Structural relationships among vegetation, soil fauna and humus form in a subalpine forest ecosystem: a Hierarchical Multiple Factor Analysis (HMFA)

Aboveground vegetation, four belowground fauna groups and humus composition have been analyzed in order to investigate the links between autotrophic and heterotrophic communities in a Norway-spruce mountain forest in Tours-en-Savoie (France). The aboveground plant community was recorded in small patches corresponding to contrasting microhabitats. Animal communities and humus layers were sampled within the same patches. The relationships between humus profile, faunistic and floristic compositional gradients were investigated by Multiple Factor Analysis (MFA) and, for the first time in ecology, a Hierarchical Multiple Factor Analysis (HMFA) was used to interpret differences among humus layers. The analysis revealed a pattern with three main groups of microhabitats. The thorough study of separate humus layers could explain this result. The interplay of plant-animal-soil interactions is likely to drive the ecosystem toward three alternative states supporting humus traditional classification between mull-mor-moder. HMFA revealed the importance of depth to explain this contrast among humus forms, using humus layers as diagnostic tools in both inert and living components. HMFA also showed contrast between unexploited and exploited parts of the forest, but the study of soil and vegetation indicate that this contrast does not only hold in forest management but also in geomorphology. RV-coefficients among the six groups of variables showed significant fauna-fauna relationships in almost all humus layers except Actinedida. Plant-soil interactions are not as strong as expected and are even weaker when the soil in question is deep. In addition, HMFA failed to show direct interactions between plant and soil fauna but, paradoxically, HMFA does suggest that indirect plant-fauna interactions are at the focus of the ecosystem strategy that leads to the differentiation of ecological niches within the forest mosaic.

[1]  J. Laganière,et al.  Linking the abundance of aspen with soil faunal communities and rates of belowground processes within single stands of mixed aspen-black spruce , 2009 .

[2]  Jean-François Ponge Humus forms in terrestrial ecosystems: a framework to biodiversity , 2003 .

[3]  Jean-François Ponge,et al.  The heterogeneity of humus profiles and earthworm communities in a virgin beech forest , 1995, Biology and Fertility of Soils.

[4]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[5]  L. E. Lowe,et al.  Taxonomic Classification of Humus Forms in Ecosystems of British Columbia. First Approximation. , 1982 .

[6]  Jean Thioulouse,et al.  CO‐INERTIA ANALYSIS AND THE LINKING OF ECOLOGICAL DATA TABLES , 2003 .

[7]  C. Körner,et al.  Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems , 2000, Plant and Soil.

[8]  M. Bradford,et al.  Linkages between below and aboveground communities: Decomposer responses to simulated tree species loss are largely additive , 2009 .

[9]  P. Lebrun,et al.  Are there real endogeic species in temperate forest mites , 2004 .

[10]  A. Buttler,et al.  Plant species richness and environmental heterogeneity in a mountain landscape: effects of variability and spatial configuration , 2006 .

[11]  D. Coleman,et al.  Litter complexity and composition are determinants of the diversity and species composition of oribatid mites (Acari: Oribatida) in litterbags , 1998 .

[12]  E. Doblas-Miranda,et al.  Different microhabitats affect soil macroinvertebrate assemblages in a Mediterranean arid ecosystem , 2009 .

[13]  M. Loreau Are communities saturated? On the relationship between α, β and γ diversity , 2000 .

[14]  Guillaume Boudin,et al.  Earthworm distribution and humus forms in the development of a semi-natural alpine spruce forest , 1999 .

[15]  R. Bardgett,et al.  Functional aspects of soil animal diversity in agricultural grasslands , 1998 .

[16]  P. Robert,et al.  A Unifying Tool for Linear Multivariate Statistical Methods: The RV‐Coefficient , 1976 .

[17]  H. Appel Phenolics in ecological interactions: The importance of oxidation , 1993, Journal of Chemical Ecology.

[18]  S. Hobbie Interactions between Litter Lignin and Nitrogenitter Lignin and Soil Nitrogen Availability during Leaf Litter Decomposition in a Hawaiian Montane Forest , 2000, Ecosystems.

[19]  H. W. Hunt,et al.  Relationships at the aboveground-belowground interface: plants, soil biota and soil processes , 2003 .

[20]  S. Scheu,et al.  Feeding biology of oribatid mites : a minireview , 2004 .

[21]  R. Edmonds,et al.  Soil arthropod responses to different patch types in a mixed-conifer forest of the Sierra Nevada , 2005 .

[22]  Sébastien Lê,et al.  FactoMineR: An R Package for Multivariate Analysis , 2008 .

[23]  Jean-François Ponge Etude écologique d'un humus forestier par l'observation d'un petit volume, premiers résultats. I: La couche L1 d'un moder sous pin sylvestre , 1984 .

[24]  D. Coleman,et al.  A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling , 1995, Plant and Soil.

[25]  Thomas P. Clausen,et al.  Effects of balsam poplar (Populus balsamifera) tannins and low molecular weight phenolics on microbial activity in taiga floodplain soil: implications for changes in N cycling during succession , 1996 .

[26]  D. Tilman,et al.  Dynamics of plant and arthropod diversity during old field succession , 1999 .

[27]  R. Aerts Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems : a triangular relationship , 1997 .

[28]  Jean-François Ponge,et al.  Humus form dynamics during the sylvogenetic cycle in a mountain spruce forest , 1994 .

[29]  J. P. Grime,et al.  Benefits of plant diversity to ecosystems: immediate, filter and founder effects , 1998 .

[30]  V. Russo Bed Orientation and Position in Field Inconsistently Affect Yields of Strip-Cropped Vegetables , 2001 .

[31]  J. Pagès,et al.  Analyse factorielle multiple hiérarchique , 2003 .

[32]  W. Handley Mull and mor formation in relation to forest soils , 1955 .

[33]  S. N,et al.  Climatic effects on soil trophic networks and the resulting humus profiles in holm oak ( Quercus rotundifolia ) forests in the High Atlas of Morocco as revealed by correspondence analysis , 2010 .

[34]  Gerhard Zachariae Spuren Tierischer Tätigkeit im Boden des Buchenwaldes , 1965 .

[35]  Michael A. Huston,et al.  Local processes and regional patterns : appropriate scales for understanding variation in the diversity of plants and animals , 1999 .

[36]  Jérôme Pagès,et al.  Multiple factor analysis (AFMULT package) , 1994 .

[37]  François Gillet,et al.  Integrated synusial phytosociology: some notes on a new, multiscalar approach to vegetation analysis , 1996 .

[38]  Charles C. Schwartz,et al.  Role of Tannins in Defending Plants Against Ruminants: Reduction in Protein Availability , 1987 .

[39]  N. Bernier Altitudinal changes in humus form dynamics in a spruce forest at the montane level , 2004, Plant and Soil.

[40]  Nicolas Bernier,et al.  The Forest Regeneration Puzzle Biological mechanisms in humus layer and forest vegetation dynamics , 1998 .

[41]  A. Ernoult,et al.  Variability and heterogeneity of humus forms at stand level: Comparison between pure beech and mixed beech-hornbeam forest , 2006 .

[42]  W. Whitman,et al.  Linking species richness, biodiversity and ecosystem function in soil systems , 2005 .

[43]  T. Nakashizuka,et al.  The effect of shelterwood logging on the diversity of plant species in a beech (Fagus crenata) forest in Japan , 1999 .

[44]  P. Jouquet,et al.  Spatial patterns of grasses influence soil macrofauna biodiversity in Amazonian pastures , 2009 .

[45]  K. Thompson,et al.  Integrated screening validates primary axes of specialisation in plants , 1997 .

[46]  P. Lavelle,et al.  A Hierarchical Model for Decomposition in Terrestrial Ecosystems: Application to Soils of the Humid Tropics , 1993 .

[47]  F. S. Chapin,et al.  The Mineral Nutrition of Wild Plants Revisited: A Re-evaluation of Processes and Patterns , 1999 .

[48]  C. Preston,et al.  Variability in litter quality and its relationship to litter decay in Canadian forests. , 2000 .

[49]  T. M. Bezemer,et al.  Soil invertebrate fauna enhances grassland succession and diversity , 2003, Nature.

[50]  Jean-François Ponge,et al.  Humus Index: an integrated tool for the assessment of forest floor and topsoil properties , 2002 .

[51]  P. Giller The diversity of soil communities, the ‘poor man's tropical rainforest’ , 1996, Biodiversity & Conservation.

[52]  W. Silver,et al.  Interactions between Aboveground and Belowground Biodiversity in Terrestrial Ecosystems: Patterns, Mechanisms, and Feedbacks , 2000 .

[53]  P. Kareiva Diversity begets productivity , 1994, Nature.

[54]  Wardle How soil food webs make plants grow. , 1999, Trends in ecology & evolution.

[55]  Karin S. Fassnacht,et al.  Comparison of the litterfall and forest floor organic matter and nitrogen dynamics of upland forest ecosystems in north central Wisconsin , 1999 .

[56]  Eugene P. Odum,et al.  A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling , 1995 .

[57]  R. Bardgett,et al.  Changes in species evenness of litter have no effect on decomposition processes , 2002 .

[58]  F. Provenza,et al.  Linking herbivore experience, varied diets, and plant biochemical diversity , 2003 .

[59]  Pierre Legendre,et al.  Numerical Ecology with R , 2011 .

[60]  Christian J. M. G. Pieri,et al.  Fertility of Soils: A Future for Farming in the West African Savannah , 1992 .

[61]  M. Argyropoulou,et al.  Two scale patterns of spatial distribution of oribatid ites (Acari, Cryptostigmata) in a Greek mountain , 2002 .

[62]  Jean-François Ponge,et al.  Biocenoses of Collembola in atlantic temperate grass-woodland ecosystems , 1993, Pedobiologia.

[63]  Randy A. Dahlgren,et al.  Polyphenol control of nitrogen release from pine litter , 1995, Nature.

[64]  Jens Emborg,et al.  Biodiversity in natural versus managed forest in Denmark , 1996 .

[65]  L. Pieters,et al.  Condensed vegetable tannins: Biodiversity in structure and biological activities , 1999 .

[66]  Deutsche Ausgabe World Reference Base for Soil Resources 2006 , 2007 .

[67]  M. Zimmer Is decomposition of woodland leaf litter influenced by its species richness , 2002 .

[68]  T. Filley,et al.  Earthworms, stand age, and species composition interact to influence particulate organic matter chemistry during forest succession , 2009 .

[69]  E. Schulze,et al.  THE ROLE OF PLANT DIVERSITY AND COMPOSITION FOR NITRATE LEACHING IN GRASSLANDS , 2003 .

[70]  V. Wolters,et al.  Humus structure during a spruce forest rotation: quantitative changes and relationship to soil biota , 2007 .

[71]  Jérôme Pagès,et al.  Testing the significance of the RV coefficient , 2008, Comput. Stat. Data Anal..

[72]  L. Frizzera,et al.  Linking forest dynamics to richness and assemblage of soil zoological groups and to soil mineralization processes , 2008 .

[73]  M. Berg,et al.  Dynamics and stratification of functional groups of micro- and mesoarthropods in the organic layer of a Scots pine forest , 1998, Biology and Fertility of Soils.

[74]  E. Crompton The Soils of Europe , 1954, Nature.

[75]  J. Deckers,et al.  World Reference Base for Soil Resources , 1998 .

[76]  S. Pickett,et al.  Beyond biodiversity: individualistic controls of invasion in a self‐assembled community , 2004 .

[77]  David A. Wardle,et al.  Communities and Ecosystems: Linking the Aboveground and Belowground Components , 2002 .

[78]  Jean-François Ponge,et al.  Comment distinguer dysmoder et mor? L'exemple de la forêt domaniale de Perche-Trappe (Orne) , 2000 .

[79]  J. Barkman,et al.  Synusial Approaches to Classification , 1978 .

[80]  K. Klinka,et al.  Towards a taxonomic classification of humus forms , 1993 .

[81]  Jean-François Ponge,et al.  Climatic effects on soil trophic networks and the resulting humus profiles in holm oak (Quercus rotundifolia) forests in the High Atlas of Morocco as revealed by correspondence analysis , 2003 .

[82]  R. Aerts Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks , 1999 .

[83]  D. Tilman Causes, consequences and ethics of biodiversity , 2000, Nature.

[84]  D. Tilman,et al.  Plant diversity and ecosystem productivity: theoretical considerations. , 1997, Proceedings of the National Academy of Sciences of the United States of America.