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Climate changes affecting biotic interactions, phenology, and reproductive success in a savanna community over a 10-year period

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Abstract

Climatic parameters are able to influence the timing of phenological events affecting the degree of synchrony among plant species, their interactions, and reproductive success. Shrubs of Malpighiaceae family in the Brazilian Tropical Savanna present sequential flowering phenology. We verified variations in climatic factors (temperature and precipitation) over a period of 10 years (2005–2014) and correlated them with the onset of flowering of four of these Malpighiaceae species. Furthermore, we tested whether the phenological synchronization among species has changed over time affecting the herbivory and fruit set. Herbivory and fruit production were recorded during three reproductive seasons (2008/2009, 2011/2012, 2013/2014). We developed a mathematical model to estimate the flower and fruit production in response to phenological changes for the next 5 years. Results show that climatic factors changed, influencing the onset of species flowering. The degree of overlap among species also changed and the effects on species interactions were species specific. The mathematical model successfully presented a tendency on flower and fruit production contributing to the predictions of the outcomes in response to phenological changes. We confirm the effects of climate changes on plant phenological events and the importance of feature plasticity for better performance of species.

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References

  • Aide TM (1991) Synchronous leaf production and herbivory in juveniles of Gustavia superba. Oecologia 88:511–514

    Article  CAS  PubMed  Google Scholar 

  • Alves-Silva E, Del-Claro K (2013) Effect of post-fire resprouting on leaf fluctuating asymmetry, extrafloral nectar quality, and ant–plant–herbivore interactions. Naturwissenschaften 100:525–532

    Article  CAS  PubMed  Google Scholar 

  • Alves-Silva E, Barônio GJ, Torezan-Silingardi HM, Del-Claro K (2013) Foraging behavior of Brachygastra lecheguana (Hymenoptera: Vespidae) on Banisteriopsis malifolia (Malpighiaceae): Extrafloral nectar consumption and herbivore predation in a tending ant system. Entomol Sci 16:162–169

    Article  Google Scholar 

  • Alves-Silva E, Bachtold A, Barônio GJ, Torezan-Silingardi HM, Del-Claro K (2014) Ant–herbivore interactions in an extrafloral nectaried plant: are ants good plant guards against curculionid beetles? J Nat Hist 49:841–851

    Article  Google Scholar 

  • Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013

    Article  CAS  PubMed  Google Scholar 

  • Anderson WR (1990) The origin of the Malpighiaceae - the evidence from morphology. Mem N Y Bot Gard 64:210–224

    Google Scholar 

  • Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20

    Article  Google Scholar 

  • Beattie AJ, Breedlove DE, Ehrlich PR (1973) The ecology of the pollination and predation of Frasera speciose. Ecology 54:81–91

    Article  Google Scholar 

  • Bishop JG, Schemske DW (1998) Variation in flowering phenology and its consequences for lupines colonizing Mount St Helens. Ecology 79:534–546

    Article  Google Scholar 

  • Bock A, Sparks TH, Estrella N, Jee N, Casebow A, Schunk C, Leuchner M, Menzel A (2014) Changes in first flowering dates and flowering duration of 232 plant species on the island of Guernsey. Glob Change Biol 20:3508–3519

    Article  Google Scholar 

  • Brito AF, Presley SJ, Santos GMM (2012) Temporal and trophic niche overlap in a guild of flower-visiting ants in a seasonal semi-arid tropical environment. J Arid Environ 87:161–167

    Article  Google Scholar 

  • Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615

    Article  CAS  PubMed  Google Scholar 

  • Camargo MBP (2010) The impact of climatic variability and climate change on arabica coffee crop in Brazil. Brag Camp 69:239–247

    Article  Google Scholar 

  • CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. Proc Natl Acad Sci USA 111:4916–4921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardoso FCG, Marques R, Botosso PC, Marques MCM (2012) Stem growth and phenology of two tropical trees in contrasting soil conditions. Plant Soil 354:269–281

    Article  CAS  Google Scholar 

  • Castro-Arellano I, Lacher TE Jr, Willig MR, Rangel TF (2010) Assessment of assemblage-wide temporal-niche segregation using null models. Methods Ecol Evol 1:311–318

    Google Scholar 

  • Chambers LE, Altwegg R, Barbraud C, Barnard P, Beaumont LJ, Crawford RJM et al (2013) Phenological changes in the southern hemisphere. PLoS ONE 8(10):e75514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark DB, Clark DA (1991) Herbivores, herbivory, and plant phenology: patterns and consequences in a tropical rain-forest cycad. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, p 639

    Google Scholar 

  • Claro VTS (2015) Programa CSVM®—INPI—BR 51 2015 000482-4 Revista de Propriedade Industrial, Patentes RPI—DOU, 179

  • Del-Claro K, Marquis RJ (2015) Ant species identity has a greater effect than fire on the outcome of an ant protection system in Brazilian Cerrado. Biotropica 47(4):1–9

    Article  Google Scholar 

  • Del-Claro K, Torezan-Silingardi HM (2012) Ecologia das interações plantas-animais: Uma abordagem ecológico-evolutiva. Technical Books, Rio de Janeiro

    Google Scholar 

  • Del-Claro K, Stefani V, Lange D, Vilela AA, Nahas L, Velasques M, Torezan-Silingardi HM (2013) The importance of natural history studies for a better comprehension of animal-plant interactions networks. Biosci J 29:439–448

    Google Scholar 

  • Del-Claro K, Rico-Gray V, Torezan-Silingardi HM, Aalves-Silva E, Fagundes R, Lange D, Dátillo W, Vilela AA, Aguirre A, Rodriguez-Morales D (2016) Loss and gains in ant–plant interactions mediated by extrafloral nectar: fidelity, cheats, and lies. Insect Soc 63:207–221

    Article  Google Scholar 

  • Diez JM, Ibanez I, Miller-Rushing AJ, Mazer SJ, Crimmins TM, Crimmins MA, Bertelsen CD, Inouye DW (2012) Forecasting phenology: from species variability to community patterns. Ecol Lett 15:545–553

    Article  PubMed  Google Scholar 

  • Domınguez CA, Dirzo R (1995) Rainfall and flowering synchrony in a tropical shrub: variable selection on the flowering time of Erythroxylum havanense. Evol Ecol 9:204–216

    Article  Google Scholar 

  • Encinas-Viso F, Revilla TA, Etienne RS (2012) Phenology drives mutualistic network structure and diversity. Ecol Lett 15:198–208

    Article  PubMed  Google Scholar 

  • English-Loeb GM, Karban R (1992) Consequences of variation in flowering phenology for seed head herbivory and reproductive success in Erigeron glaucus (Compositae). Oecologia 89:588–595

    Article  PubMed  Google Scholar 

  • Fabina NS, Abbot KC, Gilman RT (2010) Sensitivity of plant - pollinator-herbivore communities to changes in phenology. Ecol Modell 221:453–458

    Article  Google Scholar 

  • Feinsinger P, Spears EE, Poole RW (1981) A simple measure of niche breadth. Ecology 62:27–32

    Article  Google Scholar 

  • Ferreira CA, Torezan Silingardi HM (2013) Implications of the floral herbivory on Malpighiaceae plant fitness: visual aspect of the flower affects the attractiveness to pollinators. Sociobiology 60:323–328

    Article  Google Scholar 

  • Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491

    Article  Google Scholar 

  • Forrest JRK, Inouye DW, Thomson JD (2010) Flowering phenology in subalpine meadows: does climate variation influence community co-flowering patterns? Ecology 91:431–440

    Article  PubMed  Google Scholar 

  • Franks PJ, Adams MA, Amthor JS, Barbour MM, Berry JA, Ellsworth DS, Farquhar GD, Ghannoum O, Lloyd J, McDowell N, Norby RJ (2013) Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. New Phytol 197:1077–1094

    Article  CAS  PubMed  Google Scholar 

  • Gates B (1982) Banisteriopsis, Diplopterys (Malpighiaceae). Fl Neotrop Monogr 30:1–236

    Google Scholar 

  • Gilman RT, Fabina NS, Abbott KC, Rafferty NE (2012) Evolution of plant-pollinator mutualisms in response to climate change. Evol Appl 5:2–16

    Article  PubMed  Google Scholar 

  • Gross CL, Mackay DA, Whalen MA (2000) Aggregated flowering phenologies among three sympatric legumes: the degree of non-randomness and the effect of overlap on fruit set. Plant Ecol 148:13–21

    Article  Google Scholar 

  • Hegland SJ, Nielsen A, Lazaro A, Bjerknes AL, Totland O (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195

    Article  PubMed  Google Scholar 

  • Herrera CM, Medrano M, Rey PJ, Sanchez-Lafuente M, Garcia MB, Guitian J, Manzaneda AJ (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proc Natl Acad Sci USA 99:16823–16828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoogenboom, G, JW Jones, PW Wilkens, CH Porter, KJ Boote, LA Hunt, U Singh, JI Lizaso, JW White, O Uryasev, R Ogoshi, J Koo, V Shelia, GY Tsuji (2015) Decision Support System for Agrotechnology Transfer (DSSAT) Version 46 (http://dssat.net) DSSAT Foundation, Prosser, Washington

  • Hoye TT, Forchhammer MC (2008) Phenology of high-Arctic arthropods: effects of climate on spatial, seasonal and inter-annual variation. Adv Ecol Res 40:299–324

    Article  Google Scholar 

  • Hunter AF, Elkinton JS (2000) Effects of synchrony with host plant on populations of a spring-feeding Lepidopteran. Ecology 81:1248–1261

    Article  Google Scholar 

  • Johnson SD, Burgoyne PM, Harder LD, Dötterl S (2011) Mammal pollinators lured by the scent of a parasitic plant. Proc R Soc Lond B 278:2303–2310

    Article  CAS  Google Scholar 

  • Jones JW, Hoogenboom G, Porter CH, Boote KJ, Batchelor WD, Hunt LA, Wilkens PW, Singh U, Gijsman AJ, Ritchie JT (2003) DSSAT Cropping System. Model Eur J Agron 18:235–265

    Article  Google Scholar 

  • Kaiser-Bunbury CN, Traveset A, Hansen DM (2010) Conservation and restoration of plant-animal mutualisms on oceanic islands Perspect. Plant Ecol 12:131–143

    Google Scholar 

  • Kawagoe T, Kudoh H (2010) Escape from floral herbivory by early flowering in Arabidopsis halleri subsp gemmifera. Oecologia 164:713–720

    Article  PubMed  Google Scholar 

  • Lamarre GPA, Mendoza I, Fine PVA, Baraloto C (2014) Leaf synchrony and insect herbivory among tropical tree habitat specialists. Plant Ecol 215:209–220

    Article  Google Scholar 

  • Lange D, Del-Claro K (2014) Ant-plant interaction in a tropical savanna: may the network structure vary over time and influence on the outcomes of associations? PLoS ONE 9(8):e105574

    Article  PubMed  PubMed Central  Google Scholar 

  • Lazaro A, Lundgren R, Totland O (2009) Co-flowering neighbors influence the diversity and identity of pollinator groups visiting plant species. Oikos 118:691–702

    Article  Google Scholar 

  • Liu Y, Reich PB, Li G, Sun S (2011) Shifting phenology and abundance under experimental warming alters trophic relationships and plant reproductive capacity. Ecology 92:1201–1207

    Article  PubMed  Google Scholar 

  • Liuth HS, Talora DC, Amorim AM (2013) Phenological synchrony and seasonality of understory Rubiaceae in the Atlantic Forest, Bahia, Brazil. Acta Bot Bras 27:195–204

    Article  Google Scholar 

  • Lobato FS, Steffen V (2007) Engineering system design with multi-objective differential evolution. Proc COBEM 19:1–10

    Google Scholar 

  • Lobato FS, Steffen V (2008) Otimização multi-objetivo para o projeto de sistemas de engenharia Doc Thesis Universidade Federal de Uberlândia

  • Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717

    Article  PubMed  Google Scholar 

  • Mendes FN, Rêgo MMC, Albuquerque PMC (2011) Phenology and reproductive biology of two species of Byrsonima Rich. Biota Neotrop 11:104–115

    Google Scholar 

  • Miller-Rushing AJ, Hoye TT, Inouye DW, Post ES (2010) The effects of phenological mismatches on demography. Philos Trans 365:3177–3186

    Article  Google Scholar 

  • Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD (2009) Ecology and evolution of plant-pollinator interactions. Ann Bot 103:1355–1363

    Article  PubMed  PubMed Central  Google Scholar 

  • Moeller DA (2006) Geographic structure of pollinator communities, reproductive assurance, and the evolution of self-pollination. Ecology 87(6):1510–1522

    Article  PubMed  Google Scholar 

  • Moreira VSS, Del-Claro K (2005) The outcomes of an ant–treehopper association on Solanum lycocarpum St Hill: increased membracid fecundity and reduced damage by chewing herbivores. Neotrop Entomol 34:881–887

    Article  Google Scholar 

  • Morellato LPC, Talora DC, Takahasi A, Bencke CSC, Romera EC, Zipparro V (2000) Phenology of atlantic rain forest trees: a comparative study. Biotropica 32:811–823

    Article  Google Scholar 

  • Morellato LPC, Alberti LF, Hudson IL (2010) Applications of circular statistics in plant phenology: a case studies approach. In: Keatley M, Hudson IL (eds) Phenological research: methods for environmental and climate change analysis. Springer, New York, pp 357–371

    Google Scholar 

  • Morellato LPC, Camargo MGG, Gressler E (2013) A review of plant phenology in South and Central America. In: Schwartz MD (ed) Phenology: an integrative environmental science. Springer, Heidelberg, pp 91–113

    Chapter  Google Scholar 

  • Muchhala N, Thomson JD (2012) Interspecific competition in pollination systems: costs to male fitness via pollen misplacement. Funct Ecol 26:476–482

    Article  Google Scholar 

  • Munhoz CBR, Felfili JM (2005) Fenologia do estrato herbáceo-subarbustivo de uma comunidade de campo sujo na Fazenda Água Limpa no Distrito Federal, Brasil. Acta Bot Bras 19:981–990

    Article  Google Scholar 

  • Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado Biome. In: Marquis RJ, Oliveira PS (eds) The Cerrados of Brazil PS. Ecology and Natural History of a Neotropical Savanna Columbia University, New York, pp 91–120

    Chapter  Google Scholar 

  • Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol Syst 4:53–74

    Article  Google Scholar 

  • Pilson D (2000) Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus. Oecologia 122:72–82

    Article  CAS  PubMed  Google Scholar 

  • Porter JR, Jamieson PD, Wilson DR (1993) A comparison of the wheat simulation models AFRCWHEAT2, CERES-wheat and SWHEAT for nonlimiting conditions of growth. Field Crop Res 33:131–157

    Article  Google Scholar 

  • Rafferty NE, Ives AR (2011) Effects of experimental shifts in flowering phenology on plant -pollinator interactions. Ecol Lett 14:69–74

    Article  PubMed  Google Scholar 

  • Rafferty NE, Ives AR (2012) Pollinator effectiveness varies with experimental shifts in flowering time. Ecology 93:803–814

    Article  PubMed  PubMed Central  Google Scholar 

  • Rafferty NE, CaraDonna PJ, Burkle LA, Iler AM, Bronstein JL (2013) Phenological overlap of interacting species in a changing climate: an assessment of available approaches. Ecol Evol 3:3183–3193

    Article  PubMed  PubMed Central  Google Scholar 

  • Rafferty NE, CaraDonna PJ, Bronstein JL (2015) Phenological shifts and the fate of mutualisms. Oikos 124:14–21

    Article  PubMed  Google Scholar 

  • Réu WF, Del-Claro K (2005) Natural history and biology of Chlamisus minax Lacordaire (Chrysomelidae: Chlamisinae). Neotrop Entomol 34:357–362

    Article  Google Scholar 

  • Robertson C (1895) The philosophy of flower seasons and the phenological relations of the entomophilous flora and the anthophilous insect fauna. Am Nat 29:97–117

    Article  Google Scholar 

  • Runquist RB, Stanton ML (2013) Asymmetric and frequency-dependent pollinator-mediated interactions may influence competitive displacement in two vernal pool plants. Ecol Lett 16:183–190

    Article  PubMed  Google Scholar 

  • Staggemeier VG, Morellato LPC (2011) Reproductive phenology of coastal plain Atlantic forest vegetation: comparisons from seashore to foothills. Int J Biometeorol 55:843–854

    Article  PubMed  Google Scholar 

  • Staggemeier VG, Diniz-Filho JAF, Morellato LPC (2010) The shared influence of phylogeny and ecology on the reproductive patterns of Myrteae (Myrtaceae). J Ecol 98:1409–1421

    Article  Google Scholar 

  • Takakura K, Nishida T, Matsumoto T, Nishida S (2009) Alien dandelion reduces the seed-set of a native congener through frequency-dependent and one-sided effects. Biol Inv 11:973–981

    Article  Google Scholar 

  • Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Phil Trans R Soc B 365:3187–3199

    Article  PubMed  PubMed Central  Google Scholar 

  • Torezan-Silingardi HM (2007) A influência dos herbívoros florais, dos polinizadores e das características fenológicas sobre a frutificação das espécies da família Malpighiaceae em um cerrado de Minas Gerais Doc Thesis. Universidade de São Paulo

  • Torezan-Silingardi HM (2011) Predatory behavior of Pachodynerus brevithorax (Hymenoptera: Vespidae, Eumeninae) on endophytic herbivore beetles in the Brazilian Tropical Savanna. Sociobiology 57:181–189

    Google Scholar 

  • Torezan-Silingardi HM, Oliveira PEAM (2004) Phenology and reproductive ecology of Myrcia rostrata and M. tomentosa (Myrtaceae) in Central Brazil. Phyton 44:23–44

    Google Scholar 

  • Torres C, Galetto L (2011) Flowering phenology of co-occurring Asteraceae: a matter of climate, ecological interactions, plant attributes or of evolutionary relationships among species? Org Divers Evol 11:9–19

    Article  Google Scholar 

  • Van Asch M, Van Tienderen PH, Holleman LJM, Visser ME (2007) Predicting adaptation of phenology in response to climate change, an insect herbivore example. Glob Change Biol 13:1596–1604

    Article  Google Scholar 

  • Van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377

    Article  Google Scholar 

  • Vanderplaats GN (2005) Numerical optimization techniques for engineering design. Vanderplaats Research and Development Inc, Colorado Springs

    Google Scholar 

  • Velasque M, Del-Claro K (2016) Host plant phenology may determine the abundance of an ecosystem engineering herbivore in a tropical savanna. Ecol Entomol 41:421–430

    Article  Google Scholar 

  • Vilela AA, Torezan-Silingardi HM, Del-Claro K (2014) Conditional outcomes in ant-plant-herbivore interactions influenced by sequential flowering. Flora 209:359–366

    Article  Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall International Editions, New Jersey

    Google Scholar 

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Acknowledgements

We thank the three anonymous reviewers for reviewing the manuscript. We also thank CNPq and FAPEMIG for funding this research (KDC/HMTS/VTSDC) and FAPEMIG for awarding fellowships to AAV.

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Correspondence to Kleber Del-Claro.

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Handling Editor: Heikki Hokkanen.

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Supplementary material 1 (AVI 57599 kb)

AVI movie produced in CSVM program (Claro 2015) showing the influence of climatic parameters in real field data of leaf, bud, flower, and fruit production over 3 years to the Brazilian savanna Malpighiaceae: Banisteriopsis laevifolia, Peixotoa tomentosa, Banisteriopsis malifolia and Banisteriopsis campestris

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Vilela, A.A., Del Claro, V.T.S., Torezan-Silingardi, H.M. et al. Climate changes affecting biotic interactions, phenology, and reproductive success in a savanna community over a 10-year period. Arthropod-Plant Interactions 12, 215–227 (2018). https://doi.org/10.1007/s11829-017-9572-y

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