of Champagne. Preliminary results. In On earthworms. (A. M. Bonvicini Pagliai and P. Omodeo, Eds), pp. 465-484. Selected symposia and monographs U.Z.I., 2,.
Soil Bid. Biochem. Vol. 29, No. 314, pp. 511-583, 1997 0 1997 Elsevier Science Ltd. All rights reserved
PII: soo38-0717(%)00182-4
Printed in Great Britain 003%0717/97$17.00+ 0.00
AGRICULTURAL PRACTICES AND THE SPATIAL DISTRIBUTION OF EARTHWORMS IN MAIZE FIELDS. RELATIONSHIPS BETWEEN EARTHWORM ABUNDANCE, MAIZE PLANTS AND SOIL COMPACTION F. BINET,‘*
V. HALLAIRE2
and P. CURMI*
‘Lab. Ecologic du Sol et Biologie des Populations, CNRS URA 1853 - Station Biologique, 35380, Paimpont, France and ‘Lab. Sciences du Sol, INRA ENSA - 65, route de St Brieuc, 35042, Rennes, France (Accepted 26 June 1996)
Snmmary-The relationships between the spatial heterogeneity of maize fields, due to row-cropping and farm machinery traffic, and earthworm abundance were studied in three plots receiving different organic matter treatments: no organic fertilizer, pig slurry and farmyard-manure. In all plots, there was no significant effect of farm machinery traffic although there was a tendancy for earthworms to be less abundant under inter-rows (wheel tracks) than in traffic-free inter-rows. In both the maize field without organic fertiliir and the maize treated with pig slurry, earthworms were primarily located along the maize row. Earthworm abundances were greater within than between rows (16 vs 6 nos 0.1 m-* in control, 30 vs 15 nos 0.1 m-* in slurry). In the farmyard-manure treatment, no row effect on the spatial pattern in earthworm numbers was found. However, worm biomass was approximately twice as high under the maize row as under the inter-row. This suggested a greater migration of adults to the maize roots or that juvenile worms grew faster there. Earthworm populations showed spatial variance in life cycle stage with populations under the maize row having proportionally more adults than populations between rows. Soil bulk-density was lower in than between maize rows and lower in maize fields amended with organic matter. Soil bulk-density and earthworm biomass were shown to be negatively correlated (r = - 0.92, n = 6). Image analysis of resin-impregnated soil blocks within and between rows showed that the soil under the row was characterized by a higher macroporosity (5.7 vs 0.7%) and also a greater diversity in size and shape of the macropores than occurred between the rows. c) 1997 Elsevier Science Ltd
INTRODUCTION
ery traffic. The investigation was conducted in three plots receiving different organic matter applications to also determine the influence of organic fertilizers on earthworm distribution. Soil bulk-density and macroporosity were analysed to specify relationships between earthworms, plants and soil compaction.
In grassland ecosystems, the spatial variability of plant cover (Babel et al., 1992) as well as disturbances
related
to dung
pat
deposits
(James,
1992;
Knight et al., 1992) can lead to a discontinuous distribution of earthworms across the site. Pizl (1992) noted that horizontal distribution of earthworms became more uneven during succession from cultivated fields to meadow and forest. In cultivated soils, Poier and Richter (1992) observed a spatial variation in earthworm numbers within 20-50 m under sugar beet and winter barley crops. They also reported differences among species: the larger the worm species, the greater the spatial distribution heterogeneity. The objective of this study was to investigate whether earthworm distribution under maize fields is a&ted by the spatial heterogeneity of the crop, due to both the row-cropping and the farm machin-
MATERIALSAND METHODS
The study was conducted in maize fields at the site of Le Rheu near Rennes experimental (Brittany, N.W. France). The fields had been planted to continuous maize (Zea mays L.) under conventional tillage since 1975 (Binet, 1993). Sampling for earthworms was carried out in three maize plots (size of each plot, 18 x 16 m) receiving different organic matter applications, in the fall of 1986 following harvest. The plot treatments were: maize without organic fertilizer (control), maize with pig slurry (40 t ha-’ year-‘) and maize with farmyard-manure (FYM, 45 t ha-’ year-‘). These organic fertilizers were uniformly distributed on overall soil surface before ploughing.
*Author for correspondence. Present address: CNRS URA 1853, Station Biologique, F 35380 - Paimpont, France. Fax: (011 33) 2.99.61.81.87. 577
F. Binet Edal.
578
0
A
0
(o.5d:5xo.lmq
0 0
B
0
(0.5 mz)
0 I Diatance/rowof~(an) Rowofmaize
lgxl
TraNldced Inter-row
m
m
hmp~bdonofaoilblodu
Row YKJrriT
Comp~n
Fig. 1. Position of the 1 m2 frame for the sampling of earthworms in relation to the crop row. Earthworm sampling
Macroporosity analysis
In each plot, three different zones were sampled: (1) the maize row, (2) the traffic-free inter-row, (3) the inter-row (wheel-tracks). A square metre iron frame divided into two 0.5 m* quadrats was positioned over all three zones with the row of maize in the middle of the frame (Fig. 1). Each 0.5 m* quadrat was divided into five units of 0.1 m*, with the central unit corresponding to the maize row, defined as point zero. The two units on the right side centred 20 and 40 cm from the row - covered the traffic-free inter-rows, whereas the two units on the left side - centred -20 and -40 cm from the row - were on the wheel-tracks. A total of six quadrats of 0.5 m2 were sampled from along three different maize rows. Earthworms were extracted using the formaldehyde method (Bouche and Aliaga, 1986). The formalin was applied across 0.5 m* areas and emerging worms from each 0.1 m* area were counted. Abundance (number 0.1 mw2) and biomass (g 0.1 m-*, on fresh wt basis) from the five sampled zones were compared pair-wise using the MannWhitney U-test. Soil bulk-density and maize crop measurements were also conducted in the same areas, where earthworms were sampled, by Barloy and Le Floch (1986). Bulk density of the upper 30 cm (ploughpan) of the soil under the maize row and under the traffic-free inter-row was measured using a densitometer (no data from the wheel-tracks was available). Density of rooting was determined by counting the number of roots in 5 x 5 cm quadrats, to a depth of 75 cm. The relationship between soil bulk-density and earthworm abundance was measured using the correlation test of Pearson (Minitab 7.1).
Image analysis techniques were used to characterize the macroporosity within the upper 10 cm of the soil profile in the maize row and at 20 and 40cm from the row under the traffic-free inter-row, in the maize plot without organic matter amendment. horizontally oriented soil blocks Four (15 x 10 x 5 cm) were taken from each of these three sampling locations. The soil blocks were impregnated with a polyester resin containing a UV fluorescent dye (Uvitex-O.B., Ciba-Geigy). For each soil block sampled, height images (four blocks x2 faces) were taken with a CCD camera, under UV illumination provided by two UV lamps (emission at 350 nm wavelength) oriented at an angle of 45”. Accurate images were obtained using the following acquisition parameters: diaphragm 4, gain 255, offset 175. The spectral resolution was 256 grey levels. Optical images were then digitized at the 75 grey level using VISILOG image-processing software. Images had a spatial resolution of 768 by 576 pixels and the corresponding photograph area was 69 x 52 mm. Pores smaller than 50 pixels (approximately 400 m equivalent-diameter) were considered as background noise or unrelated to fauna activity and were not included in the analysis. Properties recorded for pores of 50 pixels or larger were (1) the area which defined the pore size (in kilopixels, 1 kp = 1.6 mm equivalent-diameter) and (2) the index of elongation (area/perimeter*) which defined the pore shape. An elongation index of 1 corresponded to a nearly circular pore image, higher indices indicated more convoluted and irregularly elongated pore image. Macroporosity as % was obtained by dividing the total pore area by image area.
519
Spatial distribution of earthworms in maize fields
Table 1. Number (nos 0.1 rnm2)and biomass (g 0.1 m-*) (*SE) of earthworms under maize rows and traffic-free inter-rows (wheel tracks), in the three plot treatments Sampled zone
Inter-row with wheel tracks
Distance (cm) from row of maize
-40
Maize control Maize slurry Maize FYM
5.3 f l.lac 10.8 j, 3.0” 22.8 f 5Sa
Maize control Maize slurry Maize FYM
0.9 * 0.3” 1.5 k 0.6a 2.3 f 0.8”
-20
crop row 0
Numbers (nos 0.1 m-*) 3.7 + 1.1= 16.2 + 18.0 f 3.0” 29.7 k 24.5 + 6.3” 26.8 f Biomass (g 0.1 m-*) 0.7 f 0.2O 4.2 f 3.3 * l.OSb 4.9 f 4.9 f 1.vb 7.3 *
Traffic-free inter-row 20
+40
2.6b 5.&’ 1.6”
8.2 f 0.9’ 16.7 + 3.9@ 32.2 + 5.8”
6.3 f 1.3”’ 16.3 f 4.3”b 29.0 + 3.3L
0.7b 0.6b l.3b
1.7 * 0.T 3.0 * 0.9ab 6.4 + 1.Ob
1.5 f 0.2= 2.6 k 0.6” 3.2 + 0.4”
Note: means in the same row followed by the same letter are not significantly different at P < 0.05 (Mann-Whitney RESULTS
Abundance and distribution of earthworms
The earthworm community under maize crop was mainly composed of endogeic species. The endogeic Aporectodea caliginosa was most commonly found, accounting for 83, 69 and 56% of the population abundance under control, slurry and FYM plot treatments, respectively (Binet, 1993). Numbers and biomass of earthworms observed under maize rows, wheel-tracks and traffic-free inter-rows are presented in Table 1. Overall average number of earthworms was lower under inter-rows (wheel tracks) than in traffic-free inter-rows (4 vs 7, 14 vs 16 and 24 vs 3 1 earthworms 0.1 mP2 in control, slurry and FYM plots, respectively) although the difference was not significant. In each treatment, earthworm number and/or biomass decreased with distance from maize plants, but earthworm distribution in relation to the row varied also with the organic matter treatment. In plots not receiving organic matter, the numbers and biomass of earthworms were significantly two to four times greater within than between rows (16 vs 6 nos 0.1 m-’ and 4 vs 1 g 0.1 m-‘). In plot-treated
f/-test).
with pig slurry, earthworm abundances were significantly lower in the quadrat farthest from the maize row compared with under the maize row (30 vs 13 nos 0.1 me2 and 5 vs 2 g 0.1 m-*). In the plots receiving farmyard-manure, no significant variation due to row effect was found in earthworm numbers, but the biomass was two times greater within than between rows. This suggested a greater migration of adults to the maize roots or that juvenile worms grew faster there. Analysis of the age structure of the earthworm community (Fig. 2) also indicated that the proportion of adults decreased with distance from maize plants, especially in the FYM plot. Relationships between earthworms, soil bulk-density
maize plants and
Mean values of soil bulk-density related to the upper 30 cm of the soil profile (plough-pan) and maize rooting density are presented in Table 2. In each plot, soil bulk-density was lower in row than between rows, and also was lower in fields amended with organic matter, especially in FYM treatment. The highest rooting density was observed in the FYM plot; similar plant rooting was observed in
Fig. 2. Age structure of earthworm community as related to maize rows and compaction (0, maize rows; -20 and -40 cm, wheel tracks; + 20 and + 40 cm, traffic-free inter-rows).
F. Binet et al
580
Table 2. Bulk-density of the plough-pan (upper 30 cm of the soil profile) and characteristics of the maize crop observed in the three plot treatments (after. Barley and Le F&h, 1986) Organic amendments SlllIly
Farmyard-manure
Control
Soil Bulk-density (g cm-‘) Row Inter-row Organic matter (%)
1.32 + 0.08” 1.50 f O.Olb 1.5
l.12?0.068 1.41 + 0.03’ 2.2
1.48 f O& 1s2 + o& 1.4
Maize crop Height (cm) Yield(t maize stalks ha-‘) Density of rooting (nos 25 cm-‘)
143 7.9 119
158 9.4 118
173 12.4 149
Note: means in the same row and in the same column followed by the same letter are not significantly different at P < 0.05 (MannWhitney U-test)
control and pig slurry treatments. These results suggest that farmyard-manure, which is characterized by high organic matter release, interacts with plant roots to decrease soil compaction. Soil compaction was also shown to be related to earthworm distribution. A correlation coefficient of -0.920 (n = 6, critical value of r is 0.917 at P < 0.01) between earthworm biomass and soil bulk-density was found. This significant negative correlation suggests that earthworms contribute also to reduce soil compaction.
Distribution of the macroporosity
Macroporosity under the crop row (mean f SE: 5.7 f 0.9%) was nine times higher than under the inter-row at both 20 and 40 cm from the maize row (0.6 + 0.3 and 0.7 k 0.2%, respectively). This indicates that earthworms had a great effect on the macroporosity, but within a localized region. Figure 3 shows the distribution of pores with regard to the size and the shape. Macroporosity within rows was characterized by a great diversity in size and shape of pores. In particular, elongated pores (index of
1.6
l-l.5 Cl
1.5-2 Row
23
3-5 m
5-10
>lO
Inter- row
1.6
#
Pore shape_.~._.__........_ _____........_.__......___. ~--....-----._......... (index of elonption) ._.. 1.2 _--.----.___...___._-.-......____.___.__ n l-l _-....____..
r-r---
Fig. 3. Distribution of macroporosity as a function of pore size and pore shape within and between rows in unamended maize crops (the size is expressed in kilopixels, 1 kp = 1.6 mm equivalent-diameter; an index of elongation define the shape: an index of 1 corresponds to a circular pore image, higher indices indicate convoluted and elongated pore image).
Spatial distribution of earthworms in maize fields
581
Fig. 4. Comparative schema of the spatial distribution of earthworms in maize crops not receiving organic fertilization and amended with farmyard-manure. elongation > 3-4) were common within rows but none between rows. These elongated and irregularly shaped pores might be related to earthworm filled channels and obliquely cut channels. DISCUSSION Many studies have reported that soil compaction due to intensive machinery traffic greatly reduces earthworm populations in arable fields (Bostrom, 1986; Siichtig and Larink, 1992) apple orchards (Pizl, 1992) and vineyards (Cluzeau et al., 1987). Large decreases in earthworm abundance have also been observed in temperate grassland soils subjected to heavy cattle trampling (Piearce, 1984; Cluzeau et al., 1992). Conversely, Cuendet (1992) reported that the soil compaction induced by pedestrian activity increased the total earthworm population in a deciduous forest but reduced it in a coniferous forest. This was explained by the difference in availability and quality of the litter supplied in the top soil. Although earthworms were less abundant under the wheel tracks than under the traffic-free inter-rows, no significant effect of farm machinery traffic was observed in all of the three treatments investigated in our study. This lack of significant reduction may have been due to less compaction in our study (compaction due mainly to the machinery traffic used to harvest the crop) compared with heavy and repeated compaction conducted in the agricultural fields studies cited. SBB 2913-L-M
Crushing (direct effect) and soil compaction (indirect effects such as porosity decrease, waterlogging) are common explanations for reduction of earthworm populations. Binet et al. (1987) reported that over a 12 h night period, Lumbricus terrestris spent more time under the soil burrowing, and less time on the soil surface (searching for food and mating) in compacted soils (1.6 g cme3) than in light soils (1.1 g cm-‘). Activity of endogeic earthworms, measured as the numbers and the lengths of burrows, was significantly higher in less dense soils (Sochtig and Larink, 1992). Therefore, soil compaction may reduce the time available to earthworms for feeding and mating and as a long-term consequence lead to lower populations. As our investigations were conducted just after the harvest, there may not have been enough time for this long-term effect of soil compaction to occur. The tendancy for reduction that was observed might simply reflect earthworm crushing and possibly also the temporary water-logging observed under the wheel tracks. This study showed a preference of earthworms for soils sown to maize. From investigations on the relationships between earthworms and some plant species in a meadow, Babel et al. (1992) observed an attraction of earthworms to Rumex plants in contrast to other grasses (Graminae). This preference could not be interpreted in terms of soil moisture, nor soil organic matter content, and was therefore attributed to palatable substances associated with Rumex plants. In our case, the high abun-
582
F. Binet et al.
dance of earthworm under maize rows may be related to a higher reproduction and survival there. This concentration might also be related to a migration of earthworms to lower soil density, greater availability of trophic resources (decaying roots, rhizosphere microorganisms) and microclimate induced by the plant cover. The reduction in spatial bias in earthworm abundance with addition of farmyard-manure suggests this preference is primarly regulated by the trophic component that maize supplies. Therefore, homogeneous organic matter applications to throughout fields might reduce the trophic heterogeneity induced by the row-cropping of maize and consequently reduce the patchy distribution of earthwoms (Fig. 4). The higher aggregation of adult earthworms along the crop row is consistent with that observed for dung pats in grassland pastures (Hendriksen, 1991; TrChen et al., 1992; James, 1992). It suggests that both maize roots and dung pats (1) constitute a suitable environment for a faster growth of juveniles to mature stage or (2) are preferential sites for cocoon deposition. Indeed, it has been widely observed in situ that earthworms lay their cocoons in organic matter rich sites, such as the root density layer in grasslands (Gerard, 1967; Satchell, 1977) or in the soil beneath the litter layer in forests (Rtindgren, 1977). The present study showed an inverse relation between earthworm abundance and soil bulk-density. A similar relation was noted by Clements et al. (1991), who observed a dramatic increase in bulkdensity (from 1.O to 1.6 g cme3) in a grassland soil kept free of earthworms by repeated heavy pesticide applications for 20 years. Although it is difficult to distinguish clearly the effects of earthworms and roots, these negative correlations suggest that earthworm activity reduces compaction. The loosening effect of earthworms was also reported for a field study by Atlavinyte and Zimkuviene (1985) and from laboratory experiments by Joschko er al. (1989) and Rushton (1986). Analysis of soil blocks taken from the maize field not receiving organic fertilizer demonstrated that earthworms affected mainly the macroporosity. A positive correlation between earthworm abundance and the proportion of macropores has also been reported by Lee (1985), Shipitalo and Protz (1987) and Tomlin et al. (1992). As in our study, Knight et al. (1992) observed an increase in the proportion of macropores under dung pats in a grassland pasture as the consequence of earthworm aggregation below the dung pats, but no change in total porosity. This difference between the effect of earthworms on soil macroporosity and soil bulk-density must be related to the redistribution of the pore size which occurred through the earthworm burrowing activities. Previously discussed by Syers and Springett (1983), the phenomenon was demonstrated by West et al.
(1991) and by Binet and Curmi (1992) from morphological analysis of soil thin sections. It is likely that the pore redistribution varies with the initial compaction of the soil. Under the crop row where the earthworms were most numerous, the macroporosity was nine times higher than in other parts of the soil; however, this represents only 5% of the total porosity. Our calculation fits with the ones of Singh et al. (1991) which range from 3 to 5% in the upper 30 cm of a loamy soil, and with the estimate (5%) of Edwards and Lofty (1977) based on several studies. This proportion probably varies with soil properties as well as earthworm populations, but it indicates the small part of total soil porosity represented by macropores. Macroporosity associated with earthworms was diverse in size and shape, and there were especially more elongate pores. Similar findings were observed in cultivated soils under no-tillage (Shipitalo and Protz, 1987). This fact may be as important as the quantity of macropores. As shown by Joschko et al. (1992) morphological characteristics of earthworm channels affect water movement. It can be suggested that the diversity in size and shapes of macropores may also influence greatly the soil hydraulic properties even at a modest proportion of soil pores. In conclusion, the spatial distribution of earthworms in a maize field is influenced by at least three strongly interdependent factors. These are, the presence of maize plants, the soil density and the cultural practices with regard to organic fertilizer applications. This latter management factor was shown to play a major role since it affects the size of the earthworm population, their distribution regarding the plant roots, the soil compaction and finally the yield crop.
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Siichtig W. and Larink 0. (1992) Effect of soil compaction on activity and biomass of endogeic lumbricids in arable soils. Soil Biology & Biochemistry 24, 1595-1599. Syers J. K. and Springett J. A. (1983) Earthworm ecology in grassland soils. In Earthworm Ecology From Darwin to Vermiculfure (J. E. Satchell, Ed.), pp. 67-83. Chapman and Hall, London. Tomlin A. D., Penney R. and Miller J. J. (1992) Response of soil microfauna, microflora and structure to agricultural practices in corn, soybean and cereal rotations. In Soil Organisms and Soil Health, XI Imernarional Colloquium on Soil Zoology, Jyviiskylii. Finland.
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