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Nutrient accumulation in aboveground biomass ofplanted tropical trees: a meta-analysisMasahiro Inagakia & Takeshi Tangeba Kyushu Research Center, Forestry and Forest Products Research Institute, 4-11-16Kurokami, Chuo-ku, Kumamoto 8600862, Japanb Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi,Bunkyo-ku, Tokyo 1138657, JapanPublished online: 24 Jun 2014.

To cite this article: Masahiro Inagaki & Takeshi Tange (2014) Nutrient accumulation in aboveground biomass of plantedtropical trees: a meta-analysis, Soil Science and Plant Nutrition, 60:4, 598-608, DOI: 10.1080/00380768.2014.929025

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ORIGINAL ARTICLE

Nutrient accumulation in aboveground biomass of planted tropicaltrees: a meta-analysis

Masahiro INAGAKI1 and Takeshi TANGE2

1Kyushu Research Center, Forestry and Forest Products Research Institute, 4-11-16 Kurokami, Chuo-ku, Kumamoto 8600862,Japan and 2Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 1138657,Japan

Abstract

Efficient nutrient use is essential for biomass production by tropical trees growing in infertile soils.Accumulation of nitrogen (N) and phosphorus (P) in the aboveground biomass of four groups of tree stands[Acacia, Eucalyptus, N2-fixing trees excluding Acacia, and other non-N2-fixing broadleaved (ONNFB) trees]were investigated using meta-analyses of a range of biomass data to test the hypothesis that fast-growingAcacia and Eucalyptus trees accumulate fewer nutrients. Data for 83 tropical tree stands were selected fromthe literature. Standardized major axis regressions were applied between the log10-transformed biomass andN or P accumulation. Nutrient use efficiency was compared with aboveground biomass and topsoil condi-tions. The slope of the regression between aboveground biomass and N accumulation for Eucalyptus wassignificantly smaller than the slopes for the N2-fixing trees (excluding Acacia) and the ONNFB trees. N useefficiency of Eucalyptus increased with biomass more than that of N2-fixing trees (excluding Acacia) and theONNFB trees, because their stems and twigs tended to accumulate less N than in the other groups asbiomass increased. The regressions between aboveground biomass and P accumulation had a common slope,and the intercepts of Acacia and Eucalyptus were significantly lower than that of ONNFB trees. P useefficiency of Acacia was consistently higher than that of the ONNFB trees. P use efficiency is more affectedby other factors like soil conditions than is N use efficiency, and the differences in the tree groupssignificantly affect the use efficiency of both nutrients. These results explained some aspects of the generalsuitability of Acacia and Eucalyptus species for tropical plantations on infertile soils.

Key words: biomass production, nitrogen, nutrient use efficiency, phosphorus, tropical forest plantation.

INTRODUCTION

Tropical forest plantations are increasingly importantbecause of their ability to enhance biomass/carbonresources in an area (FAO 2006) and improve degradedsoil organic matter after disturbances (Lugo 1997; Garayet al. 2004; Macedo et al. 2008; Wang et al. 2010). Fast-growing trees, including several species of Eucalyptusand Acacia, are often chosen for such purposes, because

these trees can produce a profitable yield of more than15 m3 ha1 year1 of biomass for small log production(Cossalter and Pye-Smith 2003). Weathered soils pro-duced by long-term pedogenesis, which are usually infer-tile, have developed across wide areas of the humidtropics. In addition, harvesting operations and removalof tree biomass can cause serious nutrient deficits inforest soils (Nykvist 2000; Laclau et al. 2010; Dovey2012). Wood biomass production is primarily regulatedby nutrients, rather than water, in wet tropical areas(Jordan 1985). Species with the lowest nutrient demandsmay therefore be the best biomass producers in suchsoils.Fast-growing tree species are generally considered to

accumulate soil nutrients faster than slow-growing oneswhen multiple rotations are implemented (Cossalter and

Correspondence: M. INAGAKI, Kyushu Research Center,Forestry and Forest Products Research Institute, 4-11-16Kurokami, Chuo-ku, Kumamoto 8600862, Japan. Tel: +8196 343 3739; Fax: +81 96 344 5054.Email: inagaki@affrc.go.jpReceived 10 January 2014.Accepted for publication 26 May 2014.

Soil Science and Plant Nutrition (2014), 60, 598608 http://dx.doi.org/10.1080/00380768.2014.929025

2014 Japanese Society of Soil Science and Plant Nutrition

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Pye-Smith 2003). However, whether nutrient accumula-tion per unit biomass differs between fast- and slow-grow-ing trees is not known. Previous studies compared nutrientuse efficiencies among several fast-growing trees (Kumaret al. 1998; Hiremath et al. 2002), some Acacia species(Kimaro et al. 2007) and some Eucalyptus species (Laclauet al. 2000), but differences in nutrient use efficiencyamong Acacia, Eucalyptus and other slower-growingtrees are undocumented. Some fast-growing tree specieshave strategies that allow them to grow on degradedsoils. In a nursery experiment, Acacia mangium Willd.had enhanced phosphorus (P) use efficiency under P-lim-ited conditions (Ribet and Drevon 1996). Some Acaciaspecies selectively translocate a large proportion of P (rela-tive to nitrogen, N) away from their leaves before senes-cence (He et al. 2011; Inagaki et al. 2011). SomeEucalyptus plantations experience higher primary produc-tivity with a low N investment (Binkley et al. 2004).Therefore, some Acacia and Eucalyptus trees may usenutrients more efficiently than other species.Both N and P are major nutrients for tree growth

(Chapin et al. 2011). However, they differ in theirsources (Chapin et al. 2011), site availability(McGroddy et al. 2004; Chapin et al. 2011), metabolicforms (Matzek and Vitousek 2009) and degrees of trans-location in plant organs (Laclau et al. 2001;Httenschwiler et al. 2008; Inagaki et al. 2011).Therefore, they may not accumulate in abovegroundbiomass in the same way. Recent meta-analyses haveclarified the relationship between leaf nutrient concentra-tions and some environmental and genetic factors (e.g.McGroddy et al. 2004; Townsend et al. 2007; Fyllaset al. 2009). A study of leaf analyses across theAmazon Basin revealed that leaf N is influenced mainlyby genetic factors (family/genus/species), while leaf P ismore strongly affected by the environment (Fyllas et al.2009). Thus, the differing degree of structural depen-dency on these nutrients should be taken into accountwhen assessing genetic differences in these levels in treesgrowing under different environmental conditions. Inaddition, the factors regulating N and P levels in plantorgans other than leaves are poorly known (Kerkhoffet al. 2006). Understanding the accumulation of nutri-ents and total aboveground biomass in plants, includingwoody parts, will require additional research.Trees increase the ratio of structural organs (woody

parts) to metabolic organs (leaves) during their growth(Mori et al. 2010; Dovey 2012). When nutrient accumu-lation in aboveground biomass is considered, shift ininvestment between metabolic and structural organsmust be considered. To evaluate this shift, forest standsranging from juvenile to mature are needed for analysis.In contrast to leaf analyses, measuring the abovegroundbiomass and accumulated nutrients of entire trees is

difficult because it requires destructive measurements.Until recently, very limited information on the above-ground biomass of tropical trees has been available.The results of a few international research projects,such as Site management and productivity in tropicalplantation forests conducted by the Center forInternational Forestry Research (CIFOR), haveimproved the body of knowledge and, recently, a largeamount of biomass and nutrient content data hasbecome available (Nambiar et al. 2004; Nambiar2008). Most of these studies have included soil para-meters that help to elucidate the nitrogen use efficiency(NUE) and phosphorus use efficiency (PUE) characteris-tics of species growing on various levels of soil fertility.We investigated the accumulation and allocation of N

and P in the aboveground biomass of four tree groups[Acacia trees, Eucalyptus trees, N2-fixing trees excludingAcacia, and other non-N2-fixing broadleaved (ONNFB)trees], across a range of biomasses, using a meta-analy-sis. The aim of this study was to test the hypothesis thatfast-growing Acacia and Eucalyptus tree species usesmaller amounts of nutrients per unit of abovegroundbiomass for their growth than other tree species. Effectsof topsoil conditions on N and P accumulation in treebiomass are also discussed.

MATERIALS AND METHODS

Sources of data on aboveground biomass andnutrient accumulation in tropical timber treesAboveground biomass and nutrient data were derivedfrom reports on tropical plantation trees. The majorityof the data was taken from a CIFOR report (Yamadaet al. 2004), while other information was gleaned fromthe literature (see Appendix 1). Data for conifers wereomitted because only two datasets were available. Wecompiled data for 83 tropical tree stands: 20 stands ofAcacia species, 21 stands of N2-fixing species excludingAcacia (hereafter simply called N2-fixing species), 26stands of Eucalyptus species, and 16 stands of ONNFBspecies. Acacia and Eucalyptus are two large genera offast-growing trees and are planted throughout much ofthe tropics and in some temperate areas (Cossalter andPye-Smith 2003). Most of the N2-fixing trees sampledbelong to the Fabaceae, with the exception of Casuarinaequisetifolia L. (Casuarinaceae). The ONNFB treessampled grew in India and Central America, since theavailable data were limited to these areas.The mean annual increments (MAI) of biomass (dry

weight basis) of Acacia and Eucalyptus were 16.3 and15.7 Mg ha1 year1, respectively (Fig. 1). These MAIexceeded 15 m3 ha1 year1, given the wood densities of0.55 g cm3 for Acacia and 0.64 g cm3 for Eucalyptus

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(Ogata et al. 2008). However, the MAI of ONNFB treeswas significantly smaller than those of Acacia andEucalyptus, and the MAI of N2-fixing trees was two-thirds of those of Acacia and Eucalyptus. In this study,we considered Acacia and Eucalyptus to be fast-growingtrees, although a broader definition would encompasssome rapidly growing trees in the N2-fixing and ONNFBtree groups. Total aboveground biomass was partitionedinto (1) leaf biomass and (2) stem + twig biomass; weanalyzed nutrient accumulation in these structural units.Total N and available P concentrations in the surface

soil layer, mostly at depths of 010 cm, were used.Although the extraction methods for available P differedamong studies, we did not adjust the values because nomethod exists to account for a variety of soil conditions.The soil data from some A. mangium stands (Nykvistand Sim 2009) were provided as mass values (kg ha1) inthe original literature, so we estimated the concentra-tions using assumed bulk density (1.2). Some of thedata were supplied by N. Nykvist (pers. comm.).

Nitrogen and phosphorus use efficiencyIn this study, we defined NUE and PUE as units ofaboveground biomass per accumulated N and P, respec-tively (Kumar et al. 1998; Laulau et al. 2000; Kimaroet al. 2007). The original definition of nutrient use effi-ciency was net primary production per amount of nutri-ents taken up (Hirose 1975). We omitted belowground

and litterfall components as these are not removed dur-ing harvesting. We targeted a range of tree ages whenanalyzing aboveground biomasses. Biomasses for thefour tree groups were: (1) Acacia trees (6326Mg ha1), (2) N2-fixing trees (18.2121 Mg ha

1), (3)Eucalyptus trees (5.9324 Mg ha1) and (4) ONNFBtrees (2.5191 Mg ha1) (see Appendix 1).

Statistical analysesWe applied standardized major axis (SMA) regression(Sokal and Rohlf 2011) to examine relationships betweenthe log10-transformed biomass (Mg ha

1) and accumu-lated N or P (kg ha1). All biomass data were categorizedinto one of the four tree groups listed above. The differ-ences in slopes and intercepts of the SMA regressions weretested between these four tree groups using Sidaksadjusted pair-wise test, depending on the significance ofthe null hypothesis that the slopes were equal. Analysis ofcovariance (ANCOVA) was applied to NUE and PUEwith the factors of aboveground biomass and the treegroup. Differences in slopes were tested with Holmsadjusted pairwise test, and the differences in interceptswere tested using the Tukey-Kramer honestly significantdifference (HSD) test. Log10-transformed NUE and PUEwere compared by analysis of variance (ANOVA) amongspecies represented by more than four stands. A post-hocTukey-Kramer HSD test was performed if the ANOVAwas significant. All statistical analyses were performedusing R 2.15.3 (R Core Team 2013) with the SMATR3.3 package (Warton et al. 2012).

RESULTS

Relationship between aboveground biomass andN and P accumulationTo evaluate the biomass allocation and nutrient accumu-lation in an entire tree and in each structural unit atdifferent growth stages, we compared total abovegroundbiomass, leaf biomass and stem + twig biomass to N andP accumulation. All the regressions comparing biomassto N and P accumulation across the four tree groupswere significant except those between total abovegroundbiomass as well as stem + twig biomass and P accumula-tion for ONNFB trees (P = 0.33 and 0.62, respectively;Table 1). Although almost all of the regression slopeswere similar among tree groups, the slopes of the regres-sions between total aboveground biomass and N accu-mulation and between stem + twig biomass and Naccumulation were significantly different (P < 0.001).The slope for the regression of total aboveground bio-mass and N accumulation of Eucalyptus (0.615; 95%confidential interval, 0.5350.706) was significantly

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Figure 1 Mean annual increment (MAI) of aboveground bio-mass in four tree groups: Acacia, Eucalyptus, other non-nitro-gen (N2)-fixing broadleaved (ONNFB) trees, and N2-fixingtrees excluding Acacia. Bars indicate the standard error of themean. Letters indicate significant differences among tree groupsaccording to analysis of variance and post-hoc Tukey-Kramerhonestly significant difference (HSD) tests (P < 0.05). Numbersin parentheses after the names of the tree groups indicate thenumbers of tree stands.

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Tab

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