Abstract
Many studies have evaluated and categorized the pollination systems of plants in different regions. These studies resulted in the definition of new pollination systems, such as that by small diverse insects (SDI). Although SDI systems are frequent in tropical communities, we know little about the species of plants and pollinators that compose these systems. This study synthesized knowledge of SDI systems through a systematic review of the literature, in order to characterize the composition of plants and pollinator species related to this pollination system. Most studies of SDI systems were carried out in tropical rainforest communities, and used a variety of terminologies and concepts. We found 362 plant species assigned to the SDI system, distributed in 76 families and 35 orders. These species are mainly trees and have inconspicuous greenish flowers, and most are hermaphroditic or dioecious. Few studies provided information on the composition of pollinators, which encompassed small and large insects; beetles, wasp, flies, and bees were the most frequent groups. We suggest adoption of the term “pollination system by diverse insects” instead of “small diverse insects.” We discuss conceptual aspects and questions for studies with this pollination system.
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References
Alves-dos-Santos I, Silva CI, Pinheiro M, Kleinert AMP (2016) Quando um visitante floral é um polinizador? Rodriguésia 67:295–307
Armbruster WS (2017) The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct Ecol 31:88–100
Bawa KS (1980) Evolution of dioecy in flowering plants. Annu Rev Ecol Syst 11:15–39
Bawa KS (1990) Plant pollination interaction in tropical rain forest. Annu Rev Ecol Syst 21:399–422
Bawa KS, Bullock SH, Perry DR, Coville RE, Grayum MH (1985b) Reproductive biology of tropical lowland rain forest trees II Pollination systems. Am J Bot 72(3):346–356
Bawa KS, Opler PA (1975) Dioecism in tropical forest trees. Evolution 29:167–179
Bawa KS, Perry DR, Beach JH (1985a) Reproductive biology of tropical lowland rain forest trees. I. Sexual systems and incompatibility mechanisms. Am J Bot 72:331–345
Côté IM, Curtis PS, Rothstein HR, Stewart GB (2013) Gathering data: searching literature and selection criteria. In: Koricheva J, Gurevitch J, Mengersen K (eds) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton, p 37
Endress PK (1994) Diversity and Evolution Biology of Tropical Flowers. Cambridge University Press, Cambridge, UK, p 511
Endress PK, Davis CC, Matthews ML (2013) Advances in the floral structural characterization of the major subclades of Malpighiales, one of the largest orders of flowering plants. Ann Bot 111:969–985
Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon, Oxford, p 243
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403
Freitas L (2013) Concepts of pollinator performance: is a simple approach necessary to achieve a standardized terminology? Rev Bras Bot 36:3–8
Freitas L, Sazima M (2006) Pollination biology in a tropical high-altitude grassland in Brazil: interactions at the community level. Ann Mo Bot Gard 93:465–516
Gómez JM, Muñoz-Pajares AJ, Abdelaziz M, Lorite J, Perfectti F (2014a) Evolution of pollination niches and floral divergence in the generalist plant Erysimum mediohispanicum. Ann Bot 113:237–249
Gómez JM, Perfectti F, Abdelaziz M, Lorite J, Muñoz-Pajares AJ, Valverde J (2014b) Evolution of pollination niches in a generalist plant clade. New Phytol 205:440–453
Kevan PG (1972) Insect pollination of high arctic flowers. J Ecol 60:831–847
Lindsey AH, Bell CR (1985) Reproductive biology of Apiaceae. II. Cryptic specialization and floral evolution in Thaspium and Zizia. Am J Bot 72:231–247
Machado IC, Loiola MI (2000) Fly pollination and pollinator sharing in two synchronopatric species: Cordia multispicata (Boraginaceae) and Borreria alata (Rubiaceae). Rodriguésia 23:305–311
Machado IC, Lopes AV (2004) Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Ann Bot 94:365–376
Maddison WP, Maddison DR (2018) Mesquite: a modular system for evolutionary analysis. Version 3.6. http://www.mesquiteproject.org
Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, Sakai S, Harrison RD, Itioka T, Hamid AA, Inoue T (1998) Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am J Bot 85:1477–1501
Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56:717–728
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326
Pombal ECP, Morellato LPC (2000) Differentiation of floral color and odor in two fly pollinated species of Metrodorea (Rutaceae) from Brazil. Plant Syst Evol 221:141–156
Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Inc., Portland, p 479
Rech AR, Dalsgaard B, Sandel B, Sonne J, Svenning JC, Holmes N, Ollerton J (2016) The macroecology of animal versus wind pollination: ecological factors are more important than historical climate stability. Plant Ecol Divers 9:253–262
Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606
Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecol Lett 17:388–400
Sigut M, Sigutová H, Pyszko P, Dolnýl A, Drozdová M, Drozd P (2017) Avoiding erroneous citation in ecological research: read before apply. Oikos 126:1523–1532
Teixeira MC, Thomaz SM, Michelan TS, Mormul RP, Meurer T, Fasolli JVB, Silveira MJ (2013) Incorrect citations give unfair credit to review authors in ecology journals. PLoS One 8(12):e81871. https://doi.org/10.1371/journal.pone.0081871
THE ANGIOSPERM PHYLOGENY GROUP (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20
Vamosi JC, Otto SP, Barret SCH (2003) Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. J Evol Biol 16:1006–1018
Wardhaugh CW (2015) How many species of arthropods visit flowers? Arthropod Plant Interact 9:547–565
Waser NM (2006) Specialization and generalization in plant pollinator interactions: a historical perspective. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 3–17
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060
Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton, p 778
Yumoto T, Momose K, Nagamasu H (2000) A new pollination syndrome – squirrel pollination in a tropical rainforest in Lambir Hills National Park, Sarawak, Malaysia. Tropics 9:147–151
Zych M (2007) On flower visitors and true pollinators: the case of Heracleum sphondylium L. (Apiaceae). Plant Syst Evol 263:159–179
Acknowledgments
We thank the Coordination for the Improvement of Higher Education Personnel (CAPES) for awarding a PhD scholarship to MMM. We also thank the National Council of Technological and Scientific Development (CNPq) and the Foundation for Support of Research in the State of Rio de Janeiro (FAPERJ) for PQ and CNE scholarships to LF and for funding the project (PVE-CNPQ 400789/2014-0), and Igor Musauer Kessous and Alessandra Ribeiro Pinto for helping to draw the tree in Mesquite.
Author Contribution Statement
Both authors contributed to the study conception and design. MMM performed the literature search and data analysis. Both authors drafted and critically revised the work. Both authors have read and approved the final manuscript.
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Table S1
List of 282 articles obtained through this systematic review, including: author names, article title, publication year, journal name, indication that the study was used in the review (yes = we selected the study, no = we did not select the study), and the type of search (Search 1 = key-words; Search 2 = cited Bawa et al 1985a). (XLSX 44 kb)
Table S2
List of 47 articles that satisfied the selection criteria adopted in this review. (XLSX 18 kb)
Table S3
List of 362 species of plants classified in the SDI pollination system and list of the five studies that evaluated the floral visitors. (XLSX 57 kb)
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Moreira, M.M., Freitas, L. Review of the Pollination System by Small Diverse Insects. Neotrop Entomol 49, 472–481 (2020). https://doi.org/10.1007/s13744-020-00779-6
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DOI: https://doi.org/10.1007/s13744-020-00779-6