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Increased atmospheric CO2 combined with local climatic variation affects phenolics and spider mite populations in coffee trees

Abstract

Modelling studies on climate change predict continuous increases in atmospheric carbon dioxide concentration [CO2] and increase in temperature. This may alter carbon-based phytochemicals such phenolics and modify plant interactions with herbivorous. We investigated the effects of enhanced [CO2] and local climatic variation on young coffee plants, Coffea arabica L. cv Catuaí vermelho IAC-144 and Obatã vermelho IAC-1669-20, cultivated in the FACE (Free-Air Carbon Dioxide Enrichment) facility under two atmospheric [CO2] conditions. Coffee leaves were evaluated for total soluble phenolics (TSP), chlorogenic (5-CQA) and caffeic (CAF) acids, diversity and population size of mites, along two dry and two rainy seasons. Elevated atmospheric CO2 (e[CO2]) significantly decreased 5-CQA in cv. Catuaí but did not affect cv. Obatã. Species richness and population size of mites in coffee leaves were not affected by e[CO2] but were strongly related to the seasonal variability of coffee leaf phenolics. In general, high levels of phenolics were negatively correlated with population size while the mite species richness were negatively correlated with 5-CQA and TSP levels. Our findings show that [CO2] enhancement affects phenolics in coffee plants differentially by cultivars, however seasonality is the key determinant of phenolics composition, mite species richness and population size.

Key words
Coffea arabica; climate change; free-air CO2 enrichment (FACE); chlorogenic and caffeic acids; total phenolics; mites

INTRODUCTION

Agricultural production faces the challenge to produce more food while constrained by a number of biotic and abiotic factors. Elevated atmospheric CO2 (e[CO2]) and temperature are altering the interactions between plants and insects with important implications for food security and natural ecosystems (DeLucia et al. 2012DELUCIA EH, NABITY PD, ZAVALA JA & BERENBAUM MR. 2012. Climate change: resetting plant-insect interactions. Plant Physiol 160: 1677-1685.). The [CO2] is estimated to continually increase from current the level of 400 ppm to between 750 and 1,300 ppm by the end of this century (IPCC 2014IPCC. 2014. Proceedings of the 5th assessment report, WGII, climate change 2014: impacts, adaptation, and vulnerability. Cambridge University Press, Cambridge, UK.). The global mean surface air temperature is predicted to increase about 1.7–6.7 °C by the end of the 21st century in South America (Magrin et al. 2014MAGRIN GO, MARENGO JA, BOULANGER J-P, BUCKERIDGE MS, CASTELLANOS E, POVEDA G, SCARANO FR & VICUÑA S. 2014. Central and South America. In: Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, p. 1499-1566.). Although [CO2] effects have been shown to be important for economic and food security impacts of climate change, no models currently account for all the interactions of [CO2] with temperature, crop species, water status, and nitrogen availability, but these interrelationships are of similar importance as regional differences in climate effects and should be included in models (McGrath & Lobell 2013MCGRATH JM & LOBELL DB. 2013. Regional disparities in the CO2 fertilization effect and implications for crop yield. Environ Res Lett 8: 1-9.). Thus, even though global [CO2] is increasing roughly uniformly, regional yield response to increased [CO2] will vary due to differences in climate and the mixture of crops.

About three decades ago, free-air CO2 enrichment (FACE) technology was developed that enabled the air above open-field plots to be enriched with CO2 for entire growing seasons; since then an enormous amount has been learned about how plants respond to the projected future levels of [CO2] (Kimball 2016KIMBALL BA. 2016. Plant responses to elevated CO2 and interactions with H2O, N, and temperature. Curr Opin Plant Biol 31: 36-43.). Elevated [CO2] generally increases leaf mass per area, photosynthetic rate, foliar C/N ratio, and plant growth and yield (Ainsworth & Long 2005Ainsworth EA & Long SP. 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165: 351-371., Zhang et al. 2017ZHANG S, FU W, ZHANG Z, FAN Y & LIU T. 2017. Effects of elevated CO2 concentration and temperature on some physiological characteristics of cotton (Gossypium hirsutum L.) leaves. Environ Exp Bot 133: 108-117.). Moreover, [CO2] enhancement can lead to reallocation of carbon and nitrogen resources among plant organs, and change the secondary metabolites content of plant tissues (Salazar-Parra et al. 2015SALAZAR-PARRA C, ARANJUELO I, PASCUAL I, ERICE G, SANZ-SAÉS Á, AGUIRREOLEA J, SÁNCHEZ-DIÁZ M, IRIGOYEN JJ, ARAUS JL & MORALES F. 2015. Carbon balance, partitioning and photosynthetic acclimation in fruit-bearing grapevine (Vitis vinifera L. cv. Tempranillo) grown under simulated climate change (elevated CO2, elevated temperature and moderate drought) scenarios in temperature gradient greenhouses. J Plant Physiol 174: 97-109.). These changes in primary and secondary metabolite under elevated [CO2] may lead to reduction in leaf damage by herbivores and their performance (Valkama et al. 2007VALKAMA E, KORICHEVA J & OKSANEN E. 2007. Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob Chang Biol 13: 184-201.). However, in combination with elevated temperature, elevated [CO2] decreases nitrogen content, thus lowering plant nutritional value (Saha et al. 2015SAHA S, SEHGAL VK, CHAKRABORTY D & PAL M. 2015. Atmospheric carbon dioxide enrichment induced modifications in canopy radiation utilization, growth and yield of chickpea (Cicer arietinum L.). Agric For Meteorology 202: 102-111., Zhang et al. 2017ZHANG S, FU W, ZHANG Z, FAN Y & LIU T. 2017. Effects of elevated CO2 concentration and temperature on some physiological characteristics of cotton (Gossypium hirsutum L.) leaves. Environ Exp Bot 133: 108-117.) and causing increased leaf consumption by herbivores to meet their nutritional needs (DeLucia et al. 2012DELUCIA EH, NABITY PD, ZAVALA JA & BERENBAUM MR. 2012. Climate change: resetting plant-insect interactions. Plant Physiol 160: 1677-1685.). Part of the extra carbon assimilated as consequence of increased photosynthesis under CO2-enriched atmospheric conditions is directed to the synthesis of phenolic compounds. These effects of elevated CO2 on the concentration of phenolic compounds vary depending on the level and duration of exposure (Valkama et al. 2007VALKAMA E, KORICHEVA J & OKSANEN E. 2007. Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob Chang Biol 13: 184-201.) besides the management conditions, environmental factors and genetics also play a role (Ahmed et al. 2014AHMED s ET AL. 2014. Effects of extreme climate events on tea (Camellia sinensis) functional quality validate indigenous farmer knowledge and sensory preferences in tropical China. PLoS ONE 9(10): e109126. Online Publication.). Phenolics can potentially be influenced by changes in carbon inputs (Johnson & Pregitzer 2007JOHNSON RM & PREGITZER KS. 2007. Concentration of sugars, phenolic acids, and amino acids in forest soils exposed to elevated atmospheric CO2 and O3. Soil Biol Biochem 39: 3159-3166.), and elevated CO2 may influence the chemical pathways that regulate gene expression and synthesis of secondary compounds (Lindroth 2010LINDROTH RL. 2010. Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36: 2-21.). The shikimic acid pathway, known to produce phenolic compounds in trees, was found to be the most influenced pathway by CO2 treatment (Lindroth 2010LINDROTH RL. 2010. Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36: 2-21., Kim et al. 2015KIM K, LABBÉ N, WARREN JM, ELDER T & RIALS TG. 2015. Chemical and anatomical changes in Liquidambar styraciflua L. xylem after long term exposure to elevated CO2. Environ Pollut 198: 179-185.). Most of the studies on the effects of e[CO2] have focused on the biochemical composition of plants, and very few studies have been carried out about the effects of e[CO2] on insect–host plant interactions (Zavala et al. 2013ZAVALA JA, NABITY PD & DELUCIA EH. 2013. An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Ann Rev Entomol 58: 79-97., Sharma et al. 2016SHARMA HC, WAR AR, PATHANIA M, SHARMA SP, AKBAR SM & MUNGHATE RS. 2016. Elevated CO2 influences host plant defense response in chickpea against Helicoverpa armigera. Arthropod Plant Interact 10: 171-181.). In general, phenolics are involved in the response to biotic and abiotic stresses mainly due to their antioxidant properties. In this way, they may play a role in adaptation to environmental change and in coevolution with pests and diseases (McElrone et al. 2010MCELRONE AJ, HAMILTON JG, KRAFNICK AJ, ALDEA M, KNEPP RG & DELUCIA EH. 2010. Combined effects of elevated CO2 and natural climatic variation on leaf spot diseases of redbud and sweetgum trees. Environ Pollut 158: 108-114., Campa et al. 2012CAMPA C, MONDOLOT L, RAKOTONDRAVAO A, BIDEL LPR, GARGADENNEC A, COUTURON E, LA FISCA P, RAKOTOMALALA J-J, JAY-ALLEMAND C & DAVIS AP. 2012. A survey of magiferin and hydroxycinnamic acid ester accumulation in coffee (Coffea) leaves: biological implications and uses. Ann Bot 110: 595-613.). Consequently, phenolics could be critical to understanding plant–animal interactions which are important in predicting the effects of climate change on expression and stability of host plant resistance to pest attack (Sharma et al. 2016SHARMA HC, WAR AR, PATHANIA M, SHARMA SP, AKBAR SM & MUNGHATE RS. 2016. Elevated CO2 influences host plant defense response in chickpea against Helicoverpa armigera. Arthropod Plant Interact 10: 171-181.).

High contents of natural phenolic acids and flavonoids are found in green tea, fruits, and vegetables, while lower concentrations of phenolics exist in coffee (Ghasemzadeh et al. 2010GHASEMZADEH A, JAAFAR HZE & RAHMAT A. 2010. Elevated carbon dioxide increases contents of flavonoids and phenolic compounds, and antioxidant activities in Malaysian young ginger (Zingiber officinale Roscoe.) varieties. Molecules 15: 7907-7922.). Coffee is popular worldwide. The beverage production is mainly based on two plant species, Coffea arabica and Coffea canephora, also known as arabica and robusta coffees, respectively, which are cultivated in different countries around the world. Coffee is attractive for health benefits due to its antioxidant properties (Iwai et al. 2004IWAI K, KISHIMOTO N, KAKINO Y, MOCHIDA K & FUJITA T. 2004. In vitro antioxidant effects and tyrosinase inhibitory activities of seven hydroxycinnamoyl derivatives in green coffee beans. J Agric Food Chem 52: 4893-4898., Sato et al. 2011SATO Y, ITAGAKI S, KUROKAWA T, OGURA J, KOBAYASHI M, HIRANO T, SUGAWARA M & ISEKI K. 2011. In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. Int J Pharm 403: 136-138., Tajik et al. 2017TAJIK N, TAJIK M, MACK I & ENCK P. 2017. The potential effects of chlorogenic acid, the main phenolic components in coffee, on health: a comprehensive review of the literature. Eur J Nutr, published online: 08 February.). Phenolic compounds, as major sources of antioxidant activity in coffee beans and have been receiving considerable attention as potentially protective factors against human chronic degenerative diseases, such as cancer and cardiovascular disease (Somporn et al. 2012SOMPORN C, KAMTUO A, THEERAKULPISUT P & SIRIAMORNPUN S. 2012. Effect of shading on yield, sugar content, phenolic acids and antioxidant property of coffee beans (Coffea Arabica L. cv. Catimor) harvested from north-eastern Thailand. J Sci Food Agric 92: 1956-1963., Ludwig et al. 2014LUDWIG I, CLIFFORD M, LEAN M, ASHIHARA H & CROZIER A. 2014. Coffee: Biochemistry and potential impact on health. Food Funct 5: 1695-1717.). In coffee, phenolic compounds are present predominantly as a family of esters formed between certain hydroxycinnamic acids (caffeic acid, ferulic and p-coumaric) and quinic acid, collectively known as chlorogenic acids found in high concentrations in green coffee seeds (Clifford 2000CLIFFORD MN. 2000. Chlorogenic acids and other cinnamates – Nature, occurrence, dietary burden, absorption and metabolism. J Sci Food Agric 80: 1033-1043.). The best-known conjugate is 5-caffeoylquinic acid, 5-CQA, commonly referred to as chlorogenic acid (CGA), which is naturally found in coffee leaves, as the caffeic acid. Chlorogenic acids have a marked influence in determining coffee quality and play an important role in formation of coffee flavor (Farah & Donangelo 2006FARAH A & DONANGELO CM. 2006. Phenolic compounds in coffee. Braz J Plant Physiol 18: 23-36., Somporn et al. 2012SOMPORN C, KAMTUO A, THEERAKULPISUT P & SIRIAMORNPUN S. 2012. Effect of shading on yield, sugar content, phenolic acids and antioxidant property of coffee beans (Coffea Arabica L. cv. Catimor) harvested from north-eastern Thailand. J Sci Food Agric 92: 1956-1963., Clemente et al. 2015CLEMENTE JM, MARTINEZ HEP, ALVES LC, FINGER FL & CECON PR. 2015. Effects of nitrogen and postassium on the chemical composition of coffee beans and on beverage quality. Acta Sci 37(3): 297-305.).

In contrast to the considerable amount of research on coffee green beans, there are relatively few studies concerned with the metabolite content of the other parts of coffee plant, such as leaves (Campa et al. 2012CAMPA C, MONDOLOT L, RAKOTONDRAVAO A, BIDEL LPR, GARGADENNEC A, COUTURON E, LA FISCA P, RAKOTOMALALA J-J, JAY-ALLEMAND C & DAVIS AP. 2012. A survey of magiferin and hydroxycinnamic acid ester accumulation in coffee (Coffea) leaves: biological implications and uses. Ann Bot 110: 595-613.). For example, the activity of some pathogens has been limited when phenolic compounds are expressed in some coffee leaves showing higher resistance to the leaf miner Leucoptera coffeella, Guérin-Méneville (Lepidoptera: Lyonetiidae) a serious coffee pest (Magalhães et al. 2010MAGALHÃES ST, FERNANDES FL, DEMUNER AJ, PICANÇO MC & GUEDES RNC. 2010. Leaf alkaloids, phenolics, and coffee resistance to the leaf miner Leucoptera coffeella (Lepidoptera: Lyonetiidae). J Econ Entomol 103: 1438-1443.). Also Silva et al. (2006)SILVA M DO C, VÁRZEA V, GUERRA-GUIMARÃES L, AZINHEIRA HG, FERNANDEZ D, PETITOT A-S, BERTRAND B, LASHERMES P & NICOLE M. 2006. Coffee resistance to the main diseases: leaf rust and coffee berry disease. Braz J Plant Physiol 18: 119-147. described early accumulation of phenolic compounds in coffee associated with resistance to coffee rust disease caused by the fungus Hemileia vastatrix Berkeley & Broome (Uredinales).

Phytophagous mites are considered one of the most important pests causing significant damage to coffee plants in Brazil. Tetranychidae, Tenuipalpidae and Tarsonemidae families of mites are the key arthropod pests in coffee orchards, while the coffee red mite, Oligonychus ilicis (McGregor) (Acari: Tetranychidae) and the false spider mite Brevipalpus sp. (Acari: Tenuipalpidae), the latter as vector of the Coffee Ringspot Virus (CRV), are among the most important pests of the crop present in the main coffee producing areas in Brazil (Ajila et al. 2018AJILA HEV, FERREIRA JA, COLARES F, OLIVEIRA CM, BERNARDO AMG, VENZON M & PALLINI A. 2018. Ricoseius loxocheles (Acari: Phytoseiidae) is not a predator of false spider mite on coffee crops: What does it eat? Exp Appl Acarol 74: 1-11.). The coffee red spider mite O. ilicis is considered a key coffee pest in many producing countries because it feeds on the upper leaf surface, causing reduction of photosynthesis rate and premature leaf drop as a consequence of infestation (Teodoro et al. 2009TEODORO A, KLEIN AM, REIS PR & TSCHARNTKE T. 2009. Agroforestry management affects coffee pests contingent on season and developmental stage. Agr Forest Entomol 11: 295-300.). The Phytoseiidae, predatory mites, is widely and commonly found in a range of different coffee management systems (Mineiro et al. 2008MINEIRO JLC, SATO ME, RAGA A & ARTHUR V. 2008. Population dynamics of phytophagous and predaceous mites on coffee in Brazil, with emphasis on Brevipalpus phoenicis (Acari: Tenuipalpidae). Exp Appl Acarol 44: 277-291., Teodoro et al. 2009TEODORO A, KLEIN AM, REIS PR & TSCHARNTKE T. 2009. Agroforestry management affects coffee pests contingent on season and developmental stage. Agr Forest Entomol 11: 295-300., Peixoto et al. 2017PEIXOTO ML, FERNANDES LG, CARVALHO MAC, OLIVEIRA MLD, PUTTI FF & REIS ARD. 2017. Assessment of mite fauna in different coffee cropping systems in Brazil. Biocontrol Sci Technol 27: 424-432.). Phytoseiid mites (Acari: Phytoseiidae) are efficient predators of phytophagous mites and are considered the most efficient natural enemies for biological control of pest mites (Reis et al. 2008REIS PR, ZACARIAS M, SILVA R & MARAFELI P. 2008. Manejo de ácaros em cafeeiro. In: Manejo fitossanitário da cultura do cafeeiro, Fernandes LHM (Org). Brasília: Sociedade Brasileira de Fitopatologia, 2008, p. 173-184., Toledo et al. 2013TOLEDO MA, REIS PR, DA SILVEIRA EC, MARAFELI P DE P & DE SOUZA-PIMENTEL GC. 2013. Predatory potential of Euseius alatus (Phytoseiidae) on different life stages of Oligonychus ilicis (Tetranychidae) on coffee leaves under laboratory conditions. Neotrop Entomol 42: 185-190. ). The regular occurrence of pests including mite populations, year after year, reduces productivity and the quality of coffee and is known that the coffee management production interferes on mite population, being that more sustainable systems of production present smaller abundance of mites (Peixoto et al. 2017PEIXOTO ML, FERNANDES LG, CARVALHO MAC, OLIVEIRA MLD, PUTTI FF & REIS ARD. 2017. Assessment of mite fauna in different coffee cropping systems in Brazil. Biocontrol Sci Technol 27: 424-432.). However, the relationship between mites and coffee plants in a high CO2 environments has not been investigated.

Thus, considering the importance of the coffee production and the lack of knowledge about the effects of e[CO2] in coffee leaf phenolics and its correlation with mite populations, the purpose of this work was to assess whether [CO2] combined with local climate variability affects the leaf levels of coffee phenolic compounds and, consequently, the mite populations. For this, two coffee cultivars (Coffea arabica cv. Catuaí Vermelho IAC 144 and cv. Obatã IAC 1669–20) were cultivated under ambient or elevated [CO2] (390 and 550 ppm respectively) in free-air CO2 enrichment (FACE) during two rainy and two dry seasons. The levels of total soluble phenols, chlorogenic and caffeic acids were assessed in mature coffee leaves and the relationship between those compounds and the abundance and diversity of mites was quantified. Our hypothesis were: (1) elevated [CO2] increases phenolic compounds in coffee leaves reducing mite populations; (2) local climatic variability combined with different [CO2] treatments can change the levels of phenolic compounds modifying mite diversity and abundance in coffee leaves.

MATERIALS AND METHODS

Site description, CO2 treatments, plant materials, and samplings

We carried out the experiment using the ClimapestFACE facility located in Jaguariúna municipality (22°43’10”S 47°01’16”W, 615 m above sea level), southeastern Brazil. The soil at the experimental area is a typical dystroferric red latosol. The climate is humid subtropical, a Cfa type according to the Köppen classification, with hot rainy summers and cold dry winters. Maximum and minimum mean monthly air temperature and precipitation were recorded during the experiment. To mimic coffee agroecosystems, the FACE system increased the ambient [CO2] in six 10 m diameter ring plots (elevated CO2) within a continuous 7 ha coffee field. Six additional 10 m diameter ring plots served as controls, i.e. were left under ambient [CO2] conditions. Elevated and ambient-CO2 plots were at least 70 m apart to minimize cross-plot contamination. Fumigation with CO2 began on 25 August 2011. The average [CO2] at the beginning of the experiment was approximately 390 μmol mol–1. The performance of the FACE system was adjusted so that the [CO2] as measured at the centre of the ring achieved target levels of 550 μmol mol–1 of air. The plots were not enriched with CO2 at night. Further details regarding the experimental site set-up and CO2 control performance can be found in Ghini et al. (2015)GHINI R, TORRE-NETO A, DENTZIEN AFM, GUERREIRO-FILHO O, IOST R, PATRÍCIO FRA, PRADO JSM, THOMAZIELLO RA & BETTIOL W. 2015. Coffee growth, pest and yield responses to free-air CO2 enrichment. Climatic Change 132: 307-320.. Monthly the minimum and maximum mean of air temperature and precipitation were recorded during the experiment. Two coffee (Coffea arabica L.) cultivars, cv. Catuaí Vermelho IAC 144 and cv. Obata IAC 1669-20, were assessed. Plantlets with three to four pairs of leaves were transplanted into the plots in March 2011. The cultivars were interspersed in rows that were 1.75 m apart, with 0.60 m between plants in the rows. The plants were submitted to routine agricultural practices for commercial coffee bean production, including applications of fungicides and insecticides. Each tree was fertilized annually with 46 g of N, 9 g of P and 23 g of K plus micronutrients. The crop was grown without supplemental irrigation.The youngest fully expanded leaves (the third or fourth leaf pair from the apex of the plagiotropic branches) in the upper third of three plants were collected for each biological sample. Sampling was carried out monthly in two contrasting periods of the coffee growth cycle: May to August (Dry season) and October to January (Rainy season) between 2012 and 2014. A total of two dry periods and two rainy ones were assessed. Immediately after harvesting, leaves were ground under liquid nitrogen with a mortar and pestle before being lyophilized for 36 hours (EC-Super Modulyo Model, Edwards, Crawley, UK) and stored at –20 ºC until analysis. Three replicates per biological sample were analyzed.

Chemicals and reagents

Chemical reagents such as tannic (TA), chlorogenic (5-O-caffeoilquinic acid,5-CQA) and caffeic acids (3,4-dihydroxycinnamic acid, CAF) were 99.0; 98.0 and 99.5% analytical purity, respectively. Commercial standards were purchased from Sigma–Aldrich Brazil Ltda, São Paulo. Solvents and phosphoric acid were HPLC-grade, from J.T. Baker, and the water used was ultra-purified by a Milli-Q© system (Millipore, Brazil). Samples were filtered by cellulose ester membrane 0.45 µm (Millipore, Brazil). The total concentration of soluble phenolic compounds was determined using Folin–Ciocalteu reagent according to Spanos & Wrolstad (1990)SPANOS GA & WROLSTAD RE. 1990. Influence of variety, maturity, processing and storage on the phenolic composition of pear juice. J Agric Food Chem 38: 817-824. and the absorbance was measured at 765 nm by spectrophotometry (UV-Vis, Lambda 20 model, Perkin Elmer). The total soluble phenolic contents (TSP) of the samples were estimated in milligrams of tannic acid equivalents (TAeq) and expressed by mg TAeq g-1 SP. Extractions of CAF and 5-CQA acids were adapted from Ky et al. (1997)KY CL, NOIROT M & HAMON S. 1997. Comparison of five purification methods for chlorogenic acids in green coffee beans (Coffea sp). J Agric Food Chem 48: 786-790. and Hinneburg & Neubert (2005)HINNEBURG IE & NEUBERT RHH. 2005. Influence of parameters on the phytochemical characteristics of extracts from buckwheat (Fagopyrum esculentum) Herb. J Agric Food Chem 53: 3-7.. Coffee sample (0.030g) was extracted with methanol:water (70:30, v/v, 3 mL) and heat at 60°C for 30 min in water bath (B480 model, Büchi). After cooling, extracts were filtered and its volume was completed to 10 mL with methanol:water (70:30, v/v). 2 mL of extract was filtered (0.45 µm pore size) and analyzed using a HPLC system (Agilent, 1100 Series). CAF and 5-CQA separation and quantification were adapted from Pellati et al. (2005)PELLATI F, BENVENUTI S, MELEGARI M & LASSEIGNE T. 2005. Variability in the composition of antioxidant compounds in Echinacea species by HPLC. Phytochem Anal 16: 77-85. and the HPLC analysis was carried out using a UV-visible detector that operated at 325 nm, injection volume 10 µL, C-18 Partisil 5 ODS-2 column; reversed phase, 4,6 x 250 mm, with mobile phase of ultra-purified water with phosphoric acid 0.1% (solvent A) and acetonitrile (solvent B) at flow rate of 0.9 mL min−1 stabilized with 90% solvent A and 10% solvent B (time zero). Identification was performed by comparing spectra and retention times with commercial standards by extract fortification; results were expressed in mg g-1.

Mite collection and identification

The analysis of mite fauna in coffee plants was performed on eighteen leaves of each cultivar (from six plants/cultivar/plot) that were collected monthly within each ring of the FACE (three leaves per plant, one from each third of vertical profile- upper, middle and lower.) totaling 108 leaves assessed of each cultivar per [CO2] treatment. Each sample was stored separately in a labelled paper bag and stored cold during transit until the lab. The leaves of each plant were immersed for 10 min in alcohol solution (70%), and these solutions were slightly shaken to remove the mites from the leaves. The alcohol containing the mites was passed through a sieve of 400 mesh (wire mesh opening: 0.038 mm). The mites retained on the screen were kept in 70% ethanol (Mineiro et al. 2009MINEIRO JLC, RAGA A, SATO ME & LOFEGO AC. 2009. Ácaros associados ao cafeeiro (Coffea spp.) no estado de São Paulo, Brasil. Parte I. Mesostigmata. Biota Neotrop 9: 37-46.). Mite populations were quantified and the species were identified.

Statistical analysis

The experiment was set up in a 2x2 factorial design with two levels of [CO2], ambient and elevated, and two seasons, dry and rainy, with 24 replicates. Data collected for each response variable were subjected to analysis of variance (ANOVA) and Tukey’s test was performed after significant Anova, to compare means employing the SAS GLM procedure (SAS 2008). Finally, Pearson Correlation was performed within all response variables utilizing the CORR procedure of SAS (SAS 2008).

RESULTS AND DISCUSSION

Weather conditions over two years of the experiment (Figure 1) were characterized by low average air temperatures (±18oC) and precipitation (5~10mm) from May to August period (dry season) and high average temperatures (±26 oC) and precipitation (80~130mm) from October to January (rainy season).

Figure 1
Monthly minimum and maximum mean air temperatures, rainfall distribution and phenological stage of coffee plants in FACE octagons.

Most of the significant treatment effects on the variables analysed were observed for the seasonality factor (dry/rainy) rather than for [CO2] factor in both coffee cultivars (Catuaí and Obatã). In cv. Catuaí the [CO2] factor (ambient/elevated) had a significant effect only in the 5-CQA contents (p=0.002) and an interactive trend of [CO2] x seasonality was observed for this variable (p=0.087) (Table I). Additionally, seasonality had a highly significant effect on TSP amounts (p<0.0001), 5-CQA (p<0.0001), CAF (p=0.0019) and spmites (p=0.034). No significant effects of [CO2] was observed in cv. Obatã but seasonality had significant effect on TSP (p<0.0001), 5-CQA (p<0.0001) and spmites (p=0.032) (Table I).

Table I
Variance analysis of TSP, CAF, 5-CQA, mite diversity (spmites) and mite population (nmites), in two coffee cultivars (Catuaí and Obatã), with two levels of [CO2] (elevated/ambient), in two seasons (dry/rainy) under factorial arrange.

Means comparisons (Tukey’s test, 5%) indicated reduction of 5-CQA levels in cv. Catuaí growing under e[CO2] and significantly lower TSP, 5-CQA and CAF contents in dry season comparing with the rainy one. Instead, spmites was significantly higher during dry season than rainy season (Table II). In cv. Obatã TSP and 5-CQA contents were reduced significantly in dry season, whereas an increase was observed for spmites. No significant effects of [CO2] treatments were detected for Obatã plants (Table II).

Table II
Average content of TSP, CAF and 5-CQA; mite diversity (spmites) and mite population (nmites), in coffee cultivars Catuaí and Obatã, in a factorial experiment with two levels of [CO2] (elevated/ambient) and leaves collected in two seasons (dry/rainy).

Our results showed that elevated CO2 only affected concentrations of 5-CQA in cv. Catuaí coffee leaves. Like green tea and green coffee beans, the main phenolic constituent of coffee leaves is 5-CQA that is significantly correlated with antioxidant and anti-inflammatory activities in human health (Campa et al. 2012CAMPA C, MONDOLOT L, RAKOTONDRAVAO A, BIDEL LPR, GARGADENNEC A, COUTURON E, LA FISCA P, RAKOTOMALALA J-J, JAY-ALLEMAND C & DAVIS AP. 2012. A survey of magiferin and hydroxycinnamic acid ester accumulation in coffee (Coffea) leaves: biological implications and uses. Ann Bot 110: 595-613., Somporn et al. 2012SOMPORN C, KAMTUO A, THEERAKULPISUT P & SIRIAMORNPUN S. 2012. Effect of shading on yield, sugar content, phenolic acids and antioxidant property of coffee beans (Coffea Arabica L. cv. Catimor) harvested from north-eastern Thailand. J Sci Food Agric 92: 1956-1963., Vagiri et al. 2017VAGIRI M, JOHANSSON E & RUMPUNEN K. 2017. Phenolic compounds in black currant leaves–an interaction between the plant and foliar diseases? J Plant Interact 12: 193-199., Chen et al. 2018CHEN XM, MA Z & KITTS DD. 2018. Effects of processing method and age of leaves on phytochemical profiles and bioactivity of coffee leaves. Food Chem 249: 143-153.). In coffee beans chlorogenic acids (CGA) such as 5-CQA, are important determinant of coffee flavor contributing to the astringency and beverage bitterness (Clifford et al. 2017CLIFFORD MN, JAGANATH IB, LUDWIG IA & CROZIER A. 2017. Chlorogenic acids and the acyl-quinic acids: discovery, biosynthesis, bioavailability and bioactivity.Nat Prod Rep 34: 1391-1421.). Additionally, CGA synthesis in the coffee plant may contribute to the control of seed germination and cell growth, through regulations of the levels of indolacetic acid, a plant growth hormone of physiological significance during the formation of the beans (Farah & Donangelo 2006FARAH A & DONANGELO CM. 2006. Phenolic compounds in coffee. Braz J Plant Physiol 18: 23-36.). Considering its relevance to coffee plants, reduction of 5-CQA levels could be an undesirable effect of e[CO2].

Contrary to the Carbon–Nutrient Balance Hypothesis that predicts an increase of carbon-based defence compounds as a result of the ‘excess’ C under e[CO2] (Robinson et al. 2012ROBINSON E, RYAN G & NEWMAN J. 2012. A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194: 321-336.) we found relatively low changes of phenolic concentration in coffee leaves. However, such alterations are in accordance with several studies demonstrating little or no effect of e[CO2] on phenolics, or even decreases in their levels (Robinson et al. 2012ROBINSON E, RYAN G & NEWMAN J. 2012. A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194: 321-336., Goufo et al. 2014GOUFO P, PEREIRA J, MOUTINHO-PEREIRA J, CORREIA CM & TRINDADE H. 2014. Rice (Oryza sativa L.) phenolic compounds under elevated carbon dioxide (CO2) concentration. Environ Exp Bot 99: 28-37., Saha et al. 2015SAHA S, SEHGAL VK, CHAKRABORTY D & PAL M. 2015. Atmospheric carbon dioxide enrichment induced modifications in canopy radiation utilization, growth and yield of chickpea (Cicer arietinum L.). Agric For Meteorology 202: 102-111., AbdElgawad et al. 2016ABDELGAWAD H, ZINTA G, BEEMSTER G, JANSSENS I & ASARD H. 2016. Future Climate CO2 Levels Mitigate Stress Impact on Plants: Increased Defense or Decreased Challenge? Frontiers in Plant Science 7: 556.). Noteworthy alterations of phenolic compounds were observed in white and brown rice (Goufo et al. 2014GOUFO P, PEREIRA J, MOUTINHO-PEREIRA J, CORREIA CM & TRINDADE H. 2014. Rice (Oryza sativa L.) phenolic compounds under elevated carbon dioxide (CO2) concentration. Environ Exp Bot 99: 28-37.) and in two varieties of ginger (Ghasemzadeh et al. 2010GHASEMZADEH A, JAAFAR HZE & RAHMAT A. 2010. Elevated carbon dioxide increases contents of flavonoids and phenolic compounds, and antioxidant activities in Malaysian young ginger (Zingiber officinale Roscoe.) varieties. Molecules 15: 7907-7922.). Some explanation to inconsistency on antioxidant responses to e[CO2] is that in FACE experiments the effects of CO2 on growth are less pronounced than in growth cabinet experiments (Ainsworth et al. 2008AINSWORTH EA, LEAKEY AD, ORT DR & LONG SP. 2008. FACE-ing the facts: inconsistencies and interdependence among field, chamber and modeling studies of elevated [CO2] impacts on crop yield and food supply. New Phytol 179: 5-9.). Other authors have suggested that the relatively large variety in antioxidant responses to e[CO2] may not directly correlate to the stress and CO2 treatment only, but there are an integrated response of changes in various metabolic processes (AbdElgawad et al. 2016ABDELGAWAD H, ZINTA G, BEEMSTER G, JANSSENS I & ASARD H. 2016. Future Climate CO2 Levels Mitigate Stress Impact on Plants: Increased Defense or Decreased Challenge? Frontiers in Plant Science 7: 556.).

Our study showed significant effects of seasonality in phenolic levels of coffee leaves indicating low levels in dry seasons and higher contents in the rainy season. Coffee plants are more affected by low temperatures than by water restriction (Silva et al. 2004SILVA EA, DAMATTA FM, DUCATTI C, REGAZZI AJ & BARROS RS. 2004. Seasonal changes in vegetative growth and photosynthesis of arabica coffee trees. Field Crops Res 89: 349-357., Amaral et al. 2006AMARAL JAT, RENA AB & AMARAL JFT. 2006. Crescimento vegetativo sazonal do cafeeiro e sua relação com fotoperíodo, frutificação, resistência estomática e fotossíntese. Pesq Agrop Bras 41(3): 377-384.) in dry seasons. In the same experimental plots of this study, Ghini et al. (2015)GHINI R, TORRE-NETO A, DENTZIEN AFM, GUERREIRO-FILHO O, IOST R, PATRÍCIO FRA, PRADO JSM, THOMAZIELLO RA & BETTIOL W. 2015. Coffee growth, pest and yield responses to free-air CO2 enrichment. Climatic Change 132: 307-320. verified in both, Catuaí and Obatã coffee plants, that photosynthesis was stimulated by e[CO2] but the carbon assimilation was limited by diffusive constrains in leaf mesophyll observed in dry season. This physiological limitation of coffee plants could explain low carbon availability to investments in carbon-based phenolic compounds resulting in low levels of these secondary metabolites in coffee leaves in dry season, contrary to the rainy ones, when both photosynthesis (Ghini et al. 2015GHINI R, TORRE-NETO A, DENTZIEN AFM, GUERREIRO-FILHO O, IOST R, PATRÍCIO FRA, PRADO JSM, THOMAZIELLO RA & BETTIOL W. 2015. Coffee growth, pest and yield responses to free-air CO2 enrichment. Climatic Change 132: 307-320.) and phenolic leaf levels were higher. To corroborate this assumption, Salgado et al. (2008)SALGADO PR, FAVARIN JL, LEANDRO RA & LIMA FILHO OF. 2008. Total phenol concentration in coffee tree leaves during fruit development. Sci Agr 65(4): 354-359. also verified in ambient [CO2] that phenolic levels of coffee leaves were conditioned by competition for carbohydrates between the primary and secondary metabolism along phenological phases.

No effects of e[CO2] were observed on mite abundance and diversity on coffee leaves, however, seasonality had a significant effect on diversity of mites in both cultivars. The higher diversity of mites during the dry seasons is probably associated with the favorable conditions for the population increase of several species of phytophagous (e.g., Tetranychidae, Tenuipalpidae) and predatory (e.g., Stigmaeidae) mites, besides lower predation rates by phytoseiid mites (Acari: Phytoseiidae), which are negatively affected by the low humidity (Gerson et al. 2003GERSON U, SMILEY RL & OCHOA R. 2003. Mites (Acari) for pest control. Blackwell Science, Oxford., Matioli & Oliveira 2007MATIOLI AL & OLIVEIRA CAL. 2007. Biologia de Agistemus brasiliensis Matioli, Ueckermann and Oliveira (Acari: Stigmaeidae) e sua potencialidade de predação sobre Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae). Neotrop Entomol 36: 557-582., Mineiro et al. 2008MINEIRO JLC, SATO ME, RAGA A & ARTHUR V. 2008. Population dynamics of phytophagous and predaceous mites on coffee in Brazil, with emphasis on Brevipalpus phoenicis (Acari: Tenuipalpidae). Exp Appl Acarol 44: 277-291.). The phytoseiid mites (Acari: Phytoseiidae) are considered the most important natural enemies for biological control of pest mites in high abundance periods (Reis et al. 2008REIS PR, ZACARIAS M, SILVA R & MARAFELI P. 2008. Manejo de ácaros em cafeeiro. In: Manejo fitossanitário da cultura do cafeeiro, Fernandes LHM (Org). Brasília: Sociedade Brasileira de Fitopatologia, 2008, p. 173-184., Toledo et al. 2013TOLEDO MA, REIS PR, DA SILVEIRA EC, MARAFELI P DE P & DE SOUZA-PIMENTEL GC. 2013. Predatory potential of Euseius alatus (Phytoseiidae) on different life stages of Oligonychus ilicis (Tetranychidae) on coffee leaves under laboratory conditions. Neotrop Entomol 42: 185-190., Castilho et al. 2015CASTILHO RC, DUARTE VS, MORAES GJ DE, WESTRUM K, TRANDEM N, ROCHA LCD, DELALIBERA I & KLINGEN I. 2015. Two-spotted spider mite and its natural enemies on strawberry grown as protected and unprotected crops in Norway and Brazil. Exp Appl Acarol 66: 509-528.), however they also may compete with predatory mites of other families (Sato et al. 2001SATO ME, RAGA A, CERÁVOLO LC, SOUZA FILHO MF, ROSSI AC & MORAES GJ DE. 2001. Effect of insecticides and fungicides on the interaction between members of the mite families Phytoseiidae and Stigmaeidae on citrus. Exp Appl Acarol 25: 809-818., Mineiro et al. 2008MINEIRO JLC, SATO ME, RAGA A & ARTHUR V. 2008. Population dynamics of phytophagous and predaceous mites on coffee in Brazil, with emphasis on Brevipalpus phoenicis (Acari: Tenuipalpidae). Exp Appl Acarol 44: 277-291.). The lower abundance of mites observed during rainy seasons when compared to dry seasons may be also due to abiotic factors such as temperature and relative air humidity. Gherlenda et al. (2016)GHERLENDA A, CROUS N, MOORE K, HAIGH Y, JOHNSON B & RIEGLER D. 2016. Precipitation, not CO2 enrichment, drives insect herbivore frass deposition and subsequent nutrient dynamics in a mature Eucalyptus woodland. Plant and Soil 399: 29-39. verified significant effects of rainfall-driven leaf phenology and no effect of e[CO2] on leaf consumption or preference of insects herbivores in mature Eucalyptus woodland canopy after two years of fumigation in FACE. Castilho et al. (2015)CASTILHO RC, DUARTE VS, MORAES GJ DE, WESTRUM K, TRANDEM N, ROCHA LCD, DELALIBERA I & KLINGEN I. 2015. Two-spotted spider mite and its natural enemies on strawberry grown as protected and unprotected crops in Norway and Brazil. Exp Appl Acarol 66: 509-528. correlated heavy rainfall to population decrease of predatory mites while rainfall affected the number of predatory (Phytoseiidae and Stigmaeidae) and phytophagous mites (Tenuipalpidae and Tetranychidae) in a range of crop management systems (Neto et al. 2010NETO MP, REIS PR, SILVA RA, ZACARIAS MS & MESQUITA DN. 2010. Influência do regime pluviométrico na distribuição de ácaros em cafeeiros conduzidos em sistemas orgânico e convencional. Coffee Sci 5: 67-74.). Negative correlations between mite densities and temperature were observed for Euseius concordis (Chant) (Acari: Phytoseiidae) on leaf surfaces and branches, and for Zetzellia malvinae Matioli, Ueckermann & Oliveira (Acari: Stigmaeidae) in domatia, that are minute structures found on the underside of the leaves. A positive correlation between the number of mites (per plant) and temperature was detected for Brevipalpus sp. on fruits, in a coffee plantation (C. arabica cv Mundo Novo) in the State of São Paulo (Mineiro et al. 2008MINEIRO JLC, SATO ME, RAGA A & ARTHUR V. 2008. Population dynamics of phytophagous and predaceous mites on coffee in Brazil, with emphasis on Brevipalpus phoenicis (Acari: Tenuipalpidae). Exp Appl Acarol 44: 277-291.). Additionally, Abreu et al. (2014)abreu Fa, reis pr, marafeli pp, silva ra, bernardi lfo & carvalho cf. 2014. Influência da precipitação pluvial na abundância de ácaros em cafeeiro. Coffee Sci 9(3): 329-335. verified negative correlation between total number of mites and precipitation levels in Arabic coffee cv. Paraiso.

Besides the climatic factors, food resources availability determines abundance and diversity of mites in coffee plantations. For example, Ricoseius loxocheles (De Leon) (Acari: Phytoseiidae) is often found in coffee crops and is known to feed on coffee leaf rust, H. vastatrix (Ajila et al. 2018AJILA HEV, FERREIRA JA, COLARES F, OLIVEIRA CM, BERNARDO AMG, VENZON M & PALLINI A. 2018. Ricoseius loxocheles (Acari: Phytoseiidae) is not a predator of false spider mite on coffee crops: What does it eat? Exp Appl Acarol 74: 1-11.). Populations densities of red spider mites, O. ilicis, were positively correlated with populations densities of coffee leaf miner, Leucoptera coffeella Guérin-Méneville (Lepidoptera: Lyonetiidae) and leaf rust in the field (Teodoro et al. 2009TEODORO A, KLEIN AM, REIS PR & TSCHARNTKE T. 2009. Agroforestry management affects coffee pests contingent on season and developmental stage. Agr Forest Entomol 11: 295-300.). In the same experiment of this study, Ghini et al. (2015)GHINI R, TORRE-NETO A, DENTZIEN AFM, GUERREIRO-FILHO O, IOST R, PATRÍCIO FRA, PRADO JSM, THOMAZIELLO RA & BETTIOL W. 2015. Coffee growth, pest and yield responses to free-air CO2 enrichment. Climatic Change 132: 307-320. related a peak of leaf miner incidence on the second dry season of this study, when weather conditions were favorable to pest infestation. In this study, the diversity of mites in coffee plants was related to phytochemical profile of leaves that presented higher levels of phenolic compounds in rainy season. Phenolics inhibit the digestion of proteins in various herbivores and thus commonly act as plant defenses (Ballhorn et al. 2011BALLHORN DJ, SCHMITT I, FANKHAUSER JD, KATAGIRI F & PFANZ H. 2011. CO2-mediated changes of plant traits and their effects on herbivores are determined by leaf age. Encol Entomol 36: 1-13.) and these effects may also have been responsible for the low levels of mite diversity on coffee leaves during rainy seasons. Insect performance usually correlates positively with nitrogen concentration and negatively with the concentration of carbon-based compounds (Kuokkanen et al. 2003KUOKKANEN K, YAN S & NIEMELA P. 2003. Effects of elevated CO2 and temperature on the leaf chemistry of birch Betula pendula (Roth) and the feeding behaviour of the weevil Phyllobius maculicornis. Agric Forest Entomol 5: 209-217., Lindroth 2010LINDROTH RL. 2010. Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36: 2-21.) but these relationships were not described for mites up to date. In our study, mite diversity in cv. Catuaí presented a negative correlation with 5-CQA, CAF and TSP levels while abundance of mites was negatively correlated only with 5-CQA level (Table III). In cv. Obatã mite diversity was negatively correlated with 5-CQA and TSP while mite abundance was negatively correlated with TSP only (Table III). During dry and rainy seasons, mite diversity was negatively correlated with 5-CQA and TSP and with CAF levels only in the rainy season (Table III). In all treatment levels (cultivar, season and [CO2]) mite diversity was negatively correlated to 5-CQA and TSP levels indicating the importance of these compounds in mite-coffee leaves interrelationships. Interestingly, abundance but not diversity of mites, always correlated negatively with all phenolic compounds only under e[CO2] (Table III).

Table III
Earson correlation coefficient (R) between variables evaluated in coffee leaves of Catuaí and Obatã cultivars collected in two seasons (dry/rainy) and cultivated in two levels of [CO2] (elevated/ambient).

Magalhães et al. (2010)MAGALHÃES ST, FERNANDES FL, DEMUNER AJ, PICANÇO MC & GUEDES RNC. 2010. Leaf alkaloids, phenolics, and coffee resistance to the leaf miner Leucoptera coffeella (Lepidoptera: Lyonetiidae). J Econ Entomol 103: 1438-1443. showed no correlation between resistance to L. coffeella and the leaf levels of alkaloids and phenolics, however, infestation by leaf miners led to a nearly four-fold decline in the leaf levels of chlorogenic acid promoting infestation by generalist insects, such as Coccus viridis (Hemiptera: Sternorrhyncha: Coccidae). Ramiro et al. (2006)RAMIRO DA, GUERREIRO-FILHO O & MAZZAFERA P. 2006. Phenol contents, oxidase activities, and the resistance of coffee to the leaf miner Leucoptera coffeella. J Chem Ecol 32: 1977-1988. investigating 5-CQA participation on coffee resistance to L. coffeella, suggest that phenol content apparently does not play a central role but, conversely, the reduction of soluble phenols in leaves is a general plant response to feeding damage making proteins less available for assimilation by the digestive tract of the insects.

This is the first study about phenolic compounds interactions with mite infestations in coffee growing under FACE system. Our assumption is that in dry season the lower levels of TSP, 5-CQA and CAF resulted from low carbon availability to the synthesis of phenolic compounds contributing for higher mite diversity in coffee leaves. Additionally, e[CO2] intensified this effect in cv. Catuaí resulting in lower levels of 5-CQA, which could indicate a higher susceptibility of that cultivar to attack of pests and diseases when subjected to an increase of [CO2] in atmosphere.

CONCLUSIONS

The interaction between e[CO2] and natural climatic variability, besides its effects on plant chemistry and insect herbivores needs to be further investigated. Here we analyzed alterations in leaf phenolic compounds of young coffee plants growing in FACE and the respective relationships with abundance and diversity of mites. Contrary to our hypothesis, e[CO2] did not elevate coffee leaf phenolics, but reduced concentration of chlorogenic acid (5-CQA) of C. arabica cv Catuaí in the dry season. Results showed that phenolic levels were higher during rainy than the dry seasons but no interaction with e[CO2] occurred. Additionally, diversity and abundance of mites in coffee leaves were not affected by e[CO2], but the diversity of mites were strongly related to the seasonal variability of coffee leaf phenolics. In general, high levels of phenolics were negatively correlated to abundance of mites, while the diversity was negatively correlated with 5-CQA and TSP levels. Considering that 5-CQA is known to be responsible for many aspects of coffee beverage quality and to have important participation on ecological interactions, like suggested by our results with mite population analysis, reductions of 5-CQA levels in coffee leaves is an undesirable effect of e[CO2], especially during dry seasons, when high incidence of mites and other pests are observed in many crop systems. Further investigations may highlight the contribution of different secondary metabolites in the mite-coffee leaf interactions. Finally, the relationship between [CO2] atmospheric and phenolic compounds in coffee plants was described in this work for the first time and draws attention to the need to consider the natural variability of plant defenses for the phytosanitary management of coffee plantations.

ACKNOWLEDGMENTS

The authors are grateful to Embrapa (project 01.07.06.002.00: Climapest—Impacts of global climate changes on plant diseases, pests and weeds; and project 02.12.01.018.00: Impact of increased atmospheric carbon dioxide concentration and water availability on the coffee agroecosystem under the FACE facility) for financial support. We thank Dagmar N. dos S. Oliveira and Melissa Baccan for laboratory analysis; the field staff of Embrapa Environment and Dr. Roberto A. Thomaziello expert in coffee growing.

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  • ERRATUM

    In the article Increased atmospheric CO2 combined with local climatic variation affects phenolics and spider mite populations in coffee trees, with DOI number: http://doi.org/10.1590/0001-3765202120190696, published in the journal Anais da Academia Brasileira de Ciências, 93(3): e20190696.
    Page 6
    Reads:
    Figure 1 Monthly minimum and maximum mean air temperatures, rainfall distribution and phenological stage of coffee plants in FACE octagons.
    Should read:
    Figure 1 Monthly minimum and maximum mean air temperatures, rainfall distribution and phenological stage of coffee plants in FACE octagons.
    Page 7
    Reads:
    Table I Variance analysis of TSP, CAF, 5-CQA, mite diversity (spmites) and mite population (nmites), in two coffee cultivars (Catuaí and Obatã), with two levels of [CO2] (elevated/ambient), in two seasons (dry/rainy) under factorial arrange.
    Variable Factor Catuaí Obatã
    F ( 1 ) P ( 2 ) ≥|F| F P ( 2 ) ≥|F|
    Total Soluble Phenolics (TSP) CO2 0.74 0.3934 0.47 0.4938
    Season 16.72 <0.0001 17.82 <0.0001
    CO2xSeason 1.12 0.2921 3.29 0.0732
    Caffeic acid (CAF) CO2 0.70 0.4049 1.34 0.2505
    Season 10.21 0.0019 2.07 0.1539
    CO2xSeason 0.00 0.9744 0.01 0.9039
    Chlorogenic acid (5-CQA) CO2 10.04 0.0021 0.09 0.7691
    Season 101.38 <0.0001 143.35 <0.0001
    CO2xSeason 2.99 0.0874 0.12 0.7313
    # sp mites CO2 3.82 0.0538 0.03 0.8673
    Season 4.62 0.0342 4.74 0.0320
    CO2xSeason 0.00 1.0000 0.11 0.7383
    ## n mites CO2 0.98 0.3248 0.39 0.5344
    Season 1.32 0.2544 3.50 0.0645
    CO2xSeason 0.89 0.3486 0.24 0.6288
  • (1) df = 1; (2) nominal significance level of F-test; Values in bold indicate statistical significance by ANOVA; in all cases, df of: model = 3; error = 92; corrected total = 95; # number of mite species identified; ## total number of mites collected.
Should read:
Table I Variance analysis of TSP, CAF, 5-CQA, mite diversity (spmites) and mite population (nmites), in two coffee cultivars (Catuaí and Obatã), with two levels of [CO2] (elevated/ambient), in two seasons (dry/rainy) under factorial arrange.
Variable Factor Catuaí Obatã
F ( 1 ) P ( 2 ) ≥|F| F P ( 2 ) ≥|F|
Total Soluble Phenolics (TSP) CO2 0.74 0.3934 0.47 0.4938
Season 16.72 <0.0001 17.82 <0.0001
CO2xSeason 1.12 0.2921 3.29 0.0732
Caffeic acid (CAF) CO2 0.70 0.4049 1.34 0.2505
Season 10.21 0.0019 2.07 0.1539
CO2xSeason 0.00 0.9744 0.01 0.9039
Chlorogenic acid (5-CQA) CO2 10.04 0.0021 0.09 0.7691
Season 101.38 <0.0001 143.35 <0.0001
CO2xSeason 2.99 0.0874 0.12 0.7313
# sp mites CO2 3.82 0.0538 0.03 0.8673
Season 4.62 0.0342 4.74 0.0320
CO2xSeason 0.00 1.0000 0.11 0.7383
## n mites CO2 0.98 0.3248 0.39 0.5344
Season 1.32 0.2544 3.50 0.0645
CO2xSeason 0.89 0.3486 0.24 0.6288
  • (1) df = 1; (2) nominal significance level of F-test; Values in bold indicate statistical significance by ANOVA; in all cases, df of: model = 3; error = 92; corrected total = 95; # number of mite species identified; ## total number of mites collected.
  • Page 10
    Reads:
    Table III. earson correlation coefficient (R) between variables evaluated in coffee leaves of Catuai and Obatã cultivars collected in two seasons (dry/rainy) and cultivated in two levels of [CO2] (elevated/ambient).
    Should read:
    Table III. Pearson correlation coefficient (R) between variables evaluated in coffee leaves of Catuai and Obatã cultivars collected in two seasons (dry/rainy) and cultivated in two levels of [CO2] (elevated/ambient).

    Publication Dates

    • Publication in this collection
      10 May 2021
    • Date of issue
      2021

    History

    • Received
      27 June 2019
    • Accepted
      27 Oct 2019
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