Abstract
The aim of this work was to exemplify the specific contribution of both two- and three-dimensional (3D) X-ray computed tomography to characterise earthworm burrow systems. To achieve this purpose we used 3D mathematical morphology operators to characterise burrow systems resulting from the activity of an anecic ( Aporrectodea nocturna), and an endogeic species ( Allolobophora chlorotica), when both species were introduced either separately or together into artificial soil cores. Images of these soil cores were obtained using a medical X-ray tomography scanner. Three-dimensional reconstructions of burrow systems were obtained using a specifically developed segmentation algorithm. To study the differences between burrow systems, a set of classical tools of mathematical morphology (granulometries) were used. So-called granulometries based on different structuring elements clearly separated the different burrow systems. They enabled us to show that burrows made by the anecic species were fatter, longer, more vertical, more continuous but less sinuous than burrows of the endogeic species. The granulometry transform of the soil matrix showed that burrows made by A. nocturna were more evenly distributed than those of A. chlorotica. Although a good discrimination was possible when only one species was introduced into the soil cores, it was not possible to separate burrows of the two species from each other in cases where species were introduced into the same soil core. This limitation, partly due to the insufficient spatial resolution of the medical scanner, precluded the use of the morphological operators to study putative interactions between the two species
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References
Baker GH, Carter P, Barrett V, Hirth J, Mele P, Gourley C (2002) Does the deep-burrowing earthworm, Aporrectodea longa , compete with resident earthworm communities when introduced to pastures in south-eastern Australia? Eur J Soil Biol 38:39–42
Bastardie F, Cannavacciuolo M, Capowiez Y, de Dreuzy J-R, Bellido A, Cluzeau D (2002) A new simulation for modelling the topology of earthworm burrow systems and their effects on macropore flow in experimental soils. Biol Fertil Soils 36:161–169
Beven K, Germann P (1980) The role of macropores in the hydrology of field soils. Report no. 69. Institute of Hydrology, Wallingford Oxfordshire
Bouché MB (1972) Lombriciens de France. Ecologie et systématique. INRA, Paris
Bouma J (1991) Influence of soil macroporosity on environmental quality. Adv Agron 46:1–37
Capowiez Y (2000) Difference in burrowing behaviour and spatial interaction between the two earthworm species Aporrectodea nocturna and Allolobophora chlorotica. Biol Fertil Soils 30:341–346
Capowiez Y, Belzunces L (2001) Dynamic study of the burrowing behaviour of Aporrectodea nocturna and Allolobophora chlorotica: interactions between earthworms and spatial avoidance of burrows. Biol Fertil Soils 33:310–316
Capowiez Y, Pierret A, Daniel O, Monestiez P, Kretzschmar A (1998) 3D skeleton reconstructions of natural earthworm burrow systems using CAT scan images of soil cores. Biol Fertil Soils 27:51–59
Capowiez Y, Monestiez P, Belzunces L (2001) Burrow systems made by Aporrectodea nocturna and Allolobophora chlorotica in artificial cores: morphological differences and effects of interspecific interactions. Appl Soil Ecol 16:109–120
Delerue JF (2001) Segmentation 3D, application à l'extraction de réseaux de pores et à la caractérisation hydrodynamique des sols. Université Paris XI, Paris
Edwards WM, Shipitalo MJ, Owens LB, Norton LD (1989) Water and nitrate movement in earthworm burrows within long-term no-till cornfields. J Soil Water Conserv :240–243
Ehlers W (1975) Observations on earthworm channels and infiltration on tilled and untilled loess soil. Soil Sci 119:242–249
Elton KL, Koppi AJ (1994) Image analysis of apedal soil following burrowing activities of Microscolex dubius (Flechter) and Aporrectodea trapezoides (Duges) (Oligochaeta: Megascolecidae, Lumbricidae). In: Pankhurst CE (ed) Soil biota—management in sustainable farming systems. CSIRO, Melbourne East, pp 133–136
Fragoso C, Rojas P (1997) Size shift in the mexican earthworm species Balanteodrilus pearsei (Megascolecidae, Acanthodrilini): a possible case of character displacement. Soil Biol Biochem 29:237–240
Jégou D, Cluzeau D, Wolf HJ, Gandon Y, Trehen P (1998) Assessment of the burrow system of Lumbricus terrestris, Aporrectodea giardi and Aporrectodea caliginosa using X-ray computed tomography. Biol Fertil Soils 26:116–121
Jégou D, Hallaire V, Cluzeau D, Tréhen P (1999) Characterization of the burrow system of the earthworm Lumbricus terrestris and Aporrectodea giardi using X-ray computed tomography and image analysis. Biol Fertil Soils 29:314–318
Jégou D, Capowiez Y, Cluzeau D (2001) Interactions between earthworm species in artificial soil cores assessed through the 3D reconstruction of the burrow systems. Geoderma 102:123–137
Joschko M, Graff O, Muller PC, Kotzke K, Lindner P, Prestchner DP, Larink O (1991) A non-destructive method for the morphological assesment of earthworm burrow system in three dimensions by X-ray computed tomography. Biol Fertil Soils 11:88–92
Joschko M, Muller PC, Kotzke K, Dohring W, Larink O (1993) Earthworm burrow system development assessed by means of X-ray computed tomography. Geoderma 56:209–221
Kretzschmar A (1982) Éléments de l'activité saisonnière des vers de terre en prairie permanente. Rev Ecol Biol Sol 19:193–201
Kretzschmar A (1991) Burrowing activity of the earthworm Apporectodea longa limited by soil compaction and water potential. Biol Fertil Soils 11:48–51
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
Lavelle P (1997) Faunal activities and soil processes: adaptative strategies that determine ecosystem function. Adv Ecol Res 27:93–132
Lee KE, Foster RC (1991) Soil fauna and soil structure. Aust J Soil Sci 29:745–775
Li Y, Ghodrati M (1995) Transport of nitrate in soils as affected by earthworm activities. J Environ Qual 24:432–438
Ligthart TN, Peek GJCW (1997) Evolution of earthworm burrow systems after inoculation of lumbricid earthworms in a pasture in the Netherlands. Soil Biol Biochem 29:453–462
Lowe CN, Butt KR (1999) Interspecific interactions between earthworms: a laboratory-based investigation. Pedobiologia 44:808–817
Lowe CN, Butt KR (2002) Growth of hatchling earthworms in the presence of adults: interactions in laboratory culture. Biol Fertil Soils 35:204–209
McCoy EL, Boast CW, Stehouver RC, Kladivko EJ (1994) Macropore hydraulics: taking a sledgehammer to classical theory. In: Lal R, Stewart BA (eds) Soil processes and water quality. Lewis, Boca Raton, Fla., pp 303–348
Meyer F (1992) Mathematical morphology: from two dimensions to three dimensions. J Microsc 165:5–28
Monestiez P, Kretzschmar A (1992) Estimation of the relationship between structural parameters of simulated burrow systems and their partitionning effect. Soil Biol Biochem 24:1549–1554
Mooney SJ (2002) Three-dimensional visualization and quantification of soil macroporosity and water flow patterns using computer tomography. Soil Use Manage 18:142–151
Moran CJ (1994) Image processing and soil micromorphology. In: Ringrose-Voase AJ, Humphreys GS (eds) Proceedings of the IXth International Working Meeting on Soil Micromorphology, Townsville, Australia, July 1992. Elsevier, Amsterdam, pp 459–482
Moran CJ, McBratney AB (1992) Acquisition and analysis of three-component digital images of soil pores structure. I. Method. J Soil Sci 43:541–549
Munyankusi E, Gupta SC, Moncrief JF, Berry EC (1994) Earthworm macropores and preferential transport in a long-term manure applied Typic Hapludalf. J Environ Qual 23:773–784
Perret J, Prasher SO, Kantzas A, Langford C (1999) Three-dimensional quantification of macropore networks in undisturbed soil cores. Soil Sci Soc Am J 63:1530–1543
Pierret A, Moran CJ, Pankhurst CE (1999) Differentiation of soil properties related to the spatial association of wheat roots and soil macropores. Plant Soil 211:51–58
Pierret A, Capowiez Y, Belzunces L, Moran CJ (2002) 3D reconstruction and quantification of macropores using X-ray computed tomography and image analysis. Geoderma 106:247–271
Quillin KJ (1999) Kinematic scaling of locomotion by hydrostatic animals: ontogeny of peristaltic crawling by the earthworm Lumbricus terrestris. J. Exp Biol 202:661–674
Rogasik H, Crawford JW, Wendroth O, Young IM, Joschko M, Ritz K (1999) Discrimination of soil phases by dual-energy X-ray tomography. Soil Sci Soc Am J 63:741–751
Serra J (1982) Image analysis and mathematical morphology. Academic Press, London
Shuster WD, Subler S, McCoy EL (2001) Deep-burrowing earthworm additions changed the distribution of soil organic carbon on a chisel-tilled soil. Soil Biol Biochem 33:983–996
Vogel HJ (1997) Morphological determination of pore connectivity as a function of pore size using serial sections. Eur J Soil Sci 48:365–377
Volkmar KM (1996) Effects of biopores on the growth and N-uptake of wheat at three levels of soil moisture. Can J Soil Sci 76:453–458
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Capowiez, Y., Pierret, A. & Moran, C.J. Characterisation of the three-dimensional structure of earthworm burrow systems using image analysis and mathematical morphology. Biol Fertil Soils 38, 301–310 (2003). https://doi.org/10.1007/s00374-003-0647-9
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DOI: https://doi.org/10.1007/s00374-003-0647-9