Abstract
Context
Persistence of organisms in fragmented landscapes often depends on the ability of individuals to move between habitat patches. This movement can be limited by variables of the species, patch, and/or matrix, but we often lack a comprehensive understanding of the relative importance of each of the variables and their interactions. As central place foragers, bees need to move to access resources, but we have a poor understanding of what impacts their movement in fragmented landscapes. This lack of information affects conservation efforts.
Objectives
The primary objective was to understand the effects of species, patch, and matrix variables on bee movement between habitat patches.
Methods
Using the naturally fragmented Ozark Mountain glade ecosystem (Missouri, USA), we marked over 4500 bees in 2017 and 2018. Recapture took place 24 h later. Species, patch, and matrix variables were measured or classified including nesting location, bee size class, distance between patches, nesting resources, canopy cover, and floral resources. Principal components were used for patch and some matrix resource variables in models.
Results
Only 8% of recaptured marked bees moved between habitat patches. Increased movement was observed for larger bees and shorter distances between patches. Bees moved up resource gradients to more rewarding patches unless the matrix provided supplementary resources.
Conclusions
Though bees are often considered highly mobile and able to use nearby habitat patches, the rarity of movement in this natural system highlights the importance of patch and nearby matrix resources for supporting bee communities. While many recent studies have emphasized the species, patch, and matrix variables that may influence bee movement, the overall lack of movement even across high variability in these traits suggests conservation should not expect connectivity to help maintain community diversity.
Similar content being viewed by others
References
Baird E, Dacke M (2016) Finding the gap: a brightness-based strategy for guidance in cluttered environments. Proc Biol Sci 283(1828):1794–1799
Bates D, Bolker BM, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48
Bennett JA, Gensler GC, Cahill JF (2014) Small-scale bee patch use is affected equally by flower availability and local habitat configuration. Basic Appl Ecol 15(3):260–268
Bergerot B, Julliard R, Baguette M (2010) Metacommunity dynamics: decline of functional relationship along a habitat fragmentation gradient. PLoS ONE 5(6):e11294
Bivand R, Lewin-Koh N (2022) maptools: tools for handling spatial objects. https://cran.r-project.org/package=maptools
Bivand R, Rundel C (2022) rgeos: interface to geometry engine—open source ('GEOS’). https://cran.r-project.org/package=rgeos
Bivand RS, Pebesma E, Gomez-Rubio V (2013) Applied spatial data analysis with R, 2nd edn. Springer, New York
Bommarco R, Biesmeijer JC, Meyer B, Potts SG, Pöyry J, Roberts SPM, Steffan-Dewenter I, Ockinger E (2010) Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc R Soc Sci 277(1690):2075–2082
Cane JH (2001) Habitat fragmentation and native bees a premature verdict? Conserv Ecol. https://doi.org/10.5751/ES-00265-050103
Cariveau DP, Winfree R (2015) Causes of variation in wild bee responses to anthropogenic drivers. Curr Opin Insect Sci 10:104–109
Chetkiewicz C-LB, St. Clair CC, Boyce MS (2006) Corridors for conservation: Integrating pattern and process. Annu Rev Ecol Evol Syst 37(1):317–342
Coulston JW, Moisen GG, Wilson BT, Finco MV, Cohen WB, Brewer CK (2012) Modeling percent tree canopy cover: a pilot study. Photogramm Eng Remote Sens 78(7):715–727
Cranmer L, McCollin D, Ollerton J (2012) Landscape structure influences pollinator movements and directly affects plant reproductive success. Oikos 121(4):562–568
Davison PJ, Field J (2018) Environmental barriers to sociality in an obligate eusocial sweat bee. Insectes Soc 65(4):549–559
Donald PF, Evans AD (2006) Habitat connectivity and matrix restoration: the wider implications of agri-environment schemes. J Appl Ecol 43(2):209–218
Dorchin A, Filin I, Izhaki I, Dafni A (2012) Movement patterns of solitary bees in a threatened fragmented habitat. Apidologie 44(1):90–99
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, Mcclean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography (cop) 36(1):27–46
Driscoll DA, Banks SC, Barton PS, Lindenmayer DB, Smith AL (2013) Conceptual domain of the matrix in fragmented landscapes. Trends Ecol Evol 28(10):605–613
Eickwort GC (1986) First steps into eusociality : the sweat bee Dialictus lineatulus. Florida Entomol 69(4):742–754
Evans BS, Kilpatrick AM, Hurlbert AH, Marra PP (2017) Dispersal in the urban matrix : assessing the influence of landscape permeability on the settlement patterns of breeding songbirds. Front Ecol Evol. https://doi.org/10.3389/fevo.2017.00063
Everaars J, Settele J, Dormann CF (2018) Fragmentation of nest and foraging habitat affects time budgets of solitary bees, their fitness and pollination services, depending on traits: Results from an individual-based model. PLoS ONE 13(2):1–28
Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142
Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40(9):1649–1663
Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst 48:1–23
Feigs JT, Holzhauer SIJ, Huang S, Brunet J, Diekmann M, Hedwall PO, Kramp K, Naaf T (2022) Pollinator movement activity influences genetic diversity and differentiation of spatially isolated populations of clonal forest herbs. Front Ecol Evol 10:1–19
Fox J, Weisberg S (2018) An R companion to applied regression, third. Sage, Thousand Oaks
Franzén M, Larsson M, Nilsson SG (2009) Small local population sizes and high habitat patch fidelity in a specialised solitary bee. J Insect Conserv 13(1):89–95
Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71(5):757–764
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153(3):589–596
Grundel R, Jean RP, Frohnapple KJ, Glowacki GA, Scott PE, Pavlovic NB, Scott E, Pavlovic NB (2010) Floral and nesting resources, habitat structure, and fire influence bee distribution across an open-forest gradient. Ecol Appl 20(6):1678–1692
Gruter C, Hayes L (2022) Sociality is a key driver of foraging ranges in bees. Curr Biol 32:5390–5397
Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM, Damschen EI, Ewers RM, Foster BL, Jenkins CN, King AJ, Laurance WF, Levey DJ, Margules CR, Melbourne BA, Nicholls AO, Orrock JL, Song D, Townshend JR (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052
Hadley AS, Betts MG (2012) The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol Rev Camb Philos Soc 87(3):526–544
Hanski I, Poyry J (2007) Insect populations in fragmented habitats. In: Stewart AJA, New T, Lewis OT (eds) Insect conservation biology, 1st edn. CABI, Oxfordshire, pp 175–202
Hatfield RG, LeBuhn G (2007) Patch and landscape factors shape community assemblage of bumble bees, Bombus spp. (Hymenoptera: Apidae), in montane meadows. Biol Conserv 139:150–158
Helbach J, Frey J, Messier C, Mörsdorf M, Scherer-Lorenzen M (2022) Light heterogeneity affects understory plant species richness in temperate forests supporting the heterogeneity–diversity hypothesis. Ecol Evol 12(2):1–14
Hillaert J, Hovestadt T (2018) Size-dependent movement explains why bigger is better in fragmented landscapes. Ecol Evol 8:10754–10767
Howell AD, Alarcón R, Minckley RL (2017) Effects of habitat fragmentation on the nesting dynamics of desert bees. Ann Entomol Soc Am 110(2):233–243
Huais PY, Grilli G, Galetto L (2022) Forest connectivity boosts pollen flow among populations of the oil-producing Nierembergia linariifolia. Landsc Ecol 37(9):2435–2450
Jules ES, Shahani P, Erik S (2003) A broader ecological context to habitat fragmentation: why matrix habitat is more important than we thought. J Veg Sci 14(3):459–464
Kendall LK, Mola JM, Portman ZM, Cariveau DP, Smith HG, Bartomeus I (2022) The potential and realized foraging movements of bees are differentially determined by body size and sociality. Ecology 103(11):1–8
Lane IG, Herron-Sweet CR, Portman ZM, Cariveau DP (2020) Floral resource diversity drives bee community diversity in prairie restorations along an agricultural landscape gradient. J Appl Ecol 57(10):2010–2018
Lüdecke D (2018) ggeffects: tidy data frames of marginal effects from regression models. J Open Source Softw 3(26):772
Maitra S, Yan J (2008) Principle component analysis and partial least squares: two dimension reduction techniques for regression. Applying multivariate statistical models. Casualty Actuarial Society, Quebec City, pp 1–194
Marini L, Bruun HH, Heikkinen RK, Helm A, Honnay O, Krauss J, Kühn I, Lindborg R, Pärtel M, Bommarco R (2012) Traits related to species persistence and dispersal explain changes in plant communities subjected to habitat loss. Divers Distrib 18(9):898–908
M’Gonigle LK, Ponisio LC, Cutler K, Kremen C (2015) Habitat restoration promotes pollinator persistence and colonization in intensively managed agriculture. Ecol Appl 25(6):103–112
Missouri Department of Natural Resources (2014) Missouri Glades. https://data-msdis.opendata.arcgis.com/datasets/MSDIS::mo-2018-natural-glades/about
Mola JM, Miller MR, O’Rourke S, Williams N, Entomology E (2020) Forests do not limit bumble bee foraging movements in a montane meadow complex. Ecol Entomol 45(5):955–965
Monteiro LR (2013) Morphometrics and the comparative method: studying the evolution of biological shape. Hystrix 24(1):25–32
Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci USA 105(49):19052–19059
Nelson CJ, Frost CM, Nielsen SE (2021) Narrow anthropogenic linear corridors increase the abundance, diversity, and movement of bees in boreal forests. For Ecol Manag 489:119044
Nijs V, von Hertzen N (2023) radiant.data: data menu for radiant: business analytics using R and shiny
Osborne JL, Williams IH (2001) Site constancy of bumble bees in an experimentally patchy habitat. Agric Ecosyst Environ 83:129–141
Pebesma EJ, Bivand RS (2005) Classes and methods for spatial data in R. R News 5(2):9–13
Pedersen TL (2022) patchwork: the composer of plots. https://cran.r-project.org/package=patchwork
Pinto CE, Awade M, Watanabe MTC, Brito RM, Costa WF, Maia UM, Imperatriz-Fonseca VL, Giannini TC (2020) Size and isolation of naturally isolated habitats do not affect plant-bee interactions: a case study of ferruginous outcrops within the eastern Amazon forest. PLoS ONE 15:1–17
Prevedello JA, Vieira MV (2010) Does the type of matrix matter? A quantitative review of the evidence. Biodivers Conserv 19(5):1205–1223
QGIS: QGIS Development Team (2021) QGIS: QGIS Development Team (2021). QGIS Geographic Information System. https://qgis.osgeo.org
R Core Team (2022) R. R Foundation for Statistical Computing, Vienna, Austria
Richards MH (2011) Colony social organisation and alternative social strategies in the Eastern Carpenter Bee Xylocopa Virginica. J Insect Behav 24(5):399–411
Sakagami SF, Munakata M (1972) Distribution and bionomics of a transpalaearctic eusocial Halictine bee, Lasioglossum (Evylaeus) calceatum, in Northern Japan, with reference to its solitary lifestyle at high altitude. 北海道大學理學部紀要 18(3):411–439
Selfridge J, Frye C, Gibbs J, Jean RP (2017) The bee fauna of inland sand dune and ridge woodland communities in Worcester County, Maryland. Northeast Nat 24(4):421–445
Storck-Tonon D, Peres CA (2017) Forest patch isolation drives local extinctions of Amazonian orchid bees in a 26 years old archipelago. Biol Conserv 214:270–277
Tilman D, Clark M, Williams DR, Kimmel K, Polasky S, Packer C (2017) Future threats to biodiversity and pathways to their prevention. Nature 546:73–81
van Etten J (2017) R package gdistance: distances and routes on geographical grids. J Stat Softw 76(13):21
Volenec ZM, Smith CM (2021) Not all matrix habitat is created equal for rare bee species in forest habitat. Ecol Entomol 46(4):926–935
Westerfelt P, Weslien J, Widenfalk O (2018) Forest ecology and management population patterns in relation to food and nesting resource for two cavity- nesting bee species in young boreal forest stands. For Ecol Manag 430:629–638
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Williams NM, Kremen C (2007) Resource distributions among habitats determine solitary bee offspring production in a mosaic landscape. Ecol Appl 17(3):910–921
Wyman LM, Richards MH (2003) Colony social organization of Lasioglossum malachurum Kirby (Hymenoptera, Halictidae) in southern Greece. Insectes Soc 50:1–12
Zurbuchen A, Cheesman S, Klaiber J, Müller A, Hein S, Dorn S (2010) Long foraging distances impose high costs on offspring production in solitary bees. J Anim Ecol 79(3):674–681
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer-Verlag, New York
Acknowledgements
The authors would like to thank Katherine Barie, Jonathan Tetlie, Paul Ruiz-Lopez, Mary Powley, Kelcie Brown, and Matthew Tryc for their assistance with data collection. Missouri Department of Conservation and Missouri Department of Natural Resources kindly provided access to properties for this project. We are also greatly appreciative of comments from the HT lab and 2 anonymous reviewers that greatly improved the manuscript.
Funding
Funding was provided by National Science Foundation- Division of Environmental Biology #1649652.
Author information
Authors and Affiliations
Contributions
AH-T designed the study and sampling. Both authors completed the sampling and handling of materials. NLA completed the data analysis and prepared the figures. Both authors worked on the drafts and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no competing financial or other interests relevant to this publication.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Harmon-Threatt, A.N., Anderson, N.L. Bee movement between natural fragments is rare despite differences in species, patch, and matrix variables. Landsc Ecol 38, 2519–2531 (2023). https://doi.org/10.1007/s10980-023-01719-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10980-023-01719-6