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

Springer Science and Business Media LLC - Tập 54 Số 3-4 - Trang 239-256 - 2019
Emerson Antônio Rocha1, Arthur Domingos‐Melo2, Daniela C. Zappi3, Isabel Cristina Machado2
1Departamento de Ciências Biológicas, Pavilhão Jorge Amado, Universidade Estadual de Santa Cruz, Rod. Ilhéus-Itabuna km 16, Ilhéus, BA, 45662-900, Brazil
2Departamento de Botânica, Centro de Biociências, Universidade Federal de Pernambuco, Recife, PE, 50670-423, Brazil
3Instituto Tecnológico Vale, Museu Paraense Emilio Goeldi, Coord Botânica, R. Boaventura da Silva 955, CEP, Belém, Pará, 66055-090, Brazil

Tóm tắt

Từ khóa


Tài liệu tham khảo

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