape perspectives on agricultural intensification and biodiversity â€“ ecosystem service management Tscharntke, Teja; Klein, Alexandra M.; Kruess, Andreas Ecology Letters, Vol. 8, Issue 8 https://doi.org/10.1111/j.1461-0248.2005.00782.x	journal	August 2005
Wild bee community change over a 26-year chronosequence of restored tallgrass prairie: Bee communities of restored tallgrass prairie Griffin, Sean R.; Bruninga-Socolar, Bethanne; Kerr, Morgan A. Restoration Ecology, Vol. 25, Issue 4 https://doi.org/10.1111/rec.12481	journal	January 2017
Alternative states and positive feedbacks in restoration ecology Suding, Katharine N.; Gross, Katherine L.; Houseman, Gregory R. Trends in Ecology & Evolution, Vol. 19, Issue 1 https://doi.org/10.1016/j.tree.2003.10.005	journal	January 2004
Regrowth forests on abandoned agricultural land: A review of their habitat values for recovering forest fauna Bowen, Michiala E.; McAlpine, Clive A.; House, Alan P. N. Biological Conservation, Vol. 140, Issue 3-4 https://doi.org/10.1016/j.biocon.2007.08.012	journal	December 2007
Post-Agricultural Succession in El Peten, Guatemala Ferguson, Bruce G.; Vandermeer, John; Morales, Helda Conservation Biology, Vol. 17, Issue 3 https://doi.org/10.1046/j.1523-1739.2003.01265.x	journal	June 2003
Weather During Bloom Affects Pollination and Yield of Highbush Blueberry Tuell, Julianna K.; Isaacs, Rufus Journal of Economic Entomology, Vol. 103, Issue 3 https://doi.org/10.1603/EC09387	journal	June 2010
Strong legacy of agricultural land use on soils and understory plant communities in longleaf pine woodlands Brudvig, Lars A.; Grman, Emily; Habeck, Christopher W. Forest Ecology and Management, Vol. 310 https://doi.org/10.1016/j.foreco.2013.09.053	journal	December 2013
Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances Zurbuchen, Antonia; Landert, Lisa; Klaiber, Jeannine Biological Conservation, Vol. 143, Issue 3 https://doi.org/10.1016/j.biocon.2009.12.003	journal	March 2010
Agricultural landscapes with organic crops support higher pollinator diversity Holzschuh, Andrea; Steffan-Dewenter, Ingolf; Tscharntke, Teja Oikos, Vol. 117, Issue 3 https://doi.org/10.1111/j.2007.0030-1299.16303.x	journal	March 2008
Global pollinator declines: trends, impacts and drivers Potts, Simon G.; Biesmeijer, Jacobus C.; Kremen, Claire Trends in Ecology & Evolution, Vol. 25, Issue 6 https://doi.org/10.1016/j.tree.2010.01.007	journal	June 2010
History and Future of the Longleaf Pine Ecosystem Frost, Cecil Springer Series on Environmental Management https://doi.org/10.1007/978-0-387-30687-2_2	book	January 2007
Floral and nesting resources, habitat structure, and fire influence bee distribution across an open-forest gradient Grundel, Ralph; Jean, Robert P.; Frohnapple, Krystalynn J. Ecological Applications, Vol. 20, Issue 6 https://doi.org/10.1890/08-1792.1	journal	September 2010
Removing an invasive shrub (Chinese privet) increases native bee diversity and abundance in riparian forests of the southeastern United States: Bee diversity and abundance in riparian forests Hanula, James L.; Horn, Scott Insect Conservation and Diversity, Vol. 4, Issue 4 https://doi.org/10.1111/j.1752-4598.2011.00131.x	journal	January 2011
Larger patches of diverse floral resources increase insect pollinator density, diversity, and their pollination of native wildflowers Blaauw, Brett R.; Isaacs, Rufus Basic and Applied Ecology, Vol. 15, Issue 8 https://doi.org/10.1016/j.baae.2014.10.001	journal	December 2014
Historical land use and present-day canopy thinning differentially affect the distribution and abundance of invasive and native ant species Stuhler, John D.; Orrock, John L. Biological Invasions, Vol. 18, Issue 7 https://doi.org/10.1007/s10530-016-1122-5	journal	March 2016
Agricultural land-use history increases non-native plant invasion in a southern Appalachian forest a century after abandonment Kuhman, Timothy R.; Pearson, Scott M.; Turner, Monica G. Canadian Journal of Forest Research, Vol. 41, Issue 5 https://doi.org/10.1139/x11-026	journal	May 2011
Bees and Butterflies in Burned and Unburned Alvar Woodland: Evidence for the Importance of Postfire Succession to Insect Pollinator Diversity in an Imperiled Ecosystem Taylor, Alana N.; Catling, Paul M. The Canadian Field-Naturalist, Vol. 125, Issue 4 https://doi.org/10.22621/cfn.v125i4.1258	journal	October 2011
Effects of black mustard population size on the taxonomic composition of pollinators Conner, Jeffrey K.; Neumeier, Rachel Oecologia, Vol. 104, Issue 2 https://doi.org/10.1007/BF00328586	journal	October 1995
A general and simple method for obtaining R ² from generalized linear mixed-effects models Nakagawa, Shinichi; Schielzeth, Holger Methods in Ecology and Evolution, Vol. 4, Issue 2 https://doi.org/10.1111/j.2041-210x.2012.00261.x	journal	December 2012
ENDANGERED MUTUALISMS: The Conservation of Plant-Pollinator Interactions Kearns, Carol A.; Inouye, David W.; Waser, Nickolas M. Annual Review of Ecology and Systematics, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.ecolsys.29.1.83	journal	November 1998
Spatial arrangement of canopy structure and land-use history alter the effect that herbivores have on plant growth Hahn, Philip G.; Orrock, John L. Ecosphere, Vol. 6, Issue 10 https://doi.org/10.1890/ES15-00036.1	journal	October 2015
Removing an exotic shrub from riparian forests increases butterfly abundance and diversity Hanula, James L.; Horn, Scott Forest Ecology and Management, Vol. 262, Issue 4 https://doi.org/10.1016/j.foreco.2011.04.040	journal	August 2011
Bee foraging ranges and their relationship to body size Greenleaf, Sarah S.; Williams, Neal M.; Winfree, Rachael Oecologia, Vol. 153, Issue 3 https://doi.org/10.1007/s00442-007-0752-9	journal	May 2007
Freshwater biodiversity: importance, threats, status and conservation challenges Dudgeon, David; Arthington, Angela H.; Gessner, Mark O. Biological Reviews, Vol. 81, Issue 02 https://doi.org/10.1017/S1464793105006950	journal	December 2005
Historical land use and stand age effects on forest soil properties in the Mid-Atlantic US Yesilonis, I.; Szlavecz, K.; Pouyat, R. Forest Ecology and Management, Vol. 370 https://doi.org/10.1016/j.foreco.2016.03.046	journal	June 2016
Irreversible Impact of past land use on Forest Soils and Biodiversity Dupouey, J. L.; Dambrine, E.; Laffite, J. D. Ecology, Vol. 83, Issue 11 https://doi.org/10.1890/0012-9658(2002)083[2978:IIOPLU]2.0.CO;2	journal	November 2002
Revision and reclassification of <i>Lasioglossum</i> (<i>Evylaeus</i>), <i>L.</i> (<i>Hemihalictus</i>) and <i>L.</i> (<i>Sphecodogastra</i>) in eastern North America (Hymenoptera: Apoidea: Halictidae) Gibbs, Jason; Packer, Laurence; Dumesh, Sheila Zootaxa, Vol. 3672, Issue 1 https://doi.org/10.11646/zootaxa.3672.1.1	journal	June 2013
Non-bee insects are important contributors to global crop pollination Rader, Romina; Bartomeus, Ignasi; Garibaldi, Lucas A. Proceedings of the National Academy of Sciences, Vol. 113, Issue 1 https://doi.org/10.1073/pnas.1517092112	journal	November 2015
Spatial patterns of bee captures in North American bowl trapping surveys Droege, Sam; Tepedino, Vincent J.; Lebuhn, Gretchen Insect Conservation and Diversity, Vol. 3, Issue 1 https://doi.org/10.1111/j.1752-4598.2009.00074.x	journal	February 2010
Recovery of forest plant communities in post-agricultural landscapes Flinn, Kathryn M.; Vellend, Mark Frontiers in Ecology and the Environment, Vol. 3, Issue 5 https://doi.org/10.1890/1540-9295(2005)003[0243:ROFPCI]2.0.CO;2	journal	June 2005
Conserving Pollinators in North American Forests: A Review Hanula, James L.; Ulyshen, Michael D.; Horn, Scott Natural Areas Journal, Vol. 36, Issue 4 https://doi.org/10.3375/043.036.0409	journal	October 2016
Abundance of common species, not species richness, drives delivery of a real-world ecosystem service Winfree, Rachael; W. Fox, Jeremy; Williams, Neal M. Ecology Letters, Vol. 18, Issue 7 https://doi.org/10.1111/ele.12424	journal	May 2015
Colour-coded sampling: the pan trap colour preferences of oligolectic and nonoligolectic bees associated with a vernal pool plant Leong, JoaN. M.; Thorp, Robbin W. Ecological Entomology, Vol. 24, Issue 3 https://doi.org/10.1046/j.1365-2311.1999.00196.x	journal	August 1999
How global biodiversity hotspots may go unrecognized: lessons from the North American Coastal Plain Noss, Reed F.; Platt, William J.; Sorrie, Bruce A. Diversity and Distributions, Vol. 21, Issue 2 https://doi.org/10.1111/ddi.12278	journal	November 2014
Global environmental impacts of agricultural expansion: The need for sustainable and efficient practices Tilman, D. Proceedings of the National Academy of Sciences, Vol. 96, Issue 11 https://doi.org/10.1073/pnas.96.11.5995	journal	May 1999
Legacies of the agricultural past in the forested present: an assessment of historical land-use effects on rich mesic forests Bellemare, Jesse; Motzkin, Glenn; Foster, David R. Journal of Biogeography, Vol. 29, Issue 10-11 https://doi.org/10.1046/j.1365-2699.2002.00762.x	journal	October 2002
History of land-use intensity can modify the relationship between functional complexity of the soil fauna and soil ecosystem services – A microcosm study Liiri, M.; Häsä, M.; Haimi, J. Applied Soil Ecology, Vol. 55 https://doi.org/10.1016/j.apsoil.2011.12.009	journal	April 2012
A review of the bee genus Augochlorella (Hymenoptera: Halictidae: Augochlorini): Augochlorella (Halictidae) Coelho, B. W. T. Systematic Entomology, Vol. 29, Issue 3 https://doi.org/10.1111/j.0307-6970.2004.00243.x	journal	June 2004
Honeybees and Rapeseed: A Pollinator–Plant Interaction Abrol, D. P. Advances in Botanical Research https://doi.org/10.1016/S0065-2296(07)45012-1	book	January 2007
Land-Use History as Long-Term Broad-Scale Disturbance: Regional Forest Dynamics in Central New England Foster, David R.; Motzkin, Glenn; Slater, Benjamin Ecosystems, Vol. 1, Issue 1 https://doi.org/10.1007/s100219900008	journal	January 1998
Agricultural Legacies in Forest Environments: tree Communities, soil Properties, and Light Availability Flinn, Kathryn M.; Marks, P. L. Ecological Applications, Vol. 17, Issue 2 https://doi.org/10.1890/05-1963	journal	March 2007
Global environmental change effects on ecosystems: the importance of land-use legacies Perring, Michael P.; De Frenne, Pieter; Baeten, Lander Global Change Biology, Vol. 22, Issue 4 https://doi.org/10.1111/gcb.13146	journal	February 2016
Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini) Gibbs, Jason Zootaxa, Vol. 3073, Issue 1 https://doi.org/10.11646/zootaxa.3073.1.1	journal	October 2011
Agricultural land-use history causes persistent loss of plant phylogenetic diversity Turley, Nash E.; Brudvig, Lars A. Ecology, Vol. 97, Issue 9 https://doi.org/10.1002/ecy.1443	journal	September 2016
Restoration of Nontarget Species: Bee Communities and Pollination Function in Riparian Forests Williams, Neal M. Restoration Ecology, Vol. 19, Issue 4 https://doi.org/10.1111/j.1526-100X.2010.00707.x	journal	July 2010
Global effects of land use on local terrestrial biodiversity Newbold, Tim; Hudson, Lawrence N.; Hill, Samantha L. L. Nature, Vol. 520, Issue 7545 https://doi.org/10.1038/nature14324	journal	April 2015
Estimating historical changes in global land cover: Croplands from 1700 to 1992 Ramankutty, Navin; Foley, Jonathan A. Global Biogeochemical Cycles, Vol. 13, Issue 4 https://doi.org/10.1029/1999GB900046	journal	December 1999
Factors affecting bee communities in forest openings and adjacent mature forest Roberts, H. Patrick; King, David I.; Milam, Joan Forest Ecology and Management, Vol. 394 https://doi.org/10.1016/j.foreco.2017.03.027	journal	June 2017
Beyond plant-soil feedbacks: mechanisms driving plant community shifts due to land-use legacies in post-agricultural forests de la Peña, Eduardo; Baeten, Lander; Steel, Hanne Functional Ecology, Vol. 30, Issue 7 https://doi.org/10.1111/1365-2435.12672	journal	May 2016
Assessing bee (Hymenoptera: Apoidea) diversity of an Illinois restored tallgrass prairie: methodology and conservation considerations Geroff, Ray K.; Gibbs, Jason; McCravy, Kenneth W. Journal of Insect Conservation, Vol. 18, Issue 5 https://doi.org/10.1007/s10841-014-9703-z	journal	September 2014
Dispersal and establishment limitation slows plant community recovery in post-agricultural longleaf pine savannas Turley, Nash E.; Orrock, John L.; Ledvina, Joseph A. Journal of Applied Ecology, Vol. 54, Issue 4 https://doi.org/10.1111/1365-2664.12903	journal	April 2017
Abiotic and biotic factors influencing nest‐site selection by Halictus rubicundus , a ground‐nesting halictine bee Potts, Simon; Willmer, Pat Ecological Entomology, Vol. 22, Issue 3 https://doi.org/10.1046/j.1365-2311.1997.00071.x	journal	August 1997
History and restoration of the longleaf pine-grassland ecosystem: Implications for species at risk Van Lear, David H.; Carroll, W. D.; Kapeluck, P. R. Forest Ecology and Management, Vol. 211, Issue 1-2 https://doi.org/10.1016/j.foreco.2005.02.014	journal	June 2005
Insights from measuring pollen deposition: quantifying the pre-eminence of bees as flower visitors and effective pollinators Willmer, P. G.; Cunnold, H.; Ballantyne, G. Arthropod-Plant Interactions, Vol. 11, Issue 3 https://doi.org/10.1007/s11829-017-9528-2	journal	May 2017

Similar Records

Bees as Biosensors: Chemosensory Ability, Honey Bee Monitoring Systems, and Emergent Sensor Technologies Derived from the Pollinator Syndrome

Journal Article · Fri Oct 30 00:00:00 EDT 2015 · Biosensors · OSTI ID:1471549

Bromenshenk, Jerry; Henderson, Colin; Seccomb, Robert; +3 more

Land-use history, historical connectivity, and land management interact to determine longleaf pine woodland understory richness and composition.

Journal Article · Fri Aug 13 00:00:00 EDT 2010 · Ecography (Online) · OSTI ID:1471549

Brudvig, Lars A.; Damschen, Ellen L.

If you build it, will they come? Insect community responses to habitat establishment at solar energy facilities in Minnesota, USA

Journal Article · Mon Dec 18 00:00:00 EST 2023 · Environmental Research Letters · OSTI ID:1471549

Walston, Leroy J.; Hartmann, Heidi M.; Fox, Laura; +4 more

Related Subjects

60 APPLIED LIFE SCIENCES
54 ENVIRONMENTAL SCIENCES
agricultural history
community ecology
ecological restoration
ecosystem services
land-use legacy
longleaf pine savanna

Title: Restoration increases bee abundance and richness but not pollination in remnant and post-agricultural woodlands

Citation Formats

References (63)

Similar Records

Related Subjects