Plant Ecology and Evolution 154(3): 447-457, doi: 10.5091/plecevo.2021.1860
Flower morphological differentiation and plant-pollinator interactions among sympatric Aframomum species (Zingiberaceae) with floral trumpet type in the tropical African rainforest
expand article infoElie Chrisnel Nzigou Doubindou, Alexandra C. Ley§
‡ Faculté des Sciences, Université des Sciences et Techniques de Masuku, Franceville, Gabon§ Institut für Geobotanik und Botanischer Garten, University Halle-Wittenberg, Halle (Saale), Germany
Open Access
Abstract

Background and aims – Diversification in plant-pollinator interactions based on floral diversity is potentially a mechanism of coexistence in angiosperms. However, besides high floral diversity, some genera seemingly exhibit the same floral type in many of their species. This contradicts some expectations of competitive exclusion. We thus tested on a finer flower morphological scale whether five sympatric Aframomum species (61 spp., Zingiberaceae) in southeastern Gabon exhibiting the same general floral type (trumpet) were differentiated, and whether this resulted in different “pollinator niches”.

Material and methods – We carried out a detailed survey measuring 18 flower morphological parameters as well as nectar volume (μl) and sugar concentration (% Brix) on five flowers per species and locality. Furthermore, we observed inflorescence phenology and pollinator activity from 8 am to 4 pm for 12 to 50 hours per species and conducted pollinator exclusion experiments.

Key results – This study proves fine-scale flower morphological and resource differentiation within the trumpet floral type. Pollination-relevant parts of the flowers, however, remain constant across species. Our pollinator observations reveal the same broad bee pollinator spectrum for all observed simultaneously flowering sympatric species.

Conclusion – As we could not detect a pollinator-based differentiation in the studied sympatric Aframomum species we assume that species boundaries developed randomly by genetic drift during geographic isolation in the past. The trumpet floral type and its pollinator guild, however, were maintained due to similar selection pressures in comparable habitats during isolation and are potentially an advantage for increased pollinator attraction through co-flowering.

Keywords
Aframomum, Africa, bee pollination, floral morphology, floral type, Gabon, pollinator sharing, tropics, Zingiberaceae

References

  • Armbruster W.S., Edwards M.E. & Debevec E.M. 1994. Floral character displacement generates assemblage structure of western Australian trigger plants (Stylidium). Ecology 75: 315–329. https://doi.org/10.2307/1939537
  • Auvray G., Harris D.J., Richardson J.E., Newman M.F. & Särkinen T.E. 2010. Phylogeny and dating of Aframomum (Zingiberaceae). In: Barfod A., Davis J.I., Petersen G. & Seberg O. (eds) Diversity, phylogeny, and evolution in the Monocotyledons: 287–305. Aarhus University Press, Aarhus.
  • Bastida J.M., Alcántara J.M., Rey P.J., Vargas P. & Herrera C.M. 2009. Extended phylogeny of Aquilegia: the biogeographical and ecological patterns of two simultaneous but contrasting radiations. Plant Systematics and Evolution 284(3–4): 171–185. https://doi.org/10.1007/s00606-009-0243-z
  • Bates D., Maechler M. & Bolker B. 2011. Lme4: linear mixed-effects models using s4 classes. R package version 0. 999375-38. Available from http://cran.r-project.org/package=lme4 [accessed 11 Aug. 2021].
  • Bawa K.S. 1990. Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology & Systematics 21: 399–422. https://www.jstor.org/stable/2097031
  • Brisson J.D., Lajoie M., Jacques Allard J. & Jacobe-Remacle A. 1994. Les insectes pollinisateurs: des alliés à protéger. Fleurs Plantes Jardins 3: 1–143.
  • Claßen-Bockhoff R., Speck T., Tweraser E., Wester P., Thimm S. & Reith M. 2004. Staminal lever mechanism in Salvia. Organisms, Diversity & Evolution 4: 189–205. https://doi.org/10.1016/j.ode.2004.01.004
  • Couvreur T.L., Dauby G., Blach‐Overgaard A., et al. 2020. Tectonics, climate and the diversification of the tropical African terrestrial flora and fauna. Biological Reviews 96(1): 16–51. https://doi.org/10.1111/brv.12644
  • Cruden R.W. 1976. Intraspecific variation in pollen-ovule ratios and nectar secretion – Preliminary evidence of ecotypic adaptation. Annals of the Missouri Botanical Garden 63(2): 277–289. https://doi.org/10.2307/2395306
  • Dhetchuvi J.B. 1996. Taxonomie et phytogéographie des Marantaceae et Zingiberaceae d’Afrique centrale (Gabon, Congo, Zaïre, Rwanda & Burundi). PhD thesis, Université Libre de Bruxelles, Belgium.
  • Eardley C., Kuhlmann M. & Pauly A. 2010. The bee genera and subgenera of sub-Saharan Africa. ABC Taxa 7: 1–138.
  • Farkas Á., Molnár R., Morschhauser T. & Hahn I. 2012. Variation in nectar volume and sugar concentration of Allium ursinum L. ssp. ucrainicum in three habitats. The Scientific World Journal 2012: 138579. https://doi.org/10.1100/2012/138579
  • Fohouo F.N.T., Djonwangwe D., Messi J. & Brückner D. 2010. Activité de butinage et de pollinisation de Apis mellifera andonsonii Latreille (Hymenoptera: Apidae) sur les fleurs de Helianthus annus (Asteraceae) à Ngaoundere (Cameroun). Cameroon Journal of Experimental Biology 5(1): 1–9. https://doi.org/10.4314/cajeb.v5i1.44442
  • Giannini T.C., Garibaldi L.A., Acosta A.L., et al. 2015. Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLoS ONE 10(9): e0137198. https://doi.org/10.1371/journal.pone.0137198
  • Gottsberger G. 1989. Beetle pollination and flowering rhythm of Annona spp. (Annonaceae) in Brazil. Plant Systematics and Evolution 167(3–4): 165–187. https://doi.org/10.1007/bf00936404
  • Grant V. 1994. Modes and origins of mechanical and ethological isolation in angiosperms. Proceedings of the National Academy of Sciences of the United States of America 91(1): 3–10. https://doi.org/10.1073/pnas.91.1.3
  • Grey-Wilson C. 1980. Impatiens of Africa. A.A. Balkema, Rotterdam.
  • Hammer Ø., Harper D.A.T. & Ryan P.D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): art. 4. Available from http://palaeo-electronica.org/2001_1/past/issue1_01.htm [accessed 11 Aug. 2021].
  • Harris D.J., Poulsen A.D., Frimodt-Møller C., Preston J. & Cronk Q.C.B. 2000. Rapid radiation in Aframomum (Zingiberaceae): evidence from nuclear ribosomal DNA internal transcribed spacer (ITS) sequences. Edinburgh Journal of Botany 57(3): 377–395. https://doi.org/10.1017/s0960428600000378
  • Harris D.J. & Wortley A.H. 2018. Monograph of Aframomum (Zingiberaceae). Systematic Botany Monographs 104: 1–204.
  • Herrera C.M., Pérez R. & Alonso C. 2006. Extreme intraplant variation in nectar sugar composition in an insect-pollinated perennial herb. American Journal of Botany 93(4): 575–581. https://doi.org/10.3732/ajb.93.4.575
  • Horvitz C.C. & Schemske D.W. 1988. A test of the pollinator limitation hypothesis for a neotropical herb. Ecology 69(1): 200–206. https://doi.org/10.2307/1943175
  • Johnson S.D., Linder H.P. & Steiner K.E. 1998. Phylogeny and radiation of pollination systems in Disa (Orchidaceae). American Journal of Botany 85(3): 402–411. https://doi.org/10.2307/2446333
  • Kim W., Gilet T. & Bush J.W.M. 2011. Optimal concentrations in nectar feeding. Proceedings of the National Academy of Sciences of the United States of America 108(40): 16618–16621. https://doi.org/10.1073/pnas.1108642108
  • Koechlin J. 1964. Zingibéracées. Flore du Gabon 9: 15–88.
  • Lekane Tsobgou D. 2009. L’impact socioéconomique et spatial de la microfinance sur le développement rural au Cameroun: le cas des mutuelles communautaires de croissance (mc2). PhD thesis, Université de Yaoundé 1, Cameroun.
  • Ley A.C. 2008. Evolutionary tendencies in African Marantaceae: evidence from floral morphology, ecology and phylogeny. PhD thesis, Johannes Gutenberg University, Germany. https://doi.org/10.25358/openscience-2617
  • Ley A.C. & Claßen-Bockhoff R. 2011. Evolution in African Marantaceae - Evidence from phylogenetic, ecological and morphological studies. Systematic Botany 36(2): 277–290. https://doi.org/10.1600/036364411x569480
  • Ley A.C. & Claßen-Bockhoff R. 2013. Breeding system and fruit set in African Marantaceae. Flora - Morphology, Distribution, Functional Ecology of Plants 208(8): 532–537. https://doi.org/10.1016/j.flora.2013.07.011
  • Ley A.C. & Harris D.J. 2014. Flower morphological diversity in Aframomum (Zingiberaceae) from Africa – the importance of distinct floral types with presumably specific pollinator associations, differential habitat adaptations & allopatry in speciation and species maintenance. Plant Ecology and Evolution 147(1): 33–48. https://doi.org/10.5091/plecevo.2014.824
  • Lock J.M., Hall J.B. & Abbiw D.K. 1977. The cultivation of melegueta pepper (Aframomum melegueta) in Ghana. Economic Botany 31(3): 321–330. https://doi.org/10.1007/bf02866884
  • Macior L.W. 1971. Coevolution of plants and animals - Systematic insights from plant-insect interactions. Taxon 20: 17–28. https://doi.org/10.2307/1218530
  • Maley J. 1996. The African rain forest – main characteristics of changes in vegetation and climate from the Upper Cretaceous to the Quaternary. Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences 104: 31–73. https://doi.org/10.1017/S0269727000006114
  • Morales C.L. & Traveset A. 2008. Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Critical Reviews in Plant Sciences 27(4): 221–238. https://doi.org/10.1080/07352680802205631
  • Ollerton J. & Watts S. 2000. Phenotype space and floral typology: towards and objective assessment of pollination syndromes. In: Scandinavian Association for Pollination Ecology honours Knut Faegri. Det Norske Videnskaps-Akademi. I. Matematisk Naturvidenskapelige Klasse, Skrifter, Ny Serie 39: 149–159.
  • Perret M., Chautems A., Spichiger R., Peixoto M. & Savolainen V. 2001. Nectar sugar composition in relation to pollination syndromes in Sinningieae (Gesneriaceae). Annals of Botany 87(2): 267–273. https://doi.org/10.1006/anbo.2000.1331
  • R Core Team 2020. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from https://www.R-project.org [accessed 20 Jul. 2021].
  • Roubik D.W., Yanega D., Aluja S.M., Buchmann S.L. & Inouye D.W. 1995. On optimal nectar foraging by some tropical bees (Hymenoptera: Apidae). Apidologie 26: 197–211. https://doi.org/10.1051/apido:19950303
  • Schemske D.W. 1981. Floral convergence and pollinator sharing in two bee pollinated tropical herbs. Ecology 62(4): 946–954. https://doi.org/10.2307/1936993
  • Silva F.A., Chatt E.C., Mahalim S.-N., et al. 2020. Metabolomic profiling of Nicotiana spp. nectars indicate that pollinator feeding preference is a stronger determinant than plant phylogenetics in shaping nectar diversity. Metabolites 10(5): 214. https://doi.org/10.3390/metabo10050214
  • Specht C.D., Kress W.J., Stevenson D.W. & De Salle R. 2001. A molecular phylogeny of Costaceae (Zingiberales). Molecular Phylogenetics and Evolution 21(3): 333–345. https://doi.org/10.1006/mpev.2002.1144
  • Stanley D.A. & Stout J.C. 2014. Pollinator sharing between mass-flowering oilseed rape and co-flowering wild plants: implications for wild plant pollination. Plant Ecology 215(3): 315–325. https://doi.org/10.1007/s11258-014-0301-7
  • Sutherland S. & Delph L.F. 1984. On the importance of male fitness in plants: patterns of fruit-set. Evolution (65): 1093–1104. https://doi.org/10.2307/1938317
  • Tachiki Y., Iwasa Y. & Satake A. 2010. Pollinator coupling can induce synchronized flowering in different plant species. Journal of Theoretical Biology 267: 153–163. https://doi.org/10.1016/j.jtbi.2010.08.023
  • Tomlinson K.W., Poorter L., Sterck F.J., et al. 2013. Leaf adaptations of evergreen and deciduous trees of semi‐arid and humid savannas on three continents. Journal of Ecology 101(2): 430–440. https://doi.org/10.1111/1365-2745.12056
  • Tukey J.W. 1957. On the comparative anatomy of transformations. The Annals of Mathematical Statistics. 28: 602–632. https://www.jstor.org/stable/2237223
  • Viana B.F., Boscolo D., Mariano Neto E., et al. 2012. How well do we understand landscape effects on pollinators and pollination services? Journal of Pollination Ecology 7: 31–40. https://doi.org/10.26786/1920-7603(2012)2
  • Wang G., Cannon C.H. & Chen J. 2016. Pollinator sharing and gene flow among closely related sympatric dioecious fig taxa. Proceedings of the Royal Society B 283: 20152963. https://doi.org/10.1098/rspb.2015.2963
  • Wester P. & Claßen-Bockhoff R. 2007. Floral diversity and pollen transfer mechanisms in bird-pollinated Salvia species. Annals of Botany 100(2): 401–421. https://doi.org/10.1093/aob/mcm036
  • Zajácz E., Zaják Á., Szalai-Mátray E. & Szalai T. 2006. Nectar production of some sunflower hybrids. Journal of Apicultural Science 50(2): 7–11.
  • Zakaria C.A. 2013. Études chimiques et biologiques d’Aframomum sceptrum (Zingiberaceae) et de la curcumine. PhD thesis, Université Paris-Sud, France.