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

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Abstract

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.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Aak A, Knudsen GK (2011) Sex differences in olfaction-mediated visual acuity in blowflies and its consequences for gender-specific trapping. Entomol Exp Appl 139:25–34

    Article  Google Scholar 

  • Beattie AJ (2006) The evolution of ant pollination systems. Botanische Jahrbücher 127:43–55

    Article  Google Scholar 

  • 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 71:421–426

    Article  Google Scholar 

  • Bruyns P (1999) The systematic position of Eustegia R Br(Apocynaceae-Asclepiadoideae). Botanische Jahrbücher 121:19–44

    Google Scholar 

  • 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 232:83–91

    Article  Google Scholar 

  • Clarke KR, Warwick R (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E Ltd, Plymouth

    Google Scholar 

  • Coombs G, Peter CI, Johnson SD (2009) A test for Allee effects in the self-incompatible wasp-pollinated milkweed Gomphocarpus physocarpus. Austral Ecol 34:688–697

    Article  Google Scholar 

  • Cruden RW (1972) Pollination biology of Nemophila menziesii (Hydrophyllaceae) with comments on the evolution of oligolectic bees. Evolution 26:373–389

    Article  PubMed  Google Scholar 

  • 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 11:339–349

    Article  Google Scholar 

  • 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 304:357–372

    Article  Google Scholar 

  • Endress ME, Liede-Schumann S, Meve U (2014) An updated classification for Apocynaceae. Phytotaxa 159:175–194

    Article  Google Scholar 

  • 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 92:268–274

    Google Scholar 

  • Hardy DE (1950) A monographic study of the African Bibionidae (Diptera). Part I: introduction and genus Bibio Geoffroy. J Kans Entomol Soc 23:137–153

    Google Scholar 

  • Heine E (1937) Observations on the pollination of New Zealand flowering plants. Trans Proc R Soc NZ 2:133–148

    Google Scholar 

  • Higham R, McQuillan P (2000) Cyathodes divaricata (Epacridaceae)—the first record of a bird-pollinated dioecious plant in the Australian flora. Aust J Bot 48:93–99

    Article  Google Scholar 

  • 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 261:89–98

    Article  Google Scholar 

  • Johnson SD (2010) The pollination niche and its role in the diversification and maintenance of the southern African flora. Philos Trans Roy Soc B 365:499–516

    Article  Google Scholar 

  • 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 2:64–66

    Google Scholar 

  • Johnson SD, Steiner KE (2003) Specialized pollination systems in southern Africa. S Afr J Sci 99:345–348

    Google Scholar 

  • 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 271:803–809

    Article  Google Scholar 

  • Jürgens A, Dötterl S, Meve U (2006) The chemical nature of fetid floral odours in stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytol 172:452–468

    Article  CAS  PubMed  Google Scholar 

  • Jürgens A, Dötterl S, Liede-Schumann S, Meve U (2008) Chemical diversity of floral volatiles in Asclepiadoideae-Asclepiadeae (Apocynaceae). Biochem Syst Ecol 36:842–852

    Article  CAS  Google Scholar 

  • 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 76:749–761

    Article  CAS  Google Scholar 

  • Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120

    Article  Google Scholar 

  • Lehnebach CA, Robertson AW (2004) Pollination ecology of four epiphytic orchids of New Zealand. Ann Bot 93:773–781

    Article  PubMed  PubMed Central  Google Scholar 

  • Liede S (1997) Subtribes and genera of the tribe Asclepiadeae (Apocynaceae, Asclepiadoideae)—a synopsis. Taxon 46:233–247

    Article  Google Scholar 

  • Liede S (2001) Subtribe Astephaninae (Apocynaceae-Asclepiadoideae) reconsidered: new evidence based on cpDNA spacers. Ann Mo Bot Garden 88:657–668

    Article  Google Scholar 

  • Manning JC, Goldblatt P (2012) Plants of the Greater Cape Floristic Region 1: the Core Cape Region. Strelitzia 29. South African National Biodiversity Institute, Pretoria

    Google Scholar 

  • 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 34:233–241

    Article  Google Scholar 

  • Meve U, Liede S (2004) Subtribal division of Ceropegieae (Apocynaceae-Asclepiadoideae). Taxon 53:61–72

    Article  Google Scholar 

  • Ollerton J, Johnson SD, Cranmer L, Kellie S (2003) The pollination ecology of an assemblage of grassland asclepiads in South Africa. Ann Bot 92:807–834

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 123:311–325

    Article  PubMed  Google Scholar 

  • Pauw A (1998) Pollen transfer on birds’ tongues. Nature 394:731–732

    Article  CAS  Google Scholar 

  • Peter CI, Shuttleworth A (2014) Catching on to concatenation: evidence for pre-pollination intrasexual selection in plants. New Phytol 203:4–6

    Article  PubMed  Google Scholar 

  • Primack RB (1983) Insect pollination in the New Zealand mountain flora. NZ J Bot 21:317–333

    Article  Google Scholar 

  • Rapini A, Chase MW, Goyder DJ, Griffiths J (2003) Asclepiadeae classification: evaluating the phylogenetic relationships of New World Asclepiadoideae (Apocynaceae). Taxon 52:33–50

    Article  Google Scholar 

  • Rapini A, van den Berg C, Liede-Schumann S (2007) Diversification of Asclepiadoideae (Apocynaceae) in the New World. Ann Mo Bot Garden 94:407–422

    Article  Google Scholar 

  • Shaw DC, Taylor RJ (1986) Pollination ecology of an alpine fell-field community in the North Cascades. Northwest Sci 60:21–31

    Google Scholar 

  • 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 66:63–75

    Article  CAS  Google Scholar 

  • Shuttleworth A, Johnson SD (2009a) The importance of scent and nectar filters in a specialized wasp-pollination system. Funct Ecol 23:931–940

    Article  Google Scholar 

  • 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 280:37–44

    Article  Google Scholar 

  • Shuttleworth A, Johnson SD (2009c) New records of insect pollinators for South African asclepiads (Apocynaceae: Asclepiadoideae). S Afr J Bot 75:689–698

    Article  Google Scholar 

  • Shuttleworth A, Johnson S (2010) Floral scents of chafer-pollinated asclepiads and a potential hybrid. S Afr J Bot 76:770–778

    Article  CAS  Google Scholar 

  • 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 168:278–299

    Article  Google Scholar 

  • Shuttleworth A, Johnson SD, Jürgens A (2017) Entering through the narrow gate: a morphological filter explains specialized pollination of a carrion-scented stapeliad. Flora 232:92–103

    Article  Google Scholar 

  • Snijman DA (ed) (2013) Plants of the Greater Cape Floristic Region 2: the extra Cape Flora. Strelitzia 30. South African National Biodiversity Institute, Pretoria

    Google Scholar 

  • 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 5:1872–1885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 174:601–619

    Article  Google Scholar 

  • Vergara CH, Badano EI (2009) Pollinator diversity increases fruit production in Mexican coffee plantations: the importance of rustic management systems. Agric Ecosyst Environ 129:117–123

    Article  Google Scholar 

  • Wall R, Fisher P (2001) Visual and olfactory cue interaction in resource-location by the blowfly, Lucilia sericata. Physiol Entomol 26:212–218

    Article  Google Scholar 

  • Wyatt R, Broyles SB (1994) Ecology and evolution of reproduction in milkweeds. Ann Rev Ecol Syst 25:423–441

    Article  Google Scholar 

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Acknowledgements

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.

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Correspondence to Adam Shuttleworth.

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Chirango, Y., Steenhuisen, SL., Bruyns, P.V. et al. The March fly and the ant: the unusual pollination system of Eustegia minuta (Apocynaceae: Asclepiadoideae). Arthropod-Plant Interactions 13, 745–755 (2019). https://doi.org/10.1007/s11829-019-09675-2

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