Phenology of two co-occurring Piper (Piperaceae) species in Brazil
Adriano Valentin-Silva A B and Milene F. Vieira AA Universidade Federal de Viçosa, Departamento de Biologia Vegetal, Laboratório de Biologia Reprodutiva, 36570-900, Viçosa, Minas Gerais, Brasil.
B Corresponding author. Email: adrianovalentin86@gmail.com
Australian Journal of Botany 63(7) 581-589 https://doi.org/10.1071/BT14332
Submitted: 6 December 2014 Accepted: 7 July 2015 Published: 24 August 2015
Abstract
The co-occurrence of some species, including members of the Piper genus, has been shown to be associated with phenological factors. In the present study we analysed vegetative (sprout production and leaf flush) and reproductive phenophases (spike production, flowering, spike abortion, fruiting and dispersed spikes) of the co-occurring species Piper gaudichaudianum Kunth and Piper vicosanum Yunck. and checked the influence of abiotic factors on their phenological behaviour. Our study addressed natural populations in a semi-deciduous seasonal forest in south-eastern Brazil. In both species, the phenophases occurred mainly in the rainy season, were seasonal and associated with environmental variables, especially day length. However, sequential flowering and fruiting isolated them temporally from each other. Other differences were the growth of sexually reproductive sprouts (45.7% of the total sprouts) and the production of latent spikes in P. vicosanum; in P. gaudichaudianum, only 7.1% of the sprouts produced spikes that were not latent. Spike abortion was high: 73.8% (n = 474) in P. vicosanum and 84.8% (n = 231) in P. gaudichaudianum. The remaining spikes with fruits dispersed, on average, 293 and 1168 seeds per spike respectively. Although annual phenological behaviour of the species is regulated by similar environmental variables, their distinct reproductive strategies seem to favour the maintenance of the co-occurring populations.
References
Aide TM (1993) Patterns of leaf development and herbivory in a tropical understory community. Ecology 74, 455–466.| Patterns of leaf development and herbivory in a tropical understory community.Crossref | GoogleScholarGoogle Scholar |
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Köppen’s classification map for Brazil. Meteorologische Zeitschrift 22, 711–728.
Angulo-Sandoval P, Aide TM (2000) Leaf phenology and leaf damage of saplings in the Luquillo Experimental Forest, Puerto Rico. Biotropica 32, 415–422.
| Leaf phenology and leaf damage of saplings in the Luquillo Experimental Forest, Puerto Rico.Crossref | GoogleScholarGoogle Scholar |
Araújo AC, Fischer EA, Sazima M (1994) Floração seqüencial e polinização de três espécies de Vriesea (Bromeliaceae) na região da Juréia, sudeste do Brasil. Revista Brasileira de Botânica 17, 113–118.
Augspurger CK (1981) Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62, 775–788.
| Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae).Crossref | GoogleScholarGoogle Scholar |
Ayres M, Ayres Júnior M, Ayres DL, Santos AA (2007) ‘BioEstat – aplicações estatísticas nas áreas das ciências biomédicas.’ (Ong Mamiraua: Belém)
Bawa KS, Kang H, Grayum MH (2003) Relationships among time, frequency, and duration of flowering in tropical rain forest trees. American Journal of Botany 90, 877–887.
| Relationships among time, frequency, and duration of flowering in tropical rain forest trees.Crossref | GoogleScholarGoogle Scholar | 21659182PubMed |
Bencke CSC, Morellato LPC (2002) Comparação de dois métodos de avaliação da fenologia em plantas, sua interpretação e representação. Revista Brasileira de Botânica 25, 269–275.
| Comparação de dois métodos de avaliação da fenologia em plantas, sua interpretação e representação.Crossref | GoogleScholarGoogle Scholar |
Carvalho-Okano RM, Alves SAM (1998) Piperaceae C. Agardh da Estação Experimental Mata do Paraíso, Viçosa, MG. Acta Botanica Brasilica 12, 497–513.
| Piperaceae C. Agardh da Estação Experimental Mata do Paraíso, Viçosa, MG.Crossref | GoogleScholarGoogle Scholar |
Crawley MJ (2007) ‘The R book.’ (Wiley: Chichester, UK)
d’Eça-Neves FF, Morellato LPC (2004) Métodos de amostragem e avaliação utilizados em estudos fenológicos de florestas tropicais. Acta Botanica Brasilica 18, 99–108.
| Métodos de amostragem e avaliação utilizados em estudos fenológicos de florestas tropicais.Crossref | GoogleScholarGoogle Scholar |
de Figueiredo RA, Sazima M (2000) Pollination biology of Piperaceae species in southeastern Brazil. Annals of Botany 85, 455–460.
| Pollination biology of Piperaceae species in southeastern Brazil.Crossref | GoogleScholarGoogle Scholar |
Figueiredo RA, Sazima M (2004) Pollination ecology and resource partitioning in neotropical Pipers. In ‘Piper: a model genus for studies of phytochemistry, ecology, and evolution’. (Eds LA Dyer, ADN Palmer) pp. 33–57. (Kluwer Academic Publishers: New York)
Fleming TH (1985) Coexistence of five sympatric Piper (Piperaceae) species in a tropical dry forest. Ecology 66, 688–700.
| Coexistence of five sympatric Piper (Piperaceae) species in a tropical dry forest.Crossref | GoogleScholarGoogle Scholar |
Fleming TH (2004) Dispersal ecology of neotropical Piper shrubs and treelets. In ‘Piper: a model genus for studies of phytochemistry, ecology, and evolution’. (Eds LA Dyer, ADN Palmer) pp. 58–77. (Kluwer Academic Publishers: New York)
Fournier LA, Charpantier C (1975) El tamaño de la muestra y la frecuencia de las observaciones en el estudio de las características fenológicas de los árboles tropicales. Turrialba 25, 45–48.
Gartner BL (1989) Breakage and regrowth of Piper species in rain forest understory. Biotropica 21, 303–307.
| Breakage and regrowth of Piper species in rain forest understory.Crossref | GoogleScholarGoogle Scholar |
Greig N (1993) Regeneration mode in neotropical Piper: habitat and species comparisons. Ecology 74, 2125–2135.
| Regeneration mode in neotropical Piper: habitat and species comparisons.Crossref | GoogleScholarGoogle Scholar |
Guimarães EF, Carvalho-Silva M, Monteiro D, Medeiros ES, Queiroz GA (2015) ‘Piperaceae.’ (Jardim Botânico do Rio de Janeiro: Rio de Janeiro) Available at http://www.floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB190 [Verified 07 April 2015]
Hartshorn GS, Hammel BE (1994) Vegetation types and floristic patterns. In ‘La Selva: ecology and natural history of a neotropical rain forest’. (Eds LA McDade, KS Bawa, HA Hespenheide, GS Hartshorn) pp. 73–89. (University Chicago Press: Chicago, IL, USA)
Jaramillo MA, Manos PS (2001) Phylogeny and patterns of floral diversity in the genus Piper (Piperaceae). American Journal of Botany 88, 706–716.
| Phylogeny and patterns of floral diversity in the genus Piper (Piperaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsVWgsL4%3D&md5=792f5c745b6013de8829bfbd0dc21b35CAS | 11302858PubMed |
Lasso E, Engelbrecht BMJ, Dalling JW (2009) When sex is not enough: ecological correlates of resprouting capacity in congeneric tropical forest shrubs. Oecologia 161, 43–56.
| When sex is not enough: ecological correlates of resprouting capacity in congeneric tropical forest shrubs.Crossref | GoogleScholarGoogle Scholar | 19412623PubMed |
Lasso E, Dalling JW, Bermingham E (2012) Tropical understory Piper shrubs maintain high levels of genotypic diversity despite frequent asexual recruitment. Biotropica 44, 35–43.
| Tropical understory Piper shrubs maintain high levels of genotypic diversity despite frequent asexual recruitment.Crossref | GoogleScholarGoogle Scholar |
Marinho-Filho JS (1991) The coexistence of two frugivorous bat species and the phenology of their food plants in Brazil. Journal of Tropical Ecology 7, 59–67.
| The coexistence of two frugivorous bat species and the phenology of their food plants in Brazil.Crossref | GoogleScholarGoogle Scholar |
Mariot A, Mantovani A, Reis MS (2003) Uso e conservação de Piper cernuum Vell. (Piperaceae) na Mata Atlântica: I. Fenologia reprodutiva e dispersão de sementes. Revista Brasileira de Plantas Medicinais 5, 1–10.
Marquis RJ (1988) Phenological variation in the neotropical understory shrub Piper arieianum: causes and consequences. Ecology 69, 1552–1565.
| Phenological variation in the neotropical understory shrub Piper arieianum: causes and consequences.Crossref | GoogleScholarGoogle Scholar |
Martins FR, Batalha MA (2011) Formas de vida, espectro biológico de Raunkiaer e fisionomia da vegetação. In ‘Fitossociologia no Brasil. Métodos e estudos de caso. Vol. I’. (Orgs JM Felfili, PV Eisenlohr, MMRF Melo, LA Andrade, JAA Meira Neto) pp. 44–85. (Editora UFV: Viçosa, Brazil)
Mello MAR, Schittini GM, Selig P, Bergallo HG (2004) A test of the effects of climate and fruiting of Piper species (Piperaceae) on reproductive patterns of the bat Carollia perspicillata (Phyllostomidae). Acta Chiropterologica 6, 309–318.
| A test of the effects of climate and fruiting of Piper species (Piperaceae) on reproductive patterns of the bat Carollia perspicillata (Phyllostomidae).Crossref | GoogleScholarGoogle Scholar |
Morellato LPC, Leitão-Filho HF (1996) Reproductive phenology of climbers in a southeastern Brazilian forest. Biotropica 28, 180–191.
| Reproductive phenology of climbers in a southeastern Brazilian forest.Crossref | GoogleScholarGoogle Scholar |
Morellato LPC, Rodrigues RR, Leitão Filho HF, Joly CA (1989) Estudo comparativo da fenologia de espécies arbóreas de floresta de altitude e floresta mesófila semidecídua na Serra do Japi, Jundiaí, São Paulo. Revista Brasileira de Botânica 12, 85–98.
Morellato LPC, Camargo MGG, d’Eça-Neves FF, Luize BG, Mantovani A, Hudson IL (2010a) The influence of sampling method, sample size, and frequency of observations on plant phenological patterns and interpretation in tropical forest trees. In ‘Phenological research: methods for environmental and climate change analysis’. (Eds IL Hudson, MR Keatley) pp. 99–121. (Springer: Dordrecht, The Netherlands)
Morellato LPC, Alberti LF, Hudson IL (2010b) Applications of circular statistics in plant phenology: a case studies approach. In ‘Phenological research: methods for environmental and climate change analysis’. (Eds IL Hudson, MR Keatley) pp. 339–359. (Springer: Dordrecht, The Netherlands)
Newstrom LE, Frankie GW, Baker HG (1994) A new classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica. Biotropica 26, 141–159.
| A new classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica.Crossref | GoogleScholarGoogle Scholar |
Opler PA, Frankie GW, Baker HG (1976) Rainfall as a factor in the release, timing, and synchronization of anthesis by tropical trees and shrubs. Journal of Biogeography 3, 231–236.
| Rainfall as a factor in the release, timing, and synchronization of anthesis by tropical trees and shrubs.Crossref | GoogleScholarGoogle Scholar |
Opler PA, Frankie GW, Baker HG (1980) Comparative phenological studies of treelet and shrub species in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology 68, 167–188.
| Comparative phenological studies of treelet and shrub species in tropical wet and dry forests in the lowlands of Costa Rica.Crossref | GoogleScholarGoogle Scholar |
Palmeirim JM, Gorchov DL, Stoleson S (1989) Trophic structure of a neotropical frugivore community: is there competition between birds and bats? Oecologia 79, 403–411.
| Trophic structure of a neotropical frugivore community: is there competition between birds and bats?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sfnsFShsQ%3D%3D&md5=c644ef2f29c5e3a5b658a9a07c8cc822CAS | 23921407PubMed |
R Development Core Team (2010) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org [Verified 4 May 2015]
Rubim P, Nascimento HEM, Morellato LPC (2010) Variações interanuais na fenologia de uma comunidade arbórea de floresta semidecídua no sudeste do Brasil. Acta Botanica Brasilica 24, 756–764.
| Variações interanuais na fenologia de uma comunidade arbórea de floresta semidecídua no sudeste do Brasil.Crossref | GoogleScholarGoogle Scholar |
Silva CA, Vieira MF, Carvalho-Okano RM, Oliveira LO (2014) Reproductive success and genetic diversity of Psychotria hastisepala (Rubiaceae), in fragmented Atlantic forest, Southeastearn Brazil. Revista de Biología Tropical 62, 309–319.
Snow DW (1965) A possible selective factor in the evolution of fruiting seasons in tropical forest. Oikos 15, 274–281.
| A possible selective factor in the evolution of fruiting seasons in tropical forest.Crossref | GoogleScholarGoogle Scholar |
Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12, 253–279.
| Flower and fruit abortion: proximate causes and ultimate functions.Crossref | GoogleScholarGoogle Scholar |
Stevenson PR, Castellanos MC, Cortés AI, Link A (2008) Flowering patterns in a seasonal tropical lowland Forest in western Amazonia. Biotropica 40, 559–567.
| Flowering patterns in a seasonal tropical lowland Forest in western Amazonia.Crossref | GoogleScholarGoogle Scholar |
Stranghetti V, Ranga NT (1997) Phenological aspects of flowering and fruiting at the Ecological Station of Paulo de Faria-SP-Brazil. Tropical Ecology 38, 323–327.
Thies W, Kalko EKV (2004) Phenology of neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia perspicillata and C. castanea (Phyllostomidae). Oikos 104, 362–376.
| Phenology of neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia perspicillata and C. castanea (Phyllostomidae).Crossref | GoogleScholarGoogle Scholar |
Thomson JD (1980) Skewed flowering distributions and pollinator attraction. Ecology 61, 572–579.
| Skewed flowering distributions and pollinator attraction.Crossref | GoogleScholarGoogle Scholar |
Valentin-Silva A, Coelho VPM, Ventrella MC, Vieira MF (2015) Timing of pollen release and stigma receptivity period of Piper vicosanum: new insights into sexual reproduction of the genus. American Journal of Botany 102, 626–633.
| Timing of pollen release and stigma receptivity period of Piper vicosanum: new insights into sexual reproduction of the genus.Crossref | GoogleScholarGoogle Scholar | 25878095PubMed |
van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology, Evolution, and Systematics 24, 353–377.
| The phenology of tropical forests: adaptive significance and consequences for primary consumers.Crossref | GoogleScholarGoogle Scholar |
Veloso HP, Rangel Filho ALR, Lima JCA (1991) ‘Classificação da vegetação brasileira, adaptada a um sistema universal.’ (IBGE: Rio de Janeiro)
Wright SJ (1991) Seasonal drought and the phenology of understory shrubs in a tropical moist forest. Ecology 72, 1643–1657.
| Seasonal drought and the phenology of understory shrubs in a tropical moist forest.Crossref | GoogleScholarGoogle Scholar |
Wright SJ, Calderon O (1995) Phylogenetic patterns among tropical flowering phenologies. Journal of Ecology 83, 937–948.
| Phylogenetic patterns among tropical flowering phenologies.Crossref | GoogleScholarGoogle Scholar |
Wright SJ, van Schaik CP (1994) Light and the phenology of tropical trees. American Naturalist 143, 192–199.
| Light and the phenology of tropical trees.Crossref | GoogleScholarGoogle Scholar |
Yuncker TG (1972) The Piperaceae of Brazil – I. Hoehnea 2, 19–366.
Yuncker TG (1973) The Piperaceae of Brazil – II: Piper group V, Ottonia, Pothomorphe, Sarcorhachis. Hoehnea 3, 29–284.
Zar JH (1999) ‘Biostatistical analysis.’ (Prentice-Hall: Upper Saddle River, NJ, USA)