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Reproductive biology of columnar cacti: are bats the only protagonists in the pollination of Pilosocereus, a typical chiropterophilous genus?

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Abstract

The Cactaceae display a wide array of pollination systems, with many different animals already confirmed as pollinators. Pilosocereus is one of the most conspicuous bat-pollinated genera characteristic of the tropical dry forests of Brazil, known as Caatinga. The role of bats, hawkmoths and bees as pollinators in natural populations was investigated for four Pilosocereus species (P. catingicola, P. chrysostele, P. gounellei and P. pachycladus). Earlier results obtained with P. tuberculatus were also included in the comparative discussion. These species depend mainly upon nocturnal visitors; however, Xylocopa grisescens bees also play a secondary role in the fruit set. Although chiropterophily is predominant in Pilosocereus, P. gounellei was visited and pollinated at night exclusively by sphingids. All species are described as presenting a chiropterophilous syndrome based on their nocturnal anthesis, strong and unpleasant flower scent, pale, white or cream inner perianth, compact and abundant flower parts, and large volume of nectar with low sugar concentration. Pollen is available and the stigma is receptive throughout anthesis. With the exception of P. gounellei, there was no fruit set from spontaneous or manual self-pollination, indicating that allogamy is the predominant reproductive system in all the species studied. These species thus rely on animals that function as efficient pollen vectors for their sexual reproduction. The Pilosocereus species present different levels of dependence on bats, from the participation of secondary pollinators to not being visited by bats at all. Dependence levels are associated with the species floral attributes, which, although subdued, can determine different pollination systems.

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References

  • Alcorn SM, McGregor SE, Butler GD, Kurtz EB (1959) Pollination requirements of the saguaro (Carnegiea gigantea). Cact Succ J 31:39–41

  • Alvarez T, González LQ (1970) Análisis polínico del contenido gástrico del murciélagos Glossophaginae de México. Anales Esc Nac Ci Biol 18:137–165

  • Andrade KVSA, Rodal MJN, Lucena, MFA, Gomes APS (2004) Composição florística de um trecho do Parque Nacional do Catimbau, Buíque, Pernambuco – Brasil. Hoehnea 31:337–348

  • Andrade-Lima D (1989) Plantas das caatingas. Academia Brasileira de Ciências. Rio de Janeiro

  • Aona LYS, Machado M, Pansarin ER, Castro CC, Zappi D, Amaral, MCE (2006) Pollination biology of three Brazilian species of Micranthocereus Backeb. (Cereeae, Cactoideae) endemic to the “campos rupestres”. Bradleya 24:39–53

  • Astúa D, Guerra DQ (2008) Caatinga bats in the Mammal Collection of the Universidade Federal de Pernambuco. Chiropt Neotrop 14:326–338

  • Baker HG (1961) The adaptation of flowering plants to nocturnal and crepuscular pollinators. Quart Rev Biol 36:64–73

  • Baker HG, Baker I (1982) Chemical constituents of nectar in relation to pollination mechanisms and phylogeny. In: MH Nitecki (ed) Biochemical aspects of evolutionary biology. Chicago: The University of Chicago Press, pp 131–171

  • Baker H.G., Baker I. (1983) Floral nectar sugar constituents in relation to pollinator type. In Jones CE, Little RJ (eds) Handbook of experimental pollination biology. New York: Van Nostrand Reinhold, pp 117–141

  • Baker HG, Baker I, Hodges SA (1998) Sugar composition of nectars and fruits consumed by birds and bats in the tropics and the subtropics. Biotropica 30:559–586

  • Batagelj V, Mrvar A (1998) Pajek-program for large network analysis. Connections 21:47–57

  • BFG (BRAZIL FLORA GROUP) (2015) Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66:1085–1113

  • Boiça Jr AL, Santos TM, Passilongo J (2004) Trigona spinipes (Fabr.) (Hymenoptera: Apidae) em espécies de maracujazeiro: flutuação populacional, horário de visitação e danos às flores. Neotrop Entomol 33:135–139

  • Bustamante E, Búrquez A (2005) Fenología y biología reproductiva de las cactáceas columnares. Cact Suc Mex 50:68–88

  • Colaço MAS, Fonseca RBS, Lambert SM, Costa CBN, Machado CG, Borba EL (2006) Biologia reprodutiva de Melocactus glaucescens Buining and Brederoo e M. paucispinus G. Heimen and R. Paul (Cactaceae), na Chapada Diamantina, Nordeste do Brasil. Revista Brasil Bot 29:239–249

  • Dafni A, Kevan P G, Husband BC (2005) Practical pollination biology. Enviroquest Ltd, xv + 590 pp

  • Dobat K, Peikert-Holle T (1985) Blüten und Fledermäuse. Frankfurt: Waldemar Kramer

  • Domingos-Melo A (2015) Partição de nicho entre besouros florívoros a partir da altura das flores em Pilosocereus pachycladus F. Ritter (Cactaceae). In Sfair J., Calaça T., Câmara T., Ribeiro Neto J., Melo F., Leal I.R., Tabarelli M. Ecologia da Caatinga Curso de Campo 2013. Recife: Livrinho de Papel Finíssimo, pp 342–355

  • Domingos-Melo A, Nadia TL, Machado IC (2017) Complex flowers and rare pollinators: Does ant pollination in Ditassa show a stable system in Asclepiadoideae (Apocynaceae)? Arthropod Pl Interact 11:339–349

  • Duarte-Junior JA, Schlindwein, C (2005) The highly seasonal hawkmoth fauna (Lepidoptera Sphingidae:) of the caatinga of northeast Brazil: a case study in the state of Rio Grande do Norte. J Lepidopt Soc 59:212

  • Faegri K, van der Pijl L (1979) The principles of pollination ecology. London: Pergamon Press

  • Feinsinger P, Colwell RK (1978) Community organization among neotropical nectar-feeding birds. Amer Zoologist 18:779–795

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Ecol Evol Syst 35:375–403

  • Ferreira BHS, Gomes AC, Souza CS, Fabri JR, Sigrist MR (2018) Pollination and reproductive system of synchronopatric species of Cactaceae (Cactoideae) subject to interspecific flow of pollen: an example of ecological adaptation in the Brazilian Chaco. Pl Biol 20:101–112

  • Fleming TH, Maurice S, Buchmann SL, Tuttle MD (1994) Reproductive biology and related male and female fitness in trioecious cactus, Pachycereus pringlei (Cactaceae). Amer J Bot 81:858–867

  • Fleming TH, Tuttle MD, Horner MA (1996) Pollination biology and relative importance of noturnal and diurnal pollinators in three species of Sonoran Desert columnar cacti. S W Naturalist 41:257–269

  • Fleming TH, Sahley CT, Holland JN, Nason J, Hamrich JL (2001) Sonoran desert columnar cacti and the evolution of generalized pollination systems. Ecol Monogr 71:511–530

  • Fleming TH, Geiselman C, Kress WJ (2009) The evolution of bat pollination: a phylogenetic perspective. Ann Bot (Oxford) 104:1017–1043

  • Galen C, Plowright RC (1987) Testing the accuracy of using peroxidase activity to indicate stigma receptivity. Canad J Bot 65:107–111

  • Gomes VGN, Quirino ZGM, Machado IC (2014) Pollination and seed dispersal of Melocactus ernestii Vaupel subsp. ernestii (Cactaceae) by lizards: an example of double mutualism. Pl Biol 16:315–322

  • Gorostiague P, Ortega-Baes P (2017) Pollination biology of Echinopsis leucantha (Cactaceae): passerine birds and exotic bees as effective pollinators. Botany 95:53–59

  • Governo da Paraíba (2007) Sito do Governo da Paraíba. Available at http://www.paraiba.pb.gov.br (Accessed 28 March 2007)

  • Grant V, Grant KA (1979a) Pollination of Echinocereus fasciculatus and Ferocactus wislizenii. Pl Syst Evol 132:85–90

  • Grant V, Grant KA (1979b) Pollination of Opuntia basilaris and O. littoralis. Pl Syst Evol 132:321–325

  • Grant V, Grant KA (1979c) The pollination spectrum in the southwestern American cactus flora. Pl Syst Evol 133:29–37

  • Grant V, Grant KA, Hurd PD (1979) Pollination of Opuntia lindheimeri and related species. Pl Syst Evol 132:313–320

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

  • Hernández-Hernández T, Hernández HM, De-Nova JA, Puente R, Eguiarte LE, Magallón S (2011) Phylogenetic relationships and evolution of growth from in Cactaceae (Caryophyllales, Eudicotyledoneae). Amer J Bot 98:44–61

  • Hernández-Hernández T, Brown JW, Schlumpberger BO, Eguiarte LE, Magallón S (2014) Beyond aridification: multiple explanations for the elevated diversification of cacti in the New World Succulent Biome. New Phytol 202:1382–1397

  • Herrera CM (1995) Floral traits and plant adaptation to insect pollinators: a devil’s advocate approach. In DG Lloyd, SCH Barrett (eds) Floral biology. Boston, Springer, pp. 65–87

  • Hoffman MT (1992) Functional dioecy in Echinocereus coccineus (Cactaceae): breeding system, sex ratios and geographical range of sexual dimorphism. Amer J Bot 79:1382–1388

  • Hunt D, Taylor NP (1990) The genera of Cactaceae: progress towards consensus. Bradleya 8:85–107

  • Hunt D, Taylor NP, Charles G (2006) The New Cactus Lexicon. DH Books, Milborne Port, Sherborne, England

  • Ibarra-Cerdeña CN, Iñiguez-Davalos LI, Sánchez-Cordero V (2005) Pollination ecology of Stenocereus queretaroensis (Cactaceae), a chiropterophilous columnar cactus, in a tropical dry forest of Mexico. Amer J Bot 92:503–509

  • Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends Ecol Evol 15:140–143

  • Lau MK, Borrett SR, Baiser B, Gotelli NJ, Ellison AM (2017) Ecological network metrics: opportunities for synthesis. Ecosphere 8:1–17

  • Lehner PN (1979) Handbook of ethological methods. New York: Garland STPM Press

  • Lemke T.O. (1984) Foraging ecology of the long-nosed bat, Glossophaga soricina, with respect to resource availability. Ecology 65:538–548

  • Lloyd DG (1972) Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21:29–45

  • Locatelli E, Machado ICS (1999a) Comparative study of the floral biology in two ornithophilous species of Cactaceae: Melocactus zehntneri and Opuntia palmadora. Bradleya 17:75–85

  • Locatelli E, Machado ICS (1999b) Floral biology of Cereus fernambucensis: a sphingophilous cactus of the restinga. Bradleya 17:86–94

  • Locatelli E, Machado ICS, Medeiros P (1997) Floral biology and pollination in Pilosocereus catingicola (Cactaceae) in Northeastern Brazil. Bradleya 15:28–34

  • Machado IC, Vogel S (2004) The North-east-Brazilian liana Adenocalymma dichilum (Bignoniaceae) pollinated by bats. Ann Bot (Oxford) 93:609–613

  • Machado ICS, Sazima I, Sazima M. (1998) Irlbachia alata (Gentianaceae), a bat-pollinated herb from the Atlantic forest in notheastern Brazil. Pl Syst Evol 209:23–137

  • Malerbo-Souza DT, Nogueira-Couto RH, Toledo VDAA (2002) Insetos associados às flores de diferentes espécies de maracujá (Passiflora spp.). Acta Sci Agron 24:1269–1274

  • Mandujano MDC, Carrillo-Angeles I, Martínez-Peralta C, Globulov J (2010) Reproductive biology of Cactaceae. In Ramawat KG (ed) Desert plants. Springer-Verlag Berlim pp 197–230

  • Martins C, Freitas L (2018) Functional specialization and phenotypic generalization in the pollination system of an epiphytic cactus. Acta Bot Brasil 32:359–366

  • Martins C, Oliveira R, Mendonça Filho CV, Antonini Y (2016) Reproductive biology of Cipocereus minensis (Cactaceaee) – a columnar cactus endemic to rupestrian fields of a Neotropical savannah. Flora 218:62–67

  • McGregor SE, Alcorn SM, Olin G (1962) Pollination and pollinating agents of the saguaro. Ecology 43:260–267

  • Molina-Freaner F, Rojas-Martínez A, Fleming TH, Valiente-Banuet A (2004) Pollination biology of the columnar cactus Pachycereus pecten-aboriginum in north-western México. J Arid Environm 56:117–127

  • Moura RA, Wada CS, Purchio A, Almeida TV (1987) Técnicas de laboratório. Atheneu, Rio de Janeiro

  • Muchhala N (2006) Nectar bat stows huge tongue in its rib cage. Nature 444:701

  • Muchhala N, Jarrin VP (2002) Flower visitation by bats in cloud forests of western Ecuador. Biotropica 34:387–395

  • Muchhala N, Thomson JD (2010) Fur versus feathers: pollen delivery by bats and hummingbirds and consequences for pollen production. Amer Naturalist 175:717–726

  • Muchhala N, Caiza A, Vizuete JC, Thomson JD (2009) A generalized pollination system in the tropics: bats, birds and Aphelandra acanthus. Ann Bot (Oxford) 103:1481–1487

  • Munguía-Rosas MA, Sosa VJ, Jácome-Flores ME (2009) Pollination system of the Pilosocereus leucocephalus columnar cactus (tribe Cereeae) in eastern Mexico. Pl Biol 12:578–586

  • Mutke J, Burstedde K, Geffert JL, Miebach A, Rafiqpoor MD, Stein A, Barthlott W (2015) Patterns of diversity and endemism. In Barthlott W, Burstedde K, Geffert JL, Ibisch PL, Krotkova N, Miebach A, Rafiqpoor MD, Stein A, Mutke J (eds) Biogeography and biodiversity of cacti. Schumannia 7:37–67

  • Nassar JM, Ramírez N, Linares O (1997) Comparative pollination biology of Venezuelan columnar cacti and the role of nectar-feeding bats in their sexual reproduction. Amer J Bot 84:918–927

  • Nassar JM, Ramírez N, Lampo M, González JA, Casado R, Nava F (2006) Reproductive biology and mating system estimates of two Andean melocacti, Melocactus schatzlii and M. andinus (Cactaceae). Ann Bot (Oxford) 99:29–38

  • 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

  • Ortega-Baes P, Sühring S, Godínez-Alvarez H, Zamar M (2011) Reproductive biology of Echinopsis terscheckii (Cactaceae): the role of nocturnal and diurnal pollinators. Pl Biol 13:33–40

  • Parfitt BD (1985) Dioecy in North American Cactaceae: a review. Sida 11:200–206

  • Petit S (1997) The diet and reproductive schedules of Leptonycteris curasoae and Glossophaga longirostris elongate (Chiroptera: Glossophaginae) on Curaçao, Netherlands Antilles. Biotropica 27:538–541

  • Petit S, Freeman CE (1997) Nectar production of two sympatric columnar cacti. Biotropica 29:175–183

  • Porsch O (1939) Cactaceae. In: JN Druck. Das Bestäubungsleben der Kakteen-blüte II. Jahrbucher der Deutschen Kakteen-Gesellchaft E.V

  • Primo LM, Duarte-Junior JA, Machado IC (2013). Hawkmoth fauna (Sphingidae, Lepidoptera) in a semi-deciduous rainforest remnant: composition, temporal fluctuations, and new records for northeastern Brazil. Anais Acad Brasil Ci 85:1177–1188

  • Queiroz JA, Quirino ZG, Machado IC (2015) Floral traits driving reproductive isolation of two co-flowering taxa that share vertebrate pollinators. AoB Pl 7:1–13

  • Queiroz JA, Quirino ZGM, Lopes AV, Machado IC (2016) Vertebrate mixed pollination system in Encholirium spectabile: a bromeliad pollinated by bats, opossum and hummingbirds in a tropical dry forest. J Arid Environm 125:21–30

  • Radford AE, Dickison WC, Massey JR, Bell CR (1974) Vascular plant systematics. New York: Harper & Row publishers

  • Raw A (1996) Territories of the ruby-topaz hummingbird, Chrysolampis mosquitus at flowers of the “turk’s-cap” cactus, Melocatus salvadorensis in the dry Caatinga of north-eastern Brazil. Revista Brasil Biol 56:581–584

  • Rego JO, Franceschinelli EV, Zappi DC (2012) Reproductive biology of a highly endemic species: Cipocereus laniflorus N.P. Taylor & Zappi (Cactaceae). Acta Bot Brasil 26:243–250

  • Renner S (1983) The widespread ocurrence of anther destruction by Trigona bees in Melastomataceae. Biotropica 15:251–256

  • Rivera-Marchand B, Ackerman JD (2006) Bat pollination breakdown in the Caribbean columnar cactus Pilosocereus royenii. Biotropica 38:635–642

  • Robinsohn I (1924) Die farbunsreaktion der narbe, stigmatochromie, als morpho-biologische blütenuntersuchungs methode. Sitzungsber Kaiserl Akad Wiss Math-Naturwiss Cl 33:180–213

  • Rocha EA (2007a) Fenologia, biologia da polinização e da reprodução de Pilosocereus Byles & Rowles (Cactaceaee) no Nordeste do Brasil. Tese de Doutorado. Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Pernambuco, Recife, Brasil

  • Rocha EA, Machado ICS, Zappi DC (2007b) Floral biology of Pilosocereus tuberculatus (Wederm.) Byles & Rowley: a bat pollinated cactus endemic from the “Caatinga” in northeastern Brazil. Bradleya 25:129–144

  • Rodal MJN, Andrade KVA, Sales MF, Gomes APS (1998) Fitossociologia do componente lenhoso de um refúgio vegetacional no município de Buíque, Pernambuco. Revista Brasil Biol 58:517–526

  • 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 Letters 17:388–400

  • Ruiz A, Santos M, Soriano PJ, Cavelier J, Cadena A (1997) Relaciones mutualísticas entre el murciélago Glossophaga longirostris y las cactáceas columnares en la zona árida de la Tatacoa, Colombia. Biotropica 29:469–479

  • Schlindwein C, Wittmann D (1995) Specialized solitary bees as effective pollinators of south Brazilian species of Notocatus and Gymnocalycium (Cactaceae). Bradleya 13:25–34

  • Schlindwein C, Wittmann D (1997) Stamen movements in flowers of Opuntia (Cactaceae) favour oligolectic pollinators. Pl Syst Evol 24:179–193

  • Schlumpberger BO (2010) A survey on pollination modes in cacti and a potential key innovation. In Patiny S (ed) Evolution of plant-pollinator relationships. Cambridge University Press, London, pp 301–319

  • Scogin R (1985) Nectar constituents of the Cactaceae. S W Naturalist 30:77–82

  • Shepherd GJ (2009) FITOPAC 2.1 (versão preliminar). Departamento de Biologia Vegetal, Universidade Estadual de Campinas

  • Silva WR, Sazima M (1995) Hawkmoth pollination in Cereus peruvianus, a columnar cactus from southeastern Brazil. Flora 190:339–343

  • Simmons NB, Wetterer AL (2002) Phylogeny and convergence in cactophilic bats. In Fleming TH, Valient-Banuet A (eds) Columnar cacti and their mutualists: evolution, ecology, and conservation. Tucson: The University of Arizona Press, pp 87–121

  • Siqueira Filho JD, Machado ICS (2001) Biologia reprodutiva de Canistrum aurantiacum E. Morren (Bromeliaceae) em remanescente da Floresta Atlântica, nordeste do Brasil. Acta Bot Brasil 15:427–443

  • Soriano PJ, Ruiz A (2002) The role of bats and birds in the reproduction of columnar cacti in the Northern Andes. In Fleming TH, Valiente-Banuet A (eds) Columnar cacti and their mutualists: evolution, ecology, and conservation. Tucson: The University of Arizona Press, pp. 241–263

  • Sosa M, Soriano PJ (1992) Los murciélagos y los cactus: una relación muy estrecha. Carta Ecol, 61:7–10

  • Sosa M, Soriano PJ (1996) Resource availability, diet and reproduction in Glossophaga longirostris (Mammalia: Chiroptera) in an arid zone of the Venezuelan Andes. J Trop Ecol 12:805–818

  • Taylor NP, Zappi DC (2002) Distribuição das espécies de Cactaceae na Caatinga. In Sampaio EVSB, Giulietti AM, Virgínio J, Rojas CFLG (eds) Vegetação e flora da Caatinga. Recife: Associação Plantas do Nordeste, Centro Nordestino de Informações sobre Plantas, pp 123–125

  • Taylor NP, Zappi DC (2004) Cacti of eastern Brazil. Kew: Royal Botanic Gardens

  • Taylor NP, Zappi DC (2008) A neglected species of Cipocereus. Cactaceae Syst Init 24:8–11

  • Tschapka M, von Helversen O, Barthlott W (1999) Bat Pollination of Weberocereus tunilla, an epiphytic rain forest cactus with functional flagelliflory. Pl Biol 1:554–559

  • Valiente-Banuet A (2002) Vulnerabilidad de los sistemas de polinización de Cactáceas columnares de México. Revista Chileana Hist Nat 75:99–104

  • Valiente-Banuet A, Arizmendi MC, Rojas-Martínez A, Domingues-Canseco L (1996) Ecological relationship between columnar cacti and nectar-feeding bats in Mexico. J Trop Ecol 12:103–119

  • Valiente-Banuet A, Rojas-Martínez A, Casas A, Arizmendi MDC, Dávila P (1997a). Pollination biology of two winter-blooming giant columnar cacti in the Tehuacán Valley, central Mexico. J Arid Environm 37:331–341

  • Valiente-Banuet A, Rojas-Martínez A, Arizmendi MDC, Dávila P (1997b) Pollination biology of two columnar cacti (Neobuxbaumia mezcalaensis and Neobuxbaumia macrocephala) in the Tehuacán Valley, Central México. Amer J Bot 84:452–455

  • Valiente-Banuet A, Gally RS, Arizmendi MC, Casas A (2007) Pollination biology of the hemiepiphytic cactus Hylocereus undatus in the Tehuacan Valley, Mexico. J Arid Environm 68:1–8

  • Viana ML, Ortega-Baes P, Saravia M, Badano EI, Schlumpberger O (2001) Biologia floral y polinizadores de Trichocereus pasacana (Cactaceae) en el Parque Nacional Los Cardones, Argentina. Revista Biol Trop 49:279–285

  • Vogel S (1968) Chiropterophilie in der neotropischen Flora. Neue Mitteilungen I. flora 157:562–602

  • Walter H (2010) Floral biology of Echinopsis chiloensis spp. chiloensis (Cactaceae): Evidence for a mixed pollination syndrome. Flora 205:757–763

  • Waser NM (1983) The adaptative nature of floral traits: ideas and evidence. In Real L (ed) Pollination biology. New York: Academic Press, pp 241–285

  • Willmer P (2011) Pollination and floral ecology. Princeton University Press

  • Zappi DC (1989) A família Cactaceae nos Campos Rupestres da Cadeia do Espinhaço Minas Gerais, Brasil. Dissertação de Mestrado. Universidade de São Paulo: Instituto de Biociências

  • Zappi DC (1994) Pilosocereus (Cactaceae). The genus in Brazil. Succ Pl Res, 3:1–160

  • Zeisler M (1938) Über die Abgrenzung der eigentlichen Narbenfläche mit Hilfe von Reaktionen. Zentralbl Beih Bot 58:308–318

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Acknowledgements

We are grateful to MSc. Deoclécio Queiroz Guerra (in memoriam) and Dr Ivan Sazima for bat identification; V. Zappi-Taylor for the English revision; Dr Elisangela Bezerra and Genivaldo Constantino for field support; Dr Joel Queiroz for helping to build Fig. 2; IBAMA for fieldwork licence (number 081/2004); DCB/Universidade Estadual de Santa Cruz (UESC) for allowing time for EAR to conclude his PhD; ICM and DCZ hold CNPq productivity grants.

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Rocha, E.A., Domingos-Melo, A., Zappi, D.C. et al. Reproductive biology of columnar cacti: are bats the only protagonists in the pollination of Pilosocereus, a typical chiropterophilous genus?. Folia Geobot 54, 239–256 (2019). https://doi.org/10.1007/s12224-019-09357-0

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