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Impacts of fauna on an upland grassland soil as determined by micromorphological analysis
Applied Soil Ecology 20 (2002) 133–143
Impacts of fauna on an upland grassland soil as determined by micromorphological analysis D.A. Davidson a,∗ , P.M.C. Bruneau a , I.C. Grieve a , I.M. Young b a
Department of Environmental Science, Stirling University, Stirling, Scotland FK9 4LA, UK b SIMBIOS, University of Abertay Dundee, Dundee, Scotland DD1 1HG, UK
Received 23 August 2001; received in revised form 4 February 2002; accepted 5 February 2002
Abstract It is widely recognised that soil fauna are distinguished by their abundance and diversity. However, there is a surprising lack of knowledge on the precise functional roles played by many animals within soils. This is the basis to the UK NERC Thematic Programme on Biological Diversity and Ecosystem Function in Soil in an upland grassland ecosystem. In this programme 19 team projects have the overall objective of assessing such biological diversity and ecosystem function. This paper reports preliminary results from a project designed to investigate the interactions between the activity of fauna and soil structure. The approach is based on investigating the nature and distribution of excremental pedofeatures using soil micromorphology. The experimental site, at an elevation of 320 m, is situated on the Macaulay Land Use Research Institute’s Sourhope Research Station in the Bowmont valley to the south of Kelso in the Scottish Borders. The vegetation at the site is an acid upland grassland, dominated by Agrostis capillaris, developed on a brown forest soil (Sourhope Series) which has been cultivated in the past. For the upper soil horizons, eight types of excremental pedofeatures are identified according to the size, shape and composition. In both the organic horizon (H) and the underlying mineral horizon (Ah), the bulk of the soil volume consists of excremental pedofeatures derived from enchytraeids, earthworms with excrement either in vermiform or mammilated forms and surface feeding animals such as beetles. Enchytraeid excrement increases with depth from 13% in the LF to 29% in the Ah horizon. Excrement from oribatid mites is only present to a limited extent (4%) in the LF horizon. Earthworm excrement is present in all horizons. Within the lower part of the H horizon, some profiles have a narrow (1–1.5 cm) dark grey organic layer dominated by phytoliths and also distinguished by having fewer excremental features. The key finding is the extent to which excrement from a fairly small range of soil fauna is dominant in the upper organic and organo-mineral horizons. Overall, the results demonstrate a close relationship between soil horizons and faunal activity as expressed in excremental pedofeatures. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Soil fauna; Faecal material; Micromorphology; Upland soil
1. Introduction Knowledge of the diversity and functional roles of soil fauna is essential from the scientific and management standpoints. In soil ecology, the general approach ∗ Corresponding author. E-mail address: [email protected] (D.A. Davidson).
is to investigate the effects of faunal groups on key ecological processes, such as carbon cycling (e.g. Hassink et al., 1993); in contrast, relatively little is known about the interaction in cool temperate areas of soil fauna with soil, with the exception of earthworm activity in arable soils. In grassland ecosystems, soil faunal diversity and community structure have been studied for their impacts on key ecological processes such as
0929-1393/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 9 - 1 3 9 3 ( 0 2 ) 0 0 0 1 7 - 3
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carbon cycling or respiration, for interspecies relationships or for effects of management practices (Lavelle et al., 1997, Maire et al., 1999, Bardgett et al., 1999, Fromm et al., 1993). However, quantification of faunal communities is in itself not sufficient to understand soil ecosystems as ecological change involves modification of the soil environment in which fauna exist (Bardgett and Cook, 1998). The link between soil structure and soil fauna has been investigated mainly in the mineral soil and for meso to macro fauna. The impact of earthworms on soil structure has been widely investigated, as the burrowing effect is important in modifying the overall physical properties of agricultural soil including aggregate stability (Lee and Foster, 1991, Wolters, 1991, Decaens et al., 1998, Topoliantz et al., 2000). Bioturbation by earthworms not only changes soil drainage properties but also modifies the organisation of void space. In organic horizons, soil fauna exert a profound influence on the soil fabric. Their excrement (faecal pellets) constitute most of the microaggregates in organic horizons (Babel, 1975, Ponge, 1991, Barois et al., 1998, Phillips and Fitzpatrick, 1999). Faecal materials can accumulate to such an extent that they dominate the horizons. Different groups of animals can produce excrement which cannot be distinguished by micromorphology. The size of excrement is dependent on mouth size and excretal mechanisms, while excrement composition depends upon food intake. Overall, it is difficult to link particular fauna with distinctive excremental types (Ponge, 1991; Kooistra, 1991; Martin and Marinissen, 1993; Phillips and Fitzpatrick, 1999). Soil micromorphology is based on the analysis of thin sections prepared from undisturbed blocks of soil. Thus, it provides a method for studying the interactions between fauna and soils, as demonstrated in the study by Bal (1970) who investigated the extent to which soil fauna influenced the development of humus profiles under two contrasting tree types. It was found, for example, that the H horizon under oak consisted entirely of loose faecal material. The investigation of excremental pedofeatures is integral to micromorphological description and is the basis to the project reported in this paper. The approach used to characterise excremental pedofeatures is based on the work of Babel (1975), Bullock et al. (1985) and Fitzpatrick (1993). The aims of the study are to:
1. determine the impact of fauna on soils within the experimental site through investigating the type, amount and distribution of excrement in the upper horizons, 2. compare soil faunal activity in different horizons, as expressed in excremental pedofeatures, 3. determine the effects of soil faunal activity on the development of the upper horizons of an upland grassland soil.
2. Materials and methods 2.1. The experimental site and sampling The experimental site (NT855196) is situated in the Bowmont valley to the south of Kelso in the Scottish Borders. The site has been cultivated in the past, as indicated by the presence of rig and furrow features. The effect of such cultivation and associated manuring was to stimulate soil faunal activity in the topsoil (Davidson, in press). Pollen investigation at a nearby site at Sourhope by Tipping (1997) indicated that cereal and oat pollen were present from ca. a.d. 1100; no cereal pollen were recorded after a.d. 1650. This would indicate that the experimental site at Sourhope is likely to have been cultivated and manured until the middle of 17th century and possibly even slightly later. Sheep grazed the site for the past 50 years, but have been excluded from the experimental plot since April 1998. The soil is a brown forest soil belonging to the Sourhope Series (SH 74711) and is developed on a glacial till derived from andesitic lava, (Kenny, 1998). A representative profile description is provided in Table 1. Cultivation in the past would have homogenised the upper horizons and improved drainage through rig construction. Following abandonment, the upper litter and peaty horizons would have gradually formed. Near the base of the H horizon, a dark reddish grey to dark grey (5YR4/2 to 10YR 4/1) horizon (1–1.5 cm thick) occurs in parts of the experimental site. Examination of the thin sections indicated that this thin horizon is coincident with a much higher phytolith content than the upper H horizon. These occur dominantly as fragments, ca. 10 m in length; where complete phytoliths are evident, they are dominantly rectangular with smooth parallel sides, but examples
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Table 1 Soil profile description for the Soil Biodiversity experimental site on Sourhope farm (from baseline data provided by Kenny (1998) as part of the NERC Thematic Programme on Soil Biodiversity) Horizon
Depth (cm)
Soil description
LF FH
0–1 1–3
H
3–8
Ah
8–26
AB
26–37
Bsh
37–55
BCx
55–78
C
78–90
No identifiable mineral grains; fibrous; moist; no stones; clear smooth boundary Dark grey, 10YR 4/1 matrix colour; no identifiable mineral grains; fibrous; moist; abundant very fine fibrous roots; common fine fleshy roots; no stones; sharp wavy boundary Very dark grey, 10YR 3/1 matrix colour; loamy peat; amorphous; moist; weak medium subangular blocky structure; abundant very fine fibrous roots; common fine fleshy roots; no stones; sharp irregular boundary Dark reddish brown, 5YR 3/2 matrix colour; sandy silt loam; no mottles; moderate medium angular blocky structure; moist; friable; many very fine fibrous roots; common fine fleshy roots; common medium subangular undifferentiated intermediate igneous stones; common large subangular andesite stones; clear smooth boundary Brown, 7.5YR 5/2 matrix colour; fine sandy silt loam; no mottles; weak fine subangular blocky structure; moist; friable; many very fine fibrous roots; common fine fleshy roots; many very small angular undifferentiated intermediate igneous stones; few small subangular undifferentiated intermediate igneous stones; clear irregular boundary Yellowish red, 5YR 5/6 matrix colour; fine sandy silt loam; no mottles; weak fine subangular blocky structure; moist; friable; common very fine fibrous roots; few fine fleshy roots; abundant very small angular undifferentiated intermediate igneous stones; common small subangular undifferentiated intermediate igneous stones; sharp wavy boundary Reddish brown, 2.5YR 4/4 matrix colour; strong brown, 7.5YR 5/6 mottle colour; sandy clay loam; common fine distinct clear mottles; massive structure tending to moderate medium platy structure; moist; moderate induration; few very fine fibrous roots; very abundant very small angular andesite stones; common medium subangular andesite stones; clear wavy boundary Reddish brown, 5YR 5/3 matrix colour; sandy silt loam; no mottles; massive structure; moist; firm; no roots; very abundant very small angular undifferentiated intermediate igneous stones; common medium subangular andesite stones
Altitude
308 m
Slope description
7◦
Soil drainage
Free
Series
Sourhope
Major soil subgroup
Brown forest soil
Rock type
Andesite and undifferentiated intermediate igneous
of rectangular tapered with smooth or serrated sides, as well as dumbbell and sinuate (polylobate) forms are also present. Sizes range from 25 to 250 m and these phytoliths are assumed to have been derived from grasses following the abandonment of the rigs for cultivation. This organic horizon is labelled as Hphy to indicate its high phytolith content. Diatoms also occur in this horizon. In this study, interest is focused on
the effect of soil animals on the upper soil horizons, principally the LF, H, Hphy and upper part of the Ah. The experimental site (100 m × 120 m) is located on a north-facing slope at ca. 5◦ (Fig. 1). The experimental design consists of five blocks arranged downslope. Each block contains six main plots (12 m×10 m) which are subdivided into sub-plots to allow for individual sampling by the various project participants.
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Fig. 1. Location of the Sourhope experimental site in south-east Scotland and the distribution of plots and soil sub-types. Samples were collected from plots 1B, 1F, 2B, 2C, 3B, 3D, 4D, 4F, 5A and 5B.
The results reported in this paper are determined from initial sampling in May 1999 of two plots in each of the five blocks. Within each of the 10 plots, four randomly selected samples were collected from the H and upper Ah horizons for micromorphological and chemical analysis. Disturbed samples from each major horizon were air-dried and used to determine the pH,
organic carbon and cation exchange properties. The 40 undisturbed blocks for micromorphological analysis were extracted from near the base of the LF horizon extending to the upper part of the Ah horizon, using vertically aligned 75 mm × 55 mm Kubiena tins. This sampling was done at the start of the field experiment, and thus all plots had been subject to the same previous
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Table 2 Average properties of soil horizons for the three soil sub-typesa
LF horizon Depth (cm) Moisture content H horizon Depth Colour Moisture content pH (in water) Total C (%) CEC (mmol kg−1 ) Hphy horizon Depth Colour Ah horizon Colour Moisture content pH (in water) Total C (%) CEC (mmol kg−1 )
Soil sub-type 1 (LF and Ah horizons)
Soil sub-type 2 (LF, H and Ah horizons)
Soil sub-type 3 (LF, H, Hphy and Ah horizons)
3.8 ± 0.2 0.28 ± 0.02
3.7 ± 0.2 0.36 ± 0.01
3.5 ± 0.2 0.39 ± 0.02
n.a.
3.0 ± Black 0.42 ± 5.3 ± 14.2 ± 106 ±
2.4 ± Black 0.42 ± 5.2 ± 16.2 ± 72 ±
0.2 0.02 0.05 0.6 16
0.1 0.02 0.06 0.5 11
n.a.
n.a.
1.3 ± 0.2 cm 5YR 4/2 to 10YR 4/1
10 to 7.5YR 3/2 0.2 ± 0.02 5.7 ± 0.04 7.2 ± 0.6 63 ± 8
7.5YR 3/2 0.31 ± 0.01 5.3 ± 0.04 6.50 ± 0.4 72 ± 3
10YR 3/2 0.31 ± 0.02 5.1 ± 0.04 6.8 ± 0.3 80 ± 3
Here, n.a. means not applicable a Moisture content values (m3 m−3 ) refer to one sampling event (May 1999).
management. Samples collected after May 1999 will be analysed to determine the effect of liming on soil faunal activity. Sampling was restricted to raised rigs and excluding the furrows where drainage conditions were different. From an initial survey of the soils within the experimental site at Sourhope, three sequences of upper horizons were identified (Table 2). Soil sub-type 1 has an LF directly overlying an Ah horizon. This sub-type is more associated with the soils on higher, and thus better, drained rigs. Soils of sub-type 2 have LF and H horizons which overlie the Ah horizon. Soil sub-type 3 is distinguished by the presence of two H horizons (viz. H and Hphy ). Despite these differences in upper soil horizon sequences, the soil sub-types all belong to the Sourhope Soil Series, though some variation in soil drainage is evident over the experimental site. 2.2. Thin section preparation and analysis From the samples collected in the Kubiena tins, thin sections (30 m thick) were prepared using standard procedures in the micromorphological laboratory
at the Department of Environmental Science, University of Stirling (http://www.envsci.stir.ac.uk/thin). Thin sections were described using a modification of the soil micromorphological systems of Brewer (1964), Bullock et al. (1985) and Fitzpatrick (1984, 1993). Each thin section was first divided into apparently homogeneous areas on the basis of visual examination. These areas of interest were assigned to soil horizons using the field profile descriptions and thin section evidence. The 40 slides were then systematically examined using a petrological microscope at magnifications ranging from 12.5 to 40× using plane and cross-polarised light. For each horizon, soil structure, void space, characteristics of the fine material and of larger organic and/or mineral features were recorded. The presence of roots, plant fragments, lignified materials, charcoal, sclerotia, fruiting bodies, mycorrhiza, fungal spores, phytoliths and mineral and rock fragments were also noted. Particular emphasis was given to the nature and occurrence of excremental pedofeatures with distinctive morphologies (Fig. 2). The classification system, summarised in Table 3, is based on the types described
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Fig. 2. Examples of excremental pedofeatures. (A) Excrement derived from enchytraeids (scale bar 0.5 mm). (B) Excrement derived from earthworms (scale bar 1.0 mm).
by Babel (1975) and Bullock et al. (1985). Links between excrement type and soil animals are proposed, but these need to be interpreted with care. Babel (1975) comments that excrement from enchytraeids and Collembola is very similar though granular enchytraeid excrement is more distinctive in F and H horizons where enchytraeids are active as secondary decomposers. An additional problem is that excrement from primary consumers is quickly consumed by other animals. The growth of fungal hyphae can also cause the disintegration of excrement where enchytraeids are active as secondary decomposers. Babel (1975) also notes that it is difficult to distinguish between excrement from isopods and diplopods. The investigation of excremental pedofeatures was done at two levels.
2.2.1. Level 1 analysis For each horizon in the 40 slides, the abundance of each class of excremental pedofeature was recorded using six frequency categories: (1) not present (<0.5%), (2) very low (0.5–4%), (3) few (5–14%), (4) frequent (15–29%), (5) dominant (30–50%) and (6) very dominant (>50%). Other details recorded for each type of excrement were average size (in m), content (e.g. organo-mineral/organic, particulate/organic, amorphous), distribution (random/cluster/tubulic), association with other features, degree of coalescence and colour. 2.2.2. Level 2 analysis To provide more quantitative data, manual point counting of excremental pedofeatures was done on 10
Table 3 Different types of excremental pedofeatures as found in upper soil horizons of the Sourhope site Type A Type B Type C Type D Type E Type F Type G Type H
Fine to moderately fine micro-excrements (<150 m), spherical/oblong shape with sharp boundaries, dominantly from enchytraeids but also including fine micro-excrements from mites and associated with plant fragments Fine to moderately fine (<250 m) undifferentiated faecal material coating void spaces Moderately fine to coarse faecal material (150–500 m), ellipsoidal in shape and with rough surfaces, open clustered distribution, dominantly from isopods Medium coarse to coarse faecal material (> 500 m), ellipsoidal in shape and with smooth surfaces, not clustered (e.g. from beetle larvae) Very coarse to extremely coarse faecal material (> 1000 m), irregular shape, rough surfaces, mainly organic with recognisable plant tissues (e.g. from diptera larvae) Medium faecal material (200–500 m), spherical, smooth surfaces in open clusters; probably from earthworms Coarse faecal material (>500 m), mammilated shape; from earthworms Coarse micro- to macro-excrements (>500 m), vermiform shape; from earthworms
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slides (one per plot). Use of an X–Y mechanical microscope stage permitted observations to be made on the occurrence of excrement types using a 2 mm grid. Such counting continued wherever possible in order to generate ca. 150 observations per horizon. In the level 1 analysis, a qualitative judgement was made on the extent of excremental pedofeatures with distinctive morphologies (Table 3). For the level 2 analysis, an additional excrement type (type I) was added since there were instances when material could be identified as of excremental origin, but no distinctive morphology could be determined within the field of view. Much of this undifferentiated excremental may be derived from earthworms. Point counting leads to a focus of attention on categorising individual excremental features which occur on grid intersections. Wider evidence for excrement being of earthworm origin may well be missed resulting in the potential under-representation of earthworm activity. Such difficulties can be avoided if use is made of image analysis for the identification and resultant measurement of excremental pedofeatures. In this project, it has been proved that it is possible, using this technique, to isolate excrement dominantly from enchytraeids and earthworms, though further work is required.
3. Results 3.1. Level 1 From the soil, thin sections, 14 LF, 30 H, 20 Hphy and 37 Ah horizons were identified and described. In this grassland system, excremental pedofeatures features are well preserved in the soil with morphologies which can be assigned to the classes summarised in Table 3. Excrement constitutes the bulk of the LF, H and Ah horizon with the remainder dominantly void space in the H horizon and void space and mineral fragments in the Ah horizon. Fig. 3 shows for each horizon the modal frequency class for each type of excremental pedofeature feature. Excrement associated dominantly with enchytraeids (type A) and earthworms (types G and H) is the most abundant in all horizons. Type F is absent in the LF horizon, but occurs as few in the H and Hphy horizons and as frequent in the Ah horizon. It is likely that this excrement is derived from earthworms. The H
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Fig. 3. Modal class of excrement type per soil horizon. See Table 3 for description of excrement types.
horizon has the widest range of faecal types and the modal frequency of enchytraeid (type A) excrement is frequent while earthworm (types G and H) and isopod (type C) types are present in significant quantities. In contrast, in the Ah horizon, the modal frequency of type A is very dominant and that of earthworms and isopods are both very low. Sample sizes for the LF and Hphy horizons were much smaller than for the H and Ah due to their limited occurrence on the thin sections. Earthworm (types G and H) dominate the LF horizon. The Hphy horizon has less abundant faecal material, but, as in the H horizon, enchytraeid and earthworm excrement dominate. 3.2. Level 2 Table 4 gives the percentage of the area sampled in each horizon of each feature determined by point counting. These data are determined from summing the point counts on a horizon basis; it should be noted that the point counts for the LF and Hphy horizons were smaller due to their limited extent on the slides. Enchytraeid excrement appears to be dominant in the Ah horizon with a mean area of 29%. Excrement of definite earthworm origin is much less extensive and
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Table 4 Occurrence (%) of different excremental types and other features based on point counting (total of 3653) of 10 slides for the upper four soil horizonsa Horizon
LF H Hphy Ah
Excremental types
Other features
Type A (enchytraeids/ mites)
Type C (isopods)
Types F, G and H (earthworms)
Type I (undifferentiated)
Total excrement
Type J (organomineral)
Type K (plant fragment)
Type L (mineral fragment)
Type M (void space)
17.6 23.9 23.6 29.0
8.0 4.7 1.8 1.5
0.0 4.9 1.0 3.9
30.9 25.0 32.8 12.4
56.5 58.5 59.2 46.8
15.4 17.2 17.0 13.8
14.1 6.7 5.0 4.6
0.0 1.3 6.2 23.6
12.2 15.2 12.6 11.0
a These percents are determined from adding all the observations per horizon. Rare occurrences of other excremental types are not included.
predominantly located in the H and Ah horizons, but 25–33% of the slides from the LF and H horizons consists of organo-mineral material that appeared to be faecal in origin but cannot be identified with a particular morphology (type I). These data again suggest that different soil horizons have characteristically different animal activity, as revealed by the occurrence of their faeces. Table 4 also shows the differences in the distribution of void space and rock fragments between horizons. The H horizon has an average void space of 15% and a very low rock fragment content (1%), and as was expected, the Ah horizon has the highest rock fragment content (24%). Calculation of skewness indicated that the data for each excrement type, with the exception of earthworm excrement, could be considered to have an approximately normal distribution. Directional two-sample ‘t’ tests were used to test the hypothesis that faunal activity, as expressed in excremental features and void space, was greater in the H horizon
Table 5 Results from ‘t’ tests comparing means (%) calculated for each horizon on every slide Feature
Mean ± S.D. Mean ± S.D. Significance error (Ah) error (H)
Enchytraeid/mite 29.3 ± 5.5 excrement Isopod excrement 1.6 ± 0.6 Earthworm 3.9 ± 3.5 excrement Undifferentiated 12.5 ± 2.8 excrement Void space 10.9 ± 1.2
24.2 ± 5.6
ns
5.2 ± 1.1 5.7 ± 2.4
P = 0.007 ns
23.4 ± 4.3
P = 0.026
16.4 ± 2.2
P = 0.025
than in the Ah (Table 5). The table shows that no significant difference could be established between the horizons in the percentage area of either enchytraeid or earthworm excrement. However, there was a significantly greater isopod excrement in the H, with a mean value of just over thrice of that in the Ah, and significantly more undifferentiated excrement in the H, nearly twice of that in the Ah. Void space in the H horizon was also significantly greater, with approximately 50% more than in the Ah horizon.
4. Discussion The first objective of this study was to determine the impact of fauna on soils within the Sourhope experimental site through investigating the type, amount and distribution of excrement in the upper horizons. The results demonstrate that 56–59% of the upper organic horizons are composed of excrement, a clear indication on the impact of fauna; excrement also constitutes 47% of the upper part of the first organo-mineral horizon. Soil fauna thus play a crucial role in the development of an upland grassland soil such as this. The only cautionary note is that, such figures may be particularly high due to the past legacy at the Sourhope site of cultivation and manuring. The second objective was to compare soil faunal activity in different horizons as expressed in excremental pedofeatures. The differences in faunal activity among the horizons follow a consistent pattern. The greatest number of different forms of excrement is found in the H horizon. Enchytraeids and earthworms are both
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important contributors to faecal material in the organic horizons, but earthworms are much reduced and enchytraeids dominate in the Ah. This is consistent with soil chemical differences between the horizons. Exchangeable calcium is far greater in the H horizon, constituting about 40% of the CEC compared to less than 10% in the Ah horizon. The pH of both horizons is acidic, with values (measured in 0.01 mol l−1 CaCl2 ) between 2.8 and 4.2 in both horizons in the sampled plots. The third objective was to determine the effects of soil faunal activity on the development of the upper horizons. As already stated, the outstanding impact of fauna on the upper horizons of this upland grassland soil is in terms of digestion and organic and organo-mineral material to produce an abundance of excrement. Bal (1970) found similar results for moder-humus profiles and distinguished an upper H horizon formed by an accumulation of excrements and a lower H horizon consisting of ‘aged’ excrements. Ageing refers to gradual morphological changes in excrement arising from microbiological, physical and chemical processes with the ultimate collapse of soil aggregates consisting of excrement. Resistance to ageing can be provided by a ‘peritrophic membrane’ around excrement (Bal, 1970). The apparent durability of enchytraeid excrement as seen on the Sourhope slides may suggest a similar mechanism for their preservation. The generation of excrement is likely to be greatest in soils in the upper horizons where there is an abundance of organic matter. A soil formation question is, whether this excrement moves down-profile as a result of infiltration. Bal (1970) argues that the humus aggregates which occur between sand grains in an A1(2) horizon result from illuviation from upper organic horizons. The Ah horizon of the Sourhope soil consists of enchytraeid excrement (29%) surrounded by mineral fragments (24%). There is no micromorphological evidence to support the view that this material has been translocated from upper horizons, instead an in situ genesis is proposed. In a study on similar soils, and designed to investigate the translocation of soil pollen, Davidson et al. (1999) found evidence for movement by bioturbation processes rather than by water movement. The Hphy horizon seems unattractive to earthworms, though the presence of phytoliths seems to present
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little constraint to enchytraeids and to the animals who generated the undifferentiated forms of excrement. The formation of this horizon has been interpreted as a result of a particular concentration of phytoliths. An alternative possibility is that it is equivalent to an albic (E) horizon, but formed in organic matter. Jongerius and Pons (1962) describe soil formation (horizonation) in reclaimed peats in the Netherlands. They describe the process of illuviation of humic matter within the peat; this could result in a colour change from black (H horizon) to dark reddish grey to dark grey. In the process of peat ‘ripening,’ they ascribe key significance to the role of microarthropods, enchytraeids and various species of earthworms to soil development. The beginning of an E horizon within ca. 200 years accords with the papers on podzolisation, for example Bormann et al. (1995), who found that a welldeveloped E horizon formed in soils within 150 years. However, the micromorphological evidence suggests the concentration of phytoliths as the dominant reason for the formation of this horizon. As to be expected, the wetter areas are found mainly on the lower parts of the Sourhope experimental site where the thickness of the organic horizons (LF and H) is greater than on other parts of the site. It is in such localities that the Hphy horizon occurs. On average, the Hphy horizon has a lower void space than adjacent horizons and has fewer recognisable excremental pedofeatures. Where it occurs, the Hphy horizon is shallow (1.0–1.5 cm), albeit distinctive. In this horizon, vertical channels probably formed by earthworms, linking the upper H to the lower Ah horizon. In order to explain the distribution of phytoliths in Australian podzols, Hart and Humphreys (1997) proposed two hypotheses: (1) the static hypothesis, whereby a concentration of phytoliths results from an increase in deposition at some time in the past, and (2) the mobile hypothesis, whereby processes of bioturbation or shrink–swell cause the redistribution of phytoliths and their possible concentration in one horizon. Either of these hypotheses could apply at the Sourhope experimental site to explain the formation of the Hphy horizon. According to the first, the horizon may have formed simply by the concentration of grass phytoliths after abandonment of cultivation ca. 200 years ago, followed by the accumulation of a shallow peat, the H horizon. For the second, the net downward movement of phytoliths would have been greater than net upward
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redistribution by bioturbation, resulting in an enriched layer. Hart and Humphreys (1997) conclude by supporting this second hypothesis, though it should be noted that they were dealing with a thick and porous E horizon overlying a pan. The soil at Sourhope is analogous in that, the Hphy horizon, where it occurs, directly overlies the first organo-mineral horizon (Ah). It thus seems likely that the formation of this phytolith rich horizon is partially due to soil animals and then this horizon would have had an effect on further faunal activity.
5. Conclusions Overall, the micromorphological results as derived from an upland experimental site under acid grassland confirm the association between faunal activity and horizons. This is an interesting pedological outcome in that, the soil horizons are distinguished in the field on the basis of attributes such as colour and structure. Relationships between horizons and soil, physical and chemical properties are to be expected, but the results from these Sourhope slides also indicate that the soil horizons are also distinguished by having characteristic types of animal activity as expressed in the nature of excrement. The formation of horizons with distinctive physical, chemical and biological properties is a central concept in pedogenesis. These properties are necessarily interdependent and evolve as the soil develops. The identification of the cause and effect of relationships is particularly difficult in any type of ecosystem, but it may well be the case in upland organic rich soils, such that the formation of upper soil horizons is largely controlled by faunal activity rather than by the translocation of organic matter and iron and aluminium oxides.
Acknowledgements This work was funded by a grant (GST/02/2127) from the NERC Soil Biodiversity Programme. The authors also wish to acknowledge the technical assistance of George MacLeod who prepared the thin sections and Kate Howie who gave statistical advice.
References Babel, U., 1975. Micromorphology of soil organic matter. In: Gieseking, J.E. (Ed.), Soil Components, Vol. 1. Organic Components. Springler, Berlin, pp. 369–473 (Chapter 4). Bal, L., 1970. Morphological investigation in two moder-humus profiles and the role of the soil fauna in their genesis. Geoderma 4, 5–36. Bardgett, R.D., Cook, R., 1998. Functional aspects of soil animal diversity in agricultural grasslands. Appl. Soil Ecol. 10 (3), 263–276. Bardgett, R.D., Cook, R., Yeates, G.W., Denton, C.S., 1999. The influence of nematodes on below-ground processes in grassland ecosystems. Plant and Soil 212, 23–33. Barois, I., Dubroeucq, D., Rojas, P., Lavelle, P., 1998. Andosolforming process linked with soil fauna under the perennial grass Mulhembergia mascroura. Geoderma 86, 241–260. Bormann, B.T., Spaltenstein, H., McClellan, M.H., Ugulini, F.C., Cromack, K., Nay, S.M., 1995. Rapid soil development after windthrow disturbance in pristine forest. J. Ecol. 83, 747–757. Brewer, R., 1964. Fabric and Mineral Analysis of Soils. Wiley, New York, p. 470 Bullock, P., Fedoroff, N., Jongerius, A., Stoops, G., Tursma, T., Babel, U., 1985. Handbook for Soil Thin Section Description. Waine Publications, Wolverhampton, p. 152 Davidson, D.A., in press. Bioturbation in old arable soils: quantitative evidence from soil micromorphology. J. Arch. Sci. Davidson, D.A., Carter, S., Boag, B., Long, D., Tipping, R., Tyler, A., 1999. Analysis of pollen in soils: processes of incorporation and redistribution of pollen in five soil profile types. Soil Biol. Biochem. 31, 643–653. Decaens, T., Dutoit, T., Alard, D., Lavelle, P., 1998. Factors influencing soil macrofaunal communities in post-pastoral successions of western France. Appl. Soil Ecol. 9, 361–367. Fitzpatrick, E.A., 1984. Micromorphology of Soils. Chapman & Hall, London, p. 433. Fitzpatrick, E.A., 1993. Soil Microscopy and Micromorphology. Wiley, Chicester, p. 304. Fromm, H., Winter, K., Filser, J., Hantschel, R., Beese, F., 1993. The influence of soil type and cultivation system on the spatial distributions of soil fauna and micro-organisms and their interactions. Geoderma 60, 109–118. Hart, D.M., Humphreys, G.S., 1997. The mobility of phytoliths in soils: pedological considerations. In: Pinella, A., Juan-Tresserras, J., Machado, M. (Eds.), Proceedings of the First European Meeting on Phytolith Research: The State-ofthe-Art of Phytoliths in Soils and Plants. Centre de Ciencias Medioambientales, Madrid, pp. 93–99. Hassink, J., Bouwman, L.A., Zwart, K.B., Bloem, J., Brussard, L., 1993. Relationship between soil texture, physical protection of organic matter, soil biota, and C and N mineralization in grassland soils. Geoderma 57, 105–128. Jongerius, A., Pons, L.J., 1962. Soil genesis in organic soils. Boor en Spade 12, 156–168. Kenny, C., 1998. Soil Biodiversity NERC Thematic Programme Baseline Data. Macaulay Land Use Research Institute. Sourhope Research Station, Yetholm, Scottish Borders.
D.A. Davidson et al. / Applied Soil Ecology 20 (2002) 133–143 Kooistra, M.J., 1991. A micromorphological approach to the interactions between soil structure and soil biota. Agric. Ecosyst. Environ. 34, 315–328. Lavelle, P., Bignell, D., Lapege, M., Wolters, V., Roger, P., Ineson, P., Heal, O.W., Dhillion, S., 1997. Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur. J. Soil Biol. 33, 159–193. Lee, K.E., Foster, R.C., 1991. Soil fauna and soil structure. Aust. J. Soil Res. 29, 745–775. Maire, N., Borcard, D., Laczko, E., Matthey, W., 1999. Organic matter cycling in grassland soils of the Swiss Jura mountains: biodiversity and strategies of the living communities. Soil Biol. Biochem. 31, 1281–1293. Martin, A., Marinissen, J.C.Y., 1993. Biological and physicochemical processes in excrements of soil animals. Geoderma 56, 331–347.
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Phillips, D.H., Fitzpatrick, E.A., 1999. Biological influences on the morphology and micromorphology of selected Podzols (Spodosols) and Cambisols (Inceptisols) from the eastern United States and north-east Scotland. Geoderma 90, 327–364. Ponge, J.F., 1991. Food resources and diets of soil animals in a small area of Scots pine litter. Geoderma 49, 33–62. Tipping, R., 1997. Cereal cultivation on the Anglo-Scottish Border during the Little Ice Age. In: Mills, C.M., Coles G. (Eds.), Life on the Edge: Human Settlement and marginality. Symp. Assoc. Environ. Archaeol. 13, 1–11. Topoliantz, S., Ponge, J.F., Viaux, P., 2000. Earthworm and enchytraeid activity under different arable farming systems as exemplified by biogenic structures. Plant and Soil 225, 39– 51. Wolters, V., 1991. Soil invertebrates—effects on nutrients turnover and soil structure: a review. Z Planz Bodenkunde 154, 389–402.
Impacts of fauna on an upland grassland soil as determined by micromorphological analysis D.A. Davidson a,∗ , P.M.C. Bruneau a , I.C. Grieve a , I.M. Young b a
Department of Environmental Science, Stirling University, Stirling, Scotland FK9 4LA, UK b SIMBIOS, University of Abertay Dundee, Dundee, Scotland DD1 1HG, UK
Received 23 August 2001; received in revised form 4 February 2002; accepted 5 February 2002
Abstract It is widely recognised that soil fauna are distinguished by their abundance and diversity. However, there is a surprising lack of knowledge on the precise functional roles played by many animals within soils. This is the basis to the UK NERC Thematic Programme on Biological Diversity and Ecosystem Function in Soil in an upland grassland ecosystem. In this programme 19 team projects have the overall objective of assessing such biological diversity and ecosystem function. This paper reports preliminary results from a project designed to investigate the interactions between the activity of fauna and soil structure. The approach is based on investigating the nature and distribution of excremental pedofeatures using soil micromorphology. The experimental site, at an elevation of 320 m, is situated on the Macaulay Land Use Research Institute’s Sourhope Research Station in the Bowmont valley to the south of Kelso in the Scottish Borders. The vegetation at the site is an acid upland grassland, dominated by Agrostis capillaris, developed on a brown forest soil (Sourhope Series) which has been cultivated in the past. For the upper soil horizons, eight types of excremental pedofeatures are identified according to the size, shape and composition. In both the organic horizon (H) and the underlying mineral horizon (Ah), the bulk of the soil volume consists of excremental pedofeatures derived from enchytraeids, earthworms with excrement either in vermiform or mammilated forms and surface feeding animals such as beetles. Enchytraeid excrement increases with depth from 13% in the LF to 29% in the Ah horizon. Excrement from oribatid mites is only present to a limited extent (4%) in the LF horizon. Earthworm excrement is present in all horizons. Within the lower part of the H horizon, some profiles have a narrow (1–1.5 cm) dark grey organic layer dominated by phytoliths and also distinguished by having fewer excremental features. The key finding is the extent to which excrement from a fairly small range of soil fauna is dominant in the upper organic and organo-mineral horizons. Overall, the results demonstrate a close relationship between soil horizons and faunal activity as expressed in excremental pedofeatures. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Soil fauna; Faecal material; Micromorphology; Upland soil
1. Introduction Knowledge of the diversity and functional roles of soil fauna is essential from the scientific and management standpoints. In soil ecology, the general approach ∗ Corresponding author. E-mail address: [email protected] (D.A. Davidson).
is to investigate the effects of faunal groups on key ecological processes, such as carbon cycling (e.g. Hassink et al., 1993); in contrast, relatively little is known about the interaction in cool temperate areas of soil fauna with soil, with the exception of earthworm activity in arable soils. In grassland ecosystems, soil faunal diversity and community structure have been studied for their impacts on key ecological processes such as
0929-1393/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 9 - 1 3 9 3 ( 0 2 ) 0 0 0 1 7 - 3
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carbon cycling or respiration, for interspecies relationships or for effects of management practices (Lavelle et al., 1997, Maire et al., 1999, Bardgett et al., 1999, Fromm et al., 1993). However, quantification of faunal communities is in itself not sufficient to understand soil ecosystems as ecological change involves modification of the soil environment in which fauna exist (Bardgett and Cook, 1998). The link between soil structure and soil fauna has been investigated mainly in the mineral soil and for meso to macro fauna. The impact of earthworms on soil structure has been widely investigated, as the burrowing effect is important in modifying the overall physical properties of agricultural soil including aggregate stability (Lee and Foster, 1991, Wolters, 1991, Decaens et al., 1998, Topoliantz et al., 2000). Bioturbation by earthworms not only changes soil drainage properties but also modifies the organisation of void space. In organic horizons, soil fauna exert a profound influence on the soil fabric. Their excrement (faecal pellets) constitute most of the microaggregates in organic horizons (Babel, 1975, Ponge, 1991, Barois et al., 1998, Phillips and Fitzpatrick, 1999). Faecal materials can accumulate to such an extent that they dominate the horizons. Different groups of animals can produce excrement which cannot be distinguished by micromorphology. The size of excrement is dependent on mouth size and excretal mechanisms, while excrement composition depends upon food intake. Overall, it is difficult to link particular fauna with distinctive excremental types (Ponge, 1991; Kooistra, 1991; Martin and Marinissen, 1993; Phillips and Fitzpatrick, 1999). Soil micromorphology is based on the analysis of thin sections prepared from undisturbed blocks of soil. Thus, it provides a method for studying the interactions between fauna and soils, as demonstrated in the study by Bal (1970) who investigated the extent to which soil fauna influenced the development of humus profiles under two contrasting tree types. It was found, for example, that the H horizon under oak consisted entirely of loose faecal material. The investigation of excremental pedofeatures is integral to micromorphological description and is the basis to the project reported in this paper. The approach used to characterise excremental pedofeatures is based on the work of Babel (1975), Bullock et al. (1985) and Fitzpatrick (1993). The aims of the study are to:
1. determine the impact of fauna on soils within the experimental site through investigating the type, amount and distribution of excrement in the upper horizons, 2. compare soil faunal activity in different horizons, as expressed in excremental pedofeatures, 3. determine the effects of soil faunal activity on the development of the upper horizons of an upland grassland soil.
2. Materials and methods 2.1. The experimental site and sampling The experimental site (NT855196) is situated in the Bowmont valley to the south of Kelso in the Scottish Borders. The site has been cultivated in the past, as indicated by the presence of rig and furrow features. The effect of such cultivation and associated manuring was to stimulate soil faunal activity in the topsoil (Davidson, in press). Pollen investigation at a nearby site at Sourhope by Tipping (1997) indicated that cereal and oat pollen were present from ca. a.d. 1100; no cereal pollen were recorded after a.d. 1650. This would indicate that the experimental site at Sourhope is likely to have been cultivated and manured until the middle of 17th century and possibly even slightly later. Sheep grazed the site for the past 50 years, but have been excluded from the experimental plot since April 1998. The soil is a brown forest soil belonging to the Sourhope Series (SH 74711) and is developed on a glacial till derived from andesitic lava, (Kenny, 1998). A representative profile description is provided in Table 1. Cultivation in the past would have homogenised the upper horizons and improved drainage through rig construction. Following abandonment, the upper litter and peaty horizons would have gradually formed. Near the base of the H horizon, a dark reddish grey to dark grey (5YR4/2 to 10YR 4/1) horizon (1–1.5 cm thick) occurs in parts of the experimental site. Examination of the thin sections indicated that this thin horizon is coincident with a much higher phytolith content than the upper H horizon. These occur dominantly as fragments, ca. 10 m in length; where complete phytoliths are evident, they are dominantly rectangular with smooth parallel sides, but examples
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Table 1 Soil profile description for the Soil Biodiversity experimental site on Sourhope farm (from baseline data provided by Kenny (1998) as part of the NERC Thematic Programme on Soil Biodiversity) Horizon
Depth (cm)
Soil description
LF FH
0–1 1–3
H
3–8
Ah
8–26
AB
26–37
Bsh
37–55
BCx
55–78
C
78–90
No identifiable mineral grains; fibrous; moist; no stones; clear smooth boundary Dark grey, 10YR 4/1 matrix colour; no identifiable mineral grains; fibrous; moist; abundant very fine fibrous roots; common fine fleshy roots; no stones; sharp wavy boundary Very dark grey, 10YR 3/1 matrix colour; loamy peat; amorphous; moist; weak medium subangular blocky structure; abundant very fine fibrous roots; common fine fleshy roots; no stones; sharp irregular boundary Dark reddish brown, 5YR 3/2 matrix colour; sandy silt loam; no mottles; moderate medium angular blocky structure; moist; friable; many very fine fibrous roots; common fine fleshy roots; common medium subangular undifferentiated intermediate igneous stones; common large subangular andesite stones; clear smooth boundary Brown, 7.5YR 5/2 matrix colour; fine sandy silt loam; no mottles; weak fine subangular blocky structure; moist; friable; many very fine fibrous roots; common fine fleshy roots; many very small angular undifferentiated intermediate igneous stones; few small subangular undifferentiated intermediate igneous stones; clear irregular boundary Yellowish red, 5YR 5/6 matrix colour; fine sandy silt loam; no mottles; weak fine subangular blocky structure; moist; friable; common very fine fibrous roots; few fine fleshy roots; abundant very small angular undifferentiated intermediate igneous stones; common small subangular undifferentiated intermediate igneous stones; sharp wavy boundary Reddish brown, 2.5YR 4/4 matrix colour; strong brown, 7.5YR 5/6 mottle colour; sandy clay loam; common fine distinct clear mottles; massive structure tending to moderate medium platy structure; moist; moderate induration; few very fine fibrous roots; very abundant very small angular andesite stones; common medium subangular andesite stones; clear wavy boundary Reddish brown, 5YR 5/3 matrix colour; sandy silt loam; no mottles; massive structure; moist; firm; no roots; very abundant very small angular undifferentiated intermediate igneous stones; common medium subangular andesite stones
Altitude
308 m
Slope description
7◦
Soil drainage
Free
Series
Sourhope
Major soil subgroup
Brown forest soil
Rock type
Andesite and undifferentiated intermediate igneous
of rectangular tapered with smooth or serrated sides, as well as dumbbell and sinuate (polylobate) forms are also present. Sizes range from 25 to 250 m and these phytoliths are assumed to have been derived from grasses following the abandonment of the rigs for cultivation. This organic horizon is labelled as Hphy to indicate its high phytolith content. Diatoms also occur in this horizon. In this study, interest is focused on
the effect of soil animals on the upper soil horizons, principally the LF, H, Hphy and upper part of the Ah. The experimental site (100 m × 120 m) is located on a north-facing slope at ca. 5◦ (Fig. 1). The experimental design consists of five blocks arranged downslope. Each block contains six main plots (12 m×10 m) which are subdivided into sub-plots to allow for individual sampling by the various project participants.
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Fig. 1. Location of the Sourhope experimental site in south-east Scotland and the distribution of plots and soil sub-types. Samples were collected from plots 1B, 1F, 2B, 2C, 3B, 3D, 4D, 4F, 5A and 5B.
The results reported in this paper are determined from initial sampling in May 1999 of two plots in each of the five blocks. Within each of the 10 plots, four randomly selected samples were collected from the H and upper Ah horizons for micromorphological and chemical analysis. Disturbed samples from each major horizon were air-dried and used to determine the pH,
organic carbon and cation exchange properties. The 40 undisturbed blocks for micromorphological analysis were extracted from near the base of the LF horizon extending to the upper part of the Ah horizon, using vertically aligned 75 mm × 55 mm Kubiena tins. This sampling was done at the start of the field experiment, and thus all plots had been subject to the same previous
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Table 2 Average properties of soil horizons for the three soil sub-typesa
LF horizon Depth (cm) Moisture content H horizon Depth Colour Moisture content pH (in water) Total C (%) CEC (mmol kg−1 ) Hphy horizon Depth Colour Ah horizon Colour Moisture content pH (in water) Total C (%) CEC (mmol kg−1 )
Soil sub-type 1 (LF and Ah horizons)
Soil sub-type 2 (LF, H and Ah horizons)
Soil sub-type 3 (LF, H, Hphy and Ah horizons)
3.8 ± 0.2 0.28 ± 0.02
3.7 ± 0.2 0.36 ± 0.01
3.5 ± 0.2 0.39 ± 0.02
n.a.
3.0 ± Black 0.42 ± 5.3 ± 14.2 ± 106 ±
2.4 ± Black 0.42 ± 5.2 ± 16.2 ± 72 ±
0.2 0.02 0.05 0.6 16
0.1 0.02 0.06 0.5 11
n.a.
n.a.
1.3 ± 0.2 cm 5YR 4/2 to 10YR 4/1
10 to 7.5YR 3/2 0.2 ± 0.02 5.7 ± 0.04 7.2 ± 0.6 63 ± 8
7.5YR 3/2 0.31 ± 0.01 5.3 ± 0.04 6.50 ± 0.4 72 ± 3
10YR 3/2 0.31 ± 0.02 5.1 ± 0.04 6.8 ± 0.3 80 ± 3
Here, n.a. means not applicable a Moisture content values (m3 m−3 ) refer to one sampling event (May 1999).
management. Samples collected after May 1999 will be analysed to determine the effect of liming on soil faunal activity. Sampling was restricted to raised rigs and excluding the furrows where drainage conditions were different. From an initial survey of the soils within the experimental site at Sourhope, three sequences of upper horizons were identified (Table 2). Soil sub-type 1 has an LF directly overlying an Ah horizon. This sub-type is more associated with the soils on higher, and thus better, drained rigs. Soils of sub-type 2 have LF and H horizons which overlie the Ah horizon. Soil sub-type 3 is distinguished by the presence of two H horizons (viz. H and Hphy ). Despite these differences in upper soil horizon sequences, the soil sub-types all belong to the Sourhope Soil Series, though some variation in soil drainage is evident over the experimental site. 2.2. Thin section preparation and analysis From the samples collected in the Kubiena tins, thin sections (30 m thick) were prepared using standard procedures in the micromorphological laboratory
at the Department of Environmental Science, University of Stirling (http://www.envsci.stir.ac.uk/thin). Thin sections were described using a modification of the soil micromorphological systems of Brewer (1964), Bullock et al. (1985) and Fitzpatrick (1984, 1993). Each thin section was first divided into apparently homogeneous areas on the basis of visual examination. These areas of interest were assigned to soil horizons using the field profile descriptions and thin section evidence. The 40 slides were then systematically examined using a petrological microscope at magnifications ranging from 12.5 to 40× using plane and cross-polarised light. For each horizon, soil structure, void space, characteristics of the fine material and of larger organic and/or mineral features were recorded. The presence of roots, plant fragments, lignified materials, charcoal, sclerotia, fruiting bodies, mycorrhiza, fungal spores, phytoliths and mineral and rock fragments were also noted. Particular emphasis was given to the nature and occurrence of excremental pedofeatures with distinctive morphologies (Fig. 2). The classification system, summarised in Table 3, is based on the types described
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Fig. 2. Examples of excremental pedofeatures. (A) Excrement derived from enchytraeids (scale bar 0.5 mm). (B) Excrement derived from earthworms (scale bar 1.0 mm).
by Babel (1975) and Bullock et al. (1985). Links between excrement type and soil animals are proposed, but these need to be interpreted with care. Babel (1975) comments that excrement from enchytraeids and Collembola is very similar though granular enchytraeid excrement is more distinctive in F and H horizons where enchytraeids are active as secondary decomposers. An additional problem is that excrement from primary consumers is quickly consumed by other animals. The growth of fungal hyphae can also cause the disintegration of excrement where enchytraeids are active as secondary decomposers. Babel (1975) also notes that it is difficult to distinguish between excrement from isopods and diplopods. The investigation of excremental pedofeatures was done at two levels.
2.2.1. Level 1 analysis For each horizon in the 40 slides, the abundance of each class of excremental pedofeature was recorded using six frequency categories: (1) not present (<0.5%), (2) very low (0.5–4%), (3) few (5–14%), (4) frequent (15–29%), (5) dominant (30–50%) and (6) very dominant (>50%). Other details recorded for each type of excrement were average size (in m), content (e.g. organo-mineral/organic, particulate/organic, amorphous), distribution (random/cluster/tubulic), association with other features, degree of coalescence and colour. 2.2.2. Level 2 analysis To provide more quantitative data, manual point counting of excremental pedofeatures was done on 10
Table 3 Different types of excremental pedofeatures as found in upper soil horizons of the Sourhope site Type A Type B Type C Type D Type E Type F Type G Type H
Fine to moderately fine micro-excrements (<150 m), spherical/oblong shape with sharp boundaries, dominantly from enchytraeids but also including fine micro-excrements from mites and associated with plant fragments Fine to moderately fine (<250 m) undifferentiated faecal material coating void spaces Moderately fine to coarse faecal material (150–500 m), ellipsoidal in shape and with rough surfaces, open clustered distribution, dominantly from isopods Medium coarse to coarse faecal material (> 500 m), ellipsoidal in shape and with smooth surfaces, not clustered (e.g. from beetle larvae) Very coarse to extremely coarse faecal material (> 1000 m), irregular shape, rough surfaces, mainly organic with recognisable plant tissues (e.g. from diptera larvae) Medium faecal material (200–500 m), spherical, smooth surfaces in open clusters; probably from earthworms Coarse faecal material (>500 m), mammilated shape; from earthworms Coarse micro- to macro-excrements (>500 m), vermiform shape; from earthworms
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slides (one per plot). Use of an X–Y mechanical microscope stage permitted observations to be made on the occurrence of excrement types using a 2 mm grid. Such counting continued wherever possible in order to generate ca. 150 observations per horizon. In the level 1 analysis, a qualitative judgement was made on the extent of excremental pedofeatures with distinctive morphologies (Table 3). For the level 2 analysis, an additional excrement type (type I) was added since there were instances when material could be identified as of excremental origin, but no distinctive morphology could be determined within the field of view. Much of this undifferentiated excremental may be derived from earthworms. Point counting leads to a focus of attention on categorising individual excremental features which occur on grid intersections. Wider evidence for excrement being of earthworm origin may well be missed resulting in the potential under-representation of earthworm activity. Such difficulties can be avoided if use is made of image analysis for the identification and resultant measurement of excremental pedofeatures. In this project, it has been proved that it is possible, using this technique, to isolate excrement dominantly from enchytraeids and earthworms, though further work is required.
3. Results 3.1. Level 1 From the soil, thin sections, 14 LF, 30 H, 20 Hphy and 37 Ah horizons were identified and described. In this grassland system, excremental pedofeatures features are well preserved in the soil with morphologies which can be assigned to the classes summarised in Table 3. Excrement constitutes the bulk of the LF, H and Ah horizon with the remainder dominantly void space in the H horizon and void space and mineral fragments in the Ah horizon. Fig. 3 shows for each horizon the modal frequency class for each type of excremental pedofeature feature. Excrement associated dominantly with enchytraeids (type A) and earthworms (types G and H) is the most abundant in all horizons. Type F is absent in the LF horizon, but occurs as few in the H and Hphy horizons and as frequent in the Ah horizon. It is likely that this excrement is derived from earthworms. The H
139
Fig. 3. Modal class of excrement type per soil horizon. See Table 3 for description of excrement types.
horizon has the widest range of faecal types and the modal frequency of enchytraeid (type A) excrement is frequent while earthworm (types G and H) and isopod (type C) types are present in significant quantities. In contrast, in the Ah horizon, the modal frequency of type A is very dominant and that of earthworms and isopods are both very low. Sample sizes for the LF and Hphy horizons were much smaller than for the H and Ah due to their limited occurrence on the thin sections. Earthworm (types G and H) dominate the LF horizon. The Hphy horizon has less abundant faecal material, but, as in the H horizon, enchytraeid and earthworm excrement dominate. 3.2. Level 2 Table 4 gives the percentage of the area sampled in each horizon of each feature determined by point counting. These data are determined from summing the point counts on a horizon basis; it should be noted that the point counts for the LF and Hphy horizons were smaller due to their limited extent on the slides. Enchytraeid excrement appears to be dominant in the Ah horizon with a mean area of 29%. Excrement of definite earthworm origin is much less extensive and
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Table 4 Occurrence (%) of different excremental types and other features based on point counting (total of 3653) of 10 slides for the upper four soil horizonsa Horizon
LF H Hphy Ah
Excremental types
Other features
Type A (enchytraeids/ mites)
Type C (isopods)
Types F, G and H (earthworms)
Type I (undifferentiated)
Total excrement
Type J (organomineral)
Type K (plant fragment)
Type L (mineral fragment)
Type M (void space)
17.6 23.9 23.6 29.0
8.0 4.7 1.8 1.5
0.0 4.9 1.0 3.9
30.9 25.0 32.8 12.4
56.5 58.5 59.2 46.8
15.4 17.2 17.0 13.8
14.1 6.7 5.0 4.6
0.0 1.3 6.2 23.6
12.2 15.2 12.6 11.0
a These percents are determined from adding all the observations per horizon. Rare occurrences of other excremental types are not included.
predominantly located in the H and Ah horizons, but 25–33% of the slides from the LF and H horizons consists of organo-mineral material that appeared to be faecal in origin but cannot be identified with a particular morphology (type I). These data again suggest that different soil horizons have characteristically different animal activity, as revealed by the occurrence of their faeces. Table 4 also shows the differences in the distribution of void space and rock fragments between horizons. The H horizon has an average void space of 15% and a very low rock fragment content (1%), and as was expected, the Ah horizon has the highest rock fragment content (24%). Calculation of skewness indicated that the data for each excrement type, with the exception of earthworm excrement, could be considered to have an approximately normal distribution. Directional two-sample ‘t’ tests were used to test the hypothesis that faunal activity, as expressed in excremental features and void space, was greater in the H horizon
Table 5 Results from ‘t’ tests comparing means (%) calculated for each horizon on every slide Feature
Mean ± S.D. Mean ± S.D. Significance error (Ah) error (H)
Enchytraeid/mite 29.3 ± 5.5 excrement Isopod excrement 1.6 ± 0.6 Earthworm 3.9 ± 3.5 excrement Undifferentiated 12.5 ± 2.8 excrement Void space 10.9 ± 1.2
24.2 ± 5.6
ns
5.2 ± 1.1 5.7 ± 2.4
P = 0.007 ns
23.4 ± 4.3
P = 0.026
16.4 ± 2.2
P = 0.025
than in the Ah (Table 5). The table shows that no significant difference could be established between the horizons in the percentage area of either enchytraeid or earthworm excrement. However, there was a significantly greater isopod excrement in the H, with a mean value of just over thrice of that in the Ah, and significantly more undifferentiated excrement in the H, nearly twice of that in the Ah. Void space in the H horizon was also significantly greater, with approximately 50% more than in the Ah horizon.
4. Discussion The first objective of this study was to determine the impact of fauna on soils within the Sourhope experimental site through investigating the type, amount and distribution of excrement in the upper horizons. The results demonstrate that 56–59% of the upper organic horizons are composed of excrement, a clear indication on the impact of fauna; excrement also constitutes 47% of the upper part of the first organo-mineral horizon. Soil fauna thus play a crucial role in the development of an upland grassland soil such as this. The only cautionary note is that, such figures may be particularly high due to the past legacy at the Sourhope site of cultivation and manuring. The second objective was to compare soil faunal activity in different horizons as expressed in excremental pedofeatures. The differences in faunal activity among the horizons follow a consistent pattern. The greatest number of different forms of excrement is found in the H horizon. Enchytraeids and earthworms are both
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important contributors to faecal material in the organic horizons, but earthworms are much reduced and enchytraeids dominate in the Ah. This is consistent with soil chemical differences between the horizons. Exchangeable calcium is far greater in the H horizon, constituting about 40% of the CEC compared to less than 10% in the Ah horizon. The pH of both horizons is acidic, with values (measured in 0.01 mol l−1 CaCl2 ) between 2.8 and 4.2 in both horizons in the sampled plots. The third objective was to determine the effects of soil faunal activity on the development of the upper horizons. As already stated, the outstanding impact of fauna on the upper horizons of this upland grassland soil is in terms of digestion and organic and organo-mineral material to produce an abundance of excrement. Bal (1970) found similar results for moder-humus profiles and distinguished an upper H horizon formed by an accumulation of excrements and a lower H horizon consisting of ‘aged’ excrements. Ageing refers to gradual morphological changes in excrement arising from microbiological, physical and chemical processes with the ultimate collapse of soil aggregates consisting of excrement. Resistance to ageing can be provided by a ‘peritrophic membrane’ around excrement (Bal, 1970). The apparent durability of enchytraeid excrement as seen on the Sourhope slides may suggest a similar mechanism for their preservation. The generation of excrement is likely to be greatest in soils in the upper horizons where there is an abundance of organic matter. A soil formation question is, whether this excrement moves down-profile as a result of infiltration. Bal (1970) argues that the humus aggregates which occur between sand grains in an A1(2) horizon result from illuviation from upper organic horizons. The Ah horizon of the Sourhope soil consists of enchytraeid excrement (29%) surrounded by mineral fragments (24%). There is no micromorphological evidence to support the view that this material has been translocated from upper horizons, instead an in situ genesis is proposed. In a study on similar soils, and designed to investigate the translocation of soil pollen, Davidson et al. (1999) found evidence for movement by bioturbation processes rather than by water movement. The Hphy horizon seems unattractive to earthworms, though the presence of phytoliths seems to present
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little constraint to enchytraeids and to the animals who generated the undifferentiated forms of excrement. The formation of this horizon has been interpreted as a result of a particular concentration of phytoliths. An alternative possibility is that it is equivalent to an albic (E) horizon, but formed in organic matter. Jongerius and Pons (1962) describe soil formation (horizonation) in reclaimed peats in the Netherlands. They describe the process of illuviation of humic matter within the peat; this could result in a colour change from black (H horizon) to dark reddish grey to dark grey. In the process of peat ‘ripening,’ they ascribe key significance to the role of microarthropods, enchytraeids and various species of earthworms to soil development. The beginning of an E horizon within ca. 200 years accords with the papers on podzolisation, for example Bormann et al. (1995), who found that a welldeveloped E horizon formed in soils within 150 years. However, the micromorphological evidence suggests the concentration of phytoliths as the dominant reason for the formation of this horizon. As to be expected, the wetter areas are found mainly on the lower parts of the Sourhope experimental site where the thickness of the organic horizons (LF and H) is greater than on other parts of the site. It is in such localities that the Hphy horizon occurs. On average, the Hphy horizon has a lower void space than adjacent horizons and has fewer recognisable excremental pedofeatures. Where it occurs, the Hphy horizon is shallow (1.0–1.5 cm), albeit distinctive. In this horizon, vertical channels probably formed by earthworms, linking the upper H to the lower Ah horizon. In order to explain the distribution of phytoliths in Australian podzols, Hart and Humphreys (1997) proposed two hypotheses: (1) the static hypothesis, whereby a concentration of phytoliths results from an increase in deposition at some time in the past, and (2) the mobile hypothesis, whereby processes of bioturbation or shrink–swell cause the redistribution of phytoliths and their possible concentration in one horizon. Either of these hypotheses could apply at the Sourhope experimental site to explain the formation of the Hphy horizon. According to the first, the horizon may have formed simply by the concentration of grass phytoliths after abandonment of cultivation ca. 200 years ago, followed by the accumulation of a shallow peat, the H horizon. For the second, the net downward movement of phytoliths would have been greater than net upward
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redistribution by bioturbation, resulting in an enriched layer. Hart and Humphreys (1997) conclude by supporting this second hypothesis, though it should be noted that they were dealing with a thick and porous E horizon overlying a pan. The soil at Sourhope is analogous in that, the Hphy horizon, where it occurs, directly overlies the first organo-mineral horizon (Ah). It thus seems likely that the formation of this phytolith rich horizon is partially due to soil animals and then this horizon would have had an effect on further faunal activity.
5. Conclusions Overall, the micromorphological results as derived from an upland experimental site under acid grassland confirm the association between faunal activity and horizons. This is an interesting pedological outcome in that, the soil horizons are distinguished in the field on the basis of attributes such as colour and structure. Relationships between horizons and soil, physical and chemical properties are to be expected, but the results from these Sourhope slides also indicate that the soil horizons are also distinguished by having characteristic types of animal activity as expressed in the nature of excrement. The formation of horizons with distinctive physical, chemical and biological properties is a central concept in pedogenesis. These properties are necessarily interdependent and evolve as the soil develops. The identification of the cause and effect of relationships is particularly difficult in any type of ecosystem, but it may well be the case in upland organic rich soils, such that the formation of upper soil horizons is largely controlled by faunal activity rather than by the translocation of organic matter and iron and aluminium oxides.
Acknowledgements This work was funded by a grant (GST/02/2127) from the NERC Soil Biodiversity Programme. The authors also wish to acknowledge the technical assistance of George MacLeod who prepared the thin sections and Kate Howie who gave statistical advice.
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