Abstract
The species of the family Malpighiaceae are mainly diversified in the Neotropical Region as a consequence of a specialized pollination system. Due to the production of floral oils as a reward to pollinators, and their interaction with Centris, Epicharis (Centridini) and Monoeca (Tapinotaspidini) oil-collecting bee species in most neotropical species, many studies were focused on this interesting mutualistic interaction. However, a few have approached the reproductive biology of these species. The aim of this study was to gather all the existing information to date on the reproductive biology, megagametophyte development and apomixis of the Malpighiaceae species and analyze it together. We found 39 studies on the reproductive biology of 66 species, of which 47% are self-compatible, 33.3% self-incompatible, 18.2% have a mixed system, showing variable behavior among populations and 1.5% agamospermic species. We also found studies/reports on apomixis for eight species (three genera), polyembryony for six species (five genera) and on the development of megagametophyte for 14 species. We showed that our knowledge about the reproductive biology of Malpighiaceae species is scarce and fragmented, obtaining data for only 70–80 species (6–7% out of the total), most of which belonged to one population and/or few analyzed individuals. Further studies about the integral reproductive biology of these species that focus on the analysis of inter-population variations of the reproductive characters should be carried out to better understand how certain reproductive traits of Malpighiaceae species might have evolved and to provide valuable information on the mechanisms of population differentiation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguiar CML (2003) Flower visits of Centris bees (Hymenoptera: Apidae) in an area of caatinga (Bahia, Brazil). Stud Neotrop Fauna Environm 38:41–45. https://doi.org/10.1076/snfe.38.1.41.14029
Aliscioni SS, Gotelli MM, Torretta JP (2018) Structure of the stigma and style of Callaeum psilophyllum (Malpighiaceae) and its relation with potential pollinators. Protoplasma 255:1433–1442. https://doi.org/10.1007/s00709-018-1245-x
Aliscioni SS, Gotelli M, Torretta JP (2019) Gynoecium with carpel dimorphism in Tricomaria usillo, comparison with other genera of the Carolus clade (Malpighiaceae). Protoplasma 256:1133–1144. https://doi.org/10.1007/s00709-019-01373-3
Aliscioni SS, Gomiz NE, Agüero JI, Torretta JP (2022) Structural diversity of elaiophores in Argentine species of Malpighiaceae: morphology, anatomy, and interaction with pollinators. Protoplasma 259:789–807. https://doi.org/10.1007/s00709-021-01699-x
Amorim ME, De Marco P (2011) Polinização de Byrsonima cocolobifolia: isolamento de curta distância e as possíveis causas para baixa produção de frutos. Brazil J Biol 71:709–717. https://doi.org/10.1590/S1519-69842011000400016
Anderson CE (1982a) A monograph of the genus Peixotoa (Malpichiaceae). Contr Univ Michigan Herb 15:1–92
Anderson WR (1979) Floral conservatism in Neotropical Malpighiaceae. Biotropica 11:219–223
Anderson WR (1980) Crypt self-fertilization in the Malpighiaceae. Science 207:892–893. https://doi.org/10.1126/science.207.4433.892
Anderson WR (1982b) Malpighiaceae. Mem New York Bot Gard 32:21–305
Anderson WR (1990) Notes on neotropical Malpighiaceae-III. Contr Univ Michigan Herb 17:39–54
Anderson WR, Anderson C, Davis CC (2006) Malpighiaceae. Available at: http://herbarium.lsa.umich.edu/malpigh/index.html. Accessed 1 Jul 2022
Arévalo-Rodrigues G, de Almeida RF, Cardoso-Gustavson P (2020) Anatomy of staminal glands in the Stigmaphylloid clade sheds light into new morphotypes of elaiophores and osmophores in Malpighiaceae. Pl Syst Evol 306:1–9. https://doi.org/10.1007/s00606-020-01680-w
Asker SE, Jerling L (1992) Apomixis in plants. CRC Press, Boca Ratón
Assunção MA, Torezan-Silingardi HM, Del-Claro K (2014) Do ant visitors to extrafloral nectaries of plants repel pollinators and cause an indirect cost of mutualism? Flora 209:244–249. https://doi.org/10.1016/j.flora.2014.03.003
Avalos AA, Marrero HJ, Ferrucci MS, Torretta JP (2021) Stigmas arrangement, reproductive system, and maternal reproductive success in two species of Stigmaphyllon (Malpighiaceae): Does pollinator size matter? Pl Ecol 222:1263–1279. https://doi.org/10.1007/s11258-021-01176-8
Avalos AA, Torretta JP, Lattar EC, Ferrucci MS (2020) Structure and development of anthers and connective glands in two species of Stigmaphyllon (Malpighiaceae): are heteromorphic anthers related to division of labour? Protoplasma 257:1165–1181. https://doi.org/10.1007/s00709-020-01497-x
Báez-Lizarazo MR, Eggers L, Aguiar AJ, Chauveau O (2021) Contrasting patterns of plant–pollinator interactions among four oil-secreting species of Iridaceae from Pampean and Cerrado provinces (Brazil). Bot J Linn Soc 196:256–277. https://doi.org/10.1093/botlinnean/boaa104
Balestra CL, Fachardo ALS, Soares MP, Reys P, Silva FG (2014) Reproductive biology and pollination of two species of Byrsonima Kunth in a Cerrado fragment in Central Brazil. Biociências 20:71–81
Barônio GJ, Haleem MA, Marsaioli AJ, Torezan-Silingardi HM (2017) Characterization of Malpighiaceae flower-visitor interactions in a Brazilian savannah: how do floral resources and visitor abundance change over time. Flora 234:126–134. https://doi.org/10.1016/j.flora.2017.07.015
Barros MAG (1992) Fenologia da floração, estratégias reprodutivas e polinização de espécies simpátricas do gênero Byrsonima Rich. (Malpighiaceae). Rev Brasil Biol 52:343–353
Batista JA, Pacheco MFJ, Santos ML (2005) Biologia reprodutiva de três espécies de Byrsonima Rich. ex Kunth (Malpighiaceae) em um cerrado sensu stricto no campus da Universidade Estadual de Goiás, Anápolis, Goiás. Brasil Rev Biol Trop 2:109–122
Bawa KS (1974) Breeding systems of tree species of a lowland tropical community. Evolution 28:85–92
Benezar RM, Pessoni LA (2006) Floral biology and the reproductive system of Byrsonima coccolobifolia (Kunth) in an Amazonian savanna. Acta Amazon 36:159–168. https://doi.org/10.1590/S0044-59672006000200005
Bezerra ELS (2004) Polinização e fenologia reprodutiva de Byrsonima gardneriana Juss. e Stigmaphyllon paralias Juss. (Malpighiaceae) em área de Caatinga, Nordeste do Brasil. MSc Thesis, Universidade Federal de Pernambuco, Recife
Bezerra ELS (2008) Guilda de flores de óleo do Parque Nacional do Catimbau: fenología, polinizacao e sistema reprodutivo. PhD Thesis, Universidade Federal de Pernambuco, Recife
Bezerra ELS, Lopes AV, Machado IC (2009) Reproductive biology of Byrsonima gardnerana A. Juss. (Malpighiaceae) and interactions with Centris bees (Centridini) in northeastern Brazil. Brazil J Bot 32:95–108. https://doi.org/10.1590/S0100-84042009000100010
Bonifácio SKV, de Almeida RF, Amorim AMA, Oliveira DMT (2021) Floral synorganization in acmantheroid clade suggests hypotheses to explain elaiophore suppression in Malpighiaceae. Flora 281:151870. https://doi.org/10.1016/j.flora.2021.151870
Buchmann SL (1987) The ecology of oil flowers and their bees. Annual Rev Ecol Evol Syst 18:343–369. https://doi.org/10.1146/annurev.es.18.110187.002015
Cappellari SC (2011) Evolutionary ecology of Malpighiaceae pollination at the species and community levels. PhD Thesis, University of Texas at Austin, Austin
Cappellari SC, Haleem MA, Tidon AJ, Simpson BB (2011) Pterandra pyroidea: a case of pollination shift within neotropical Malpighiaceae. Ann Bot (Oxford) 107:1323–1334. https://doi.org/10.1093/aob/mcr084
Carman JG (1995) Gametophitic angiosperm apomicts and the occurrence of polyspory and polyembryony among their relatives. Apomixis Newslett 8:220–222
Carman JG (1997) Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol J Linn Soc 61:51–94. https://doi.org/10.1111/j.1095-8312.1997.tb01778.x
Carneiro LT, Aguiar AJC, Martins CF, Machado IC, Alves-dos-Santos I (2015) Krameria tomentosa oil flowers and their pollinators: bees specialized on trichome elaiophores exploit its epithelial oil glands. Flora 215:1–8. https://doi.org/10.1016/j.flora.2015.06.002
Cocucci AA (1991) Pollination biology of Nierembergia (Solanaceae). Pl Syst Evol 174:17–35. https://doi.org/10.1007/BF00937691
Cocucci AA, Sérsic A, Roig-Alsina AH (2000) Oil-collecting structures in Tapinotaspidini: their diversity, function and probable origin (Hymenoptera: Apidae). Mitt Münch Entomol Ges 90:51–74
Cocucci AA, Vogel S (2001) Oil-producing flowers of Sisyrinchium species (Iridaceae) and their pollinators in southern South America. Flora 196:26–46. https://doi.org/10.1016/S0367-2530(17)30010-5
Cortini C (1958) Sviluppo del gametofito femminile in Malpighia fucata Ker-Gawl. (Malpighiaceae). Caryologia 11:42–56. https://doi.org/10.1080/00087114.1958.10797028
Cosacov A, Nattero J, Cocucci AA (2008) Variation of pollinator assemblages and pollen limitation in a locally specialized system: the oil-producing Nierembergia linariifolia (Solanaceae). Ann Bot (Oxford) 102:723–734. https://doi.org/10.1093/aob/mcn154
Costa CBN, Costa JA, Ramalho M (2006) Biologia reprodutiva de espécies simpátricas de Malpighiaceae em dunas costeiras da Bahia, Brasil. Rev Brasil Bot 29:103–114. https://doi.org/10.1590/S0100-84042006000100010
Davis CC, Anderson WR (2010) A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. Amer J Bot 97:2031–2048. https://doi.org/10.3732/ajb.1000146
Davis CC, Schaefer H, Xi Z, Baum DA, Donoghue MJ, Harmone LJ (2014) Long-term morphological stasis maintained by a plant–pollinator mutualism. Proc Natl Acad Sci USA 111:5914–5919. https://doi.org/10.1073/pnas.1403157111
de Melo BT, Mota T, Schlindwein C, Antonini Y, Oliveira R (2018) Floral colour change in Byrsonima variabilis (Malpighiaceae) as a visual cue for pollen but not oil foraging by oil-collecting bees. Sci Nat 105:1–10. https://doi.org/10.1007/s00114-018-1572-y
Downing JL, Liu H (2013) Self-incompatibility in Byrsonima lucida (Malpighiaceae), a threatened pine rockland specialist. Castanea 78:95–102. https://doi.org/10.2179/12-031
Dunley BS, Freitas L, Galetto L (2009) Reproduction of Byrsonima sericea (Malpighiaceae) in Restinga fragmented habitats in Southeastern Brazil. Biotropica 41:692–699. https://doi.org/10.1111/j.1744-7429.2009.00524.x
Feinsinger P (1987) Effects of plant species on each other’s pollination: is community structure influenced? Trends Ecol Evol 2:123–126. https://doi.org/10.1016/0169-5347(87)90052-8
Freitas BM, Alves JE, Brandão GF, Araújo ZB (1999) Pollination requirements of West Indian cherry (Malpighia emarginata) and its putative pollinators, Centris bees, in NE Brazil. J Agric Res 133:303–311. https://doi.org/10.1017/S0021859699006930
Giraldo-Cañas D (2021) Malpighiaceae de Colombia: Patrones de distribución, riqueza, endemismo y diversidad filogenética. Darwiniana 9:39–54. https://doi.org/10.1452/darwiniana.2021.91.923
Gomiz NE, Torretta JP, Aliscioni SS (2014) Zygostates alleniana (Orchidaceae: Epidendroideae: Cymbidieae: Oncidiinae): estructura floral relacionada a la polinización. Anales Jard Bot Madrid 71:1–9. https://doi.org/10.3989/ajbm.2378
Gonçalves MDPM, Piña-Rodrigues FC (2007) Sistema de reprodução de Lophanthera lactescens Juss. (Malpighiaceae) em área de introdução. Revista Ci Eletrônica Engenharia Florest 6:1–14
Gotelli MM, Aliscioni SS, Kuo PT, Torretta JP (2022) Are the floral morphology and anatomy of Galphimia australis, an atypical neotropical Malpighiaceae, associated to a new pollination syndrome? Protoplasma 260:1047–1062. https://doi.org/10.1007/s00709-022-01829-z
Hanna WW, Bashaw EC (1987) Apomixis: its identification and use in plant breeding. Crop Sci 27:1136–1139. https://doi.org/10.2135/cropsci1987.0011183X002700060010x
Hojsgaard D, Klatt S, Baier R, Carman JG, Hörandl E (2014) Taxonomy and biogeography of apomixis in angiosperms and associated biodiversity characteristics. Crit Rev Pl Sci 33:414–427. https://doi.org/10.1080/07352689.2014.898488
Hughes FM (2021) Reciprocal intercompatibility between Byrsonima Rich. ex Kunth species (Malpighiaceae), in an urban ecotonal fragment of semi-deciduous seasonal forest and Cerrado. Anales Biol 43:211–221. https://doi.org/10.6018/analesbio.43.20
IPNI (2022) International Plant Names Index. The Royal Botanic Gardens, Kew, Harvard University Herbaria & Libraries and Australian National Botanic Gardens. Available at: http://www.ipni.org. Accessed 1 Jul 2022
Jasmitha BG, Honnabyraiah MK (2021) West Indian cherry: nature’s vitamin-C capsule. AgriCos e-Newslett 2:5–8
Jaimes I, Ramirez N (1999) Breeding systems in a secondary deciduous forest in Venezuela: the importance of life form, habitat, and pollination specificity. Pl Syst Evol 215:23–36. https://doi.org/10.1007/BF00984645
Johri BM, Ambegaokar KB, Srivastava PS (1992) Comparative embryology of angiosperms. Springer, Heidelberg
Jones NT, Husband BC, MacDougall AS (2013) Reproductive system of a mixed-mating plant responds to climate perturbation by increased selfing. Proc Roy Soc B 280:20131336. https://doi.org/10.1098/rspb.2013.1336
Lombello RA, Forni-Martins ER (2003) Malpighiaceae: correlations between habit, fruit type and basic chromosome number. Acta Bot Brasil 17:171–178
Lorenzo E (1981) Sobre la inflorescencia, morfología floral y embriología de Janusia guaranitica (Malpighiaceae). Kurtziana 14:101–124
Machado IC, Vogel S, Lopes AV (2002) Pollination of Angelonia cornigera Hook. (Scrophulariaceae) by long-legged, oil-collecting bees in NE Brazil. Pl Biol 4:352–359. https://doi.org/10.1055/s-2002-32325
Magalhães CB, Freitas BM (2013) Introducing nests of the oil-collecting bee Centris analis (Hymenoptera: Apidae: Centridini) for pollination of acerola (Malpighia emarginata) increases yield. Apidologie 44:234–239. https://doi.org/10.1007/s13592-012-0175-4
Magalhaes LMF, De Oliveira D, Ohashi OS (1997) Pollination and pollen vectors in Acerola, Malphighia punicifolia L. Acta Hortic 437:419–424. https://doi.org/10.17660/ActaHortic.1997.437.55
Maheshwari P, Johri BM (1950) Development of the embryo sac, embryo and endosperm in Helixanthera ligustrina (Wall.) Dans. Nature 165:978–979. https://doi.org/10.1038/165978c0
Mamede MCH (1993) Estudo comparativo de flores casmógamas, cleistógamas e de frutos de Camarea affinis St.-Hil. (Malpighiaceae). Acta Bot Brasil 7:21–31. https://doi.org/10.1590/S0102-33061993000100002
Mandujano MC, Carrillo-Angeles I, Martínez-Peralta C, Golubov J (2010) Reproductive biology of cactaceae. In: Ramawat K (ed) Desert plants. Springer, Berlin, pp 197–230. https://doi.org/10.1007/978-3-642-02550-1_10
Martins AC, Melo GAR, Renner SS (2015) Gain and loss of specialization in two oil bee lineages, Centris and Epicharis (Apidae). Evolution 69:1835–1844. https://doi.org/10.1111/evo.12689
Martins AC, Melo GAR (2016) The New World oil-collecting bees Centris and Epicharis (Hymenoptera, Apidae): molecular phylogeny and biogeographic history. Zool Scr 45:22–33. https://doi.org/10.1111/zsc.12133
Matallana G, Marcarini L, de Menezes LFT (2016) Crescimento de tubos polínicos e local de incompatibilidade em Byrsonima sericea DC (Malpighiaceae). Bol Mus Biol Mello-Leitão 38:59–71
Mendes FN, Rêgo MMC, Albuquerque PMCD (2011) Fenologia e biología municipio va de duas espécies de Byrsonima Rich. (Malpighiaceae) em área de Cerrado no Nordeste do Brasil. Biota Neotrop 11:103–115
Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins, Baltimore
Murúa M, Espíndola A (2015) Pollination syndromes in a specialised plant pollinator interaction: Does floral morphology predict pollinators in Calceolaria? Pl Biol 17:551–557. https://doi.org/10.1111/plb.12225
Neff JL, Simpson BB (1981) Oil-collecting structures in the Anthophoridae (Hymenoptera): morphology, function, and use in systematics. J Kans Entomol Soc 54:95–123
Oliveira GA, Aguiar CML, Silva M, Gimenes M (2013) Centris aenea (Hymenoptera, Apidae): a ground-nesting bee with high pollination efficiency in Malpighia emarginata DC (Malpighiaceae). Sociobiology 60:317–322. https://doi.org/10.13102/sociobiology.v60i3.317-322
Oliveira LC, Nunes CEP, Brito VLG, Caetano APS (2022) Floral oil production in a family dominated by pollen flowers: The case of Macairea radula (Melastomataceae). Flora 288:152008. https://doi.org/10.1016/j.flora.2022.152008
Oliveira MB, Polido CA, Costa LC, Fava WS (2007) Sistema reprodutivo e polinização de Byrsonima intermedia A. Juss. (Malpighiaceae) em Mato Grosso do Sul, Brasil. Rev Brasil Biosci 5:756–758
Pandey AK (1997) Introduction to the embryology of Angiosperms. CBS, New Delhi
Peixoto SK, de Almeida DS, Capuzzo JP, da Silva Elias MA, da Silva MM, de Morais RJ, Ribeiro MN (2011) Sistema de polinização e reprodução do Muricizeiro Byrsonima crassa (Malpighiaceae). Revista Eletrônica Interdiscipl Univar 6:17–21
Pereira JOP, Freitas BM (2002) Estudo da biologia floral e requerimentos de polinização do muricizeiro (Byrsonima crassifolia L.). Ci Agron 33:5–12
Possobom CCF, Machado SR, Guimaraes E (2016) Reproductive system of Diplopterys pubipetala (Malpighiaceae) plants from a savanna ecosystem. Int J Pl Biol 8:7–13
POWO (2022) Plants of the World Online. The Royal Botanic Gardens, Kew. Available at: http://www.plantsoftheworldonline.org/. Accessed 1 Jul 2022
Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Harper Collins Publishers, London
Qian ZN, Meng QW, Ren MX (2016) Pollination ecotypes and herkogamy variation of Hiptage benghalensis (Malpighiaceae) with mirror-image flowers. Biodivers Sci 24:1364. https://doi.org/10.17520/biods.2016248
Raven PH (1979) A survey of reproductive biology in Onagraceae. New Zealand J Bot 17:575–593. https://doi.org/10.1080/0028825X.1979.10432572
Ren MX, Zhong YF, Song XQ (2013) Mirror-image flowers without buzz pollination in the Asian endemic Hiptage benghalensis (Malpighiaceae). Bot J Linn Soc 173:764–774. https://doi.org/10.1111/boj.12101
Renner SS, Schaefer H (2010) The evolution and loss of oil offering flowers: new insights from dated phylogenies for plants and bees. Philos Trans Roy Soc London Ser B 365:423–435. https://doi.org/10.1098/rstb.2009.0229
Ribeiro EK. (2007) Sistema de polinização e reprodução do “murici pitanga’’ (Byrsonima chrysophylla Kunth.) em uma área de restinga. MSc Thesis, Universidade Federal do Maranhão, São Luís
Richards AJ (1986) Plant breeding systems. George Allen & Unwin, London
Ritzerow H (1908) Ueber Bau und Befruchtung kleistogamer Blüten. Bot Centralbl 2:163–212. https://doi.org/10.1016/S0367-1615(17)32223-1
Robertson K, Goldberg EE, Igić B (2011) Comparative evidence for the correlated evolution of polyploidy and self-compatibility in Solanaceae. Evol Int J Org Evol 65:139–155. https://doi.org/10.1111/j.1558-5646.2010.01099.x
Rocha-Filho LC, Melo GAR (2011) Nesting biology and behavioural ecology of the solitary bee Monoeca haemorrhoidalis (Smith) and its cleptoparasite Protosiris gigas Melo (Hymenoptera: Apidae: Tapinotaspidini; Osirini). J Nat Hist 45:2815–2840. https://doi.org/10.1080/00222933.2011.616271
Roig-Alsina A (1997) A generic study of the bees of the tribe Tapinotaspidini, with notes on the evolution of their oil-collecting structures (Hymenoptera, Apidae). Mitt Münch Entomol Ges 87:3–21
Salomão AN, Allem AC (2001) Polyembryony in angiospermous trees of the Brazilian Cerrado and Caatinga vegetation. Acta Bot Brasil 15:369–378
Sazan MS, Bezerra ADM, Freitas BM (2014) Oil collecting bees and Byrsonima cydoniifolia A. Juss. (Malpighiaceae) interactions: the prevalence of long-distance cross pollination driving reproductive success. Anais Acad Brasil Ci 86:347–358. https://doi.org/10.1590/0001-3765201420130049
Sazima M, Sazima I (1989) Oil-gathering bees visit flowers of eglandular morphs of the oil-producing Malpighiaceae. Bot Acta 102:106–111. https://doi.org/10.1111/j.1438-8677.1989.tb00073.x
Sigrist MR, Sazima M (2004) Pollination and reproductive biology of twelve species of neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. Ann Bot (Oxford) 94:33–41. https://doi.org/10.1093/aob/mch108
Silva JV, Souto LS, Sebastiani R (2018) Occurrence of aborted seeds in the cleistogamous flowers of Janusia guaranitica (A. St.-Hil.) A. Juss. (Malpighiaceae). Brazil J Biol 79:358–360. https://doi.org/10.1590/1519-6984.174319
Simpson BB (1982) Krameria (Krameriaceae) flowers: orientation and elaiophore morphology. Taxon 31:517–528. https://doi.org/10.2307/1220683
Simpson BB (1989) Pollination biology and taxonomy of Dinemandra and Dinemagonum (Malpighiaceae). Syst Bot 14:408–426. https://doi.org/10.2307/2418932
Steiner KE (1985) Functional dioecism in the Malpighiaceae: the breeding system of Spachea membranacea Cuatr. Amer J Bot 72:1537–1543. https://doi.org/10.1002/j.1537-2197.1985.tb08417.x
Subba Rao AM (1937) A note on the development of the female gametophytes of some Malpighiaceae and polyembryony in Hiptage madablota. Curr Sci 6:280–282
Subba Rao AM (1940) Studies in the Malphigiaceae. I. Embryo sac development and embryogeny in the genera Hiptage, Banisteria and Stigmatophyllum. J Indian Bot Soc 18:145–156
Subba Rao AM (1941) Studies in the Malpighiaceae. II. Structure and development of the ovules and embryo sacs of Malpighia coccifera Linn. and Tristellatela australis. Biol Sci 7:393–404
Teixeira LAG, Machado IC (2000) Sistema de polinização e reprodução de Byrsonima sericea DC (Malpighiaceae). Acta Bot Brasil 14:347–357. https://doi.org/10.1590/S0102-33062000000300011
Torretta JP, Aliscioni SS, González Arzac A, Avalos AA (2017) Is the variation of floral elaiophore size in two species of Stigmaphyllon (Malpighiaceae) dependent on interaction with pollinators? Pl Ecol Divers 10:403–418. https://doi.org/10.1080/17550874.2018.1434567
Torretta JP, Aliscioni SS, Marrero HJ, Avalos AA (2022) Oil flowers of Malpighiaceae and oil-collecting bees: loyalty and robbery in a highly specialized system. Apidologie 53:1–15. https://doi.org/10.1007/s13592-022-00945-2
Torretta JP, Roig-Alsina A (2016) First report of Monoeca in Argentina, with description of two new species (Hymenoptera: Apidae). J Melittol 59:1–12. https://doi.org/10.17161/jom.v0i59.5031
Tropicos (2022) Tropicos, botanical information system at the Missouri Botanical Garden. Available at: http://www.tropicos.org. Accessed 1 Jul 2022
Vilas-Boas JC, Santos Fava W, Laroca S, Sigrist MR (2013) Two sympatric Byrsonima species (Malpighiaceae) differ in phenological and reproductive patterns. Flora 208:360–369. https://doi.org/10.1016/j.flora.2013.05.003
Vilela AA, Del Claro VTS, Torezan-Silingardi HM, Del-Claro K (2018) Climate changes affecting biotic interactions, phenology, and reproductive success in a savanna community over a 10-year period. Arthropod Pl Interact 12:215–227. https://doi.org/10.1007/s11829-017-9572-y
Vogel S (1969) Flowers offering fatty oil instead of nectar. In: Abstracts of the Papers Presented at the XI International Botanical Congress, August 24–September 2, 1969, Seattle, p 229
Vogel S (1974) Ölblumen und Ölsammelnde Bienen. Trop Subtrop Pflanzenwelt 7:285–547
Vogel S (1990) History of the Malpighiaceae in the light of pollination ecology. Mem New York Bot Gard 55:130–142
Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton. https://doi.org/10.1515/9781400838943
Yamane GM, Nakasone KY (1961) Pollination and fruit set studies of acerola Malpighia glabra L. in Hawaii. J Amer Soc Hortic Sci 78:141–148
Zambão FR (2011) Biologia da polinização de Byrsonima intermedia A. Juss. (“Murici”): floração, visitantes florais e sistema reprodutivo, em área de cerrado no distrito de itahum, municipio de Dourados-MS. MSc Thesis, Universidade Federal da Grande Dourados, Dourados
Zapata TR, Arroyo MTK (1978) Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10:221–230. https://doi.org/10.2307/2387907
Zhang W, Kramer EM, Davis CC (2016) Differential expression of CYC2 genes and the elaboration of floral morphologies in Hiptage, an Old World genus of Malpighiaceae. Int J Pl Sci 177:551–558. https://doi.org/10.1086/687225
Acknowledgements
We thank to the anonymous reviewers and Vinicius Brito by critical reading of preliminary version of manuscript and to Agustina Torretta for the English correction of this manuscript.
Funding
This work was supported for JPT (Grant UBACyT 20020170200252BA of the Universidad de Buenos Aires).
Author information
Authors and Affiliations
Contributions
JPT conceived this research; SDR and JPT wrote the paper; and all authors participated in the reading papers, analysis, discussion and revisions, and read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest or competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Vinícius L. G. Brito.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Reposi, S.D., Avalos, A.A., Gotelli, M.M. et al. Reproductive biology of Malpighiaceae: How much do we know?. Plant Syst Evol 309, 25 (2023). https://doi.org/10.1007/s00606-023-01863-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-023-01863-1