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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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References

  • Agosta SJ, Janzen DH (2005) Body size distributions of large Costa Rican dry forest moths and the underlying relationship between plant and pollinator morphology. Oikos 108:183–193

    Article  Google Scholar 

  • Amorim FW, Avila RS Jr, Camargo JA, Vieira A, Oliveira PE (2009) A hawkmoth crossroads? Species richness, seasonality and biogeographical affinities of Sphingidae in a Brazilian Cerrado. J Biogeogr 36:662–674

    Article  Google Scholar 

  • Amorim FW, Galetto L, Sazima M (2013) Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae). Plant Biol 15:317–327

    Article  PubMed  CAS  Google Scholar 

  • Arditti J, Elliott J, Kitching IJ, Wasserthal LT (2012) ‘Good Heavens what insect can suck it’—Charles Darwin, Angraecum sesquipedale and Xanthopan morganii praedicta. Bot J Linn Soc 169:403–432

    Article  Google Scholar 

  • Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347–349

    Article  Google Scholar 

  • Batista JAN, Bianchetti LB, Miranda ZJ (2006) A revision of Habenaria section Macroceratitae (Orchidaceae) in Brazil. Brittonia 58:10–41

    Article  Google Scholar 

  • Bawa KS, Bullock SH, Perry DR, Coville RE, Grayum MH (1985) Reproductive biology of tropical lowland rain forest II. Pollination systems. Am J Bot 72:346–356

    Article  Google Scholar 

  • Beach J (1983) Posoqueria latifolia (Boca de Vieja, Guayaba de Mico, Fruta de Mono). In: Janzen DH (ed) Costa Rican natural history. University of Chicago Press, Chicago, pp 307–308

    Google Scholar 

  • Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139

    Article  Google Scholar 

  • Carnaval AC, Moritz C, Hickerson M, Haddad C, Rodrigues M (2009) Stability predicts diversity in the Brazilian Atlantic Forest hotspot. Science 323:785–789

    Article  PubMed  CAS  Google Scholar 

  • Darrault RO, Schlindwein C (2002) Esfingídeos (Lepidoptera, Sphingidae) no Tabuleiro Paraibano, nordeste do Brasil: abundância, riqueza e relação com plantas esfingófilas. Rev Bras Zool 19:429–443

    Article  Google Scholar 

  • Darrault RO, Schlindwein C (2005) Limited fruit production in Hancornia speciosa (Apocynaceae) and pollination by nocturnal and diurnal insects with long mouth parts. Biotropica 37:381–388

    Article  Google Scholar 

  • Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilised by insects. D. Appleton, New York

    Google Scholar 

  • Delprete PG (2009) Taxonomic history, morphology, and reproductive biology of the tribe Posoquerieae (Rubiaceae, Ixoroideae). Ann Mo Bot Gard 96:79–89

    Article  Google Scholar 

  • Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analysing bipartite ecological networks. Open Ecol J 2:7–24

    Article  Google Scholar 

  • Dressler RL (1993) Phylogeny and classification of the orchid family. Dioscorides Press, Portland

    Google Scholar 

  • Erdtman G (1960) The acetolysis method. A revised description. Sven Bot Tidskr 54:561–564

    Google Scholar 

  • Fallen ME (1986) Floral structure in the Apocynaceae: morphological, functional, and evolutionary aspects. Bot Jahrb Syst 106:245–286

    Google Scholar 

  • Fausto JA, Eckhart VM, Geber MA (2001) Reproductive assurance and the evolutionary ecology of self-pollination in Clarkia xantiana (Onagraceae). Am J Bot 88:1794–1800

    Article  PubMed  Google Scholar 

  • Galetto L, Bernardello G (2005) Nectar. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Enviroquest, Ontario, pp 261–313

    Google Scholar 

  • Glinos E, Cocucci AA (2011) Pollination biology of Canna indica (Cannaceae) with particular reference to the functional morphology of the style. Plant Syst Evol 291:49–58

    Article  Google Scholar 

  • Haber WA (1984) Pollination by deceit in an mass-flowering tropical tree Plumeria rubra L. (Apocynaceae). Biotropica 16:269–275

    Article  Google Scholar 

  • Haber WA, Frankie GW (1989) A tropical hawkmoth community: Costa Rican dry forest Sphingidae. Biotropica 21:155–172

    Article  Google Scholar 

  • Hallé F (1967) Etude biologique et morphologique de la tribu des Gardéniées (Rubiacées). Mém ORSTOM 22:1–146

    Google Scholar 

  • Harder LD, Johnson SD (2009) Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol 183:530–545

    Article  PubMed  Google Scholar 

  • Herrera CM (1990) The adaptedness of the floral phenotype in a relict endemic, hawkmoth-pollinated violet. 1. Patterns of variation among disjunct populations. Biol J Linn Soc 40:275–291

    Article  Google Scholar 

  • Huang S-Q, Fenster CB (2007) Absence of long-tongued pollinators for long corolla-tube Himalayan Pedicularis species: implications for the evolution of corolla length. Int J Plant Sci 168:325–331

    Article  Google Scholar 

  • Ignatov II, Janovec JP, Centeno P, Tobler MW, Grados J, Lamas G, Kitching IJ (2011) Patterns of Richness, composition, and distribution of sphingid moths along an elevational gradient in the andes-amazon region of southeastern Peru. Ann Entomol Soc Am 104:68–76

    Article  Google Scholar 

  • Janzen DH (1986) Biogeography of an unexceptional place: what determines the saturniid and sphingid moth fauna of Santa Rosa National Park, Costa Rica, and what does it mean to conservation biology? Brenesia 25(26):51–87

    Google Scholar 

  • Janzen DH (1987) How moths pass the dry season in a Costa Rican dry forest. Insect Sci Appl 8:489–500

    Google Scholar 

  • Johnson SD, Neal PR, Peter CI, Edwards TJ (2004) Fruiting failure and limited recruitment in remnant populations of the hawkmoth-pollinated tree Oxyanthus pyriformis subsp. pyriformis (Rubiaceae). Biol Conserv 120:31–39

    Article  Google Scholar 

  • Joly CA, Assis MA, Bernacci LC, Tamashiro JY, Campos MCR, Gomes JAMA et al (2012) Floristic and phytosociology in permanent plots of the Atlantic Rainforest along an altitudinal gradient in southeastern Brazil. Biota Neotr 12:123–145

    Google Scholar 

  • Kearns CA, Inouye DW (1993) Techniques for pollination biologists. Colorado University Press, Niwot

    Google Scholar 

  • Kislev ME, Kravitz Z, Lorch J (1972) A study of hawkmoth pollination by a palynological analysis of the proboscis. Israel J Bot 21:57–75

    Google Scholar 

  • Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen limitation in plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497

    Article  Google Scholar 

  • Köppen W (1948) Climatologia. Fondo de Cultura Econômica, México

    Google Scholar 

  • Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520

    Article  Google Scholar 

  • Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol 34:125–128

    PubMed  CAS  Google Scholar 

  • Martins DJ, Johnson SD (2007) Hawkmoth pollination of aerangoid orchids in Kenya, with special reference to nectar sugar concentration gradients in the floral spurs. Am J Bot 94:650–659

    Article  PubMed  Google Scholar 

  • Martins DJ, Johnson SD (2013) Interactions between hawkmoths and flowering plants in East Africa: polyphagy and evolutionary specialization in an ecological context. Biol J Linn Soc 110:199–213

    Article  Google Scholar 

  • Maruyama PK, Oliveira GM, Ferreira C, Dalsgaard B, Oliveira PE (2013) Pollination syndromes ignored: importance of non-ornithophilous flowers to neotropical savanna hummingbirds. Naturwissenschaften 100:1061–1068

    Article  PubMed  CAS  Google Scholar 

  • Moeller DA (2006) Geographic structure of pollinator communities, reproductiveassurance, and the evolution of self-pollination. Ecology 87:1510–1522

    Article  PubMed  Google Scholar 

  • Moody-Weis JM, Heywood JS (2001) Pollination limitation to reproductive success in the Missouri evening primrose, Oenothera macrocarpa (Onagraceae). Am J Bot 88:1615–1622

    Article  PubMed  CAS  Google Scholar 

  • Moré M, Sérsic AN, Cocucci AA (2007) Restriction of pollinator assemblage through flower length and width in three long-tongued hawkmoth-pollinated species of Mandevilla (Apocynaceae, Apocynoideae). Ann Mo Bot Gard 94:487–506

    Article  Google Scholar 

  • Moré M, Amorim FW, Benitez-Vieyra S, Medina AM, Sazima M, Cocucci AA (2012) Armament imbalances: match and mismatch in plant-pollinator traits of highly specialized long-spurred orchids. PLoS ONE 7:e41878. doi:10.1371/journal.pone.0041878

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller F (1866) Über die Befruchtung der Martha (Posoqueria?) fragrans. Bot Zeit 23:129–133

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Nilsson LA (1988) The evolution of flowers with deep corolla tubes. Nature 334:147–149

    Article  Google Scholar 

  • Nilsson LA, Jonsson L, Ralison L, Randrianjohany E (1987) Angraecoid orchids and hawkmoths in central Madagascar: specialized pollination systems and generalist foragers. Biotropica 19:310–318

    Article  Google Scholar 

  • Oliveira PE, Gibbs PE (2000) Reproductive biology of woody plants in a Cerrado community of central Brazil. Flora 195:311–329

    Google Scholar 

  • Oliveira PE, Gibbs PE, Barbosa AA (2004) Moth pollination of woody species in the Cerrados of Central Brazil: a case of so much owed to so few? Plant Syst Evol 245:41–54

    Article  Google Scholar 

  • Ollerton J, Tarrant S, Winfree R (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Article  Google Scholar 

  • Ortega-Baes P, Gorostiague P (2013) Extremely reduced sexual reproduction in the clonal cactus Echinopsis thelegona. Plant Syst Evol 299:785–791

    Article  Google Scholar 

  • Pedron M, Buzatto CR, Singer RB, Batista JAN, Moser A (2012) Pollination biology of four sympatric species of Habenaria (Orchidaceae: Orchidinae) from southern Brazil. Bot J Linn Soc 170:141–156

    Article  Google Scholar 

  • Puff CAI, Buchner R, Rohrhofer U (1995) The united stamens of Rubiaceae. Morphology, anatomy; their role in pollination ecology. Ann Mo Bot Gard 82:357–382

    Article  Google Scholar 

  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) Brazilian Atlantic forest: how much is left and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153

    Article  Google Scholar 

  • Rosas‐Guerrero V, Aguilar R, Martén‐Rodríguez S, Ashworth L, Lopezaraiza‐Mikel M, Bastida JM, Quesada M, Irwin R (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecol Lett 17:388–400

    Article  PubMed  Google Scholar 

  • Silberbauer-Gottsberger I, Gottsberger G, Ehrendorfer F (1992) Hybrid speciation and radiation in the neotropical woody genus Tocoyena (Rubiaceae). Plant Syst Evol 181:143–169

    Article  Google Scholar 

  • Taylor CM (1994) Revision of Hillia (Rubiaceae). Ann Mo Bot Gard 81:571–609

    Article  Google Scholar 

  • Vamosi JC, Knight TM, Steets JA, Mazer SJ, Burd M, Ashman TL (2006) Pollination decays in biodiversity hotspots. Proc Natl Acad Sci USA 103:956–961

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Veloso HP, Rangel-Filho ALR, Lima JCA (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. IBGE, Departamento de Recursos Naturais e Estudos Ambientais

  • Wasserthal LT (1997) The pollinators of the Malagasy star orchids Angraecum sesquipedale, A. sororium and A. compactum and the evolution of extremely long spurs by pollinator shift. Bot Acta 110:343–359

    Article  Google Scholar 

  • Wolowski M, Ashman T-L, Freitas L (2013) Community-wide assessment of pollen limitation in hummingbird-pollinated plants of a tropical montane rain forest. Ann Bot London 112:903–910

    Article  Google Scholar 

  • Wolowski M, Ashman T-L, Freitas L (2014) Meta-analysis of pollen limitation reveals the relevance of pollination generalization in the Atlantic Forest of Brazil. PLoS ONE 9(2):e89498. doi:10.1371/journal.pone.0089498

    Article  PubMed  PubMed Central  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, New Jersey

    Google Scholar 

  • Zhang Z-Q, Kress WJ, Xie W-J, Ren P-Y, Gao J-Y, Li Q-J (2011) Reproductive biology of two Himalayan alpine gingers (Roscoea spp., Zingiberaceae) in China: pollination syndrome and compensatory floral mechanisms. Plant Biol 13:582–589

    Article  PubMed  CAS  Google Scholar 

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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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Authors and Affiliations

  1. Departamento de Botânica, Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Distrito de Rubião Junior s/n; Cx. Postal 510, 18618-970, Botucatu, São Paulo, Brazil

    Felipe W. Amorim

  2. Programa de Pós-Graduação em Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, São Paulo, Brazil

    Felipe W. Amorim & Graham E. Wyatt

  3. Department of Plant Biology, University of Georgia, Athens, GA, USA

    Graham E. Wyatt

  4. Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, São Paulo, Brazil

    Marlies Sazima

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  1. Felipe W. Amorim
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  3. Marlies Sazima
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Correspondence to Felipe W. Amorim.

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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). https://doi.org/10.1007/s00114-014-1230-y

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