Continental-scale patterns and climatic drivers of fruiting phenology: A quantitative Neotropical review

Alencar, 1979, Fenologia de espécies florestais em floresta tropical úmida de terra firme na Amazônia Central, Acta Amazon., 1, 63 Allen, 1956 Alvim, 1964, 405 Antonelli, 2011, Why are there so many plant species in the Neotropics?, Taxon, 60, 403, 10.1002/tax.602010 Arbeláez, 2005, Seed dispersal modes of the sandstone plateau vegetation of the middle Caquetá river region, Colombian Amazonia, Biotropica, 37, 64, 10.1111/j.1744-7429.2005.03077.x Archibold, 1994 Arroyo, 2010 Barlow, 2006, Effects of single and recurrent wildfires on fruit production and large vertebrate abundance in a central Amazonian forest, Biodivers. Conserv., 15, 985, 10.1007/s10531-004-3952-1 Batalha, 2004, Reproductive phenology of the cerrado plant community in Emas National Park (central Brazil), Aust. J. Bot., 52, 149, 10.1071/BT03098 Bendix, 2006, Seasonality of weather and tree phenology in a tropical evergreen mountain rain forest, Int. J. Biometeorol., 50, 370, 10.1007/s00484-006-0029-8 Blake, 1990, Quantifying abundance of fruits for birds in tropical habitats, Stud. Avian Biol., 13, 73 Borchert, 1996, Phenology and flowering periodicity of neotropical dry forest species: evidence from herbarium collections, J. Trop. Ecol., 12, 65, 10.1017/S0266467400009317 Borchert, 2005, Photoperiodic induction of synchronous flowering near the equator, Nature, 433, 627, 10.1038/nature03259 Borchert, 2015, Insolation and photoperiodic control of tree development near the equator, New Phytol., 205, 7, 10.1111/nph.12981 Both, 2006, Climate change and population declines in a long-distance migratory bird, Nature, 441, 81, 10.1038/nature04539 Boubli, 1997, Ecology of the Black Uakari Monkey, Cacajao melanocephaus melanocephalus Butt, 2015, Cascading effects of climate extremes on vertebrate fauna through changes to low-latitude tree flowering and fruiting phenology, Glob. Chang. Biol., 21, 3267, 10.1111/gcb.12869 Calle, 2010, Seasonal variation in daily insolation induces synchronous bud break and flowering in the tropics, Trees, 24, 865, 10.1007/s00468-010-0456-3 Camargo, 2013, Fruit color and contrast in seasonal habitats — a case study from a cerrado savanna, Oikos, 122, 1335, 10.1111/j.1600-0706.2013.00328.x Catanzaro, 2014, South American science: big players, Nature, 510, 204, 10.1038/510204a Chambers, 2013, Changes in southern hemisphere phenology, PLoS Biol., 8 Chang-Yang, 2016, ENSO and frost codetermine decade-long temporal variation in flower and seed production in a subtropical rain forest, J. Ecol., 104, 44, 10.1111/1365-2745.12481 Chapman, 1994, Indexes of habitat-wide fruit abundance in tropical forests, Biotropica, 26, 160, 10.2307/2388805 Chapman, 1992, Estimators of fruit abundance of tropical trees, Biotropica, 24, 527, 10.2307/2389015 Chen, 2016, Plants show more flesh in the tropics: variation in fruit type along latitudinal and climatic gradients, Ecography Cleland, 2007, Shifting plant phenology in response to global change, Trends Ecol. Evol., 22, 357, 10.1016/j.tree.2007.04.003 Cook, 2012, Divergent responses to spring and winter warming drive community level flowering trends, Proc. Natl. Acad. Sci. U. S. A., 109, 9000, 10.1073/pnas.1118364109 Cortés-Flores, 2013, Fruiting phenology of seed dispersal syndromes in a Mexican neotropical temperate forest, For. Ecol. Manag., 289, 445, 10.1016/j.foreco.2012.10.038 Croat, 1969, Seasonal flowering behavior in Central Panama, Ann. Mo. Bot. Gard., 56, 295 Croat, 1975, Phenological behavior of habit and habitat classes on Barro Colorado Island (Panama Canal Zone), Biotropica, 7, 270, 10.2307/2989739 Davis, 1933, The vegetation of Moraballi creek, British Guiana: an ecological study of a limited area of tropical forest. Parts I, J. Ecol., 21, 350, 10.2307/2256587 Davis, 1997 d'Eça-Neves, 2004, Métodos de amostragem e avaliação utilizados em estudos fenológicos de florestas tropicais, Acta Bot. Bras., 18, 99, 10.1590/S0102-33062004000100009 Demarée, 2009, Origins of the word “phenology”, EOS Trans. Am. Geophys. Union, 90, 291, 10.1029/2009EO340004 Demarée, 2011, From “periodical observations” to “anthochronology” and “phenology” – the scientific debate between Adolphe Quetelet and Charles Morren on the origin of the word “phenology”, Int. J. Biometeorol., 55, 753, 10.1007/s00484-011-0442-5 Develey, 2000, Resource seasonality and the structure of mixed species bird flocks in a coastal Atlantic forest of southeastern Brazil, J. Trop. Ecol., 16, 33, 10.1017/S0266467400001255 Diffenbaugh, 2011, Observational and model evidence of global emergence of permanent, unprecedented heat in the 20th and 21st centuries, Clim. Chang., 107, 615, 10.1007/s10584-011-0112-y Dose, 2004, Bayesian analysis of climate change impacts in phenology, Glob. Chang. Biol., 10, 259, 10.1111/j.1529-8817.2003.00731.x Ehrlén, 2015, Selection on flowering time in a life-cycle context, Oikos, 124, 92, 10.1111/oik.01473 Engel, 2005, Reproductive phenology of Atlantic forest tree species in Brazil: an eleven year study, Trop. Ecol., 46, 1 Estrada, 2001, Species composition and reproductive phenology of bats in a tropical landscape at Los Tuxtlas, Mexico, J. Trop. Ecol., 17, 627, 10.1017/S026646740100147X Fenner, 1998, The phenology of growth and reproduction in plants, Perspect. Plant Ecol., Evol. Syst., 1, 78, 10.1078/1433-8319-00053 Forrest, 2016, Complex responses of insect phenology to climate change, Curr. Opin. Insect Sci., 17, 49, 10.1016/j.cois.2016.07.002 Fournier, 1974, Un método cuantitativo para la medición de características fenológicas en árboles, Turrialba, 24, 422 Frankie, 1974, Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica, J. Ecol., 62, 881, 10.2307/2258961 Franklin, 1989, Importance and Justification of Long-Term Studies in Ecology, 3 2005 Frenedozo, 2004, Plant reproductive phenology and dispersal patterns after natural regeneration in a limestone mining spoil banks, Braz. Arch. Biol. Technol., 47, 261, 10.1590/S1516-89132004000200014 Gallinat, 2015, Autumn, the neglected season in climate change research, Trends Ecol. Evol., 30, 169, 10.1016/j.tree.2015.01.004 Garwood, 1983, Seed germination in a seasonal tropical forest in Panama: a community study, Ecology, 53, 159 Gautier, 1986, Ritmos de reproducción en el estrato arbóreo del Arborétum Jenaro Herrera (provincia de Requena, departamento de Loreto, Perú). Contribución al estudio de la flora y de la vegetación de la Amazonia peruana. X, Candollea, 41, 193 Genini, 2009, Fruiting phenology of palms and trees in an Atlantic rainforest land-bridge island, Flora, 204, 131, 10.1016/j.flora.2008.01.002 Gill, 2015, Changes in autumn senescence in northern hemisphere deciduous trees: a meta-analysis of autumn phenology studies, Ann. Bot., 116, 875, 10.1093/aob/mcv055 González-Zamora, A. et al., 2014. Contagious deposition of seeds in spider monkeys' sleeping trees limits effective seed dispersal in fragmented landscapes. PLoS One, 9(2), e89346. Gordo, 2010, Impact of climate change on plant phenology in Mediterranean ecosystems, Glob. Chang. Biol., 16, 1082, 10.1111/j.1365-2486.2009.02084.x Griz, 2001, Fruiting phenology and seed dispersal syndromes in caatinga, a tropical dry forest in the northeast of Brazil, J. Trop. Ecol., 17, 303, 10.1017/S0266467401001201 Grossman, 2016, Amazon rainforest to get a growth check, Science, 352, 635, 10.1126/science.352.6286.635 Gupta, 1997, Growth of research literature in scientific specialities. A modelling perspective, Scientometrics, 40, 507, 10.1007/BF02459297 Hanya, 2013, Fruiting and flushing phenology in Asian tropical and temperate forests: implications for primate ecology, Primates, 54, 101, 10.1007/s10329-012-0341-3 Hawes, 2016, Patterns of plant phenology in Amazonian seasonally flooded and unflooded forests, Biotropica, 465, 10.1111/btp.12315 Hemingway, 1999, Sampling effects on food availability estimates: phenological method, sample size, and species composition, Biotropica, 31, 354, 10.1111/j.1744-7429.1999.tb00147.x Hudson, 2010 Hudson, 2011, Wavelet characterization of eucalypt flowering and the influence of climate, Environ. Ecol. Stat., 18, 513, 10.1007/s10651-010-0149-5 Hudson, 2010, Climatic influences on the flowering phenology of four eucalypts: a GAMLSS approach, 209 Ibáñez, 2010, Forecasting phenology under global warming, Philos. Trans. R. Soc., B, 365, 3247, 10.1098/rstb.2010.0120 IPCC, 2013 IPCC, 2014 Janzen, 1967, Synchronization of sexual reproduction of trees within dry season in Central America, Evolution, 21, 620, 10.1111/j.1558-5646.1967.tb03416.x Janzen, 1971, Seed predation by animals, Annu. Rev. Ecol. Syst., 2, 465, 10.1146/annurev.es.02.110171.002341 Jaramillo, 2013, Global warming and neotropical rainforests: a historical perspective, Annu. Rev. Earth Planet. Sci., 41, 741, 10.1146/annurev-earth-042711-105403 Joetzjer, 2013, Present-day and future Amazonian precipitation in global climate models: CMIP5 versus CMIP3, Clim. Dyn., 41, 2921, 10.1007/s00382-012-1644-1 Justiniano, 2000, Phenology of tree species in Bolivian dry forests, Biotropica, 32, 276 Keatley, 2010, Introduction and overview, 1 Keatley, 2012, Detecting change in an Australian flowering record: comparisons of linear regression and cumulative sum analysis change point analysis, Austral Ecology, 37, 825, 10.1111/j.1442-9993.2011.02344.x Kelly, 2002, Mast seeding in perennial plants: why, how, where?, Annu. Rev. Ecol. Syst., 33, 427, 10.1146/annurev.ecolsys.33.020602.095433 Kharin, 2013, Changes in temperature and precipitation extremes in the CMIP5 ensemble, Clim. Chang., 119, 345, 10.1007/s10584-013-0705-8 Kier, 2005, Global patterns of plant diversity and floristic knowledge, J. Biogeogr., 32, 1107, 10.1111/j.1365-2699.2005.01272.x Knowles, 1997, Phenological observations and tree seed characteristics in an equatorial moist forest at trombetas, Para State, Brazil, 67 Kubitzki, 1994, Seed dispersal in flood-plain forests of Amazonia, Biotropica, 26, 30, 10.2307/2389108 Lieth, 1973, 29 Lindenmayer, 2010, The science and application of ecological monitoring, Biol. Conserv., 143, 1317, 10.1016/j.biocon.2010.02.013 Lobo, 2008, Phenology of tree species of the Osa Peninsula and Golfo Dulce region, Costa Rica, 547 Malhi, 2009, Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest, Proc. Natl. Acad. Sci. U. S. A., 106, 20610, 10.1073/pnas.0804619106 Marengo, 2011, Extreme climatic events in the Amazon basin, Theor. Appl. Climatol., 107, 73 Memmott, 2007, Global warming and the disruption of plant-pollinator interactions, Ecol. Lett., 10, 710, 10.1111/j.1461-0248.2007.01061.x Mendoza, 2015, Does masting result in frugivore satiation? A test with Manilkara trees in French Guiana, J. Trop. Ecol., 2015, 553, 10.1017/S0266467415000425 Menzel, 2006, European phenological response to climate change matches the warming pattern, Glob. Chang. Biol., 12, 1969, 10.1111/j.1365-2486.2006.01193.x Metzger, 2013, A high-resolution bioclimate map of the world: a unifying framework for global biodiversity research and monitoring, Glob. Ecol. Biogeogr., 22, 630, 10.1111/geb.12022 Mikich, 2001, Floristic and phenological study of zoochoric species of Semideciduous Seasonal Forest remnants in the mid-west region of Parana State, Brazil, Acta Bot. Bras., 15, 89, 10.1590/S0102-33062001000100010 Miller-Rushing, 2006, Photographs and herbarium specimens as tools to document phenological changes in response to global warming, Am. J. Bot., 93, 1667, 10.3732/ajb.93.11.1667 Morellato, 1996, Reproductive phenology of climbers in a Southeastern Brazilian forest, Biotropica, 28, 180, 10.2307/2389073 Morellato, 2013, South and Central America: Phenology overview and perspectives, 91 Morellato, 2000, Phenology of Atlantic rain forest trees: a comparative study, Biotropica, 32, 811, 10.1111/j.1744-7429.2000.tb00620.x Morellato, 2010, The influence of sampling method, sample size, and frequency of observations on plant phenological patterns and interpretation in tropical forest trees, Phenological Research: Methods for Environmental and Climate Change Analysis, 10.1007/978-90-481-3335-2_5 Morellato, 2016, Linking plant phenology to conservation biology, Biol. Conserv., 195, 60, 10.1016/j.biocon.2015.12.033 Morren, 1849, Le Globe, le Temps et la Vie. Bulletins de l'Académie royale des Sciences, des Lettres et des Beaux-Arts de Belgique, XVI, 660 Myers, 2000, Biodiversity hotspots for conservation priorities, Nature, 403, 853, 10.1038/35002501 Newstrom, 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, 10.2307/2388804 Olson, 2001, Terrestrial ecoregions of the world: a new map of life on earth a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity, Bioscience, 51, 933, 10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2 Opler, 1980, Comparative phenological studies of treelet and shrub species in tropical wet and dry forests in the lowlands of Costa Rica, J. Ecol., 68, 167, 10.2307/2259250 Owens, 1995, Constraints to seed production: temperate and tropical forest trees, Tree Physiol., 15, 477, 10.1093/treephys/15.7-8.477 Palminteri, 2012, Advantages of granivory in seasonal environments: feeding ecology of an arboreal seed predator in Amazonian forests, Oikos, 121, 1896, 10.1111/j.1600-0706.2012.20456.x Parmesan, 2006, Ecological and evolutionary responses to recent climate change, annual review of ecology evolution and systematics, Annu. Rev. Ecol. Evol. Syst., 637, 10.1146/annurev.ecolsys.37.091305.110100 Parmesan, 2007, Influences of species, latitudes and methodologies on estimates of phenological response to global warming, Glob. Chang. Biol., 13, 1860, 10.1111/j.1365-2486.2007.01404.x Parmesan, 2015, Plants and climate change: complexities and surprises, Ann. Bot., 116, 849, 10.1093/aob/mcv169 Parmesan, 2003, A globally coherent fingerprint of climate change impacts across natural systems, Nature, 421, 37, 10.1038/nature01286 Parolin, 2000, Phenology and CO2-assimilation of trees in central Amazonian floodplains, J. Trop. Ecol., 16, 465, 10.1017/S0266467400001516 Pau, 2013, Clouds and temperature drive dynamic changes in tropical flower production, Nat. Clim. Chang., 3, 838, 10.1038/nclimate1934 Peres, 1994, Primate responses to phenological changes in an Amazonian terra-firme forest, Biotropica, 26, 98, 10.2307/2389114 Persson, 2005 Polansky, 2013, Long-term changes in fruit phenology in a west African lowland tropical rain forest are not explained by rainfall, Biotropica, 45, 434, 10.1111/btp.12033 Polansky, 2013, Generalized additive mixed models for disentangling long-term trends, local anomalies, and seasonality in fruit tree phenology, Ecol. Evol., 3, 3141, 10.1002/ece3.707 Primack, 2004, Herbarium specimens demonstrate earlier flowering times in response to warming in Boston, Am. J. Bot., 91, 1260, 10.3732/ajb.91.8.1260 Primack, 2009, Spatial and interspecific variability in phenological responses to warming temperatures, Biol. Conserv., 142, 2569, 10.1016/j.biocon.2009.06.003 Proença, 2012, Phenological predictability index in BRAHMS: a tool for herbarium-based phenological studies, Ecography, 35, 289, 10.1111/j.1600-0587.2011.07329.x Quesada, 2009, Succession and management of tropical dry forests in the Americas: review and new perspectives, For. Ecol. Manag., 258, 1014, 10.1016/j.foreco.2009.06.023 Ragusa-Netto, 2007, Canopy phenology of a dry forest in western Brazil, Braz. J. Biol., 67, 569, 10.1590/S1519-69842007000300024 Rathcke, 1985, Phenological patterns of terrestrial plants, Annu. Rev. Ecol. Syst., 16, 179, 10.1146/annurev.es.16.110185.001143 Regalado, 2010, Brazilian science: riding a gusher, Science, 330, 1306, 10.1126/science.330.6009.1306 Reich, 1995, Phenology of tropical forests — patterns, causes, and consequences, Canadian Journal of Botany-Revue Canadienne De Botanique, 73, 164 Reys, 2005, Fenologia reprodutiva e disponibilidade de frutos de espécies arbóreas em mata ciliar no rio formoso, Mato Grosso do Sul., Biota Neotropica, 5, 10.1590/S1676-06032005000300021 Richardson, 2013, Climate change, phenology, and phenological control of vegetation feedbacks to the climate system, Agric. For. Meteorol., 169, 156, 10.1016/j.agrformet.2012.09.012 Root, 2003, Fingerprints of global warming on wild animals and plants, Nature, 421, 57, 10.1038/nature01333 Rosenzweig, 2008, Attributing physical and biological impacts to anthropogenic climate change, Nature, 453, 353-U20, 10.1038/nature06937 Sabatier, 1985, Saisonnalité et déterminisme du pic de fructification en fôret guyanaise, Revue d'Écologie (Terre et Vie), 40, 289, 10.3406/revec.1985.5286 Sakai, 2001, Phenological diversity in tropical forests, Popul. Ecol., 43, 77, 10.1007/PL00012018 Sánchez-Azofeifa, 2005, Research priorities for neotropical dry forests 1, Biotropica, 37, 477 Santos, 2013, Seasonal variation of consumption of the species used as fruit source by brown howler monkeys (Alouatta clamitans) in southern Brazil, Biol. Neonate, 13, 148 Schleip, 2008, Time series modeling and central European temperature impact assessment of phenological records over the last 250years, J. Geophys. Res. Biogeosci., 113, 10.1029/2007JG000646 Schleip, 2010, 229 Schöngart, 2002, Phenology and stem-growth periodicity of tree species in Amazonian floodplain forests, J. Trop. Ecol., 18, 581, 10.1017/S0266467402002389 Schwartz, 2013, Introduction, 1 Schwartz, 2000, Changes in north American spring, Int. J. Climatol., 20, 929, 10.1002/1097-0088(20000630)20:8<929::AID-JOC557>3.0.CO;2-5 Schwartz, 2006, Onset of spring starting earlier across the northern hemisphere, Glob. Chang. Biol., 12, 343, 10.1111/j.1365-2486.2005.01097.x Snow, 1965, A possible selective factor in evolution of fruiting seasons in tropical forest, Oikos, 15, 274, 10.2307/3565124 Sparks, 2002, Observed changes in seasons: an overview, Int. J. Climatol., 22, 1715, 10.1002/joc.821 Staggemeier, 2011, Reproductive phenology of coastal plain Atlantic forest vegetation: comparisons from seashore to foothills, Int. J. Biometeorol., 55, 843, 10.1007/s00484-011-0482-x Stevenson, 1998, Annual variation in fruiting pattern using two different methods in a lowland tropical forest, Tinigua National Park, Colombia, Biotropica, 30, 129, 10.1111/j.1744-7429.1998.tb00376.x Tannus, 2006, Reproductive phenology in dry and wet grassland in an area of cerrado at southeastern Brazil, Itirapina - SP., Biota Neotropica, 6 Ter Steege, 1991, The phenology of a Guyanese timber species — a compilation of a century of observations, Vegetatio, 95, 177, 10.1007/BF00045216 Ter Steege, 2013, Hyperdominance in the Amazonian tree flora, Science, 342, 10.1126/science.1243092 Terborgh, 1983, The study site: its climate and vegetation, 8 Ting, 2008, Global patterns in fruiting seasons, Glob. Ecol. Biogeogr., 17, 648, 10.1111/j.1466-8238.2008.00408.x van Schaik, 1993, The phenology of tropical forests: adaptive significance and consequences for primary consumers, Annu. Rev. Ecol. Syst., 24, 353, 10.1146/annurev.es.24.110193.002033 Vinkler, 2010 Wallace, 2002, Phenological patterns in a southern Amazonian tropical forest: implications for sustainable management, For. Ecol. Manag., 160, 19, 10.1016/S0378-1127(00)00723-4 Wheelwright, 1986, A seven-year study of individual variation in fruit production in tropical bird-dispersed tree species in the family Lauraceae, 19 Wolkovich, 2012, Warming experiments underpredict plant phenological responses to climate change, Nature, 485, 494, 10.1038/nature11014 Wright, 1995, Phylogenetic patterns among tropical flowering phenologies, J. Ecol., 83, 937, 10.2307/2261176 Wright, 2006, Seasonal, El Niño and longer term changes in flower and seed production in a moist tropical forest, Ecol. Lett., 9, 35 Wright, 1999, The El Niño southern oscillation variable fruit production, and famine in a tropical forest, Ecology, 80, 1632 Xu, 2013, Temperature and vegetation seasonality diminishment over northern lands, Nat. Clim. Chang., 3, 581, 10.1038/nclimate1836 Zalamea, 2011, Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens, Proc. R. Soc. B Biol. Sci., 278, 2437, 10.1098/rspb.2010.2259 Zhang, 1995, Comparison of three fruit census methods in French Guiana, J. Trop. Ecol., 11, 281, 10.1017/S0266467400008750 Zimmerman, 2007, Flowering and fruiting phenologies of seasonal and aseasonal neotropical forests: the role of annual changes in irradiance, J. Trop. Ecol., 23, 231, 10.1017/S0266467406003890