Changes in humus forms and soil animal communities in two developmental phases of Norway spruce on an acidic substrate

Forest Ecology and Management 237 (2006) 47–56 www.elsevier.com/locate/foreco

Changes in humus forms and soil animal communities in two developmental phases of Norway spruce on an acidic substrate Sandrine Salmon a,*, Je´rome Mantel a, Lorenzo Frizzera b,c, Augusto Zanella c a

Muse´um National d’Histoire Naturelle, De´partement Ecologie et Gestion de la Biodiversite´, USM 301, 4 Avenue du Petit-Chaˆteau, 91800 Brunoy, France b Centro di Ecologia Alpina, Gruppo Humus, 38040 Viote Monte Bondone (TN), Italy c Universita` di Padova, Facolta` di Agraria, Dip. TeSAF, 35020 Legnaro, Italy Received 14 September 2005; received in revised form 12 July 2006; accepted 21 September 2006

Abstract This study focuses on the relationships between forest dynamics and changes in humus forms and animal communities in three areas of spruce forest at two developmental phases: two areas with 24-year-old trees (mean age) and one area with 136-year-old trees located in the Italian Alps. Mesofauna and macroarthropods were identified at the level of zoological group, order, super-family or family, when possible. They were then classified into morphotypes on the basis of features observable under a magnifying glass. The humus form varied from amphimull to dysmull in the 24-year-old spruce stands (regeneration), and was a dysmoder under the 136-year-old trees (adult). Results of correspondence analysis and ANOVA indicated that soil pH was higher in regeneration stands, where animal communities were mainly characterized by high densities of collembola, centipedes, and macrofauna. The diversity of zoological (and functional) groups was also higher in regeneration stands. The two regeneration stands differed only in the abundance of gamasids and Protura. Soil carbon and nitrogen contents increased in the mature spruce stand, as did the C/N ratio. The abundance of animals increased due to higher densities of mites, particularly oribatids while collembola, macrofauna, zoological diversity and the rate of disappearance of the litter decreased. The comparison of morphotype assemblages by hierarchical agglomerative clustering indicated that the shift between 24-year-old and 136-year-old trees, observed for humus forms, also occurred for animal communities. Differences in soil characteristics and animal communities between the two phases of the forest cycle corresponded to those generally observed between mull and moder, except for collembola which are generally more abundant in the thick organic layers of moder soils. Our findings confirm the change in humus form previously noted by other authors in the French Alps, but are inconsistent with data on humus forms and collembola and oribatid mite populations from Northern Europe. We conclude that changes in invertebrate communities, particularly arthropods, with the growth phases of spruce may be attributed to (1) soil impoverishment, due to the increased rate of nutrients and water uptake by growing trees; and (2) increase in recalcitrant litter input, mostly transformed by oribatid mites. Our data indicated that animal communities and humus forms could be a reliable means of assessing functional characteristics of the ecosystem corresponding to each growth phase of spruce. # 2006 Elsevier B.V. All rights reserved. Keywords: Forest dynamics; Humus forms; Invertebrate communities; Soil fauna; Spruce cycle phases; Zoological diversity

1. Introduction As stated by Bengtsson et al. (2000), current forestry practices must incorporate more knowledge about natural forest dynamics, particularly natural disturbance dynamics, in order to improve the management of European forests for both production and biodiversity. Soils store the bulk of ecosystem carbon in the form of organic matter (Wall, 1999) and soil biota, which condition the cycling of carbon and nitrogen, and control

* Corresponding author. Tel.: +33 1 60 47 92 11; fax: +33 1 60 46 57 19. E-mail address: [email protected] (S. Salmon). 0378-1127/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2006.09.089

nutrient availability for primary producers. Humus forms, found at the interface between plants, animals and microbes, are the seat of most biological activities occurring in forest ecosystems (Ponge, 2003). Humus forms are the result of animal and microbial activity in the soil (Rusek, 1975; Kubiena, 1955), and in turn they condition the development of terrestrial plant, animal and microbial communities (Ponge et al., 1997; Ponge, 1999; Hooper et al., 2000). Mull, characterized by the rapid disappearance of leaf litter through the activity of burrowing animals and white-rot fungi, and by the mixing of humified organic matter with mineral particles within macroaggregates, is associated with the most fertile soils and supports an abundant and diversified herbaceous layer (Ponge, 2003).

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In moder humus, organic matter accumulates in the form of three holorganic horizons, without cementation of organic matter by mineral particles (Ponge, 2003). The humus form also depends on parent-rock and climate (Toutain, 1987), but, in constant conditions of climate and substrate, it may change only with the vegetation cover. Bernier and Ponge (1994) studied changes in humus forms according to developmental phases of a spruce forest in the French Alps. They observed that the humus form changed along a spruce chronosequence. However, their findings were based on the observation of a small area without replication (one sample per growth phase). In other cases, such change did not appear to occur; for example in Germany, where trees had grown after clear-cutting (Zaitsev et al., 2002). Moreover, with regards soil fauna, only three groups have been studied separately in two geographically different spruce forests (Ha˚gvar, 1982; Bernier and Ponge, 1994; Migge et al., 1998; Zaitsev et al., 2002; Chauvat et al., 2003), but no comparison of a wider animal community has been carried out in different phases of the forest cycle. Our objectives were (1) to assess whether changes in humus forms are correlated with spruce forest dynamics in the Italian Alps and thus are general, and (2) to determine whether and how the animal community parallels this trend. 2. Material and methods 2.1. Site description and sampling design The present study was carried out in a south-facing site located on acid parent-rock. It will be compared with investigations in forests with different types of parent-rock (basic and intermediate) and various exposures. Soil samples were taken in September 2002 in a spruce forest situated near the village of Madonna di Campiglio, in the Southeastern Italian Alps. The sample site is located at an altitude of 1770 m a.s.l. and faces South. Granites of the geological substrate belong to the plutonic rock of Adamello and are covered by late-Wurm moraine deposits, rich in silicates. The tree layer is dominated by Picea abies (L.) Karst. (94.8%), with a low percentage of Larix decidua Mill. (5.2%). Regeneration is natural and follows marginal cutting or canopy opening. The mean annual temperature is 3.9 8C (minimum: 3.4 8C, maximum: 12.7 8C), and the mean annual rainfall is 1311 mm (minimum: 29.7 mm in February, maximum: 186.2 mm in October). Two growth phases of spruce, distributed in three main areas, were investigated: (1) regenerating trees (9–40 years, mean = 24 years) and (2) adult trees (104–172 years, mean = 136 years). Sampling points were chosen randomly in each growth phase and were distributed as follows: - eight in the area ‘‘adult trees’’ (A) which covers 45 m2; - four in the area ‘‘regenerating trees’’ (Rb) of 16 m2, which adjoins area A; - four in the area ‘‘regenerating trees’’ (Ra) of 10 m2, located 200 m from Rb. Two regeneration areas (Ra and Rb) were chosen in order to complete the sampling regime.

The age of trees was estimated by two methods according to the height of trees. For trees with a diameter inferior to 7 cm (measured at a height of 130 cm), the number of whorls was counted and a regression was performed between the height of trees and the number of whorls. For trees with a diameter superior to 7 cm, a probing was taken in order to count the rings and a regression between the height of trees and the number of rings was done. The slope was 32–338 in each sampling area. Dominant plant species of the ground vegetation (abundance–dominance index AD > 2, Gallandat et al., 1995) were as follows: - Area A: Hieracium murorum, Deschampsia flexuosa, Oxalis acetosella, Luzula nivea. The mean vegetation cover varied from 0 to 25% over the whole sampling area but no plants were growing at the sampling points. - Area Rb: Oxalis acetosella, Hieracium murorum. The mean cover was 30% except for sample Rb2 that hosted Festuca heterophylla, Potentilla erecta, Anthoxanthum odoratum, Deschampsia flexuosa, Carex gr. Ornithopoda, Viola biflora, Aposeris foetida (mean coverage: 95%). - Area Ra: Calamagrostis arundinacea (mean vegetation cover not determined). At each sampling point, three soil cores were taken using a rectangular 9.5 cm  5.5 cm (15 cm depth) box: one for the collection of arthropods, one for the extraction of enchytraeids and one for chemical analyses. 2.2. Collection and identification of fauna Soil arthropods were extracted by the dry funnel method (Edwards and Fletcher, 1971) and kept in 90% alcohol. Each sample was placed in a flat glass cup, the bottom of which was divided into 200 compartments (5 mm  5 mm square areas, delineated by vertical walls), which force the animals to fall within the squares. Macrofauna invertebrates were counted in the 200 compartments and classified into groups under a binocular magnifying glass (40 magnification), while microarthropods were counted in 25 randomly-chosen compartments (Alden et al., 1982; Mo¨ller and Bernhard, 1974), except for one sample (Rb1) where all compartments were scored. To assess the validity of this partial sampling method with our samples, the total abundance of the Rb1 sample was compared to the mean abundance of the seven other replicates for which microarthropods were partially counted, using a t-test (Sokal and Rohlf, 1995). The total abundance of samples from regeneration areas Ra and Rb were previously log-transformed to ensure a normal distribution of the residues. The observed t-value (0.0884 < t[0.05, n = 6]) indicated that the probability of obtaining the total abundance of the sample Rb1 fell within the confidence limits of the mean abundance of the seven other samples which were partially counted. Animals were identified at the level of the order, superfamily or family and classified into morphotypes on the base of morphological features (Dindal, 1990; Coineau et al., 1997; Dunger and Fiedler, 1997). For mites, these features were body shape, presence of pteromorphs, distance between anal and

S. Salmon et al. / Forest Ecology and Management 237 (2006) 47–56

genital plates and presence of leg nodules. For collembola, morphological characteristics included the presence and shape of eye spots, body shape and pigmentation, while for insect larvae (Diptera and Coleoptera), body and head shape were used. Enchytraeids were extracted by the modified wet-funnel method of O’Connor (1957). The soil sample was placed under a light bulb on a 2 mm-mesh plastic gauze at the top of a funnel, which was filled with water. The nose of the funnel was extended with a polyethylene tube closed by a Hoffmann clamp. Enchytraeids were collected after 6, 12 and 24 h in Petri dishes, and counted immediately under a magnifying glass (40 magnification). 2.3. Physical and chemical soil characteristics Each humus form at each sampling point was classified and given a Humus Index by examining the soil profile and measuring humus layer thickness (Breˆthes et al., 1995; Ponge et al., 2002). Humus Index is a number varying from 1 to 7 and attributed to humus forms on the basis of the thickness and number of organic layers, which allows to processes humus forms as numerical data (Ponge et al., 2002). Organic carbon and total nitrogen content were measured in 50 mg of dried and defaunated soil. Soil samples were ground to 100 mm and homogenized before measurements were done with a CHN atomic analyzer (Perkin-Elmer CHNS/O Analyzer 2400 Series II). In order to estimate organic carbon content, any calcium carbonate present in the sample was removed by treatment with HCl prior to analysis. Soil pH–H2O was measured on soil mixed with deionized water (soil:water 1:5, v/v) for 5 min, pH being measured 3 h after this procedure (Anonymous, 1999). 2.4. Statistical analysis Prior to analysis, faunal variables and population indices were calculated: total abundance, number of predators (Gamasida + Pseudoscorpionida + Araneida + Chilopoda + Staphylinidae + Coccinellidae), taxonomic richness (number of main zoological groups; see names in bold type in Table 2), morphotype richness, and Shannon diversity index based on zoological (taxonomic) groups (Legendre and Legendre, 1998; Mc Cune and Grace, 2002). The Shannon index (H) was calculated according to the following formula: S X H¼ pi log2 pi ; i¼1

xi where pi ¼ PS

i¼1 xi

where pi = proportion of individuals belonging to the animal category ‘‘i’’, S = number of animal categories and xi = number of individuals in the animal category ‘‘i’’. Numbers of animals per sample were compared by correspondence analysis, a multivariate method using the Chi-square distance (Greenacre, 1984). This method represents variables and samples simultaneously in a plane formed by the first factorial axes. The different zoological groups were the

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Table 1 Contents in organic carbon and total nitrogen, C/N and pH values (mean  standard error) in soils from regeneration and adult tree stands Regeneration (Ra + Rb) 1

Organic carbon (g kg ) Total nitrogen (g kg1) C/N pH–H2O Humus Index

129.71  36.07 8.44  2.15 21.41  0.68a 4.43  0.29b 4.13  0.21b

b

Adult trees (A) 224.48  61.37a 10.36  2.06 15.29  2.18b 4.23  0.24a 7.00  0.00a

Different letters within the same line indicate a significant difference (one-way ANOVA, p < 0.05).

active variables, while morphotypes, physical and chemical parameters (soil pH, soil organic carbon, soil nitrogen, C/N ratio, Humus Index), sampling areas (A, Ra and Rb), age of tree stands (regeneration and adult) and animal community indices (predator numbers, total abundance, Shannon index, taxonomic and morphotype richness) were treated as passive variables. Passive variables were projected on factorial axes as if they had been involved in the analysis, without contributing to them. All variables were transformed prior to analysis, according to the formula X = (x  m)/s + 20 (Ponge and Delhaye, 1995), where X is the standardized value; x, the original value; m, the mean of the variable; and s is its standard deviation (S.D.). Each variable was associated with a conjugate, varying in an opposite sense (x0 = 20  x). Thus, each animal group was represented by two points, one indicating higher numbers for this group, the other lower numbers. Following this standardization, factorial coordinates of variables can be interpreted directly in terms of their contribution to factorial axes. The farther a variable was projected from the origin of a factorial axis, the more it contributed to this axis. In order to ensure a clear graphical representation of these results, physical and chemical soil characteristics and faunal variables are represented separately, and only variables corresponding to higher abundances of animal groups are represented. Correlations between variables and factorial axes were calculated by the Spearman rank correlation coefficient (Sokal and Rohlf, 1995). Variation in the abundance of various zoological groups or soil characteristics according to tree age, as indicated by correspondence analysis, was tested by ANOVA (one-way ANOVA, eight replicates). Data were previously log-transformed when necessary. The Humus Index, which was not normally distributed even after transformation of the data, was compared with a Mann–Whitney test. Only variables that contributed significantly to factorial axes were tested. Differences between the two regeneration areas were previously compared using an ANOVA (one-way, four replicates) to assess whether data from Ra and Rb could be pooled to test the effect of the tree age. When animal abundance differed in Ra and Rb, they were compared separately with the abundance in area A by a one-way ANOVA with four replicates, a sub-sample of four replicates in A being selected randomly without replacement. Similarity between morphotype composition at varied age of tree stands was analyzed with hierarchical agglomerative clustering based on the Euclidian distance using Ward’s method

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Fig. 1. Correspondence analysis. Projection along Axes 1 and 2 of tree stands (Rx and A), sampling areas (Ra, Rb, A) and soil characteristics (passive variables). Bordered names are significantly correlated to Axis 1; underlined names are significantly correlated to Axis 2.

(Legendre and Legendre, 1998). StaboxPro 5 software (Grimmersoft1) was used for all analyses. 3. Results 3.1. Physical and chemical soil parameters The humus form varied from amphimull to dysmull under regeneration (Ra and Rb), and was a dysmoder in the adult tree stand (A), although the thickness of horizons varied from one sampling point to another. The Humus Index varied from 3 to 5 in regeneration stands to 7 in the adult tree stand. The two first factorial axes of correspondence analysis represented 19.1 and 16.3% of the total variance of zoological groups, respectively. Axes 1 and 2 were strongly related to tree stands that were well separated by both axes (Figs. 1 and 2). The projection of zoological groups and soil characteristics showed distinct patterns related to regeneration (Rx = Ra + Rb) and adult tree (A) stands.

Axis 1 is negatively correlated with the quantity (soil carbon and nitrogen content) and positively correlated with the quality of organic matter (Fig. 1). It indicates that the highest content in organic carbon and total nitrogen, and the higher values of the C/N ratio, which reflects a slow decomposition of the litter, occurred in the adult tree stand (Fig. 1). The Humus Index was also higher in the adult tree stand (Fig. 1) and corresponded to a dysmoder with a lower pH than mulls (dysmulls and amphimulls; Fig. 1), which were found only in regeneration stands. ANOVAs (Table 1) confirmed all the above differences except for N content ( p = 0.085). 3.2. Soil fauna Densities of zoological groups in each sampling area are listed in Table 2. Axis 1 displays a gradient opposing faunal diversity (morphotype richness, Shannon index diversity) to faunal abundance. It indicates that the abundance of mites, in particular Oribatida and Actinedida (oribatids accounting for

Fig. 2. Correspondence analysis. Projection along Axes 1 and 2 of zoological groups (active variables), tree stands (Rx and A), sampling areas (Ra, Rb, A), and indexes related to soil fauna. Zoological groups are encoded with three to five letters (see Table 2). Surrounded names are significantly correlated to Axis 1; underlined names are significantly correlated to Axis 2.

S. Salmon et al. / Forest Ecology and Management 237 (2006) 47–56

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Table 2 Density (mean number per square meter  standard-error) of zoological groups, codes used in correspondence analysis and total faunal abundance in each sampling area Zoological group

Code

Trophic type*

Regeneration x (a + b)

Regeneration a

Acari Oribatida Actinedida Acarididae Gamasina Uropodina Ixodidae

MITES ORIBT ACT ACAR GAM URO IXO

sa/mi/zo sa/mi zo/sa sa zo zo/sa –

323684.2  36903.1 255717.7  29291.9* 51076.6  14969.3** 0.0 16674.6  2786.0 Ra*, RbNS 191.4  191.4 23.9  23.9

297464.1  56069.2NS 247703.3  50488.3NS 27559.8  13274.4NS 0.0 22201.0  3671.4A 0.0 0.0

Collembola Entomobryomorpha Poduromorpha Symphypleona

COLL C.ENT C.POD C.SYMP

mi/sa mi/sa mi/sa mi/sa

60430.6  8906.2* 43205.7  6283.6* 17033.5  3630.6NS 191.4  191.4

74641.1  13191.4NS 52057.4  7552.7NS 22583.7  6262.4NS 0.0

Araneida Pseudoscorpionida Protura Psocoptera Thysanoptera Hymenoptera

ARAI PSEUD PROT PSOC THYS HYM

zo zo mi/sa mi phy/zo/sa zo/phy

119.6  71.8NS 0.0 5215.3  3262.4 Ra*, RbNS 0.0 23.9  23.9 23.9  23.9

47.8  47.8NS 0.0 9569.4  6072.3A 0.0 0.0 47.8  47.8

Coleoptera Staphilinidae Curculionidae Coccinellidae Cerambycidae Ptilidae Staphilinidae larvae Other Coleoptera larvae

COL STAPH CURC COCC LONG PTIL L.STAPH L.COL

zo/phy/mi zo sa zo/phy phy mi zo zo/phy

885.2  265.6NS 382.8  153.5NS 47.8  31.3 0.0 0.0 47.8  47.8 119.6  35.0NS 287.1  108.5*

717.7  361.2NS 287.1  227.8NS 95.7  55.2 0.0 0.0 0.0 95.7  55.2NS 239.2  181.1

Homoptera adult Homoptera larvae Diptera larvae

HOM L.HOM L.DIP

phy phy sa

215.3  189.5 47.8  31.3 454.5  144.4NS

0.0 95.7  55.2 287.1  165.7

Chilopoda Geophilomorpha Lithobiomorpha

CHIL GEO LITH

zo zo zo

956.9  306.9* 885.2  327.4NS 71.8  50.3

478.5  123.5NS 334.9  163.4NS 143.5  91.6

Diplopoda Iulidae Glomeridae

DIP IUL GLOM

sa sa sa

119.6  95.3NS 23.9  23.9 95.7  95.7

47.8  47.8NS 47.8  47.8 0.0

Isopoda Symphila Enchytraeidae Indetermined larvae Predators

ISOP SYMPH ENC L.IND

sa mi/phy sa/mi/phy

23.9  23.9 95.7  51.2NS 13325.4  1808.8 47.8  31.3 18253.6  2686.7NS

0.0 143.5  91.6 13923.4  1407.2 95.7  55.2 23110.0  3523.3

405669.9  35896.8*

397559.8  61425.7NS

zo

Total density

*

Zoological group

Regeneration b

Adult trees

Acari Oribatida Actinedida Acarididae Gamasina Uropodina Ixodidae

349904.3  52470.5 263732.1  37579.0 74593.3  22378.8 0.0 11148.3  1543.8B 382.8  382.8 47.8  47.8

527368.4  37283.7 392727.3  40128.1 116842.1  15743.9 6507.2  2663.8 11291.9  2419.8 0.0 0.0

Collembola Entomobryomorpha Poduromorpha Symphypleona

46220.1  7843.6 34354.1  8658.9 11483.3  1326.0 382.8  382.8

31411.5  12277.2 17990.4  8043.5 13421.1  4480.6 0.0

Araneida Pseudoscorpionida Protura Psocoptera

191.4  135.3 0.0 861.2  394.6B 0.0

143.5  118.6 47.8  31.3 574.2  280.2 23.9  23.9

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Table 2 (Continued ) Zoological group

Regeneration b

Adult trees

Thysanoptera Hymenoptera

47.8  47.8 0.0

0.0 23.9  23.9

Coleoptera Staphilinidae Curculionidae Coccinellidae Cerambycidae Ptilidae Staphilinidae larvae Other Coleoptera larvae

1052.6  424.4 478.5  227.8 0.0 0.0 0.0 95.7  95.7 143.5  47.8 334.9  143.5

1028.7  184.2 95.7  51.2 0.0 23.9  23.9 71.8  35.0 0.0 95.7  51.2 741.6  175.1

Homoptera adult Homoptera larvae Diptera larvae

430.6  369.6 622.0  226.1 0.0

4043.1  2689.0 550.2  318.3 0.0

Chilopoda Geophilomorpha Lithobiomorpha

1435.4  521.2 1435.4  521.2 0.0

287.1  114.4 287.1  114.4 0.0

Diplopoda Iulidae Glomeridae

191.4  191.4 191.4  191.4 0.0

23.9  23.9 23.9  23.9 0.0

Isopoda Symphila Enchytraeidae Indetermined larvae Predators

191.4  191.4 47.8  47.8 12727.3  3612.4 47.8  47.8 13397.1  2355.7

0.0 0.0 24856.5  9245.6 167.5  116.9 11985.6  2647.0

Total density

413779.9  46866.0

590550.2  52017.3

The trophic type of zoological groups was determined from Harding and Stuttard (1974), Athias-Binche (1982), Ponge (1985) and Schaefer (1991). sa: saprophages, mi: microphytophages, phy: phytophages, zo: zoophages, pan: pantophages; (*) and (**) in the column ‘‘regeneration x’’ indicate significant differences ( p < 0.05 and p < 0.01, respectively) between regeneration areas and adult tree area. Letters in the column ‘‘regeneration a’’ indicate significant differences between the two regeneration areas a and b. NS: not significant.

75% of total mites) increased in humus forms with a thick litter layer (higher carbon and nitrogen content, higher Humus Index), namely in the adult tree stand (Figs. 1 and 2). Highest values of total animal abundance also occurred in the adult tree stand (Fig. 2), mainly due to a higher number of mites (Table 2). Conversely, the Shannon diversity index (based on the main zoological groups) like the number of predators and the abundance of most other groups were higher in soils with a low Humus Index, namely mulls of regeneration stands Ra and Rb (Figs. 1 and 2). For example, collembola (including Entomobryomorpha), and predators like spiders, gamasids, chilopods and Coleoptera (Staphylinidae included) were more abundant in Ra and Rb, while Uropods, isopods, Symphypleona (collembola) and Ptilidae (Coleoptera) occurred exclusively in Ra and Rb. It may be noticed that Axis 1 showed characteristics of the adult tree stand in contrast with the two regeneration stands Ra and Rb. The factorial Axis 2 (Figs. 1 and 2) also reveals differences between adult and regeneration tree stands, but particularly it highlights differences between A and Ra. These results confirm that the density of mites, particularly Acarididae, was higher in soils with a higher Humus Index, namely the moder of the adult tree stand. Higher abundances of Homoptera and Coleoptera larva (Staphylinidae excluded) occurred in the adult tree stand, and Pseudoscorpions were only found in this area (Fig. 2). Conversely, regeneration stands, particularly Ra, were char-

acterized by a higher abundance of chilopods Lithobiomorpha, Protura, and Homoptera larvae. Neither taxonomic richness (main zoological groups) nor morphotype richness differed between adult and regeneration trees although four zoological groups (Thysanoptera, Isopoda, Symphila, Diptera larvae) were completely absent from the adult tree stand against one (Pseudoscorpionida) from regeneration areas (Table 2). Among zoological groups, seven family or super-family taxa (Uropodina, Ixodidae, Symphipleona, Curculionidae, Ptilidae, Chilopoda Lithobiomorpha, Glomeridae) were absent from the adult tree stand compared to two (Coccinellidae and Cerambicidae) from regeneration stands. ANOVAs demonstrated that the abundance of main zoological groups, the total abundance, and the predator abundance were not significantly different between Ra and Rb (Table 2). Only the densities of gamasids and Protura in Ra were higher than in Rb, the Shannon diversity index being not different between the two areas (Table 3). ANOVAs used to test differences in the abundance of animal groups confirmed that total faunal densities and densities of Coleoptera larvae and Acari (including Oribatida, Actinedida and Acarididae) were higher in the adult stand than in regeneration stands (Table 2). On the contrary, the Shannon diversity index and the abundance of chilopods and collembola, including Entomobryomorpha, were higher in regeneration

S. Salmon et al. / Forest Ecology and Management 237 (2006) 47–56 Table 3 Shannon index, zoological richness and morphotype richness in a 52.25 cm2 area (mean  standard-error) in each sampling area

Regeneration x (a + b) Regeneration a Regeneration b Adult trees

Shannon index

Zoological richness

Morphotypes richness

0.96  0.28a

8.25  1.04

33.13  6.90

1.09  0.23 0.82  0.30 0.59  0.26b

8.50  1.29 8.00  0.82 7.35  2.19

28.25  2.36 38.00  6.48 31.20  7.98

Different letters within a column indicate a significant difference ( p < 0.05) between regeneration areas and the adult tree area.

stands (Tables 2 and 3). Abundances of Protura and gamasids (which were tested in areas Ra and Rb separately) were higher in Ra than in A, but were not different in Rb and A (Table 2). With regards morphotypes, correspondence analysis indicated that four Oribatida and one Actinedida morphotype were

Fig. 3. Results of the hierarchical agglomerative clustering used for testing the similarity of morphotype communities between sampling points in the two spruce cycle phases. Classification is based on the calculation of the Euclidian distance and the clustering by Ward’s method.

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more abundant in the adult stand than in regeneration stands, while regeneration areas were characterized by higher densities of five collembola, two gamasids and three Coleoptera morphotypes (data not shown). ANOVAs confirmed that the densities of three Oribatida and one Actinedida morphotypes were higher ( p < 0.05) in the adult tree area than in regeneration areas while three collembola morphotypes (two Isotomidae and one Poduromorpha) were significantly more abundant in regeneration areas ( p < 0.05 except for one Isotomidae: p < 0.01). The analysis of morphotype communities clearly separated samples of regeneration from those of adult tree area, except one Rb sample, the animal community of which was closer to that of A (Fig. 3). 4. Discussion Highest organic carbon and total nitrogen contents, as well as highest values of the C/N ratio, occurred in moder soil of the adult tree stand. These results reflect a higher input but a slower decomposition of the litter than in mulls at higher pH recorded in regeneration tree stands. In the spruce forests of Norway, lower soil pH and thicker organic layers have been found in 160-yearold compared to 50–60-year-old stands (Ha˚gvar, 1982). Changes in the humus form confirmed the shift from mull to moder observed by Bernier and Ponge (1994) during the growth phase of spruce in French Alps, where the recovery of mull humus occurred under senescent trees. However, this change appears to depend on climate, altitude (Bernier, 1996) and forest management practices since Zaitsev et al. (2002) found no differences in the thickness of organic layers between 25 and 95 years in a planted spruce forest. These authors even reported a more acidic pH under 25 compared to 95-year-old trees. Faunal communities in the studied spruce forest were, in terms of density, dominated by mites, particularly oribatids and to a lesser extent by collembola, independently of the growth phase of trees. The greater abundance of oribatid mites in moder humus (under adult trees) compared to mull humus (under regeneration trees) confirms the observation of several authors (Petersen and Luxton, 1982; Schaefer and Schauermann, 1990). Such a difference is explained by the thicker and older litter layer under adult trees (Luxton, 1982; Irmler, 2000) and by the fact that several oribatid species are the more important consumers and transformers of coniferous needles (Ponge, 1985; Hasegawa and Takeda, 1996). They are probably responsible, for a large part (together with enchytraeids) for the thick OH layer (3–5 cm) observed under 136-year-old trees. Oribatids also feed on fungal mycelium (Ha˚gvar and Kjøndal, 1981) which are more abundant in moder humus (Schaefer, 1991; Ponge, 2003). Because of the higher densities of mites, particularly oribatids, in the moder soil of the adult tree stand, this area also had the highest total faunal abundance. Since the adult tree stand was contiguous or close to regeneration stands, the three areas shared either exactly (Rb, A) or approximately (Ra) the same site-specific effects, only differing in vegetation cover and tree age. Consequently, the

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heterogeneity in the spatial distribution of soil animal groups related to humus forms may be attributed to the age of spruce. The 136-year-old spruce stand was characterized by a higher abundance of mites and total fauna. The distribution of oribatid mites noted here is in contrast with that recorded in spruce forests in Germany (Migge et al., 1998; Zaitsev et al., 2002). Migge et al. (1998) found no difference between the two studied age classes, while Zaitsev et al. (2002) observed the highest oribatid density in the 25 (compared to 5, 45 and 95)year-old tree stand, which also had the lowest pH. Since the thickness of the organic layer in Zaitsev et al.’s (2002) study was the same in all four stands (see above), the higher numbers of oribatid mites may be more related to soil pH than to litter thickness. Unexpectedly, the abundance of enchytraeids did not differ significantly between the two growth phases in our study. Mulls of the two regeneration areas were characterized by a higher number of collembola. This result is in contrast with other soil studies that indicated higher densities of collembola and gamasids in moder or in soils at a lower pH than mulls (Schaefer and Schauermann, 1990; Loranger et al., 2001). Even Ha˚gvar (1982), who studied varied coniferous forest ecosystems, found increased densities of collembola in moder soils of old spruce stands (160 years), while Chauvat et al. (2003) who studied a spruce chronosequence found no differences in the abundance of collembola between four growth stages from 5 to 95 years. The lower water availability resulting from a more dense root system (Babel, 1977) in the adult tree stand may be responsible for the lower abundance of collembola in this stand, collembola being less resistant than oribatids to desiccation (Coleman et al., 2004). Competition between collembola and oribatids for microbial food (Kaneko et al., 1995; Irmler, 2000) may also explain the observed spatial distribution. The density of Chilopoda, particularly Geophilomorpha, and saprophagous macrofauna (Diplopoda, Isopoda, Diptera larvae) was higher in mulls of regeneration stands than in moder of the adult tree stand, which supports previous observations (Athias-Binche, 1982; Schaeffer, 1991b; David et al., 1993; Lavelle, 2001). The increased density of Chilopoda Geophilomorpha must be highlighted since it is 50 times higher than that observed in a spruce forest in Germany (Albert, 1982). The animal diversity (Shannon diversity index) was higher in regeneration than in adult tree stands, indicating that a high number of zoological groups occurred at higher densities in regeneration stands, which reflects a higher functional diversity. It should be noted that highest zoological diversities are observed in mull (Schaefer and Schauermann, 1990; Ponge, 2003) where the rate of decomposition is also elevated. We observed only two differences in the abundance of invertebrates between the two regeneration areas. Thus, the abundance of these two groups, Gamasids and Protura, appears to be uncorrelated with the developmental phase of spruce, although higher densities of Protura in mull corroborate the observations of other authors (Athias-Binche, 1982; Schaefer and Schauermann, 1990) for deciduous forests. Moreover,

higher densities of Protura have already been associated with an increased abundance of collembola (Petersen and Luxton, 1982). With regards gamasids, their abundance appears to rise when the density of oribatids diminishes (Luxton, 1982), and when the density of their collembolan prey increases (Hopkin, 1997) such as in regeneration stands. Finally, regeneration stands were characterized by a greater abundance of several collembolan and gamasid morphotypes while the adult tree stand hosted particular oribatid morphotypes. A relationship between the spatial distribution of collembola, particularly entomobryids, and tree stand type has already been reported (Huhta and Mikkonen, 1982). The comparison of morphotype communities indicated that the shift in humus form between 24-year-old and 136-year-old trees is paralleled by a change in animal community composition, morphotypes being a rather reliable mean of studying animal communities and characterizing a spruce cycle phase, without identification at the species level. Bernier and Ponge (1994) attributed the formation of mull to anecic and endogeic earthworms, which they found to be more abundant under 30–50 than under 130-year-old spruce at 1700 m (Bernier, 1996). These authors noted that the return of earthworms, along with herbaceous vegetation and mull humus forms, occurred when trees were 160–190 years old, after their intense growth phase. Contradictory results about changes in humus form and some animal communities (especially oribatids and collembola, see Zaitsev et al., 2002; Chauvat et al., 2003, and above) may be due to variations in climate, vegetation cover, tree age, and particularly forest management practices. For example, the more extensive surface of each cycle phase in German forest stands (4 ha instead of 10–45 m2) probably reduces the recolonization ability of soil fauna when the depressive effect of tree growth is alleviated. In addition, the correlation between age and forest cycle phases (rotation) varies with altitude (Bernier, 1996). Changes in invertebrate communities, particularly arthropods, may be explained by (1) soil impoverishment due to the increased rate of nutrients and water uptake by trees from the regeneration stage until the canopy closure (Miller, 1981), and (2) the increase of litter input, composed almost exclusively of spruce needles that are particularly recalcitrant (Gallet, 1992) and less palatable than herbaceous litter (Edwards, 1974; Ponge, 1991; Edwards and Bohlen, 1996) occurring in the clearing near the studied areas or, to a lesser extent, in regeneration areas. In fact few organisms are able to consume coniferous needles (Ponge, 1988, 1991), the transformation by oribatid mites being the most efficient. Moreover, the accumulation of litter is accompanied by a decrease of soil pH that affects the distribution of soil animals (Salmon and Ponge, 1999; Schaefer and Schauermann, 1990; Edwards and Bohlen, 1996), particularly macrofauna which, in turn, conditions the formation of mull and a rapid turn-over of nutrients. In addition, increased microarthropod densities in the adult tree stand may reduce soil respiration (thus litter decomposition), through overgrazing on micro-organisms (Cole et al., 2004), which further slows down litter decomposition in a positive feedback process.

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5. Conclusions Although a wider range of tree ages sampled over several sampling seasons would have permit to better assess the impact of trees age, our study indicates that deep modifications of animal communities occur between 24-year-old and 136-yearold tree stands. Variation between the two developmental phases of spruce was more substantial than variation within each sampling area. Differences in the characteristics of animal communities found in the two tree stands corresponded to that already reported between mull and moder soils, except for collembola which were more abundant under regeneration trees in the present study. Since animal communities and humus forms are closely correlated with spruce growth phases, we suggest that humus forms could be indicative of the functional state of forest ecounits. This should be confirmed by a study of faunal communities over a higher number of growth phases under other environmental conditions (north exposure, sub-acidic and sub-neutral parent-rock) which is currently underway. If the hypothesis that soil impoverishment by growing trees and accumulation of spruce needles are responsible for the changes in animal communities and humus form is verified, our results would suggest that a decrease in the size of stand management areas or a lower tree density in adult stands encourages an increased animal diversity and decomposition rate of the litter and, consequently, the conservation or more rapid recovery of mull. Acknowledgements This study was funded by the Autonomous Province of Trento and the Center of Alpine Ecology of Trento (Italy) as part of the DINAMUS (Humus and forest dynamics) project which aims at studying the impact of environmental variables on changes in humus forms in various developmental phases of spruce forests, in order to improve forest management practices. The authors are grateful to Dr. Nicolas Bernier from the Muse´um National d’Histoire Naturelle for the extraction of enchytraeids, and his assistance with the identification of mites. They thank Dr. Sylvaine Camaret from the University of Chambe´ry (France) for vegetation data, Dr. Silvia Chersich and Dr. Roberto Zampedri from the Center of Alpine Ecology of Trento (Italy) for geology, temperature and rainfall data, Gianluca Soncin for the history of sites, Mirco Tomasi and Matteo Girardi for carbon and nitrogen analysis, and Annalisa Losa and Dr. Heidi Hauffe for language correction. The authors are also grateful to Prof. Jean-Franc¸ois Ponge from the Muse´um National d’Histoire Naturelle for fruitful discussion. References Albert, A.M., 1982. Species spectrum and dispersion patterns of chilopods in three Solling habitats. Pedobiologia 23, 337–347. Alden, R.W., Dahiya, R.C., Young Jr., R.J., 1982. A method for the enumeration of zooplankton subsamples. J. Exp. Mar. Biol. Ecol. 59, 185–206.

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