Ecological Variation in Response to Mass-Flowering Oilseed Rape and Surrounding Landscape Composition by Members of a Cryptic Bumblebee Complex

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Stanley, Dara A ^a   Knight, Mairi E ^b   Stout, Jane C ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF PLYMOUTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BOMBUS CRYPTARUM; BOMBUS LAPIDARIUS; BOMBUS LUCORUM; BOMBUS SENSU STRICTO; BOMBUS TERRESTRIS; BUMBLEBEE; CONTROLLED STUDY; ECOLOGICAL SPECIALIZATION; FEMALE; FORAGING; GENE LOCUS; GENETIC IDENTIFICATION; GENOTYPE; GEOGRAPHICAL VARIATION (SPECIES); HABITAT USE; LAND USE; LANDSCAPE; NONHUMAN; ORGANISM COLONY; RAPESEED; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SHORT TANDEM REPEAT; SPECIES DIFFERENCE; SPECIES IDENTIFICATION; ANIMAL; BEE; CLASSIFICATION; CROP; DNA SEQUENCE; ECOSYSTEM; FEEDING BEHAVIOR; FLOWER; GENETIC VARIATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; POLLINATION; PROCEDURES;

APOIDEA; BOMBUS CRYPTARUM; BOMBUS LAPIDARIUS; BOMBUS LUCORUM; BOMBUS TERRESTRIS; BRASSICA NAPUS;

MICROSATELLITE DNA;

ANIMALS; BEES; BRASSICA NAPUS; CROPS, AGRICULTURAL; ECOSYSTEM; FEEDING BEHAVIOR; FLOWERS; GENETIC VARIATION; MICROSATELLITE REPEATS; POLLINATION; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 84879209696     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065516     Document Type: Article

References (61)

1. Corbet SA, Williams IH, Osborne JL, (1991) Bees and the pollination of crops and wild flowers in the European community. Bee World 72: 47-59.
2. Williams PH, Brown MJF, Carolan JC, An J, Goulson D, et al. (2012) Unveiling cryptic species of the bumblebee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae). Systematics and Biodiversity: 1-36.
3. Goulson D, Hanley ME, Darvill B, Ellis JS, Knight ME, (2005) Causes of rarity in bumblebees. Biological Conservation 122: 1-8.
4. Bommarco R, Lundin O, Smith HG, Rundlöf M, (2011) Drastic historic shifts in bumble-bee community composition in Sweden. Proceedings of the Royal Society B-Biological Sciences 279: 309-315.
5. Wolf S, Rohde M, Moritz RFA, (2010) The reliability of morphological traits in the differentiation of Bombus terrestris and B. lucorum (Hymenoptera: Apidae). Apidologie 41: 45-53.
6. Carolan JC, Murray TE, Fitzpatrick Ú, Crossley J, Schmidt H, et al. (2012) Colour patterns do not diagnose species: quantitative evaluation of a DNA barcoded cryptic bumblebee complex. PLoS ONE 7: e29251.
7. Bertsch A, Schweer H, Titze A, Tanaka H, (2005) Male labial gland secretions and mitochondrial DNA markers support, species status of Bombus cryptarum and B. magnus (Hymenoptera, Apidae). Insectes Sociaux 52: 45-54.
8. Murray TE, Fitzpatrick U, Brown MJF, Paxton RJ, (2008) Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conservation Genetics 9: 653-666.
9. Waters J, Darvill B, Lye GC, Goulson D, (2011) Niche differentiation of a cryptic bumblebee complex in the Western Isles of Scotland. Insect Conservation and Diversity 4: 46-52.
10. Fitzpatrick U, Murray TE, Byrne A, Paxton RJ, Brown MJF (2006) Regional red list of Irish bees. Ireland: Higher Education Authority.
11. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, et al. (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences of the United States of America 108: 662-667.
12. Fitzpatrick U, Murray TE, Paxton RJ, Breen J, Cotton D, et al. (2007) Rarity and decline in bumblebees- a test of causes and correlates in the Irish fauna. Biological Conservation 136: 185-194.
13. Williams PH, Osborne JL, (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40: 367-387.
14. Whitehorn PR, O'Connor S, Wackers FL, Goulson D, (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336: 351-352.
15. Goulson D, Lye GC, Darvill B, (2008) Decline and conservation of bumble bees. Annual Review of Entomology 53: 191-208.
16. Grixti JC, Wong LT, Cameron SA, Favret C, (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biological Conservation 142: 75-84.
17. Bommarco R, Marini L, Vaissière B, (2012) Insect pollination enhances seed yield, quality, and market value in oilseed rape. Oecologia 169: 1025-1032.
18. Frondel M, Peters J, (2005) Biodiesel: A new Oildorado? Energy Policy 35: 1675-1684.
19. Gathmann A, Tscharntke T, (2002) Foraging ranges of solitary bees. Journal of Animal Ecology 71: 757-764.
20. Charman TG, Sears J, Green RE, Bourke AFG, (2010) Conservation genetics, foraging distance and nest density of the scarce Great Yellow Bumblebee (Bombus distinguendus). Molecular Ecology 19: 2661-2674.
21. Zurbuchen A, Landert L, Klaiber J, Mueller A, Hein S, et al. (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biological Conservation 143: 669-676.
22. Murray TE, Fitzpatrick Ú, Byrne A, Fealy R, Brown MJF, et al. (2012) Local-scale factors structure wild bee communities in protected areas. Journal of Applied Ecology 49: 998-1008.
23. Westphal C, Steffan-Dewenter I, Tscharntke T, (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149: 289-300.
24. Carvell C, Jordan WC, Bourke AFG, Pickles R, Redhead JW, et al. (2012) Molecular and spatial analyses reveal links between colony-specific foraging distance and landscape-level resource availability in two bumblebee species. Oikos 121: 734-742.
25. Goulson D, Lepais O, O'Connor S, Osborne JL, Sanderson RA, et al. (2010) Effects of land use at a landscape scale on bumblebee nest density and survival. Journal of Applied Ecology 47: 1207-1215.
26. Westphal C, Steffan-Dewenter I, Tscharntke T, (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecology Letters 6: 961-965.
27. Morandin LA, Winston ML, Abbott VA, Franklin MT, (2007) Can pastureland increase wild bee abundance in agriculturally intense areas? Basic and Applied Ecology 8: 117-124.
28. Steffan-Dewenter I, Munzenberg U, Burger C, Thies C, Tscharntke T, (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83: 1421-1432.
29. Knight ME, Osborne JL, Sanderson RA, Hale RJ, Martin AP, et al. (2009) Bumblebee nest density and the scale of available forage in arable landscapes. Insect Conservation and Diversity 2: 116-124.
30. Osborne JL, Martin AP, Shortall CR, Todd AD, Goulson D, et al. (2008) Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. Journal of Applied Ecology 45: 784-792.
31. Chapman RE, Wang J, Bourke AFG, (2003) Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators. Molecular Ecology 12: 2801-2808.
32. Darvill B, Knight ME, Goulson D, (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos 107: 471-478.
33. Knight ME, Martin AP, Bishop S, Osborne JL, Hale RJ, et al. (2005) An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species. Molecular Ecology 14: 1811-1820.
34. EPA (2006) Corine Land Cover- Ireland. Land cover update for 2006. Environmental Protection Agency & European Environment Agency.
35. Holehouse KA, Hammond RL, Bourke AFG, (2003) Non-lethal sampling of DNA from bumble bees for conservation genetics. Insectes Sociaux 50: 277-285.
36. Tanaka H, Roubik DW, Kato M, Liew F, Gunsalam G, (2001) Phylogenetic position of Apis nuluensis of northern Borneo and phylogeography of A. cerana as inferred from mitochondrial DNA sequences. Insectes Sociaux 48: 44-51.
37. Estoup A, Scholl A, Pouvreau A, Solignac M, (1995) Monoandry and polyandry in Bumble Bees (Hymenoptera- Bombinae) as evidenced by highly variable microsatellites. Molecular Ecology 4: 89-93.
38. Estoup A, Solignac M, Cornuet JM, Goudet J, Scholl A, (1996) Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Molecular Ecology 5: 19-31.
39. Funk CR, Schmid-Hempel R, Schmid-Hempel P, (2006) Microsatellite loci for Bombus spp. Molecular Ecology Notes 6: 83-86.
40. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535-538.
41. Jones OR, Wang J, (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10: 551-555.
42. Wang JL, (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166: 1963-1979.
43. Lepais O, Darvill B, O'Connor S, Osborne JL, Sanderson RA, et al. (2010) Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Molecular Ecology 19: 819-831.
44. Raymond M, Rousset F, (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248-249.
45. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available: http://www2unilch/popgen/softwares/fstathtm. Updated from Goudet (1995). Accessed 2013 Feb 26.
46. Anderson EC, Dunham KK, (2008) The influence of family groups on inferences made with the program Structure. Molecular Ecology Resources 8: 1219-1229.
47. Miller CR, Joyce P, Waits LP, (2005) A new method for estimating the size of small populations from genetic mark-recapture data. Molecular Ecology 14: 1991-2005.
48. Hothorn T, Bretz F, Westfall P, (2008) Simultaneous inference in general parametric models. Biometrical Journal 50: 346-363.
49. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed Effects Models and Extensions in Ecology with R; Gail M, Krickeberg K, Samet JM, Tsiatis A, Wong W, editors. New York: Springer.
50. R Development Core Team (2008) R: A language and environment for statistical computing.: R Foundation for Statistical Computing, Vienna, Austria. Available: http://www.R-project.org. Accessed 2012 Nov 03.
51. Byrne E (2011) Ecological, molecular and morphological characterization of cryptic bumblebees. Dublin: MSc Thesis, Trinity College Dublin.
52. Hanley ME, Franco M, Dean CE, Franklin EL, Harris HR, et al. (2011) Increased bumblebee abundance along the margins of a mass flowering crop: evidence for pollinator spill-over. Oikos 120: 1618-1624.
53. Westphal C, Steffan-Dewenter I, Tscharntke T, (2009) Mass flowering oilseed rape improves early colony growth but not sexual reproduction of bumblebees. Journal of Applied Ecology 46: 187-193.
54. Herrmann F, Westphal C, Moritz RFA, Steffan-Dewenter I, (2007) Genetic diversity and mass resources promote colony size and forager densities of a social bee (Bombus pascuorum) in agricultural landscapes. Molecular Ecology 16: 1167-1178.
55. Goulson D, Hughes WOH, Derwent LC, Stout JC, (2002) Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130: 267-273.
56. Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME, et al. (2008) Bumblebee flight distances in relation to the forage landscape. Journal of Animal Ecology 77: 406-415.
57. Heard MS, Carvell C, Carreck NL, Rothery P, Osborne JL, et al. (2007) Landscape context not patch size determines bumble-bee density on flower mixtures sown for agri-environment schemes. Biology Letters 3: 638-641.
58. Goulson D, Stout JC, (2001) Homing ability of the bumblebee Bombus terrestris (Hymenoptera: Apidae). Apidologie 32: 105-111.
59. Diekotter T, Kadoya T, Peter F, Wolters V, Jauker F, (2010) Oilseed rape crops distort plant-pollinator interactions. Journal of Applied Ecology 47: 209-214.
60. Palmer TM, Stanton ML, Young TP, (2003) Competition and coexistence: Exploring mechanisms that restrict and maintain diversity within mutualist guilds. American Naturalist 162: S63-S79.
61. Goulson D, Darvill B, (2004) Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 35: 55-63.