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Life cycle of pollen grains in mormoder humus forms of young acid forest soils: a micromorphological approach
Catena 54 (2003) 651 – 663 www.elsevier.com/locate/catena
Life cycle of pollen grains in mormoder humus forms of young acid forest soils: a micromorphological approach J.M. Van Mourik * Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Nieuwe Achtergracht 166, NL-1066-WV Amsterdam, The Netherlands
Abstract Horizons of humus profiles contain pollen and spores. The palynological information of pollen spectra of terrestrial humus forms must be validated by micropedological knowledge of the processes of infiltration, incorporation, conservation, transport and decay of pollen grains in the soil system. This study presents the results of combined palynological and micromorphological analyses of two mormoder humus forms, sampled in the Forestry Gieten, The Netherlands. The aim of this study was to establish the distribution pattern and life cycle of pollen grains in mormoders. The first step of this cycle of pollen grains in the humus profile is eolian deposition on the soil surface. The second step is incorporation of the grains in organic aggregates in the upper part of the F horizon. In ‘acid’ mormoders, grains are embedded by ageing small excrements of micro-arthropods and incorporated in the resulting organic aggregates. In ‘mild’ mormoders, the same process is observable, but additional pollen grains are also directly incorporated (and slightly transported) in medium excrements of small earthworm. The third step in the cycle is release by microbial attack of the aggregates in the lower part of the F horizon and the H and Ah horizons. The fourth step is reincorporation of the released grains in organic aggregates of ageing small sized excrements of microarthropods, which consume decaying root tissue. Not re-incorporated grains will finally mineralise by microbial consumption. Mineralising of released pollen grains is the main process in the mineral AE horizon. Based on knowledge of the distribution pattern and life cycle of pollen grains in mormoders, pollen diagrams can be used for the reconstruction of the forest development. D 2003 Elsevier B.V. All rights reserved. Keywords: Micromorphology; Soil-palynology; Pollen-conservation; Humus-form; Forest-soil; The Netherlands
* Tel.: +31-205257451; fax: +31-205257431. E-mail address: [email protected] (J.M. Van Mourik). 0341-8162/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0341-8162(03)00116-4
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1. Introduction Soil pollen diagrams, as published in the standard studies of Havinga (1963) and Guillet (1971, 1972), showed that pollen spectra of humic horizons could be used to investigate the correlation between soil development and vegetation succession. But general acceptance of the validity of soil palynological data required additional knowledge of the processes of infiltration and conservation of pollen in various soil horizons. In studies of semi-terrestrial and aquatic deposits, pollen is considered to be part of the sediment. Anaerobic conditions in water-saturated deposits promote pollen conservation. This is not the case for pollen preserved in terrestrial soils. Aerobic conditions in well-drained soils result in microbial decay of unprotected pollen grains. Interpretation of soil pollen associations requires knowledge of the processes of incorporation, conservation and transport of pollen grains in soil. Micromorphology is an important technique to observe the presence and distribution of pollen grains in thin sections of various mineral soil horizons. Pollen grains precipitate on the surface and infiltrate into the soil. Preliminary research showed that the distribution of pollen in various mineral soil horizons is correlated with the retrogressive distribution of (paleo) soil fauna activity (Havinga, 1963; Van Mourik, 1986, 1999, 2001). Pollen infiltration and conservation starts in ectorganic horizon of the humus form. Pollen diagrams of humus profiles show both pollen zonation and a specific pollen density distribution (Dijkstra and Van Mourik, 1995, 1996). Validation of the palynological data of humus forms requires additional knowledge of the presence and distribution of pollen grains in the organic soil horizons. In general, traditional micromorphological descriptions of humus forms did not pay much attention to the presence of pollen grains (Bal, 1973; Babel, 1985). The main objective of the present study was to understand the life cycle of a pollen grain in a humus profile from the moment of deposition to the final decay. Two mormoder humus forms in the Forestry Gieten in The Netherlands (Fig. 1) were selected for combined palynological and micromorphological analysis. These profiles are
Fig. 1. Location of the forestry Gieten in The Netherlands.
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the result of 70 years forest soil development under planted Larix and Fagus trees. Most of the Dutch forests are younger than 100 years. Especially in the Pleistocene coversand district, much reforestation occurred on the former heath after the traditional plaggen agriculture system was abandoned, due to the introduction of chemical fertilizers. After the First World War, the State decided to start a reforestation program for wood production. Pinus sylvestris plantations form the majority of the ‘new forests’ but in some forests also Pinus nigra, Larix kaempferi, Quercusrobur, Quercus rubra, Picea abies and Fagus sylvatica were used. Before planting, the former soil profile of the heath lands (in general carbic podzols) was deeply ploughed to prepare ‘fresh’ parent material for the forest development. The present forest soils can be described as ‘micropodzols’ with well-developed humus forms. According to the classification of Green et al. (1993), all the humus forms must be classified as mormoders. Field observations, sustained by micromorphological analyses, show a soil ecological gradient from ‘mild’ mormoders under Fagus and Quercus toward ‘acid’ mormoders under Picea and Larix.
2. Palynological observations Since the reforestation around 1930 AD, the development of the forest soil is still restricted to the first decimetre of the total soil profile. This 10 cm section was sampled for the preparation of thin sections and pollen slides. The pollen extractions were based on the KOH Z H Z Acetolysis method and an exotic marker was added for the estimation of pollen densities (Moore et al., 1991). The observed pollen zonation and pollen density distribution of the selected mormoders confirms the results of preliminary investigations (Dijkstra and Van Mourik, 1995, 1996). The diagram information is useful for the interpretation of the micropedological features. Therefore the diagrams will be briefly discussed before the micromorphological observations will be presented. 2.1. Pollen diagram mormoder profile under Larix The forest soil profile under Larix is an example of an ‘acid’ mormoder, showing the sequence of the following horizons: L – F –(H) – AE (Fig. 2). The L (Litter) horizon is very thin and consists of scattered fresh needles. The F (Fermentation) horizon is loose and consists of litter fragments and fine excremental matter without a clearly developed structure. The distinction between the F1 (loose, coarse fragmented litter) and F2 (dense, matted, fine fragmented litter) is also based on a sudden increase of living roots. The brown black H (Humus) horizon is clearly but discontinuously developed. It consists of fine organic material with a very fine granular structure. In the AE horizon structures are lacking and the concentration of leached mineral grains increases. The pollen diagram reflects the transition from the former heath to the present Larix forest. The Ericaceae – Poaceae association of the mineral horizons reflect the former heath. The Ectorganic part of the humus form shows a pollen stratification that reflects three phases in the forest development. The pioneer phase is represented by the temporal increase of Betula. The first succession phase is reflected in the increase of Larix and other
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Fig. 2. Pollen diagram Larix.
planted trees in the surrounding. The second succession phase is represented by a slight decrease of Larix and an increase of Poaceae. The pollen density distribution shows maximal values in the lower part of the F2 and the H horizons. This is caused by relative increase of the resistant pollen grains in the organic residue during litter decomposition. The pollen concentrations decrease sharply in the mineral horizons. The pollen content of the AE and 2ABp horizons is mainly a relict of the former heath. The pollen density in this zone is low. It must be taken into account that this part of the profile has been disturbed by ploughing during the preparation of the heath soil before forest plantation. The stratification and density distribution of the pollen profile point to a very low rate of vertical bioactivity in this ‘acid’ mormoder humus form. 2.2. Pollen diagram mormoder profile under Fagus The forest soil profile under Fagus is an example of a ‘mild’ mormoder, showing the sequence of the following horizons: L –F – H –Ah –AE (Fig. 3). The F horizon is loose and consists of litter fragments and excremental material with a crumbled structure. The distinction between the F1 and F2 is based on the gradual increase of living roots. The black H and Ah horizons are well developed. The H consists of fine organic material with a medium fine crumb structure. The organic matter in the Ah equals the H. The Ah shows a fine to medium fine crumb structure. In the AE this structure is absent and the concentration of leached mineral grains increases. The pollen diagram reflects the transition from the former heath to the present Fagus forest. The Alnus – Ericaceae –Poaceae association of the mineral horizons reflects the former heath. The proximity of the brook valley and associated hedges and wetlands
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Fig. 3. Pollen diagram Fagus.
explains the relatively high percentages of Alnus and Poaceae, due to distance transport of pollen. Also in this diagram the ectorganic part of the humus form reflects the three phases in forest development. Due to a lower pollen production rate, the contribution of Fagus to the total pollen influx is restricted (Moore et al., 1991). This results in rather low percentages of this tree species in its forest soil associations. In comparison with the Larix profile, the transitions between the pollen zones are gradual. The pollen density distribution shows maximum concentrations in the H horizon. In comparison with the Larix profile the increase of concentrations with depth in the ectorganic horizons and the decrease in the mineral horizons are more gradual. The gradual stratification and density distribution of this pollen profile indicate a higher rate of vertical bio-activity in this ‘mild’ mormoder humus form.
3. Micromorphological observations Bal (1970) published the first detailed description of the micromorphology of moder humus. The role of soil fauna was the main subject in this investigation. Input and distribution of pollen grains in the humus form remained outside the scope of this study. The inventory of pollen grains in thin sections requires a magnification factor of at least 250 – 500. An additional problem is the state of the grains in thin sections. Pollen grains belong to the coarse silt fraction. Most of them have been cut during the preparation of the thin section and fine material covers the natural pollen wall. Palynological features as sculpture and aperture are invisible because the pollen wall is not cleaned (as during the pollen extraction method) and polluted by fine material (Van Mourik, 1999).
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The input of organic matter in the forest soil system is mainly controlled by eolian deposition of organic litter (including pollen grains) on the soil surface and decaying roots in the soil profile. Litter and roots form the basic food for various soil biota, living in various horizons of the humus form. Microbial synthesized polysaccharides also contribute to food storage, and are available for decomposition by soil fauna (Dijkstra et al., 1998). The chemical quality of litter controls the composition of soil biota, involved in the decomposition of organic matter (Coleman and Crossley, 1996). Litter with a low ( < 20) C/ N ratio promotes earthworm activity, resulting in the development of mull humus forms. Increase in the C/N ratio is a limiting factor for earthworm activity but stimulates arthropods and soil fungi, resulting in the development of moder and even mor humus forms. The pollen influx of a terrestrial soil system is part of the eolian litter deposit on the actual soil surface. Continuous litter accumulation, decomposition and pollen conservation, controlled by fungi and soil fauna, must be responsible for the development of pollen zonation in ectorganic horizons. In the field study of ectorganic layers hyphae of fungi could hardly be observed, but the pollen extractions show high concentration of hyphae fragments and fungus spores (Fig. 4). This indicates a systematic underestimation of fungal activity in the ectorganic layers and of the role of fungi in the decomposition process. Samples of the endorganic mineral horizons also contain pollen grains. The Pleistocene sandy sediments were originally free of pollen. Holocene pollen infiltration from the land surface into the endorganic mineral horizons is controlled by soil fauna activity (Van Mourik, 1999, 2001). Validation of pollen zonation of humus forms requires evidence of the processes, responsible for incorporation, preservation, transport and decay of pollen and spores in the various soil horizons. It is shown here that these processes can be explained with the assistance of micromorphological observations. 3.1. Profile Larix In the upper part of the F1 horizon, free pollen grains occur between litter fragments (Fig. 5). Fresh litter is affected by microbial activity. Soil fungi are responsible for the
Fig. 4. Pollen grains and fungal remains in a pollen slide of a sample of the F1-horizon of profile Larix, ppl.
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Fig. 5. Decayed pollen grains (by microbial consumption) in a pollen slide of a sample of the AE-horizon of profile Larix, ppl.
decomposition of the epidermis of the needles (Fig. 6). Fungal attack is followed by the consumption of the content of needles by soil fauna. Micro-arthropods and enchytraeidae are involved in this phase of decomposition of litter in acid, well-drained forest soils with a high (>25) C/N ratio (Wallwork, 1976). They consume soft litter tissue but also the fresh biomass, produced by the soil fungi (Coleman and Crossley, 1996). Most of the excrements are dropped inside or just outside the space of the consumed leaf tissue. They are small (F 50– 100 Am) and consist of small black organic particles and black brown organic plasma (Fig. 7). Pollen is not present in such excrements because these small soil animals cannot consume such big grains (Davidson et al., 1999). Initially, litter fragments dominate the soil matrix of the F1. As a result of the decomposition, the macro porosity of the matrix decreases and voids are filled with ageing excrements, embedding original free pollen grains. This process results in pollen containing organic aggregates. The micro-environment in these aggregates offers the embedded pollen grains a perfect protection against microbial decay (Fig. 8). This process is recently confirmed in a study of Davidson et al. (1999) to explain the pollen distribution in acid soils in the United Kingdom.
Fig. 6. Free pollen grain in fresh litter in the F1-horizon, thin section Larix, ppl.
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Fig. 7. Free pollen grain on a litter fragment, attacked by fungi in the F1-horizon, thin section Fagus, ppl.
The soil matrix of the F2 horizon is composed of fragmented litter particles and organic aggregates. The matrix of the H horizon is dominated by organic aggregates. This part of the ectorganic profile is characterized by a high root density and by fungal attack of organic aggregates. The decomposition of the aggregates is not only responsible for the release of nutrients but also of the incorporated pollen grains (Figs. 9 and 10), which are again exposed to possible decay. There is no evidence of consumption of the content of the decomposing aggregates by soil fauna. However, the biomass of the fungi together with decaying root tissue is consumed by the same micro-arthropods and enchytraeidae as in the F1 horizon. This results in the supply of fresh small sized excrements (Fig. 11). Previously released pollen are re-embedded by fine organic matter and finally re-incorporated and conserved in secondary aggregates, composed by ageing excremental particles. Sand grains dominate the soil matrix of the endorganic AE horizon. Black organic aggregates are randomly distributed in the voids. The density of fresh and decaying roots is low. Most of the organic aggregates look stable, a few are attacked by soil fungi. It is
Fig. 8. Small excrements produced by the consumption of decayed leaf tissue in the F1-horizon, thin section Larix, ppl.
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Fig. 9. Pollen grain, incorporated in an organic aggregate in the F2-horizon, thin section Fagus, ppl.
important to realize that most of these aggregates are inherited from the former heath soil system. Incidental released pollen grains from ageing aggregates are present. In thin sections it is impossible to observe features of decay of the pollen wall, due to the contamination of the grains. But after extraction, the grains are cleaned and the effects of decay can be observed in the pollen slides (Elsik, 1971). Many pollen grains show traces of mechanical damage. The process of embedding, incorporation, release, re-embedding and re-incorporation promotes this type of damage. Some grains show also traces of microbiological damage. The final process of decay is mineralization of the pollen wall by bacterial consumption (Fig. 12). The mineralization rate of various pollen types is different and the composition of pollen spectra in soil horizons with released grains can be affected by selective corrosion (Havinga, 1984). The rate of degradation of organic aggregates in acid mineral soil horizons is low and soil pollen can survive in the protecting microenvironment of organic aggregates for thousands of years (Van Mourik, 1986, 1999).
Fig. 10. Fungal attack of an organic aggregate in the H-horizon, thin section Larix, ppl.
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Fig. 11. Release of pollen grains in the H-horizon, thin section Larix, ppl.
3.2. Profile Fagus As in the profile Larix, the decomposition of fresh litter (including pollen grains) starts in the top of the F1 horizon with fungal attack. Micro-arthropods and enchytraeidae consume leaf tissue and produce small sized excrements. Pollen is incorporated in aggregates, composed by ageing excrements. In contrast to the ‘acid’ mormoder, small (F 50 – 100 Am) and medium (F 100– 300 Am) excrements occur in the ‘mild’ mormoder in the ectorganic and Ah horizons (Fig. 13). The medium excrements are produced by small, pigmented earthworms (Lumbricus festivus) living in weak acid, well drained soil systems with a moderate (20 –25) C/N ratio (Wallwork, 1976). These earthworms consume the relatively nitrogen rich excrements of the arthropods. The medium sized excrements, present in the F1 and F2
Fig. 12. Production of small sized excrements by consumption of decaying root tissue in the F2-horizon, thin section Fagus, ppl.
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Fig. 13. Medium sized excrements with some silt particles in the H-horizon, thin section Fagus, ppl.
horizons, are composed of black organic particles and brown organic plasma. In the H and Ah horizons these excrements contain few mineral silt grains. This points to limited vertical movement of these soil animals in the humus profile. Pollen is part of the consumed food but the grains cannot be digested and are directly incorporated in their excrements. The acid and anaerobic micro-environment inside the excrements offers a perfect preservation for pollen grains. The vertical transport of pollen in the soil profile correlates with the depth of burring activity of these worms. The restriction of the vertical movement of these earthworms and the mixing of soil material is reflected by the observed gradual zonation of the pollen diagram. More vertical transport may result in palynological homogenisation. Similar to the small sized excrements of the micro-arthropods, the medium sized excrements of the earthworms show features of ageing and cluster into organic aggregates that will be subjected to fungal attack. In the F2, H and Ah horizons, fresh organic litter is supplied in the form of decaying roots. In mormoders these roots are ‘in situ’ consumed by micro-arthropods, producing fresh small sized ‘secondary’ faecal pallets. In this section of the profile, released pollen grains can be re-embedded by fine organic excremental material and re-incorporated in secondary aggregates. If a released grain will not be re-incorporated, it will finally be mineralised by microbial consumption. Medium sized excrements are not present in the AE horizon. The activity of small sized earthworms avoids this section of the profile. As in profile Larix, the organic matter in this horizon is an inheritance of the heath soil system.
4. Conclusions In thin sections of moder humus forms, free pollen grains can only be observed in the L and the upper part of F1 horizons. Further, the distribution of pollen in the humus form is controlled by the development and degradation of organic aggregates, incorporating and
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protecting pollen grains. The life cycle of a pollen grain in a mormoder profile can be summarized by the following steps:
The influx of pollen in a terrestrial soil system is part of the eolian organic litter deposit on the soil surface. In the upper part of the F1 horizon, free pollen grains are present between relative fresh litter fragments. In the F1 horizon of ‘acid’ mormoders, ageing small excrements embed pollen grains and incorporate them into organic aggregates. The small sized excrements are produced by micro-arthropods and enchytraeidae. These humus inhabiting soil animals consume decayed leaf tissue and soil fungi. In the F horizon of ‘mild’ mormoders, pollen grains are also directly incorporated into medium excrements of small earthworms. In the next phase, soil fungi attack organic aggregates. This results in the release of incorporated pollen grains. In the F2 and H micro-arthropods produce small sized excrements in this section of the profile and previously released pollen from primary aggregates can be re-embedded by small ageing excrements and re-incorporated in secondary organic aggregates. Not re-incorporated released pollen grains will mineralise, due to microbial consumption. The micromorphological features contribute to the explanation of the observed pollen zonation and pollen density distribution of the analysed mormoders and validate the use of pollen spectra of humus forms for palynological – ecological reconstructions.
References Bal, L., 1970. Morphological investigation in two moder-humus profiles and the role of soil fauna in their genesis. Geoderma 4, 5 – 36. Bal, L., 1973. Micrmorphological analysis of soils. Lower levels in the organization of organic soil materials. Soil Survey Papers, vol. 6. Netherlands Soil Survey Institute, Wageningen. Babel, U., 1985. Basic organic components. In: Bullock, P., Federoff, N., Jongerius, A., Stoops, G., Tursina, T. (Eds.), Handbook for Soil Thin Section Description. Waine Research Publications, England, pp. 74 – 87. Coleman, D.C., Crossley, D.A., 1996. Fundamentals of Soil Ecology. Academic Press, London/New York. 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 Biology and Biochemistry 31, 643 – 653. Dijkstra, E.F., Van Mourik, J.M., 1995. Palynology of young acid forest soils in the Netherlands. Mededelingen Rijks Geologische Dienst 52, 283 – 296. Dijkstra, E.F., Van Mourik, J.M., 1996. Reconstruction of forest dynamics based on pollen analysis and micromorphological studies of young acid forest soils under Scots pine plantations. Acta Bot. Neerl. 45, 393 – 410. Dijkstra, E.F., Boon, J.J., Van Mourik, J.M., 1998. Analytical pyrolysis of a soil profile under Scots pine. Eur. J. Soil Sci. 49, 295 – 304. Elsik, W.C., 1971. Microbiological degradation of sporopollenin. In: Brooks, J., Grant, P.R., Muir, R., Van Gijzel, P., Shaw, G. (Eds.), Sporopollenin. Academic Press, London, pp. 480 – 511. Green, R.N., Towbridge, R.L., Klinka, K., 1993. Towards a Taxonomic Classification of Humus Forms. Forest Science, Monograph 29 (49 pp.). Guillet, B., 1971. Etude palynologique des podzols I: La podzolisation sur alluvions ancienne en Loraine. Pollen Spores 12, 45 – 69.
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Guillet, B., 1972. Etude palynologique des podzols II: La podzolisation sur les versants secs gre´seux des Basses Vosges. Pollen Spores 13, 233 – 254. Havinga, A.J., 1963. A Palynological Investigation of Soil Profiles Developed in Cover Sand. Veenman, Wageningen. Havinga, A.J., 1984. A 20-year experimental investigation into the differential corrosion susceptibility of pollen and spores in various soil types. Pollen Spores 26, 541 – 558. Moore, P.D., Webb, J.A., Collinson, M.E., 1991. Pollen Analysis, 2nd ed. Blackwell, Oxford. Van Mourik, J.M., 1986. Pollen profiles of slope deposits in the Galician area (N.W. Spain). Netherlands Geographical Studies, vol. 12, p. 171. Amsterdam. Van Mourik, J.M., 1999. The use of micromorphology in soil pollen analysis. Catena 35, 239 – 257. Van Mourik, J.M., 2001. Pollen and spores, preservation in ecological settings. In: Briggs, E.G., Crowther, P.R. (Eds.), Palaeobiology II. Blackwell, Oxford, pp. 315 – 318. Wallwork, J.A., 1976. The Distribution and Diversity of Soil Fauna. Academic Press, London/New York.
Life cycle of pollen grains in mormoder humus forms of young acid forest soils: a micromorphological approach J.M. Van Mourik * Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Nieuwe Achtergracht 166, NL-1066-WV Amsterdam, The Netherlands
Abstract Horizons of humus profiles contain pollen and spores. The palynological information of pollen spectra of terrestrial humus forms must be validated by micropedological knowledge of the processes of infiltration, incorporation, conservation, transport and decay of pollen grains in the soil system. This study presents the results of combined palynological and micromorphological analyses of two mormoder humus forms, sampled in the Forestry Gieten, The Netherlands. The aim of this study was to establish the distribution pattern and life cycle of pollen grains in mormoders. The first step of this cycle of pollen grains in the humus profile is eolian deposition on the soil surface. The second step is incorporation of the grains in organic aggregates in the upper part of the F horizon. In ‘acid’ mormoders, grains are embedded by ageing small excrements of micro-arthropods and incorporated in the resulting organic aggregates. In ‘mild’ mormoders, the same process is observable, but additional pollen grains are also directly incorporated (and slightly transported) in medium excrements of small earthworm. The third step in the cycle is release by microbial attack of the aggregates in the lower part of the F horizon and the H and Ah horizons. The fourth step is reincorporation of the released grains in organic aggregates of ageing small sized excrements of microarthropods, which consume decaying root tissue. Not re-incorporated grains will finally mineralise by microbial consumption. Mineralising of released pollen grains is the main process in the mineral AE horizon. Based on knowledge of the distribution pattern and life cycle of pollen grains in mormoders, pollen diagrams can be used for the reconstruction of the forest development. D 2003 Elsevier B.V. All rights reserved. Keywords: Micromorphology; Soil-palynology; Pollen-conservation; Humus-form; Forest-soil; The Netherlands
* Tel.: +31-205257451; fax: +31-205257431. E-mail address: [email protected] (J.M. Van Mourik). 0341-8162/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0341-8162(03)00116-4
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J.M. Van Mourik / Catena 54 (2003) 651–663
1. Introduction Soil pollen diagrams, as published in the standard studies of Havinga (1963) and Guillet (1971, 1972), showed that pollen spectra of humic horizons could be used to investigate the correlation between soil development and vegetation succession. But general acceptance of the validity of soil palynological data required additional knowledge of the processes of infiltration and conservation of pollen in various soil horizons. In studies of semi-terrestrial and aquatic deposits, pollen is considered to be part of the sediment. Anaerobic conditions in water-saturated deposits promote pollen conservation. This is not the case for pollen preserved in terrestrial soils. Aerobic conditions in well-drained soils result in microbial decay of unprotected pollen grains. Interpretation of soil pollen associations requires knowledge of the processes of incorporation, conservation and transport of pollen grains in soil. Micromorphology is an important technique to observe the presence and distribution of pollen grains in thin sections of various mineral soil horizons. Pollen grains precipitate on the surface and infiltrate into the soil. Preliminary research showed that the distribution of pollen in various mineral soil horizons is correlated with the retrogressive distribution of (paleo) soil fauna activity (Havinga, 1963; Van Mourik, 1986, 1999, 2001). Pollen infiltration and conservation starts in ectorganic horizon of the humus form. Pollen diagrams of humus profiles show both pollen zonation and a specific pollen density distribution (Dijkstra and Van Mourik, 1995, 1996). Validation of the palynological data of humus forms requires additional knowledge of the presence and distribution of pollen grains in the organic soil horizons. In general, traditional micromorphological descriptions of humus forms did not pay much attention to the presence of pollen grains (Bal, 1973; Babel, 1985). The main objective of the present study was to understand the life cycle of a pollen grain in a humus profile from the moment of deposition to the final decay. Two mormoder humus forms in the Forestry Gieten in The Netherlands (Fig. 1) were selected for combined palynological and micromorphological analysis. These profiles are
Fig. 1. Location of the forestry Gieten in The Netherlands.
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the result of 70 years forest soil development under planted Larix and Fagus trees. Most of the Dutch forests are younger than 100 years. Especially in the Pleistocene coversand district, much reforestation occurred on the former heath after the traditional plaggen agriculture system was abandoned, due to the introduction of chemical fertilizers. After the First World War, the State decided to start a reforestation program for wood production. Pinus sylvestris plantations form the majority of the ‘new forests’ but in some forests also Pinus nigra, Larix kaempferi, Quercusrobur, Quercus rubra, Picea abies and Fagus sylvatica were used. Before planting, the former soil profile of the heath lands (in general carbic podzols) was deeply ploughed to prepare ‘fresh’ parent material for the forest development. The present forest soils can be described as ‘micropodzols’ with well-developed humus forms. According to the classification of Green et al. (1993), all the humus forms must be classified as mormoders. Field observations, sustained by micromorphological analyses, show a soil ecological gradient from ‘mild’ mormoders under Fagus and Quercus toward ‘acid’ mormoders under Picea and Larix.
2. Palynological observations Since the reforestation around 1930 AD, the development of the forest soil is still restricted to the first decimetre of the total soil profile. This 10 cm section was sampled for the preparation of thin sections and pollen slides. The pollen extractions were based on the KOH Z H Z Acetolysis method and an exotic marker was added for the estimation of pollen densities (Moore et al., 1991). The observed pollen zonation and pollen density distribution of the selected mormoders confirms the results of preliminary investigations (Dijkstra and Van Mourik, 1995, 1996). The diagram information is useful for the interpretation of the micropedological features. Therefore the diagrams will be briefly discussed before the micromorphological observations will be presented. 2.1. Pollen diagram mormoder profile under Larix The forest soil profile under Larix is an example of an ‘acid’ mormoder, showing the sequence of the following horizons: L – F –(H) – AE (Fig. 2). The L (Litter) horizon is very thin and consists of scattered fresh needles. The F (Fermentation) horizon is loose and consists of litter fragments and fine excremental matter without a clearly developed structure. The distinction between the F1 (loose, coarse fragmented litter) and F2 (dense, matted, fine fragmented litter) is also based on a sudden increase of living roots. The brown black H (Humus) horizon is clearly but discontinuously developed. It consists of fine organic material with a very fine granular structure. In the AE horizon structures are lacking and the concentration of leached mineral grains increases. The pollen diagram reflects the transition from the former heath to the present Larix forest. The Ericaceae – Poaceae association of the mineral horizons reflect the former heath. The Ectorganic part of the humus form shows a pollen stratification that reflects three phases in the forest development. The pioneer phase is represented by the temporal increase of Betula. The first succession phase is reflected in the increase of Larix and other
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Fig. 2. Pollen diagram Larix.
planted trees in the surrounding. The second succession phase is represented by a slight decrease of Larix and an increase of Poaceae. The pollen density distribution shows maximal values in the lower part of the F2 and the H horizons. This is caused by relative increase of the resistant pollen grains in the organic residue during litter decomposition. The pollen concentrations decrease sharply in the mineral horizons. The pollen content of the AE and 2ABp horizons is mainly a relict of the former heath. The pollen density in this zone is low. It must be taken into account that this part of the profile has been disturbed by ploughing during the preparation of the heath soil before forest plantation. The stratification and density distribution of the pollen profile point to a very low rate of vertical bioactivity in this ‘acid’ mormoder humus form. 2.2. Pollen diagram mormoder profile under Fagus The forest soil profile under Fagus is an example of a ‘mild’ mormoder, showing the sequence of the following horizons: L –F – H –Ah –AE (Fig. 3). The F horizon is loose and consists of litter fragments and excremental material with a crumbled structure. The distinction between the F1 and F2 is based on the gradual increase of living roots. The black H and Ah horizons are well developed. The H consists of fine organic material with a medium fine crumb structure. The organic matter in the Ah equals the H. The Ah shows a fine to medium fine crumb structure. In the AE this structure is absent and the concentration of leached mineral grains increases. The pollen diagram reflects the transition from the former heath to the present Fagus forest. The Alnus – Ericaceae –Poaceae association of the mineral horizons reflects the former heath. The proximity of the brook valley and associated hedges and wetlands
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Fig. 3. Pollen diagram Fagus.
explains the relatively high percentages of Alnus and Poaceae, due to distance transport of pollen. Also in this diagram the ectorganic part of the humus form reflects the three phases in forest development. Due to a lower pollen production rate, the contribution of Fagus to the total pollen influx is restricted (Moore et al., 1991). This results in rather low percentages of this tree species in its forest soil associations. In comparison with the Larix profile, the transitions between the pollen zones are gradual. The pollen density distribution shows maximum concentrations in the H horizon. In comparison with the Larix profile the increase of concentrations with depth in the ectorganic horizons and the decrease in the mineral horizons are more gradual. The gradual stratification and density distribution of this pollen profile indicate a higher rate of vertical bio-activity in this ‘mild’ mormoder humus form.
3. Micromorphological observations Bal (1970) published the first detailed description of the micromorphology of moder humus. The role of soil fauna was the main subject in this investigation. Input and distribution of pollen grains in the humus form remained outside the scope of this study. The inventory of pollen grains in thin sections requires a magnification factor of at least 250 – 500. An additional problem is the state of the grains in thin sections. Pollen grains belong to the coarse silt fraction. Most of them have been cut during the preparation of the thin section and fine material covers the natural pollen wall. Palynological features as sculpture and aperture are invisible because the pollen wall is not cleaned (as during the pollen extraction method) and polluted by fine material (Van Mourik, 1999).
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The input of organic matter in the forest soil system is mainly controlled by eolian deposition of organic litter (including pollen grains) on the soil surface and decaying roots in the soil profile. Litter and roots form the basic food for various soil biota, living in various horizons of the humus form. Microbial synthesized polysaccharides also contribute to food storage, and are available for decomposition by soil fauna (Dijkstra et al., 1998). The chemical quality of litter controls the composition of soil biota, involved in the decomposition of organic matter (Coleman and Crossley, 1996). Litter with a low ( < 20) C/ N ratio promotes earthworm activity, resulting in the development of mull humus forms. Increase in the C/N ratio is a limiting factor for earthworm activity but stimulates arthropods and soil fungi, resulting in the development of moder and even mor humus forms. The pollen influx of a terrestrial soil system is part of the eolian litter deposit on the actual soil surface. Continuous litter accumulation, decomposition and pollen conservation, controlled by fungi and soil fauna, must be responsible for the development of pollen zonation in ectorganic horizons. In the field study of ectorganic layers hyphae of fungi could hardly be observed, but the pollen extractions show high concentration of hyphae fragments and fungus spores (Fig. 4). This indicates a systematic underestimation of fungal activity in the ectorganic layers and of the role of fungi in the decomposition process. Samples of the endorganic mineral horizons also contain pollen grains. The Pleistocene sandy sediments were originally free of pollen. Holocene pollen infiltration from the land surface into the endorganic mineral horizons is controlled by soil fauna activity (Van Mourik, 1999, 2001). Validation of pollen zonation of humus forms requires evidence of the processes, responsible for incorporation, preservation, transport and decay of pollen and spores in the various soil horizons. It is shown here that these processes can be explained with the assistance of micromorphological observations. 3.1. Profile Larix In the upper part of the F1 horizon, free pollen grains occur between litter fragments (Fig. 5). Fresh litter is affected by microbial activity. Soil fungi are responsible for the
Fig. 4. Pollen grains and fungal remains in a pollen slide of a sample of the F1-horizon of profile Larix, ppl.
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Fig. 5. Decayed pollen grains (by microbial consumption) in a pollen slide of a sample of the AE-horizon of profile Larix, ppl.
decomposition of the epidermis of the needles (Fig. 6). Fungal attack is followed by the consumption of the content of needles by soil fauna. Micro-arthropods and enchytraeidae are involved in this phase of decomposition of litter in acid, well-drained forest soils with a high (>25) C/N ratio (Wallwork, 1976). They consume soft litter tissue but also the fresh biomass, produced by the soil fungi (Coleman and Crossley, 1996). Most of the excrements are dropped inside or just outside the space of the consumed leaf tissue. They are small (F 50– 100 Am) and consist of small black organic particles and black brown organic plasma (Fig. 7). Pollen is not present in such excrements because these small soil animals cannot consume such big grains (Davidson et al., 1999). Initially, litter fragments dominate the soil matrix of the F1. As a result of the decomposition, the macro porosity of the matrix decreases and voids are filled with ageing excrements, embedding original free pollen grains. This process results in pollen containing organic aggregates. The micro-environment in these aggregates offers the embedded pollen grains a perfect protection against microbial decay (Fig. 8). This process is recently confirmed in a study of Davidson et al. (1999) to explain the pollen distribution in acid soils in the United Kingdom.
Fig. 6. Free pollen grain in fresh litter in the F1-horizon, thin section Larix, ppl.
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Fig. 7. Free pollen grain on a litter fragment, attacked by fungi in the F1-horizon, thin section Fagus, ppl.
The soil matrix of the F2 horizon is composed of fragmented litter particles and organic aggregates. The matrix of the H horizon is dominated by organic aggregates. This part of the ectorganic profile is characterized by a high root density and by fungal attack of organic aggregates. The decomposition of the aggregates is not only responsible for the release of nutrients but also of the incorporated pollen grains (Figs. 9 and 10), which are again exposed to possible decay. There is no evidence of consumption of the content of the decomposing aggregates by soil fauna. However, the biomass of the fungi together with decaying root tissue is consumed by the same micro-arthropods and enchytraeidae as in the F1 horizon. This results in the supply of fresh small sized excrements (Fig. 11). Previously released pollen are re-embedded by fine organic matter and finally re-incorporated and conserved in secondary aggregates, composed by ageing excremental particles. Sand grains dominate the soil matrix of the endorganic AE horizon. Black organic aggregates are randomly distributed in the voids. The density of fresh and decaying roots is low. Most of the organic aggregates look stable, a few are attacked by soil fungi. It is
Fig. 8. Small excrements produced by the consumption of decayed leaf tissue in the F1-horizon, thin section Larix, ppl.
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Fig. 9. Pollen grain, incorporated in an organic aggregate in the F2-horizon, thin section Fagus, ppl.
important to realize that most of these aggregates are inherited from the former heath soil system. Incidental released pollen grains from ageing aggregates are present. In thin sections it is impossible to observe features of decay of the pollen wall, due to the contamination of the grains. But after extraction, the grains are cleaned and the effects of decay can be observed in the pollen slides (Elsik, 1971). Many pollen grains show traces of mechanical damage. The process of embedding, incorporation, release, re-embedding and re-incorporation promotes this type of damage. Some grains show also traces of microbiological damage. The final process of decay is mineralization of the pollen wall by bacterial consumption (Fig. 12). The mineralization rate of various pollen types is different and the composition of pollen spectra in soil horizons with released grains can be affected by selective corrosion (Havinga, 1984). The rate of degradation of organic aggregates in acid mineral soil horizons is low and soil pollen can survive in the protecting microenvironment of organic aggregates for thousands of years (Van Mourik, 1986, 1999).
Fig. 10. Fungal attack of an organic aggregate in the H-horizon, thin section Larix, ppl.
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Fig. 11. Release of pollen grains in the H-horizon, thin section Larix, ppl.
3.2. Profile Fagus As in the profile Larix, the decomposition of fresh litter (including pollen grains) starts in the top of the F1 horizon with fungal attack. Micro-arthropods and enchytraeidae consume leaf tissue and produce small sized excrements. Pollen is incorporated in aggregates, composed by ageing excrements. In contrast to the ‘acid’ mormoder, small (F 50 – 100 Am) and medium (F 100– 300 Am) excrements occur in the ‘mild’ mormoder in the ectorganic and Ah horizons (Fig. 13). The medium excrements are produced by small, pigmented earthworms (Lumbricus festivus) living in weak acid, well drained soil systems with a moderate (20 –25) C/N ratio (Wallwork, 1976). These earthworms consume the relatively nitrogen rich excrements of the arthropods. The medium sized excrements, present in the F1 and F2
Fig. 12. Production of small sized excrements by consumption of decaying root tissue in the F2-horizon, thin section Fagus, ppl.
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Fig. 13. Medium sized excrements with some silt particles in the H-horizon, thin section Fagus, ppl.
horizons, are composed of black organic particles and brown organic plasma. In the H and Ah horizons these excrements contain few mineral silt grains. This points to limited vertical movement of these soil animals in the humus profile. Pollen is part of the consumed food but the grains cannot be digested and are directly incorporated in their excrements. The acid and anaerobic micro-environment inside the excrements offers a perfect preservation for pollen grains. The vertical transport of pollen in the soil profile correlates with the depth of burring activity of these worms. The restriction of the vertical movement of these earthworms and the mixing of soil material is reflected by the observed gradual zonation of the pollen diagram. More vertical transport may result in palynological homogenisation. Similar to the small sized excrements of the micro-arthropods, the medium sized excrements of the earthworms show features of ageing and cluster into organic aggregates that will be subjected to fungal attack. In the F2, H and Ah horizons, fresh organic litter is supplied in the form of decaying roots. In mormoders these roots are ‘in situ’ consumed by micro-arthropods, producing fresh small sized ‘secondary’ faecal pallets. In this section of the profile, released pollen grains can be re-embedded by fine organic excremental material and re-incorporated in secondary aggregates. If a released grain will not be re-incorporated, it will finally be mineralised by microbial consumption. Medium sized excrements are not present in the AE horizon. The activity of small sized earthworms avoids this section of the profile. As in profile Larix, the organic matter in this horizon is an inheritance of the heath soil system.
4. Conclusions In thin sections of moder humus forms, free pollen grains can only be observed in the L and the upper part of F1 horizons. Further, the distribution of pollen in the humus form is controlled by the development and degradation of organic aggregates, incorporating and
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protecting pollen grains. The life cycle of a pollen grain in a mormoder profile can be summarized by the following steps:
The influx of pollen in a terrestrial soil system is part of the eolian organic litter deposit on the soil surface. In the upper part of the F1 horizon, free pollen grains are present between relative fresh litter fragments. In the F1 horizon of ‘acid’ mormoders, ageing small excrements embed pollen grains and incorporate them into organic aggregates. The small sized excrements are produced by micro-arthropods and enchytraeidae. These humus inhabiting soil animals consume decayed leaf tissue and soil fungi. In the F horizon of ‘mild’ mormoders, pollen grains are also directly incorporated into medium excrements of small earthworms. In the next phase, soil fungi attack organic aggregates. This results in the release of incorporated pollen grains. In the F2 and H micro-arthropods produce small sized excrements in this section of the profile and previously released pollen from primary aggregates can be re-embedded by small ageing excrements and re-incorporated in secondary organic aggregates. Not re-incorporated released pollen grains will mineralise, due to microbial consumption. The micromorphological features contribute to the explanation of the observed pollen zonation and pollen density distribution of the analysed mormoders and validate the use of pollen spectra of humus forms for palynological – ecological reconstructions.
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