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Pollination generalization and reproductive assurance by selfing in a tropical montane ecosystem

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Abstract

Pollination and reproduction are important processes for understanding plant community dynamics. Information regarding pollination and reproduction is urgent for threatened ecosystems, such as tropical montane ecosystems. In tropical mountains, pollination patterns are expected to conform to the reproductive assurance theory (due to low pollinator activity) and old, climatically buffered and infertile landscapes (OCBIL) theory (due to restricted plant range size). For 82 plant species of the Itatiaia National Park (including endemic and endangered species), we evaluated at least one of the following features: pollinator identity, flower color and size, flowering phenology, and pollinator dependence. Most plant species (ca. 60%) were pollinated by two or more functional groups of pollinators (generalized pollination), with high importance of flies as pollinators. There was low pollinator activity overall (less than one visit per flower per hour). Notably, the invasive honeybee Apis mellifera L. performed half of the visits to this entire plant community, suggesting an impact on the native pollinator fauna and consequently on the native flora. Most endemic plants were generalized with white and small flowers, while endangered species were pollination-specialized with colorful and large flowers. Thus, endangered species are susceptible to changes in pollinator fauna. Flowering seasonality reflected the importance of climatic constraints in this environment. One-third of the plant species were autogamous. Our data suggest that pollinator scarcity may have promoted reproductive assurance strategies such as generalization and pollinator independence. Our community-level study highlighted consistent pollination patterns for tropical mountains and emphasized threats for specialized endangered species.

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Data availability

Part of the data used here is already available in Bergamo et al. (2020a, 2020b). The data is available in the following https://doi.org/10.6084/m9.figshare.16777729.

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References

  • Altshuler DL (2003) Flower color, hummingbird pollination, and habitat irradiance in four Neotropical forests. Biotropica 35:344–355

    Article  Google Scholar 

  • Arroyo MTK, Primack R, Armesto J (1982) Community studies in pollination ecology in the high temperate Andes of central Chile. I. Pollination mechanisms and altitudinal variation. Am J Bot 69:82–97

    Article  Google Scholar 

  • Assis MV, Mattos EA (2016) Vulnerabilidade da vegetação de campos de altitude às mudanças climáticas. Oecol Austr 20:24–36

    Article  Google Scholar 

  • Aximoff I, Nunes-Freitas AF, Braga JMA (2016) Regeneração natural pós-fogo nos campos de altitude do Parque Nacional do Itatiaia, sudeste do Brasil. Oecol Austr 20:62–80

    Article  Google Scholar 

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

    Google Scholar 

  • Bartoš M, Janeček Š, Janečková P et al (2020) Self-compatibility and autonomous selfing of plants in meadow communities. Plant Biol 22:120–128

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Bergamo PJ, Rech AR, Brito VLG, Sazima M (2016) Flower colour and visitation rates of Costus arabicus support the ‘bee avoidance’ hypothesis for red-reflecting hummingbird-pollinated flowers. Func Ecol 30:710–720

    Article  Google Scholar 

  • Bergamo PJ, Wolowski M, Telles FJ, Brito VLG, Varassin IG, Sazima M (2019) Bracts and long-tube flowers of hummingbird-pollinated plants are conspicuous to hummingbirds but not to bees. Biol J Linn Soc 126:533–544

    Article  Google Scholar 

  • Bergamo PJ, Streher NS, Traveset A, Wolowski M, Sazima M (2020a) Pollination outcomes reveal negative-density dependence coupled with interspecific facilitation among plants. Ecol Lett 23:129–139

    Article  PubMed  Google Scholar 

  • Bergamo PJ, Streher NS, Wolowski M, Sazima M (2020b) Pollinator-mediated facilitation is associated to floral abundance, trait similarity and enhanced community-level fitness. J Ecol 108:1334–1346

    Article  Google Scholar 

  • Brade AC (1956) A flora do Parque Nacional do Itatiaia. Boletim Do Parque Nacional Do Itatiaia 5:7–85

    Google Scholar 

  • Brito VLG, Rech AR, Ollerton J, Sazima M (2017) Nectar production, reproductive success and the evolution of generalised pollination within a specialised pollen-rewarding plant family: a case study using Miconia theizans. Plant Syst Evol 303:709–718

    Article  Google Scholar 

  • Buzato S, Sazima M, Sazima I (2000) Hummingbird-pollinated floras at three Atlantic forest sites. Biotropica 32:824–841

    Article  Google Scholar 

  • Camargo MGG, Lunau K, Batalha MA, Brings S, Brito VLG, Morellato LPC (2019) How flower colour signals allure bees and hummingbirds: a community-level test of the bee avoidance hypothesis. New Phytol 222:1112–1122

    Article  PubMed  Google Scholar 

  • Carstensen DW, Sabatino M, Morellato LPC (2016) Modularity, pollination systems, and interaction turnover in plant-pollinator networks across space. Ecology 97:1298–1306

    Article  PubMed  Google Scholar 

  • Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A 170:533–543

    Article  Google Scholar 

  • Coimbra G, Araujo C, Bergamo PJ, Freitas L, Rodríguez-Gironés MA (2020) Flower conspicuousness to bees across pollination systems: a generalized test of the bee-avoidance hypothesis. Front Plant Sci 11 558684

  • Danieli-Silva A, Souza JMT, Donatti AJ, Campos RP, Vicente-Silva J, Freitas L, Varassin IG (2012) Do pollination syndromes cause modularity and predict interactions in a pollination network in tropical high-altitude grasslands? Oikos 121:35–43

    Article  Google Scholar 

  • Eisen KE, Geber MA (2018) Ecological sorting and character displacement contribute to the structure of communities of Clarkia species. J Evol Biol 31:1440–1458

    Article  PubMed  Google Scholar 

  • Endress PK (1994) Floral structure and evolution of primitive angiosperms: recent advances. Plant Syst Evol 192:79–97

    Article  Google Scholar 

  • E-Votjkó A, Bello F, Walter D, Ingolf K, Götzenberger L, (2020) The neglected importance of floral traits in trait-based plant community assembly. J Veget Sci 31:529–539

    Article  Google Scholar 

  • Fang Q, Huang S-Q (2013) A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology 94:1176–1185

    Article  PubMed  Google Scholar 

  • Flora do Brasil 2020 under construction. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br. Accessed 02 Nov 2020

  • Freitas L, Sazima M (2003) Daily blooming pattern and pollination by syrphids in Sisyrinchium vaginatum (Iridaceae) in southeastern Brazil. J Torr Bot Soc 130:55–61

    Article  Google Scholar 

  • Freitas L, Sazima M (2006) Pollination biology in a tropical high-altitude grassland in Brazil: interactions at the community level. Ann Miss Bot Gard 93:465–516

    Article  Google Scholar 

  • Freitas L, Galetto L, Sazima M (2006) Pollination by hummingbirds and bees in eight syntopic species and a putative hybrid of Ericaceae in southeastern Brazil. Plant Syst Evol 258:49–61

    Article  Google Scholar 

  • Garibaldi LA, Carvalheiro LG, Vaissière BE et al (2016) Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science 351:388–391

    Article  PubMed  CAS  Google Scholar 

  • Grossenbacher DL, Brandvain Y, Auld JR et al (2017) Self-compatibility is over-represented on islands. New Phytol 215:469–478

    Article  PubMed  Google Scholar 

  • Herrera G, Zagal JC, Diaz M et al (2008) Spectral sensitivities of photoreceptors and their role in colour discrimination in the green-backed firecrown hummingbird (Sephanoides sephaniodes). J Comp Physiol A 194:785–794

    Article  CAS  Google Scholar 

  • Herrera CM (2020) Flower traits, habitat, and phylogeny as predictors of pollinator service: a plant community perspective. Ecol Monogr 90:e01402

  • Hoiss B, Krauss J, Potts SG, Roberts S, Steffan-Dewenter I (2012) Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proc R Soc B 279:4447–4456

    Article  PubMed  PubMed Central  Google Scholar 

  • Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86

    Article  CAS  Google Scholar 

  • Inouye DW, Larson BMH, Ssymank A, Kevan PG (2015) Flies and flowers III: ecology of foraging and pollination. J Pollinat Ecology 16:115–133

    Article  Google Scholar 

  • Johnson AL, Ashman T-L (2019) Consequences of invasion for pollen transfer and pollination revealed in a tropical island ecosystem. New Phytol 221:142–154

    Article  PubMed  Google Scholar 

  • Karoly K (1992) Pollinator limitation in the facultatively autogamous annual, Lupinus nanus (Leguminosae). Am J Bot 79:49–56

    Article  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Ann Rev Ecol Evol Syst 29:83–112

    Article  Google Scholar 

  • Kevan PG (1972) Floral colors in the high arctic with reference to insect-flower relations and pollination. Canad J Bot 50:2289–2316

    Article  Google Scholar 

  • Lanuza JB, Bartomeus I, Godoy O (2018) Opposing effects of floral visitors and soil conditions on the determinants of competitive outcomes maintain species diversity in heterogeneous landscapes. Ecol Lett 21:865–874

    Article  PubMed  Google Scholar 

  • Lázaro A, Hegland SJ, Totland Ø (2008) The relationships between floral traits and specificity of pollination systems in three Scandinavian plant communities. Oecologia 157:249–257

    Article  PubMed  Google Scholar 

  • Leal RLB, Moreira MM, Pinto AR, Ferreira JO, Rodríguez-Gironés M, Freitas L (2020) Temporal changes in the most effective pollinator of a bromeliad pollinated by bees and hummingbirds. PeerJ 8:e8836

  • Lunau K, Papiorek S, Eltz T, Sazima M (2011) Avoidance of achromatic colours by bees provides a private niche for hummingbirds. J Exp Biol 214:1607–1612

    Article  PubMed  Google Scholar 

  • Lunau K (2014) Visual ecology of flies with particular reference to colour vision and colour preferences. J Comp Physiol A 200:497–512

    Article  Google Scholar 

  • Machado CG, Coelho AG, Santana CS, Rodrigues M (2007) Beija-flores e seus recursos florais em uma área de campo rupestre da Chapada Diamantina, Bahia. Rev Bras Ornitol 15:267–279

    Google Scholar 

  • Martinelli G, Moraes MA (2013) Livro vermelho da Flora do Brasil. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro

    Google Scholar 

  • Menzel R, Ventura DF, Werner A, Joaquim LCM, Backhaus W (1989) Spectral sensitivity of single photoreceptors and color vision in the stingless bee, Melipona quadrifasciata. J Comp Physiol A 166:151–164

    Article  Google Scholar 

  • Monteiro BL, Camargo MGG, Loiola PP, Carstensen DW, Gustafsson S, Morellato LPC (2021) Pollination in the campo rupestre: a test of hypothesis for an ancient tropical mountain vegetation. Biol J Linn Soc 133:512–530

    Article  Google Scholar 

  • Morales CL, Aizen MA (2002) Does invasion of exotic plants promote invasion of exotic flower visitors? A case study from the temperate forests of the southern Andes. Biol Invas 4:87–100

    Article  Google Scholar 

  • Moreira MM, Freitas L (2020) Review of the pollination system by small diverse insects. Neotrop Entomol 49:472–481

    Article  PubMed  CAS  Google Scholar 

  • Moreira MM, Carrijo TT, Alves-Araújo A et al (2020) Using online databases to produce comprehensive accounts of the vascular plants from the Brazilian protected areas: the Parque Nacional do Itatiaia as a case study. Biodiv Data J 8:e50837

  • Morellato LPC, Alberti LF, Hudson IL (2010) Applications of circular statistics in plant phenology: a case studies approach. In: Hudson I, Keatley M (eds) Phenological research, 1st edn. Springer, Dodrecht, pp 339–359

    Chapter  Google Scholar 

  • Moritz RFA, Härtel S, Neumann P (2005) Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Écoscience 12:289–301

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Papiorek S, Junker RR, Alves-dos-Santos I et al (2016) Bees, birds and yellow flowers: pollinator-dependent convergent evolution of UV patterns. Plant Biol 18:46–55

    Article  PubMed  CAS  Google Scholar 

  • Rader R, Bartomeus I, Garibaldi LA et al (2016) Non-bee insects are important contributors to global crop pollination. PNAS 113:146–151

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro KT, Medina BMO, Scarano FR (2007) Composição de espécies e relações biogeográficas da flora sobre afloramentos rochosos do Planalto do Itatiaia, SE do Brasil. Braz J Bot 30:623–639

    Article  Google Scholar 

  • Ribeiro KT, Freitas L (2010) Impactos potenciais das alterações no Código Florestal sobre a vegetação de campos rupestres e campos de altitude. Biota Neotrop 10:239–246

    Article  Google Scholar 

  • Safford HDF (1999a) Brazilian Páramos II: Macro- and mesoclimate of the campos de altitude and affinities with high mountain climates of the tropical Andes and Costa Rica. J Biogeog 26:713–737

    Article  Google Scholar 

  • Safford HDF (1999b) Brazilian Páramos I: an introduction to the physical environment and vegetation of the campos de altitude. J Biogeog 26:693–712

    Article  Google Scholar 

  • Safford HDF (2007) Brazilian Páramos IV: phytogeography of the campos de altitude. J Biogeog 34:1701–1722

    Article  Google Scholar 

  • Santamaría S, Galeano J, Pastor JM, Méndez M (2018) Robustiness of alpine pollination networks: effects of network structure and consequences for endemic plants. Arct Antarct Alp Res 46:568–580

    Article  Google Scholar 

  • Sazima I, Buzato S, Sazima M (1996) An assemblage of hummingbird-pollinated flowers in a montane forest in Southeastern Brazil. Plant Biol 109:149–160

    Google Scholar 

  • Schiestl FP, Johnson SD (2013) Pollinator-mediated evolution of floral signals. Trends Ecol Evol 28:307–315

    Article  PubMed  Google Scholar 

  • Staggemeier VG, Camargo MGG, Diniz-Filho JAF, Freckleton R, Jardim L, Morellato LPC (2020) The circular nature of recurrent life cycle events: a test comparing tropical and temperate phenology. J Ecol 108:393–404

    Article  Google Scholar 

  • Streher NS, Bergamo PJ, Ashman T-L, Wolowski M, Sazima M (2020) Effect of heterospecific pollen deposition on pollen tube growth depends on the phylogenetic relatedness between donor and recipient. AoB Plants 12:plaa016

  • Traveset A, Navarro L (2018) Plant reproductive ecology and evolution in the Mediterranean islands: state of the art. Plant Biol 20:63–77

    Article  PubMed  Google Scholar 

  • Totland Ø (1993) Pollination in alpine Norway: flowering phenology, insect visitors, and visitation rates in two plant communities. Canad J Bot 71:1072–1079

    Article  Google Scholar 

  • Troje N (1993) Spectral categories in the learning behavior of blowflies. Z Naturforsch C J Biosci 48:96–104

    Article  Google Scholar 

  • Vizentin-Bugoni J, Maruyama PK, Sazima M (2014) Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proc R Soc B 281:20132397

    Article  PubMed  PubMed Central  Google Scholar 

  • Vorobyev M, Osorio D, Bennett TD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633

    Article  PubMed  CAS  Google Scholar 

  • Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060

    Article  Google Scholar 

  • Wolowski M, Saad CF, Ashman T-L, Freitas L (2013) Predominance of self-compatibility in hummingbird-pollinated plants in the Neotropics. Sci Nat 100:69–79

    Article  CAS  Google Scholar 

  • Wolowski M, Nunes CEP, Amorim FW et al (2016) Interções planta-polinizador em vegetação de altitude na Mata Atlântica. Oecol Austr 20:7–23

    Article  Google Scholar 

  • Wolowski M, Carvalheiro LG, Freitas L (2017) Influence of plant-pollinator interactions on the assembly of plant and hummingbird communities. J Ecol 105:332–344

    Article  Google Scholar 

  • Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Braz J Bot 34:431–446

    Article  Google Scholar 

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Acknowledgements

We thank Suzana Costa, Nicoll Escobar, Pamela Medina, Amanda Mesquita, and Pamela Santana and for help in the field. We thank Juliana Amaral, Lucas Bacci, João Carmo, Julie Dutilh, Marcelo Egea, Camila Inácio, Leonardo Meireles, André Scatigna, João Semir, and Gustavo Shimizu for plant identification. We thank Marina Moreira for help with gathering endemism and conservation status data.

Funding

PJB was funded by FAPESP during the data collection (Process nº 2016/06434–0). MS (grant 302781/2016–1) and MW (436335/2018–2) received financial support and NSS (157687/2019–8) received scholarships from CNPq. This study was financed in part by CAPES (Finance code 001).

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PJB, NSS, and VZ collected data. PJB analyzed data. PJB, NSS, MW, and MS conceived the study. PJB wrote the first draft and all authors contributed to the last version of the manuscript.

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Correspondence to Pedro Joaquim Bergamo.

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Communicated by: Tatiana Cornelissen

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Bergamo, P.J., Streher, N.S., Zambon, V. et al. Pollination generalization and reproductive assurance by selfing in a tropical montane ecosystem. Sci Nat 108, 50 (2021). https://doi.org/10.1007/s00114-021-01764-8

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