- Email: [email protected]
Slow recovery of earthworm populations after heavy traffic in two forest soils in northern France
Applied Soil Ecology 73 (2014) 130–133
Contents lists available at ScienceDirect
Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Short communication
Slow recovery of earthworm populations after heavy traffic in two forest soils in northern France N. Bottinelli a,b,∗ , Y. Capowiez c , J. Ranger a a b c
INRA, UR1138 INRA, Biogéochimie des Ecosystèmes Forestiers, F-54280 Champenoux, France State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, CAS, Nanjing 210008, China INRA, UR 1115 Plantes et Systèmes Horticoles, Domaine Saint Paul, 84914 Avignon Cedex 09, France
a r t i c l e
i n f o
Article history: Received 9 April 2013 Received in revised form 26 August 2013 Accepted 30 August 2013 Keywords: Soil compaction Earthworms Recolonisation
a b s t r a c t To determine the role of earthworms in regenerating compacted zones, it is essential to consider their capacity to colonise these zones. This study aimed to determine the short-term (3–4 years) response of earthworm populations to heavy traffic in two forest soils, at Azerailles (AZ) and Clermont-en-Argonne (CA) in north-eastern France. Earthworm populations were recorded immediately and for 3–4 years after heavy traffic by a 8-wheel drive forwarder with a load of about 23 Mg at AZ and 17 Mg at CA. To test the capacity of earthworms to recolonise traffic plot from the edges, an extra sampling was performed at the border of the traffic plots at AZ. Heavy traffic had a detrimental impact on the density and biomass of three earthworm functional groups. At AZ, earthworm populations, dominated by endogeic species, followed by anecic and epigeic species, had not fully recovered four years after compaction. The absence of statistically significant colonisation by the three functional groups from control to traffic plots indicated that the soil habitat was not yet favourable. At CA, earthworm populations, represented exclusively by epigeic species, had fully recovered three years after compaction, suggesting that the soil habitat was already suitable for them. This strong dependence on soil habitat quality is discussed and may be one reason for variation in the recovery rate of earthworms after compaction reported in the literature. In conclusion, this study did not support the hypothesis that earthworms play a role in regenerating soil structure the first few years following forest-soil compaction. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The growing mechanisation of forest operations is increasing soil compaction, resulting in degradation of soil structure and soil functioning (Greacen and Sands, 1980; Horn et al., 2004). In forest ecosystems, the remediation of compaction by tillage is rarely used, being difficult to apply due to the presence of stumps and large roots. Therefore, compacted forest soils must recover their structure through natural processes (i.e., wetting–drying cycles, freeze–thaw cycles during winter or biological activity) (Greacen and Sands, 1980). Among the main biological regulators of soil structure in temperate regions are earthworms, often called “soil engineers” due to the importance of their burrowing and casting activity to soil structure (Lee and Foster, 1991; Jouquet et al., 2006). It is generally claimed that earthworm activities contribute to the regeneration
∗ Corresponding author at: Agriculture, Institute of Soil Science, Chinese Academy of Sciences, 71 East Beijing Road, Nanjing 210008, China. Tel.: +86 25 8688 1198; fax: +86 25 8688 1000. E-mail address: [email protected] (N. Bottinelli). 0929-1393/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.apsoil.2013.08.017
of compacted zones, and it is well-documented under controlled conditions where earthworms are forced to move through compacted zones (Langmaack et al., 1999; Larink et al., 2001; Capowiez et al., 2009; Jouquet et al., 2012; Müller-Inkmann et al., 2013). Few, however, have validated this role in the field (Capowiez et al., 2012). Because soil compaction is a physical disturbance that leads to a decrease in earthworm populations (Söchtig and Larink, 1992; Jordan et al., 1999; Althoff et al., 2009; Capowiez et al., 2012), the regeneration of soil structure by earthworms initially should depend on their capacity to colonise these zones. The colonisation of new environments by earthworms has been extensively studied (reviewed in Eijsackers, 2011). Even if in this review, soil bulk density was indicated as a limiting factor for colonisation, very few studies have investigated the natural recovery of earthworm populations after heavy traffic. Moreover they have produced inconsistent results, with full recovery of earthworm abundance varying from a few months to several years (Jordan et al., 1999; Althoff et al., 2009; Capowiez et al., 2012). Two experimental sites were set up in two temperate forests in north-eastern France to monitor changes and recovery in physical, chemical and biological properties following traffic by a full-loaded forwarder (Goutal et al., 2012a,b; Goutal et al., 2013). In the initial
N. Bottinelli et al. / Applied Soil Ecology 73 (2014) 130–133
study, Goutal et al. (2012a) reported that soil specific volume to a depth of 10 cm had been completely restored on one site three years after traffic, whereas recovery was not achieved (1.01 vs. 0.95 cm3 g−1 in control and traffic plots, respectively) fourth year of monitoring at a second site. This study raised the question of which natural processes contributed to such a difference in recovery rate between the two sites. In this study, we hypothesised that the different recovery rates of specific soil volume at these sites could be explained by differing recovery rates of earthworm populations. The objective of this study was, therefore, to determine the short-term response of earthworm populations (abundance, biomass and diversity) to heavy traffic in two temperate-forest soils. Earthworm populations were recorded immediately and for 3–4 years after heavy traffic at two sites. 2. Materials and methods 2.1. Study sites The two study sites are located in two state-owned forests in north-eastern France: near Azerailles (AZ) (48◦ 29 19 N, 6◦ 41 43 E) and near Clermont-en-Argonne (CA) (49◦ 06 23 N, 5◦ 04 18 E). As described by Goutal et al. (2012a), the two sites had similar soil morphology, classified as Luvisol (ruptic) (FAO/WRB). Yet, differences occurred in soil organic carbon (SOC) content, pH and mull types, which are known to influence earthworm populations. Down to 30 cm, the soil at AZ had a SOC content of 11–27 g kg1 and a pH water of 4.6–4.8, while that at CA had a SOC content of 5–26 g kg−1 and a pH water of 4.4–4.5 (Goutal et al., 2012a). The humus forms varied from Mull mesomull at AZ to Mull dysmull and Moder at CA. The two forest stands dominated by beech (Fagus sylvatica L.) and oak (Quercus petraea L.) were clear-cut over a 5-ha area. Each site was divided into three blocks. In each block, the same fullyloaded 8-wheel drive forwarder (1996 Valmet 840) drove on land strips for an equivalent of two passes (one forward and one rearward pass) in May 2007 and March 2008 at AZ and CA, respectively. The tires of the forwarder were 60 cm wide, had a diameter of 133 cm (600/55 × 26.5) and were inflated to a pressure of 360 kPa for both sites. The empty forwarder weighed 11.4 Mg, the four front wheels supporting 6.9 Mg and the four rear wheels supporting 4.5 Mg. In AZ, the wood-loaded forwarder weighed 23.3 Mg, the four front and the four rear wheels supporting 7.56 Mg (i.e. the empty weight on the four front wheels + 5% of the load) and 15.76 Mg (i.e. the unloaded weight on the four rear wheels + 95% of the load), respectively. In CA, we only weighed the wood load and deduced the total weight of the loaded forwarder (16.7 Mg), the loaded weight on the four front wheels (7.17 Mg) and rear wheels (9.57 Mg) according to the measurements taken in AZ. The soil at CA was wetter (0.49 g g−1 at 5 cm depth) at the time of traffic than at AZ (0.34 g g−1 at 5 cm depth). Each plot measured 50 m × 50 m, with two undisturbed control 10 m × 50 m strips of land on each side of the 30 m × 50 m traffic area. In autumn 2007 (AZ) and 2008 (CA) the entire surface of each site was planted with sessile oak (Quercus petraea L.) at a density of 1600 seedlings ha−1 . 2.2. Earthworm sampling and identification Earthworms were sampled during three sampling dates in the centre of traffic (10–15 m from control plots) and control plots, corresponding to June 2007, November 2008 and April 2011 (i.e., one month, one year and four years after heavy traffic) for AZ and to April 2008, November 2009 and April 2011 (i.e., one month, one year and three years after heavy traffic) for CA. To test the capacity of earthworms to recolonise traffic-plot edges, extra sampling was
131
performed at the border of the traffic plots (e.g. less than 2 m from control plots) in April 2011 at AZ. In total, 117 sampling points were analysed (i.e., three dates × two sites × two locations: the centre of control and traffic plots x three blocks × three sampling points + one location: traffic-plot edges × three blocks x three sampling points). Earthworms were collected by hand sorting within 0.09 m2 (i.e., 0.3 m × 0.3 m) to a depth of 25 cm, and species were identified using Bouché’s (1972) key in the laboratory. Earthworm density and biomass were quantified (m−2 ) and species were classified into epigeic, anecic and endogeic functional groups. 2.3. Statistical analysis One-way ANOVA models were used to test the effect of treatment (e.g. the centre and border of the traffic plots and the centre of the control plots) on earthworm density and biomass for each sampling date and study site. Treatment was the main fixed effect, and blocks were the random effect. Analyses were performed with a balanced mixed-effects model (aov) using R software. When effects were found to be significant at p < 0.05, means were compared using the Tukey test. 3. Results and discussion 3.1. Earthworm abundance and diversity Earthworm density ranged from 69 to 177 and 0 to 91 individuals m−2 in control plots at AZ and CA, respectively (Fig. 1), while earthworm biomass ranged from 21 to 67 and 0 to 31 g m2 in control plots at AZ and CA, respectively (Fig. 2). The number of species found in control plots in 2011 was higher at AZ than at CA (5 vs. 2, respectively), as was the number of functional groups (3 vs. 1, respective). At AZ, the endogeic species Aporrectodea caliginosa (30%) and Aporrectodea rosea (34%) dominated, followed by the anecic species Lumbricus terrestris (26%). The anecic species Aporrectodea giardi and the epigeic species Lumbricus castaneus were uncommon, together representing only 10%. At CA, the community was dominated by the epigeic L. castaneus (71%) followed by the epigeic species Lumbricus rubellus (29%). The difference in earthworm populations may be attributed partly to the lower pH found at CA (4.4–4.5 in the upper 30 cm) than at AZ (4.6–4.8 in the upper 30 cm). The abundance, biomass and diversity of earthworms found in our study are consistent with previous studies regarding pH values and humus forms (e.g. Mull vs. Moder) (Deleporte et al., 1997; Muys and Granval, 1997; Potthoff et al., 2008). 3.2. Initial effect of heavy traffic on earthworms Our results showed that epigeic species found in both sites were missing at T0 (Fig. 1), indicating that deforestation, including vegetation destruction, litter removal, and changes in soil moisture and temperature regime, impacted them more than anecic and endogeic species. Because epigeic species use the litter layer both as habitat and as food source (Bouché, 1977), this result is expected. The passage of the heavy forwarder decreased the specific soil volume by 17 and 21% at CA and AZ, respectively (Goutal et al., 2012a). Moreover, it is thought that soil compaction can displace topsoil along with accompanying soil organic matter, decrease structural porosity and increase water stagnation (Greacen and Sands, 1980; Horn et al., 2004). All of these effects may have contributed to the significant decrease in the density (by 97%, p < 0.001) and biomass (by 94%, p < 0.001) of earthworms measured at AZ, which agrees with previous studies carried out in forest (Jordan et al., 1999), prairie (Althoff et al., 2009) and agricultural systems (Söchtig and Larink, 1992; Capowiez et al., 2012). When the effect is analysed by functional group, endogeic species seemed less sensitive than
N. Bottinelli et al. / Applied Soil Ecology 73 (2014) 130–133
Density of earthworms (number m-2)
132
200
AZ site
200 Epigeic
160
CA site
160
Anecic 120
Endogeic
120
80
80
40
40
0
0 Co
Tr
Co
T0 June
Tr
Co
T+1 November
Tr-b
Tr
Tr
Co
T+4
T0 April
April
Co
Tr
Co
T+1 November
Tr
T+3 April
Fig. 1. Mean density of the three earthworm functional groups by treatment and number of years after compaction: AZ, Azerailles; CA, Clermont-en-Argonne; Co, control plot; Tr, traffic plot; Tr-b, border of traffic plot; T0 , T+1 , T+2 , T+3 , T+4 , zero, first, second, third and fourth years after compaction, respectively. Error bars represent 1 standard deviation (n = 3).
anecic species since, on average, five endogeic m−2 were found in traffic plots after trafficking whereas no anecic species were found. Because endogeic species are soil feeders that live in the organomineral soil and construct non-permanent burrows (Bouché, 1977), they are assumed to be less affected by loss of topsoil organic matter and disturbance of their burrow systems (Cuendet, 1992). At CA, because earthworms were exclusively represented by epigeic species, the effect of compaction was masked by the deforestation at T0 . Nevertheless, the lower density (by 74%, p < 0.001) and biomass (by 85%, p < 0.001) of earthworms observed at T+1 in traffic compared to control plots also revealed the negative effect of compaction at this site. 3.3. Recovery of earthworms in traffic plots At AZ, the density of the five earthworm species and their biomass did not exhibit any clear recovery four years after heavy traffic (Figs. 1 and 2). Their abundance and biomass were lower in traffic than in control plots at T+1 (p < 0.01) and T+4 (p < 0.01). When the effect was analysed by functional group, epigeic species had significantly lower density in traffic than in control plots at T+1 (p < 0.05) and T+4 (p < 0.01). Anecic species were always lower in
Biomass of earthworms (g m-2)
80
AZ site
traffic than in control plots; however, results were statistically significant only at T+4 (p < 0.01). Endogeic species were lower in traffic than in control plots at T+1 (p < 0.001) and T+4 (p < 0.01). The recovery of earthworm populations after traffic should depend first on the soil habitat quality for colonisation and second on earthworm mobility. Hence, we propose two alternate hypotheses to explain the results: (i) earthworms had low mobility (Eijsackers, 2011), and measurement performed in the centre of the traffic plots (i.e., 10–15 m from the control) was thus unable to detect their recovery and (ii) soil habitat quality (porosity, moisture and temperature regime, soil organic matter and vegetation) remained unsuitable for them, preventing their migration from control to traffic plots. To test the first hypothesis, we added an extra sampling point in the border of traffic plots at T+4 . Results showed that the density and biomass of earthworms measured in the border were not significantly different from those measured in centre (Figs. 1 and 2), confirming the second hypothesis. This means that soil habitat quality was not yet favourable for earthworms. In contrast, the density and biomass of the two epigeic species at CA increased gradually from T+1 to T+3 , and control and traffic plots were no longer significantly different at T+3 . Here, the complete recovery of epigeic species indicates that the soil habitat was suitable for them
80
70
70
60
60
50
50
40
40
30
30
20
20
10
10
0
CA site
0 Tr
Co T0 June
Co
Tr
T+1 November
Co
Tr-b T+4 April
Tr
Tr
Co T0 April
Co
Tr
T+1 November
Co
Tr T+3 April
Fig. 2. Mean biomass of earthworms by treatment and number of years after compaction: AZ, Azerailles; CA, Clermont-en-Argonne; Co, control plot; Tr, traffic plot; Tr-b, border of traffic plot; T0 , T+1 , T+2 , T+3 , T+4 , zero, first, second, third and fourth year after compaction, respectively. Error bars represent 1 standard deviation (n = 3).
N. Bottinelli et al. / Applied Soil Ecology 73 (2014) 130–133
for feeding and reproduction. Our findings thus raise the question of which factors at the two sites contributed to such different recovery rates of epigeic species. Because epigeic species live mainly on the soil surface (Bouché, 1977), it is unlikely that soil porosity explains the recovery of epigeic species. This is confirmed by Goutal et al. (2012a), who reported that the soil specific volume determined at 0–10 cm depth in the traffic plots at T+4 and T+3 in AZ and CA, respectively, was similar. We thus assume that differences in organic horizon layers between AZ and CA explain the different recovery rates observed. Before heavy traffic, the humus form at AZ was a Mull mesomull, while it varied from a Mull dysmull to a Moder at CA. Thus, both sites had a litter layer, but only CA had a thin humus layer. After heavy traffic, the litter layer disappeared and had barely recovered by the end of the study. Furthermore, traffic at CA did not affect the humus layer, indicating that it provides a suitable environment for epigeic species living there. In this case, the time necessary for epigeic species to recover at CA was linked more to their mobility (e.g. from control plots or refuge zones like stumps in traffic plots to compacted zones) than the recovery of soil porosity. Studies of the natural recovery of earthworm populations after compaction are few and show different times to recovery, varying from a few months to several years (Jordan et al., 1999; Althoff et al., 2009; Capowiez et al., 2012). The slow recovery of earthworms in our study can be explained as follows: (i) at AZ, soil properties were not yet suitable for earthworms, and the soil litter had not yet recovered after heavy traffic; and (ii) at CA, even though topsoil habitat was suitable for earthworms (e.g. presence of humus), the large size of the traffic plots (30 m × 50 m) did not allow for rapid colonisation from control plots. In other studies, Jordan et al. (1999) observed a complete recovery of earthworm density (Diplocardia omata and Diplocardia smithii) one year after forest soil compaction, while Althoff et al. (2009) reported that earthworm density recovered completely two to four years after compaction in a tallgrass prairie. Nevertheless, the width of traffic plots in these studies did not exceed 1 m, which could partly explain the high recovery rates observed. 4. Conclusions In our study, earthworm populations barely recovered within a four years study period at one site and those found at another site belonged only to the epigeic functional group, which is thought to play a minor role in soil structure. Thus, our results did not support our main hypothesis that the short-term recovery of soil specific volume after heavy traffic is caused by earthworm activities. Acknowledgements We are grateful to Boris Fratré and Fabrice Elegbede for their help in earthworm sampling and Michael and Michelle Corson for
133
useful English corrections on the manuscript. This work was financially supported by the GIP Ecofor Soere F-ore-T network and Feder grants for the project ‘Effets du tassement des sols forestiers sur le fonctionnement biogéochimique de l’écosystème et sur sa durabilité pour plusieurs fonctions’. References Althoff, P.S., Todd, T.C., Thien, S.J., Callaham Jr., M.A., 2009. Response of soil microbial and invertebrate communities to tracked vehicle disturbance in tallgrass prairie. Appl. Soil Ecol. 43, 122–130. Bouché, M.B., 1972. Lombriciens de France. Ecologie et systématique, Paris. Bouché, M.B., 1977. Stratégies lombriciennes. In: Lohm, U., Persson, T. (Eds.), Soil Organisms and Components of Ecosystems. Ecology Bulletin/NFR, Stockholm. Capowiez, Y., Cadoux, S., Bouchand, P., Roger-Estrade, J., Richard, G., Boizard, H., 2009. Experimental evidence for the role of earthworms in compacted soil regeneration based on field observations and results from a semi-field experiment. Soil Biol. Biochem. 41, 711–717. Capowiez, Y., Samartino, S., Cadoux, S., Bouchant, P., Richard, G., Boizard, H., 2012. Role of earthworms in regenerating soil structure after compaction in reduced tillage systems. Soil Biol. Biochem. 55, 93–103. Cuendet, G., 1992. Effect of pedestrian activity on earthworm populations of two forests in Switzerland. Soil Biol. Biochem. 24, 1467–1470. Deleporte, S., Hallaire, V., Tillier, P., 1997. Application of image analysis to a quantitative micromorphological study of forest humus. Eur. J. Soil Biol. 33, 83–88. Eijsackers, H., 2011. Earthworms as colonisators of natural and cultivated soil environments. Appl. Soil Ecol. 50, 1–13. Goutal, N., Boivin, P., Ranger, J., 2012a. Assessment of the natural recovery rate of soil specific volume following forest soil compaction. Soil Sci. Soc. Am. J. 76, 1426–1435. Goutal, N., Parent, F., Bonnaud, P., Demaison, J., Nourrisson, G., Epron, D., Ranger, J., 2012b. Soil CO2 concentration and efflux as affected by heavy traffic in forest in northeast France. Eur. J. Soil Sci. 63, 261–271. Goutal, N., Renault, P., Ranger, J., 2013. Forwarder traffic impacted over at least four years soil air composition of two forest soils in northeast France. Geoderma 193–194, 29–40. Greacen, E.L., Sands, R., 1980. Compaction of forest soils: a review. Aust. J. Soil Res. 18, 163–189. Horn, R., Vossbrink, J., Becker, S., 2004. Modern forestry vehicles and their impacts on soil physical properties. Soil Till. Res. 79, 207–219. Jordan, D., Li, F., Ponder Jr., F., Berry, E.C., Hubbard, V.C., Kim, K.Y., 1999. The effects of forest practices on earthworm populations and soil microbial biomass in a hardwood forest in Missouri. Appl. Soil Ecol. 13, 31–38. Jouquet, P., Dauber, J., Lagerlof, J., Lavelle, P., Lepage, M., 2006. Soil invertebrates as ecosystem engineers: Intended and accidental effects on soil and feedback loops. Appl. Soil Ecol. 32, 153–164. Jouquet, P., Huchet, G., Bottinelli, N., Thu, T., Duc, T., 2012. Does the influence of earthworms on water infiltration, nitrogen leaching and soil respiration depend on the initial soil bulk density? A mesocosm experiment with the endogeic species Metaphire posthuma. Biol. Fertil. Soils 48, 561–567. Langmaack, M., Schrader, S., Rapp-Bernhardt, U., Kotzke, K., 1999. Quantitative analysis of earthworm burrow systems with respect to biological soil-structure regeneration after soil compaction. Biol. Fertil. Soils 28, 219–229. Larink, O., Werner, D., Langmaack, M., Schrader, S., 2001. Regeneration of compacted soil aggregates by earthworm activity. Biol. Fertil. Soils 33, 395–401. Lee, K.E., Foster, R.C., 1991. Soil fauna and soil structure. Aust. J. Soil Res. 29, 745–775. Müller-Inkmann, M., Fründ, H.-C., Hemker, O., 2013. An experimental setup to assess earthworm behaviour in compacted soil. Biol. Fertil. Soils 49, 363–366. Muys, B., Granval, P., 1997. Earthworms as bio-indicators of forest site quality. Soil Biol. Biochem. 29, 323–328. Potthoff, M., Asche, N., Stein, B., Muhs, A., Beese, F., 2008. Earthworm communities in temperate beech wood forest soils affected by liming. Eur. J. Soil Biol. 44, 247–254. Söchtig, W., Larink, O., 1992. Effect of soil compaction on activity and biomass of endogeic lumbricids in arable soils. Soil Biol. Biochem. 24, 1595–1599.
Contents lists available at ScienceDirect
Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Short communication
Slow recovery of earthworm populations after heavy traffic in two forest soils in northern France N. Bottinelli a,b,∗ , Y. Capowiez c , J. Ranger a a b c
INRA, UR1138 INRA, Biogéochimie des Ecosystèmes Forestiers, F-54280 Champenoux, France State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, CAS, Nanjing 210008, China INRA, UR 1115 Plantes et Systèmes Horticoles, Domaine Saint Paul, 84914 Avignon Cedex 09, France
a r t i c l e
i n f o
Article history: Received 9 April 2013 Received in revised form 26 August 2013 Accepted 30 August 2013 Keywords: Soil compaction Earthworms Recolonisation
a b s t r a c t To determine the role of earthworms in regenerating compacted zones, it is essential to consider their capacity to colonise these zones. This study aimed to determine the short-term (3–4 years) response of earthworm populations to heavy traffic in two forest soils, at Azerailles (AZ) and Clermont-en-Argonne (CA) in north-eastern France. Earthworm populations were recorded immediately and for 3–4 years after heavy traffic by a 8-wheel drive forwarder with a load of about 23 Mg at AZ and 17 Mg at CA. To test the capacity of earthworms to recolonise traffic plot from the edges, an extra sampling was performed at the border of the traffic plots at AZ. Heavy traffic had a detrimental impact on the density and biomass of three earthworm functional groups. At AZ, earthworm populations, dominated by endogeic species, followed by anecic and epigeic species, had not fully recovered four years after compaction. The absence of statistically significant colonisation by the three functional groups from control to traffic plots indicated that the soil habitat was not yet favourable. At CA, earthworm populations, represented exclusively by epigeic species, had fully recovered three years after compaction, suggesting that the soil habitat was already suitable for them. This strong dependence on soil habitat quality is discussed and may be one reason for variation in the recovery rate of earthworms after compaction reported in the literature. In conclusion, this study did not support the hypothesis that earthworms play a role in regenerating soil structure the first few years following forest-soil compaction. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The growing mechanisation of forest operations is increasing soil compaction, resulting in degradation of soil structure and soil functioning (Greacen and Sands, 1980; Horn et al., 2004). In forest ecosystems, the remediation of compaction by tillage is rarely used, being difficult to apply due to the presence of stumps and large roots. Therefore, compacted forest soils must recover their structure through natural processes (i.e., wetting–drying cycles, freeze–thaw cycles during winter or biological activity) (Greacen and Sands, 1980). Among the main biological regulators of soil structure in temperate regions are earthworms, often called “soil engineers” due to the importance of their burrowing and casting activity to soil structure (Lee and Foster, 1991; Jouquet et al., 2006). It is generally claimed that earthworm activities contribute to the regeneration
∗ Corresponding author at: Agriculture, Institute of Soil Science, Chinese Academy of Sciences, 71 East Beijing Road, Nanjing 210008, China. Tel.: +86 25 8688 1198; fax: +86 25 8688 1000. E-mail address: [email protected] (N. Bottinelli). 0929-1393/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.apsoil.2013.08.017
of compacted zones, and it is well-documented under controlled conditions where earthworms are forced to move through compacted zones (Langmaack et al., 1999; Larink et al., 2001; Capowiez et al., 2009; Jouquet et al., 2012; Müller-Inkmann et al., 2013). Few, however, have validated this role in the field (Capowiez et al., 2012). Because soil compaction is a physical disturbance that leads to a decrease in earthworm populations (Söchtig and Larink, 1992; Jordan et al., 1999; Althoff et al., 2009; Capowiez et al., 2012), the regeneration of soil structure by earthworms initially should depend on their capacity to colonise these zones. The colonisation of new environments by earthworms has been extensively studied (reviewed in Eijsackers, 2011). Even if in this review, soil bulk density was indicated as a limiting factor for colonisation, very few studies have investigated the natural recovery of earthworm populations after heavy traffic. Moreover they have produced inconsistent results, with full recovery of earthworm abundance varying from a few months to several years (Jordan et al., 1999; Althoff et al., 2009; Capowiez et al., 2012). Two experimental sites were set up in two temperate forests in north-eastern France to monitor changes and recovery in physical, chemical and biological properties following traffic by a full-loaded forwarder (Goutal et al., 2012a,b; Goutal et al., 2013). In the initial
N. Bottinelli et al. / Applied Soil Ecology 73 (2014) 130–133
study, Goutal et al. (2012a) reported that soil specific volume to a depth of 10 cm had been completely restored on one site three years after traffic, whereas recovery was not achieved (1.01 vs. 0.95 cm3 g−1 in control and traffic plots, respectively) fourth year of monitoring at a second site. This study raised the question of which natural processes contributed to such a difference in recovery rate between the two sites. In this study, we hypothesised that the different recovery rates of specific soil volume at these sites could be explained by differing recovery rates of earthworm populations. The objective of this study was, therefore, to determine the short-term response of earthworm populations (abundance, biomass and diversity) to heavy traffic in two temperate-forest soils. Earthworm populations were recorded immediately and for 3–4 years after heavy traffic at two sites. 2. Materials and methods 2.1. Study sites The two study sites are located in two state-owned forests in north-eastern France: near Azerailles (AZ) (48◦ 29 19 N, 6◦ 41 43 E) and near Clermont-en-Argonne (CA) (49◦ 06 23 N, 5◦ 04 18 E). As described by Goutal et al. (2012a), the two sites had similar soil morphology, classified as Luvisol (ruptic) (FAO/WRB). Yet, differences occurred in soil organic carbon (SOC) content, pH and mull types, which are known to influence earthworm populations. Down to 30 cm, the soil at AZ had a SOC content of 11–27 g kg1 and a pH water of 4.6–4.8, while that at CA had a SOC content of 5–26 g kg−1 and a pH water of 4.4–4.5 (Goutal et al., 2012a). The humus forms varied from Mull mesomull at AZ to Mull dysmull and Moder at CA. The two forest stands dominated by beech (Fagus sylvatica L.) and oak (Quercus petraea L.) were clear-cut over a 5-ha area. Each site was divided into three blocks. In each block, the same fullyloaded 8-wheel drive forwarder (1996 Valmet 840) drove on land strips for an equivalent of two passes (one forward and one rearward pass) in May 2007 and March 2008 at AZ and CA, respectively. The tires of the forwarder were 60 cm wide, had a diameter of 133 cm (600/55 × 26.5) and were inflated to a pressure of 360 kPa for both sites. The empty forwarder weighed 11.4 Mg, the four front wheels supporting 6.9 Mg and the four rear wheels supporting 4.5 Mg. In AZ, the wood-loaded forwarder weighed 23.3 Mg, the four front and the four rear wheels supporting 7.56 Mg (i.e. the empty weight on the four front wheels + 5% of the load) and 15.76 Mg (i.e. the unloaded weight on the four rear wheels + 95% of the load), respectively. In CA, we only weighed the wood load and deduced the total weight of the loaded forwarder (16.7 Mg), the loaded weight on the four front wheels (7.17 Mg) and rear wheels (9.57 Mg) according to the measurements taken in AZ. The soil at CA was wetter (0.49 g g−1 at 5 cm depth) at the time of traffic than at AZ (0.34 g g−1 at 5 cm depth). Each plot measured 50 m × 50 m, with two undisturbed control 10 m × 50 m strips of land on each side of the 30 m × 50 m traffic area. In autumn 2007 (AZ) and 2008 (CA) the entire surface of each site was planted with sessile oak (Quercus petraea L.) at a density of 1600 seedlings ha−1 . 2.2. Earthworm sampling and identification Earthworms were sampled during three sampling dates in the centre of traffic (10–15 m from control plots) and control plots, corresponding to June 2007, November 2008 and April 2011 (i.e., one month, one year and four years after heavy traffic) for AZ and to April 2008, November 2009 and April 2011 (i.e., one month, one year and three years after heavy traffic) for CA. To test the capacity of earthworms to recolonise traffic-plot edges, extra sampling was
131
performed at the border of the traffic plots (e.g. less than 2 m from control plots) in April 2011 at AZ. In total, 117 sampling points were analysed (i.e., three dates × two sites × two locations: the centre of control and traffic plots x three blocks × three sampling points + one location: traffic-plot edges × three blocks x three sampling points). Earthworms were collected by hand sorting within 0.09 m2 (i.e., 0.3 m × 0.3 m) to a depth of 25 cm, and species were identified using Bouché’s (1972) key in the laboratory. Earthworm density and biomass were quantified (m−2 ) and species were classified into epigeic, anecic and endogeic functional groups. 2.3. Statistical analysis One-way ANOVA models were used to test the effect of treatment (e.g. the centre and border of the traffic plots and the centre of the control plots) on earthworm density and biomass for each sampling date and study site. Treatment was the main fixed effect, and blocks were the random effect. Analyses were performed with a balanced mixed-effects model (aov) using R software. When effects were found to be significant at p < 0.05, means were compared using the Tukey test. 3. Results and discussion 3.1. Earthworm abundance and diversity Earthworm density ranged from 69 to 177 and 0 to 91 individuals m−2 in control plots at AZ and CA, respectively (Fig. 1), while earthworm biomass ranged from 21 to 67 and 0 to 31 g m2 in control plots at AZ and CA, respectively (Fig. 2). The number of species found in control plots in 2011 was higher at AZ than at CA (5 vs. 2, respectively), as was the number of functional groups (3 vs. 1, respective). At AZ, the endogeic species Aporrectodea caliginosa (30%) and Aporrectodea rosea (34%) dominated, followed by the anecic species Lumbricus terrestris (26%). The anecic species Aporrectodea giardi and the epigeic species Lumbricus castaneus were uncommon, together representing only 10%. At CA, the community was dominated by the epigeic L. castaneus (71%) followed by the epigeic species Lumbricus rubellus (29%). The difference in earthworm populations may be attributed partly to the lower pH found at CA (4.4–4.5 in the upper 30 cm) than at AZ (4.6–4.8 in the upper 30 cm). The abundance, biomass and diversity of earthworms found in our study are consistent with previous studies regarding pH values and humus forms (e.g. Mull vs. Moder) (Deleporte et al., 1997; Muys and Granval, 1997; Potthoff et al., 2008). 3.2. Initial effect of heavy traffic on earthworms Our results showed that epigeic species found in both sites were missing at T0 (Fig. 1), indicating that deforestation, including vegetation destruction, litter removal, and changes in soil moisture and temperature regime, impacted them more than anecic and endogeic species. Because epigeic species use the litter layer both as habitat and as food source (Bouché, 1977), this result is expected. The passage of the heavy forwarder decreased the specific soil volume by 17 and 21% at CA and AZ, respectively (Goutal et al., 2012a). Moreover, it is thought that soil compaction can displace topsoil along with accompanying soil organic matter, decrease structural porosity and increase water stagnation (Greacen and Sands, 1980; Horn et al., 2004). All of these effects may have contributed to the significant decrease in the density (by 97%, p < 0.001) and biomass (by 94%, p < 0.001) of earthworms measured at AZ, which agrees with previous studies carried out in forest (Jordan et al., 1999), prairie (Althoff et al., 2009) and agricultural systems (Söchtig and Larink, 1992; Capowiez et al., 2012). When the effect is analysed by functional group, endogeic species seemed less sensitive than
N. Bottinelli et al. / Applied Soil Ecology 73 (2014) 130–133
Density of earthworms (number m-2)
132
200
AZ site
200 Epigeic
160
CA site
160
Anecic 120
Endogeic
120
80
80
40
40
0
0 Co
Tr
Co
T0 June
Tr
Co
T+1 November
Tr-b
Tr
Tr
Co
T+4
T0 April
April
Co
Tr
Co
T+1 November
Tr
T+3 April
Fig. 1. Mean density of the three earthworm functional groups by treatment and number of years after compaction: AZ, Azerailles; CA, Clermont-en-Argonne; Co, control plot; Tr, traffic plot; Tr-b, border of traffic plot; T0 , T+1 , T+2 , T+3 , T+4 , zero, first, second, third and fourth years after compaction, respectively. Error bars represent 1 standard deviation (n = 3).
anecic species since, on average, five endogeic m−2 were found in traffic plots after trafficking whereas no anecic species were found. Because endogeic species are soil feeders that live in the organomineral soil and construct non-permanent burrows (Bouché, 1977), they are assumed to be less affected by loss of topsoil organic matter and disturbance of their burrow systems (Cuendet, 1992). At CA, because earthworms were exclusively represented by epigeic species, the effect of compaction was masked by the deforestation at T0 . Nevertheless, the lower density (by 74%, p < 0.001) and biomass (by 85%, p < 0.001) of earthworms observed at T+1 in traffic compared to control plots also revealed the negative effect of compaction at this site. 3.3. Recovery of earthworms in traffic plots At AZ, the density of the five earthworm species and their biomass did not exhibit any clear recovery four years after heavy traffic (Figs. 1 and 2). Their abundance and biomass were lower in traffic than in control plots at T+1 (p < 0.01) and T+4 (p < 0.01). When the effect was analysed by functional group, epigeic species had significantly lower density in traffic than in control plots at T+1 (p < 0.05) and T+4 (p < 0.01). Anecic species were always lower in
Biomass of earthworms (g m-2)
80
AZ site
traffic than in control plots; however, results were statistically significant only at T+4 (p < 0.01). Endogeic species were lower in traffic than in control plots at T+1 (p < 0.001) and T+4 (p < 0.01). The recovery of earthworm populations after traffic should depend first on the soil habitat quality for colonisation and second on earthworm mobility. Hence, we propose two alternate hypotheses to explain the results: (i) earthworms had low mobility (Eijsackers, 2011), and measurement performed in the centre of the traffic plots (i.e., 10–15 m from the control) was thus unable to detect their recovery and (ii) soil habitat quality (porosity, moisture and temperature regime, soil organic matter and vegetation) remained unsuitable for them, preventing their migration from control to traffic plots. To test the first hypothesis, we added an extra sampling point in the border of traffic plots at T+4 . Results showed that the density and biomass of earthworms measured in the border were not significantly different from those measured in centre (Figs. 1 and 2), confirming the second hypothesis. This means that soil habitat quality was not yet favourable for earthworms. In contrast, the density and biomass of the two epigeic species at CA increased gradually from T+1 to T+3 , and control and traffic plots were no longer significantly different at T+3 . Here, the complete recovery of epigeic species indicates that the soil habitat was suitable for them
80
70
70
60
60
50
50
40
40
30
30
20
20
10
10
0
CA site
0 Tr
Co T0 June
Co
Tr
T+1 November
Co
Tr-b T+4 April
Tr
Tr
Co T0 April
Co
Tr
T+1 November
Co
Tr T+3 April
Fig. 2. Mean biomass of earthworms by treatment and number of years after compaction: AZ, Azerailles; CA, Clermont-en-Argonne; Co, control plot; Tr, traffic plot; Tr-b, border of traffic plot; T0 , T+1 , T+2 , T+3 , T+4 , zero, first, second, third and fourth year after compaction, respectively. Error bars represent 1 standard deviation (n = 3).
N. Bottinelli et al. / Applied Soil Ecology 73 (2014) 130–133
for feeding and reproduction. Our findings thus raise the question of which factors at the two sites contributed to such different recovery rates of epigeic species. Because epigeic species live mainly on the soil surface (Bouché, 1977), it is unlikely that soil porosity explains the recovery of epigeic species. This is confirmed by Goutal et al. (2012a), who reported that the soil specific volume determined at 0–10 cm depth in the traffic plots at T+4 and T+3 in AZ and CA, respectively, was similar. We thus assume that differences in organic horizon layers between AZ and CA explain the different recovery rates observed. Before heavy traffic, the humus form at AZ was a Mull mesomull, while it varied from a Mull dysmull to a Moder at CA. Thus, both sites had a litter layer, but only CA had a thin humus layer. After heavy traffic, the litter layer disappeared and had barely recovered by the end of the study. Furthermore, traffic at CA did not affect the humus layer, indicating that it provides a suitable environment for epigeic species living there. In this case, the time necessary for epigeic species to recover at CA was linked more to their mobility (e.g. from control plots or refuge zones like stumps in traffic plots to compacted zones) than the recovery of soil porosity. Studies of the natural recovery of earthworm populations after compaction are few and show different times to recovery, varying from a few months to several years (Jordan et al., 1999; Althoff et al., 2009; Capowiez et al., 2012). The slow recovery of earthworms in our study can be explained as follows: (i) at AZ, soil properties were not yet suitable for earthworms, and the soil litter had not yet recovered after heavy traffic; and (ii) at CA, even though topsoil habitat was suitable for earthworms (e.g. presence of humus), the large size of the traffic plots (30 m × 50 m) did not allow for rapid colonisation from control plots. In other studies, Jordan et al. (1999) observed a complete recovery of earthworm density (Diplocardia omata and Diplocardia smithii) one year after forest soil compaction, while Althoff et al. (2009) reported that earthworm density recovered completely two to four years after compaction in a tallgrass prairie. Nevertheless, the width of traffic plots in these studies did not exceed 1 m, which could partly explain the high recovery rates observed. 4. Conclusions In our study, earthworm populations barely recovered within a four years study period at one site and those found at another site belonged only to the epigeic functional group, which is thought to play a minor role in soil structure. Thus, our results did not support our main hypothesis that the short-term recovery of soil specific volume after heavy traffic is caused by earthworm activities. Acknowledgements We are grateful to Boris Fratré and Fabrice Elegbede for their help in earthworm sampling and Michael and Michelle Corson for
133
useful English corrections on the manuscript. This work was financially supported by the GIP Ecofor Soere F-ore-T network and Feder grants for the project ‘Effets du tassement des sols forestiers sur le fonctionnement biogéochimique de l’écosystème et sur sa durabilité pour plusieurs fonctions’. References Althoff, P.S., Todd, T.C., Thien, S.J., Callaham Jr., M.A., 2009. Response of soil microbial and invertebrate communities to tracked vehicle disturbance in tallgrass prairie. Appl. Soil Ecol. 43, 122–130. Bouché, M.B., 1972. Lombriciens de France. Ecologie et systématique, Paris. Bouché, M.B., 1977. Stratégies lombriciennes. In: Lohm, U., Persson, T. (Eds.), Soil Organisms and Components of Ecosystems. Ecology Bulletin/NFR, Stockholm. Capowiez, Y., Cadoux, S., Bouchand, P., Roger-Estrade, J., Richard, G., Boizard, H., 2009. Experimental evidence for the role of earthworms in compacted soil regeneration based on field observations and results from a semi-field experiment. Soil Biol. Biochem. 41, 711–717. Capowiez, Y., Samartino, S., Cadoux, S., Bouchant, P., Richard, G., Boizard, H., 2012. Role of earthworms in regenerating soil structure after compaction in reduced tillage systems. Soil Biol. Biochem. 55, 93–103. Cuendet, G., 1992. Effect of pedestrian activity on earthworm populations of two forests in Switzerland. Soil Biol. Biochem. 24, 1467–1470. Deleporte, S., Hallaire, V., Tillier, P., 1997. Application of image analysis to a quantitative micromorphological study of forest humus. Eur. J. Soil Biol. 33, 83–88. Eijsackers, H., 2011. Earthworms as colonisators of natural and cultivated soil environments. Appl. Soil Ecol. 50, 1–13. Goutal, N., Boivin, P., Ranger, J., 2012a. Assessment of the natural recovery rate of soil specific volume following forest soil compaction. Soil Sci. Soc. Am. J. 76, 1426–1435. Goutal, N., Parent, F., Bonnaud, P., Demaison, J., Nourrisson, G., Epron, D., Ranger, J., 2012b. Soil CO2 concentration and efflux as affected by heavy traffic in forest in northeast France. Eur. J. Soil Sci. 63, 261–271. Goutal, N., Renault, P., Ranger, J., 2013. Forwarder traffic impacted over at least four years soil air composition of two forest soils in northeast France. Geoderma 193–194, 29–40. Greacen, E.L., Sands, R., 1980. Compaction of forest soils: a review. Aust. J. Soil Res. 18, 163–189. Horn, R., Vossbrink, J., Becker, S., 2004. Modern forestry vehicles and their impacts on soil physical properties. Soil Till. Res. 79, 207–219. Jordan, D., Li, F., Ponder Jr., F., Berry, E.C., Hubbard, V.C., Kim, K.Y., 1999. The effects of forest practices on earthworm populations and soil microbial biomass in a hardwood forest in Missouri. Appl. Soil Ecol. 13, 31–38. Jouquet, P., Dauber, J., Lagerlof, J., Lavelle, P., Lepage, M., 2006. Soil invertebrates as ecosystem engineers: Intended and accidental effects on soil and feedback loops. Appl. Soil Ecol. 32, 153–164. Jouquet, P., Huchet, G., Bottinelli, N., Thu, T., Duc, T., 2012. Does the influence of earthworms on water infiltration, nitrogen leaching and soil respiration depend on the initial soil bulk density? A mesocosm experiment with the endogeic species Metaphire posthuma. Biol. Fertil. Soils 48, 561–567. Langmaack, M., Schrader, S., Rapp-Bernhardt, U., Kotzke, K., 1999. Quantitative analysis of earthworm burrow systems with respect to biological soil-structure regeneration after soil compaction. Biol. Fertil. Soils 28, 219–229. Larink, O., Werner, D., Langmaack, M., Schrader, S., 2001. Regeneration of compacted soil aggregates by earthworm activity. Biol. Fertil. Soils 33, 395–401. Lee, K.E., Foster, R.C., 1991. Soil fauna and soil structure. Aust. J. Soil Res. 29, 745–775. Müller-Inkmann, M., Fründ, H.-C., Hemker, O., 2013. An experimental setup to assess earthworm behaviour in compacted soil. Biol. Fertil. Soils 49, 363–366. Muys, B., Granval, P., 1997. Earthworms as bio-indicators of forest site quality. Soil Biol. Biochem. 29, 323–328. Potthoff, M., Asche, N., Stein, B., Muhs, A., Beese, F., 2008. Earthworm communities in temperate beech wood forest soils affected by liming. Eur. J. Soil Biol. 44, 247–254. Söchtig, W., Larink, O., 1992. Effect of soil compaction on activity and biomass of endogeic lumbricids in arable soils. Soil Biol. Biochem. 24, 1595–1599.