Anionic exchange membranes, a promising tool to

Ecological Indicators 94 (2018) 254–256

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Short Note

Anionic exchange membranes, a promising tool to measure distribution of soil nutrients in tropical multispecific plantations Edith Le Cadrea,1, Merveil Kinkondib, Lydie-Stella Koutikab, Daniel Epronc, Louis Mareschala,d,

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Eco&Sols, Univ Montpellier, CIRAD, INRA, IRD, Montpellier SupAgro, France Centre de Recherche sur la Durabilité et la Productivité des Plantations Industrielles, B.P. 1291, Pointe-Noire, People’s Republic of Congo c Université de Lorraine, INRA, UMR 1137, Ecologie et Ecophysiologie Forestières, Faculté des Sciences, F-54500 Vandoeuvre-les-Nancy, France d CIRAD, UMR Eco&Sols, F-34060 Montpellier, France b

A R T I C LE I N FO

A B S T R A C T

Keywords: Congo Tropical soil Forest plantation Mixed species Ecological intensification Method Anionic exchange membranes Phosphorus Nitrate

Establishing highly productive forest plantations or crops on poor soils requires appropriate management to ensure sustainable production. The current development of various ecological intensification practices calls for efficient tools to monitor their effects on agro-ecosystems. Ecological intensification such as an association between a N2-fixing tree species and a highly productive species, e.g. an acacia and a eucalypt, is an agroecological plantation design that can enhance nutrient cycling and preserve soil fertility in tropical and subtropical areas. In this study, Anionic Exchange Membranes (AEM) were used to assess in situ the effect of tree species on the availability and spatial variability of nitrate (N) and phosphorus (P) in pure Acacia mangium (A), pure eucalypt (E) and mixed-species treatments (MA-ME) in a randomized complete block design on a ferralitic arenosol. The results showed that the AEM detected the specific influence of tree species on N and P availability at the stand level as well as interactions between trees in the mixed-species treatment. Moreover, nutrients trapped using AEM were significantly correlated with N and P immobilized in the tree biomass. In the mixed stand, AEM made it possible to understand the specific impact of each tree species on N and P availability reflecting the respective biogeochemical mechanisms at work. This preliminary study showed that AEM are a promising tool that can be used in situ for intensive sampling in multi-local comparisons to highlight the effect of management practices on soil fertility as well as the relationships between vegetation cover and soil.

1. Introduction In subtropical and tropical areas, forest plantations represent 80 million ha dominated by genus Eucalyptus. They provide biomass for timber, paper pulp and fuelwood as substitute for fossil fuels (Achat et al., 2015; Booth, 2013) and can thereby contribute to shield native forest ecosystems from human pressure. However, several authors claim that eucalypt monocropping systems deplete soil fertility (Liao et al., 2012; Madejon et al., 2016), decrease biodiversity and require high inputs that impair sustainability on the long term (Gonçalves et al., 2008; Smethurst et al., 2004). In reaction, several management practices are proposed in the literature, such as the improvement of harvest residue management (Kumaraswamy et al., 2014) or associations with N2-fixing trees. Multi-species associations are considered as an ecological and practical alternative to monocropping (Gaba et al., 2015; Malézieux et al., 2009), in particular associations between Acacia spp., which are N2-fixing species, and Eucalyptus spp. (Bachmann et al., 2014;

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Bouillet et al., 2013; Forrester and Smith, 2012; Santos et al., 2016). However, acacias require a significant phosphorus (P) supply (Isaac et al., 2011; Koutika et al., 2014) for N2 fixation, an element in which tropical soils are dramatically deficient (Vitousek et al., 2010). Moreover, only few studies have been performed linking the effect of spatial and temporal variability in resources availability (e.g. nutrients) with tree growth in mixture (Forrester, 2014). The ecological intensification practice of introducing a legume species in monospecific plantations, implying concomitant changes in N and P status, provides an adequate environment in which to test Anionic Exchange Membranes (AEM). The use of AEM in situ allows the simultaneous extraction of different anions such as nitrate and phosphate in the same soil conditions. In a context of ecological intensification, AEM are potentially a useful tool since they integrate nutrient diffusion at the soil-solution interface with limited disturbance of soil communities or rhizospheric soil (Durán et al., 2013) and also integrate competition for nutrients between roots and microorganisms, unlike soil extraction in the laboratory. Siddique

Corresponding author at: CIRAD, UMR Functional Ecology and Biogeochemistry of Soil Agro Ecosystems, Bâtiment 12, 2, place Pierre Viala, 34 060 Montpellier, France. E-mail addresses: [email protected] (E.L. Cadre), [email protected] (D. Epron), [email protected] (L. Mareschal). Permanent address: AGROCAMPUS OUEST, UMR Soil, Agro- and Hydro-systems, Spatialization (SAS), 65 route de Saint Brieuc, CS 84215, 35 042 Rennes, France.

https://doi.org/10.1016/j.ecolind.2018.06.041 Received 31 March 2017; Received in revised form 14 June 2018; Accepted 20 June 2018 1470-160X/ © 2018 Elsevier Ltd. All rights reserved.


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et al (2008) used an exchange resin to show at the stand level that legume-dominated treatments were richer in nitrate and poorer in phosphorus than legume-poor mixed plantations. The objectives of this study are i) to ascertain whether AEM can be used to determine at a finer scale the spatial distribution of nitrate and phosphorus reflecting the biogeochemical processes at work in acacias and eucalypts respectively, and ii) to correlate the availability of these nutrients assessed using AEM with their immobilization in the biomass of each tree species. 2. Materials and methods The experimental site is located in the Congo (Africa), on a plateau (4°S, 12°E, 100Alt.) close to Tchissoko village, on a deep ferralic arenosol overlying a bedrock of thick detrital strata (Mareschal et al., 2011). Climate is sub-equatorial, with a cooler dry season from June to September. The original vegetation was a native tropical grassland. This was afforested in 1984 with eucalypt hybrids that were harvested in 2003. In 2004, a complete randomized block design was established comprising 5 blocks. Each block comprised 3 plots, each consisting in an inner core of 36 trees (6 x 6) surrounded by 2 buffer rows. Plots were either pure Acacia mangium plots (A), pure eucalypt plots (E) or a 1:1 mixed plot of these two species (Epron et al., 2013). In the mixed treatment (mixed acacia MA, and mixed eucalypt ME), the two species were planted alternately along each row (checkerboard pattern). The spacing between rows was 3.75 m, with 3.33 m between successive trees in a row. These are densities commonly used in commercial plantations, optimal for stem wood production in pure eucalypt stands at this site. The trial was harvested in January 2012. A new trial was planted in March 2012 using the same experimental design, with the same species as before, planted just beside the stumps (Tchichelle et al., 2017). Our study was carried out in 3 of the 5 blocks in April-May 2014. Anion-exchange membranes (AEM, 551642S VWR, 2 × 12.5 cm) were deployed in situ in the study plots. The AEM were transported in plastic bags before installation to prevent drying. Membranes were incubated in the surface soil layer (0–5 cm). Nine AEM were used per plot in A and E, and eighteen per plot in the mixed stand (nine in the vicinity of acacias and nine in the vicinity of eucalypts) in each of the three blocks. The membranes were set up 0.25, 1.25 and 2.50 m away from the target tree along a transect starting from that tree and ending at the centre of the area delimited by four trees (diagonal of the rectangle between four trees = 5 m). Chloride was chosen as counter ion to avoid any effect of pH change on nutrient availability (16 h, HCL 0.5 M on shaker). Membranes were retrieved after about 1 month, corresponding to 100 mm of rainfall, and stored in individual bags, then quickly rinsed under low-pressure running water and stored at 4 °C before analysis. N and P anions were extracted with HCl (16 h, HCL 0.5 M on shaker) as in the saturation process. Nitrate concentration was measured by colorimetry (SAN++, Skalar, Breda, The Netherlands) and P concentration using the green malachite method (Ohno and Zibilske, 1991). The total surface of each membrane was measured with a planimeter (CID BioScience, CI-202, USA) and used to normalize the N and P soil solution concentrations per resin area, to take into account possible damage after incubation in the soil. Total N and P content of the trees (wood, bark and leaves) were estimated following Tchichelle et al (2017). Differences between treatments regarding N and P concentrations in resin extracts and N and P stocks in trees were assessed using analyses of variance with a threshold level of P < 0.05. Homogeneity of variance was tested with Levene’s test. Treatment means were compared using Student–Newman–Keuls’ multiple range tests, and the Pearson correlation coefficient was calculated in the regression analyses (UNISTAT® 6.5, UNISTAT, London, UK).

Fig. 1. Concentration of nitrate (A) and orthophosphate ions (B) according to the tree species (A: Acacia; E: Eucalypt; MA: mixed acacia; ME: mixed eucalypt). Vertical error bars represent the standard deviation. Letters above the bars represent the post hoc mean groups at 5% level. Immobilization of nitrogen and phosphorus in trees per treatment is indicated above each bar in kg.ha−1, with associated post hoc mean groups at 5% level.

Fig. 2. Concentration of nitrate (A) and orthophosphate ions (B) trapped using AEM according to the distance to the trees in the mixed acacia and eucalypt treatment. The verticals error bars represent standard deviations (mean of the three blocks) and the lower-case letters represent the post hoc mean groups at 5% level.

3. Results and discussion AEM exchangeable orthophosphates and nitrates were significantly 255


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influenced by the tree species (Fig. 1) and the distance to the tree (Fig. 2). Without any consideration of distance to the tree (Fig. 1A), N concentration in soil solutions was greater in pure acacia stands than in pure eucalypt stands, with intermediate concentrations measured near acacias and near eucalypts in mixed stands. An inverse trend was measured for P, with lower concentrations in presence of acacias, particularly in pure acacia stands (Fig. 1B). Moreover, a significant positive relationship existed between N content of trees and N availability in the soil assessed using AEM, while this relationship was negative for P (correlation coefficient of 0.79 and −0.72 for N and P respectively, p value < 0.05). AEM were able to differentiate the relative influence of acacia and eucalypt on nutrient availability in the mixed plot since AM and EM exhibited intermediate values. When considering distance to the tree, a significant influence was observed in the mixed treatment, suggesting a local influence of the tree species on nutrient availability (Fig. 2). In this treatment, AEM revealed that beside greater immobilization of nitrogen in acacia biomass than in eucalypt (189 vs 47 kg.ha−1), the amount of nitrogen trapped on AEM was significantly higher in the vicinity of acacia trees (Fig. 2A). The opposite was observed with phosphorus, with lower amounts in the vicinity of acacias compared with eucalypts (Fig. 2B). The spatial distribution of nitrate and orthophosphate between eucalypt and acacia trees differed strongly: the decrease in orthophosphate concentration from eucalypts to acacias was linear (Fig. 2B), while the distribution was curvilinear for nitrate (Fig. 2A). The first pattern indicates orthophosphate mining, to a different degree depending on the tree species, while the curvilinear distribution of nitrate, along with greater concentrations in the vicinity of acacias, suggests an uptake but also a replenishment in nitrogen by the legume species. While no significant difference was detected between MA and ME at the stand level for both available nitrate and available orthophosphate (Fig. 1), AEM proved to be an efficient tool to describe the pattern of nutrient distribution at the infra-stand scale (Fig. 2). Furthermore, whereas ionic exchange resin beads were considered to be the most reliable way of measuring nutrient availability in crops (Cheesman et al., 2010; Ziadi et al., 2006; Qian and Schoenau, 2002), resin in membrane form has the major advantage of limiting soil disturbance (Durán et al., 2013). We conclude that resin in the membrane form can be used not only at the stand level to measure nutrient availability for crops, but also at an infra-stand level in order to describe the spatial variability of nutrients. Exchange membranes can be used for the simultaneous sampling of different elements to shed light on how plant species affect the spatial distribution of available nutrients, and beyond that, to give indications regarding species requirements and their specific biogeochemical mechanisms, especially in multi-species stands.

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Acknowledgements The authors thank Tiburce Matsoumbou and Sylvain Ngoyi (CRDPI, Congo) for their help in the field and laboratory. Financial support was provided by an internal grant from UMR Eco&Sol. The experimental site was set up by the Intens & Fix Project (ANR-2010-STRA-004-03) and belongs to the SOERE F-ORE-T, which is supported annually by Ecofor, Allenvi and the French national research infrastructure ANAEEF (http://www.anaee-france.fr/fr/). References Achat, D.L., Deleuze, C., Landmann, G., Pousse, N., Ranger, J., Augusto, L., 2015.

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