Diversity matters: how bees benefit from different resin sources

Oecologia

Volumn 176, Issue 4, 2014, Pages 943-953

  Drescher, Nora ^a   Wallace, Helen M ^b   Katouli, Mohammad ^b   Massaro, Carmelina F ^b   Leonhardt, Sara Diana ^a,c  

^a LEUPHANA UNIVERSITY OF LÜNEBURG   (Germany)

^b UNIVERSITY OF THE SUNSHINE COAST   (Australia)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Complementary effect; Functional properties; Plant resin; Resource use; Stingless bees

Indexed keywords

BEE; BIODIVERSITY; COMPLEMENTARITY; CONSUMER-RESOURCE INTERACTION; RESIN; RESOURCE AVAILABILITY; RESOURCE USE; SPECIES DIVERSITY;

APOIDEA; MELIPONINAE;

PLANT RESIN;

ANIMAL; BEE; BIODIVERSITY; BIOMASS; POPULATION DYNAMICS;

ANIMALS; BEES; BIODIVERSITY; BIOMASS; POPULATION DYNAMICS; RESINS, PLANT;

EID: 84908364378     PISSN: 00298549     EISSN: 14321939     Source Type: Journal    
DOI: 10.1007/s00442-014-3070-z     Document Type: Article

References (70)

1. Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybee immunocompetence. Biol Lett 6:562–565
2. Armbruster WS (1984) The role of resin in angiosperm pollination—ecological and chemical considerations. Am J Bot 71:1149–1160
3. Balvanera P, et al. (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156
4. Bankova VS, de Castro SL, Marcucci MC (2000) Propolis: recent advances in chemistry and plant origin. Apidologie 31:3–15
5. Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187
6. Blüthgen N, Klein AM (2011) Functional complementarity and specialisation: why biodiversity is important in plant-pollinator interactions. Basic Appl Ecol 12:282–291
7. Brittain C, Kremen C, Klein AM (2013) Biodiversity buffers pollination in changing environmental conditions. Glob Change Biol 19:540–547
8. Burwell CJ (2007) Ants of Brisbane. Queensland Museum, Brisbane
9. Cardinale BJ, Harvey CT, Gross K, Ives AR (2003) Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecol Lett 6:857–865
10. Chou T-C (2010) Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res 70:440–446
11. Cushnie TPT, Lamb AJ (2011) Recent advances in understanding the antibacterial properties of flavonoids. Int J Antimicrob Agents 38:99–107
12. Damiani N, Fernández NJ, Maldonado LM, Alvarez AR, Eguaras MJ, Marcangeli JA (2010) Bioactivity of propolis from different geographical origins on Varroa destructor (Acari: Varroidae). Parasitol Res 107:31–37
13. De Deyn GB, Raaijmakers CE, van Ruijven J, Berendse F, van der Putten WH (2004) Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos 106:576–586
14. Dollin AE, Dollin LJ, Sakagami SF (1997) Australian stingless bees of the genus Trigona (Hymenoptera: Apidae). Invertebr Taxon 11:861–896
15. Duangphakdee O, Koeniger N, Koeniger G, Wongsiri S, Deowanish S (2005) Reinforcing a barrier—a specific social defense of the dwarf honeybee (Apis florea) released by the weaver ant (Oecophylla smaragdina). Apidologie 36:505–511
16. Duangphakdee O, Koeniger N, Deowanish S, Hepburn HR, Wongsiri S (2009) Ant repellent resins of honeybees and stingless bees. Insect Soc
17. Duffy JE, Carinale BJ, France KE, McIntyre PB, Thebault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10:522–538
18. Eckhardt M, Haider M, Dorn S, Müller A (2014) Pollen mixing in pollen generalist solitary bees: a possible strategy to complement or mitigate unfavourable pollen properties? J Anim Ecol 83:588–597
19. Finke DL, Snyder WE (2008) Niche partitioning increases resource exploitation by diverse communities. Science 321:1488–1490
20. Gamfeldt L, Hillebrand H, Jonsson PR (2005) Species richness changes across two trophic levels simultaneously affect prey and consumer biomass. Ecol Lett 8:696–703
21. Garedew A, Lamprecht I, Schmolz E, Schricker B (2002) The varroacidal action of propolis: a laboratory assay. Apidologie 33:41–50
22. Garedew A, Schmolz E, Lamprecht I (2004) Effect of the bee glue (propolis) on the calorimetrically measured metabolic rate and metamorphosis of the greater wax moth Galleria mellonella. Thermochim Acta 413:63–72
23. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414
24. Ghisalberti EL (1996) Bioactive acylphloroglucinol derivatives from Eucalyptus species. Phytochemistry 41:7–22
25. Greco MK, Hoffmann D, Dollin A, Duncan M, Spooner-Hart R, Neumann P (2010) The alternative pharao approach: stingless bees mummify beetle parasites alive. Naturwissenschaften 97:319–323
26. Hägele BF, Rowell-Rahier M (1999) Dietary mixing in three generalist herbivores: nutrient complementation or toxin dilution? Oecologia 119:521–533
27. Halcroft M, Spooner-Hart R, Neumann P (2011) Behavioral defense strategies of the stingless bee, Austroplebeia australis, against the small hive beetle, Aethina tumida. Insect Soc 58:245–253
28. Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218
29. Höcherl N, Siede R, Illies I, Gätschenberger H, Tautz J (2012) Evaluation of the nutritive value of maize for honey bees. J Insect Physiol 58:278–285
30. Hooper DU (1998) The role of complementarity and competition in ecosystem responses to variation in plant diversity. Ecology 79:704–719
31. Ives RA, Cardinale BJ, Snyder WE (2005) A synthesis of subdisciplines: predator–prey interactions, and biodiversity and ecosystem functioning. Ecol Lett 8:102–116
32. Junker RR, Blüthgen N (2008) Floral scents repel potentially nectar-thieving ants. Evol Ecol Res 10:295–308
33. Junker RR, Blüthgen N (2010) Floral scents repel facultative flower visitors, but attract obligate ones. Ann Bot. doi:10.1093/aob/mcq1045
34. Junker RR, Gershenzon J, Unsicker SB (2011) Floral odour bouquet loses its ant repellent properties after inhibition of terpene biosynthesis. J Chem Ecol 37:1323–1331
35. Kujumgiev A, Tsvetkova I, Serkedjieva Y, Bankova V, Christov R, Popov S (1999) Antibacterial, antifungal and antiviral activity of propolis of different geographic origin. J Ethnopharmacol 64:235–240
36. Langenheim JH (2003) Plant resins: chemistry, evolution, ecology and ethnobotany. Timber Press, Portland
37. Leonhardt SD, Blüthgen N (2009) A sticky affair: resin collection by Bornean stingless bees. Biotropica 41:730–736
38. Leonhardt SD, Blüthgen N, Schmitt T (2009) Smelling like resin: terpenoids account for species-specific cuticular profiles in Southeast-Asian stingless bees. Insect Soc 56:157–170
39. Leonhardt SD, Jung L-M, Schmitt T, Blüthgen N (2010) Terpenoids tame aggressors: role of chemicals in stingless bee communal nesting. Behav Ecol Sociobiol 64:1415–1423
40. Leonhardt SD, Schmitt T, Blüthgen N (2011a) Tree resin composition, collection behavior and selective filters shape chemical profiles of tropical bees (Apidae: Meliponini). PLoS One 6:e23445
41. Leonhardt SD, Wallace HM, Schmitt T (2011b) The cuticular profiles of Australian stingless bees are shaped by resin of the eucalypt tree Corymbia torelliana. Austral Ecol 36:537–543
42. Leonhardt SD, Rasmussen C, Schmitt T (2013) Genes vs. environment: geography and phylogenetic relationships shape the chemical profiles of stingless bees on a global scale. Proc R Soc Lond B 280: 20130680
43. Litman JR, Danforth BN, Eardley CD, Praz CJ (2011) Why do leafcutter bees cut leaves? New insights into the early evolution of bees. Proc R Soc Lond B 278:3593–3600
44. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76
45. Loreau M, et al. (2001) Ecology—biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808
46. Massaro CF, et al. (2014) Anti-staphylococcal activity of C-methyl flavanones from propolis of Australian stingless bees (Tetragonula carbonaria) and fruit resins of Corymbia torelliana (Myrtaceae). Fitoterapia 95:247–257
47. Michener CD (2007) The bees of the world. John Hopkins University Press, Baltimore
48. Mihai CM, Mărghitaş LA, Dezmirean DS, Chirilă F, Moritza RFA, Schlüns H (2012) Interactions among flavonoids of propolis affect antibacterial activity against the honeybee pathogen Paenibacillus larvae. J Invertebr Pathol 110:68–72
49. Nicodemo D, Malheiros EB, De Jong D, Couto RHN (2013) Increased brood viability and longer lifespan of honeybees selected for propolis production. Apidologie 45:269–275
50. Petchey OL (2003) Integrating methods that investigate how complementarity influences ecosystem functioning. Oikos 101:323–330
51. Popova MP, et al. (2007) Chemical characteristics of poplar type propolis of different geographic origin. Apidologie 38:306–311
52. R Development Core Team (2013) R: a language and environment for statistical computing http://www.R-project.org. R Foundation for Statistical Computing, Vienna
53. Rosenfeld JS (2002) Functional redundancy in ecology and conservation. Oikos 98:156–162
54. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New York
55. Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124–143
56. Seeley TD, Seeley RH, Akratanakul P (1982) Colony defense strategies of the honeybees in Thailand. Ecol Monogr 52:43–63
57. Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79:2057–2070
58. Simone M, Evans JD, Spivak M (2009) Resin collection and social immunity in honey bees. Evolution 63:3016–3022
59. Simone-Finstrom M, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41:295–311
60. Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, Princeton
61. Tilman D (1999) The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80:1455–1474
62. Unsicker SB, Oswald A, Köhler G, Weisser WW (2008) Complementarity effects through dietary mixing enhance the performance of a generalist insect herbivore. Oecologia 156:313–324
63. Walker K (2010) “Austroplebeia australis” sugarbag bee (Austroplebeia australis). PaDIL. http://www.padil.gov.au
64. Wallace HM, Lee DJ (2010) Resin-foraging by colonies of Trigona sapiens and T. hockingsi (Hymenoptera: Apidae, Meliponini) and consequent seed dispersal of Corymbia torelliana (Myrtaceae). Apidologie 41:428–435
65. Wallace HM, Trueman SJ (1995) Dispersal of Eucalyptus torelliana seeds by the resin-collecting stingless bee, Trigona carbonaria. Oecologia 104:12–16
66. Wardle DA, Nicholson KS (1996) Synergistic effects of grassland plant species on soil microbial biomass and activity: implications for ecosystem-level effects of enriched plant diversity. Funct Ecol 10:410–416
67. Wenzel F (2011) Smell and repel: resin based defense mechanisms and interactions between Australian ants and stingless bees. Master's degree, Theodor-Boveri-Institut für Biowissenschaften, University of Würzburg, Würzburg
68. Wilson MB, Spivak M, Hegeman AD, Rendahl A, Cohen JD (2013) Metabolomics reveals the origins of antimicrobial plant resins collected by honey bees. PLoS One 8:e77512
69. Wohl DL, Arora S, Gladstone JR (2004) Functional redundancy supports biodiversity and ecosystem function in a closed and constant environment. Ecology 85:1534–1540
70. Yachi S, Loreau M (2007) Does complementary resource use enhance ecosystem functioning? A model of light competition in plant communities. Ecol Lett 10:54–62