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Low abundance of long-tongued pollinators leads to pollen limitation in four specialized hawkmoth-pollinated plants in the Atlantic Rain forest, Brazil

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Abstract

Long-tubed hawkmoth-pollinated species present some of the most remarkable examples of floral specialization depending exclusively on long-tongued hawkmoths for sexual reproduction. Nonetheless, long-tongued hawkmoths do not rely exclusively on specialized plants as nectar sources, which may limit sexual reproduction through pollen limitation. However, very few studies have quantified the level of pollen limitation in plants with highly specialized floral traits in tropical regions. In this context, we studied four sympatric hawkmoth-pollinated species in a highland Atlantic Rain forest and assessed pollen limitation and their dependence on pollinators by analyzing the floral biology, breeding system, pollination mechanisms, and abundance of long-tongued pollinators. We showed that the four species are self-compatible, but are completely dependent on long-tongued hawkmoths to set fruits, and that flower visitation was infrequent in all plant species. Pollen limitation indices ranged from 0.53 to 0.96 showing that fruit set is highly limited by pollen receipt. Long-tongued moths are much less abundant and comprise only one sixth of the hawkmoth fauna. Pollen analyses of 578 sampled moths revealed that hawkmoths visited ca. 80 plant species in the community, but only two of the four species studied. Visited plants included a long-tubed hawkmoth-pollinated species endemic to the lowland forest ca. 15–20 km away from the study site. Specialization index (H 2 ′ = 0.20) showed that community-level interactions between hawkmoths and plants are generalized. We suggest that sexual reproduction of these highly specialized hawkmoth-pollinated species is impaired by competition among plants for pollinators, in conjunction with the low abundance and diversity of long-tongued pollinators.

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Acknowledgments

We thank João P. Villani on behalf of all the people of the Santa Virgínia Field Station for the facilities and help during field work; Instituto Florestal for the granting permission for field work; A.M.S. Corrêa and M.A.V. Cruz-Barros for their help in the pollen analyses; A.P. Moraes, C.E.P. Nunes, and M. Fernández Otárola for their help during the field work; and K. Agostini, M. Moré, P.E. Oliveira, R.E. Wyatt, S. Benitez-Vieyra, and W.R. Silva for their critical reading and valuable suggestions in an earlier version of the manuscript. We are also very grateful to Peter E. Gibbs, Pietro K. Maruyama, Dave Kelly, and two anonymous referees for their valuable suggestions on the final version of the manuscript. This research was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) as part of the Thematic Project Functional Gradient (Process Number 03/12595-7), within the BIOTA/FAPESP Program—The Biodiversity Virtual Institute (http://www.biota.org.br); Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (Grant 303084/2011-1 to MS). This study is part of FWA’s PhD supported by FAPESP (grant 2007/58666-3).

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Correspondence to Felipe W. Amorim.

Additional information

Communicated by: Sven Thatje

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Figure S1

Pollen tubes resulting from manual self-pollinations in four hawkmoth-pollinated species in an area of Montane Ombrophilous Dense Forest in the Santa Virginia Field Station, Serra do Mar State Park, south-eastern Brazil. A Pollen tubes on the stigma of Habenaria johannensis. B Pollen tubes in the ovary of Habenaria paulistana. Note deviation from the main bundle of pollen tubes towards the ovules (arrows). C Penetration of pollen tubes into the ovules (arrows) of Hillia parasitica. D Stigmatic surface of Posoqueria latifolia with pollen grains germinating (arrows) and pollen tubes penetrating the stigma. (DOC 1303 kb)

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Amorim, F.W., Wyatt, G.E. & Sazima, M. Low abundance of long-tongued pollinators leads to pollen limitation in four specialized hawkmoth-pollinated plants in the Atlantic Rain forest, Brazil. Naturwissenschaften 101, 893–905 (2014) doi:10.1007/s00114-014-1230-y

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Keywords

  • Habenaria johannensis
  • Habenaria paulistana
  • Hillia parasitica
  • Nectar sugar gradient
  • Pollen limitation index
  • Posoqueria latifolia