Abstract
Due to its ancient origin in the Permian and the high proportion of beetle-pollinated taxa within ancestral magnoliid lineages, it has been hypothesized that beetles were among the first floral visitors of the proto-angiosperms on Earth. Thus, beetle-pollinated flowers have become important model systems essential for the study of the origin and evolution of angiosperms. Under an evolutionary perspective, in this review we synthesize what is currently known about beetles as floral visitors in the family Magnoliaceae, one of the earliest extant groups of flowering plants. Nitidulidae and Scarabaeidae are the two most common groups of beetles reported in the literature as floral visitors to Magnoliaceae; however, the evidence indicates that most modern families of beetles including all the families with known taxa associated with Magnoliaceae had already originated when the latter first appeared by the end of the early Cretaceous. Hence, Magnoliaceae could have represented a newly opened ecological niche that beetles gradually colonized and exploited, possibly shifting from gymnosperm hosts. By feeding, mating and sheltering in their flower structures, beetles have played a major role in shaping the floral biology and morphology of Magnoliaceae. Protogyny, thermogenesis, floral odors and floral movements are traits that could have evolved in response to selection pressures imposed by beetles. Further studies should assess the possible role of anthophagous scarabs (subfamilies Cetoniinae, Melolonthinae, Dynastinae and Rutelinae) in the diversification of Magnoliaceae, since this event broadly coincides with the origin of those groups of beetles in the Eocene, some of which exhibit very close associations with several Magnoliaceae species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahrens D, Schwarzer J, Vogler AP (2014) The evolution of scarab beetles tracks the sequential rise of angiosperms and mammals. Proc R Soc Lond, Ser B: Biol Sci 281:20141470. https://doi.org/10.1098/rspb.2014.1470
Allain LK, Zavada MS, Matthews DG (1999) The reproductive biology of Magnolia grandiflora. Rhodora 101:143–162
Armstrong JE (1997) Pollination by deceit in nutmeg (Myristica insipida, Myristicaceae): floral displays and beetle activity at male and female trees. Am J Bot 84:1266–1274. https://doi.org/10.2307/2446051
Armstrong JE, Irvine AK (1990) Functions of staminodia in the beetle-pollinated flowers of Eupomatia laurina. Biotropica 22:429–431. https://doi.org/10.2307/2388563
Azuma H et al (1997) Chemical divergence in floral scents of Magnolia and allied genera (Magnoliaceae). Plant Species Biol 12:69–83. https://doi.org/10.1111/j.1442-1984.1997.tb00159.x
Azuma H, Thien LB, Kawano S (1999a) Floral scents, leaf volatiles and thermogenic flowers in Magnoliaceae. Plant Species Biol 14:121–127. https://doi.org/10.1046/j.1442-1984.1999.00015.x
Azuma H, Thien LB, Kawano S (1999b) Molecular phylogeny of Magnolia (Magnoliaceae) inferred from cpDNA sequences and evolutionary divergence of the floral scents. J Plant Res 112:291–306. https://doi.org/10.1007/pl00013885
Azuma H, García-Franco JG, Rico-Gray V, Thien LB (2001) Molecular phylogeny of the Magnoliaceae: the biogeography of tropical and temperate disjunctions. Am J Bot 88:2275–2285
Bao T, Wang B, Li J, Dilcher D (2019) Pollination of Cretaceous flowers. Proc Natl Acad Sci 116:24707–24711. https://doi.org/10.1073/pnas.1916186116
Bell CD, Soltis DE, Soltis PS (2010) The age and diversification of the angiosperms re-revisited. Am J Bot 97:1296–1303. https://doi.org/10.3732/ajb.0900346
Bernhardt P (2000) Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Plant Syst Evol 222:293–320
Bernhardt P, Thien LB (1987) Self-isolation and insect pollination in the primitive angiosperms: new evaluations of older hypotheses. Plant Syst Evol 156:159–176. https://doi.org/10.1007/bf00936071
Bertin RI, Newman CM (1993) Dichogamy in angiosperms. Bot Rev 59:112–152. https://doi.org/10.1007/BF02856676
Cai C, Escalona HE, Li L, Yin Z, Huang D, Engel MS (2018) Beetle pollination of cycads in the Mesozoic. Curr Biol 28:2806–2812. https://doi.org/10.1016/j.cub.2018.06.036
Chen Y, Chen G, Yang J, Sun W (2016) Reproductive biology of Magnolia sinica (Magnoliaecea), a threatened species with extremely small populations in Yunnan, China. Plant Diversity 38:253–258. https://doi.org/10.1016/j.pld.2016.09.003
Cheng A-X, Lou Y-G, Mao Y-B, Lu S, Wang L-J, Chen X-Y (2007) Plant terpenoids: biosynthesis and ecological functions. J Integr Plant Biol 49:179–186. https://doi.org/10.1111/j.1744-7909.2007.00395.x
Crepet WL, Friis EM (1987) The evolution of insect pollination in angiosperms. In: Friis EM, Chaloner WG, Crane PR (eds) The origins of angiosperms and their biological consequences. Cambridge University Press, England, pp 181–201
Diels L (1916) Kaferblumen bei den Ranales und ihre bedeutung fur die phylogenese der angiospermen. Berichte der Deutschen Botanischen Gesellschaft:758–774
Dieringer G, Delgado L (1994) Notes on the biology of Cyclocephala jalapensis (Coleoptera: Scarabaeidae): an endemic of eastern Mexico. Southwest Entomol 19:309–311
Dieringer G, Espinosa JE (1994) Reproductive ecology of Magnolia schiedeana (Magnoliaceae), a threatened cloud forest tree species in Veracruz, Mexico. Bull Torrey Bot Club 121:154–159
Dieringer G, Castillo PR, Lara M, Cabrera L, Loya L (1998) Endothermy and floral utilization of Cyclocephala caelestis (Coleoptera: Scarabaeoidea; Melolonthidae): a cloud forest endemic beetle. Acta Zoológica Mexicana (nueva serie):145–153
Dieringer G, Cabrera RL, Lara M, Loya L, Reyes-Castillo P (1999) Beetle pollination and floral thermogenicity in Magnolia tamaulipana (Magnoliaceae). Int J Plant Sci 160:64–71. https://doi.org/10.1086/314099
Dilcher DL, Crane PR (1984) Archaeanthus: an early angiosperm from the Cenomanian of the western interior of North America. Ann Mo Bot Gard 71:351–383. https://doi.org/10.2307/2399030
Doyle JA, Endress PK (2010) Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. J Syst Evol 48:1–35. https://doi.org/10.1111/j.1759-6831.2009.00058.x
Endress PK (1984) The role of inner staminodes in the floral display of some relic Magnoliales. Plant Syst Evol 146:269–282. https://doi.org/10.1007/BF00989551
Endress PK (1987) The early evolution of the angiosperm flower. Trends Ecol Evol 2:300–304. https://doi.org/10.1016/0169-5347(87)90082-6
Endress PK (1990) Evolution of reproductive structures and functions in primitive angiosperms (Magnoliidae). Memoires New York Botanical Garden 55:5–34
Endress PK (2010) The evolution of floral biology in basal angiosperms. Philos Trans R Soc Lond B Biol Sci 365:411–421. https://doi.org/10.1098/rstb.2009.0228
Erichson WF (1847) Naturgeschichte der Insecten Deutschlands. Erste Abtheilung. Coleoptera. vol 3 Lieferung 4. Nicolaischen Buchhandlung, Berlin
Erwin TL (1982) Tropical forests: their richness in Coleoptera and other arthropod species. Coleopt Bull 36:74–75
Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon Press, New York
Farrell BD (1998) “Inordinate Fondness” explained: why are there so many beetles? Science 281:555–559. https://doi.org/10.1126/science.281.5376.555
Figlar RB, Nooteboom HP (2004) Notes on Magnoliaceae IV. Blumea Biodiversity, Evol Biogeogr Plants 49:87–100. https://doi.org/10.3767/000651904x486214
Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci USA 106:18054–18061. https://doi.org/10.1073/pnas.0904106106
Gottsberger G (1974) The structure and function of the primitive angiosperm flower—a discussion. Acta Bot Neerl 23:461–471. https://doi.org/10.1111/j.1438-8677.1974.tb00962.x
Gottsberger G (1989) Beetle pollination and flowering rhythm of Annona spp. (Annonaceae) in Brazil. Plant Syst Evol 167:165–187. https://doi.org/10.2307/23673946
Gottsberger G (1999) Pollination and evolution in neotropical Annonaceae. Plant Species Biol 14:143–152. https://doi.org/10.1046/j.1442-1984.1999.00018.x
Gottsberger G, Silberbauer-Gottsberger I, Seymour RS, Dötterl S (2012) Pollination ecology of Magnolia ovata may explain the overall large flower size of the genus. Flora 207:107–118. https://doi.org/10.1016/j.flora.2011.11.003
Grimaldi D, Engel MS (2005) Evolution of the Insects. Cambridge Evolution, first edn. Cambridge University Press
Gullan PJ, Cranston PS (2014) The insects: an outline of entomology., 5th edn. John Wiley & Sons, Oxford
Gutiérrez-Carvajal L (1993) Estudio biológico de una especie forestal endémica (Magnolia dealbata Zucc.). Universidad Autónoma de Nuevo León
Heiser CB (1962) Some observations on pollination and compatibility in Magnolia. Proc Indiana Acad Sci 72:259–266
Hirayama K, Ishida K, Tomaru N (2005) Effects of pollen shortage and self-pollination on seed production of an endangered tree, Magnolia stellata. Ann Bot 95:1009–1015. https://doi.org/10.1093/aob/mci107
Hirthe G, Porembski S (2003) Pollination of Nymphaea lotus (Nymphaeaceae) by Rhinoceros beetles and bees in the northeastern Ivory Coast. Plant Biol 5:670–676. https://doi.org/10.1055/s-2003-44717
Hunt T et al (2007) A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science 318:1913–1916. https://doi.org/10.1126/science.1146954
Ishida K (1996) Beetle pollination of Magnolia praecocissima var. borealis. Plant Species Biol 11:199–206. https://doi.org/10.1111/j.1442-1984.1996.tb00146.x
Jelínek J, Carlton CE, Cline AR, Leschen RAB (2010) Nitidulidae Latreille 1802. In: Leschen RAB, Beutel RG, Lawrence JF (eds) Handbook of Zoology Arthropoda: Insecta. Coleoptera, Beetles, vol 4. De Gruyter GmbH & Co., Berlin, pp 390–407
Labandeira CC (2000) The Paleobiology of pollination and its precursors. Paleontol Soc Papers 6:233–270. https://doi.org/10.1017/S1089332600000784
Labandeira C (2006) Silurian to Triassic plant and hexapod clades and their associations: new data, a review, and interpretations. Arthropod Syst Phylogeny 64:53–94
Labandeira CC, Currano ED (2013) The fossil record of plant-insect dynamics. Annu Rev Earth Planet Sci 41:287–311
Labandeira CC, Kvaček J, Mostovski MB (2007) Pollination drops, pollen, and insect pollination of mesozoic gymnosperms. Taxon 56:663–695. https://doi.org/10.2307/25065853
Lai J-Y, Pan C-L, Qin W-G, Wei G-F (2007) Pollination ecology of rare and endangered species Kmeria septentrionalis. Guihaia:736–740
Law YH (2004) Magnolias of China. Beijing Science & Technology Press, Beijing
Leppik EE (1975) Morphogenic stagnation in the evolution of Magnolia flowers. Phytomorphology 25:451–464
Leschen RAB (1999) Systematics of Nitidulinae (Coleoptera: Nitidulidae): phylogenetic relationships, convexity and the origin of phallalophagy. Invertebr Syst 13:845–882. https://doi.org/10.1071/IT98016
Lidgard S, Crane PR (1988) Quantitative analyses of the early angiosperm radiation. Nature 331:344–346
Lidgard S, Crane PR (1990) Angiosperm diversification and Cretaceous floristic trends: a comparison of palynofloras and leaf macrofloras. Paleobiology 16:77–93. https://doi.org/10.1017/S009483730000974X
Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. N Z J Bot 24:135–162. https://doi.org/10.1080/0028825X.1986.10409725
Loughrin JH, Manukian A, Heath RR, Turlings TCJ, Tumlinson JH (1994) Diurnal cycle of emission of induced volatile terpenoids herbivore-injured cotton plants. Proc Natl Acad Sci USA 91:11836–11840. https://doi.org/10.1073/pnas.91.25.11836
Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, Hernández-Hernández T (2015) A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol 207:437–453. https://doi.org/10.1111/nph.13264
Maia ACD, Gibernau M, Carvalho AT, Gonçalves EG, Schlindwein C (2013) The cowl does not make the monk: scarab beetle pollination of the Neotropical aroid Taccarum ulei (Araceae: Spathicarpeae). Biol J Linn Soc 108:22–34. https://doi.org/10.1111/j.1095-8312.2012.01985.x
Mayer C, Soka G, Picker M (2006) The importance of monkey beetle (Scarabaeidae: Hopliini) pollination for Aizoaceae and Asteraceae in grazed and ungrazed areas at Paulshoek. Succulent Karoo, South Africa J Insect Conserv 10:323–333. https://doi.org/10.1007/s10841-006-9006-0
McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD (2009) Temporal lags and overlap in the diversification of weevils and flowering plants. Proc Natl Acad Sci USA 106:7083–7088. https://doi.org/10.1073/pnas.0810618106
McKenna DD et al (2015) The beetle tree of life reveals that Coleoptera survived end-Permian mass extinction to diversify during the Cretaceous terrestrial revolution. Syst Entomol 40:835–880. https://doi.org/10.1111/syen.12132
Misof B et al (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767. https://doi.org/10.1126/science.1257570
Mohr BAR, Bernardes-de-Oliveira MEC (2004) Endressinia brasiliana, a magnolialean angiosperm from the lower Cretaceous Crato Formation (Brazil). Int J Plant Sci 165:1121–1133. https://doi.org/10.1086/423879
Mohr BAR, Coiffard C, Bernardes-de-Oliveira MEC (2013) Schenkeriphyllum glanduliferum, a new magnolialean angiosperm from the Early Cretaceous of northern Gondwana and its relationships to fossil and modern Magnoliales. Rev Palaeobot Palynol 189:57–72. https://doi.org/10.1016/j.revpalbo.2012.08.004
Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B (2011) How many species are there on Earth and in the ocean? PLoS Biol 9:e1001127. https://doi.org/10.1371/journal.pbio.1001127
Nie ZL et al (2008) Phylogenetic and biogeographic complexity of Magnoliaceae in the Northern Hemisphere inferred from three nuclear data sets. Mol Phylogen Evol 48:1027–1040. https://doi.org/10.1016/j.ympev.2008.06.004
Nishida H, Hayashi N (1996) Cretaceous coleopteran larva fed on a female fructification of extinct gymnosperm. J Plant Res 109:327–330. https://doi.org/10.1007/BF02344479
Nooteboom HP (1993) Magnoliaceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) Flowering plants dicotyledons. The families and genera of vascular plants, vol 2. Springer, Berlin, pp 391–401
Ollerton J, Johnson SD, Cranmer L, Kellie S (2003) The pollination ecology of an assemblage of grassland Asclepiads in South Africa. Ann Bot 92:807–834. https://doi.org/10.1093/aob/mcg206
Pellmyr O, Thien LB (1986) Insect reproduction and floral fragrances: keys to the evolution of the angiosperms? Taxon 35:76–85. https://doi.org/10.2307/1221036
Pellmyr O, Tang W, Groth I, Bergström G, Thiens LB (1991) Cycad cone and angiosperm floral volatiles: inferences for the evolution of insect pollination. Biochem Syst Ecol 19:623–627. https://doi.org/10.1016/0305-1978(91)90078-E
Peris D (2017) Early Cretaceous origin of pollen-feeding beetles (Insecta: Coleoptera: Oedemeridae). Cladistics 33:268–278. https://doi.org/10.1111/cla.12168
Peris D, Pérez-de la Fuente R, Peñalver E, Delclòs X, Barrón E, Labandeira CC (2017) False blister beetles and the expansion of gymnosperm-insect pollination modes before angiosperm dominance. Curr Biol 27:897–904. https://doi.org/10.1016/j.cub.2017.02.009
Peris D, Labandeira CC, Barrón E, Delclòs X, Rust J, Wang B (2020) Generalist pollen-feeding beetles during the mid-Cretaceous. iScience. https://doi.org/10.1016/j.isci.2020.100913
Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569. https://doi.org/10.1146/annurev.ecolsys.38.091206.095601
Romanov MS, Dilcher DL (2013) Fruit structure in Magnoliaceae s.l. and Archaeanthus and their relationships. Am J Bot 100:1494–1508. https://doi.org/10.3732/ajb.1300035
Saunders RMK (2010) Floral evolution in the Annonaceae: hypotheses of homeotic mutations and functional convergence. Biol Rev 85:571–591. https://doi.org/10.1111/j.1469-185X.2009.00116.x
Sauquet H et al (2017) The ancestral flower of angiosperms and its early diversification. Nat Commun 8:16047. https://doi.org/10.1038/ncomms16047
Scott AC, Stephenson J, Chaloner WG (1992) Interaction and coevolution of plants and arthropods during the Palaeozoic and Mesozoic. Philos Trans R Soc Lond, Ser B: Biol Sci 335:129–165. https://doi.org/10.1098/rstb.1992.0016
Seymour RS, Matthews PG (2006) The role of thermogenesis in the pollination biology of the Amazon waterlily Victoria amazonica. Ann Bot 98:1129–1135. https://doi.org/10.1093/aob/mcl201
Seymour RS, Schultze-Motel P (1997) Heat-producing flowers. Endeavour 21:125–129. https://doi.org/10.1016/S0160-9327(97)80222-0
Seymour RS, White CR, Gibernau M (2003) Heat reward for insect pollinators. Nature 426:243–244
Seymour RS, White CR, Gibernau M (2009) Endothermy of dynastine scarab beetles (Cyclocephala colasi) associated with pollination biology of a thermogenic arum lily (Philodendron solimoesense). J Exp Biol 212:2960–2968. https://doi.org/10.1242/jeb.032763
Seymour RS, Silberbauer-Gottsberger I, Gottsberger G (2010) Respiration and temperature patterns in thermogenic flowers of Magnolia ovata under natural conditions in Brazil. Funct Plant Biol 37:870–878. https://doi.org/10.1071/fp10039
Slipinski SA, Leschen RAB, Lawrence JF (2011) Order Coleoptera Linnaeus, 1758. In: Zhang ZQ (ed) Animal Biodiversity: an outline of higher-level classification and survey of taxonomic richness, vol 3148. Zootaxa, pp 203–208
Smith ABT, Hawks DC, Heraty JM (2006) An overview of the classification and evolution of the major scarab beetle clades (Coleoptera: Scarabaeoidea) based on preliminary molecular analyses. Coleopt Bull 60:35–46. https://doi.org/10.1649/0010-065X(2006)60[35:AOOTCA]2.0.CO;2
Takabayashi J, Dicke M, Posthumus MA (1994) Volatile herbivore-induced terpenoids in plant-mite interactions: variation caused by biotic and abiotic factors. J Chem Ecol 20:1329–1354. https://doi.org/10.1007/bf02059811
Takhtajan A (1991) Evolutionary trends in flowering plants. Columbia University Press, New York
Tang W (1987) Heat production in cycad cones. Bot Gaz 148:165–174. https://doi.org/10.1086/337644
Teichert H, Dötterl S, Gottsberger G (2011) Heterodichogamy and nitidulid beetle pollination in Anaxagorea prinoides, an early divergent Annonaceae. Plant Syst Evol 291:25–33. https://doi.org/10.1007/s00606-010-0367-1
Thien LB (1974) Floral biology of Magnolia. Am J Bot 61:1037–1045
Thien LB (1980) Patterns of pollination in the primitive angiosperms. Biotropica 12:1–13. https://doi.org/10.2307/2387768
Thien LB et al (1996) The floral biology of the Magnoliaceae. In: Hunt DR (ed) Magnolias and their allies. Royal Holloway University of London, Egham, pp 37–58
Thien LB, Azuma H, Kawano S (2000) New perspectives on the pollination biology of basal angiosperms. Int J Plant Sci 161:S225–S235. https://doi.org/10.1086/317575
Vázquez-García JA et al. (2021) How to save endangered magnolias? From population biology to conservation action: the case of allopatric radiation in western Mexico. In: Kumar S (ed) Endangered Plants. IntechOpen, [Online First]. https://doi.org/10.5772/intechopen.94346. https://www.intechopen.com/online-first/how-to-save-endangered-magnolias-from-population-biology-to-conservation-action-the-case-of-allopatr
Vázquez-García JA, Neill DA, Asanza M (2015) Magnolia vargasiana (Magnoliaceae), a new Andean species and a key to Ecuadorian species of subsection Talauma, with notes on its pollination biology. Phytotaxa 217:26–34. https://doi.org/10.11646/phytotaxa.217.1.2
Vázquez-García JA, Neill DA, Asanza M, Pérez ÁJ, Arroyo F, Dahua-Machoa A, Merino-Santi RE (2016) Magnolias de Ecuador: en riesgo de extinción. Universidad Estatal Amazónica, Puyo
Wang L, Wang G, Liu D, Wang X, Shen Z (2005) Pollination biology of endangered Magnolia sieboldii. Chin J Ecol 24:853–857
Wang R, Jia H, Wang J, Zhang Z (2010) Flowering and pollination patterns of Magnolia denudata with emphasis on anatomical changes in ovule and seed development. Flora 205:259–265. https://doi.org/10.1016/j.flora.2009.04.003
Wang B, Zhang H, Jarzembowski EA (2013a) Early Cretaceous angiosperms and beetle evolution. Front Plant Sci 4:360. https://doi.org/10.3389/fpls.2013.00360
Wang R, Liu X, Mou S, Xu S, Zhang Z (2013b) Temperature regulation of floral buds and floral thermogenicity in Magnolia denudata (Magnoliaceae). Trees 27:1755–1762. https://doi.org/10.1007/s00468-013-0921-x
Wang R, Xu S, Liu X, Zhang Y, Wang J, Zhang Z (2014) Thermogenesis, flowering and the association with variation in floral odour attractants in Magnolia sprengeri (Magnoliaceae). PLoS ONE 9:e99356. https://doi.org/10.1371/journal.pone.0099356
Wang B, Chen G, Li C, Sun W (2017) Floral characteristics and pollination ecology of Manglietia ventii (Magnoliaceae), a plant species with extremely small populations (PSESP) endemic to South Yunnan of China. Plant Diversity 39:52–59. https://doi.org/10.1016/j.pld.2017.01.001
Yasukawa S, Kato H, Yamaoka R, Tanaka H, Arai H, Kawano S (1992) Reproductive and pollination biology of Magnolia and its allied genera (Magnoliaceae). I. Floral volatiles of several Magnolia and Michelia species and their roles in attracting insects. Plant Species Biol 7:121–140. https://doi.org/10.1111/j.1442-1984.1992.tb00225.x
Zhang Z-Q (2013) Phylum arthropoda. Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness (Addenda 2013). Zootaxa 3703:17–26. https://doi.org/10.11646/zootaxa.3703.1.6
Zhang S-Q, Che L-H, Li Y, Dan L, Pang H, Ślipiński A, Zhang P (2018) Evolutionary history of Coleoptera revealed by extensive sampling of genes and species. Nat Commun 9:205. https://doi.org/10.1038/s41467-017-02644-4
Zhao X, Sun W (2009) Abnormalities in sexual development and pollinator limitation in Michelia coriacea (Magnoliaceae), a critically endangered endemic to Southeast Yunnan, China. Flora Morphol, Distrib, Funct Ecol Plants 204:463–470. https://doi.org/10.1016/j.flora.2008.07.001
Acknowledgements
We thank the valuable comments and suggestions of Prof. David Dilcher and Dr. Brent C. Emerson that helped to improve a previous version of the manuscript. G. H.-V. thanks the Consejo Nacional de Ciencia y Tecnología (CONACyT—México) for financial support through a postdoctoral fellowship.
Author information
Authors and Affiliations
Contributions
GH-V conceived and wrote the manuscript, reviewed the literature and prepared figures and table; JAV-G reviewed and edited the manuscript, provided pictures, information on personal field observations and relevant literature; JLN-H. reviewed and edited the manuscript, provided information on relevant literature and helped with taxonomic identification of beetles.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Heikki Hokkanen.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hernández-Vera, G., Navarrete-Heredia, J.L. & Vázquez-García, J.A. Beetles as floral visitors in the Magnoliaceae: an evolutionary perspective. Arthropod-Plant Interactions 15, 273–283 (2021). https://doi.org/10.1007/s11829-021-09819-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-021-09819-3