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This article was originally published in a journal published by Elsevier, and the attached copy is provided by Elsevier for the author’s benefit and for the benefit of the author’s institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues that you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier’s permissions site at: http://www.elsevier.com/locate/permissionusematerial

Environmental and Experimental Botany 60 (2007) 352–359

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Drought stress in rice (Oryza sativa L.) is enhanced in the presence of the compacting earthworm Millsonia anomala a

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Manuel Blouin a,b,∗ , Patrick Lavelle a , Daniel Laffray b

Laboratoire d’Ecologie des Sols Tropicaux, Institut de Recherche pour le D´eveloppement, 32 avenue Henri Varagnat, 93143 Bondy Cedex, France b Laboratoire d’Ecophysiologie Mol´ eculaire, Universit´e Paris 12 Val de Marne, 61 avenue de G´en´eral De Gaulle, 94010 Cr´eteil Cedex, France Received 15 February 2006; received in revised form 16 October 2006; accepted 28 December 2006

Abstract

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Earthworms increase growth of most plant species through a number of poorly investigated mechanisms. We tested the hypothesis that earthworm modifications of soil structure and the resulting changes in water availability to plants explain this positive effect. Addition of endogeic earthworms Millsonia anomala induced a 40% increase in shoot biomass production and a 13% increase in CO2 assimilation rate of well watered rice plants grown in pots. Conversely, when plants were subjected to water deficit, presence of earthworms had no effect on shoot biomass production and a negative impact on CO2 assimilation rate (−21%). Early stomatal closure in presence of earthworms indicated lower water availability. The hypothesis that earthworms improve plant biomass production through soil physical structure modification was thus rejected. Three hypotheses were tested to explain this decrease in water availability: (i) a decrease in soil water retention capacity, (ii) an increase in evaporation from the soil or/and (iii) an increase in plant transpiration. Results showed that earthworms significantly reduced soil water retention capacity by more than 6%, but had no effect on evaporation rate. Water losses through transpiration were greater in the presence of earthworms when the soil was maintained at field capacity, but this was not the case under drought conditions. This experiment showed that the endogeic compacting earthworm M. anomala significantly increased plant photosynthesis by an undetermined mechanism under well-watered conditions. However, photosynthesis was reduced under drought conditions due to reduced soil water retention capacity. © 2007 Elsevier B.V. All rights reserved. Keywords: Endogeic compacting species; Evaporation; Retention capacity; Soil structure modification; Transpiration; Water supply

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1. Introduction

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In most terrestrial ecosystems, excepted very cold or very dry ones, earthworms represent the majority of animal biomass—higher than herbivore (Lavelle and Spain, 2001). Because annelids appeared approximately 600–500 million years ago, terrestrial plants have always been exposed to these soil animals and have coevolved with them. Two recent reviews about the effect of earthworms on plant growth (Brown et al., 1999; Scheu, 2003) showed that plant shoot biomass is higher in the presence of earthworms (70–80% of the reviewed experiments). Five mechanisms are potentially responsible for the positive effect observed on plant production (Scheu, 2003;

∗ Corresponding author at: Laboratoire d’Ecologie des Sols Tropicaux, Institut de Recherche pour le D´eveloppement, 32 avenue Henri Varagnat, 93143 Bondy Cedex, France. Tel.: +33 148025962; fax: +33 148025970. E-mail address: [email protected] (M. Blouin).

0098-8472/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.envexpbot.2006.12.017

Brown et al., 2004): (i) increased mineralization of soil organic matter, which increases nutrient availability (Barois et al., 1987; Knight et al., 1989; James, 1991; Curry and Byrne, 1992; Lavelle et al., 1992; Subler et al., 1997); (ii) production of plant growth regulators via the stimulation of microbial activity (Frankenberger and Arshad, 1995; Muscolo et al., 1998; Nardi et al., 2002; Quaggiotti et al., 2004); (iii) biocontrol of pests and parasites (Stephens et al., 1994a,b; Clapperton et al., 2001; Blouin et al., 2005); (iv) stimulation of symbionts (Gange, 1993; Pedersen and Hendriksen, 1993; Furlong et al., 2002); (v) modification of soil porosity and aggregation (Blanchart et al., 1997, 1999; Decaens et al., 2001; Shipitalo and Le Bayon, 2004), which induces changes in water and oxygen availability to plants (Doube et al., 1997; Allaire-Leung et al., 2000). Modification of soil physical structure by earthworm burrows and casts is well documented (Blanchart et al., 2004; Shipitalo and Le Bayon, 2004). Their impact on soil hydraulic properties varies, depending on earthworm ecological strategies. (i) Epigeic species live in the litter and affect surface

M. Blouin et al. / Environmental and Experimental Botany 60 (2007) 352–359

2.1. Soil

2.2. Earthworms

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A sandy ultisol from a humid savannah in central Cˆote d’Ivoire (Lamto Research Station) was air-dried for 1 month and sieved through a 2 mm mesh. Chemical characteristics were as follows: total C, 0.91%; total N, 0.05%; pH 6.7; C/N, 18; clay, 6%; silt, 17%; sand, 78%; organic matter, 1–2% (Abbadie and Lensi, 1990; Martin, 1990; Lensi et al., 1992; Gilot, 1997; Lata et al., 1999). Pots, or microcosms, (10 cm in diameter and 16 cm in height) were filled with 1 kg of dry soil. Soil field capacity (190 g of water per kg of dry soil) was determined on five extra microcosms by weighting the pots after soil saturation with water for 3 days and drainage for 24 h.

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Earthworms M. anomala, Megascolecidae (Omodeo and Vaillaud, 1967) were collected from the same site. This mesohumic endogeic worm greatly affects soil structure since over 90% of the casts are deposited in the upper 20 cm of the soil profile (Lavelle, 1978). Casts are globular, comprised of coalescent round or flattened subunits with a higher density than the surrounding soil. M. anomala is thus considered a compacting species (Blanchart et al., 1999). One M. anomala (1 ± 0.20 g biomass, corresponding to a density of 127 g m−2 ) was added to each pot according to treatments. This abundance is higher than average abundances (about 20 g m−2 ) observed in the field (Lavelle, 1978). Since sub-adult worms ingest on average 10 times their weight daily (Lavelle, 1978), they were expected to re-aggregate 600 g out of the 1000 g of initially sieved soil during the first 60 days of plant culture.

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crusting or occlude macropores. (ii) Anecic species live in vertical burrows connected with soil surface. These burrows are used as shelters from where earthworms come to the surface to feed (Bouch´e, 1977; Lee, 1985; Bastardie et al., 2004). Anecic worms significantly influence soil erosion and water infiltration since sediment and nutrient losses in runoff waters have been reported to be halved when surface casts are present (Le Bayon and Binet, 2001); moreover, their vertical semipermanent burrows act as preferential water pathways and increase drainage by 4.5–45.2%, depending on rainfall intensity (Shuster et al., 2003). (iii) Endogeic species make horizontal or randomly oriented burrows, considered to be temporary structures because they are rarely reused. This last group has been divided between compacting species that tend to increase soil bulk density and decrease overall porosity (Blanchart et al., 2004), and decompacting species that have the opposite effect. Decompacting earthworms can disrupt large compact aggregates, decrease bulk density and increase soil porosity (Blanchart et al., 1999). Changes in porosity induced by compacting and decompacting species are likely to affect the volume of soil pores filled with water after drainage, and the availability of water for plants. However, the effect of compaction or decompaction on soil water storage capacity is difficult to predict. For example, compaction consists in the reduction in pore volume. When macropores are concerned, this leads to a reduction in the volume of draining water and thus could increase soil water retention capacity. When mesopores are concerned, this leads to an increase in the volume of water retained by microporosity (unavailable for plants) and thus decrease water availability. Since an increase in plant biomass production in the presence of earthworms occurs in parallel with the described modifications in soil structure, they were interpreted as responsible for the positive effect of earthworms on plant growth (Blanchart, 1990; Bastardie et al., 2005). This hypothesis was supported by an increase in plant water use efficiency (WUE) due to the presence of the endogeic earthworm Aporrectodea trapezo¨ıdes in soil maintained at field capacity (Doube et al., 1997). However, there is no clear demonstration that earthworms may increase plant biomass production through an increase in water availability. We thus tested this hypothesis in a situation where water availability is a major constraint for plant growth: a drying soil.

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2. Materials and methods

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A laboratory experiment was conducted on rice plants (Oryza sativa L. cv. Moroberekan). They were grown for 60 days (from d0 to d59) in the presence or absence of the endogeic compacting earthworm Millsonia anomala (Omodeo). Each treatment was then submitted to two different water regimes for 23 days (from d60 to d83): continuous watering or progressive soil dehydration. Plant response was studied by measuring plant biomass production, and analysing drought symptom development by foliar gas exchange and fluorescence measurements. Furthermore, we determine whether observed modifications in drought symptom development were due to changes in soil water retention capacity (Wmax ), water evaporation from the soil (Ev), and/or cumulative plant transpiration (Tr).

2.3. Plant culture Young rice seedlings (Oryza sativa L. cv. Moroberekan) were grown in a climatic chamber under well watered (W) or drought (D) conditions, in the absence (W and D) or presence (WE and DE) of earthworms. Each treatment was replicated six times. Air moisture was maintained at 75% ±5%, artificial light at 600 ␮mol photons m−2 s−1 during a 12 h photoperiod and temperature at 28 ◦ C during the day and 24 ◦ C at night. Pots were sown with one seed. As it is well known that there are light, humidity and/or temperature gradients in most of the growth chambers, replicates were dispatched randomly among the 4 × 6 lines of the experiment design. Consequently, these gradients could only be responsible for intra-treatment variations, not for inter-treatment variations. During the first 60 days after sowing (from d0 to d59), soil was maintained at 80% of field capacity (150 g of water per kg of dry soil, equivalent to 15% of humidity), a level known to be optimal for M. anomala (Lavelle, 1975), by addition of demineralised water. In this aim, plant weight was estimated by harvesting and weighting one extra plant in each week. At d60, soil was saturated by application of H2 O until large amounts leached from the bottom of microcosms. Soil was considered to be at field capacity 24 h after saturation (d61). No additional water was supplied to the plants in the D and DE treatments whereas those in the W and WE treatments were watered

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regularly to maintain field capacity. The experiment was carried out for 23 days under these conditions (from d61 to d83). At the end of the experiment, shoot biomass was collected, dried for 2 days at 50 ◦ C and weighted.

not removed to avoid disturbing soil structure; their dry weight (less than 2 g) was considered to be negligible.

2.4. Gas exchange and fluorescence

During the drought period (d60 to d83), drainage and evaporation occurred simultaneously with plant transpiration; cumulative water losses due to transpiration along the experiment (noted Tr) were therefore impossible to determine by weighing the pots. They were thus estimated from instantaneous transpiration rates measurements (noted T) and individual leaf area. Leaf area was determined using a non-destructive method based on length and mid-length width measurements multiplied by 0.75, the coefficient specific to grass leaf shape (De Parcevaux and Catsky, 1970; Pearcy et al., 1989). Whole plant transpiration (mmol H2 O plant−1 s−1 ) was obtained by multiplying the transpiration rate (mmol H2 O m−2 s−1 ) by the leaf area. These data were used to calculate a daily transpiration rate (mmol H2 O plant−1 d−1 ). For each pot, daily plant water losses were cumulated between d60 and d83 to estimate cumulative water loss by transpiration (Tr). The following assumptions were made: (i) single daily gas exchange measurements were representative of gas exchange over the whole light period; (ii) leaf area did not change during the experiment, particularly in drought treatments (Sharp and Davies, 1989; Kramer and Boyer, 1995); (iii) a single transpiration measurement in the youngest fully expanded leaf was representative of the entire leaf area. These assumptions probably biased the cumulative estimations (Tr). However, they allowed statistical comparison of the different treatments.

A simple equation describing soil water balance is: W = P − (O + U + Et)

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2.5. Theoretical background

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Gas exchange was measured each 4 days in the youngest fully expanded leaves after 2 h of light, using the Licor 6400 CO2 and H2 O analyser (Licor, Lincoln). During measurement, air temperature in the Licor chamber (6 cm2 area) was set at 28 ◦ C, air flow at 500 ml min−1 and CO2 at 400 ±5 ␮l l−1 . Air humidity was controlled by adjusting the dew point after saturation in hot water to maintain the vapour pressure deficit (VPD) at 0.6 kPa. The red/blue led light source (Licor, Lincoln) provided a 600 ␮mol m−2 s−1 photon flux. Leaf surface in the chamber (about 3 cm2 ) was determined and taken into account in the final calculation of CO2 assimilation, transpiration, stomatal conductance and CO2 concentration in stomata (Von Caemmerer and Farquhar, 1981). Maximal photochemical quantum yield of PSII (Fv/Fm) was measured each 4 days in the same leaves, with the mobile Teaching PAM fluorimeter (Walz, Effeltrich, Germany) before light switched on.

2.7. Estimation of cumulative water losses

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where W is soil water content, P the precipitation, O the runoff, U the drainage, and Et is evapotranspiration, i.e. the sum of water evaporation from soil to atmosphere (Ev) and plant transpiration (Tr) (Kramer and Boyer, 1995). In our experiment, runoff (O) was null:

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P = W + U + Ev + Tr Except for P which was set according to experimental conditions, earthworms could potentially modify all four variables; the equation could thus be written:

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P = Wc + Uc + Evc + Trc in control treatments,

P = We + Ue + Eve + Tre in earthworm treatments. Since water supply (P) was the same in both treatments,

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Wc + Uc + Evc + Trc = We + Ue + Eve + Tre . 2.6. Retention capacity and evaporation measurements At day 84, after cutting shoots at ground level at the end of the drought period, all pots were water saturated by immersion for 3 days. To estimate earthworm effects from a larger number of replicates, W and D pots were pooled in a “without earthworms” treatment and WE and DE pots in a “with earthworms” treatment. Retention capacity (Wmax ) was evaluated after a 24 h drainage period (d88) and evaporation (Ev) monitored by weighting the pots each 2 days, until soil was dry. Roots were

2.8. Statistical analyses Gas exchange measurements were analysed according to water regime, earthworm presence and their interaction. Dependant variables (A, T, Gs and Ci ) were measured several times on the same individuals, during drought; they were thus considered as “Repeated measures” (SAS, 1989), a procedure which takes into account the interdependence of measurements made successively on the same individual. For each parameter (CO2 assimilation (A), transpiration (T), stomatal conductance (Gs ) and CO2 internal concentration (Ci )), mean comparisons were computed for the different treatments (W, WE, D, DE). Effects of earthworms on these variables were also estimated over the whole experiment using a statistical procedure to identify significant differences (least square means (SAS, 1989)) without taking into account the variability due to other factors (date in the present experiment). Leaf area at d60 was analysed using a typical two-way ANOVA. Cumulative water losses (Tr) were analysed using a “repeated” two-way ANOVA according to the presence of earthworm, water regime and their interaction. To test the different mechanisms by which earthworms affect gas exchange, the water content of bare drying soil was analysed as “repeated measures” according to earthworm presence from d88 to d124, when soil water content was not limiting the evaporation rate. Significant differences in soil H2 O content at d88 would suggest an impact of earthworms on soil H2 O retention capacity

M. Blouin et al. / Environmental and Experimental Botany 60 (2007) 352–359

(Wmax ). On the other hand, a significant interaction between time and earthworms, corresponding to different slopes in the dehydration curves, would suggest an impact of earthworms on soil H2 O evaporation kinetics (Ev). Mean comparisons were carried out for each variable. All these analyses were performed using the SAS software (SAS, 1989).

ductance were not significantly different in the presence (DE) or in the absence of earthworms (D) until 10 days after the onset of drought (Fig. 2). After 13 days, gas exchange rates were lower in DE than in D: −43, −65 and −72% for assimilation (P = 0.021), transpiration (P = 0.003) and in stomatal conductance (P = 0.003), respectively. Internal CO2 concentration (Ci ) increased by 25% (P = 0.063). Over the whole period of drought, earthworms reduced A by 21% (P = 0.01), T by 23% (P = 0.006) and Gs by 23% (P = 0.01). Ci variations showed two distinct phases after the onset of drought (Fig. 2). It first decreased between the 10th and 13th days in the DE treatment, and between the 10th and 16th days in the D treatment; it then increased between the 13th and 16th in the DE treatment, and between the 16th and 22nd days in the D treatment. Both phases were shorter in the DE than in the D treatments, suggesting a magnification in the negative effect of water deficit on gas exchanges in the presence of earthworms. This was confirmed by the stronger reduction in maximal photochemical quantum yield (Fv/FM) in the DE than in the D treatment at day 23 (Fig. 2).

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3. Results 3.1. Impact of earthworms on biomass production

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3.3. Mechanisms involved in plant response Monitoring soil evaporation led to the observation that earthworms significantly affected water reserve in the soil at field capacity (repeated ANOVA, P = 0.05). As indicated by the two curves of decreasing soil humidity, earthworms were responsible for a significant reduction of maximal soil water content (Fig. 3). It was reduced by 13.4 ± 0.4 g (mean ± S.E.); this corresponded to a 6.4 ± 0.2% reduction in soil field capacity induced by earthworms. As a conclusion:

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Over the whole drought period (d60–d83), i.e. without taking into account the variability due to the time over the course of the study, net CO2 assimilation rate (A) was 13.4% higher (P = 0.05) in the presence (WE) than in the absence (W) of earthworms in watered treatments (Fig. 2). No significant differences were found in the transpiration rates (T) (P = 0.99), internal CO2 concentrations (Ci ) (P = 0.87) or stomatal conductance (Gs ) (P = 0.52). Under drought conditions, CO2 assimilation rate, transpiration rate, internal CO2 concentrations and stomatal con-

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An ANOVA showed that shoot biomass was significantly affected by water treatment and the presence of earthworms (Table 1). Furthermore, the significance of the interaction between water treatment and earthworm presence meant that earthworm effect depended on the amount of supplied water. Mean comparison showed that shoot biomass increased in the presence of earthworms in the watered treatments (+40% in WE as compared to W, Fig. 1). Conversely, shoot biomass did not increase in the presence of earthworms under drought conditions (D and DE). 3.2. Impact of earthworms on plant physiology

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P-value

18.24 40.73 5.12 8.88

Wmax-e ), and had no impact on evaporation rate (Evc = Eve ) (Fig. 3). This decrease in soil water retention capacity in the presence of earthworms contradicts previous study by Blanchart et al. (1997) showing a higher water retention capacity in the presence of M. anomala than in the control treatment. However, difference between treatments was small and no standard deviation was included. Our present results agree with those obtained using another endogeic compacting species (Pontoscolex corethrurus), in a field mesocosm experiment (Alegre et al., 1996; Pashanasi et al., 1996). In the presence of P. corethrurus, plant biomass production and grain yield increased during rainy seasons and decreased during dry seasons (Pashanasi et al., 1996). The proposed explanations were an increase in cumulative transpiration by larger plants in treatments with earthworms and/or a decrease in soil porosity (Alegre et al., 1996). The hypothesis of a higher evaporation rate from the soil was not considered. Our results suggested that reduced soil water storage capacity in earthworm presence was responsible for an earlier stomatal closure under drought conditions, which in turn resulted in a lower leaf biomass production. The positive effect M. anomala on rice growth cannot be due to improved water availability, as previously proposed. It would now be interesting to test the effect of others earthworm functional groups such as decompacting endogeic species on plant physiology under drought conditions. In well watered rice plants, the addition of M. anomala improved net CO2 assimilation rate and shoot biomass production, as observed in a previous experiment (Blouin et al., 2005). No increase in transpiration rate was observed in WE treatment (Fig. 2), which reinforced the idea that enhanced shoot biomass production was not due to improved water availability resulting from soil structure modifications. Improved oxygen availability in the presence of earthworms was ruled out because the sandy texture of the soil most likely ensured sufficient drainage and

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