Arthropod-Plant Interactions

, Volume 13, Issue 5, pp 745–755 | Cite as

The March fly and the ant: the unusual pollination system of Eustegia minuta (Apocynaceae: Asclepiadoideae)

  • Yolanda Chirango
  • Sandy-Lynn Steenhuisen
  • Peter V. Bruyns
  • Jeremy J. Midgley
  • Adam ShuttleworthEmail author
Original Paper


Pollination studies of South African Asclepiadeae (Apocynaceae: Asclepiadoideae) have mostly examined species in the moist summer-rainfall grasslands, with limited studies of the early-diverging groups occurring in the drier winter-rainfall habitats. This study examined the pollination and floral traits of Eustegia minuta, an unusual species endemic to the winter-rainfall Greater Cape Floristic Region and representing an early-diverging clade within the Asclepiadeae. Observations of floral visitors in Jonkershoek Nature Reserve showed that this species is visited primarily by a species of March fly, Bibio turneri (Bibionidae). These flies moved actively between plants and carried pollinaria on their mouthparts. In addition, an ant species, Camponotus vestitus (Formicidae), and a single honey bee Apis mellifera capensis (Apidae) individual carried pollinaria and may contribute to pollination. Bagging experiments confirmed that flowers require pollinators for reproduction. Flowers produced small amounts (1.2 µl per flower) of concentrated (32.5% sugar) nectar. Pollination success was low (14.5% of flowers were pollinated and 3.4% of flowers developed fruits). Pollen transfer efficiency (PTE) was 5.2%. The corolla reflectance was similar to that of green leaves, but the gynostegium exhibited a relatively bright human-white spectral curve. Floral scent comprised over 50 compounds, but was dominated by various aromatics along with 2,3-heptandione, (E)-4,8-dimethylnona-1,3,7-triene and several unidentified compounds. We conclude that E. minuta is pollinated primarily by the March fly B. turneri, although ants and possibly honey bees may make a lesser contribution. Pollination by bibionid flies has not previously been reported in asclepiads and is extremely uncommon amongst angiosperms.


Ant pollination Fynbos Myiophily Nematocera Renosterveld Eustegiinae 



We would like to thank John Skartveit and Peter Slingsby for assistance with the identification of the bibionids and ants respectively; Alex Hall, Alison Bijl and Sean Evans for assistance in the field; Steve Johnson for access to the GC-MS equipment; and, Timo van der Niet and two anonymous reviewers for comments on an earlier version of the manuscript. AS, SLS and YC thank the National Research Foundation of South Africa for funding (Grant Numbers 91441 and 90691). Finally, we would like to thank Jonkershoek Nature Reserve and CapeNature for access to the study site.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aak A, Knudsen GK (2011) Sex differences in olfaction-mediated visual acuity in blowflies and its consequences for gender-specific trapping. Entomol Exp Appl 139:25–34CrossRefGoogle Scholar
  2. Beattie AJ (2006) The evolution of ant pollination systems. Botanische Jahrbücher 127:43–55CrossRefGoogle Scholar
  3. Beattie AJ, Turnbull C, Knox RB, Williams E (1984) Ant inhibition of pollen function: a possible reason why ant pollination is rare. Am J Bot 71:421–426CrossRefGoogle Scholar
  4. Bruyns P (1999) The systematic position of Eustegia R Br(Apocynaceae-Asclepiadoideae). Botanische Jahrbücher 121:19–44Google Scholar
  5. Burger H, Jürgens A, Ayasse M, Johnson SD (2017) Floral signals and filters in a wasp-and a bee-pollinated Gomphocarpus species (Apocynaceae: Asclepiadeae). Flora 232:83–91CrossRefGoogle Scholar
  6. Clarke KR, Warwick R (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E Ltd, PlymouthGoogle Scholar
  7. Coombs G, Peter CI, Johnson SD (2009) A test for Allee effects in the self-incompatible wasp-pollinated milkweed Gomphocarpus physocarpus. Austral Ecol 34:688–697CrossRefGoogle Scholar
  8. Cruden RW (1972) Pollination biology of Nemophila menziesii (Hydrophyllaceae) with comments on the evolution of oligolectic bees. Evolution 26:373–389CrossRefGoogle Scholar
  9. Domingos-Melo A, de Lima Nadia T, Machado IC (2017) Complex flowers and rare pollinators: does ant pollination in Ditassa show a stable system in Asclepiadoideae (Apocynaceae)? Arthropod-Plant Interact 11:339–349CrossRefGoogle Scholar
  10. du Plessis M, Johnson SD, Nicolson SW, Bruyns PV, Shuttleworth A (2018) Pollination of the “carrion flowers” of an African stapeliad (Ceropegia mixta: Apocynaceae): the importance of visual and scent traits for the attraction of flies. Plant Syst Evol 304:357–372CrossRefGoogle Scholar
  11. Endress ME, Liede-Schumann S, Meve U (2014) An updated classification for Apocynaceae. Phytotaxa 159:175–194CrossRefGoogle Scholar
  12. Goldblatt P, Manning JC, Bernhardt P (2005) The floral biology of Melasphaerula (Iridaceae: Crocoideae): is this monotypic genus pollinated by March flies (Diptera: Bibionidae)? Ann Mo Bot Garden 92:268–274Google Scholar
  13. Hardy DE (1950) A monographic study of the African Bibionidae (Diptera). Part I: introduction and genus Bibio Geoffroy. J Kans Entomol Soc 23:137–153Google Scholar
  14. Heine E (1937) Observations on the pollination of New Zealand flowering plants. Trans Proc R Soc NZ 2:133–148Google Scholar
  15. Higham R, McQuillan P (2000) Cyathodes divaricata (Epacridaceae)—the first record of a bird-pollinated dioecious plant in the Australian flora. Aust J Bot 48:93–99CrossRefGoogle Scholar
  16. Huang Y, Zhang C-Q, Blackmore S, Li D-Z, Wu Z-K (2006) A preliminary study on pollination biology of Omphalogramma souliei Franch. (Primulaceae), a species endemic to China. Plant Syst Evol 261:89–98CrossRefGoogle Scholar
  17. Johnson SD (2010) The pollination niche and its role in the diversification and maintenance of the southern African flora. Philos Trans Roy Soc B 365:499–516CrossRefGoogle Scholar
  18. Johnson SD, Steiner KE (1994) Efficient pollination of the mass-flowering Cape orchid Disa obtusa Lindl. (Orchidaceae) by Bibio turneri Edwards (Diptera: Bibionidae). Afr Entomol 2:64–66Google Scholar
  19. Johnson SD, Steiner KE (2003) Specialized pollination systems in southern Africa. S Afr J Sci 99:345–348Google Scholar
  20. Johnson SD, Peter CI, Agren J (2004) The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio. Proc R Soc Lond B 271:803–809CrossRefGoogle Scholar
  21. Jürgens A, Dötterl S, Meve U (2006) The chemical nature of fetid floral odours in stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytol 172:452–468CrossRefGoogle Scholar
  22. Jürgens A, Dötterl S, Liede-Schumann S, Meve U (2008) Chemical diversity of floral volatiles in Asclepiadoideae-Asclepiadeae (Apocynaceae). Biochem Syst Ecol 36:842–852CrossRefGoogle Scholar
  23. Jürgens A, Dötterl S, Liede-Schumann S, Meve U (2010) Floral scent composition in early diverging taxa of Asclepiadoideae, and Secamonoideae (Apocynaceae). S Afr J Bot 76:749–761CrossRefGoogle Scholar
  24. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  25. Lehnebach CA, Robertson AW (2004) Pollination ecology of four epiphytic orchids of New Zealand. Ann Bot 93:773–781CrossRefGoogle Scholar
  26. Liede S (1997) Subtribes and genera of the tribe Asclepiadeae (Apocynaceae, Asclepiadoideae)—a synopsis. Taxon 46:233–247CrossRefGoogle Scholar
  27. Liede S (2001) Subtribe Astephaninae (Apocynaceae-Asclepiadoideae) reconsidered: new evidence based on cpDNA spacers. Ann Mo Bot Garden 88:657–668CrossRefGoogle Scholar
  28. Manning JC, Goldblatt P (2012) Plants of the Greater Cape Floristic Region 1: the Core Cape Region. Strelitzia 29. South African National Biodiversity Institute, PretoriaGoogle Scholar
  29. Medan D, Montaldo NH, Devoto M, Mantese A, Vasellati V, Roitman GG, Bartoloni NH (2002) Plant-pollinator relationships at two altitudes in the Andes of Mendoza, Argentina. Arct Antarct Alp Res 34:233–241CrossRefGoogle Scholar
  30. Meve U, Liede S (2004) Subtribal division of Ceropegieae (Apocynaceae-Asclepiadoideae). Taxon 53:61–72CrossRefGoogle Scholar
  31. Ollerton J, Johnson SD, Cranmer L, Kellie S (2003) The pollination ecology of an assemblage of grassland asclepiads in South Africa. Ann Bot 92:807–834CrossRefGoogle Scholar
  32. Ollerton J, Liede-Schumann S, Endress ME, Meve U, Rech AR, Shuttleworth A, Keller HA, Fishbein M et al (2019) The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study. Ann Bot 123:311–325CrossRefGoogle Scholar
  33. Pauw A (1998) Pollen transfer on birds’ tongues. Nature 394:731–732CrossRefGoogle Scholar
  34. Peter CI, Shuttleworth A (2014) Catching on to concatenation: evidence for pre-pollination intrasexual selection in plants. New Phytol 203:4–6CrossRefGoogle Scholar
  35. Primack RB (1983) Insect pollination in the New Zealand mountain flora. NZ J Bot 21:317–333CrossRefGoogle Scholar
  36. Rapini A, Chase MW, Goyder DJ, Griffiths J (2003) Asclepiadeae classification: evaluating the phylogenetic relationships of New World Asclepiadoideae (Apocynaceae). Taxon 52:33–50CrossRefGoogle Scholar
  37. Rapini A, van den Berg C, Liede-Schumann S (2007) Diversification of Asclepiadoideae (Apocynaceae) in the New World. Ann Mo Bot Garden 94:407–422CrossRefGoogle Scholar
  38. Shaw DC, Taylor RJ (1986) Pollination ecology of an alpine fell-field community in the North Cascades. Northwest Sci 60:21–31Google Scholar
  39. Shuttleworth A (2016) Smells like debauchery: the chemical composition of semen-like, sweat-like and faintly foetid floral odours in Xysmalobium (Apocynaceae: Asclepiadoideae). Biochem Syst Ecol 66:63–75CrossRefGoogle Scholar
  40. Shuttleworth A, Johnson SD (2009a) The importance of scent and nectar filters in a specialized wasp-pollination system. Funct Ecol 23:931–940CrossRefGoogle Scholar
  41. Shuttleworth A, Johnson SD (2009b) Specialized pollination in the African milkweed Xysmalobium orbiculare: a key role for floral scent in the attraction of spider-hunting wasps. Plant Syst Evol 280:37–44CrossRefGoogle Scholar
  42. Shuttleworth A, Johnson SD (2009c) New records of insect pollinators for South African asclepiads (Apocynaceae: Asclepiadoideae). S Afr J Bot 75:689–698CrossRefGoogle Scholar
  43. Shuttleworth A, Johnson S (2010) Floral scents of chafer-pollinated asclepiads and a potential hybrid. S Afr J Bot 76:770–778CrossRefGoogle Scholar
  44. Shuttleworth A, Johnson SD (2012) The Hemipepsis wasp-pollination system in South Africa: a comparative analysis of trait convergence in a highly specialized plant guild. Bot J Linn Soc 168:278–299CrossRefGoogle Scholar
  45. Shuttleworth A, Johnson SD, Jürgens A (2017) Entering through the narrow gate: a morphological filter explains specialized pollination of a carrion-scented stapeliad. Flora 232:92–103CrossRefGoogle Scholar
  46. Snijman DA (ed) (2013) Plants of the Greater Cape Floristic Region 2: the extra Cape Flora. Strelitzia 30. South African National Biodiversity Institute, PretoriaGoogle Scholar
  47. Straub SCK, Cronn RC, Edwards C, Fishbein M, Liston A (2013) Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (Apocynaceae). Genome Biol Evol 5:1872–1885CrossRefGoogle Scholar
  48. Surveswaran S, Sun M, Grimm GW, Liede-Schumann S (2014) On the systematic position of some Asian enigmatic genera of Asclepiadoideae (Apocynaceae). Bot J Linn Soc 174:601–619CrossRefGoogle Scholar
  49. Vergara CH, Badano EI (2009) Pollinator diversity increases fruit production in Mexican coffee plantations: the importance of rustic management systems. Agric Ecosyst Environ 129:117–123CrossRefGoogle Scholar
  50. Wall R, Fisher P (2001) Visual and olfactory cue interaction in resource-location by the blowfly, Lucilia sericata. Physiol Entomol 26:212–218CrossRefGoogle Scholar
  51. Wyatt R, Broyles SB (1994) Ecology and evolution of reproduction in milkweeds. Ann Rev Ecol Syst 25:423–441CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Cape TownRondeboschSouth Africa
  2. 2.Department of Plant Sciences and Afromontane Research Unit, Faculty of Natural and Agricultural SciencesUniversity of the Free StatePhuthaditjhabaSouth Africa
  3. 3.School of Life SciencesUniversity of KwaZulu-NatalScottsvilleSouth Africa

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