Abstract
The indirect estimation of leaf area (LA) in plants using non-destructive methods is a useful tool in the biological and agronomic studies, to determining the size of the capture apparatus of light energy by plants. This study aimed to determine equations that better estimate the LA of Hymenaea courbaril L. using the non-destructive methods based on leaf maximum measurements (length and width). In addition, we intended to check the accuracy of LA reading when compared with destructive methods obtained by the image analysis software (ImageJ®) and leaf area meter (LI-3100 Li-Cor). About 1000 leaves were sampled from one year old plants. To validate the models, we used an extra sample of 500 leaves with distinct age, randomly selected and collected from different canopy levels of young and adult trees. The variability observed was extreme, with values of LA for each leaf ranging from 1650 to 14018 mm2. The LA values obtained with the LI-3100 integrator were higher than those obtained by the ImageJ® software at 2.7 % and with a high correlation between them. Among the models studied to estimate the LA based on non-destructive measurements, it can be said that linear and quadratic models as well as the ellipse formula can be safely used without differing significantly from the values obtained through the LI-3100 analyzer and ImageJ® software. Thus, it is possible to use non-destructive measurements for estimating the LA of H. courbaril with accuracy using allometric models, as well as ensuring that the ImageJ® software can replace the LI-3100 analyzer to determine the leaf area at the species investigated.
Similar content being viewed by others
Abbreviations
- W:
-
Width
- L:
-
Length
- LW:
-
Length × width product
- R 2 :
-
Determination coefficient
- SDR:
-
Standard deviation of residues
- MSE:
-
Mean square error
- MIN:
-
Minimum
- MAX:
-
Maximum
- MED:
-
Medium
- CV:
-
Coefficient of variation
- ASY:
-
Asymmetry
- KUR:
-
Kurtosis
- WS:
-
Wilks–Shapiro
- F:
-
Calculated F
- MSE:
-
Sum of the square error
- PRESS:
-
Sum of squared residual prediction
- SSE:
-
Sum of squared error
- MSPR:
-
Mean square error of prediction
References
Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophot Int 11:36–42
Antunes WC, Pompelli MF, Carretero DM, Damatta FM (2008) Allometric models for non-destructive leaf area estimation in coffee (Coffea arabica and Coffea canephora). Ann Appl Biol 153:33–40
Bianco S, Bianco MS, Carvalho LB (2008) Estimate of Ageratum conyzoides leaf area using leaf blade linear measurements. Acta Sci Agron 30:519–523
Blanco FF, Folegatti MV (2005) Estimation of leaf area for greenhouse cucumber by linear measurements under salinity and grafting. Sci Agric 62:305–309
Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310
Bonser SP, Aarssen LW (2009) Interpreting reproductive allometry: individual strategies of allocation explain size-dependent reproduction in plant populations. Persp Plant Ecol Evol System 1:31–40
Bosco LC, Bergamaschi H, Cardoso LS, Paula VA, Casamali B (2012) Selection of regression models for estimating leaf area of ‘Royal gala’ and ‘Fuji suprema’ apple trees under hail net and in open sky. Rev Bras Frutic 34:504–514
Buttaro D, Rouphael Y, Rivera CM, Colla G, Gonnella M (2015) Simple and accurate allometric for leaf area estimation in Vitis vinifera L. genotypes. Photosynthetica 53:1–8
Candido WS, Coelho MFB, Maia SSS, Cunha CSM, Silva RCP (2013) Model to estimate the leaf area of Combretum leprosum Mart. Acta Agron 62:37–41
Cargnelutti Filho A, Lopes SJ, Toebe M, Silveira TR, Schwantes IA (2011) Sample size to estimate the Pearson correlation coefficient among characters of Crambe abyssinica. Rev Cien Agron 42:149–158
Carvalho SJP, Christoffoleti PJ (2007) Leaf area estimation of five Amaranthus species using leaf blade linear dimensions. Planta Dan 25:317–324
Cermák J, Nadezhdina N, Trcala M, Simon J (2014) Open field-applicable instrumental methods for structural and functional assessment of whole trees and stands. iForest: Biogeo For 8:226–278
Cristofori V, Rouphael Y, Mendoza-De Gyves E, Bigniami C (2007) A simple model for estimating leaf area of hazelnut from linear measurements. Sci Hortic 113:221–225
Cristofori V, Fallovo C, Mendoza-De Gyves E, Rivera CM, Bignami C, Rouphael Y (2008) Non-destructive, analogue model for leaf area estimation in persimmon (Diospyros kaki L. f.) based on leaf length and width measurement. Eur J Hort Sci 73:216–221
Demirsoy H, Demirsoy L, Ozturk A (2005) Improved model for the non-destructive estimation of strawberry leaf area. Fruits 60:69–73
Elsner EA, Jubb GL Jr (1988) Leaf area estimation of concord grape leaves from simple linear measurements. Am J Enol Vitic 39:95–97
Fallovo C, Cristofori V, Mendoza-De Gyves E, Rivera CM, Rea R, Fanasca S, Bignami C, Sassine Y, Rouphael Y (2008) Leaf area estimation model for small fruits from linear measurements. HortScience 43:2263–2267
Fascella G, Maggiore P, Zizzo GV, Colla G, Rouphael Y (2009) A simple and low-cost method for leaf area measurement in Euphorbia x lomi Thai hybrids. Adv Hort Sci 23:57–60
Fascella G, Darwich S, Rouphael Y (2013) Validation of leaf area prediction model proposed for rose. Chilean J Agric Res 73:73–76
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec 35:1039–1042
Francis JK (1990) Hymenaea courbaril L. Algarrobo, locust. Institute of Tropical Forestry, (SO-ITF-SM-27), USDA Forest Service, Puerto Rico, pp 279-283
Giuffrida F, Rouphael Y, Toscano S, Scuderi D, Romano D, Rivera CM, Colla G, Leonardi C (2011) A simple model for nondestructive leaf area estimation in bedding plants. Photosynthetica 49:380–388
Gorchov DL, Palmeirim JM, Ascorra CF (2004) Dispersal of seeds of Hymenaea courbaril (Fabaceae) in a logged rain forest in the Peruvian Amazonian. Acta Amaz 34:251–259
Gower ST, Kucharik CJ, Norman JM (1999) Direct and indirect estimation of leaf area index, f APAR, and net primary production of terrestrial ecosystems. Remote Sens Environ 70:29–51
Hinnah FD, Heldwein AB, Maldaner IC, Loose LH, Lucas DDP, Bortoluzzi MP (2014) Leaf area of eggplant according to leaf dimensions. Bragantia 73:213–218
Homolová L, Lukeš P, Malenovský Z, Lhotáková Z, Kaplan V, Hanus J (2013) Measurement methods and variability assessment of the Norway spruce total leaf area: implications for remote sensing. Trees 27:111–112
Igathinathane C, Prakash VSS, Padma U, Babu GR, Womac AR (2006) Interactive computer software development for leaf area measurement. Comp Electr Agric 51:1–16
Kandiannan K, Parthasarathy U, Krishnamurthy KS, Thankamani CK, Srinivasan V (2009) Modeling individual leaf area of ginger (Zingiber officinale Roscoe) using leaf length and width. Sci Hortic 120:532–537
Khan MNI, Suwa R, Hagihara A (2005) Allometric relationships for estimating the aboveground phytomass and leaf area of mangrove Kandelia candel (L.) Druce trees in the Manko Wetland, Okinawa Island, Japan. Trees 19:266–272
Kumar R (2009) Calibration and validation of regression model for non-destructive leaf area estimation of saffron (Crocus sativus L.). Sci Hortic 122:142–145
Laubhann D, Eckmüllner O, Sterba H (2010) Applicability of non-destructive substitutes for leaf area in different stands of Norway spruce (Picea abies L. Karst.) focusing on traditional forest crown measures. For Ecol Manage 260:1498–1506
Liu Z, Jin G, Chen JM, Qi Y (2015) Evaluating optical measurements of leaf area index against litter collection in a broadleaved-Korean pine forest in China. Trees 29:59–73
Lorenzi H (1998) Árvores brasileiras– Manual de identificação e cultivo de plantas arbóreas do Brasil, 2ª edn. Editora Plantarum, Nova Odessa
Lu HY, Lu CT, Wei ML, Chan LF (2004) Comparison of different methods for nondestructive leaf area estimation in taro. Agron J 96:448–453
Mason EG, Diepstraten M, Pinjuv GL, Lasserre JP (2012) Comparison of direct and indirect leaf area index measurements of Pinus radiata D. Don. Agric For Meteorol 166–167:113–119
Mendoza-De Gyves E, Rouphael Y, Cristofori V, Rosana Mira F (2007) A non-destructive, simple and accurate model for estimating the individual leaf area of kiwi (Actinidia deliciosa). Fruits 62:171–176
Miranda C, Royo JB (2003) A statistical model to estimate potential yields in peach before bloom. J Am Soc Hort Sci 128:297–301
Miranda C, Royo JB (2004) Statistical model estimates potential yields in ‘Golden Delicious’ and ‘Royal Gala’ apples before bloom. J Am Soc Hort Sci 129:20–25
NeSmith DS (1992) Estimating summer squash leaf area nondestructively. HortScience 27:77
Neter J, Kutner MH, Nachtshein CJ, Wasserman W (1996) Applied linear regression models, 3rd edn. Irwin, Homewood
Pandey SK, Singh H (2011) Simple, cost-effective method for leaf area estimation. J Bot 2011:6. doi:10.1155/2011/658240
Peksen E (2007) Non-destructive leaf area estimation model for faba bean (Vicia faba L.). Sci Hortic 113:322–328
Pompelli MF, Antunes WC, Ferreira DTRG, Cavalcante PPGS, Wanderley-Filho HCL, Endres L (2012) Allometric models for non-destructive leaf area estimation of the Jatropha curcas L. Biomass Bioenerg 36:77–85
Rivera CM, Rouphael Y, Cardarelli M, Colla G (2007) A simple and accurate equation for estimating individual leaf area of eggplant from linear measurements. Eur J Hort Sci 72:228–230
Robbins SN, Pharr DM (1987) Leaf area prediction models for cucumber from linear measurements. HortScience 22:1264–1266
Rouphael Y, Rivera CM, Cardarelli M, Fanasca S, Colla G (2006) Leaf area estimation from linear measurements in zucchini plants of different ages. J Hort Sci Biotechnol 81:238–241
Rouphael Y, Colla G, Fanasca S, Karam F (2007) Leaf area estimation of sunflower leaves from simple linear measurements. Photosynthetica 45:306–308
Rouphael Y, Mouneimne AH, Ismail A, Mendoza-de-Gyves E, Rivera CM, Colla G (2010a) Modeling individual leaf area of rose (Rosa hybrida L.) based on leaf length and width measurement. Photosynthetica 48:9–15
Rouphael Y, Mouneimne AH, Rivera CM, Cardarelli M, Marucci A, Colla G (2010b) Allometric models for non-destructive leaf area estimation in grafted and engrafted watermelon (Citrullus lanatus Thunb). J Food Agric Environ 8:161–165
Schmildt ER, Amaral JAT, Santos JS, Schmildt O (2015) Allometric model for estimating leaf area in clonal varieties of coffee (Coffea canephora). Rev Ciênc Agron 46:740–748
Silva PSL, Cunha TMS, Souza AD, Paula VFS (2007) Equations for leaf area estimation in some species adapted to the Brazilian semi-arid. Rev Caatinga 20:18–23
Silva SHMG, Lima JD, Bendini HN, Nomura ES, Moraes WS (2008) Estimating leaf area in anthurium with regression functions. Ciênc Rur 38:243–246
Souza MC, Amaral CL, Habermann G, Alves PLCA, Costa FB (2015) Non-destructive model to estimate the leaf area of multiple Vochysiaceae species. Braz J Bot 38:1–7
Srámek M, Cermák J (2012) The vertical leaf distribution of Ulmus laevis Pall. Trees 26:1781–1792
Tamayo LMA, Gonzalez DMA, Garces YJ (2008) Pharmacological properties of the carob tree (Hymenaea courbaril Linneaus) interesting for the food industry. Rev Lassalista Invest 5:100–111
Toebe M, Cargnelutti Filho A, Loose LH, Heldwein AB, Zanon AJ (2012) Leaf area of snap bean (Phaseolus vulgaris L.) according to leaf dimensions. Semina 33:2491–2500
Tsialtas JT, Maslaris N (2005) Leaf area estimation in a sugar beet cultivar by linear models. Photosynthetica 43:477–479
Tsialtas JT, Koundouras S, Zioziou E (2008) Leaf area estimation by simple measurements and evaluation of leaf area prediction models in cabernet-Sauvignon grapevine leaves. Photosynthetica 46:452–456
Williams L, Martinson TE (2003) Nondestructive leaf area estimation of ‘Niagara’ and ‘DeChaunac’ grapevines. Sci Hortic 98:493–498
Acknowledgments
To the Foundation for Research Support of the Alagoas State (FAPEAL), to the Reference Center on Recovery of Degraded Areas (CRAD) of the Lower São Francisco, and to UFAL/Arapiraca, AL, for logistical, technical and financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
dos Santos, J.C.C., Costa, R.N., Silva, D.M.R. et al. Use of allometric models to estimate leaf area in Hymenaea courbaril L.. Theor. Exp. Plant Physiol. 28, 357–369 (2016). https://doi.org/10.1007/s40626-016-0072-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-016-0072-8