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Industrial Crops and Products 44 (2013) 200– 210

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Industrial Crops and Products

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Ecophysiological traits of the macaw palm: A contribution towardsthe domestication of a novel oil crop

Thiago Pereira Pires ∗, Elma dos Santos Souza, Kacilda Naomi Kuki, Sérgio Yoshimitsu MotoikeDepartamento de Fitotecnia, Universidade Federal de Vic osa, MG, Brazil

a r t i c l e i n f o

Article history:Received 19 July 2012Received in revised form24 September 2012Accepted 25 September 2012

Keywords:Acrocomia aculeataApparent quantum efficiencyBiofuelEcophysiologyOilPalmPhotosynthesis

a b s t r a c t

Acrocomia aculeata, or macaw palm, is a highly productive oleaginous palm tree with the potential tobe a new oil crop. Plant productivity is influenced by the exchange of gases between the leaf and theatmosphere. The assimilation of CO2 is dependent on both environmental factors and the intrinsic char-acteristics of the leaf, such as age, position in the canopy, and nutrient and pigment content. This studywas conducted to characterize some ecophysiological aspects of macaw palm cultivated under fieldconditions. Foliar content and gas exchange parameters were analyzed in relation to diel variation, lightintensity, and the position within the canopy and rachis. The evolution of photosynthesis and related vari-ables during the daytime followed the standard patterns for most species with C3 metabolism, reachingpeak levels during the morning hours. The light curve response also displayed a C3 pattern; however, thisspecies demonstrated a high photosynthetic capacity with a maximum net photosynthesis and appar-ent quantum efficiency of approximately 23 �mol m−2 s−1 and 0.07 mol/mol, respectively. Gas exchangeparameters of the fronds along the canopy varied according to the leaf position and the leaflet’s insertionlocation within the rachis. Overall values indicate that the second and third leaves and the leaflets inthe middle of the rachis have the best physiological capacity. Foliar pigment and mineral content wererelatively stable among the leaves, which is a pre-requirement for long lasting leaves.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

Oil crops have been a focus in the agronomic and industry sec-tors due to the increase in worldwide demand for renewable energysources. Conflicts between food and non-food industries often arisebecause of the limited number of options among classical cultures(i.e., soy, maize, sunflower, peanuts, oil palm, etc.), which are pri-marily edible oil crops. One solution would be to introduce newoleaginous plant species that target the non-edible oil industries,such as the biofuel and pharmaceutical sectors. Tropical flora has arich biodiversity that includes many palm species known for bear-ing oil-rich fruits other than the oil palm, Elais guineensis (Lima et al.,2008; Lopes and Steidle-Neto, 2011). Although there exists a highpotential for these palms to be used as raw materials for non-foodindustries, these species have not been domesticated yet.

Acrocomia aculeata (Jacq.) Lodd. ex Martius, commonly knownas macauba or macaw palm, is a palm tree native to the trop-ical Americas. This perennial palm, because of its phenotypicdiversity, is sometimes referred to as Acrocomia sclerocarpa,

∗ Corresponding author at: Departamento de Fitotecnia, Universidade Federal deVic osa, Av. P.H. Rolfs, Campus Universitário, Vic osa, Minas Gerais 36570-000, Brazil.Tel.: +55 31 38991351; fax: +55 31 38992614.

E-mail address: thi.biologo@gmail.com (T.P. Pires).

A. intumescens or A. totai. This nomenclature conflict is not yet set-tled (http://www.palmweb.org). The macaw palm is consideredone of the most conspicuous palm species in Brazil; it naturallygrows in large populations either in degraded or intact areas andis well-adapted to different ecosystems (Motta et al., 2002; Ratteret al., 2003; Aquino et al., 2008). This species bears oleaginous fruitsin massive bunches that can weigh more than 25 kg under naturalconditions (Wandeck and Justo, 1988; Scariot et al., 1995). Becauseof this, it has been considered as a potential material for biodieselproduction (Cargnin et al., 2008). The biochemical constitution andfatty composition of fruits are remarkably diverse, and the meso-carp accumulates up to 70% oil on a dry-weight basis (CETEC, 1983;Bora and Rocha, 2004; Hiane et al., 2005, 2006; Coimbra and Jorge,2011a, 2011b, 2012) (Fig. 1A and B). The economic feasibility ofthe macaw palm rests on its high oil productivity (Fig. 1C) andthe integral use of its fruits, which can generate different prod-ucts and co-products depending upon the processed part: higholeic oil from the pulp, rich lauric oil from the kernel; protein-aceous or fibrous cakes from the kernel and the pulp, respectively;and charcoal or briquettes from the hardy endocarp. It is pro-jected that under proper agronomic care, a commercial plantationcan yield 16,000–25,000 kg of fruit per hectare and produce up to6200 kg/ha of oil, 11,500 kg/ha of cakes and 3000 kg/ha of char-coal (Fig. 2) (Wandeck and Justo, 1988; CETEC, 1983; Cargnin et al.,2008; Coimbra and Jorge, 2011b). Another fundamental value of

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Fig. 1. (A) Macaw palm fruit parts and oil distribution, based on CETEC (1983). (B) Total oil composition and some physicochemical characteristics, based on Hiane et al.(2005). (C) Actual average oil yield for well established crops, based on Sumathi et al. (2008), and the predicted average for a rational macaw palm plantation, based onWandeck and Justo (1988).

Photo by Motoike (2011).

macaw palm is its recognizable environmental utility. This palmis resilient and can populate areas containing meager resources,which is a desirable trait for plants used to rehabilitate degradedpastures or for agroforestry practices (Motoike and Kuki, 2009).

In spite of its economic prospects, the macaw palm is stillwild. Its exploitation has been carried out through extractivism,which is an often inefficient gathering modality used by few oper-ating industries that leads to low productivity and poor quality

of the products obtained. Due to the attributes and potential useof macaw palm fruits, studies have been conducted by Brazilianresearch groups funded by federal and state agencies. Their workhas addressed fruit composition and its properties, as well as thefollowing topics: phenology and reproductive biology (Scariot et al.,1991, 1995; Abreu et al., 2012); seed anatomy, physiology and ger-mination (Moura et al., 2010; Ribeiro et al., 2012; Neto et al., 2012);vegetative and seed propagation (Moura et al., 2008, 2009; Motoike

Fig. 2. Schematic and illustrative end-products of macaw palm fruit processing, based on Wandeck and Justo (1988).Photo by Motoike (2011).

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Fig. 3. Recordings of (A) rainfall, air temperature and (B) air relative humidity during a 12-month span. Data were provided by the Brazilian National Institute of Meteorology(INMET) and refers to the geographical micro-region where the Germoplasm Bank is situated.

et al., 2007); genetic characterization (Abreu et al., 2011; Manfioet al., 2012; Oliveira et al., 2012); value in industrial technologies(Vilas Boas et al., 2010; Silva and Andrade, 2011) and commercialand productivity values (Lima et al., 2008; Lopes and Steidle-Neto,2011). All these efforts converge to bring solid justification forspecies domestication and the implementation of breeding pro-grams, which will depend on a multidisciplinary approach. Thecharacterization of the ecophysiological traits of the macaw palmrepresents one of the requirements to understand how the speciesinteracts with its environment.

Research of this nature can assist in the screening and selec-tion of so-called ‘promising species’ such as the macaw palm.Studies can elucidate the traits involved in maximum productiv-ity and stability under stressful environmental conditions (Fukaiand Cooper, 1995; Nicotra et al., 2010; Harfouche et al., 2012).From an agronomic point of view, it is particularly worthwhile forthe development of varieties that can sustain growth and maintainproductivity with limited resources and withstand edaphoclimaticalterations that are a natural part of seasonality (Lamade and Setiyo,1996; Araus et al., 2008). Plant productivity is directly linked to theprocess of gas exchange between the plant and the atmosphere.The physiological parameters of plant gas exchange, such as netcarbon assimilation, transpiration, and stomatal conductance, arereadily affected by the qualitative and quantitative changes of envi-ronmental surroundings and by the leaf content, age and positionwithin the canopy (Lamade and Setiyo, 1996; Crafts-Brandner andSalvucci, 2000; Kitajima et al., 2002; Gomes et al., 2008; Reddyand Matcha, 2010). Because of this, the photosynthetic process isoften used as a physiological marker for determining plant welfare.The study of parameters involved in carbon assimilation and itsintrinsic variations can help reveal the photosynthetic patterns of a

particular species (Araus et al., 2008; Teng et al., 2004; Nunes et al.,2009).

The primary goal of this study was to characterize the generalpatterns of photosynthetic traits in juvenile macaw palm plantsgrown under field conditions. Understanding these traits can helporient the studies involved in the domestication of the species,which is an integrative endeavor.

2. Materials and methods

This work focused on the characterization of physiological traitsof juvenile macaw palm plants under field conditions. The mea-surements were performed during March of 2011, the end of therainy season, in order to avoid heavy sky nebulosity during day-light hours. The plants were sampled from a germplasm collectionand analyzed regarding their photosynthetic response to diurnalhourly variation (diel course), light intensity, leaf age/position, leafpigment content and nutrient content.

2.1. Study site and plant material

The study was conducted at the Araponga Experimental Farm(20◦40′1′′S, 42◦31′15′′W) in the municipality of Araponga, State ofMinas Gerais, Brazil. At approximately 1000 m of altitude, the cli-mate of the region is Cwb according to the Köppen classification;this region has rainy summers and dry winters. The climatic con-ditions of the geographical micro-region during a 12-month span(March/2010–March/2011) are depicted in Fig. 3. The data wereprovided by the 5th Station of the Brazilian National Institute ofMeteorology (INMET).

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This area belongs to the Universidade Federal de Vic osa andhosts one of the first germplasm collections of A. aculeata, ormacaw palm, in Brazil. The collection currently holds 145 geneticaccessions with 5–10 replicates, and its enrichment is an ongoingprocess. Once in the field, the plants periodically receive standardagricultural treatment and care to assure good growth conditions.Due to the precipitation regime in the region water is solely pro-vided by rainfall. Nutritional supplement to the plants is providedas follow: at planting, by mixing directly in the ground hole 1 kg ofmagnesium thermophosphate (18% P2O5, 9% Mg 20% Ca) and 100 gof fertilizer N–P–K (20-05-20) per plant stock; and once a year, bysupplying a mixture of 300 g of N–P–K (20-05-20), 200 g of sim-ple super phosphate (20% P2O5, 25% CaO and 12% S) and 200 g ofdolomitic limestone per plant.

The plants in the collection were obtained by seminiferouspropagation using seeds collected from native plant populationsscattered throughout the southwest territory of Brazil. Seed dor-mancy was overcome by applying a pre-germination protocol asdescribed in patent INPI 014070005335 (Motoike et al., 2007). Toallow for plant growth, pre-germinated seeds were transferred toplastic bags filled with a substrate mixture of clay:sand:humus(2:2:1) and kept under nursery conditions and supplemented withnutritional complementation and water when necessary. Eight toten month old plant stocks were planted in the field, in an areapreviously prepared for this purpose, using 5 m × 5 m spacing. Thefirst plants in the collection mostly originated in the state of MinasGerais. Those plants were 2.5 years old by the time of the measure-ments, with an average of 4 m in height and ten to twelve fronds. Ina completely randomized fashion, eight to ten plants were selectedfor leaf content and physiological measurements. Each plant wasconsidered a replicate and belonged to different genetic accessionsof the collection. The number of plants for each measurement waschosen for logistical reasons; selected plants were in the field anddistant from laboratory facilities.

2.2. Physiological measurements

Leaf gas exchange variables (net photosynthesis – A; transpi-ration – E; stomatal conductance – gs) and related parameterswere measured in attached leaflets using an infra-red gas analyzer(IRGA), LC-Pro portable model (ADC Bioscientific Ltd, Hertford-shire, UK). The equipment operates as an open system connectedto a leaf chamber of 5.8 cm2. The chamber is coupled to asource of red/blue light, ranging from 0 to 2000 �mol of pho-tosynthetic active radiation. All measurements were performedunder natural and instantaneous conditions of CO2 concentration(384.52 ppm ± 1.22; max.: 422 ppm and min.: 356 ppm), air tem-perature (27.81 ◦C ± 0.17; max.: 32.10 ◦C and min.: 21.0 ◦C) andatmospheric water vapor (20.23 mbar ± 0.17; max.: 25.20 mbar andmin.: 15.80 mbar). To minimize CO2 variations before entering theleaf chamber, reference air was collected at 1.50 m from the leavesand homogenized in a 20 l empty plastic bottle. The measurementswere carried out according to three target evaluations: diel course,response to photosynthetic photon flux density (PPFD) increments,and the position of the leaflets in the rachis and fronds within thecanopy.

The diel course of photosynthetic variables was carefully moni-tored every 2 h, from 5:00 AM to 5:00 PM, in the central portion ofthe leaflets located in the middle part of the rachis in ten selectedplants. The first fully expanded frond, i.e., the 2nd leaf below thespear-leaf, was chosen as the standard unit. The leaflets wereexposed to the actual incident PPFD when the readings were taken.The incident PPFD was measured by the IRGA’s sensor.

The photosynthetic response, as a function of increasing lightintensities, was obtained by exposing the above mention leaflets toPPFD ranging from 0 to 2000 �mol m−2 s−1. When the CO2 uptake

reached a steady state upon exposure to each light level, the netphotosynthesis was recorded. The procedure was carried out dur-ing the best time frame as revealed by the hourly variation duringdiurnal photosynthesis, with the leaf chamber temperature kept atapproximately 25 ◦C. The data were adjusted to a non-rectangularhyperbola model using the program Photosyn Assistant (DundeeScientific Co., UK) and based on the following quadratic equation:

A = a · Q + Amax −√

(a · Q + Amax)2 − 4 · a · Q · k · Amax

2k− Rday

where A is the net photosynthesis rate; is the apparent quantumefficiency; Q is the PPDF intensity; Amax is the maximum calculatedphotosynthesis; k the convexity of the curve and Rday is the rate ofdark respiration during daylight hours. The program also allowedestimations of the light compensation point (LCP) from the x-axisintercept and the light saturation point (LSP) when net photosyn-thesis reached a maximum value in the asymptotic curve. ObservedAmax (Amax obs) corresponded to the average of the measured netphotosynthesis values above 1000 �mol m−2 s−1.

The canopy photosynthetic profile of macaw palms was moni-tored in eight selected plants. The measurements were carried outin seven fronds that did not contain visible sign of senescence,numbered top to bottom from the first leaf below the spear-leaf(leaf sequence number: 1–7). Gas exchange readings were madeon leaflets from three different positions in the rachis (proximal,middle and distal); the mean of these values was used to representthe entire frond. All measurements were performed on the centralpart of the leaflets and collected according to the appropriate time-lapse of the photosynthesis diel curve under the best-suited lightintensity, as shown by the light curve response.

2.3. Leaf contents

Pigment and mineral nutrient contents in the leaf were exam-ined along the canopy profile of eight selected plants, using sevenfronds from the first leaf below the spear-leaf that did not containvisible signs of senescence (leaf sequence number: 1–7).

The determination of pigment content was carried out usingdimethyl sulfoxide (DMSO) as the extractant, which dispenses thelaborious process of grinding leaf material. Two foliar discs, 32 mm2

each, were plucked from leaflets located in the middle portion ofthe rachis; the discs were directly conditioned in darkened glassflasks filled with 7 ml of DMSO saturated with COCa2. The mixturewas taken into the laboratory within 2 h and incubated for 24 h at65 ◦C, as established by the pre-tests in this study. After 24 h, 3.0 mlaliquots of the pigment extract were placed in a quartz cuvettefor absorbance readings (chlorophyll a: 665.1 nm, chlorophyll b:649.1 nm and carotenoids: 480 nm) using a UV–vis spectropho-tometer (Shimazu Co., Japan). The content of each pigment wascalculated according to Wellburn’s methods (1994) and expressedon an area basis (�g mm−2).

The mineral nutrient content in the fronds was quantified usingcomposite samples of leaflets collected along the rachis. The mate-rial was dried at 75 ◦C until it reached a constant weight, thenground in an electrical stainless steel mill and sieved to a diam-eter of less than 1 mm. The vegetal powder samples were sent to acertified commercial laboratory to be analyzed for the contents ofnitrogen (N), phosphorous (P), potassium (K), iron (Fe) and magne-sium (Mg). The methodologies used for the determination of eachnutrient were: Kjeldahl method for total N content and nitroper-cloric digestion for the remaining nutrients. In the extract, mineralscontents were measured by colorimetry (P), flame photometry (K)and atomic absorption spectrophotometry (Mg and Fe).

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2.4. Statistical analysis

All data were submitted to an analysis of variance and pre-sented as the means and standard deviations. When necessary, theresults were submitted to correlation analysis or compared by aScott-Knott test at a probability of 5%. All statistical analyses wereperformed using the SAEG Statistic package (SAEG – UFV 9.0 ver-sion).

3. Results and discussion

The aim of this study was to characterize some of the ecophysio-logical aspects of macaw palms cultivated on an open area withoutany specific treatments. The results are divided into two parts: gen-eral gas exchange responses and a physiological and nutritionalprofile of the canopy.

3.1. Macaw palm exhibits a C3 pattern of photosynthesis with ahigh quantum yield

When water and nutrients needs are secure, most plant speciesundergo gas exchange between leaves and the atmosphere in a pre-dictable fashion within a 24-h period that parallels the availabilityof sunlight. These rates usually reach a maximum value at the mostpropitious combination of light, humidity and temperature withinthe surroundings (Schulze et al., 2005; Pugnaire and Valladares,2007).

By following the in situ available PPFD (Fig. 4), it was revealedthat the gas exchange parameters of juvenile macaw palm plantsvaried according to the time of day (Fig. 5). Since the location

Fig. 4. Average photosynthetic photon flux density (PPFD) during the measure-ments regarding the diel course of gas exchange of juvenile macaw palm plantscultivated under field conditions.

is prone to unpredictable changes in the atmosphere due to itshigh altitude and mountain topography, the observed discrepan-cies on hourly PPFD and photosynthesis rate may be related toenvironmental constraints, especially cloud formation near noontime.

The net photosynthetic rate (A) of macaw palm increased dur-ing the morning hours and reached its peak (16.69 �mol m−2 s−1)before noon (Fig. 5A). A weak linear correlation between A and gs

was obtained (r = 0.45). Diel gs was high and stable, except during

Fig. 5. Diel course of leaf gas exchange of juvenile macaw palm plants cultivated under field conditions. (A) A – net photosynthesis rate; (B) gs – stomatal conductance; (C) E– transpiration rate; (D) Ci/Ca – ratio between the concentrations of CO2 in the substomatic chamber and the atmosphere. Data are means ± S.E. for n = 10.

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Fig. 6. Photosynthetic light response curve of net photosynthesis (A) of juvenile macaw palm plants cultivated under field conditions. Inserted table variables: Rd – darkrespiration (�mol m−2 s−1), – apparent quantum efficiency, LCP – light compensation point (�mol m−2 s−1), LSP – light saturation point (�mol m−2 s−1), Amax calc – calculatedmaximum net photosynthesis (�mol m−2 s−1), Amax obs – observed maximum net photosynthesis (�mol m−2 s−1). *Significant at P ≤ 0.05. Data are means ± S.E. for n = 10.

dawn and dusk. The low values of A observed in these two periodscan be attributed to the lack of light energy. Also, because the regu-lation of guard cell movement is light- dependent the limitation of Ain the dawn and dusk can be related to stomatal restriction (Fig. 5B).The maintenance of high values of gs near noon time, combinedwith increasing values of the Ci/Ca ratio (Fig. 5D), indicates thatthe limitation of photosynthesis in macaw palm, during this periodof the day, might be the result of non-stomatal regulation as partof a daily pattern. The circadian routine is as follows: after the CO2assimilation process during the morning hours, there is an accumu-lation of metabolites (trioses, starch) in the chloroplast that slowsdown photosynthesis (Pugnaire and Valladares, 2007; Gessler et al.,2008). During peak sunlight hours, a momentary decay in photo-synthesis can occur as a sign of an ongoing protective mechanismagainst photodamage, thus preserving the integrity of the photo-synthetic apparatus (Lambers et al., 1998; Kitao et al., 2012). Thecourse of the transpiration rate (E) in macaw palm was similar tothe A pattern to some extent (Fig. 5C). The constancy of gs duringmidday hours also assured that a high E was maintained. The loss ofwater vapor by leaves can act as a cooling system, minimizing thedetrimental effects of heating due to the constant exposure of theorgan to increasing air temperature and light intensity; this eventalso helps to keep net photosynthesis at a satisfactory state (Greer,2012).

This diel course of gas exchange observed in juvenile macawpalms is quite often observed in plants with C3-type carbonmetabolism (Gessler et al., 2007; Takagi, 2009). While the photo-synthetic pattern of a given species is an intrinsic characteristic, theintensity of photosynthesis is greatly influenced by extrinsic fac-tors. Among these environmental factors, light intensity can greatlyimpair carbon assimilation by affecting the stomatal response or byinterfering with the capability of photosystem II to use light energyand predisposing it to photoinhibition phenomenon (Powles, 1984;Alves and Magalhaes, 2002).

The photosynthetic light response curve of macaw palms fol-lowed the classical pattern of species with C3 carbon metabolism,with well-defined rising and stead-state phases in the curve (Fig. 6).Microscopic observations in fresh leaf slices of macaw palm didnot reveal a Kranz anatomy pattern. The macaw palm was able

to maintain a high photosynthetic rate under light intensities upto 2000 �mol m−2 s−1, the maximum level provided by the equip-ment, without indications of photosynthesis decay. The stationaryphase in photosynthesis may represent biochemical incapacity tokeep up with incremental increases in light; however, the param-eters derived from this curve and depicted in the inserted tableindicate a considerably high photosynthetic efficacy in this palmin regard to the use of light. An observed light compensation point(LCP) of 2.9 �mol m−2 s−1 reveals that this species is capable of ini-tiating the carbon assimilation process in very dim light conditions.A light saturation point (LSP) of approximately 350 �mol m−2 s−1

indicates that the net photosynthesis rate saturates rapidly. Themacaw palm also minimizes respiratory costs, as evidenced by alow respiratory rate (Rday) (0. 22 �mol m−2 s−1). Similar LCP andRday values were found in the early successional Guazuma ulmi-folia cultivated under different light conditions. The species alsodisplayed high photosynthetic light acclimation capacity (Porteset al., 2010). Gomes et al. (2008) and Lamade and Setiyo (1996),working with coconut and oil palm respectively, found valuesof LCP ranging from 10.5 to 20 �mol m−2 s−1 and Rday rangingfrom 0.34 to 2.99 �mol m−2 s−1. In this study, the values of LCPand Rday for the macaw palm were lower and corresponded tothose of shade plants (Taiz and Zeiger, 2006). This prompts fur-ther investigation, either through controlled experiments, with amore physiological/biochemical approach, or the use of differentstatistical tools.

A low LCP accompanied by a fast-rising CO2 assimilatory ratemay be an indicative that the species efficiently captures and useslight energy for the photosynthetic process (Singsaas et al., 2001;Sage and Kubien, 2007; Pallardy, 2008). A more suitable way toaccess this efficacy is by examining the apparent quantum yield(˛). The quantum yield denotes the proportion of CO2 moleculesassimilated per mol of quanta. This parameter tends to be lesssensitive to environmental variations because of its rather conser-vative nature (Waring and Running, 1998; Portes et al., 2010). Themacaw palms achieved an estimated apparent quantum efficiency(˛) of 0.077 mol/mol and an Amax of 26.3 �mol m−2 s−1, similar tovalues verified in tropical arborous species and in pioneer or sec-ondary tree species (Mielke et al., 2005; Portes et al., 2010; Dos

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Anjos et al., 2012) or in C3 and C4 species with herbaceous growth(Ehleringer and Björkman, 1977; Ehleringer and Pearcy, 1983; Sageand McKown, 2006). Values of above 0.05 mol/mol are strongindicators that a species has an efficient use of light in regard tocarbohydrate gain (Ehleringer and Pearcy, 1983). These values arewell observed in plants adapted to sunny conditions and allowplants to thrive in light intensities that would otherwise be stressful(Singsaas et al., 2001; Skillman, 2008). For a whole-plant perspec-tive, efficient light capture, minimizations in respiratory costs andlow LCP contribute to effective carbon metabolism (Givnish, 1998).Plants species that exhibit this trait can constantly invest in growth,reserve or biomass accumulation, potentially leading to great pro-ductivity.

In fact, macaw palm and Amax values are similar to thoseobserved in the oil palm. Lamade and Setiyo (1996) studied dif-ferent clones of oil palm and found values of Amax and ofapproximately 26 �mol m−2 s−1 and 0.07 mol/mol, respectively;due to these elevated photosynthetic parameters values, theauthors emphasized that the oil palm resembles a C4 species morethan a C3 species. The macaw palm is an arborous monocotyle-donous plant without true secondary growth and most likely usesits high and net carbon assimilation to sustain fruit production.This has been suggested in both coconut and oil palms (Jayasekaraand Jayasekara, 1995; Lamade and Bouillet, 2005; Mialet-Serraet al., 2005). These three palm species produce large inflorescencesand fruit bunches that can take 6–12 months to develop and maturecompletely. To ensure a constant flow of reserves for fruit formationand secure future growth, plants must use morphological and/orphysiological mechanisms to improve carbohydrate production.This can be achieved by a great leaf area and effective photosyn-thesis (Jayasekara and Jayasekara, 1995; Pugnaire and Valladares,

Fig. 7. Correlation between leaf temperatures (◦C) versus net photosynthesis (A)of juvenile macaw palm plants cultivated under field conditions. *Significant atP ≤ 0.05. Data are measured values, n = 10.

2007), which seems to be the case in macaw palms. The leaves ofmacaw palms contain profuse parallel venations (data not shown),which account for high vein density and tight vein spacing. Thischaracteristic shared among monocotyledonous plants, leads to ashorter interveinal distance and can contribute to faster loadingand unloading of photosynthates between leaf tissues cells, thuscreating a favorable scenario for a greater quantum yield (Sage andMcKown, 2006).

Fig. 8. Variation of gas exchange parameters regarding the leaf position, top to bottom, in the canopy of juvenile macaw palm plants cultivated under field conditions. (A) A– net photosynthesis rate; (B) gs – stomatal conductance; (C) E – transpiration rate; (D) Ci/Ca – ratio between the concentrations of CO2 in the substomatic chamber and theatmosphere. Different letters indicate significant differences by Scott–Knott test (P ≤ 0.05). Each value represents the average reading of leaflets positioned in three distinctportions of the rachis, i.e. distal, middle and proximal. Data are means ± S.E. for n = 8.

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Fig. 9. Variation of gas exchange parameters regarding the leaflets positions, distal, middle and proximal, in the rachis of macaw palm fronds. (A) A – net photosynthesisrate; (B) gs – stomatal conductance; (C) E – transpiration rate; (D) Ci/Ca – ratio between the concentrations of CO2 in the substomatic chamber and the atmosphere. Differentletters indicate significant differences by Scott–Knott test (P ≤ 0.05). Data are means ± S.E. for n = 8.

Plant metabolism, particularly photosynthesis, is governed bythe activity of enzymes that are temperature dependent. A photo-synthetic resilience to temperature alterations in the macaw palmwas also detected in this study. The process remained functionaleven when the leaf temperature rose above 30 ◦C, so much sothat the leaf temperature was strongly and positively correlated(r = 0.95, *P ≤ 0.05) with A (Fig. 7). Temperature is a major regulatorof physiological processes in plants because it affects both sto-matal conductance and enzyme kinetics (Ruelland and Zachowski,2010). When leaf temperature rises, it often triggers a constrictionresponse in the carbon assimilation capacity due to the thermalliability of the key photosynthetic enzymes, Rubisco, RUBPkinaseand FBPase, even at a moderately high temperature of 30–35 ◦C(Feller et al., 1998; Salvucci and Crafts-Brandner, 2004). Plantsthat withstand the harmful effects of high temperature on the netphotosynthesis rate must possess mechanisms that either help dis-sipate excess heat or help the plant tolerate heat. Some phases of thephotosynthetic process are more prone to heat stress than others,even within the same plant (Schulze et al., 2005; Sage and Kubien,2007). The inhibition of photosynthesis in Quercus pubenscens dueto high temperature was correlated with a reduction in the Rubiscoactivation state, whereas the integrity of thylakoid components andelectron transport were protected (Haldimann and Feller, 2004).Enhancements in the capture of CO2 trough enzymatic or anatomicdevices, e.g., PEPcase activity and Kranz-like syndromes, can alsolessen heat susceptibility in plants (Sage and Kubien, 2007). Regard-less of whether heat resistance in macaw palms is due to toleranceor avoidance strategies, it has an evident flexibility to occupy siteswhere environmental factors such as temperature, light intensi-ties, and water availability are challenging. Macaw palms naturallyprosper within the large Brazilian ecoregion known as the cerrado,in which climatic conditions are similar to those of the tropicalsavanna (i.e., elevated temperatures, high solar radiation and a lin-gering seasonal lack of rainfall).

3.2. Foliar physiological and mineral profiles create a mosaicalong the canopy of juvenile macaw palm plants

The photosynthetic capacity of a leaf is generally a function ofits age; often this capacity exhibits a steady decline after full leafexpansion. In plants that display a spiral phylotaxy, such as themacaw palm, leaf age and position usually overlap. Measurementsmade in the palm help to clarify and map the gas exchange patternof the species.

The gas exchange parameters of macaw palms followed theabove-mentioned archetype, as evident in Fig. 8, creating a pho-tosynthetic mosaic in the canopy. The rate of CO2 net gain (A)dropped as much as 46% from the top to bottom leaves, witha strong negative correlation between A and the age/position ofthe leaf (r = −0.99, *P ≤ 0.05). This result could be related to thedegree of stomata aperture (gs), which substantially decreased,by 52%, between the top and bottom leaf. This age-relateddecline in photosynthesis is not an uncontrolled event of phys-iological deterioration; instead, it is influenced by a myriadof factors, ranging from hormone and enzyme balance (Guinnand Brummett, 1993) to the accumulation and redistribution ofmetabolic resources (Kitajima et al., 2002; Ishimaru et al., 2004).For example, the rates of photosynthesis in wheat were stronglycorrelated with the level of 3-phosphoglycerate and inversely cor-related with the level of triose phosphate; while the activity ofmany enzymes changed during leaf maturation, the main con-trol was attributed to RUBP carboxylase (Suzuki et al., 1987).This key enzyme is affected by a change in the ABA level as theleaf ages (Seemann and Sharkey, 1987). External factors, suchas the light microenvironment, may also contribute to a signifi-cant correlation between leaf position and photosynthetic capacity(Kitajima et al., 2002). The upper leaves of the macaw palm castshade upon the lower leaves, limiting light availability at the leafsurface.

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Table 1Foliar mineral nutrient content, dry weight basis, of juvenile macaw palm plants cultivated under field conditions: N – nitrogen, P – phosphorus, K – potassium, Mg –magnesium and Fe – iron. Different letters indicate significant differences by Scott–Knott test (P ≤ 0.05). Data are means ± S.E. for n = 8.

Nutrient Leaf position

1 2 3 4 5 6 7

N (dag kg−1 D.W.) 2.80 ± 0,17a 2.50 ± 0,16a 2.53 ± 0,15a 2.29 ± 0.15b 2.26 ± 0.15b 2.14 ± 0.10b 2.11 ± 0.04b

P (dag kg−1 D.W.) 0.18 ± 0.01a 0.17 ± 0.02a 0.16 ± 0.01a 0.17 ± 0.01a 0.14 ± 0.01b 0.14 ± 0.01b 0.14 ± 0.01b

K (dag kg−1 D.W.) 0.76 ± 0.04a 0.67 ± 0.06a 0.63 ± 0.03a 0.63 ± 0.01a 0.56 ± 0.07a 0.53 ± 0.03a 0.53 ± 0.01a

Mg (dag kg−1 D.W.) 0.17 ± 0.01a 0.21 ± 0.01a 0.23 ± 0.01a 0.24 ± 0.04a 0.24 ± 0.04a 0.27 ± 0.05a 0.24 ± 0.02a

Fe (mg kg−1 D.W.) 167.67 ± 16.22a 149.33 ± 2.60a 187.67 ± 23.02a 273.33 ± 4.33a 183.33 ± 33.89a 256.00 ± 51.88a 200.00 ± 4.00a

Even though the greatest values of A and gs in macaw palm werefound in the first expanded leaf (leaf 1), the highest Ci/Ca ratioreveals biochemical inefficiency when assimilating CO2 (Fig. 8D).This carboxylative limitation is most likely due to the physiologi-cal immaturity of leaves that, together with a high E, characterizethem as sink organs. This particular leaf is not a good candidatefor future use in ecophysiological studies. In the remaining leaves,more stable readings of gas exchange were achieved as early as thesecond leaf in sequence. The second and third leaves (leaf 1 and 2)differed from older leaves by the Scott–Knott test (p < 0.05). In oilpalm, the variation in photosynthetic rate and associated param-eters follows a similar trend; unlike macaw palms, the first fullyexpanded leaf shows the lowest value of A, which is also attributedto physiological immaturity (Suresh and Nagamani, 2006).

Leaf metabolic activity and content also vary according to loca-tion on the blade (Ishimaru et al., 2004). Long feathery leaves mayshow this heterogeneity in a more noticeable way due to organ size,and the sink-source transition depends on leaflet position withinthe rachis (Pugnaire and Valladares, 2007; Corley and Tinker, 2003).Data in Fig. 9A clearly indicate a greater photosynthetic capacity inleaflets occupying the middle portion of the rachis of macaw palmfronds. The same leaflets presented the highest gs (Fig. 9B), eitherbecause of a greater quantity of stomata or due to better control ofstomatal aperture.

One way to approximate leaf maturity and photosyntheticcapacity is to examine pigment content. In most cases, chlorophyllcontent changes consistently with different stages of leaf develop-ment (Pugnaire and Valladares, 2007). The lower average valuesof total chlorophyll content in macaw palm leaves corresponded tothose fronds either too young (leaf 1 and 2) or in the lowest positionin the sequence (leaf 6 and 7); this can be translated into their matu-rity level along the canopy profile (Fig. 10A). As mentioned earlierthere was a steep decline in macaw palm photosynthesis related tothe position of the leaves. The chlorophyll content among the leavesdid not differ significantly, except for leaf 5, so a strong correlationbetween these two variables is unlikely. This finding related wellwith the works of Suzuki et al. (1987) and Kura-Hotta et al. (1987).In both studies, photosynthetic activity in monocotyledons specieswas weakly linked to the chlorophyll content of aging leaves. Kura-Hotta et al. (1987) suggested that the decrease in photosynthesis inrice was caused mainly by the inactivation of photosystem II reac-tion centers rather than the breakdown of chlorophyll during leafsenescence. This proves once again that plant metabolism is com-plex. The total carotenoid content of macaw palms confirmed thatall examined leaves were not undergoing the senescence process(Fig. 10B).

Leaf physiology is directly affected by the amount of mineralnutrients, several of which are involved in the photosynthetic pro-cess (Marschner, 1995). Nitrogen, for instance, is a constitutiveelement largely required for protein synthesis and plant growth.In the leaves, nitrogen is found abundantly in Rubisco and chloro-phyll molecules. Data representing nutrient content in juvenilemacaw palm leaves are presented in Table 1. In the present study,the nitrogen content was significantly diminished in leaf 4 com-pared to leaf 3, similar to the results of a coconut palm study

(Broschat, 1997). This decay may be related to the decrease in netphotosynthesis in the macaw palm leaves as they age. Meziane andShipley (2001) suggested in their model that nitrogen levels in theleaf directly affect net photosynthetic rates and stomatal conduc-tance. Phosphorus content also differed between leaves, with thelower levels found in leaves 5, 6 and 7. Foliar phosphorus content isone of the most important elements in bioenergetics; inadequaciescan compromise the efficiency of metabolic processes, particularlywhere the availability of its inorganic form (Pi) affects the dynam-ics and yield of end products such as ATP and hexose-phosphate(Ramaekers et al., 2010; Hammond and White, 2011). The nutri-ents potassium, iron and magnesium showed no major difference incontent between leaves (Table 1). These nutrients are directly andindirectly involved in the photosynthetic process in the followingways: as an osmotic agent, as translocation and enzymatic co-factors and as electron transport chain and chlorophyll components

Fig. 10. Foliar pigment contents regarding leaf position, top to bottom, in the canopyof juvenile macaw palm plants cultivated under field conditions. (A) total chloro-phyll (chla + chlb). (B) carotenoids. Different letters indicate significant differencesby Scott–Knott test (P ≤ 0.05). Data are means ± S.E. for n = 8.

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(Marschner, 1995). Stable concentrations of nutrients are criticalto maintaining physiological mechanisms under a suitable perfor-mance and to maintaining long lasting leaves, such as in the macaw,oil and coconut palms. One characteristic of palm species is the highiron content in the leaf biomass (approximately 100 mg kg−1) (Nget al., 1968; Goh and Hardter, 2003; Wijebandara and Ranasinghe,2004). A greater requirement for iron may be linked to a greaterphotosynthetic capacity of these arborous palms; this metal is apowerful redox element in protein complexes involved in electrontransport within the thylakoid membrane, and its availability canhave a strong influence in the PSI/PSII ratio (Eberhard et al., 2008).

Information concerning nutrient content and translocation intropical species is scarce. The selection of tissues for nutrientanalysis is largely based on logistics rather than sensitiveness todeficiency The partial results in this study suggest for the first timethat N and P content is based on leaf position in cultivated macawpalm plants. In the oil palm, the most extensively studied palmtree, the following factors have a critical effect on leaf nutrient con-centration: leaf age, leaflet position, leaf number, tree age, fruitingcycle, planting material, tree density, fertilizer treatment, rainfalland soil composition (Corley and Tinker, 2003). There exists a needto study macaw palm nutrition further if it is to be considered as anovel oil crop.

4. Conclusion

In the present study, the general pattern of gas exchange injuvenile macaw palm trees grown under field conditions wasrevealed. Daytime photosynthesis and related variables followedthe standard pattern for most C3 species, with peak results reachedin the morning hours. The light curve response also displayed aC3 pattern; however, this species must sustain a high quantumefficiency and photosynthetic capacity. Gas exchange parametersin the fronds along the canopy varied according to the leaf posi-tion and the insertion location of leaflets in the rachis. Overallvalues indicate that the second and third leaves and the leafletsin the middle of the rachis have the greatest physiological capac-ity. Foliar pigments and mineral content were relatively stablebetween leaves, which is a pre-requirement for long-lasting func-tional leaves.

The ecophysiological gas exchange traits of this palm treeresemble those of oil palms. But unlike the African palm, the macawpalm is adapted to a wide range of environmental conditions, giventhe fact that it is broadly distributed in the Brazilian territory andin tropical America as a whole. The combination of the macawpalm’s ecological plasticity, its physiological attributes and its highproductivity makes this plant suitable for new crop development.Although it is not an easy task, the domestication of native speciesmust incorporate knowledge from different fields to be successfulfrom both agronomic and environmental perspectives. We expectthat the present findings will contribute to the understanding ofthis species and create awareness for a new vegetable oil sourcethat can be used worldwide.

Acknowledgements

This work was funded by the Brazilian agencies: Fundac ãode Amparo a Pesquisa do Estado e Minas Gerais (FAPEMIG),Coordenac ão de Aperferic amento de Pessoal de Nivel Superior(CAPES) and with the support of the Department of Plant Science,Universidade Federal de Vic osa (UFV).

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