Abstract
To date, no study has investigated how landscape structural (visual) alterations affect navigation and thus homing success in stingless bees. We addressed this question in the Australian stingless bee Tetragonula carbonaria by performing marking, release and re-capture experiments in landscapes differing in habitat homogeneity (i.e., the proportion of elongated ground features typically considered prominent visual landmarks). We investigated how landscape affected the proportion of bees and nectar foragers returning to their hives as well as the earliest time bees and foragers returned. Undisturbed landscapes with few landmarks (that are conspicuous to the human eye) and large proportions of vegetation cover (natural forests) were classified visually/structurally homogeneous, and disturbed landscapes with many landmarks and fragmented or no extensive vegetation cover (gardens and plantations) visually/structurally heterogeneous. We found that proportions of successfully returning nectar foragers and earliest times first bees and foragers returned did not differ between landscapes. However, most bees returned in the visually/structurally most (forest) and least (garden) homogeneous landscape, suggesting that they use other than elongated ground features for navigation and that return speed is primarily driven by resource availability in a landscape.
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References
Avarguès-Weber A, Mota T, Giurfa M (2012) New vistas on honey bee vision. Apidologie 43(3):244–268
Avarguès-Weber A, Dyer AG, Ferrah N, Giurfa M (2015) The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees. Proc R Soc B 282:20142384
Barton K (2013) MuMIn: Multi-model inference. R package version 190 ed
Buehlmann C, Graham P, Hansson BS, Knaden M (2015) Desert ants use olfactory scenes for navigation. Anim Behav 106:99–105. doi:10.1016/j.anbehav.2015.04.029
Collett TS, Graham P (2015) Insect navigation: do honeybees learn to follow highways? Curr Biol 25(6):240–242
Degen J, Kirbach A, Reiter L, Lehmann K, Norton P, Storms M, Koblofsky M, Winter S, Georgieva PB, Nguyen H, Chamkhi H, Greggers U, Menzel R (2015) Honeybees apply effective exploration strategies during orientation flights. Anim Behav 102:45–57
Dollin AE, Dollin LJ, Sakagami SF (1997) Australian stingless bees of the genus Trigona (Hymenoptera: apidae). Invertebr Taxon 11(6):861–896
Dollin A, Walker K, Heard T (2009) Trigona carbonaria sugarbag bee (Tetragonula carbonaria). PaDIL - http://www.padilgovau:2012. Accessed Apr 2010
Dyer FC, Could JL (1983) Honey bee navigation: the honey bee’s ability to find its way depends on a hierarchy of sophisticated orientation mechanisms. Am Sci 71(6):587–597
Dyer AG, Rosa MGP, Reser DH (2008) Honeybees can recognise images of complex natural scenes for use as potential landmarks. J Exp Biol 211:1180–1186
Farina WM, Grüter C, Diaz PC (2005) Social learning of floral odours inside the honeybee hive. Proc R Soc B 272(1575):1923–1928
Fry SN, Wehner R (2005) Look and turn: landmark-based goal navigation in honey bees. J Exp Biol 208:3945–3955. doi:10.1242/jeb.01833
Giurfa M, Hammer M, Stach S, Stollhoff N, Müller-Deisig N, Mizyrycki C (1999) Pattern learning by honeybees: conditioning procedure and recognition strategy. Proc R Soc B 57:315–324
Goulson D, Nicholls E, Botias C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957. doi:10.1126/science.1255957
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596
Heard TA (2016) The Australian native bee book. Keeping stingless bee hives for pets, pollination and sugarbag honey. Sugarbag Bees, Brisbane
Jacobs LF (2012) From chemotaxis to the cognitive map: the function of olfaction. Proc Natl Acad Sci USA 109:10693–10700
Kaluza BF, Wallace HM, Heard TA, Klein A-M, Leonhardt SD (2016) Urban gardens promote bee foraging over natural habitats and plantations. Ecol Evol. doi:10.1002/ece1003.1941
Leonhardt SD, Dworschak K, Eltz T, Blüthgen N (2007) Foraging loads of stingless bees and utilisation of stored nectar for pollen harvesting. Apidologie 38:125–135
Leonhardt SD, Zeilhofer S, Schmitt T (2010) Stingless bees use terpenes as olfactory cues to find resin sources. Chem Senses 35:603–611
Leonhardt SD, Baumann A-M, Wallace HM, Brooks P, Schmitt T (2014a) The chemistry of an unusual seed disperal mutualism: bees use a complex set of chemical cues to find their partner. Anim Behav 98:41–51
Leonhardt SD, Heard TA, Wallace HM (2014b) Differences in the resource intake of two sympatric Australian stingless bee species. Apidologie 45(4):514–525. doi:10.1007/s13592-013-0266-x
Menzel R, Greggers U (2013) Guidance by odors in honeybee navigation. J Comp Phys A 199(10):867–873
Menzel R, Greggers U (2015) The memory structure of navigation in honeybees. J Comp Phys A 201(6):547–561
Menzel R, Geiger K, Chittka L, Joerges J, Kunze J, Müller U (1996) The knowledge base of bee navigation. J Exp Biol 199:141–146
Najera DA, McCullough EL, Jander R (2015) Honeybees use celestial and/or terrestrial compass cues for inter-patch navigation. Ethology 121:94–102. doi:10.1111/eth.12319
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Method Ecol Evol 4(2):133–142
Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME, Goulson D, Hale RJ, Sanderson RA (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77(2):406–415
Osborne JL, Smith A, Clark SJ, Reynolds DR, Barron MC, Lim KS, Reynolds AM (2013) The ontogeny of bumblebee flight trajectories: from naïve explorers to experienced foragers. PLoS One 8:e78681
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trend Ecol Evol 25:345–353
R Development Core Team (2015) R: A language and environment for statistical computing, URL http://www.R-project.org. R Foundation for statistical computing, Vienna
Rasmussen C, Cameron SA (2007) A molecular phylogeny of the old world stingless bees (Hymenoptera: apidae: Meliponini) and the non-monophyly of the large genus Trigona. Syst Entomol 32:26–39
Reynolds AM, Swain J-L, Smith AD, Martin AP, Osborne JL (2009) Honeybees use a levy flight search strategy and odour-mediated anemotaxis to relocate food sources. Behav Ecol Sociobiol 64:115–123
Roulston TH, Goodell K (2011) The role of resources and risks in regulating wild bee populations. Annu Rev Entomol 56:293–312
Sánchez D, Vandame R (2012) Color and shape discrimination in the stingless bee Scaptotrigona mexicana Guérin (Hymenoptera, Apidae). Neotrop Entomol 41(3):171–177. doi:10.1007/s13744-012-0030-3
Smith JP, Heard TA, Gloag AR, Beekman M (2016) Flight range of the Australian stingless bee, Tetragonula carbonaria (Hymenoptera, Apidae). Austral Entomol (in press)
Spaethe J, Streinzer M, Eckert J, May S, Dyer AG (2014) Behavioural evidence of colour vision in free flying stingless bees. J Comp Phys A 200(6):485–496
Srinivasan MV (2014) Going with the flow: a brief history of the study of the honeybee’s navigational odometer. J Comp Phys A 200(6):563–573
Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured landscapes. Proc R Soc B 270(1515):569–575. doi:10.1098/rspb.2002.2292
Towne WF, Moscrip H (2008) The connection between landscapes and the solar ephemeris in honeybees. J Exp Biol 211:3729–3736
Vanbergen AJ, the Insect Pollinators Initiative (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Envir 11(5):251–259
von Frisch K (1967) The dance language and orientation of bees. Belknap Press of Harvard University Press, Cambridge
Wallace HM, Leonhardt SD (2015) Do hybrid trees inherit invasive characteristics? fruits of Corymbia torelliana XC. citridora hybrids and potential for seed dispersal bees. PLoS One 10(9):e0138868
Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric and geocentric information. J Exp Biol 199:129–140
Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecol Entomol 31:389–394
Williams NM, Kremen C (2007) Resource distributions among habitats determine solitary bee offspring production in a mosaic landscape. Ecol Appl 17:910–921
Winfree R, Aguilar R, Vazquez DP, LeBuhn G, Aizen MA (2009) A meta-analysis of bees responses to anthropogenic disturbance. Ecology 90(8):2068–2076
Wystrach A, Graham P (2012) What can we learn from studies of insect navigation? Anim Behav 84:13–20. doi:10.1016/j.anbehav.2012.04.01
Acknowledgments
The authors thank Julia Nagler, Manuel Pützstück, Birte Hensen, Nora Drescher and Bradley Jeffers for assistance with field work. We further thank Sahara Farms, Macadamia Farm Management Pty Ltd and Maroochy Bushland Botanic Gardens, as well as numerous private land and garden owners to keep our bee hives and let us walk around their properties. We are further grateful for the comments of two anonymous reviewers, which helped to improve our manuscript. BFK received funding from the German Academic Exchange Agency (DAAD). The project was funded by the German Research Foundation (DFG), LE 2750/1-1.
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Leonhardt, S.D., Kaluza, B.F., Wallace, H. et al. Resources or landmarks: which factors drive homing success in Tetragonula carbonaria foraging in natural and disturbed landscapes?. J Comp Physiol A 202, 701–708 (2016). https://doi.org/10.1007/s00359-016-1100-5
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DOI: https://doi.org/10.1007/s00359-016-1100-5