In the locality where this work was developed, a former cattle ranch acquired by an industry of domestic utensils, that was reforested with purposes sustainable economic exploitation and controlled of forest species. The current vegetation is divided in areas of pasture (livestock) abandoned, predominating such as vegetation quicuio-da-amazonia (*Brachiaria humidicola*) among other invasive species, beyond agroforest systems consisting of native species, the main Mogno (*Swietenia macrophylla* King), Paricá (*Schizolobium parayba var. amazonicum* Huber ex Ducke), Freijó (*Cordia goeldiana* Huber) and few exotic, such as eucalyptus (*Eucalyptus* sp) and small areas with secondary forest (capoeira) started around 40 years ago, whose seeds have been used for reforestation native species. The selected

The in the region from, According to Thorntwaite (1948) the climate classification in the studied area is type Br A'a, ("humid tropical"). The average annual rainfall is 2,200 mm not equally distributed throughout the year. However, the period from January to June is its greatest concentration (OLIVEIRA, 2009). The average temperature and relative atmospheric humidity are 26 º C and 74% respectively (CORDEIRO 2007, CORDEIRO et al., 2009). Studies conducted in Brazil (CORDEIRO et al., 2009; 2010) allowed to classify the soil in Aurora do Pará area as Yellow Latossol sandy-clay and the occurrence of concretionary laterite levels in some areas, hydromorphic soils along streams and plain relief to gently

SOUZA et al. 2007; RUIVO et al., 2007, CODEIRO et al. 2009; OLIVEIRA, 2009). It was observed that with the reforestation of these areas the quality and quantity of soil organic matter were slow and continuously recovery .

The fertility of the soil, in edaphoclimatic local conditions, is associated with the content of organic matter in the soil (MOREIRA; COSTA, 2004). However the need to seek a sustainable agriculture, the pressure of national and international society requires techniques that protect the agricultural systems After all, the model of traditional agriculture practiced in the Amazon is unsustainable.

For the reduction of land degradation is necessary the use of conservataive techniques to identify the most profitable activities in the region allowing for a harmonious environment coexistence for agricultural economically viable and environmentally sustainable (SOUSA et al., 2007). The challenge is to identify the correct combinations of species to establish synergistic relationships ideals, so that ensure the key ecological services such as nutrient cycling, biological control of pests and diseases and conservation of soil and water (CARDOSO et al., 2005).

In the state of Para, reforestation with native and exotic species reaches high levels due to the great adaptability of these species in degraded soils. The answers obtained, either in monoculture agroforestry systems, have been effective in the recovery of deforested areas, providing excellent results both for this action as for commercial use, allowing a decrease in aggression to the primary forest and improving the quality of life of populations where this does occur (CORDEIRO, 1999; MONTEIRO, 2004; RUIVO et al., 2007).

Although there are numerous studies on the growth and development of the species native species (CARVALHO, 2004; CORDEIRO, 2007; JESUS, 2004; LORENZI, 2002), comparative studies with the species subjected to different plantation systems and the nutritional behavior of soil in microbiological and biochemists terms are not commonly found in the literature, like as the influence of coverage with different systems involving the vegetables species and their influence on soil quality are still poorly understood. The addition of organic matter to soil, due to stay vegetables residues leads to creation of an enabling environment for better plant development, enhancing microbial activity and consequently the nutritional conditions of the soil. Based on this assumption this research was conducted in the city of Aurora to identifying the soils modifications under physical, chemical and biological properties in areas under reforestation in forestry cropping systems and agro forestry by antropic actions and their impact on edaphic fauna.

### **2. Materials and methods**

#### **2.1 Localization and characterization of the study area**

The study was conducted at the Farm Tramontina Belém S/A, located in the city of Aurora do Pará (Figure 1), which belongs to the Mesoregion of Northeast of Pará state and Microregion Bragantina. This area suffered intense anthropogenic changes in the last 50 years due to high extractivist activity, food production and livestock that decimated almost completely their natural vegetation. Over the years a secondary forest (locally known as capoeira) was developed. Despite being a zone considered in environmental impact, this is an area that food supply the capital, mainly grains, greens and vegetables.

Source: Maps IBGE, 2011.

SOUZA et al. 2007; RUIVO et al., 2007, CODEIRO et al. 2009; OLIVEIRA, 2009). It was observed that with the reforestation of these areas the quality and quantity of soil organic

The fertility of the soil, in edaphoclimatic local conditions, is associated with the content of organic matter in the soil (MOREIRA; COSTA, 2004). However the need to seek a sustainable agriculture, the pressure of national and international society requires techniques that protect the agricultural systems After all, the model of traditional

For the reduction of land degradation is necessary the use of conservataive techniques to identify the most profitable activities in the region allowing for a harmonious environment coexistence for agricultural economically viable and environmentally sustainable (SOUSA et al., 2007). The challenge is to identify the correct combinations of species to establish synergistic relationships ideals, so that ensure the key ecological services such as nutrient cycling, biological control of pests and diseases and conservation of soil and water

In the state of Para, reforestation with native and exotic species reaches high levels due to the great adaptability of these species in degraded soils. The answers obtained, either in monoculture agroforestry systems, have been effective in the recovery of deforested areas, providing excellent results both for this action as for commercial use, allowing a decrease in aggression to the primary forest and improving the quality of life of populations where this

Although there are numerous studies on the growth and development of the species native species (CARVALHO, 2004; CORDEIRO, 2007; JESUS, 2004; LORENZI, 2002), comparative studies with the species subjected to different plantation systems and the nutritional behavior of soil in microbiological and biochemists terms are not commonly found in the literature, like as the influence of coverage with different systems involving the vegetables species and their influence on soil quality are still poorly understood. The addition of organic matter to soil, due to stay vegetables residues leads to creation of an enabling environment for better plant development, enhancing microbial activity and consequently the nutritional conditions of the soil. Based on this assumption this research was conducted in the city of Aurora to identifying the soils modifications under physical, chemical and biological properties in areas under reforestation in forestry cropping systems and agro

The study was conducted at the Farm Tramontina Belém S/A, located in the city of Aurora do Pará (Figure 1), which belongs to the Mesoregion of Northeast of Pará state and Microregion Bragantina. This area suffered intense anthropogenic changes in the last 50 years due to high extractivist activity, food production and livestock that decimated almost completely their natural vegetation. Over the years a secondary forest (locally known as capoeira) was developed. Despite being a zone considered in environmental impact, this is

does occur (CORDEIRO, 1999; MONTEIRO, 2004; RUIVO et al., 2007).

forestry by antropic actions and their impact on edaphic fauna.

an area that food supply the capital, mainly grains, greens and vegetables.

**2.1 Localization and characterization of the study area**

matter were slow and continuously recovery .

(CARDOSO et al., 2005).

**2. Materials and methods**

agriculture practiced in the Amazon is unsustainable.

Fig. 1. Map of geographical location of FarmTramontina Belem S/A, Aurora do Pará.

In the locality where this work was developed, a former cattle ranch acquired by an industry of domestic utensils, that was reforested with purposes sustainable economic exploitation and controlled of forest species. The current vegetation is divided in areas of pasture (livestock) abandoned, predominating such as vegetation quicuio-da-amazonia (*Brachiaria humidicola*) among other invasive species, beyond agroforest systems consisting of native species, the main Mogno (*Swietenia macrophylla* King), Paricá (*Schizolobium parayba var. amazonicum* Huber ex Ducke), Freijó (*Cordia goeldiana* Huber) and few exotic, such as eucalyptus (*Eucalyptus* sp) and small areas with secondary forest (capoeira) started around 40 years ago, whose seeds have been used for reforestation native species. The selected capoeiras soil was used as a standard for comparison with the reforestations soil.

The in the region from, According to Thorntwaite (1948) the climate classification in the studied area is type Br A'a, ("humid tropical"). The average annual rainfall is 2,200 mm not equally distributed throughout the year. However, the period from January to June is its greatest concentration (OLIVEIRA, 2009). The average temperature and relative atmospheric humidity are 26 º C and 74% respectively (CORDEIRO 2007, CORDEIRO et al., 2009). Studies conducted in Brazil (CORDEIRO et al., 2009; 2010) allowed to classify the soil in Aurora do Pará area as Yellow Latossol sandy-clay and the occurrence of concretionary laterite levels in some areas, hydromorphic soils along streams and plain relief to gently

Fertility, Microbial Biomass and Edaphic

three days (AQUINO et al, 2006).

1988, BARRETO et al., 2008).

Bragança and Tailândia.

**biological analysis**

Fauna Under Forestry and Agroforestry Systems in the Eastern Amazon 235

In all locations were collected soil samples deformed and undeformed in December 2009. Samples were collected by opening mini-trenches where soil samples were extracted from

In each study area were collected 3 composite samples of soil from 5 single samples and were stored in plastic bags, conditioned in cool boxes containing ice for stagnate or decrease the microbial activity. The chemical, physical and biological analysis were made by

These traps were consisted of plastic containers (08 cm x 12 cm) buried in the soil to a depth of 12 cm, with the leaked extremity leveled with the surface of soil, where they remained for

In each plot of each treatment, the same depth, were placed four (04) traps, and inside each one of them, was added 60 ml of the preservative substance: 70% alcohol, distilled water (ratio 3:1, regarding the use of alcohol); biodegradable detergent (3 drops) and formaldehyde (10 ml). The fall of undesirable objects was prevented with a cover plate of polystyrene, supported by small wooden rods (AQUINO et al, 2006). The edaphic fauna, after collected, was taken to the laboratory where they were sieved (0.2 mm) to remove the fragments of plant and residues of soil. The identification of edaphic fauna was at the level of Order, with the aid of a stereomicroscope and the specific literature (BORROR, DELONG,

Fig. 2. Trap for capturing the edaphic fauna implanted in the Farms of Aurora do Pará,

**2.3 Collection and preparation of the soil samples for physical, chemical and**

the depths: 0-10, 10-20, 20-40 cm, from transects in areas previously determined.

technicians in the soil laboratory of the Museu Paraense Emílio Goeldi - MPEG.

The Pedofauna collections was performed using kind traps "pitfall-traps" (Figure 2).

**2.4 Collection, preparation and identification of the soil fauna**

rolling inserted on the plateau demoted from Amazon. The nutritional characteristics described in these studies show that they have a low supply of available essential nutrients and low tenor in organic matter (CORDEIRO et al., 2010).

#### **2.2 Cropping systems studied**

Since the 1990s were planted around 1,043 ha submitted to different types of planting reforestation with the use of species such as Mogno (*Swietenia macrophylla* King) by the great commercial value abroad, Ipê (*Tabebuia heptaphyta* Vellozo), Cedro (*Cedrella fissilis* Vellozo), Jatobá (*Hymenaea intermedia* Ducke var. *adenotricha* (Ducke) Lee & Lang.). Since 1994, the Paricá (*Schizolobium parayba* var. Amazonicum Huber ex Ducke), is the species with high commercial value used in the reforestation because of its applicability in the production of laminates. In 1996 the Freijó (*Cordia goeldiana* Huber) was introduced by the high referential commercial value in Europe. In 2003, was included in the reforestation process in the Tramontina area the Curauá (*Ananas comosus* var. *erectifoliu*s LBSmith), a bromeliad that in the Amazon, has a higher concentration in the municipality of Santarém, beyond the regions of Xingu River, Tocantins, Maicuru, Trombetas, Paru, Acará and Guamá. In the Pará state, the Curauá stands out in the Bragança and Santarém districts (OLIVEIRA, 2009).

The experimental design was completely randomized, with four systems under reforestation and three repetitions in each system. (S1) Monocultivation system with curauá, (S2) agroforestry system with paricá and curauá, (S3) monocultivation system with paricá, (S4) agroforestry system with paricá, freijó, mogno and (S5) varied capoeira (Table 1). All cropping systems such as the capoeira were subdivided into four parcels 24 x 19 m (456 m2), which totals 1,824 m2 of area analyzed.

At the time of planting was performed organic fertilization with manure of corral (500g/pit) and bed chicken (150g/pit) for agronomic and forest species, respectively. In the first year of the forestal planting were performed three fertilizations, at 45, 180 and 300 days, using 150 g/pl of the formula NPK 10-20-20. In the planting Curauá, we used 10 g/pl of the formula NPK 10-10-10 at the beginning and end of the rainy season, in the first two years of planting.

Table 1. System of crops, forest species and ages of reforestation, in the Farm Tramontina Belém S/A, Aurora do Pará.

In cropping systems with curauá (S1), agroforestry system with paricá, mahogany, freijó (S3) and in the cropping system with paricá (S4) occured just the cut of the grass, that was left on the soil of these cropping systems, no irrigation in any of them. In agroforestry cropping system with paricá/curauá was made fertilization with manure of corral (500 g/pit) and bed chicken (150 g/pit) (CORDEIRO et al., (2009).

rolling inserted on the plateau demoted from Amazon. The nutritional characteristics described in these studies show that they have a low supply of available essential nutrients

Since the 1990s were planted around 1,043 ha submitted to different types of planting reforestation with the use of species such as Mogno (*Swietenia macrophylla* King) by the great commercial value abroad, Ipê (*Tabebuia heptaphyta* Vellozo), Cedro (*Cedrella fissilis* Vellozo), Jatobá (*Hymenaea intermedia* Ducke var. *adenotricha* (Ducke) Lee & Lang.). Since 1994, the Paricá (*Schizolobium parayba* var. Amazonicum Huber ex Ducke), is the species with high commercial value used in the reforestation because of its applicability in the production of laminates. In 1996 the Freijó (*Cordia goeldiana* Huber) was introduced by the high referential commercial value in Europe. In 2003, was included in the reforestation process in the Tramontina area the Curauá (*Ananas comosus* var. *erectifoliu*s LBSmith), a bromeliad that in the Amazon, has a higher concentration in the municipality of Santarém, beyond the regions of Xingu River, Tocantins, Maicuru, Trombetas, Paru, Acará and Guamá. In the Pará state,

the Curauá stands out in the Bragança and Santarém districts (OLIVEIRA, 2009).

The experimental design was completely randomized, with four systems under reforestation and three repetitions in each system. (S1) Monocultivation system with curauá, (S2) agroforestry system with paricá and curauá, (S3) monocultivation system with paricá, (S4) agroforestry system with paricá, freijó, mogno and (S5) varied capoeira (Table 1). All cropping systems such as the capoeira were subdivided into four parcels 24 x 19 m (456 m2),

At the time of planting was performed organic fertilization with manure of corral (500g/pit) and bed chicken (150g/pit) for agronomic and forest species, respectively. In the first year of the forestal planting were performed three fertilizations, at 45, 180 and 300 days, using 150 g/pl of the formula NPK 10-20-20. In the planting Curauá, we used 10 g/pl of the formula NPK 10-10-10 at the beginning and end of the rainy season, in the first two years of planting.

Systems Forest species Age

Freijó (*Cordia goeldiana* Huber) 08

**S1** Monocultivation Curauá (*Ananas comosus var. erectifolius* L.B.Smith) 06 **S2** Agroforestry Paricá/Curauá (*Ananas comosus var. erectifolius* L.B.Smith) 06

**S4** Monocultivation Paricá 06 **S5** Capoeira varied 15 Table 1. System of crops, forest species and ages of reforestation, in the Farm Tramontina

In cropping systems with curauá (S1), agroforestry system with paricá, mahogany, freijó (S3) and in the cropping system with paricá (S4) occured just the cut of the grass, that was left on the soil of these cropping systems, no irrigation in any of them. In agroforestry cropping system with paricá/curauá was made fertilization with manure of corral (500

**S3** Agroforestry Paricá, Mogno (*Swietenia macrophylla* King),

g/pit) and bed chicken (150 g/pit) (CORDEIRO et al., (2009).

(years)

and low tenor in organic matter (CORDEIRO et al., 2010).

**2.2 Cropping systems studied**

which totals 1,824 m2 of area analyzed.

Belém S/A, Aurora do Pará.

#### **2.3 Collection and preparation of the soil samples for physical, chemical and biological analysis**

In all locations were collected soil samples deformed and undeformed in December 2009. Samples were collected by opening mini-trenches where soil samples were extracted from the depths: 0-10, 10-20, 20-40 cm, from transects in areas previously determined.

In each study area were collected 3 composite samples of soil from 5 single samples and were stored in plastic bags, conditioned in cool boxes containing ice for stagnate or decrease the microbial activity. The chemical, physical and biological analysis were made by technicians in the soil laboratory of the Museu Paraense Emílio Goeldi - MPEG.

### **2.4 Collection, preparation and identification of the soil fauna**

The Pedofauna collections was performed using kind traps "pitfall-traps" (Figure 2).

These traps were consisted of plastic containers (08 cm x 12 cm) buried in the soil to a depth of 12 cm, with the leaked extremity leveled with the surface of soil, where they remained for three days (AQUINO et al, 2006).

In each plot of each treatment, the same depth, were placed four (04) traps, and inside each one of them, was added 60 ml of the preservative substance: 70% alcohol, distilled water (ratio 3:1, regarding the use of alcohol); biodegradable detergent (3 drops) and formaldehyde (10 ml). The fall of undesirable objects was prevented with a cover plate of polystyrene, supported by small wooden rods (AQUINO et al, 2006). The edaphic fauna, after collected, was taken to the laboratory where they were sieved (0.2 mm) to remove the fragments of plant and residues of soil. The identification of edaphic fauna was at the level of Order, with the aid of a stereomicroscope and the specific literature (BORROR, DELONG, 1988, BARRETO et al., 2008).

Fig. 2. Trap for capturing the edaphic fauna implanted in the Farms of Aurora do Pará, Bragança and Tailândia.

Fertility, Microbial Biomass and Edaphic

**3. Results and discussion**

NOTATION **DPT**

**S1**

**S2**

**S3**

**S4**

**(cm)**

classification; SL: Sandy loam; SC:Sandy clay; **Ds:** density of soil.

studied. Farm Tramontina Belém S/A in Aurora do Pará.

our study.

Fauna Under Forestry and Agroforestry Systems in the Eastern Amazon 237

Tukey test (p <0.05). Additional analysis was also the determination of principal components (PCA) and cluster analysis to determine the degree of correlation between physical, chemical and biological data to be analyzed by soil grouping. Them, according to

**3.1 Physical and chemical properties of soil under forestry and agroforestry systems**  The production systems studied showed differences in soil physical properties. The type of soil in cropping systems S1 (monocultivation with curauá), S3 (agroforestry system with paricá, mogno, freijó and curauá) and S4 (monocultivation with paricá) is classified as franc sandy loam and only in the S2 (agroforestry system with paricá and curauá), presented soil type franc sandy clay (Table 2). Study conducted in a Latossoil in the Amazon (SILVA JUNIOR et al, 2009) showed that the study of this aspect of the soil is important because it is related to the dynamics of organic matter. This justifies the textural classification made in

the variation of its characteristics a multivariate analysis can be use.

**Ts Fs**

g/kg

**MEAN --------- 685 155 96 64 0.66 1.47**

**MEAN --------- 420 169 272 139 0.54 1.53**

**MEAN --------- 662 145 94 99 1.10 1.50**

**MEAN --------- 623 199 90 88 1.01 1.47**

With regard to the clay content in the culture system S2 (agroforestry system with paricá and curauá), in the depth from 0 – 10 cm high levels were detected when compared with

**DPT**: Depths; **Ts**: thick sandy; **Fs:** fine sand; **Cl:** clay; **S**: silt; **RSC**: relation silt clay; **TC**: textural

Table 2. Granulometry, textural classification and density of soil of cropping systems

0 - 10 729 157 68 46 0,67 S L 1,50 10 - 20 716 147 83 54 0,65 1,43 20 - 40 610 160 137 93 0,67 1,54

0 - 10 491 189 184 136 0,73 S C 1,37 10 - 20 408 169 289 134 0,46 1,62 20 - 40 362 149 343 146 0,42 1,60

0 - 10 687 148 80 85 1,06 S L 1,42 10 - 20 672 130 80 118 1,47 1,58 20 - 40 627 156 122 95 0,77 1,51

0 - 10 651 204 96 49 0,51 S L 1,36 10 - 20 630 222 80 68 0,85 1,48 20 - 40 588 170 90 152 1,68 1,57

**Cl S RSC TC Ds**

g/cm3

#### **2.5 Determination of the physical and chemical caracteristics of soil**

The granulometric composition was determined by densimeter method (EMBRAPA, 1997) and textural classification of soil in each system was performed using the textural triangle (LEMOS & SANTOS, 2006). The soil density (Ds) was determined by the volumetric ring method type Kopecky.

In the characterization of soil were performed the following measurements: total N, by distillation in semimicro Kjeldahl (BREMNER, MULVANEY, 1982), pH in potentiometer in the relation soil:water 1:2.5, organic C, by volumetric method of oxidation with K2Cr2O7 and titration with ammonium ferrous sulphate, Ca, Mg and Al exchangeable in extractor of KCl 1 mol L-1 and measured in atomic absorption, exchangeable K and Na in Mehlich-1 extraction solution and determination by flame photometry, P available in Mehlich-1 extraction solution and determination by calorimetry, H + Al were extracted with calcium acetate 0.5 mol L-1, pH 7.0 and determined volumetrically with NaOH solution.

From the values of potential acidity (H + Al), exchangeable bases and exchangeable aluminum, the capacity of total cation exchange (CTC) and cation exchange capacity effective (CTCe) were calculated. Relations were also calculated C/N of soil and the organic carbon stock (EstC), using the formula EstC = Corg x Ds x e/10, according to Freixo et al. (2002).

#### **2.6 Determination of carbon (CBM) and nitrogen (NBM) of the soil microbial biomass**

We used the fumigation-extraction method to estimate microbial biomass carbon (CBM) (Vance et al., 1987, Tate et al., 1988). The determination of microbial biomass carbon (C-BMS) of the fumigated and not fumigated extracts was made by titration (dichromatometry) according to De-Polli, Guerra (1999). For CBM calculation , the C content of fumigated samples were subtracted from the values of non-fumigated samples, the difference being divided by the value kc = 0.26 (FEIGL et al., 1995). The estimate of Nmic was made from Kjeldahl digestion. The correction factor (Kn) used for the calculation was 0.54 (BROOKES et al. 1985; Joergensen; Mueller, 1996). From the original values were calculated relations between Cmic and Corg of soil (Cmic/Corg), and Nmic and Ntotal of soil (Nmic/Ntotal), by the following equations: (Cmic/Corg)x100 and (Nmic/Ntotal)x100, respectively. These indices indicate the fractions of Corg and Ntotal that are incorporated in BM, expressing the quality of MOS (GAMA-RODRIGUES, 1999).

#### **2.7 Determination of basal respiration of microbial biomass and the soil metabolic quotient**

The basal respiration was estimated by the amount of C-CO2 released within 10 days of incubation (JENKINSON & POWLSON, 1976). This technique allows the determination of the soil microbial activity, being quantified from the evolution of CO2 produced in respiration of the microorganisms in samples free of roots and possible insects. The metabolic quotient (qCO2) is calculated as the ratio between the rate of basal respiration and the microbial biomass carbon (ANDERSON & DOMSCH, 1993).

#### **2.8 Statistical analysis**

The two-way ANOVA was used to verify differences between the cropping systems studied. When found a significant (5%), the averages of each variable were tested by the Tukey test (p <0.05). Additional analysis was also the determination of principal components (PCA) and cluster analysis to determine the degree of correlation between physical, chemical and biological data to be analyzed by soil grouping. Them, according to the variation of its characteristics a multivariate analysis can be use.

## **3. Results and discussion**

236 Forest Ecosystems – More than Just Trees

The granulometric composition was determined by densimeter method (EMBRAPA, 1997) and textural classification of soil in each system was performed using the textural triangle (LEMOS & SANTOS, 2006). The soil density (Ds) was determined by the volumetric ring

In the characterization of soil were performed the following measurements: total N, by distillation in semimicro Kjeldahl (BREMNER, MULVANEY, 1982), pH in potentiometer in the relation soil:water 1:2.5, organic C, by volumetric method of oxidation with K2Cr2O7 and titration with ammonium ferrous sulphate, Ca, Mg and Al exchangeable in extractor of KCl 1 mol L-1 and measured in atomic absorption, exchangeable K and Na in Mehlich-1 extraction solution and determination by flame photometry, P available in Mehlich-1 extraction solution and determination by calorimetry, H + Al were extracted with calcium

From the values of potential acidity (H + Al), exchangeable bases and exchangeable aluminum, the capacity of total cation exchange (CTC) and cation exchange capacity effective (CTCe) were calculated. Relations were also calculated C/N of soil and the organic carbon stock (EstC), using the formula EstC = Corg x Ds x e/10, according to Freixo et al. (2002).

**2.6 Determination of carbon (CBM) and nitrogen (NBM) of the soil microbial biomass**  We used the fumigation-extraction method to estimate microbial biomass carbon (CBM) (Vance et al., 1987, Tate et al., 1988). The determination of microbial biomass carbon (C-BMS) of the fumigated and not fumigated extracts was made by titration (dichromatometry) according to De-Polli, Guerra (1999). For CBM calculation , the C content of fumigated samples were subtracted from the values of non-fumigated samples, the difference being divided by the value kc = 0.26 (FEIGL et al., 1995). The estimate of Nmic was made from Kjeldahl digestion. The correction factor (Kn) used for the calculation was 0.54 (BROOKES et al. 1985; Joergensen; Mueller, 1996). From the original values were calculated relations between Cmic and Corg of soil (Cmic/Corg), and Nmic and Ntotal of soil (Nmic/Ntotal), by the following equations: (Cmic/Corg)x100 and (Nmic/Ntotal)x100, respectively. These indices indicate the fractions of Corg and Ntotal that are incorporated in BM, expressing the quality of

**2.7 Determination of basal respiration of microbial biomass and the soil metabolic**

the microbial biomass carbon (ANDERSON & DOMSCH, 1993).

The basal respiration was estimated by the amount of C-CO2 released within 10 days of incubation (JENKINSON & POWLSON, 1976). This technique allows the determination of the soil microbial activity, being quantified from the evolution of CO2 produced in respiration of the microorganisms in samples free of roots and possible insects. The metabolic quotient (qCO2) is calculated as the ratio between the rate of basal respiration and

The two-way ANOVA was used to verify differences between the cropping systems studied. When found a significant (5%), the averages of each variable were tested by the

**2.5 Determination of the physical and chemical caracteristics of soil**

acetate 0.5 mol L-1, pH 7.0 and determined volumetrically with NaOH solution.

method type Kopecky.

MOS (GAMA-RODRIGUES, 1999).

**2.8 Statistical analysis**

**quotient**

#### **3.1 Physical and chemical properties of soil under forestry and agroforestry systems**

The production systems studied showed differences in soil physical properties. The type of soil in cropping systems S1 (monocultivation with curauá), S3 (agroforestry system with paricá, mogno, freijó and curauá) and S4 (monocultivation with paricá) is classified as franc sandy loam and only in the S2 (agroforestry system with paricá and curauá), presented soil type franc sandy clay (Table 2). Study conducted in a Latossoil in the Amazon (SILVA JUNIOR et al, 2009) showed that the study of this aspect of the soil is important because it is related to the dynamics of organic matter. This justifies the textural classification made in our study.

**DPT**: Depths; **Ts**: thick sandy; **Fs:** fine sand; **Cl:** clay; **S**: silt; **RSC**: relation silt clay; **TC**: textural classification; SL: Sandy loam; SC:Sandy clay; **Ds:** density of soil.

Table 2. Granulometry, textural classification and density of soil of cropping systems studied. Farm Tramontina Belém S/A in Aurora do Pará.

With regard to the clay content in the culture system S2 (agroforestry system with paricá and curauá), in the depth from 0 – 10 cm high levels were detected when compared with

Fertility, Microbial Biomass and Edaphic

corroborates the assertion of those authors.

**DPT**: Depths; **Corg**: carbon organic; **Cs**: Carbon stock.

(Mg C.ha-1).

Fauna Under Forestry and Agroforestry Systems in the Eastern Amazon 239

cover. But the most plausible explanation is provided by Cordeiro et al. (2009), because the authors report that the area where this system of crops is located was fertilized with cattle manure (500 g/pit) and bed chicken (150 g/pit). This proves that even on degraded land, the use of organic cover helps soil fertility and improving the quality of it (Monteiro, 2004). In the systems studied, we observed that the Corg content decreases according to depth and clay content (Table 2) in the depth of 0 - 10 cm, the Corg content of the soil surface within the studied systems are high. The research conducted about the relation of Corg contents and soil depth (Dejardins, et al. 1994; Koutika et al., 1997) showed that the trend of content of Corg is in decreasing accordance with increasing depth. This pattern of behavior on the content of Corg was observed in our study. Study carried out in a toposequence in central Amazonia (Marques et al., 200) report that the Carbon content are high in the surface layers to 25 cm (4.48 ± 0.08). Then, the high content of Corg found in cropping systems study

The highest average of Carbon stock was found in the cultivation system S2 (Table 2), where was found the highest granulometric average, especially the clay and Ds. In descending order, the cultivation system S1 has the second highest average. In the cultivation systems S3 and S4 the average of carbon stock decreases, although the clay content is approximate to that contained in the cropping system S1. However the content of sand has an average ranging from 800 to 840 g/kg, and the variation in average clay content is between 90 and 96 g/kg (Table 1). This may be one explanation for the carbon stocks present a decrease in

NOTATION DPT **pH Corg g/kg Cs**

S1 0 - 10 4.5 13,84 20.76

**MEAN --------- 4.3 10.81 32.24**

**MEAN --------- 4.9 14.84 40.22**

**MEAN --------- 4.3 8.70 27.88**

**MEAN --------- 4.4 7.07 23.93**

Table 3. Values pH (H2O), tenors of carbon organic (Corg in g/kg) and carbon stocks

**S4** 0 - 10 4.4 9,88 13.34

**S3** 0 - 10 4.4 8,59 12.02

**S2** 0 - 10 4.9 24,52 33.61

**(cm)** Mg C.ha-1

10 - 20 4.4 11,70 33.46 20 - 40 4.1 6,90 42.50

10 - 20 4.9 12,96 41.99 20 - 40 5.0 7,04 45.05

10 - 20 4.3 7,89 24.93 20 - 40 4.3 7,73 46.68

10 - 20 4.4 7,38 21,84 20 - 40 4.4 5,83 36.31

average of these treatments compared in the cropping system S2 (Table 2).

other systems in this same depth, as shown in Table 2. Study conducted (LAVELLE et al, 1992) in the humid tropics, showed as a result a lateral variation in the soil granulometry and, according to the researchers, this may influence the training capacity of the stocks of exchangeable cations on the surfaces of colloids, this case, clay mineral. Then, the results found in this study for the S2 cultivation system may be indicative of the improved in the capacity of formation of the exchangeable cations.

The lowest content of clay fraction occur in the cropping systems S1 (monocultivation with curauá), S3 (agroforestry system with paricá, mogno, freijó and curauá) and S4 (monocultivation with paricá). The value for the lowest average was found in the cropping system S4 compared with the other cropping systems studied. Freire (1997) reports that the natural fertility of the soil depends on the adsorptive capacity of clay-minerals and organic colloids, with that, it's possible to affirm that in the cropping system S4, despite the low clay content, there are adsorption capacity and organic colloids in balance that allows the maintenance of natural soil fertility of this cropping system.

The relation silt *versus* clay proved to be higher in the cropping system S3 (Table 2), this demonstrates that the degree of weathering occurred in this area decreases with the depth, ie, the degree of weathering of the soil is high, as occur in the Latosoils.

The analysis of soil density showed that, among the systems studied, soil is more dense in the cultivation system S2 (agroforestry system with paricá and curauá). But, as pointed out Santana et al. (2006) density can be an attribute for analysis on the cohesion of the soil horizons, however there is a limitation for such use, ie, the density of the soil suffers from interference of granulometry that can presents high values, this would correspond to cohesive horizons, and this would affect the penetration of root of vegetables.

In this aspect, it was verified that, in the cropping system S2, the density is more pronounced between 10 to 20 cm when compared with other systems. In addition, this cultivation system, based on the exposed by Santana et al. (2006), we can consider this soil as "cohesive" as a results contained in Table 2.

The results indicate very low acidity (pH > 4.5), and as clay-minerals react with water from the soil, absorbing H +, this may explain the variation of acidity occurred in the cropping system S2, although present statistically significant effect. Was verified that in the cropping systems S1 (curauá monocultivation ) and S3 (agroforestry system with paricá, mogno, freijó and curauá) the pH value, on average, has no statistically significant effect (Table 3). This can be explained by the content of total clay and sand which is also equivalent between them, as shown in Table 2.

In the cropping system S4 (paricá monocultivation ), the pH was found to be constant in the three depths, and this may be due to small variations in the levels of sand and clay that were lower compared to other cropping systems, and this may explain the decrease of pH value in relation to the cropping system S2 and a slight increase in relation to cropping systems S1 and S3 (Table 2).

The tenors of Corg in cultivation system S2 (agroforestry system with paricá and curauá) were superior to other treatments evaluated (Table 3), even with scarce cover vegetation. Study conducted (Silva Junior et al, 2009) in Amazonian Oxisols after transformation to pasture, showed that carbon concentrations are high in clay soils, independent of vegetation

other systems in this same depth, as shown in Table 2. Study conducted (LAVELLE et al, 1992) in the humid tropics, showed as a result a lateral variation in the soil granulometry and, according to the researchers, this may influence the training capacity of the stocks of exchangeable cations on the surfaces of colloids, this case, clay mineral. Then, the results found in this study for the S2 cultivation system may be indicative of the improved in the

The lowest content of clay fraction occur in the cropping systems S1 (monocultivation with curauá), S3 (agroforestry system with paricá, mogno, freijó and curauá) and S4 (monocultivation with paricá). The value for the lowest average was found in the cropping system S4 compared with the other cropping systems studied. Freire (1997) reports that the natural fertility of the soil depends on the adsorptive capacity of clay-minerals and organic colloids, with that, it's possible to affirm that in the cropping system S4, despite the low clay content, there are adsorption capacity and organic colloids in balance that allows the

The relation silt *versus* clay proved to be higher in the cropping system S3 (Table 2), this demonstrates that the degree of weathering occurred in this area decreases with the depth,

The analysis of soil density showed that, among the systems studied, soil is more dense in the cultivation system S2 (agroforestry system with paricá and curauá). But, as pointed out Santana et al. (2006) density can be an attribute for analysis on the cohesion of the soil horizons, however there is a limitation for such use, ie, the density of the soil suffers from interference of granulometry that can presents high values, this would correspond to

In this aspect, it was verified that, in the cropping system S2, the density is more pronounced between 10 to 20 cm when compared with other systems. In addition, this cultivation system, based on the exposed by Santana et al. (2006), we can consider this soil as

The results indicate very low acidity (pH > 4.5), and as clay-minerals react with water from the soil, absorbing H +, this may explain the variation of acidity occurred in the cropping system S2, although present statistically significant effect. Was verified that in the cropping systems S1 (curauá monocultivation ) and S3 (agroforestry system with paricá, mogno, freijó and curauá) the pH value, on average, has no statistically significant effect (Table 3). This can be explained by the content of total clay and sand which is also equivalent between

In the cropping system S4 (paricá monocultivation ), the pH was found to be constant in the three depths, and this may be due to small variations in the levels of sand and clay that were lower compared to other cropping systems, and this may explain the decrease of pH value in relation to the cropping system S2 and a slight increase in relation to cropping systems S1

The tenors of Corg in cultivation system S2 (agroforestry system with paricá and curauá) were superior to other treatments evaluated (Table 3), even with scarce cover vegetation. Study conducted (Silva Junior et al, 2009) in Amazonian Oxisols after transformation to pasture, showed that carbon concentrations are high in clay soils, independent of vegetation

capacity of formation of the exchangeable cations.

"cohesive" as a results contained in Table 2.

them, as shown in Table 2.

and S3 (Table 2).

maintenance of natural soil fertility of this cropping system.

ie, the degree of weathering of the soil is high, as occur in the Latosoils.

cohesive horizons, and this would affect the penetration of root of vegetables.

cover. But the most plausible explanation is provided by Cordeiro et al. (2009), because the authors report that the area where this system of crops is located was fertilized with cattle manure (500 g/pit) and bed chicken (150 g/pit). This proves that even on degraded land, the use of organic cover helps soil fertility and improving the quality of it (Monteiro, 2004).

In the systems studied, we observed that the Corg content decreases according to depth and clay content (Table 2) in the depth of 0 - 10 cm, the Corg content of the soil surface within the studied systems are high. The research conducted about the relation of Corg contents and soil depth (Dejardins, et al. 1994; Koutika et al., 1997) showed that the trend of content of Corg is in decreasing accordance with increasing depth. This pattern of behavior on the content of Corg was observed in our study. Study carried out in a toposequence in central Amazonia (Marques et al., 200) report that the Carbon content are high in the surface layers to 25 cm (4.48 ± 0.08). Then, the high content of Corg found in cropping systems study corroborates the assertion of those authors.

The highest average of Carbon stock was found in the cultivation system S2 (Table 2), where was found the highest granulometric average, especially the clay and Ds. In descending order, the cultivation system S1 has the second highest average. In the cultivation systems S3 and S4 the average of carbon stock decreases, although the clay content is approximate to that contained in the cropping system S1. However the content of sand has an average ranging from 800 to 840 g/kg, and the variation in average clay content is between 90 and 96 g/kg (Table 1). This may be one explanation for the carbon stocks present a decrease in average of these treatments compared in the cropping system S2 (Table 2).

**DPT**: Depths; **Corg**: carbon organic; **Cs**: Carbon stock.

Table 3. Values pH (H2O), tenors of carbon organic (Corg in g/kg) and carbon stocks (Mg C.ha-1).

Fertility, Microbial Biomass and Edaphic

Tramontina Belém S/A. Aurora do Pará.

**3.3 Microbiological attributes**

content.

Fauna Under Forestry and Agroforestry Systems in the Eastern Amazon 241

Fig. 3. Grouping of physical and chemical attributes of the cropping systems studied. Farm

The average content of microbial biomass carbon (CBM) (Figure 4) and the values of the microbial quotient (qMIC) (Figure 5) were higher in the system S4 and S5. In the system S4 the soil was covered with coarse vegetable waste, besides presenting a spontaneous vegetable regeneration between the lines of planting paricá such factors may have favored the maintenance of microorganisms in the soil and therefore increase the microbial carbon

#### **3.2 Relation between physical and chemical attributes**

The result of the correlation (r) between the high content of Corg, clay and sand fraction in the cropping system S2, showed an increasing content of Corg in this cropping system (Table 4).

Corg: carbon organic; Ds: Density of soil.

Table 4. Analysis of canonical correlation between the physical and chemical attributes of soil in the cropping systems studied. Farm Tramontina Belém S/A in Aurora do Pará.

Study ever done on the relation Corg versus clay content (TELLES, 2002) explained that high clay content allows the formation of macroaggregates and microaggregates that promote physical protection to the Corg, and avoid rapid decomposition of the same. Correlating this result with what was obtained in our study; it is possible to explain the high content of Corg found in S2 culture system, using the same argument. As for the stock of carbon (Cs) results showed that this stock decreases in relation to the increased depth in cropping systems studied.

The determination of the hierarchical clustering (HCA) revealed a approximated relation between physical and chemical attributes of soil subjected to analysis, because, according to Barreiro & Moita Neto (1998) this suggests a correlation between the variables of this data set. The results (Figure 3) show that there is formation of two groups where in the group A there was a split in the A1 and A2. In this group there was a correlation between the pH - Ds (Group A1), Ds - Silt/Clay (group A2) and Silt/Clay - Corg (group A3).

Another group, silt and clay (group B), confirm that these two variables are heterogeneous with respect to those that make up Group A. These results show that there is variability in the functioning of studied soils in the cropping systems SI, S2, S3 and S4. S3 and S4 are more similar across pH and relation attributes of silt/clay. The cultivation system S1 showed lower similarity with cropping systems S3 and S4 for the same attributes. Thus, one can verify which variables that differentiate the systems studied each other and can interfere or not in the edaphic fauna.

The result of the correlation (r) between the high content of Corg, clay and sand fraction in the cropping system S2, showed an increasing content of Corg in this cropping system

Attributes analyzed Total clay (g/Kg) Sand (g/Kg) Ds (g/cm3) Relation

pH 0.98 (p < 0.05) - 0.98 (p < 0.05) 0.77 (ns) - 0.66 (ns)

Corg (g/kg) 0.81 (ns) - 0.57 (ns) 0.90 (ns) - 0.88 (ns)

Carbon stock (Mg C.ha-1) 0.82 (ns) - 0.75 (ns) 0.86 (ns) - 0.92 (ns)

Table 4. Analysis of canonical correlation between the physical and chemical attributes of soil in the cropping systems studied. Farm Tramontina Belém S/A in Aurora do Pará.

Study ever done on the relation Corg versus clay content (TELLES, 2002) explained that high clay content allows the formation of macroaggregates and microaggregates that promote physical protection to the Corg, and avoid rapid decomposition of the same. Correlating this result with what was obtained in our study; it is possible to explain the high content of Corg found in S2 culture system, using the same argument. As for the stock of carbon (Cs) results showed that this stock decreases in relation to the increased depth in cropping systems

The determination of the hierarchical clustering (HCA) revealed a approximated relation between physical and chemical attributes of soil subjected to analysis, because, according to Barreiro & Moita Neto (1998) this suggests a correlation between the variables of this data set. The results (Figure 3) show that there is formation of two groups where in the group A there was a split in the A1 and A2. In this group there was a correlation between the pH - Ds

Another group, silt and clay (group B), confirm that these two variables are heterogeneous with respect to those that make up Group A. These results show that there is variability in the functioning of studied soils in the cropping systems SI, S2, S3 and S4. S3 and S4 are more similar across pH and relation attributes of silt/clay. The cultivation system S1 showed lower similarity with cropping systems S3 and S4 for the same attributes. Thus, one can verify which variables that differentiate the systems studied each other and can interfere or

(Group A1), Ds - Silt/Clay (group A2) and Silt/Clay - Corg (group A3).

Silt x clay

**3.2 Relation between physical and chemical attributes**

Corg: carbon organic; Ds: Density of soil.

(Table 4).

studied.

not in the edaphic fauna.

Fig. 3. Grouping of physical and chemical attributes of the cropping systems studied. Farm Tramontina Belém S/A. Aurora do Pará.

#### **3.3 Microbiological attributes**

The average content of microbial biomass carbon (CBM) (Figure 4) and the values of the microbial quotient (qMIC) (Figure 5) were higher in the system S4 and S5. In the system S4 the soil was covered with coarse vegetable waste, besides presenting a spontaneous vegetable regeneration between the lines of planting paricá such factors may have favored the maintenance of microorganisms in the soil and therefore increase the microbial carbon content.

Fertility, Microbial Biomass and Edaphic

more similar to those found in capoeira.

components.

correlations stand out CBM qMIC and Ca.

Fauna Under Forestry and Agroforestry Systems in the Eastern Amazon 243

Overall, the results indicate that the incorporation of organic matter is favoring the edaphic conditions and the different systems, especially the S3 and S4 suffering the biggest addition of organic matter, equaling the soils are of capoeira, eventually tending to an equilibrium (OLIVEIRA, 2009; BERNARDES, 2011, PEREIRA Jr, 2011). The Table 5 presents the principal components that shows this relationship. It's possible verify that saturation of bases (V), EC, aluminum saturation (m), Na, and Al were the variables that showed more differences between the systems. In systems S2 and S3, the values of these attributes, in general, are

pH -0,027 0,144 **0,419** 0,195 0,204 Al **-0,273** 0,003 **-0,314** 0,005 -0,016 H+Al **-0,303** 0,075 -0,180 -0,018 0,055 Ca -0,235 **-0,253** -0,160 0,152 -0,059 Mg -**0,294** -0,171 0,119 0,017 -0,008 K **-0,290** -0,180 0,095 -0,047 0,032 P -0,114 **0,371** -0,206 -0,07 0,071 Na **-0,254** 0,042 0,091 **0,458** -0,084 SB **-0,298** -0,182 0,074 0,037 -0,024 CTC ef **-0,312** -0,095 -0,143 0,021 -0,019 CTC pH7 **-0,324** -0,03 -0,086 -0,022 0,022 V% -0,099 **-0,303 0,300** 0,243 -0,063 m% 0,111 -0,176 **0,406 -0,326** -0,064 Cot -0,164 **0,303** 0,231 0,030 -0,199 EC -0,126 **0,308** 0,048 **-0,421** 0,002 NT -0,147 0,153 **0,433** 0,008 -0,161 C/N -0,132 **0,358** -0,086 0,036 -0,123 CBM 0,158 **0,304** -0,018 **0,484** -0,035 NBM -0,065 -0,011 0,064 0,02 **0,908**  *q*MIC **0,279** -0,078 -0,134 **0,366** 0,031

Table 5. Correlation coefficients between original variables of response and principal

correlations for P and COT. The largest negative correlation occurred with the V%.

The principal component 1 (Comp. 1), that explains 54.00% of the variability of the data, presents the highest correlation for the SB, K, Mg, CEC, Ca and H + Al. The largest negative correlations, which also showed low values occurred with the CBM and qMIC. The principal component 2 (Comp. 2) explains 21.9% of the variability and has the highest

The principal component 3 (Comp. 3), that explains 12.2% of the variability, presents the higher correlations for P and Ca, and the largest negative correlations were found for pH and COT. In the case of principal component 4 (Comp. 4) explains 5.2% of the variability and was negatively correlated for almost all attributes except for COT. Among the negative

Comp. 1 Comp. 2 Comp.3 Comp.4 Comp.5

Attributes Principal components

Fig. 4. Values of microbial biomass carbon (CMB) in different production systems.

Fig. 5. Values of microbial quotient (qMIC) in different production systems.

For the attribute qMIC very low values were obtained, except in the S4 system, where it was recorded the highest values of qMIC, especially in the layers of the first depth of soil. Jenkinson & Ladd (1981), considered normal that 1-4% of total soil C corresponds to the microbial component, how the collection was done during the dry season, and it is known that water is an important element for microbial activity, it is possible that low values are justified by this fact.

Fig. 4. Values of microbial biomass carbon (CMB) in different production systems.

Fig. 5. Values of microbial quotient (qMIC) in different production systems.

justified by this fact.

For the attribute qMIC very low values were obtained, except in the S4 system, where it was recorded the highest values of qMIC, especially in the layers of the first depth of soil. Jenkinson & Ladd (1981), considered normal that 1-4% of total soil C corresponds to the microbial component, how the collection was done during the dry season, and it is known that water is an important element for microbial activity, it is possible that low values are

**Production Systems**

Overall, the results indicate that the incorporation of organic matter is favoring the edaphic conditions and the different systems, especially the S3 and S4 suffering the biggest addition of organic matter, equaling the soils are of capoeira, eventually tending to an equilibrium (OLIVEIRA, 2009; BERNARDES, 2011, PEREIRA Jr, 2011). The Table 5 presents the principal components that shows this relationship. It's possible verify that saturation of bases (V), EC, aluminum saturation (m), Na, and Al were the variables that showed more differences between the systems. In systems S2 and S3, the values of these attributes, in general, are more similar to those found in capoeira.

Table 5. Correlation coefficients between original variables of response and principal components.

The principal component 1 (Comp. 1), that explains 54.00% of the variability of the data, presents the highest correlation for the SB, K, Mg, CEC, Ca and H + Al. The largest negative correlations, which also showed low values occurred with the CBM and qMIC. The principal component 2 (Comp. 2) explains 21.9% of the variability and has the highest correlations for P and COT. The largest negative correlation occurred with the V%.

The principal component 3 (Comp. 3), that explains 12.2% of the variability, presents the higher correlations for P and Ca, and the largest negative correlations were found for pH and COT. In the case of principal component 4 (Comp. 4) explains 5.2% of the variability and was negatively correlated for almost all attributes except for COT. Among the negative correlations stand out CBM qMIC and Ca.

Fertility, Microbial Biomass and Edaphic

substances (Correia; Aquino, 2005).

and other soil organisms (Folgarait, 1998).

Aurora do Pará

obtained in studies in savannas of Pará (Franklin et al., 2007).

monocultivation) as well as in other culture systems studied (Table 7).

numbers, but these factors were not analyzed in this study.

Fauna Under Forestry and Agroforestry Systems in the Eastern Amazon 245

influences the physical nature of the soil changing porosity, moisture and transport of

The order Acari is a grouping of vertical habitat in three levels, euedaphics, hemiedaphics and epiedaphics, and the epiedaphics are more tolerant to desiccation (Lavelle & Spain, 2001), although there is low frequency of individuals, it is higher when compared with those

Ants have been widely used as biodindicadores in various types of impacts, such as recovery after mining activities, industrial pollution, agricultural practices and other land uses (Smith et al, 2009). In addition, the class Insecta, which belongs to the ant, often grouped according to trophic groups, and the availability of nutrients in the ecosystem (Leivas & Chips, 2008). They are important in below-ground processes, by altering the physical and chemical properties and the environment, its effects on plants, microorganisms

These may be the possible explanations for the faunistic results of this taxons (Hymenopetera) Family Formicidae, with the highest absolute frequency (Fi) in the cropping system S1 (curauá in monocultivation) and lower absolute frequency in the cropping system S4 (paricá in

Adult and immature Coleoptera, Collembola, Diplopoda, Diptera and Homoptera adults had higher absolute frequency in the cropping system S3 (paricá + mogno + freijó + curauá) (Table 7). This may show a variety nutritional or of habitat, or still an increase in the prey predator relation. The same was not found in the monocultivation systems for these taxons. Macroarthropods of soil has an important role in tropical terrestrial ecosystems, exerting a direct influence on the formation and stability, an indirect influence on the decomposition process through strong participation in the fragmentation of necromass (ARAUJO; BANDEIRA; VANSCONCELOS, 2010). Work already carried out in terra firma forest ecosystems in the state of Pará, also found the presence of Hymenoptera, Coleoptera, Collembola, Homoptera, Acari and Diplopoda, grouped or not (Macambira, 2005; & Garden Macambira, 2007; Ruivo et al. 2007 ), which corroborates with the edaphic fauna found in

The greatest diversity of species occurred at S3 (Table 7), this can be attributed, among other factors, the variety of nutrients, because S3 is an agroforestry system where there is occurrence of paricá, mogno, freijó and curauá. In addition, there may be no natural predators of these species or still the ephemeral life cycle leads to a reproduction in greater

The lowest levels of the Shannon-Wiener diversity, therefore the greater species diversity occurred in the cropping system S1 (curauá in monocultivation) and S2 (agroforestry system paricá + curauá). This may be due to movement of other species of invertebrates through of ecotones that over there exist. It is possible that this displacement has occurred in search of food or place to reproduction, or even to escape from possible predators in areas near to these cultivation systems. It should not be ruled out the hypothesis that the curauá produces some substance that is palatable to invertebrate species diversity and this is a nutritional

#### **3.4 Edaphic fauna of the forestry system and agroforestry**

The faunistic analysis performed on the Farm Tramontina Belém S/A, recorded 2.568 specimens distributed in eighteen (18) taxon of invertebrate and one (01) taxon of vertebrate of the Order Squamata (Gekkonidae) (Table 6) in five culture systems studied, where the prevailing order was Hymenoptera, composed mainly by family Formicidae with 2.151 individuals followed by Coleoptera (78), Collembola (40), Homoptera (67) and Diplopoda (74).

Ordination of taxons second Brusca & Brusca, 2007.

Table 6. Taxons identified, absolute frequency (Fi), relative frequency (Fr) and average of individuals in the cropping systems studied in the Farm Tramontina Belém S/A in Aurora do Pará.

The Diplopoda taxon is present in all treatments, but the highest concentration is in the systems of monocultivation (S1 and S4). In a study of community of invertebrates in litter in agroforestry systems, this order was the second most important (Barros et al., 2006). This importance is due to mobility that they present in the soil, surface and underground, which

The faunistic analysis performed on the Farm Tramontina Belém S/A, recorded 2.568 specimens distributed in eighteen (18) taxon of invertebrate and one (01) taxon of vertebrate of the Order Squamata (Gekkonidae) (Table 6) in five culture systems studied, where the prevailing order was Hymenoptera, composed mainly by family Formicidae with 2.151 individuals followed by Coleoptera (78), Collembola (40), Homoptera (67) and

SYSTEMS

TAXONS Fi Total Fr (%) (Mean)

Hymenoptera (Formicidae) 808 667 416 260 2.151 82,82 537,75 Coleoptera 21 15 27 15 78 3.0 19,5 Collembola 6,0 11 21 2,0 40 1.54 9.75 Diptera 13 1,0 11 5,0 30 1.15 7,50 Hemiptera 0,0 1,0 0,0 0,0 01 0.03 0,25 Homoptera 9,0 10 34 14 67 2.57 16,75 Blattariae 0,0 2,0 0,0 2,0 04 0.15 1,00 Odonata 0,0 0,0 1,0 0,0 01 0.03 0,25 Orthoptera 2,0 3,0 5,0 12 22 0.84 5,50 Psocoptera 1,0 0,0 3,0 3,0 07 0.26 1,75 Lepdoptera 0,0 28 0,0 0,0 28 1.07 7,00 Thysanoptera 0,0 0,0 1,0 0,0 01 0.03 0,25

Acari 8,0 28 14 5,0 55 2.11 13,75 Aranae 3,0 2,0 4,0 6,0 15 0.57 3,75 Opilionida 4,0 3,0 7,0 0,0 14 0.53 3,50

Isopoda 0,0 1,0 0,0 0,0 01 0.03 0,25

Chilopoda 1,0 0,0 1,0 0,0 02 0.07 0,50 Diplopoda 17 12 15 30 74 2.84 18,5

Gekkonidae 1,0 3,0 3,0 1,0 08 0.30 1,25

Table 6. Taxons identified, absolute frequency (Fi), relative frequency (Fr) and average of individuals in the cropping systems studied in the Farm Tramontina Belém S/A in Aurora

The Diplopoda taxon is present in all treatments, but the highest concentration is in the systems of monocultivation (S1 and S4). In a study of community of invertebrates in litter in agroforestry systems, this order was the second most important (Barros et al., 2006). This importance is due to mobility that they present in the soil, surface and underground, which

Total 894 785 563 355 2.597 100

Ordination of taxons second Brusca & Brusca, 2007.

**3.4 Edaphic fauna of the forestry system and agroforestry**

S1 S2 S3 S4

Diplopoda (74).

**INSECTA**

**ARACHNIDA**

**CRUSTACEA**

**MYRIAPODA**

**SQUAMATA**

do Pará.

influences the physical nature of the soil changing porosity, moisture and transport of substances (Correia; Aquino, 2005).

The order Acari is a grouping of vertical habitat in three levels, euedaphics, hemiedaphics and epiedaphics, and the epiedaphics are more tolerant to desiccation (Lavelle & Spain, 2001), although there is low frequency of individuals, it is higher when compared with those obtained in studies in savannas of Pará (Franklin et al., 2007).

Ants have been widely used as biodindicadores in various types of impacts, such as recovery after mining activities, industrial pollution, agricultural practices and other land uses (Smith et al, 2009). In addition, the class Insecta, which belongs to the ant, often grouped according to trophic groups, and the availability of nutrients in the ecosystem (Leivas & Chips, 2008). They are important in below-ground processes, by altering the physical and chemical properties and the environment, its effects on plants, microorganisms and other soil organisms (Folgarait, 1998).

These may be the possible explanations for the faunistic results of this taxons (Hymenopetera) Family Formicidae, with the highest absolute frequency (Fi) in the cropping system S1 (curauá in monocultivation) and lower absolute frequency in the cropping system S4 (paricá in monocultivation) as well as in other culture systems studied (Table 7).

Adult and immature Coleoptera, Collembola, Diplopoda, Diptera and Homoptera adults had higher absolute frequency in the cropping system S3 (paricá + mogno + freijó + curauá) (Table 7). This may show a variety nutritional or of habitat, or still an increase in the prey predator relation. The same was not found in the monocultivation systems for these taxons.

Macroarthropods of soil has an important role in tropical terrestrial ecosystems, exerting a direct influence on the formation and stability, an indirect influence on the decomposition process through strong participation in the fragmentation of necromass (ARAUJO; BANDEIRA; VANSCONCELOS, 2010). Work already carried out in terra firma forest ecosystems in the state of Pará, also found the presence of Hymenoptera, Coleoptera, Collembola, Homoptera, Acari and Diplopoda, grouped or not (Macambira, 2005; & Garden Macambira, 2007; Ruivo et al. 2007 ), which corroborates with the edaphic fauna found in Aurora do Pará

The greatest diversity of species occurred at S3 (Table 7), this can be attributed, among other factors, the variety of nutrients, because S3 is an agroforestry system where there is occurrence of paricá, mogno, freijó and curauá. In addition, there may be no natural predators of these species or still the ephemeral life cycle leads to a reproduction in greater numbers, but these factors were not analyzed in this study.

The lowest levels of the Shannon-Wiener diversity, therefore the greater species diversity occurred in the cropping system S1 (curauá in monocultivation) and S2 (agroforestry system paricá + curauá). This may be due to movement of other species of invertebrates through of ecotones that over there exist. It is possible that this displacement has occurred in search of food or place to reproduction, or even to escape from possible predators in areas near to these cultivation systems. It should not be ruled out the hypothesis that the curauá produces some substance that is palatable to invertebrate species diversity and this is a nutritional

Fertility, Microbial Biomass and Edaphic

Fauna Under Forestry and Agroforestry Systems in the Eastern Amazon 247

Fig. 6. Grouping between edaphic fauna of greater absolute frequency in the studied treatments, physical and chemical attributes of soil. Campo Experimental of the Tramontina Belém S/A. Corg = carbon organic; S/A = relation silt/clay, Ho = Homoptera; CoA = Coleoptera adult; dipl = Diplopoda; CoI = immature Coleoptera, Coll = Collembola; dipti =

The results showed that (I) the immature Coleoptera taxon has high similarity to the taxon Collembola and constitutes the group 1; (II) the taxon Diptera presents similarity to the taxon Orthoptera and constitute the second group. The group 2 has similarity with group 1, (III) the taxon Acari presents similarities with groups 1 and 2, constituting the third group, (IV) the taxon Coleoptera adult presents similarity to the taxon Diplopoda, constituting the group 4. (V) Groups 1, 2 and 3, have similarity to group 4. (VI) the taxon Homoptera has similarity as group 4, thus constituting the group 5. (VII) Groups 1, 2, 3, 4 and 5 they correlate with the physical attributes (Ds, relation silt/clay), but did not correlate

The taxon Hymenoptera showed that is not correlated with the physical attributes: Ds and relation silt/clay, and neither with chemical attributes: pH and Corg. Also has no similarity to other taxons analyzed. But it is possible that other edaphic variables correlate with this

Ants have been widely used as biodindicadores in various types of impacts, such as recovery after mining activities, industrial pollution, agricultural practices and other land uses (Smith et al, 2009). In addition, the class Insecta, which belongs to the ant, often grouped according to trophic groups, and the availability of nutrients in the ecosystem (Leivas & Chips, 2008). They are important in below-ground processes, by altering the physical and chemical properties and the environment, its effects on plants, microorganisms

Diptera; Orth = Orthoptera; Acr = Acari; Hy = Hymenoptera.

with the chemical attributes (pH, Corg).

and other soil organisms (Folgarait, 1998).

taxon, but these were not objects of the present study.

option for them because this plant is present in both cropping systems that had the lowest diversity indices of Shannon -Wiener.

Table 7. Diversity index Shannon-Wiener (H') and population density found in cropping systems studied at Fazenda Tramontina Belém S/A in Aurora do Pará.

The highest indexes of diversity of Shannon-Wiener occurred in cropping systems S3 (parica + magno + freijó + curauá) and S4 (parica in monocultivation). This shows lower diversity of species, although in S3 there is differents plant species, which would cause nutritionals offerings and different habitats, and this would promote greater diversity of species. Study performed about plant diversity and productivity of plants and the effects on the abundance of arthropods (Perna et al, 2005) showed that productivity in the plant structure, local abiotic conditions, physical disorders of the habitats are factors that interact with the diversity of plants and which also influences the abundance of arthropods. This can be an explanation for the low diversity found in the cropping system S3 in our study.

In S4, occurs monocultivation with paricá. This features a lower nutritional diversity and of habitats, which in turn attracts lower diversity of macrofauna, especially ants. Suggest the hypothesis that this plant produces some substance not palatable or that act on the reproductive cycle in the majority of taxons identified. It is also possible that there are a greater number of predators in relation to other systems cultivation studied, or even occurred edaphic variations that did not allow the diversity of species and greater population density because this cropping system, the highest number of absence (seven taxons) among the eighteen taxons identified (Table 6). When the population density, the highest concentration indivíduos/m2, occurs in S1, where there is a monocultivation of curauá. As this culture system does not present sub-forest for vegetal cover and shading that would mitigate the temperature at the soil surface, it is possible that the solar radiation incident directly on the ground promotes an increase in photosynthetic rate, increasing the supply of nutrients, as well as raises the temperature of the same and is one of the factors that contribute to the reproduction of these ants (Harada & Banner, 1994, Oliveira et al., 2009). But do not dismiss as a possible explanation for the results obtained in two cropping systems, the hypotesis of correlated interferences, for example, environmental variables, ephemeral life cycle, presence or absence of predators, temperature, precipitation, brightness, among other variables in this study were not analyzed.

#### **3.5 Edaphic fauna and attributes of soil**

The relation between edaphic fauna and soil attributes (pH, Corg, Ds, relation silt/clay) is shown in Figure 6.

option for them because this plant is present in both cropping systems that had the lowest

Diversity index (H') 0,22 0,26 0,51 0,48 Population density (individuals/m2) 0,69 0,58 0,43 0,26

The highest indexes of diversity of Shannon-Wiener occurred in cropping systems S3 (parica + magno + freijó + curauá) and S4 (parica in monocultivation). This shows lower diversity of species, although in S3 there is differents plant species, which would cause nutritionals offerings and different habitats, and this would promote greater diversity of species. Study performed about plant diversity and productivity of plants and the effects on the abundance of arthropods (Perna et al, 2005) showed that productivity in the plant structure, local abiotic conditions, physical disorders of the habitats are factors that interact with the diversity of plants and which also influences the abundance of arthropods. This can be an explanation for the low diversity found in the cropping system

In S4, occurs monocultivation with paricá. This features a lower nutritional diversity and of habitats, which in turn attracts lower diversity of macrofauna, especially ants. Suggest the hypothesis that this plant produces some substance not palatable or that act on the reproductive cycle in the majority of taxons identified. It is also possible that there are a greater number of predators in relation to other systems cultivation studied, or even occurred edaphic variations that did not allow the diversity of species and greater population density because this cropping system, the highest number of absence (seven taxons) among the eighteen taxons identified (Table 6). When the population density, the highest concentration indivíduos/m2, occurs in S1, where there is a monocultivation of curauá. As this culture system does not present sub-forest for vegetal cover and shading that would mitigate the temperature at the soil surface, it is possible that the solar radiation incident directly on the ground promotes an increase in photosynthetic rate, increasing the supply of nutrients, as well as raises the temperature of the same and is one of the factors that contribute to the reproduction of these ants (Harada & Banner, 1994, Oliveira et al., 2009). But do not dismiss as a possible explanation for the results obtained in two cropping systems, the hypotesis of correlated interferences, for example, environmental variables, ephemeral life cycle, presence or absence of predators, temperature, precipitation,

The relation between edaphic fauna and soil attributes (pH, Corg, Ds, relation silt/clay) is

Table 7. Diversity index Shannon-Wiener (H') and population density found in cropping

systems studied at Fazenda Tramontina Belém S/A in Aurora do Pará.

brightness, among other variables in this study were not analyzed.

**3.5 Edaphic fauna and attributes of soil**

shown in Figure 6.

**Systems** S1 S2 S3 S4

diversity indices of Shannon -Wiener.

S3 in our study.

Fig. 6. Grouping between edaphic fauna of greater absolute frequency in the studied treatments, physical and chemical attributes of soil. Campo Experimental of the Tramontina Belém S/A. Corg = carbon organic; S/A = relation silt/clay, Ho = Homoptera; CoA = Coleoptera adult; dipl = Diplopoda; CoI = immature Coleoptera, Coll = Collembola; dipti = Diptera; Orth = Orthoptera; Acr = Acari; Hy = Hymenoptera.

The results showed that (I) the immature Coleoptera taxon has high similarity to the taxon Collembola and constitutes the group 1; (II) the taxon Diptera presents similarity to the taxon Orthoptera and constitute the second group. The group 2 has similarity with group 1, (III) the taxon Acari presents similarities with groups 1 and 2, constituting the third group, (IV) the taxon Coleoptera adult presents similarity to the taxon Diplopoda, constituting the group 4. (V) Groups 1, 2 and 3, have similarity to group 4. (VI) the taxon Homoptera has similarity as group 4, thus constituting the group 5. (VII) Groups 1, 2, 3, 4 and 5 they correlate with the physical attributes (Ds, relation silt/clay), but did not correlate with the chemical attributes (pH, Corg).

The taxon Hymenoptera showed that is not correlated with the physical attributes: Ds and relation silt/clay, and neither with chemical attributes: pH and Corg. Also has no similarity to other taxons analyzed. But it is possible that other edaphic variables correlate with this taxon, but these were not objects of the present study.

Ants have been widely used as biodindicadores in various types of impacts, such as recovery after mining activities, industrial pollution, agricultural practices and other land uses (Smith et al, 2009). In addition, the class Insecta, which belongs to the ant, often grouped according to trophic groups, and the availability of nutrients in the ecosystem (Leivas & Chips, 2008). They are important in below-ground processes, by altering the physical and chemical properties and the environment, its effects on plants, microorganisms and other soil organisms (Folgarait, 1998).

Fertility, Microbial Biomass and Edaphic

a potential in carbon sequestration.

**5. Acknowledgements**

395, 1993.

2006. p.43 – 55.

Gráficas, 1969, 653 p.

NAEA/UFPA, 1999. 50 p

cultivo. Disponível em:

Acesso em 26 out. 2009.

cultivo. R. Bras. Ci. Agrárias. 5:49 – 53, 2010

for this project.

**6. References**

Fauna Under Forestry and Agroforestry Systems in the Eastern Amazon 249

internationally. Its rapid growth and adaptation to areas with low nutrient levels allow it to be optimum in agroforestry, being the second plant species used in reforestation in the Para state , and primarily designed for industry of lams rolled. Thus, it is necessary to intensify studies of the seasonal variation of soil attributes, the variables listed as indicators of soil quality and enhance studies in certain management practices such as tillage and the SAF as

To INCT/ CNPQ-MPEG and Projetc FAPESPA/MPEG No. 126/2008 by financial support

Anderson, J. P. E. & K. H. Domsch. The metabolic quocient (*q*CO2) as specific activity

Aquino, A.M; Aguiar-Menezes, E.L; DE Queiroz, J.M. Recomendações para coleta de

Barreta, D; Ferreira, C.S; Souza, J.P; Cardoso, E.J.B.N. Colêmbolos (hexapoda: Collembola)

Barros, E; Mathieu, J; Tapia-Coral, S; Nascimento, A.R. L; Lavelle, P. Soil macrofauna

Borror, D.J; Delong, D.M. Introdução ao estudo dos insetos. Rio de Janeiro, Indústrias

Cordeiro, I M C. C. Performance diferencial de crescimento da espécie *Schizolobium*

Cordeiro, I.M.C. C; De Barros, P.L. C; Ferreira, G.C e Filho, A.D.G. Influência da radiação e

http://www22.sede.embrapa.br/snt/viicbsaf/cdanais/tema01/01tema39.pdf>.

Cordeiro, I.M.C. C; Lameira, O.A; Barros, P.LC; Malheiros, M.A.M. Comportamento do

Cordeiro, I.M.C. C; Santana, C; Lameira, O.A; Silva, L.M. Análise econômica dos sistemas de

Brasileira de Pesquisa Agropecuária. 18:1-8, 2006.

Estatística, 2011 (www.ibge.gov.br)

parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biology and Biochemistry, v. 25, n. 3, p. 393-

artrópodes terrestres por armadilhas de queda (pitffal-traps). Seropédica: Empresa

como bioindicadores da qualidade do solo em áreas com *Araucaria angustifólia*. R.Bras.Ci. Solo, 32: 2633-2699, 2008. IBGE, Instituto Brasileiro de Geografia e

communities in Brazilian Amazonia. In: Moreira, F.M.S; Siqueira, J.O; Bursaard, L. Soil biodiversity in Amazonian and other Brazilian ecosystems. CABI Publishing,

*amazonicum* Huber (Paricá) em sítios degradados sob diferentes regimes de preparação de área na micro região do Guamá. Aurora do Pará. Apresentado originalmente como monografia de especialização. Universidade Federal do Para.

precipitação no incremento diamétrico de Paricá de diferentes idades e sistemas de

Curauá sob diferentes níveis de radiação fotossinteticamente ativa em condições de

cultivo com *Schizolobium parahyba var. amazonicum* (Huber ex Ducke) Barneby

These may be the possible explanations for the faunistic results of this taxons (Hymenopetera) Family Formicidae, with the highest absolute frequency (Fi) in the cropping system S1 (curauá in monocultivation) and lower absolute frequency in the cropping system S4 (paricá in monocultivation).

The order Acari has the major absolute frequency in S2 (Table 3), maybe has better adaptability to the SAF, and the physical attributes shown in Figure 5, which may also is occurring with Homoptera, Collembola and Coleoptera immature. Even in this agroforestry system, the absolute frequency of the taxon Coleoptera, Hymenoptera and the population density decreases, according to data contained in Table 4. This may be related to the increase of soil density and decrease in the silt/clay relation contained in Table 2.

With the modifications imposed by use of soil, particularly by agriculture, the fauna and the microorganisms, in different degrees of intensity, are affected by the impacts caused by agricultural practices, that may alter the composition and diversity of soil organisms.

The addition of new organic matter through the incorporation of waste or the maintenance of forest cover (using the agroforestry system, with or without burning the area) or even a diversified system (as occur in Aurora do Pará), show the importance of maintenance, incorporation and slow decomposition of organic matter on the ground.

So far, the studies show that the types of management adopted did not influence negatively the characteristics of soil and that adding of diversified organic matter in the soil, the retention and incorpration and slow decomposition of these residues led to the creation of an edaph-environment favorable to the maintaining soil quality.

The set of attributes of the soils here studied, especially those related to microbial biomass and chemistry, was adequate to indicate the quality of the substrate. However, the continuation of this kind of work, in the long term, it is necessary, in order to identify differences in biological characteristics of soil between the different management systems, especially taking into account the local climatic variation. Thus, it is necessary to intensify studies of the seasonal variation of soil attributes, the variables listed as indicators of soil quality and intensify the studies in determinated practices of management, such as the tillage and the SAF as potential in the carbon sequestration.

## **4. Conclusions**

The result show that the types of management adopted did not influence negatively the characteristics of soil and adding organic matter to the diverse soil, retention and development and slow decomposition of these residues led to the creation of an edafoambiente of maintaining soil quality. The set of attributes of the soil studied here, especially those related to microbial biomass and chemistry, was adequate to indicate the quality of the substrate. However, the continuation of such work in the long term and different climatic conditions, it is necessary, in order to identify differences in biological characteristics under different soil management systems, especially taking into account the local climatic variation.

The Paricá (*Schizolobium amazonicum* Huber (Ducke)) is a viable native species for recuperation of disturbed areas and with detach in the wood market, nationally and internationally. Its rapid growth and adaptation to areas with low nutrient levels allow it to be optimum in agroforestry, being the second plant species used in reforestation in the Para state , and primarily designed for industry of lams rolled. Thus, it is necessary to intensify studies of the seasonal variation of soil attributes, the variables listed as indicators of soil quality and enhance studies in certain management practices such as tillage and the SAF as a potential in carbon sequestration.

### **5. Acknowledgements**

To INCT/ CNPQ-MPEG and Projetc FAPESPA/MPEG No. 126/2008 by financial support for this project.

## **6. References**

248 Forest Ecosystems – More than Just Trees

These may be the possible explanations for the faunistic results of this taxons (Hymenopetera) Family Formicidae, with the highest absolute frequency (Fi) in the cropping system S1 (curauá in monocultivation) and lower absolute frequency in the

The order Acari has the major absolute frequency in S2 (Table 3), maybe has better adaptability to the SAF, and the physical attributes shown in Figure 5, which may also is occurring with Homoptera, Collembola and Coleoptera immature. Even in this agroforestry system, the absolute frequency of the taxon Coleoptera, Hymenoptera and the population density decreases, according to data contained in Table 4. This may be related to the increase

With the modifications imposed by use of soil, particularly by agriculture, the fauna and the microorganisms, in different degrees of intensity, are affected by the impacts caused by

The addition of new organic matter through the incorporation of waste or the maintenance of forest cover (using the agroforestry system, with or without burning the area) or even a diversified system (as occur in Aurora do Pará), show the importance of maintenance,

So far, the studies show that the types of management adopted did not influence negatively the characteristics of soil and that adding of diversified organic matter in the soil, the retention and incorpration and slow decomposition of these residues led to the creation of

The set of attributes of the soils here studied, especially those related to microbial biomass and chemistry, was adequate to indicate the quality of the substrate. However, the continuation of this kind of work, in the long term, it is necessary, in order to identify differences in biological characteristics of soil between the different management systems, especially taking into account the local climatic variation. Thus, it is necessary to intensify studies of the seasonal variation of soil attributes, the variables listed as indicators of soil quality and intensify the studies in determinated practices of management, such as the

The result show that the types of management adopted did not influence negatively the characteristics of soil and adding organic matter to the diverse soil, retention and development and slow decomposition of these residues led to the creation of an edafoambiente of maintaining soil quality. The set of attributes of the soil studied here, especially those related to microbial biomass and chemistry, was adequate to indicate the quality of the substrate. However, the continuation of such work in the long term and different climatic conditions, it is necessary, in order to identify differences in biological characteristics under different soil management systems, especially taking into account the

The Paricá (*Schizolobium amazonicum* Huber (Ducke)) is a viable native species for recuperation of disturbed areas and with detach in the wood market, nationally and

agricultural practices, that may alter the composition and diversity of soil organisms.

of soil density and decrease in the silt/clay relation contained in Table 2.

incorporation and slow decomposition of organic matter on the ground.

an edaph-environment favorable to the maintaining soil quality.

tillage and the SAF as potential in the carbon sequestration.

**4. Conclusions**

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**11**

*2Japan*

**Plant Productivity is Temporally**

*Academy of Sciences of Czech Republic, České Budějovice*

Ayu Toyota1,2,\* and Nobuhiro Kaneko2 *1Institute of Soil Biology, Biology Centre,*

*Yokohama National University,Yokohama \*1Czech Republic*

*2Soil Ecology Research Group,*

**Enhanced by Soil Fauna Depending on**

**the Life Stage and Abundance of Animals**

In terrestrial ecosystems, nutrient recycling is driven by the belowground decomposition process because it supplies most of the production to the soil system (Swift *et al*. 1979; Cebrian 1999). Soil links the aboveground plants and the belowground community (Wardle, 2002). Soil nutrient cycling is controlled by interactions among living soil organisms, plant litter quality, soil physical and chemical status, temperature, and water condition. In soil-organism processes, large soil animals rapidly change microbial activity (Hanlon and Anderson 1980) and the litter decomposition rate (Bonkowski *et al*. 1998) and modify soil structure (Barois *et al*. 1993). Consequently, primary decomposition and plant growth are affected not only by microbes but also by soil animals (Wall and Moore 1999; Wardle 2002). The overall faunal contribution to nitrogen (N) mobilization has been estimated as approximately 30% in forest ecosystems (Verhoef and Brussaard 1990). Schröter *et al*. (2003) calculated that the total amount of N mineralized by fauna in European coniferous forests ranged from 11 kg N ha-1 a-1 in northern Sweden to 73 kg N

The presence of keystone species strongly affects decomposition and nutrient dynamics. In particular, the train millipede *Parafontaria laminata* is widely dominant in soil invertebrate communities of central Japan, with its late-stage (from the 6th to final instar) larvae enhancing N availability by 69% (Toyota *et al*. in press). The enhancement of soil N availability in forest soils by late-stage larvae of this millipede can lead to changes in aboveground plant productivity. Earthworm casts stimulate the growth of most plant species in grassland soil (Zaller and Arnone 1999), but whether soil animals alter plant

productivity under natural conditions in forest soils remains poorly understood.

**1. Introduction**

ha-1 a-1 in Germany.

\*Correspondence Author

## **Plant Productivity is Temporally Enhanced by Soil Fauna Depending on the Life Stage and Abundance of Animals**

Ayu Toyota1,2,\* and Nobuhiro Kaneko2

*1Institute of Soil Biology, Biology Centre, Academy of Sciences of Czech Republic, České Budějovice 2Soil Ecology Research Group, Yokohama National University,Yokohama \*1Czech Republic 2Japan*

#### **1. Introduction**

252 Forest Ecosystems – More than Just Trees

Telles, E.C.C. Dinâmica do carbono no solo influenciado pela textura, drenagem,

Thornthwaite, C.W. An approach towards a rational classification of climate. Geographical

Vance, E.D.; Brookes, P.C.; Jenkinson, D.S. An extraction method for measuring soil

microbial biomass C. Soil Biol. Biochem., v.19, p.703-707, 1987.

Agricultura, Universidade de São Paulo.

Review, London, v.38,p.55-94, 1948.

mineralogia e carvões em florestas primárias na região centro-oriental da Amazônia. Piracicaba. 2002. 92 p. Tese (Doutorado) - Centro de Energia Nuclear na

> In terrestrial ecosystems, nutrient recycling is driven by the belowground decomposition process because it supplies most of the production to the soil system (Swift *et al*. 1979; Cebrian 1999). Soil links the aboveground plants and the belowground community (Wardle, 2002). Soil nutrient cycling is controlled by interactions among living soil organisms, plant litter quality, soil physical and chemical status, temperature, and water condition. In soil-organism processes, large soil animals rapidly change microbial activity (Hanlon and Anderson 1980) and the litter decomposition rate (Bonkowski *et al*. 1998) and modify soil structure (Barois *et al*. 1993). Consequently, primary decomposition and plant growth are affected not only by microbes but also by soil animals (Wall and Moore 1999; Wardle 2002). The overall faunal contribution to nitrogen (N) mobilization has been estimated as approximately 30% in forest ecosystems (Verhoef and Brussaard 1990). Schröter *et al*. (2003) calculated that the total amount of N mineralized by fauna in European coniferous forests ranged from 11 kg N ha-1 a-1 in northern Sweden to 73 kg N ha-1 a-1 in Germany.

> The presence of keystone species strongly affects decomposition and nutrient dynamics. In particular, the train millipede *Parafontaria laminata* is widely dominant in soil invertebrate communities of central Japan, with its late-stage (from the 6th to final instar) larvae enhancing N availability by 69% (Toyota *et al*. in press). The enhancement of soil N availability in forest soils by late-stage larvae of this millipede can lead to changes in aboveground plant productivity. Earthworm casts stimulate the growth of most plant species in grassland soil (Zaller and Arnone 1999), but whether soil animals alter plant productivity under natural conditions in forest soils remains poorly understood.

\*Correspondence Author

Plant Productivity is Temporally Enhanced by

forests in Japan.

Soil Fauna Depending on the Life Stage and Abundance of Animals 255

after adult death, the millipede decomposition increases herbaceous annual plant production and leaf P content. Specifically, we examined the effects of the millipedes on the productivity of annual dwarf bamboo, which dominates the undergrowth of temperate

**(a)**

**(c)**

**(b)**

Fig. 1. The train millipede, *P*. *laminata*, in the soil as (a) a 6th-instar larva, (b) 7th-instar larvae,

and (c) on the forest floor as an adult.

Previous studies on the effects of soil fauna on plant production have mainly been laboratory microcosm experiments, and they have produced mixed conclusions (Brown *et al*. 1999; Scheu 2003). Some studies found that soil animals increase plant production and nutrient utilization (*e*.*g*., Setälä and Huhta 1991; Bardgett and Chan 1999), while others reported redundant or negative impacts of soil animals. One possible reason for this discrepancy is that soil animals have different effects on soil nutrient dynamics depend on their feeding type (Lavelle *et al*. 1997). Another possible reason is that differences in soil chemical composition and organic matter input to soil lead to changes in soil animal effects (Tiunov and Scheu 2004).

The rates of nutrient cycling are usually not constant, even in a mature forest ecosystem, due to the effects of processes such as seed masting (Selås *et al*. 2002) and periodic insect outbreaks. The 17-year periodic appearance of cicadas in North America provides a nutrient pulse to the forest soil resulting from the mass of carcasses, in turn increasing foliage N content and seed mass (Yang 2004). Despite these temporal differences in nutrient dynamics, many studies assume links between plant growth and decomposition processes on a forest floor in the short-term.

Populations of *P*. *laminata* have a synchronized life cycle and undergo simultaneous molts at particular stages according to seasonal temperature rhythms (Fujiyama 1996). The larvae live in the soil for 7 years (Fig. 1a, b) before they reach the adult stage (Fig. 1c). Their population consists of only a single age cohort, so adult swarming is observed at 8-year intervals (Niijima and Shinohara 1988). The huge abundance and synchronized cohort of *P*. *laminata* provide a good opportunity to investigate the soil-animal contributions to nutrient dynamics at the forest floor (Hashimoto *et al*. 2004; Toyota *et al*. 2006). Due to their heterogeneous abundance within the same region in forest soil, the effects of *P*. *laminata* on plants can be distinguished, even under field conditions.

The train millipede *P*. *laminata* can enhance plant production in two major ways. First, changes in soil N availability through millipede activity affect plant production. Latestage larvae enhance N mineralization in soil when millipede abundance is high (Toyota *et al*. in press). By contrast, adults contribute to transforming plant litter into soil, but do not increase N availability in the adult phase. Due to differences in soil N dynamics with developmental stage, the larvae and adults may affect plant productivity differently. Second, carcasses of adults contain higher concentrations of available phosphorus (P) for plant (Toyota, unpublished data). Since forest production is usually limited by P availability in soil (*e*.*g*., Crews *et al*. 1995; Vitousek and Farrington 1997), the P supplied from their carcasses to the forest floor after the death of adults will result in increased plant production and changes in leaf quality.

Here, we studied how aboveground production can be affected by soil animal abundance and developmental stage. Effects of the train millipede were estimated to compare production between natural low-abundance and high-abundance millipede plots in the field. To test whether they temporally have different effects from late stage larvae to after the death of adults, the periods examined for estimating plant productivity were the 2 years before and after the adult active year, over a total of 5 years. Annual herbaceous plants should detect such temporal effects easily. In this paper, we tested the following two predictions: late stage larvae enhance leaf N content and production in the herb layer, and

Previous studies on the effects of soil fauna on plant production have mainly been laboratory microcosm experiments, and they have produced mixed conclusions (Brown *et al*. 1999; Scheu 2003). Some studies found that soil animals increase plant production and nutrient utilization (*e*.*g*., Setälä and Huhta 1991; Bardgett and Chan 1999), while others reported redundant or negative impacts of soil animals. One possible reason for this discrepancy is that soil animals have different effects on soil nutrient dynamics depend on their feeding type (Lavelle *et al*. 1997). Another possible reason is that differences in soil chemical composition and organic matter input to soil lead to changes in soil animal effects

The rates of nutrient cycling are usually not constant, even in a mature forest ecosystem, due to the effects of processes such as seed masting (Selås *et al*. 2002) and periodic insect outbreaks. The 17-year periodic appearance of cicadas in North America provides a nutrient pulse to the forest soil resulting from the mass of carcasses, in turn increasing foliage N content and seed mass (Yang 2004). Despite these temporal differences in nutrient dynamics, many studies assume links between plant growth and decomposition processes

Populations of *P*. *laminata* have a synchronized life cycle and undergo simultaneous molts at particular stages according to seasonal temperature rhythms (Fujiyama 1996). The larvae live in the soil for 7 years (Fig. 1a, b) before they reach the adult stage (Fig. 1c). Their population consists of only a single age cohort, so adult swarming is observed at 8-year intervals (Niijima and Shinohara 1988). The huge abundance and synchronized cohort of *P*. *laminata* provide a good opportunity to investigate the soil-animal contributions to nutrient dynamics at the forest floor (Hashimoto *et al*. 2004; Toyota *et al*. 2006). Due to their heterogeneous abundance within the same region in forest soil, the effects of *P*. *laminata* on

The train millipede *P*. *laminata* can enhance plant production in two major ways. First, changes in soil N availability through millipede activity affect plant production. Latestage larvae enhance N mineralization in soil when millipede abundance is high (Toyota *et al*. in press). By contrast, adults contribute to transforming plant litter into soil, but do not increase N availability in the adult phase. Due to differences in soil N dynamics with developmental stage, the larvae and adults may affect plant productivity differently. Second, carcasses of adults contain higher concentrations of available phosphorus (P) for plant (Toyota, unpublished data). Since forest production is usually limited by P availability in soil (*e*.*g*., Crews *et al*. 1995; Vitousek and Farrington 1997), the P supplied from their carcasses to the forest floor after the death of adults will result in increased

Here, we studied how aboveground production can be affected by soil animal abundance and developmental stage. Effects of the train millipede were estimated to compare production between natural low-abundance and high-abundance millipede plots in the field. To test whether they temporally have different effects from late stage larvae to after the death of adults, the periods examined for estimating plant productivity were the 2 years before and after the adult active year, over a total of 5 years. Annual herbaceous plants should detect such temporal effects easily. In this paper, we tested the following two predictions: late stage larvae enhance leaf N content and production in the herb layer, and

(Tiunov and Scheu 2004).

on a forest floor in the short-term.

plants can be distinguished, even under field conditions.

plant production and changes in leaf quality.

after adult death, the millipede decomposition increases herbaceous annual plant production and leaf P content. Specifically, we examined the effects of the millipedes on the productivity of annual dwarf bamboo, which dominates the undergrowth of temperate forests in Japan.

Fig. 1. The train millipede, *P*. *laminata*, in the soil as (a) a 6th-instar larva, (b) 7th-instar larvae, and (c) on the forest floor as an adult.

Plant Productivity is Temporally Enhanced by

**2.2 Measurements**

flow analysis.

**3. Results**

(6th instar larvae).

Kramer, *P* < 0.05).

**2.3 Statistical analysis**

2.8.0 (R Development Core Team 2008).

respectively, in October 2000 (Hashimoto *et al*., 2004).

Soil Fauna Depending on the Life Stage and Abundance of Animals 257

7th instar larvae in the low-abundance areas (plots L1 and L2) was 3.8 g m–2 and 1.0 g m–2, respectively, in October 1999, and average dry biomass of adults was 1.0 g m–2 and 1.6 g m–2,

Four quadrats (1 × 1 m) were harvested in each plot to estimate the aboveground dwarf bamboo biomass in the period of maximal development of the dwarf bamboo vegetation (from late August to early September 1999, 2000, 2001, 2002, and 2003). The aboveground herb samples were dried at 40°C for 4 days and weighed. After removing the bamboo stalks, samples were homogenized. The 20-g subsamples of dwarf bamboo leaves were ground in a blender and used for N and P analysis. The N content was analyzed using a gas chromatograph (Sumigraph NC-95A; Shimadzu, Kyoto, Japan). The P content was analyzed using a Futura autoanalyzer (Actack, Alliance Instruments, Frépillon, France) for continuous

To test for differences in aboveground biomass, leaf N and P content through the sampling years, multiple comparisons among sampling years within a treatment were performed using the Tukey–Kramer test. Linear regression was used for correlation analysis between millipede biomass and leaf N and P content. All statistical analyses were performed using R

The aboveground biomass in high-density train millipede plots varied significantly among years (H1: *P* = 0.037; H2: *P* = 0.001; Fig. 2). No significant differences among years were observed in low-density millipede plots (L1: *P* = 0.187; L2: *P* = 0.09). The observed pattern of the aboveground biomass in high-density plots tended to be high in 1999 (6th instar larvae). In plot H1, aboveground biomass in 1999 (6th instar larvae) was significantly higher than that in 2003 (2 years after adult death). In plot H2, the aboveground biomass in 1999 (6th instar larvae) and 2002 (1 year after adult death) was significantly higher than in 2000 (7th

The N content in leaves varied significantly among years in all plots. Temporal dynamics of the N content differed between high- and low-density plots. Similar to the aboveground biomass in high-density plots, the N content tended to be high in 1999 (6th instar larvae). By contrast, in low-density plots, the N content tended to be low in 1999

The P content in high-density plots varied significantly among years (*P* < 0.001), but not in the low-density plots (L1, *P* = 0.45; L2, *P* = 0.08). The P contents in 2000 (7th instar larvae), 2001 (adult) and 2002 (1 year after adult death) were significantly lower than that in 1999 (6th instar larvae) and 2003 (2 years after adult death) in both plots H1 and H2 (Tukey–

**3.1 Temporal changes in aboveground production and leaf quality**

instar larvae) and 2001 (adult) (Tukey–Kramer, *P* < 0.05).

### **2. Materials and methods**

#### **2.1 Study site**

We established research plots at four different field sites in larch forests of Mt. Yatsugatake in Yamanashi Prefecture, central Japan (1350–1400 m above sea level, 35º54'12–46"N, 138º20'32"–24'03"E). The plots comparing low- (reference) and high-abundance areas of the train millipede were carefully chosen to avoid differences in soils, vegetation, and topography among plots. This region is characterized by a cool–temperate climate with mean annual precipitation of 1100 mm and mean air temperature of 10.6°C (Japan Weather Association 1998). The vegetation is a plantation forest of Japanese larch [*Larix kaempferi* (Lamb.) Sargent]. The sizes and ages of the larch in each plot are shown in Table 1. The shrub layer was sparse and was dominated by *Quercus crispula* Blume, *Prunus incisa* Thumb., *Ligustrum tschonoskii* Decaisne, *Symplocos coreana* Ohwi, and *Rhododendron obtusum* Planch. Dwarf bamboo (*Sasa nipponica* Makino) dominates the herb layer with *Osmunda japonica* at 50–70 cm height.

Table 1. Location of the study plots and abundance of the larch trees.

The organic layer on the forest floor is mainly composed of larch foliage mixed with larch twigs and bamboo stalks and leaves. The soil type is a well-developed aggregate structure of Andosols (FAO *et al*. 1998). About 50% of the total soil C at 0–100-cm depth was stored in the surface 10 cm, and about 75% was in the upper 0–30 cm (Morisada *et al*. 2002). Volcanic material was deposited after eruptions of Mt. Yatsugatake from 1,300,000 to 10,000 years before present. After that, forests had expanded. In the region around the study plots, natural larch forests remain, and natural larch regeneration at the arly stage follows wildfires. The vegetation was fired artificially in around 1900 (Suka, 2008). In another disturbance, an extraordinarily strong typhoon passed through this region in 1959.

In October 1998, the population of *P*. *laminata* at this site consisted of only 6th instar larvae (Fig. 1a), which subsequently molted and became 7th instar larvae (Fig. 1b) in August 1999. Adults emerged in late August 2000, and swarming on the forest floor was observed from September (Fig. 1c); the adults died after egg deposition in July 2001 in the foothills of Mt. Yatsugatake (Toyota personal observations). The density of 6th instars ranged from 160 to 1088 m–2 (mean ± SD, 485 ± 302 m–2; n = 3) in October 1998 (Toyota personal observation) and from 106 to 2156 m–2 (619 ± 208 m–2; n = 10) in June 1999, in the high-abundance area. The density of 7th instar larvae in the high-abundance area ranged from 144 to 720 m–2 (469 ± 240 m–2; n = 6) in April 2000 (Toyota *et al*. 2006). The average dry biomass of 7th instar larvae in the high-abundance areas (plots H1 and H2) was 15.7 g m–2 and 12.2 g m–2, respectively, in October 1999, and the average dry biomass of adults reached 28.6 g m–2 and 15.1 g m–2, respectively, in October 2000 (Hashimoto *et al*. 2004). By contrast, the average dry biomass of 7th instar larvae in the low-abundance areas (plots L1 and L2) was 3.8 g m–2 and 1.0 g m–2, respectively, in October 1999, and average dry biomass of adults was 1.0 g m–2 and 1.6 g m–2, respectively, in October 2000 (Hashimoto *et al*., 2004).

#### **2.2 Measurements**

256 Forest Ecosystems – More than Just Trees

We established research plots at four different field sites in larch forests of Mt. Yatsugatake in Yamanashi Prefecture, central Japan (1350–1400 m above sea level, 35º54'12–46"N, 138º20'32"–24'03"E). The plots comparing low- (reference) and high-abundance areas of the train millipede were carefully chosen to avoid differences in soils, vegetation, and topography among plots. This region is characterized by a cool–temperate climate with mean annual precipitation of 1100 mm and mean air temperature of 10.6°C (Japan Weather Association 1998). The vegetation is a plantation forest of Japanese larch [*Larix kaempferi* (Lamb.) Sargent]. The sizes and ages of the larch in each plot are shown in Table 1. The shrub layer was sparse and was dominated by *Quercus crispula* Blume, *Prunus incisa* Thumb., *Ligustrum tschonoskii* Decaisne, *Symplocos coreana* Ohwi, and *Rhododendron obtusum* Planch. Dwarf bamboo (*Sasa nipponica* Makino) dominates the herb layer with *Osmunda*

L1 35º 54' N, 138º 20' E 1350 S16E, 13º 1952 950 17.5 20.4 L2 35º 54' N, 138º 21' E 1360 S42W, 18º 1951 1100 19.4 21.5 H1 35º 54' N, 138º 23' E 1400 S52E, 20º 1961 800 14.6 19.4 H2 35º 54' N, 138º 24' E 1390 N72E, 24º 1961 750 15.6 21.8

The organic layer on the forest floor is mainly composed of larch foliage mixed with larch twigs and bamboo stalks and leaves. The soil type is a well-developed aggregate structure of Andosols (FAO *et al*. 1998). About 50% of the total soil C at 0–100-cm depth was stored in the surface 10 cm, and about 75% was in the upper 0–30 cm (Morisada *et al*. 2002). Volcanic material was deposited after eruptions of Mt. Yatsugatake from 1,300,000 to 10,000 years before present. After that, forests had expanded. In the region around the study plots, natural larch forests remain, and natural larch regeneration at the arly stage follows wildfires. The vegetation was fired artificially in around 1900 (Suka, 2008). In another disturbance, an extraordinarily strong typhoon passed through this

In October 1998, the population of *P*. *laminata* at this site consisted of only 6th instar larvae (Fig. 1a), which subsequently molted and became 7th instar larvae (Fig. 1b) in August 1999. Adults emerged in late August 2000, and swarming on the forest floor was observed from September (Fig. 1c); the adults died after egg deposition in July 2001 in the foothills of Mt. Yatsugatake (Toyota personal observations). The density of 6th instars ranged from 160 to 1088 m–2 (mean ± SD, 485 ± 302 m–2; n = 3) in October 1998 (Toyota personal observation) and from 106 to 2156 m–2 (619 ± 208 m–2; n = 10) in June 1999, in the high-abundance area. The density of 7th instar larvae in the high-abundance area ranged from 144 to 720 m–2 (469 ± 240 m–2; n = 6) in April 2000 (Toyota *et al*. 2006). The average dry biomass of 7th instar larvae in the high-abundance areas (plots H1 and H2) was 15.7 g m–2 and 12.2 g m–2, respectively, in October 1999, and the average dry biomass of adults reached 28.6 g m–2 and 15.1 g m–2, respectively, in October 2000 (Hashimoto *et al*. 2004). By contrast, the average dry biomass of

Plots Altitude (m a.s.l.) Aspect and slope Latitude and Japanese larch

Table 1. Location of the study plots and abundance of the larch trees.

Planted in Canopy density (ind./ha) Average height (m) Average DBH (cm)

**2. Materials and methods**

*japonica* at 50–70 cm height.

longitude

region in 1959.

**2.1 Study site**

Four quadrats (1 × 1 m) were harvested in each plot to estimate the aboveground dwarf bamboo biomass in the period of maximal development of the dwarf bamboo vegetation (from late August to early September 1999, 2000, 2001, 2002, and 2003). The aboveground herb samples were dried at 40°C for 4 days and weighed. After removing the bamboo stalks, samples were homogenized. The 20-g subsamples of dwarf bamboo leaves were ground in a blender and used for N and P analysis. The N content was analyzed using a gas chromatograph (Sumigraph NC-95A; Shimadzu, Kyoto, Japan). The P content was analyzed using a Futura autoanalyzer (Actack, Alliance Instruments, Frépillon, France) for continuous flow analysis.

#### **2.3 Statistical analysis**

To test for differences in aboveground biomass, leaf N and P content through the sampling years, multiple comparisons among sampling years within a treatment were performed using the Tukey–Kramer test. Linear regression was used for correlation analysis between millipede biomass and leaf N and P content. All statistical analyses were performed using R 2.8.0 (R Development Core Team 2008).

### **3. Results**

#### **3.1 Temporal changes in aboveground production and leaf quality**

The aboveground biomass in high-density train millipede plots varied significantly among years (H1: *P* = 0.037; H2: *P* = 0.001; Fig. 2). No significant differences among years were observed in low-density millipede plots (L1: *P* = 0.187; L2: *P* = 0.09). The observed pattern of the aboveground biomass in high-density plots tended to be high in 1999 (6th instar larvae). In plot H1, aboveground biomass in 1999 (6th instar larvae) was significantly higher than that in 2003 (2 years after adult death). In plot H2, the aboveground biomass in 1999 (6th instar larvae) and 2002 (1 year after adult death) was significantly higher than in 2000 (7th instar larvae) and 2001 (adult) (Tukey–Kramer, *P* < 0.05).

The N content in leaves varied significantly among years in all plots. Temporal dynamics of the N content differed between high- and low-density plots. Similar to the aboveground biomass in high-density plots, the N content tended to be high in 1999 (6th instar larvae). By contrast, in low-density plots, the N content tended to be low in 1999 (6th instar larvae).

The P content in high-density plots varied significantly among years (*P* < 0.001), but not in the low-density plots (L1, *P* = 0.45; L2, *P* = 0.08). The P contents in 2000 (7th instar larvae), 2001 (adult) and 2002 (1 year after adult death) were significantly lower than that in 1999 (6th instar larvae) and 2003 (2 years after adult death) in both plots H1 and H2 (Tukey– Kramer, *P* < 0.05).

Plant Productivity is Temporally Enhanced by

2.0

0.06

 0.10

 0.14

 0.18

Phosphorus content (%) Nitrogen content (%)

0 5 10 15 20 25 30

*P* **= 0.002 R2 = 0.502**

circles, adults. Solid lines are significant linear regressions.

*P* **< 0.001 R2 = 0.728**

 2.5

 3.0

 3.5

**3.2 Effects of the train millipede on leaf quality**

Soil Fauna Depending on the Life Stage and Abundance of Animals 259

The N content of leaves was closely positively correlated with 6th instar larval biomass in 1999 (Fig. 3), but not in other years (Figs. 3, 4). The P content was positively correlated with 6th instar larvae biomass in 1999 (6th instar larvae) and adult biomass in 2003 (2 years after adult death). By contrast, it was negatively correlated with the final instar larvae biomass in

0 5 10 15 20 25 30 0 5 10 15 20 25 30

*P* **= 0.886 R2 = 0.002**

*P* **= 0.256 R2 = 0.091**

)

*P* **= 0.829 R2 = 0.003**

*P* **= 0.001 R2 = 0.536**

Biomass (g/m2

Fig. 3. Developmental stage-dependent effects of the millipede on leaf nitrogen and

phosphorus contents: open circles, 6th-instar larvae; grey circles, 7th-instar larvae; and black

2000 (7th instar larvae) and adult biomass in 2002 (1 year after adult death).

Fig. 2. Temporal variation in the aboveground biomass, nitrogen content, and phosphorus content with developmental stage: open circles, 6th-instar larvae; grey circles, 7th-instar larvae; black circles, adults; and crosses, after the adult period. The same letter indicates no significant difference among years based on the Tukey–Kramer test (*P* < 0.05).

#### **3.2 Effects of the train millipede on leaf quality**

258 Forest Ecosystems – More than Just Trees

**H1 H2 L1 L2**

**b**

**a**

**ab**

**a a**

**a**

**a a a**

**a**

**b**

**b**

**b**

**a**

**b**

**a a**

**a a a**

**a**

**a**

**a a a a**

**a**

1999 2002 1999 2002 1999 2002

**a a a a**

**a**

**a**

**b**

**c**

Year

Fig. 2. Temporal variation in the aboveground biomass, nitrogen content, and phosphorus content with developmental stage: open circles, 6th-instar larvae; grey circles, 7th-instar larvae; black circles, adults; and crosses, after the adult period. The same letter indicates no

significant difference among years based on the Tukey–Kramer test (*P* < 0.05).

**ab a**

Aboveground biomass (g/m2

Nitrogen content (%)

Phosphorus content (%)

0.06

 0.10

 0.14

**c**

 0.18

1999 2002

**ab a**

**b**

100

**ab**

**ab c bc**

**ab**

**ab**

**a**

**ab**

**a**

**b**

**c**

**a a**

**bc ab**

**c**

**c**

**b**

2.0 2.5 3.0 3.5

 200 **b**

 300

) The N content of leaves was closely positively correlated with 6th instar larval biomass in 1999 (Fig. 3), but not in other years (Figs. 3, 4). The P content was positively correlated with 6th instar larvae biomass in 1999 (6th instar larvae) and adult biomass in 2003 (2 years after adult death). By contrast, it was negatively correlated with the final instar larvae biomass in 2000 (7th instar larvae) and adult biomass in 2002 (1 year after adult death).

Fig. 3. Developmental stage-dependent effects of the millipede on leaf nitrogen and phosphorus contents: open circles, 6th-instar larvae; grey circles, 7th-instar larvae; and black circles, adults. Solid lines are significant linear regressions.

Plant Productivity is Temporally Enhanced by

**4.2 Changes in phosphorus content**

molting chamber (ca. 15 mm in diameter).

carcasses would be insufficient to increase the leaf P content.

the forest soil system.

**4.1 Temporal differences in production and nitrogen**

Soil Fauna Depending on the Life Stage and Abundance of Animals 261

Observed temporal patterns in production and N content of dwarf bamboo leaves were related to soil N availability in this forest. Increases in soil N availability for plants by 6th instar larval activity (Toyota *et al*. in press) immediately resulted in stimulation of plant biomass and N content in leaves. Under low N availability conditions during the adult phase, plant growth and N content did not increase. These patterns suggest that N limitation may occur in these forests and that millipede larvae can alleviate N limitation in

Leaf P content increased with the incremental increase in the millipede biomass of 6th instar larvae (Fig. 3). Consequently, the larvae would provide not only available N but also P. However, during the 7th instar, the millipede reduced the leaf P content (Fig. 3). Arbuscular mycorrhizal fungi (AMF), which have a critical role in P uptake by plants, are suppressed by N fertilization (Bradley *et al*. 2006). Similarly, the increase in soil N availability with 6th instar larvae would reduce AMF in the next year, so plants would utilize less P with the incremental increase in millipede biomass. Furthermore, 7th instar larvae may alter soil chemical and physical conditions for the following reasons: (1) excess P consumption by 7th instar larvae might occur to create the adult body, which might result in a reduction of soil P availability, and (2) molting chambers of 7th instar larvae could physically hold P in the soil, lead to a substantial reduction in uptake of P by plants. The train millipedes make molting chambers from their own fecal pellets during summer, for several years the compact structure of the molting chamber of last instar (7th instar) larvae remains in the field at soil depths between 5 and 15 cm (Toyota, unpublished data). Niijima (1984) suggested that the physical structure of soil is greatly altered by 7th instar larvae millipedes due to their large

After 1 year of the adult phase, the previous adult biomass was negatively correlated with the leaf P content. These decreases in leaf P content can be attributed to the following three reasons. First, P absorption ability in the soil could be high in our forests because of soil engineering by adults (so the P uptake by plants would be low). Second, adult activity might reduce P utilization ability of plants. Adult millipedes were observed in soil to a depth of around 12 cm, near dwarf bamboo roots during the winter (Niijima 1984). This adult activity in soil may damage ectomycorrhizal fungal growth and fine roots of plants due to soil disturbance, which could result in reduced P uptake by plants. Third, there would be fewer adult carcasses on forest floor in high-density millipede plots than adult abundance in the previous year (Hashimoto *et al*. 2004); consequently, phosphate from

After 2 years of the adult phase, however, the previous adult biomass was positively correlated with leaf P content. In the previous year, P was probably limited for plants. A lack of P availability leads to the preferential allocation of more resources to root biomass than to aboveground biomass as a plant response (Lynch 1995). Theory predicts a negative correlation between root allocation and aboveground growth rate. Observed low aboveground production in high-density millipede plots after 2 years of the adult phase is consistent with this prediction. Ryan *et al*. (2001) showed that organic acid was supplied

Fig. 4. Effects of adult biomass after adults died on the leaf nitrogen and phosphorus contents. The black crosses indicate 1 year after the adult period. The grey crosses indicate the 2 years after the adult period. Solid lines are significant linear regressions.

#### **4. Discussion**

Our results show that temporal changes in dwarf bamboo production and leaf P content occur in plots with high densities of the train millipede, but not in low-density millipede plots. We found that the effects of the millipede on plant leaf N and P content differed with millipede development stage. In agreement with our hypothesis, 6th instar larvae had positive effects on plant production, N and P contents in leaves. In contrast to our hypothesis, the millipede had no effect on dwarf bamboo production and leaf quality during the adult phase, negative effects on the P content for 7th instar larvae and 1 year after the adult phase, and positive effects on the P content in 2 years after the adult phase. The contribution of the millipede to plant growth is therefore twofold. Here, we discuss factors promoting the close relationship between plants and millipedes.

#### **4.1 Temporal differences in production and nitrogen**

Observed temporal patterns in production and N content of dwarf bamboo leaves were related to soil N availability in this forest. Increases in soil N availability for plants by 6th instar larval activity (Toyota *et al*. in press) immediately resulted in stimulation of plant biomass and N content in leaves. Under low N availability conditions during the adult phase, plant growth and N content did not increase. These patterns suggest that N limitation may occur in these forests and that millipede larvae can alleviate N limitation in the forest soil system.

#### **4.2 Changes in phosphorus content**

260 Forest Ecosystems – More than Just Trees

2.0

Phosphorus content (%) Nitrogen content (%)

0.06 0.08 0.10 0.12 0.14 0.16 0.18

**4. Discussion**

0 5 10 15 20 25 30

promoting the close relationship between plants and millipedes.

*P* = 0.021 R2 = 0.327

*P* = 0.235 R2 = 0.099

Adult biomass (g/m2