Changes in soil organic matter associated with pig rearing: Influence of stocking densities and land gradient on forest soils in central Italy

Agriculture, Ecosystems and Environment 211 (2015) 32–42

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Changes in soil organic matter associated with pig rearing: Influence of stocking densities and land gradient on forest soils in central Italy G. Bondi a,b, * , E. Peruzzi c, C. Macci c , G. Masciandaro c, A. Pistoia a a b c

University of Pisa, Department of Agriculture, Food and Environment (DAFE), Italy Teagasc- Crops, Environment and Land Use Programme, Jonhstown Castle, Wexford, Ireland National Research Council, Institute of Ecosystem Study (ISE), Italy

A R T I C L E I N F O

A B S T R A C T

Article history: Received 24 June 2014 Received in revised form 12 May 2015 Accepted 17 May 2015 Available online xxx

Outdoor pig rearing was reintroduced in Italy, as in the rest of Europe as a consequence of a European policy aimed to pay attention to animal welfare and food quality. Despite these advantages, outdoor pigs rearing may lead to serious damage of both vegetation and soil because of animals eating habits and behavior. In a forest ecosystem the effects of pig impact could be really negative, reducing the natural ability of soil to recover itself and causing the loss of organic matter. The aim of this study was to evaluate the effect of outdoor pig rearing in forest ecosystems in Mediterranean areas on soil, in order to identify the critical thresholds for soil organic matter quality and functionality in terms of: animal pressure (animal density); grazing livestock area (slope, depth and soil characteristics). Two farms, similar for type of vegetation (forest environment) and soil characteristics were chosen. In each farm three different situations of animal pressure (high, low animal pressure and undisturbed), combining to territorial and morphologic characteristics used for pig rearing (high, low slope and flat soil), were identified. For each experimental situation, chemical and chemical-structural parameters of soil were investigated. Grazing at high animal pressure showed a reduction of all parameters related to organic matter content, in addition to a worsening of chemical-structural characteristics, thus resulting in a loss of soil quality. Grazing at low animal pressure generally seemed not to affect chemical fertility of soil, preserving organic matter content, even though a significant worsening of chemical-structural characteristics was identified. Soil damage including mineralization of stable organic matter was greatest on the steeper slopes for both upper and lower soil layers. ã2015 Elsevier B.V. All rights reserved.

1. Introduction The outdoor pig rearing was rediscovered and re-evaluate in last two decades, as a consequence of a European policy aimed to pay greater attention to animal welfare. In many European nations, there has been a resurgence of “outdoor breeding”, as in UK, where it represents a significant part of production (Sheppard, 2004). This type of farming, coupled to a power supply based on natural products, provides advantages to the organoleptic and dietary characteristics of meat products. Furthermore, unlike conventional livestock, many studies have shown that the animals reared outdoors enjoy greater welfare (Beattie et al., 1993, 1995, 2000).

* Corresponding author at: University of Pisa, Department of Agriculture, Food and Environment, (DAFE), via del Borghetto 56124 Pisa, Tuscany, Italy. Tel.: +39 0503152483. E-mail address: [email protected] (G. Bondi). http://dx.doi.org/10.1016/j.agee.2015.05.003 0167-8809/ã 2015 Elsevier B.V. All rights reserved.

In the past, free-range and semi free-range rearing pigs were the most common rearing system used in various parts of Italy, often based on the exploitation of the forests and their products (acorns and chestnuts). However, during the last half-century, this type of livestock gave way to industrial farming systems using high density of non-native species. For different reasons which include the exploitation of marginal areas (mostly wooded), the preservation of local breeds, the affirmation of organic livestock farming, the greater consumer attention to quality products and animal welfare (Edwards, 2005), the outdoor pig rearing was recently reintroduced in Italy. However, both conventional and organic outdoor pig rearing can be potentially associated with some ecological risks. The degree of disturbance caused by pigs on a specific ecosystem, depends on the interaction between vegetation, soil and animal (Avondo et al., 2013). The intensity of outdoor pig production and its inappropriate management determine the extent of environmental impact (Quintern and Sundrum, 2006). Excessive stocking rates,

G. Bondi et al. / Agriculture, Ecosystems and Environment 211 (2015) 32–42

permanent paddocks and unsuited locations are some of the main aspects that cause this kind of problems (Quintern and Sundrum, 2006). Eating habits, especially overgrazing, may lead to serious damage to vegetation and soil. Overgrazing can reduce vegetation cover and alter the botanical composition through trampling and selective grazing (Czeglédi and Radàcsi, 2005). In terms of soil, animal rooting activity can cause surface horizon disruption, making the area particularly vulnerable to rain erosive action (Avondo et al., 2013). Soil morphological characteristics, such as slope, may be important to assess the grazing impact on soil quality. Many studies have demonstrated that grazing contributes to breakdown soil aggregates, making the soil more subject to erosion and compaction in sloping and flat soils, respectively (Manzano and Navart, 2000; Novikoff, 1983; Pluhar et al., 1987). Furthermore, the excessive trampling causes a compression of the soil decreasing its porosity, which, in turn, reduces water infiltration and percolation, thus, finally damaging soil structure (Avondo et al., 2013). Moreover, a strong and widespread grazing activity can lead to carbon losses and enhance the mineralization of native soil organic matter, causing loss of fertility and problems in regeneration of vegetation (Abril et al., 2005; Bondi et al., 2013; Pulido-Fernández et al., 2013). In a forest ecosystem these effects caused by pigs could be much more lasting and negative. In fact, in a forest soil, part of a biological balanced system, rich in biodiversity, characterized by continuous organic matter inputs and by optimal structural conditions, the rate of degradation caused by pigs can be very rapid, when the disturbance exceeds the natural ability of soil to recover. In situations where deeper soil horizons have been impacted, the restoration of the previous condition could be very difficult (Fabbio, 2009; Pulido-Fernández et al., 2013). The reduction of soil porosity by pigs trampling, together with a reduced vegetation cover, increase the water runoff and erosion potential that results in loss of soil organic matter, one of the most important factors determining soil quality and fertility, responsible for the sustainability of many agro-ecosystems (Doran and Parkin, 1994). The aim of this study was to evaluate the effect of outdoor pig rearing in two Mediterranean forest ecosystems on soil organic matter quality and functionality. The specific objective aimed to identify the critical thresholds for soil organic matter quality in terms of: I Animal pressure (animal density); II Grazing livestock area (slope, depth and soil characteristics). This objective was achieved by studying the changes of chemical and chemical-structural parameters of soil, considered as appropriate indicators of soil quality and organic matter dynamics. Pyrolysis–gas chromatography (Py–GC) has been used as a quick and generally reproducible technique to make a qualitative study of the chemico-structural characteristics of soil organic matter turnover (Ceccanti et al., 2007; Hernandez et al., 2006; Macci et al., 2012a).

2. Material and methods 2.1. Study area characteristics and farms choice The test was carried out in two Mediterranean forest ecosystem areas.

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Two distinct experimental farms, characterized by the management of outdoor pig production in a forest environment, were chosen. Furthermore, on the basis of the purpose of this study, the experimental farms were chosen in different sloping areas. The two farms were selected as representative examples of farms within a defined geographical area (region of Tuscany). This heterogeneous territory has in fact a variety of farm dimensions difficult to identify and classify. Farm dimensions in the Tuscany region highlight a high degree of variability in relation to management practices, size and natural resources, thereby making them difficult to coherently classify. It is worth considering that an optimal experimental design would have involved several farms each with different geomorphological characteristics. Nevertheless, in the geographical context under study, such a design was found to be impracticable. Indeed, the business of large landed estates with different land grades for the same land use is uncommon in the area, where farms are medium–small farms, normally characterized by uniform land grades. However, this threat to the validity of the experiment was mitigated by the choice of the two candidate farms. Such farms were selected because they were sharing similar livestock system, land use, farm management, soil type and vegetation characteristics, while the only relevant differences were the land grades of the fields under study. In a sense, and considering the constraints of the agricultural business context of the area, they were the sub-optimal choice that more closely approximated an optimal – yet impracticable – multi-farm experimental design. However, according to the definition of the study objective, and taking into account the real constraints linked to heterogeneity of the geographical area studied, the two farms have been chosen on the basis that they are representative examples of these generalized farm groupings and are considered representative of the real life situation. 2.1.1. Livestock farm “San Lorenzo”: Located in Media Valle del Serchio (municipality of Lucca; latitude N44
020 56.900 , longitude E10
650 74.400 ), at about 600 mamsl. The average rainfall in this area is about 910 mm per year. The average annual temperature is around 13.2
C with maximum temperatures of about 26.1
C in August and minimum of about 2.4
C in January–February. The area is characterized by temperate deciduous forest formations, consisting of centuries-old trees of an average height of about 10–15 m, with trunks diameter of about 20–30 cm, with a high canopy cover of about 80–90%. The forest species present are mainly chestnut (Castanea sativa Miller), ash (Fraxinus ornus L.), and black locust (Robinia pseudoacacia L.), with some exemplar of oak woodlands (Quercus ilex, Quercus cerris L., Quercus petraea). The major herbaceous undergrowth species detected were Ruscus aculeatus L. and Rubus ulmifolius. The characteristics of the geological substrate, taken from geological maps of Italy (1:100,000) of the Geological Survey of Italy (2011) are as follows: Turbiditic quartz rich (42%) sandstones, feldspar (27%) with calcite (7%) and phyllosilicates (24%) alternating with silty shale (Oligocene–Miocene). The soil examined in this study is Eutric Cambisol (IUSS Working Group WRB, 2007) with loam texture. In this area, the available slopes were 30% and 5%. 2.1.2. Livestock farm “Di Grigoli” Located in Coltano (Municipality of Pisa; latitude N43
380 23.3400 , longitude E10
220 51.0000 ) at about 100 mamsl. This area has about 867 mm rainfall per year. The average annual temperature is around 14.7
C with maximum temperatures of about 28.7
C in August and minimum of about 3.2
C in January–February. As in “San Lorenzo”

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G. Bondi et al. / Agriculture, Ecosystems and Environment 211 (2015) 32–42

farm, this area is also characterized by temperate deciduous forest formations with trees of an avarege height of about 8–9 m and a diameter of about 10–15 cm. Tree canopy density was very high, covering about 80–90%.The areas for rearing pigs consist in mixed forest composed by oak woodlands (Quercus ilex,Quercus cerris L., Quercus petraea), black locust (Robinia pseudoacacia L.), ash (Fraxinus ornus L.) and mesophilic forests of deciduous broadleaf. In addition, the landscape is characterized by shrubs and herbaceous undergrowth typical of Mediterranean areas (Laurus nobilis L., Ruscus aculeatus L., Rubus ulmifolius, Hedera helix L.). The geological substrate from geological maps of Italy (1:100,000) (Geological Survey of Italy, 2011) showed the presence in this area of continental deposits of silts, clayey silts and yellow decarbonatate sands (Pleistocene, Olocene). The soil is Eutric Cambisol (IUSS Working Group WRB, 2007) and has a sandy-loam texture. The area for pig rearing was flat (0% slope). Both farms were set up in 2000 and pig rearing was the unique activity carried on in the forest areas. The Cinta Senese’s breed were reared at the “San Lorenzo” farm, while the White Large” was the breed reared at “Di Grigoli” farm. The animals were adults of an average weight of 85 kg for Cinta Senese breed and 90 kg for Large White breed. They were reared outdoors on pasture throughout the year, and so they fed on forest fruits, shrubs, roots and tubers. However, all year round, but especially during periods of poor fruiting of the forest, feed supplements were distributed.

2.2. Site description and soil sampling In both farms a lack of natural vegetation and soil deterioration state, were evident in the areas occupied by pig rearing (Fig. 1 a and b). The situation of extreme environmental degradation had an anthropic origin for both farms, achieved through years of mismanagement (about 11 years for both farms). In both cases pig rearing made use of irrational animal husbandry techniques; for example lack of rotations in the areas occupied by pigs, high stocking density encouraging food competition between parties, improper management without respect for the natural growth cycle of turf. The major damage to soil due to the continuous pig trampling was: litter removal, shuffling of soil surface layers, soil digging, formation of preferential pathways, compaction and erosion, Furthermore a general high reduction in shrubs and undergrowth was observable associated with the eating habits and foraging behavior of the pigs. There was a observable correlation between higher animal pressure and a lower amount of vegetation. The major type of vegetation damage was: shrub biting, digging up and cutting off, young forest plants removal, digging around the root system of mature plants and subsequent biting, removal of bark due to rubbing and feeding. In each farms three different situations of animal pressure, were identified.

Fig. 1. Soil deterioration state in the areas occupied by pig rearing; a) “Di Grigoli” farm; b) “San Lorenzo” farm.

G. Bondi et al. / Agriculture, Ecosystems and Environment 211 (2015) 32–42

 HD: high animal pressure was identified in a forest area (about 2.5 ha) where the animals usually were allocated for most of the rearing stages; characterized by very high animal density (40–50 animals/ha) and extremely long residence times of animals on pasture (about 16 h/d);  LD: low animal pressure was identified in a forest area (about 2.5 ha) where the animals had access sporadically in fruiting wood periods; characterized by low animal density (1–2 animals/ha) and limited residence times on pasture (about 3 h/d);  UND: an undisturbed forest area was identified; adjacent to those where pigs were maintained, and protected from animals through fences. In relation to territorial and morphologic characteristics used for pigs rearing, three different slopes were identified.  30S: high sloping soil, approximately 30%.  5S: low sloping soil, approximately 5%.  0S: flat soil, 0%. The combinations of these factors lead to nine identifiable experimental situations. For each experimental situation, three homogeneous plots of soil of about 30 m2 each were identified, excluding toilet subareas from sampling design. Although particularly degraded, pig’s toilet areas were deliberately avoided from the sampling design because spatially they were very limited compared to the whole area studied and because they were considered atypical areas, not representative of the plot under study. Furthermore, the toilet areas presented such high manure content, sufficient to alter the results of some of the analyses carried out. Indeed, the massive presence of manure might have suggested misleading information on soil organic matter conservation status and dynamics (Pennock et al., 2008). Soil samples were collected in both farms at the beginning of March 2011, in order to reduce the potential seasonal variability. Three samples, consisting of five subsamples each, mixed to obtain a composite sample, were randomly collected in each plot at 0–10 cm (upper soil layer; us) and 10–20 cm (lower soil layer; ls). Soil samples were air-dried, sieved (2 mm) and stored at room temperature until analysis. Values reported in this paper for chemical and chemical-structural soil characteristics, correspond to the average of the three values obtained for each sampling point. 2.3. Soil analysis Electrical conductivity (EC) and pH were measured in 1:10 (w/v) aqueous solution. C and N contents were determined by dry combustion with a RC-412 multiphase carbon and a FP-528 protein/nitrogen analyser, respectively (LECO Corporation). N–NH4 and N–NO3 were determined in 1:10 (w/v) KCl extracts 0.5 M; N–NH4 was detected with ion selective electrode (SevenMulti, Mettler Toledo) and NaOH 10 M as solution to adjust pH at alkaline value (Quantification limit 0.1 mg/kg). N–NO3 was detected by Norman et al. method (1985) (Quantification limit 1 mg/kg). Water soluble carbon (WSC) was determined in water extracts 1:10 w/v (Garcia et al., 1991). Total extractable carbon (TEC) was measured in pyrophosphate 0.1 M pH 11 extract (1:10 w/v). WSC and TEC (and its fractions HA e FA) were determined by the Yeomans and Bremner (1988) method, by dichromate oxidation. Soil bulk density was measured on undisturbed cores (Blake and Hartge, 1986), while soil respiration was determined in rewetted soil (60% of water holding capacity) in closed jars at 24
C using alkali traps and titration with HCl 0.1 N (Badalucco et al., 1992).

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2.4. Pyrolysis–gas chromatography (Py–GC) technique Py–GC is a technique used to evaluate soil organic matter quality giving evidence of its micro structural differences. In soil samples a CDS Pyroprobe 190 coupled to a Carlo Erba 600 GC was used for the separation and quantification of pyrolytic fragments, following the conditions suggested by Macci et al. (2012a). Pyrograms were interpreted by quantification of seven peaks corresponding to the major volatile pyrolytic fragments (Ceccanti et al., 1986): acetic acid (K), acetonitrile (E1), benzene (B), toluene (E3), pyrrole (O), furfural (N), and phenol (Y). Acetonitrile (E1) is derived from the pyrolysis of aminoacids, proteins, and microbial cells. Furfural (N), is mostly derived from carbohydrates, lignocellulosic materials, proteins and other aliphatic organic compounds (Bracewell and Robertson, 1984), indicating the presence of rapidly metabolizable organic substances. Acetic acid is preferentially derived from pyrolysis of lipids, fats, and waxes, cellulose, carbohydrates (Bracewell and Robertson, 1984) and represents relatively less-degraded ligno-cellulose material (Buurman et al., 2007; Macci et al., 2012a; Sollins et al., 1996). Phenol is derived from amino acids, tannins and fresh or condensed (humic) lignocellulosic structures (Lobe et al., 2002; Macci et al., 2012a; Van Bergen et al., 1998). Benzene and toluene are basically derived from condensed aromatic structures of stable (humified) organic matter, particularly for benzene, since toluene must come from rings with aliphatic chains, albeit short (Macci et al., 2012a). Pyrrole is derived from nitrogenated compounds such as nucleic acids, proteins, microbial cells and condensed humic structures (Bracewell and Robertson, 1984). Peak areas were normalized, so that the area under each peak referred to the percentage of the total of the selected seven peaks (relative abundances). The alphabetic code used was conventional and has already been used in previous papers on natural soils (Alcaniz et al., 1984; Ceccanti et al., 1986). N/O, O/Y and B/E3 ratios were determined (Ceccanti et al., 2007, 1986; Macci et al., 2012a) being considered index of soil organic matter mineralization (N/O, O/Y) and humification (B/E3). AL/AR (Aliphatic/Aromatic compounds): index of “energetic reservoir” expresses the ratio between the sum of aliphatic products (K, N, and E1) and the sum of aromatic compounds (B, E3, O, and Y) (Ceccanti et al., 2007, 1986; Macci et al., 2012a). 2.5. Statistical analysis All results reported in the text are the means of determinations made on of three field replicates (n = 3). The STATISTICA 6.0 software (StatSoft Inc., Tulsa, Oklahoma, USA) was used for all statistical analysis. Analysis of variance (ANOVA) was used to evaluate the differences (p < 0.05) between density (HP and LP), slopes (0S, 5S and 30S) and depth (us, ls). Differences between treatments and the respective control (undisturbed soil, UND) within each slope and density were tested using Dunnett’s comparison test (p < 0.05). To clearly explain the overall evaluation and comparison, all parameters were graphically expressed as percentage variation (variation %) of each treatment (x) compared to the value of its undisturbed soil (UND), considering the “undisturbed” as control (100%) and calculating each treatment according to the following formula: Variation % = 100  (x  100)/UND. The results were also studied using principal component analysis (PCA). The PCA is a multivariate statistical data analysis technique, which reduces a set of raw data to a number of principal components that retain the most variance within the original data in order to identify possible patterns or clusters between objects and variables (Carroll et al., 2004).

Lower layer

pH

EC (mS/cm)

N–NH4 (mg/Kg)

N–NO3 (mg/Kg)

TN (%)

HD-30S

6.9  0.4

83.9  9.39

5.28  0.1

39.3  9.64

0.12  0.0*

7.7  0.2*

HD-5S HD-0S LD-30S LD-5S LD-0S UND-30S UND-5S UND-0S

6.9  0.5 5.8  0.9 6.7  1.2 7.3  0.3 5.5  0.1 6.8  0.2 6.6  0.1 4.7  0.1

68.4  13.3 214  8.22* 137  28.8* 40.4  3.18 358  26.8* 29.0  5.32 26.5  3.58 141  10.00

5.58  0.2 3.88  0.1* 7.06  0.3 4.59  0.1 3.80  0.3* 4.44  0.1 1.72  0.1 2.90  0.6

26.9  12.4 126  14.6* 61.0  20.1 13.7  0.55 102  30.2* 6.8  5.12 4.9  0.30 42.5  15.72

0.15  0.0* 0.30  0.0* 0.27  0.0 0.28  0.0 0.48  0.0 0.28  0.0 0.30  0.0 0.44  0.0

HD-30S

7.0  0.1

82.1  7.93*

4.86  0.0

30.0  2.25

HD-5S HD-0S LD-30S LD-5S LD-0S UND-30S UND-5S UND-0S

6.7  0.3 6.1  0.6 6.5  0.1 6.9  0.3 5.8  0.1 6.9  0.1 7.0  0.1 4.7  0.3

73.6  24.5 188  21.6* 112  20.35* 27.5  4.00 158  12.2* 15.9  0.67 22.3  4.76 59.7  9.50

5.21  0.4 2.92  0.5* 8.24  0.0 5.48  0.4 1.72  0.1 4.13  0.0 1.69  0.0 1.56  0.3

33.7  14.1 91.5  14.6 38.4  11.8 10.4  3.14 43.8  20.8 1.2  0.29 4.6  2.75 23.9  4.99

O (%)

Y (%)

N (%)

11.2  0.1

12.6  0.0*

9.3  0.0* 12.1  0.1* 10.8  0.0* 7.4  0.0 12.2  0.2* 5.7  0.0 6.4  0.1 9.3  0.0

12.2  0.2 11.5  0.1* 12.7  0.0* 10.9  0.0* 12.6  0.0* 10.7  0.1 11.1  0.1 12.8  0.2

0.18  0.0

8.9  0.0*

0.14  0.0 0.23  0.1* 0.16  0.0 0.14  0.0 0.20  0.0 0.18  0.0 0.17  0.0 0.17  0.0

9.3  0.0* 12.0  0.1* 9.7  0.0* 7.3  0.0* 10.3  0.1* 4.9  0.0 5.7  0.0 9.3  0.2

B (%)

E3 (%)

E1 (%)

K (%)

Al (K+N+E1) (%)

Ar (B+E3+O+Y) (%)

8.1  0.1*

13.0  0.4*

27.8  0.01*

19.6  0.00*

59.9  0.07*

40.1  1.10*

15.1  0.0* 16.3  0.1* 12.0  0.2* 11.7  0.0* 17.3  0.0* 13.8  0.0 15.9  0.1 16.6  0.1

8.0  0.2* 7.3  0.1* 11.1  0.3* 9.7  0.1* 8.2  0.1* 19.1  0.2 17.9  0.0 9.81  0.0

14.4  0.5* 17.0  0.0* 20.1  0.4 17.1  0.0* 16.1  0.0 18.3  0.0 16.6  0.3 14.5  0.0

22.8  0.10* 16.0  0.04* 18.7  0.01* 24.1  0.01* 15.9  0.03* 16.5  0.01 15.7  0.05 20.5  0.03

18.2  0.03* 19.8  0.02* 14.7  0.03* 19.2  0.01* 17.7  0.04* 15.8  0.06 16.3  0.02 16.5  0.04

56.0  0.18* 52.1  0.16* 45.4  0.39* 54.9  0.09* 50.9  0.12* 46.1  0.12 48.0  0.17 53.6  0.22

44.0  1.39* 47.9  0.53 54.6  0.98 45.1  0.20* 49.1  0.57 53.9  0.61 52.1  0.81 46.4  0.47

13.7  0.0*

11.8  0.2*

9.0  0.0*

12.7  0.0*

25.8  0.04*

18.2  0.06*

55.8  0.42

44.2  0.16

14.0  0.4* 14.3  0.5* 12.6  0.3 10.5  0.2* 12.3  0.3 11.5  0.3 8.5  0.2 13.0  0.0

14.0  0.1* 14.2  0.2* 16.5  0.0* 8.2  0.4* 15.9  0.2* 9.2  0.1 10.2  0.3 17.0  0.1

8.4  0.3* 9.7  0.0* 9.2  0.0* 11.0  0.2* 6.0  0.0* 12.8  0.1 12.6  0.0 7.8  0.0

13.4  0.0* 17.8  0.0* 16.8  0.0 14.2  0.0* 12.3  0.1* 16.5  0.3 16.9  0.1 14.8  0.1

22.5  0.01* 14.6  0.01* 17.6  0.04* 27.0  0.01* 24.6  0.01* 26.1  0.01 24.7  0.03 21.0  0.03

18.4  0.06* 17.4  0.01 17.6  0.01* 21.9  0.00* 18.7  0.04* 19.1  0.01 21.3  0.01 17.0  0.05

54.9  0.23* 46.2  0.35* 51.7  0.14* 57.1  0.52 59.2  0.41* 54.3  0.10 56.3  0.44 55.1  0.19

45.1  1.00 53.8  0.86* 48.3  0.42 42.9  0.73 40.8  0.75* 45.7  0.93 43.7  0.53 44.9  0.50

*Dunnett’s test (p < 0.05). HD, high animal pressure; LD, low animal pressure; UND, undisturbed; 30S, high sloping soil (30%); 5S, low sloping soil (5%); 0S, flat soil (0%). EC, Electrical Conductivity; O, Pyrrole; Y, Phenol; N, Furfural; B, Benzene; E3, Toluene; E1, Acetonitrile; K, Acetic acid; Al, Aliphatic compounds (Al = E1 + K + N); Ar, Aromatic compounds (Ar = B + O + E3 + Y).

G. Bondi et al. / Agriculture, Ecosystems and Environment 211 (2015) 32–42

Upper layer

Treatment

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3. Results

3.1. Soil characterization

Results describing soil characterization are reported in Tables 1 and 2 and in Figs. 2(a–d) and 3 (a–b). In both sloping and flat land under animal disturbance, soil pH values were similar to the undisturbed soils. In 0S soils and LD-30S EC increased significantly with respect to undisturbed soil. N–NO3 and N–NH4 contents were generally higher in disturbed 0S soils (in upper soil layer) than undisturbed ones. In the surface layer, a significant lower TOC and TN content was observed in HD soils compared to undisturbed ones, while generally no significant differences were observed in lower layer. WSC content in both layers of HD soils were generally lower than those of the undisturbed ones. The same trend was noticed for TEC in HD upper soil layer, while no difference curred in the lower soil layer. A similar trend was apparent for fulvic and humic acids where significantly lower values occurred in the HD upper soil layer, while the lower soil layer generally did not differ significantly from the undisturbed ones. In general, LD soils showed few significant changes in all chemical parameters with respect to undisturbed ones. Soil bulk density on the rearing areas was higher than those in the undisturbed area; the effect was particularly evident in 5S and 0S soils. Microbial respiration significantly decreased in HD 30S and HD 5S areas, with respect to the undisturbed areas in both soil layers.

3.2. Pyrolysis–gas chromatography (Py–GC)

The relative abundances of the main pyrolytic fragments identified under pyrolysis are reported in Tables 1 and 2 and Table 2, while the pyrolytic indices are presented in Fig 4(a–d). Benzene (B) and furfural (N) were generally higher in undisturbed soils, while in contrast, pyrrole (O) was generally higher in both layers of disturbed soils. Toluene (E3) was significantly lower in HD upper soil layer and also in the lower soil layer of HD-30S. Phenol (Y) was significantly higher for all undisturbed upper layers, excluding LD-30S, where an inverse trend was apparent. Conversely, in the lower layers, phenol values increased significantly with respect to undisturbed ones only in HD treatment. The mineralization index N/O generally showed lower values in all disturbed soils. In contrast to the N/O trend, mineralization index O/Y in disturbed upper soil layers and in 30S lower one was significantly higher with respect to undisturbed soils. The humification index (B/E3) was lower in all sloping soils. AL/AR index showed few significant differences, with the exception of the upper soil layer from HD sloping soils and LD5S values were higher compared to undisturbed ones (p < 0.05).

4. Discussion

4.1. Effects of animal density on soil properties

4.1.1. Soil characterization In this study, grazing disturbance was a determining factor in environmental impact assessment, thus leading to significant changes in soil organic matter properties (Bardgett et al., 1998; Bardgett and Wardle, 2003; Prieto et al., 2011; Schlesinger et al., 1990; Yates et al., 2000). A significant effect of grazing activity on total organic carbon (TOC) and total nitrogen (TN) content was found (Table 1 and Fig. 2a). The lower values of TOC and TN found in HD upper soil layers, in fact, suggested an influence of grazing on the potential of

Table 1 Soil chemical properties and relative abundances of main pyrolytic peaks for all treatments studied (mean of three replicates  standard deviation).

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Table 2 ANOVA, used to evaluate the differences (p < 0.05) between density (HD and LD), slopes (0S, 5S, 30S) and layers (us, ls) and their interaction in chemical and chemicalstructural parameters (*, p < 0.05; ns, not significative). EC, Electrical Conductivity; BD, Bulk density; MR, Soil microbial respiration; WSC, Water Soluble Carbon; TEC, Total Extractable Carbon; HA, Humic Acids; FA, Fulvic Acids; N/O, furfural/pyrrole; B/E3, benzene/toluene; O/Y, pyrrole/phenol; Al/Ar, aliphatic/aromatic. Abbreviations as in Table 1.

Layer (L) Density (D) Slope (S) LD LS DS LDS

pH

EC

N–NH4

N–NO3

TN

O

Y

N

B

E3

E1

K

Al

Ar

TOC

WSC

TEC

HA

FA

BD

MR

N/O

B/E3

O/Y

Al/Ar

ns ns * ns ns ns ns

* * * * * * *

* * * ns * * *

* * * ns ns * ns

* * * * * ns ns

* * * * * * *

* * * * * * *

* * * * * * *

* * * * * * *

* * * * ns * *

* * * * * * *

* * * * * * *

* * * * * * *

* * * * ns * *

* * ns ns ns ns ns

* * * ns * ns ns

* * * * ns * ns

* * * * ns * ns

* * ns * ns * ns

* * * * * * *

ns * ns * ns ns ns

* * * * * * *

ns * * * ns * *

* * * * * * ns

* * * * ns * *

Fig. 2. Percentage variation (D%) of soil chemical characteristics between each treatment and the value of its undisturbed soil; table of reference of undisturbed soil values.* Dunnett’s test (p < 0.05). Legend as in Table 1. a) TOC, Total Organic Carbon; b) WSC, Water Soluble Carbon; c) TEC, Total Extractable Carbon; d) HA, Humic Acids; FA, Fulvic Acids.

organic matter decomposition and nutrient cycling. Similar results have been found by Prieto et al. (2011), who observed reduced values of TOC and TN content in grazing bare areas. These findings highlight the role on soil nutrient turn-over of vegetation and plant canopy, usually scanty in HD soils, as observed in the sites under study (Burke et al., 1999; Carrera et al., 2003, 2009; Mazzarino et al., 1998). Soil compaction, highlighted by the increase of the bulk density (Fig. 3a), due to excessive trampling, prevents the vegetation and root system development, resulting in low soil organic matter turn-over and nutrient release (Macci et al., 2012b; Prieto et al., 2011). According to TOC and TN trend, the more resistant pool of organic matter (humic substances), evaluated by total extractable carbon (TEC) assay, showed lower values in HD upper soil layers,

thus suggesting that grazing negatively affected also the highest stable soil organic matter (Macci et al., 2012b) (Fig. 2c). This decrease was generally due to the balanced reduction of HA and FA with respect to undisturbed soil, still maintaining the natural percentage of 50% in humic carbon, typical of forest soils, as noted by Zanelli et al. (2006) (Fig. 2d). High animal impact (HD soils) was also associated with lower concentrations of WSC (Fig. 2b), the form of carbon directly available for microorganisms (Macci et al., 2010). These lower values were probably due to the total removal of edible biomass in the soil (roots, grass, foliage and small branches) caused by animal activity (Garcia et al., 1997; Macci et al., 2010, 2012b), and to a rate of mineralization.

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Fig. 3. Percentage variation (D%) of soil physical and biological characteristics between each treatment and the value of its undisturbed soil; table of reference of undisturbed soils values.*Dunnett’s test (p < 0.05), Legend as in Table 1. a) Bulk Density; b) Microbial Respiration.

A significant lower microbial respiration (Fig. 3b), was also associated with the HD soils, thus meaning a relevant alteration of soil conditions in disturbed areas with an higher degree of grazing. Biological properties, such as microbial respiration, are widely considered to be more sensitive than chemical ones in the detection of changes induced by ecosystem disturbance (Macci et al., 2010; Masciandaro and Ceccanti, 1999). In contrast, different studies on the response of microbial activity in grazed soil, recognized the capability of forest soils in maintaining high level of microbial activity. Indeed, Relva et al. (2014) and Macci et al. (2012b), reported no reduction in biological properties in forest soils disturbed by invasive grazing. Decreasing grazing intensity (LD soils), soil characteristics (WSC, TOC, TN, TEC and its fractions, soil respiration) did not change significantly with respect to undisturbed soils (Table 1 and Figs. 2a–d and 3b). This trend was probably due to the contribution of light grazing on plant and animal fresh residues incorporated into the soil, thus preserving the organic matter content and biological properties (Macci et al., 2012b; Moody and Jones, 2000). However, a negative effect of grazing was also observed in LD, as showed by the increase in bulk density in both soil layers and lower slopes (5S and 0S), meaning a worsening of soil physical properties. In LD sites, where the vegetation was not totally compromised by animal pressure, the values of the different forms of carbon (labile and stable, WSC and TEC, respectively) were similar to values found in undisturbed soils. Probably, the presence of vegetation in LD sites, just slightly compromised, may have contribute, through root exudates and fresh residues release, to increase the nutrient level and consequently the soil organic matter turnover (Garcia et al., 1997; Macci et al., 2010). As highlighted by TEC content, low density grazing seemed not affect significantly the stable soil organic matter. The HA content, one of the most stable fraction of soil organic matter, was, in fact,

not significant different in disturbed soils, thus, demonstrating that a slight grazing activity had no effect in reducing the stable nucleus of humified organic matter. As expected in both animal densities studied, the lower soil layer showed no significant differences between disturbed and undisturbed treatments for TOC, TN and TEC values, suggesting that grazing induced an alteration mainly in soil surface (Franzluebbers and Stuedemann, 2009). However, the negative effect of grazing activity in HD soil sampled for sloping land, showed an impact also on WSC in the lower layer. These lower values could be probably due to a more intensive mineralization rate, which also involved the deepest layers. 4.1.2. Pyrolysis–gas chromatography (Py–GC) Py–GC enables the dynamic characterization of soil organic matter quality from a chemical-structural point of view. A close link between pyrolytic indices and animal disturbance was also observed. Differently from chemical parameters related to organic matter, where LD sites generally differed from HD ones, pyrolytic indices generally did not differ significantly, within the same soil, at the two animal densities tested (LD and HD) (Fig. 4a–d). The lower N/O index (the lower the ratio, the higher the mineralization of the labile soil organic matter) was found generally in both soil layers subjected to animal influence with respect to undisturbed ones, thus suggested the establishment of a mineralization process of the soil labile organic matter (Fig. 4a). This result was mainly due to the decrease of furfural (N) with respect to pyrrole (O) in disturbed soils, suggesting the reduction of rapidly metabolisable organic substances (Alcaniz et al., 1984; Ceccanti et al., 2007; Macci et al., 2012a), with furfural mostly derived from carbohydrates, ligno-cellulosic materials and other aliphatic organic compounds (Bracewell and Robertson, 1984)

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39

Fig. 4. Percentage variation (D%) of major pyrolytic indices between each treatment and the value of its undisturbed soil; table of reference of undisturbed soils values. *Dunnett’s test (p < 0.05), Legend as in Table 1. a) N/O, furfural/pyrrole; b) O/Y, pyrrole/phenol; c) B/E3, benzene/toluene; d) Al/Ar, aliphatic/aromatic (AL = E1 + K + N; AR = B + O + E3 + Y).

(Table 1). The greater mineralization process in disturbed soil can be due to two concomitant different processes: 1. Stimulation of biological activity, which leaded the degradation of mineralizable compounds most subjected to microbial attack (Aranda et al., 2015). 2. Great reduction of vegetation cover and soil compaction, resulting in reducing soil fresh organic matter turnover (Macci et al., 2012b). It is worth recalling that the former process seemed to be predominant in LD soils, while the latter is more evident in HD soils. In HD soils, in fact, the mineralization process also involved the more stable soil organic matter, as confirmed by the trend of mineralization index O/Y (the higher the ratio, the higher the mineralization of the stable organic matter) (Fig. 4b). Higher values in all disturbed upper soil layers were found. This result may be due to high value of pyrrole (O) in disturbed soils, which derives from nitrogenated compounds, humified organic matter, and microbial cells (Alcaniz et al., 1984; Ceccanti et al., 2007; Macci et al., 2012a). Furthermore, lower values of phenol (Y) in disturbed soils, which derives principally from humified stable organic matter, indicated the reduction of condensed aromatic structure (Macci et al., 2012a; Masciandaro and Ceccanti, 1999) as a consequence of fast metabolism, involving the native humic matter. Besides activating microbial metabolism, animal grazing as an external factor in forest ecosystem can, in fact, induce drastic change in balance within ecosystems, boosting mineralization processes (Macci et al., 2012b).

Moreover, in the lower soil layer O/Y generally has not shown significant fluctuations with respect to undisturbed ones, with exception of 30S, thus suggesting that grazing affected mainly soil surface. According to the trend of mineralization indices, lower values of B/E3 (the higher the ratio, the higher the condensation of the organic matter) were generally found in disturbed upper soil layers, while soil for the lower layer generally did not differ significantly with respect to undisturbed ones (Fig. 4c). B/E3 was related to the intensification of humification, because benzene (B) (lower in disturbed soils) derived mainly from pyrolytic degradation of condensed aromatic structures, while toluene (E3) came from non-condensed aromatic rings with aliphatic chains (Aranda et al., 2015). Lower abundance of B fragment in disturbed soils indicated the loss of the humified stable nucleus of organic matter with a consequent reduction of soil quality (Aranda et al., 2015). The decrease in B/E3 values in soils exposed to grazing could suggest that the management influenced the more stable part of soil organic matter, thus slowing humification processes. The Al/Ar index (aliphatic/aromatic compounds), expressed the ratio between the sum of aliphatic products (acetic acid, furfural, and acetonitrile) related to the presence of easily metabolizable materials, and the sum of aromatic compounds (benzene, toluene, and phenol), more resistant and stable to biodegradation (Alcaniz et al., 1984; Aranda et al., 2015; Ceccanti et al., 2007) (Fig. 4d). The increase in Al/Ar index observed in HD sloping soils and LD-5S soil was due to higher content in aliphatic compounds, which confirmed that grazing activity forced soil dynamics more towards

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mineralization processes than humification ones (Bondi et al., 2013). In contrast to the others indices, Al/Ar in LD soils did not differ from the respective undisturbed soil; this fact, it was mainly due to low incorporation of vegetal and animal fresh residues on soil caused by grazing. 4.2. Effects of slope in soil properties 4.2.1. Soil characterization The morphological characteristics of the soil, such as slope, have been a decisive factor in determining the grazing impact on soil quality. Animal presence may have contributed to EC increase (Table 1), in particular in disturbed flat soils, through a synergetic action between the incorporation of animal manure and the decrease of water content due to soil compaction (Macci et al., 2012b; Motavalli et al., 2003; Stewart and Meek, 1977; Wood et al., 1996). Higher values of N–NO3 and N–NH4 in 0S disturbed top soils were found with respect to undisturbed ones, suggesting a close relationship between animal disturbance and N cycle (Table 1). In flat areas, the input of animal manure has contributed to an increase in these parameters; this phenomenon, even though present also on the slopes, has been mitigated by the higher runoff, which have removed part of animal fresh residues. Moreover, a substantial increase in bulk density (Fig. 3a) was mainly evident in 5S and 0S soils, suggesting the worsening of physical conditions, irrespective of degree of animal density. Despite the effects of animal impact being evident in all HD disturbed treatments, soils on slopes seemed to be more susceptible to changes in chemical characteristics. In fact, chemical parameters linked to soil organic matter (TOC, TN, WSC, and TEC and its fractions), generally showed lower values in HD sloping soils compared to soil from the flatter areas (Table 1 and Fig. 2a–d). Some studies showed a progressive decrease in carbon content of soil, with increasing slope. This phenomenon is attributable to a greater runoff and transport of organic substances as slope increases (Hao et al., 2002; Ritchie et al., 2007). 4.2.2. Pyrolysis–gas chromatography (Py–GC) The trend of major pyrolytic indices showed a boost in mineralization processes of organic matter for sloping soils (decrease in N/O and B/E3, increase of Al/Ar) with respect to 0S

Table 3 Principal component analysis (PCA): Principal component loadings. *parameters used for PCA interpretation. Abbreviations as in Table 1 and 2.

pH EC N–NH4 N–NO3 TN TOC WSC TEC HA FA N/O B/E3 O/Y Al/Ar Bulk density Microbial respiration Explained variance Total proportionality

Factor 1

Factor 2

0.49 0.23 0.11 0.09 0.89* 0.86* 0.78* 0.89* 0.80* 0.94* 0.29 0.73* 0.07 0.56 0.24 0.05 5.76 0.36

-0.42 0.92* 0.17 0.92* 0.03 0.15 0.15 0.27 0.39 0.12 0.18 -0.23 0.81* 0.02 0.78* 0.05 3.55 0.22

soil, which seems to be more humified (Fig. 4a,c,d). This result confirms what is suggested by the trend in chemical parameters in this study, underlining that soil from flatter areas seems to be less susceptible to animal disturbance. 4.3. Principal components analysis The PCA multivariate statistical analysis gives a clearer picture of the relationship between parameters, the influence of the treatments on soil properties, and the interactions among the different factors (density, slope, depth). In order to highlight the variations between all disturbed soils, the control soils (undisturbed soils) were not considered for PCA analysis. PCA analysis isolated two principal components on all variables (PC) with a total variance of 61.2% (Table 3). The 1st PC (36.0%) included all the parameters related to humification processes: TN, TOC, TEC and its fractions (HA, FA), WSC and B/E3, while the 2nd PC (22.2%) loading included: EC, N–NO3, O/Y index of mineralization process of stable organic matter and bulk density (Table 3). The score plot (Fig. 5) provides a graphical representation of the different soils, identifying the parameters that were more

Fig. 5. Principal component analysis (PCA): Score plot. Legend as in Table 1. U, Upper Soil Layer; L, Lower Soil Layer.

G. Bondi et al. / Agriculture, Ecosystems and Environment 211 (2015) 32–42

associated with each other; in fact, the graphical closeness of a variable with an object in the plot showed a correlation between them. The HD and LD soils are clearly discriminated in the plot, and were associated to the different properties describing mineralization and humification processes. As expected, the LD soils were mainly linked to humification processes, being located in the left part of the plot, while the respective HD soils were shifted on the left, along factor 1. In terms of the different slopes, the 30S soils were mainly discriminated from 5S and 0S, along factor 2: all 30S soils present positive scores for factor 2, with the exception of HD top soil, while the other soils were located in the bottom part of the plot, thus reflecting an increase of mineralization process and a decrease of compaction with increasing slopes. The dramatic changes in soil organic matter quality caused by high animal grazing at increasing slopes were particularly evident: as humification process decreased, the mineralization of stable organic matter significantly increased (shift from bottom-right to top-left). On the other hand, in LD soils, the two concomitant processes of mineralization and humification process responded differently increasing the slope: 5S soils was less humified (shift across factor 1) with respect to the flat ones, while the 30S, even if maintaining the same level of humification process, showed an impressive effect of the mineralization process which involved the more stable part of organic matter (shift along factor 2). As expected, soil from lower layers, in all treatments, presented higher organic matter content, being located in the right side, with respect to their top soils. 5. Conclusions Pig rearing is an important element of disturbance in forest balance, especially in vulnerable environments with high geomorphological risk, as sloping soils. This study showed that grazing mostly affected soil chemical and chemical-structural properties through the direct effect of trampling on soil (compaction, soil organic matter losses, etc.) and indirectly, through the removal of vegetation caused by animal activity, which results in reducing the soil chemical fertility. Grazing at high animal density showed a worsening of all soil properties, thus resulting in a loss of soil quality. Grazing at low animal density generally seemed not to affect chemical fertility of soil, preserving organic matter content, even though a significant worsening of chemical-structural and physical characteristics was present. Soil damage was also evident as the slope increased: the steeper the slopes, in fact, the grater the rate of soil mineralization processes, which involves also the stable form of the organic matter. On the other hand, soil compaction seems to be less affected by animal pressure at increasing slope gradient. Grazing activity and sloping lands seemed to make soil less resilient, highlighting an irreversible degradation in soil quality. Grazing activity in sloping soils, associated with both high and low animal densities, seemed to compromise the soil dynamic organic matter cycle, in both lower and upper soil layers, slowing humification process and speeding up mineralization process of labile and stable organic matter. The association of different animal densities to different sloping degrees is a key factor in soil management to be considered in order to maintain and recover soil quality. The European Organic Regulation 834/2007 requires particular attention to housing conditions, husbandry practices and stocking densities which should be based on soil disease prevention (EU, 2007).

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On the basis of the European regulations this study suggests not only the use of a low animal density but short residences times of permanence in the same area. A rotational grazing, basis within a select number of paddocks, may be utilised for short periods before the animals are moved on. A possible hypothesis is to limit grazing in vulnerable areas, such as forest ecosystems, particularly with steep slopes. Restrict access to grazing only in forest fruiting times can be an efficient solution in order to maintain the forest natural regeneration rates. According to the European Organic Regulation 834/2007, the choice of breeds should take into account their capacity to adapt to local conditions and to meet animals nutritional and behavioural requirements, for both respecting animal welfare and preserving the natural ecosystem balance. References Alcaniz, J.M., Seres, A., Gassiot-Matas, M., 1984. Diferenciacion entre humus mull carbonatado y mull evolucionadopor Py–GC. 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