LEAF MICRONUTRIENT CONCENTRATIONS AND POTENTIAL PHOTOSYNTHESIS IN Ochroma pyramidale ESTABLISHED IN A DEGRADED LAND

Ricardo A. MARENCO1*, Gil VIEIRA1 and José F. de C. GONÇALVES1

ABSTRACT : In the Brazilian Amazon, large areas of abandoned lands may revert to secondary forest. In the process, pioneer tree species have an important role to restore productivity in old fields and improve environmental conditions. To determine potential photosynthesis

(Apot), stomatal conductance (g ), transpiration (E), and leaf micronutrient concentrations in s Ochroma pyramidale (Cav. ex Lam.) Urban a study was carried out in the Brazilian Amazon o o (01 51' S; 60 04' W). Photosynthetic parameters were measured at increasing [CO2], saturating light intensity (1 mmol (photons) m-2 s-1), and ambient temperature. The rate of

electron-transport (J), Apot, and water-use efficiency (WUE) increased consistently at

2 2 increasing internal CO concentration (Ci). Conversely, increasing [CO ] decreased gs, E,

2 2 and photorespiration (Pr). At the CO -saturated region of the CO response curve (1.1 mmol -1 µ - -2 -1 µ -2 -1 (CO2) mol (air)), J was 120 mol (e ) m s and Apot reached up to 24 mol (CO2) m s . -2 -1 Likewise, at saturating Ci, gs and E were 30 and 1.4 mmol (H O) m s , respectively, and P 2 r µ -2 -1 µ - about 1.5 mol (CO2) m s . Foliar nutrients were 185, 134, 50, and 10 mol (element) m 2 (leaf area) for Fe, Mn, Zn, and Cu, respectively. It was concluded that [CO ] probably 2 limits light saturated photosynthesis in this site. Furthermore, from a nutritional point of view, the low Fe to Cu ratio (15:1) may reflect nutritional imbalance in O. pyramidale at this site.

KEYWORDS: Balsa wood, electron-transport rate, reforestation, stomatal conductance, transpiration, water-use efficiency.

CONCENTRAÇÃO DE MICRONUTRIENTES NAS FOLHAS E FOTOSSÍNTESE POTENCIAL EM Ochroma pyramidale ESTABELECIDO NUMA ÁREA DEGRADADA

RESUMO : Extensas áreas abandonadas na Amazônia brasileira revertem para floresta secundária. Neste processo, as espécies pioneiras desempenham um papel importante na recuperação da produtividade de campos abandonados e na melhoria das condições ambientais. Para

determinar a fotossíntese potencial (Apot), condutância estomática (gs), transpiração (E), and a concentração de micronutrientes na folha em Ochroma pyramidale (Cav. ex Lam.) Urban um estudo foi realizado na Amazônia brasileira (01o 51' LS; 60o 04' LO). Os parâmetros

1 Instituto Nacional de Pesquisas da Amazônia, Coordenação de Pesquisas em Silvicultura Tropical, Caixa Postal 478, 69011-970 Manaus, AM. *Corresponding author E-mail: [email protected]

ACTA AMAZONICA 33 (1): 23-31. 2003. 23 fotossintéticos foram medidos a níveis crescentes de CO2 sob luz saturante (1 mmol (fótons) -2 -1 m s ) e temperatura ambiente. A taxa de transporte de elétrons(J), Apot e a eficiência no uso d’água (WUE) aumentaram consistentemente com aumentos na concentração interna

de CO2 (C ). Ao contrário, aumentos na [CO2] diminuíram gs, E e a fotorrespiração (Pr). Na i -1 µ - região da curva saturada pelo CO2 (1.1 mmol (CO2) mol (ar)), J e Apot foram 120 mol (e

-2 -1 µ -2 -1 m s e 24 mol (CO2) m s , respectivamente. Paralelamente, sob Ci saturante, gs and E foram 30 e 1.4 mmol (H O) m-2s-1, respectivamente, enquanto que P foi em torno de 1.5 2 r µ -2 -1 µ mol (CO2) m s . Os teores de micronutrientes da folha foram 185,134, 50 e 10 mol (elemento) m-2 (área foliar) para Fe, Mn, Zn e Cu, respectivamente. Foi concluído que a

[CO2] provavelmente limita a fotossíntese sob luz saturante neste sítio. Além disso, do ponto de vista nutricional, a baixa relação ferro:cobre, de 15 para 1, pode indicar um debalanço nutricional em O. pyramidale neste sítio.

PALAVRAS-CHAVE: condutância estomática, eficiência no uso d’água, pau-de-balsa, eflorestamento, taxa de transporte de elétrons, transpiração.

INTRODUCTION photosynthesis in several ways. Micronutrients such as iron, manganese, and Many factors, such as availability of copper are constituents of proteins involved water, carbon dioxide, light, and nutrients in electron transfers. For example, Cu is a affect photosynthesis in several ways. component of plastocyanin and Fe is a

Increases in CO2 concentrations enhance constituent of cytochromes and required for photosynthetic rates in C3 plant species. chlorophyll biosynthesis (Beale, 1999),

Whereas, compared with C3 plants, C4 plants, whereas Mn plays a key role in which are able to concentrate CO2, show photosynthetic O2 evolution. Zn, on the other higher photosynthetic rates and are better hand, is required as a structural component of adapted to tropical regions exposed to higher several enzymes (e.g., carbonic anhydrase, temperatures and soils with lower water super oxide dismutase) and for ribosomes availability. In Brazilian Amazonia, large areas synthesis and activity (Marschner, 1995). of abandoned lands may revert to secondary Ochroma pyramidale is a pioneer forests (Houghton et al., 2000). In this process neotropical tree that grows under moist and pioneer tree species have an important role in warm conditions on disturbed lands or as a restoring productivity in old fields and colonizer of large gaps in the secondary rain improve environmental conditions. Although forest (Whitmore & Wooi-Khoon, 1983; pioneer tree species are greatly important to Kammesheidt, 2000). Its high performance in restore soil fertility of degraded lands, little is large gaps has been attributed to a high known about the physiology of pioneer trees investment in leaf biomass, which results in a in these degraded habitats. high leaf area ratio (Dalling et al., 1999). Its

In addition to CO2, light and growth is faster in fertile soils when mean temperature, mineral nutrition affects temperature ranges from 25 to 30 oC and

24 Marenco et al. average annual rainfall is from 1500 to about compared these values with published data 2000 mm (Francis, 1991; Butterfield, 1996). (e.g., Oberbauer & Strain, 1984; Neves et al.,

Besides its fast growth, direct solar radiation 1999). We also compared Apot with

(full sun) apparently does not depress photosynthetic rates of C4 plants, a group of photochemical efficiency of Ochroma seedlings plants with CO2-concentrating mechanisms. In grown with adequate availability of water and the absence of gas exchange data from C4 tree nutrients (Castro et al., 1995). Acclimation of grown in the open, we use C4 data from Ochroma and other pioneer species to high-light herbaceous dicots reported elsewhere stress under strong radiation has been attributed (Grodzinski et al., 1998). at least in part to their capability to increase the levels of photoprotective pigments (e.g., b- MATERIALS AND METHODS carotene) and the chlorophyll a/b ratio (Krause et al., 2001). Ochroma may exhibit high Data were collected from Ochroma photosynthetic rates under ambient CO2 pyramidale (Cav. ex Lam.) Urban, Bombacaceae, concentrations (Oberbauer & Strain, 1984; (hereafter, Ochroma) grown on experimental Dalling et al., 1999). However, in degraded plots located near Presidente Figueiredo (01o 51' landscapes, low availability of nitrogen and S; 60o 04' W) in the Brazilian Amazon. Ochroma magnesium appears to be factors that limit was chosen because it is one of the faster-growing carbon gain in this species (Marenco et al., 2001 species in the neotropical region under favorable a). The fast growth of Ochroma saplings conditions (Butterfield, 1996). makes this species potentially useful in The region has a humid tropical climate reforestation projects on sites with proper and receives an annual precipitation of about management, but other species should be 2200 mm, with a wet season from October considered for reforestation over large regions through June. Mean temperature is around 27 on poor soils where plantation maintenance is oC. Net assimilation rate (A), stomatal scarce (Butterfield, 1996). When Ochroma is conductance to water vapor (gs), transpiration planted in mixtures with late successional, (E), and leaf dark respiration (Rd) were measured slower-growing species, it may provide shading using an portable photosynthesis system with for the seedlings of the slower-growing species onboard LED light source and dioxide mixer to and improve soil fertility by nutrient cycling. control CO2 partial pressure (LI-6400, Li-Cor, In this study we hypothesized that Lincoln, Neb., USA). Data were collected from potential photosynthesis (Apot) (i.e., the light- September 2000 to March 2001 on fully saturated photosynthesis at CO2-saturated expanded leaves of similar age and appearance. conditions) and other photosynthetic Four one-year-old plants were randomly parameters, as well as the foliar micronutrient selected for measurements from a population of content of pioneer tree species are lower when around 100 saplings. Gas exchange parameters grown in degraded lands than under controlled were measured on fully expanded leaves (two conditions or in mature forests. Therefore, we leaves per plant) between 0900 and 1500 h. determined leaf gas exchange parameters and Measurements were taken only in open sky leaf micronutrient concentrations in O. days. Thus, when measurements were pyramidale grown in a degraded landscape and interrupted due to rainy conditions, a new set

Leaf Micronutrient Concentrations... 25 of data was taken again another day, in the same intensity and ambient CO2) and micronutrient plant. concentration was also calculated. Individual leaves were treated as sub RESULTS samples. CO2 response curves were determined for atmospheric CO2 concentration (Ca) between 15 and 2000 µmol mol-1. During measurements, Gas exchange and electron-transport light intensity was maintained at 1 mmol -2 -1 µ - (photons) m s within the leaf chamber. At ambient Ca (Ci = 255 mol(CO2) mol 1 Electron-transport rate (J) was determined (air)), light-saturated photosynthesis (Amax) µ -2 -1 according to Farquhard & Von Caemmerer was 9.3 mol (CO2) m s , whereas at µ - (1982) as: saturating Ca (i.e., Ci = 1100 mol (CO ) mol 2 1(air)), A was 24 µmol(CO ) m-2s-1 (Figure J = 4 (Vc + Vo), pot 2 1). Electron-transport rates (J) increased from where Vc and V are the rate of o 81 to 120 µmol (e-) m-2 s-1, at increasing [CO ] carboxylation and oxygenation, respectively. Vc 2 is given by: above ambient Ca (Figure 1). The Ci/Ca ratios were 0.657 and 0.55 at ambient and saturating Vc = A + 0.5Vo + Rd.

Ca, respectively. E and g decreased at elevated C . E The oxygenation rate (Vo) can be s i Φ dropped from 2.7 to 1.49 mmol(H O) m-2 s-1 calculated as: Vo = (A + Rd) / (1/ - 0.5), being 2 -2 -1 Φ described by the following equation as and gs from 170 to 35 mmol (H2O) m s at

(Lambers et al. 1998): ambient and saturating CO2 concentration, Φ = 2 (3.7 + 0.188 (T – 25) + 0.0036 respectively (Figure 2). As a result of reduction 2 in water loss and increases in A at increasing (T-25) )/Pi, o Ci, WUE was much lower at ambient Ca than where T is temperature ( C) and Pi is the at elevated CO2 concentration (i.e., 5.43 versus CO2 partial pressure (Pa). Because Vo is twice -1 15.48 mmol(CO2) mol (H2O). The CO2 the rate of photorespiration, Pr was computed compensation point (Γ) was estimated as 59.2 as: Pr = Vo/2. Net photosynthetic rate (A) data µmol(CO )mol-1(air) (Figure 1). were fit using non-linear least squared 2 regression, according to the model proposed by Herrick & Tomas (2001) as: Leaf micronutrients (1-Ci/Γ) A = A’pot[1-(1-yo/A’pot) Leaf micronutrient concentrations on a Γ leaf area basis were 185, 134, 50, and 10 µmol where yo is the y-intercept, is the (element) m-2 for Fe, Mn, Zn, and Cu, CO2-compensation point, and A’pot is the respectively. The Amax to micronutrient ratio computed Apot (i.e., the actual light-saturated - ranged from 50 to 883 mmol(CO2) mol photosynthesis at saturating Ci). 1(element) s-1. Highest and lowest A :nutrient Micronutrients (Fe, Zn, Mn, and Cu) max were determined by atomic absorption ratios involved Cu and Fe, respectively (Table spectrophotometry (Perkin Elmer 1100B, 1). The Fe to Cu ratio was rather low (15:1), Überlingen, Germany) as described by which may indicate nutritional imbalance in this Miyazawa et al. (1999). The ratio between species.

Amax (i.e., net assimilation at saturating light

26 Marenco et al. 35 160

30 140

J 25 120 O)) 2 A ), (H

-1 J -1 -1 s ( -2 -2 20 100 µ mol ( mol ) mol ) m 2 2

WUE e

15 80 - ) m -2 mol (CO mol s µ ( 10 60 -1 ) A WUE (mmol WUE (CO 5 40

0 20

-5 0 0 500 1000 1500

µ -1 Ci ( mol(CO2) mol (air))

Figure 1. Electron-transport rates (J), net photosynthesis (A), and water-use efficiency (WUE) in Ochroma pyramidale grown in experimental plots near Presidente Figueiredo (AM) as a function of the internal

CO2 concentration (Ci). Vertical dashed line shows Ci at ambient CO2 concentration (i.e., Ci = 254 µ -1 • ∆ mol mol ; Ci/Ca = 0.67). Symbols: o, electron-transport rates; , net photosynthesis; , water- 2 • (1-Ci/59.2) 2 use efficiency. J(o) = -66.72 + 26.71 ln Ci, R = 0.79; A( ) = 26[1 - (1+3.83/26) , R = 0.94; ∆ 2 Γ µ - WUE( ) = -32.02 + 6.78 ln Ci, R =0.89. The CO2 compensation point ( ) was 59.2 mol(CO2) mol 1 (air); ln, natural logarithm. Each point is the mean of four plants and two leaves per plant.

600 6 P r (

5 µ mol (CO

450 ) 2

P ) m -1 r 4 s -2 -2 -2 s

E -1 ), O) m O) 2

300 3 E (mmol (H (mmol (mmol (H

s 2 g 2 O) m 150 -2 1 s -1 )

g s 0 0 0 500 1000 1500

-1 C i (µmol(CO2 ) m ol )(air))

Figure 2. Stomatal conductance (gs), transpiration (E), and photorespiration (Pr) in Ochroma pyramidale

grown in experimental plots near Presidente Figueiredo (AM) as a function of the internal CO2

concentration (Ci). Vertical dashed line shows Ci at ambient CO2 concentration (i.e., Ci = 254 µ -1 •, ∆ mol(CO2) mol (air); Ci/Ca = 0.67). Symbols: o, stomatal conductance; transpiration; , 2 • 2 ∆ photorespiration. gs(o) = 670.9 - 90.8 ln Ci, R = 0.49; E( ) = 7.23 - 0.82 ln Ci, R = 0.41; Pr( ) 2 = 8.43 - 0.99 ln Ci, R = 0.64; ln, natural logarithm. Each point is the mean of four plants and two leaves per plant.

Leaf Micronutrient Concentrations... 27 Table 1. Leaf micronutrient concentrations and Amax to nutrient ratio in Ochroma pyramidale grown in experimental plots near Presidente Figueiredo, AM. Each value is the mean of four plants (± S.D).

Mean ± S.D Critical Amax to nutrient Parameter Mean ± S.D deficiency levels1 ratio2 -1 -2 -1 -1 -1 (mg kg DM) (µmol m leaf area) (mg kg DM) (mmol (CO2) mol s ) Iron 100.5 ± 19.1 185.1 ± 3.53 50 to 150 50.2 Zinc 32.0 ± 3.6 50.3 ± 5.7 15 to 20 184.7 Manganese 71.5 ± 5.5 133.9 ± 10.3 10 to 20 69.5 Copper 6.5 ± 1.0 10.5 ± 1.6 1 to 5 883.6 1-Leaf critical deficiency content according to Marschner (1995) 2 µ -2 -1 For an Amax of 9.3 mol(CO2) mol s

DISCUSSION bear in mind that leaf response to short-term

exposure to elevated [CO2] should not be Gas exchange and electron-transport extrapolated to whole-plant response over the long-term because several factors may

Mean Amax was much lower than modulate plant response to permanent previously reported for Ochroma (i.e., 9.3 exposure to elevated atmospheric [CO2]. versus 27 µmol (CO ) m-2 s-1.) (Figure 1, Compared with ambient [CO ], short-term 2 2 Oberbauer & Strain, 1984). This difference exposure to elevated [CO2] decreased Pr by was attributed to the fact that Oberbauer & µ -2 -1 50%, from 2.9 to 1.46 mol(CO2) m s Strain collected their data from plants grown (Figure 1). at near-optimal conditions. Thus, compared The CO2 compensation point found in with Ochroma grown in controlled conditions, µ -1 O. pyramidale (i.e., 59 mol(CO2) mol , our results suggest that in this degraded Figure 1) was lower than previously reported landscape, environmental factors such as for Swietenia macrophylla, another light- availability of nutrients in the soil may limit demanding species (Marenco et al., 2001 b), photosynthesis in this species. However, our due to the lower respiration rates of Ochroma. A values were comparable to values max Our Ci/Ca values were lower than those obtained for other pioneer tree species grown previously reported for other rainforest under natural environments (Zotz & Winter, species (Carswell et al., 2000). Differences in 1994; Ishida et al., 1999). the Ci/Ca ratio among plant species have been

On the other hand, Apot reported in this attributed at least in part to variation in study is within the range observed for some stomatal conductance to CO2 (Ehleringer &

C4 dicot species such as Amaranthus Cerling,1995). retroflexus and Gomphrena globosa Transpiration rates and gs decreased (Grodzinski et al., 1998). One could suggest consistently at increasing [CO2] confirming that expected increases in atmospheric [CO ] 2 that at elevated CO2 supply water loss may could enhance photosynthetic rates of be reduced significantly. Thus, WUE was near Ochroma in the future. However, we must three times higher at elevated [CO2] than at

28 Marenco et al. ambient CO2 concentration (i.e., 5.43 versus by Glew et al. (1997). Taking into account the -1 15.48 mmol(CO2) mol (H2O)). If this trend critical deficiency levels established for higher is maintained at the whole plant level, we may plants (Marschner, 1995), we may conclude speculate that as atmospheric [CO2] increases that in terms of mineral nutrition, contents of Ochroma could colonize areas with rainfall Fe, Cu, and Zn were within the adequate range. lower than 1500 mm year-1 or areas with a On the other hand, Mn concentrations were longer drought period. Our maximum J values slightly high, but lower than levels considered were similar to those previously observed in excessive for several plant species (i.e., above the upper canopy of Inga sp. in an 200 mg kg-1) (Marschner 1995). Furthermore, undisturbed Amazonian forest (Carswell et al., from a nutritional point of view, the low Fe 2000), indicating that the photosynthetic to Cu ratio (15:1) may reflect nutritional system of Ochroma was apparently little or imbalance in O. pyramidale at this site. None not affected by the harsh environmental of micronutrients examined was apparently conditions of this degraded landscape. insufficient or excessive for limiting the growth of Ochroma in this site, in which high Leaf micronutrients growth rate has been observed (Barbosa et al., 2000). Little is known about the mineral composition of Ochroma. Therefore, in the CONCLUSIONS absence of data from this species, we compared our results with those obtained from other In this degraded landscape, a rather low µ tropical trees. Iron content of Ochroma was Amax was found in Ochroma (9.3 mol (CO2) -2 -1 almost twice as high as those previously m s ). Mean Apot reported in this study is reported for other tropical trees (e.g., Ceiba within the range observed for some C4 dicot pentandra, Virola surinamensis), grown on species suggesting that under optimal low fertility soils (Neves et al., 1999). environmental conditions photosynthetic rates However, these differences may not of Ochroma may increase significantly. necessarily imply shortage of this element in Transpiration rates and gs lowered drastically the soil because variations in Fe content among at elevated [CO2] confirming that at elevated species appear to be common for this element. CO2 concentrations water loss may be In Burkina Faso, for example, leaf Fe content significantly reduced, and as a result WUE ranged from values as low as 14 mg kg-1 up to may be increased. Considering the critical 155 mg kg–1 (Glew et al., 1997). deficiency levels for most higher plants, we Mn leaf content in Ochroma was within may conclude that the contents of Fe, Cu, and the range reported for C. pentandra and V. Zn were apparently adequate, whereas the surinamensis by Neves et al. (1999). Zn leaf content Mn was slightly high. Finally, none concentration, on the other hand, was higher of the micronutrients examined was apparently in Ochroma than in those species studied by insufficient or excessive for limiting the Neves et al. (1999). Compared with other growth of Ochroma in this site, although the tropical species, Mn, Zn, and Cu low Fe to Cu ratio (15:1) may reflect concentrations are within the range reported nutritional imbalance in this species.

Leaf Micronutrient Concentrations... 29 ACKNOWLEDGMENTS tropical trees. Physiol. Plant., 94:560-565.

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Leaf Micronutrient Concentrations... 31