, Volume 187, Issue 3, pp 701–706 | Cite as

Changes in the bee fauna of a German botanical garden between 1997 and 2017, attributable to climate warming, not other parameters

  • Michaela M. Hofmann
  • Andreas Fleischmann
  • Susanne S. Renner
Community ecology – original research


Botanical gardens represent artificial, but stable environments. With this premise, we analyzed the Munich Botanical Garden’s bee fauna in 1997/1999 and again in 2015/2017. The garden covers 20 ha, uses no bee-relevant insecticides, has a protected layout, and on three sides abuts protected areas. Outdoors, it cultivates some 10,871 species/subspecies, many suitable as pollen and nectar sources for bees. The first survey found 79 species, the second 106, or 55% of the 192 species recorded for Munich since 1990. A Jackknife estimate for the second survey suggests 115 expected species. Classifying bees according to their thermal preferences (warm habitats, cool habitats, broad preferences, or unknown) revealed that 15 warm-loving species were gained (newly found), two lost (no longer found), and 12 retained, but only one cool-loving species was gained, three lost, and none retained, which multinomial models show to be significant differences. Of the 62 retained species, 27 changed in abundance, with 18 less frequent and nine more frequent by 2017 than they had been in 1997/1999. Retention, gain, or loss were unconnected to pollen specialization and Red List status of bee species. Between 1997 and 2017, average temperatures in Munich have increased by 0.5 °C, and climate warming over the past century is the most plausible explanation for the directional increase in warm-loving and the decrease in cool-adapted species. These results highlight the potential of botanic gardens with their artificially diverse and near-pesticide-free floras as systems in which to investigate climate change per se as a possible factor in shifting insect diversity.


Botanic gardens Bee fauna Climate warming Repeated monitoring Stable habitat Insect faunal change 



We thank B. Bembé, Munich, for information on his monitoring in the 1990s; J. Schuberth, S. Schmidt, and C. Zohner, Munich, and P. Westrich, Kusterdingen, for advice; H. Schäfer, Technical University of Munich, for unpublished primer sequences and advice; M. Silber and J. Babczinsky for help in the lab and with bee preparation; L. Alzinger, R. Thiessen-Bock, and C. Glassl for help with monitoring in 2016; M. Bräu and K. Mandery for information on bee ranges; H. Küchenhoff, and M. Bort from the LMU StaBLab for statistical advice; and the Editor-in-Chief, R. Brandl, and an anonymous reviewer for suggestions that helped improve the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

442_2018_4110_MOESM1_ESM.docx (56 kb)
Supplementary material 1 (DOCX 55 kb)


  1. Amiet F, Krebs A (eds) (2014) Bienen Mitteleuropas: Gattungen, Lebensweise, Beobachtung. 2., korrigierte Auflage. Haupt Verlag, BernGoogle Scholar
  2. Amiet F, Müller A, Neumeyer R (1999) Fauna Helvetica 9. Apidae 2: Colletes, Dufourea, Hylaeus, Nomia, Nomioides, Rhophitoides, Rophites, Sphecodes, Systropha. Centre Suisse de Cartographie de la Faune, NeuchatelGoogle Scholar
  3. Amiet F, Herrmann M, Müller A, Neumeyer R (2001) Fauna Helvetica 9. Apidae 3: Lasioglossum, Halictus. Centre Suisse de Cartographie de la Faune, Neuchatel, SwitzerlandGoogle Scholar
  4. Amiet F, Herrmann M, Müller A, Neumeyer R (2004) Fauna Helvetica 9. Apidae 4: Anthidium, Chelostoma, Coelioxys, Dioxys, Heriades, Lithurgus, Megachile, Osmia, Stelis. Centre Suisse de Cartographie de la Faune, Neuchatel, SwitzerlandGoogle Scholar
  5. Amiet F, Herrmann M, Müller A, Neumeyer R (2007) Fauna Helvetica 9. Apidae 5: Ammobates, Ammobatoides, Anthophora, Biastes, Ceratina, Dasypoda, Epeoloides, Epeolus, Eucera, Macropis, Melecta, Melitta, Nomada, Pasites, Tetralonia, Thyreus, Xylocopa. Centre Suisse de Cartographie de la Faune, Neuchatel, SwitzerlandGoogle Scholar
  6. Baal T, Denker B, Mühlen W, Surholt B (1994) Die Ursachen des Massensterbens von Hummeln unter spätblühenden Linden. Nat Landsch 69:412–418Google Scholar
  7. Bembé B, Gerlach G, Schuberth J, Schönitzer K (2001) Die Wildbienen im Botanischen Garten München. Nachrichtenblatt der bayererischen Entomologen 50:30–41Google Scholar
  8. Bräu M, Nützel R (2010) Bienen und Wespen in München. Bund Naturschutz in Bayern e.V, MunichGoogle Scholar
  9. Bußler H (2007) Mediterrane Holzbienen entdecken Bayern. LWF Aktuell 58:50–51Google Scholar
  10. Dathe HH (1980) Die Arten der Gattung Hylaeus F. in Europa (Hymenoptera: Apoidea, Colletidae). Mitteilungen aus dem Zoologischen Museum in Berlin 56:207–294Google Scholar
  11. Dorn M, Weber D (1988) Die Luzerne-Blattschneiderbiene und ihre Verwandten in Mitteleuropa. A. Ziemsen Verlag, WittenbergGoogle Scholar
  12. Falk SJ, Lewington R (2015) Field guide to the bees of Great Britain and Ireland. Bloomsbury, LondonGoogle Scholar
  13. Frommer U, Flügel H-J (2005) Zur ausbreitung der furchenbiene Halictus scabiosae (Rossi, 1790) in mitteleuropa unter besonderer berücksichtigung der situation in hessen (Hymenoptera: Apidae). Mitteilungen des Internationalen Entomologischen Vereins 30:51–79Google Scholar
  14. Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208CrossRefPubMedGoogle Scholar
  15. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957CrossRefPubMedGoogle Scholar
  16. Haeseler V, Ritzau C (1998) Zur Aussagekraft wirbelloser Tiere in Umwelt-und Naturschutzgutachten. Zeitschrift für Ökologie und Naturschutz 7:45–66Google Scholar
  17. Hage HJ (2005) Die Holzbiene Xylocopa violacea (LlNNAEUS 1758) in Bayern (Hymenoptera, Apidae). Nachrichtenblatt der Bayerischen Entomologen 54:39–46Google Scholar
  18. Hall DM, Camilo GR, Tonietto RK, Ollerton J, Ahrné K, Arduser M, Ascher JS, Baldock KCR, Fowler R, Frankie G, Goulson D, Gunnarsson B, Hanley ME, Jackson JI, Langellotto G, Lowenstein D, Minor ES, Philpott SM, Potts SG, Sirohi MH, Spevak EM, Stone GN, Threlfall CG (2016) The city as a refuge for insect pollinators. Conserv Biol 31:24–29CrossRefGoogle Scholar
  19. Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, Goulson D (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One 12(10):e0185809CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hernandez JL, Frankie GW, Thorp RW (2009) Ecology of urban bees: a review of current knowledge and directions for future study. Cities Environ 2:1–15CrossRefGoogle Scholar
  21. Hopfenmüller S (2014) Folgt die Efeu-Seidenbiene Colletes hederae Schmidt & Westrich, 1993 dem Ausbreitungsweg der Furchenbiene Halictus scabiosae (Rossi, 1790) in Bayern? (Hymenoptera: Apoidea). Nachrichtenblatt der Bayerischen Entomologen 63:2–7Google Scholar
  22. Knoerzer A (1941) Bemerkenswerte Hymenopterenfunde in Südbayern. Mitteilungen der Münchner Entomologischen Gesellschaft 31:934–937Google Scholar
  23. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353CrossRefPubMedGoogle Scholar
  24. Primack RB, Miller-Rushing AJ (2009) The role of botanical gardens in climate change research. New Phytol 182:303–313CrossRefPubMedGoogle Scholar
  25. Renner SS (2014) 100 Jahre Botanischer Garten München-Nymphenburg. Berichte der Bayerischen Botanischen Gesellschaft 84:35–38Google Scholar
  26. Scheuchl E, Schwenninger HR (2015) Kritisches Verzeichnis und aktuelle Checkliste der Wildbienen Deutschlands (Hymenoptera Anthophila) sowie Anmerkungen zur Gefährdung. Mitteilungen des Entomologischen Vereins Stuttgart 50:3–225Google Scholar
  27. Scheuchl E, Willner W (2016) Taschenlexikon der Wildbienen Mitteleuropas: alle Arten im Porträt. Quelle & Meyer, WiebelsheimGoogle Scholar
  28. Schmalz K-H (2005) Erste Sichtnachweise der blauschwarzen Holzbiene Xylocopa violacea (Hymenoptera Apidae) in Osthessen. Beiträge zur Naturkunde in Osthessen 41:45–46Google Scholar
  29. Schmidt S, Schmid-Egger C, Morinière J, Haszprunar G, Hebert PDN (2015) DNA barcoding largely supports 250 years of classical taxonomy: identifications for Central European bees (Hymenoptera, Apoidea partim). Mol Ecol Resour 15:985–1000CrossRefPubMedGoogle Scholar
  30. von Hagen E, Aichhorn A (2014) Hummeln: Bestimmen, Ansiedeln, Vermehren, Schützen, 6th edn. Fauna Verlag, GermanyGoogle Scholar
  31. Westrich P (1989) Die Wildbienen Baden-Württembergs. E. Ulmer, StuttgartGoogle Scholar
  32. Westrich P, Frommer U, Mandery K, Riemann H, Ruhnke H, Saure C, Voith J (2011) Rote Liste und Gesamtartenliste der Bienen (Hymenoptera, Apidae) Deutschlands. Naturschutz und Biologische Vielfalt 70:373–416Google Scholar
  33. Williams PH, Araújo MB, Rasmont P (2007) Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth? Biol Cons 138:493–505CrossRefGoogle Scholar
  34. Yee TW (2010) The VGAM package for categorical data analysis. J Stat Softw 32:1–34CrossRefGoogle Scholar
  35. Zohner CM, Renner SS (2014) Common garden comparison of the leaf-out phenology of woody species from different native climates, combined with herbarium records, forecasts long-term change. Ecol Lett 17:1016–1025CrossRefPubMedGoogle Scholar
  36. Zurbuchen A, Müller A (2012) Wildbienenschutz: von der Wissenschaft zur Praxis. Haupt Verlag, BernGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Systematic Botany and MycologyUniversity of Munich (LMU)MunichGermany
  2. 2.Botanische Staatssammlung MünchenMunichGermany

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