Sampling season affects conclusions on soil arthropod community structure responses to metal pollution in Mediterranean urban soils

Geoderma 226–227 (2014) 47–53

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Sampling season affects conclusions on soil arthropod community structure responses to metal pollution in Mediterranean urban soils Lucia Santorufo a,⁎, Cornelis A.M. Van Gestel b, Giulia Maisto a a b

Department of Structural and Functional Biology, University of Naples Federico II, Complesso Universitario di Monte Sant’Angelo, via Cinthia, 80126 Naples, Italy Department Ecological Science, Faculty of Earth and Life Sciences, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands

a r t i c l e

i n f o

Article history: Received 16 November 2012 Received in revised form 19 November 2013 Accepted 2 February 2014 Available online 22 March 2014 Keywords: Climatic conditions Soil arthropod Acarina Collembola Metal pollution

a b s t r a c t This study aimed to assess if the period of sampling affected conclusions on the responses of arthropod community structure to metal pollution in urban soils in the Mediterranean area. Higher temperature and lower precipitation were detected in autumn than in spring. In both samplings, the most abundant taxa were Acarina and Collembola, although their relative abundances were differently affected by seasonality and metal contamination. The relative abundance of Acarina was higher in autumn and positively related with soil total Cu, whereas Collembola abundance was higher in spring and correlated with water-extractable Cu. Arthropod community was heavily affected by seasonal variations in climatic conditions in high and low polluted soils, showing for the same soil different responses dependent on the sampling season. Sampling time therefore is a fundamental factor when assessing the effects of metal pollution on soil arthropod communities. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Soils host the greater part of the terrestrial biosphere. Soil arthropod communities are extremely rich in species, comprising a high proportion of diversity, and contribute to fundamental services for terrestrial ecosystems (Brussaard et al., 1997; Chapman, 2012; Faber and van Wensem, 2012). Arthropods, in fact, play an important role in decomposition processes through litter breakdown and faecal production, and top-down control of decomposers (Sackett et al., 2010). Beside their fundamental role in nutrient cycling, arthropods contribute to the maintenance of good soil quality (Brussaard et al., 1997). Mediterranean soils are the product of interactions between natural processes and human activities that have sometimes been beneficial but all too often have led to more or less advanced environmental degradation (De Franchis and Ibanez, 2003). Mediterranean arthropod distribution is strongly dependent on climatic conditions as the ecosystems in this area are characterized by large diurnal, seasonal, annual and inter-annual oscillations (Stamou et al., 2004). Changes in climatic condition together with soil use can directly alter soil properties such as temperature, moisture content, chemical composition, and physical properties. These alterations consequently lead to a different soil arthropod community assemblage and, in turn, alter important ecosystem services such as litter decomposition and nutrient cycling (Castro et al., 2010; Kardol et al., 2010).

Many studies describe effects of climatic condition on soil fauna in Mediterranean forests or areas not impacted by human activities (Cortet and Poinsot-Balaguer, 1998; Doblas-Miranda et al., 2007; Gergócs et al., 2011; Stamou and Argyropoulou, 1995). These studies suggest that abundance and diversity of soil invertebrates may differ dependent on the season of sampling. In fact, different seasons are characterized by different climatic conditions as well as different parts of the life cycles of organisms. This may also affect the response of soil invertebrates to pollution. A previous study (Santorufo et al., 2012) highlighted variations in arthropod community structure in soils differently contaminated with metals. Despite the growing interest about, little is known on the effects of climatic conditions on soil invertebrates in metal polluted soils. The present study aimed at evaluating the structure of soil arthropod communities exposed to metal polluted soils in two different seasons, in autumn after a warmdry summer period and in spring after a cold-humid winter period, in an urban Mediterranean area. In particular, this study tried to assess if conclusions on the response of the arthropod community structure to metal pollution can vary depending upon the season of sampling. Our hypothesis was that the long-term exposure has shaped the soil arthropod communities in metal-polluted field sites in such a way that differences would be clearly independent of the time of sampling. 2. Materials and methods 2.1. Soil sampling

⁎ Corresponding author. Tel.: +39 081 679095; fax: +39 081 679223. E-mail address: [email protected] (L. Santorufo).

http://dx.doi.org/10.1016/j.geoderma.2014.02.001 0016-7061/© 2014 Elsevier B.V. All rights reserved.

Starting from the results obtained in a previous sampling (September 2010) and reported in Santorufo et al. (2012), further sampling was

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carried out at the same sites and in the same way in April 2011. All the sites are filling soils about 200 years old. RS1 and RS2 are gardens near a road side, MW1 and MW2 are gardens near a motorway, UP is a garden at the centre of an urban park. At each garden that was approximately 100 m2, five samples were collected at 20 m apart. 2.2. Climatic conditions of the investigated area Data on the climatic conditions of the investigated area from April 2010 to April 2011 were obtained from the web-site: http://www. ilmeteo.it. In particular, for downtown Naples, monthly rainfall and mean temperature were considered and reported in Fig. 1. 2.3. Physical and chemical analyses The soils were characterized for pH, measured in a soil:distilled water suspension (1:2.5 = w:w) by electrometric method, for organic matter content, evaluated by loss of weight after ignition at 500 °C for 8 h, and water content, determined by gravimetric method after ovendrying to constant weight at 105 °C. These analyses were carried out following the methods reported by Allen (1989). The soil Cu and Pb concentrations were measured after sieving (2 mm) and oven drying (75 °C) the soil samples. To measure total metal concentrations, 0.1 g oven-dried soil samples were digested with 2 ml of a mixture (4:1 = v:v) of HNO3 (65%, p.a., Riedel-deHaën, Seelze, Germany) and HCl (37%, p.a., Baker Philipsburg, NJ, USA) at 140 °C for 7 h in a macro-destruction oven. To measure water-extractable metal concentrations, an oven-dried soil:distilled water suspension (1:2.5 = w:w) was prepared, shaken for 2 h at 200 rpm and filtered over a 0.45 μm Whatman filter. Cu and Pb concentrations were measured by atomic absorption spectrometry equipped with a graphite furnace unit (PerkinElmer 5100). The quality of the analysis was checked using ISE sample 989 (International Soil-Analytical Exchange) certified by Wageningen Evaluating Programs for Analytical Laboratories as reference material. Recoveries of Cu and Pb were always within 10–15% of the certified concentrations. The metal concentrations were reported as μg g− 1 dry weight (d.w.) and in order to have a summed measure of soil contamination, metal concentrations were also reported as the sum of toxic units (ΣTUs). TUs were calculated as the ratio between measured and background metal concentrations in the soils. The background levels of total (4.53 μg Cu g− 1 d.w.; 18.7 μg Pb g− 1 d.w.) and waterextractable metal concentrations (0.07 μg Cu g−1 d.w.; 0.02 μg Pb g−1 d.w.) were measured in the natural standard soil Lufa 2.2 (Speyer,

2.4. Arthropod community analyses The analyses of the soil communities were performed on five subsamples collected at each site. To extract the arthropods, the soil samples were placed in a Tullgren apparatus at VU University (Amsterdam, The Netherlands) for 4 weeks following the method of Van Straalen and Rijninks (1982). The air temperature above the samples was 30 °C while the bottom of the samples was kept at 5 °C. The arthropods were collected in jars containing a 70% ethanol solution. In the final step, the animals were counted and identified according to the major taxonomic groups. The results of the arthropod community analyses are reported as density (i.e. individual number/m2 soil), richness (sum of different taxa in each soil) and relative abundance (i.e. individual number of each taxon/total number of organisms). In addition, for each sampling the Shannon (1948), Simpson (1949), Menhinick (1964), and Pielou (1969) indices, Acarina/Collembola ratios and the QBS index (Parisi et al., 2005) were calculated as reported in Santorufo et al. (2012). 2.5. Statistical analyses

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The Kolmogorov–Smirnov test was applied to assess the normality of the distribution of the data sets. Pearson's regression test was performed to evaluate the correlations (considered significant when P b 0.05) between the parameters describing the community and the individual physical–chemical soil characteristics. One-way Analysis of Variance (ANOVA), with Holm–Sidak posthoc test, was performed to highlight differences (considered significant when P b 0.05) among the sites with respect to the parameters describing the community and soil metal concentrations. Student t-test was carried out to highlight differences in each investigated parameter between the samplings. Sigma-Plot 11.0 (Jandel Scientific, San Josè, USA) was used for all these analyses. In order to test the direct relationships between biological parameters and the season or soil properties, a redundancy analysis (RDA), a canonical multivariate method, was carried out by the package Syntax 2000 (Australia). The RDA was carried out considering independent variables such as air temperature, soil water and organic matter content, soil total and water-extractable Cu and Pb, and dependent variables such as soil organism density, taxa richness, and relative abundance of Acarina and Collembola (the most abundant taxa). To further investigate the influence of abiotic factors identified by the RDA, some biological parameters (i.e. density, richness, Acarina and Collembola abundances, and QBS index) were related to soil organic matter content, ΣTUs, and Cu and Pb concentrations obtained at both sampling times.

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A pr ' M 10 ay ' Ju 10 n '1 Ju 0 l' 1 A 0 ug ' Se 10 p '1 O 0 ct '1 N 0 ov ' D 10 ec '10 Ja n '1 Fe 1 b '1 M 1 ar ' A 11 pr '11

Precipitation (mm)

Temperature Precipitation

Temperature (°C)

Germany). For each site and sampling time, the chemical and physical analyses were performed in triplicate.

Fig. 1. Mean temperature (black line) and rainfall amount (dotted lines) in the investigated area of downtown Naples from April 2010 to April 2011; the arrows indicate the sampling times. Data were obtained from the web-site: http://www.ilmeteo.it/.

3.1. Climatic conditions and soil physical and chemical properties Over the investigated period, the area showed a typical Mediterranean climate with a warm and dry summer, and a cold and rainy winter (Fig. 1). The mean temperature and total amount of rainfall in the last 3 months before the samplings in autumn (September 2010) and spring (April 2011) were 25 °C and 100 mm and 10 °C and 250 mm, respectively. Soil pH-H20 ranged between 5.45 and 7.33 (Table 1), and was lowest at RS1 compared to all other sites. The soil organic matter content was particularly high at RS2 and UP, for both the samplings, where also the highest water content was measured (Table 1). Soil pH and organic matter content did not differ between the samplings, whereas the mean soil moisture content was significantly (P b 0.05) higher in spring 2011 (water content 34.5 ± 5.77% d.w.) than in autumn 2010 (water content 15.1 ± 2.58% d.w.) (Table 1).

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Table 1 Mean (±s.e.) pH, organic matter (OM), water content (WC) and total (tot) and water-extractable (w.e.) metal concentrations and total (tot) and water-extractable (w.e.) of toxic unit sum (ΣTU) of urban soils from Naples, Italy. Different capital and small letters indicate statistically significant differences among the sites for the samplings in September 2010 and April 2011, respectively (One-way Analysis of Variance with Holm-Sidak post-hoc test at P b 0.05). In bold the lowest and highest values of total and water-extractable Cu, Pb concentrations and the ΣTU are reported. Asterisks indicate the statistically significant differences of metal concentrations between autumn and spring for each site (One-way Analysis of Variance with HolmSidak post-hoc test at P b 0.05). Soils

pH

OM (% d.w.)

WC (% d.w.)

Cutot (μg g−1 d.w.)

Pbtot (μg g−1 d.w.)

Cuwe (μg g−1 d.w.)

Pbwe (μg g−1 d.w.)

ΣTUtot

ΣTUwe

RS1 aut

5.45A (0.01) 6.33a (0.04) 7.11A (0.01) 6.64a (0.01) 6.88A (0.00) 6.93a (0.02) 7.33A (0.00) 6.96a (0.02) 7.27A (0.02) 6.70a (0.06)

10.1A (0.03) 8.59a (3.47) 25.7B (0.48) 25.3b (4.69) 10.1A (0.16) 11.5a (2.29) 11.1A (0.03) 13.0a (1.89) 16.7C (0.06) 18.7c (0.30)

6.8A* (0.02) 27.6a (1.38) 21.2A* (0.15) 54.0b (0.02) 13.5A* (0.11) 34.1a (1.89) 14.2A (0.04) 19.4c (1.58) 19.9A* (0.06) 37.44a (1.65)

90.0 A * (2.91) 30.6 a (3.63) 176 B * (5.09) 114 b * (8.65) 73.5 C * (1.26) 33.7 a (1.62) 146 D * (4.81) 58.7 a (6.36) 43.8 E * (1.74) 26.6 a (2.18)

218 A * (6.39) 76.0 a (8.45) 233 A * (3.87) 94.9 a (7.41) 183 B * (0.97) 126 a (6.56) 695 C (63.90) 684 b (114) 109 B (3.58) 167 c (80.6)

0.23 A (0.03) 0.58 a * (0.11) 0.43 B (0.03) 0.62 a * (0.03) 0.20 A (0.00) 0.51 a * (0.03) 0.16 AC (0.00) 0.40 ab * (0.04) 0.06 C (0.00) 0.35 b * (0.08)

0.03 A (0.00) 0.14 a * (0.04) 0.04 A (0.00) 0.07 b * (0.01) 0.02 B (0.00) 0.14 a * (0.01) 0.15 C (0.00) 0.10 c (0.03) 0.02 B (0.01) 0.09 c * (0.03)

31.5 A (0.83) 10.8 a* (1.19) 51.3 A (1.33) 30.3 b* (1.86) 25.9 A (0.27) 14.2 a* (0.63) 69.4 B (4.47) 49.6 c (7.44) 15.5 C (0.37) 11.0 a (3.97)

5.83 A* (0.37) 16.2 a* (3.53) 9.39 B (0.72) 13.1 b* (0.71) 4.48 C (0.00) 15.0 c* (0.68) 12.2 D (0.00) 11.1 d (1.67) 1.87 E (0.40) 10.1 e* (0.55)

RS1 spr RS2 aut RS2 spr MW1 aut MW1 spr MW2 aut MW2 spr UP aut UP spr

For both the samplings, the total and water extractable Cu and Pb concentrations in the soils showed wide variations among the sites, clearly representing a gradient of pollution. The highest total and water-extractable Cu concentrations were detected at RS2 for both the samplings, whereas the highest total Pb content, sum of total TUs and high total Cu content were measured at MW2 for both the samplings. In the urban park (UP), the lowest Cuwe and Pbwe concentrations, and sum of water-extractable TUs were measured (Table 1). In general, Cutot and Pbtot concentrations and ΣTUtot were higher in autumn than in spring, whereas Cuwe, Pbwe and ΣTUwe were higher in spring (Table 1).

3.2. Analysis of the soil mesofauna community The highest arthropod density was measured in the soil collected at the urban park (UP), but only for the sampling in autumn it was significantly different from all the other sites (Fig. 2a), whereas the lowest density was detected at RS1 and MW2, respectively in autumn and spring. On average, the density was higher in autumn. Density showed

a

wide differences among the sites with highest values detected at UP for both seasons (Fig. 2a). For each sampling, the sum of taxa did not differ among the sites, and it was significantly (P b 0.05) higher in autumn than in spring (Fig. 2b). For both samplings, the relative soil arthropod abundances did not differ among the sites. The most abundant taxa were Acarina and Collembola, which dominated the community (87%). For this reason only these two taxa were chosen to perform the RDA. Diplopoda, Blattoptera larvae, Chilopoda, Symphyla and Diptera larvae accounted for about 10% (Fig. 3). Other taxa found were Isopoda, Lepidoptera larvae, Diplura, Araneae, Formicidae, Tysanoptera, Blattoptera, Pseudoscorpiones, Embioptera, Diptera, and Pauropoda, which together accounted for the remaining 3% and were grouped in others (Fig. 3). Acarina, Collembola and Diplopoda showed the highest relative abundance. In all the soils collected in autumn, the relative abundance of Acarina was higher than that of Collembola and Diplopoda, whereas in spring the relative abundance of Acarina decreased and that of Collembola increased (Fig. 3). In addition, in autumn the relative

b

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Fig. 2. Mean (±s.e.) a) organism density and b) taxa richness of soil arthropod communities collected in the soils from different sites in downtown Naples, Italy, in September 2010 (white bars) and in April 2011 (fine pattern bars). Different capital and small letters indicate statistically significant (P b 0.05) differences among the sites, respectively, for autumn and spring (One-way Analysis of Variance with Holm–Sidak post-hoc test).

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MW1 100

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0 A Co car lle ina m Di bol a pl o Bl C po att hil da op op ter od al a a Sy rva Di mp e h pt er yla al ar va e Ot he r

A Co cari lle na m Di bol a pl o Bl Ch poda att op ilop ter od al a a Sy rvae Di mp pt er hyla al ar va e Ot he r

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A Co car lle ina m D bo ip la lo Bl C po at hi da to lo pt po er a l da a Sy rva D m e ip ph te ra yla la rv ae O th er

Relative abundance (%)

RS1 100

Fig. 3. Mean values of relative abundance of the different taxa found in the soils collected from different sites in downtown Naples, Italy, in September 2010 (white bars) and in April 2011 (fine pattern bars).

abundance of Acarina was significantly higher than those of Collembola and Diplopoda, while in spring the relative abundance of Acarina did not significantly differ from that of Collembola but the relative abundances of these two taxa significantly differed from that of Diplopoda (Fig. 3). In general, in spring the relative abundance of Acarina was significantly lower than in autumn, while the relative abundance of Collembola was significantly higher (Fig. 3). The Redundancy analysis (RDA) showed a clear site separation on the basis of sampling season, with all the soils collected in autumn on one side and all soils collected in spring on the other side (Fig. 4).

Organism density, taxa richness and abundance of Acarina were more abundant in autumn, and positively related with air temperature, soil organic matter content, and total Cu content (Fig. 4). Collembola showed high abundance in soils collected in spring, and abundance was positively related to soil water content and water-extractable Cu content. For both samplings, a sharp separation is shown by the MW2 site, which was rich in total Pb content and poor in soil fauna (Fig. 4). The biological indices analysis highlighted contrasting results among the soils and between the sampling times. The diversity indices showed different results: Shannon index suggested that diversity in autumn was highest at RS1 and in spring at RS2, whereas Simpson index highlighted highest biodiversity at RS2 both in autumn and in spring; both indices showed lowest diversity at MW1 in autumn and at RS1 in spring (Table 2). Menhinick and Pielou indices showed the highest evenness in autumn at RS1 and in spring at MW2, but according to Menhinick evenness was lowest at UP in autumn and at RS1 in spring while Pielou found lowest evenness at UP both in autumn and spring (Table 2). The highest ratio between Acarina and Collembola was observed at MW2 in autumn and at RS1 in spring, while the lowest ratios were found at RS1 in autumn and at RS2 and UP in spring (Table 2). The QBS index indicated soil quality was highest at UP in both the seasons, but lowest at RS1 in autumn and at MW2 in spring (Table 2). Arthropod density, richness, QBS index, Acarina abundances increased with increasing soil organic matter content and Cutot concentrations, whereas Collembola abundances decreased. By contrast all the parameters decreased with increasing of Pbtot concentrations and ΣTUtot (Fig. 5). At intermediate values of ΣTUtot and Pbtot concentrations, these biological parameters showed small variations between the two sampling seasons, but the variations were higher in the sites with lower and higher ΣTUtot and Pbtot concentrations (Fig. 5). 4. Discussion

Fig. 4. Results of ordination (RDA) analysis of data on the arthropod community in soils sampled in downtown Naples, Italy, in two seasons. RDA was analysed taking into account sites, soil parameters, climatic conditions, arthropod density, taxa richness, Acarina and Collembola abundance. Two tables were constructed with fauna data and climatic conditions and soil parameters. The figure represents the constraint ordination of the site samples, soil parameters (water content, organic matter content, soil total and water extractable Cu and Pb concentrations), climatic conditions (temperature) and soil fauna.

The study area of downtown Naples is inserted in a typical Mediterranean climate, characterized by strong fluctuations in temperature and precipitation between the seasons. Although the mean temperature and precipitation were similar for the two months of sampling, the seasonal values, calculated as the mean of the three months before sampling,

133BC (8.90)* 83.2A (8.04) 92.0AC (11.9)* 145B (12.9)* 1.9a (0.60) 2.44a (0.19) 2.57a (0.10) 1.92a (0.53) 14.5AB (4.70)* 4.15AB (0.81)* 15.0B (2.9)* 5.21AB (2.5)* 0.64a (0.04) 0.67a (0.05) 0.78b (0.05) 0.57a (0.02) 0.52A (0.05) 0.52A (0.04) 0.56A (0.02) 0.43B (0.04) 0.82a (0.11) 0.80a (0.16) 1.19b (0.19) 0.73a (0.05) 0.95A (0.08) 0.92A (0.14) 0.85A (0.06) 0.80A (0.04) 0.42a (0.05) 0.43a (0.05) 0.47a (0.11) 0.44a (0.02) 0.38A (0.08) 0.49A (0.05) 0.41A (0.02) 0.46A (0.04) 1.12a (0.12) 1.10a (0.18) 0.98a (0.11) 1.80a (0.04) 1.24A (0.11) 0.97A (0.09) 1.15A (0.05) 1.13A (0.09) RS2 MW1 MW2 UP

Spring

47.0a (2.00) 98.0b (4.06) 86.8b (13.8) 40.0a (7.73) 109c (2.92) 78.0 A (16.0)* 3.53a (1.92) 1.98A (0.71)* 0.62a (0.03) 0.60A (0.06) 0.70a (0.17) 1.16A (0.10)* 0.54a (0.05) 0.41A (0.09) 0.83a (0.10) 1.36A (0.10)* RS1

QBS

Autumn Spring

A/C

Autumn Spring

Pielou

Autumn Spring

Menhinick

Autumn Spring

Simpson

Autumn Autumn

Spring Shannon

Table 2 Mean (±s.e.) of the Shannon, Simpson, Menhinick and Pielou indices, the Acarina and Collembola ratios (A/C), and the soil biological quality indices (QBS) calculated for the invertebrates collected from urban soils from Naples, Italy, in September 2010 (autumn) and April 2011 (spring). Different capital and small letters indicate statistically significant differences among the sites for the samplings in autumn and spring respectively (One-way Analysis of Variance with Holm–Sidak post-hoc test at P b 0.05). In bold and italic the highest and the lowest values of biological indices, respectively are reported. Asterisks indicate the statistically significant differences among the samplings (One-way Analysis of Variance with Holm–Sidak post-hoc test at P b 0.05).

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strongly differed, showing a cold and rainy winter and a hot and dry summer (Fig. 1). Soil water content appeared directly dependent on precipitation, showing higher values in spring after a rainy winter (Fig. 1) than in autumn (Table 1). By contrast, soil pH and organic matter content were not affected by climatic conditions and sampling time (Table 1). Soil metal content varied among the soils and between the sampling times. In particular, the most polluted soils (MW2 and RS2), showing the highest ΣTU contents and Cu and Pb concentrations, were placed in proximity to very busy urban roads and motorways, which acted as mobile sources of Cu and Pb (Davis et al., 2001). The variations in total Cu and Pb concentrations detected between the two samplings could be mainly due to the high heterogeneity of the investigated areas. On the other hand, highest metal water solubility was measured in the rainy period, likely due to the high soil water content. In fact, high rainfall can lead to an increase of dissolved organic matter concentration in the pore water. Since the dissolved organic matter forms stable, soluble complexes with heavy metals (Ashworth and Alloway, 2004) an increase of dissolved organic matter content can also lead to an increased metal concentration of the soil pore water. Different sampling times can be characterized by different climatic conditions that, altering soil microclimate and indirectly modifying resource availability and food web composition (Block et al., 1990; Frampton et al., 2000), affect arthropod community structure. In addition, soil arthropod abundance will fluctuate due to normal seasonal variations associated with the life cycle of the different species. In fact, the performed RDA highlighted that organism density and richness sharply differed between autumn and spring. High temperatures in summer caused an increase of organism density and taxa richness in autumn (Fig. 4). Cold-wet conditions caused a substantial reduction of organism density and richness that occurred to the same extent for each sampling site (Fig. 2). The obtained results agree with those reported for Mediterranean climatic conditions by various authors (Antunes et al., 2008; Stamou et al., 2004; Touloumis and Stamou, 2009) who found an increase of arthropod abundance and taxa richness in periods characterized by high temperature. In particular, Stamou et al. (2004) reported that in Mediterranean fields the optimum temperature for soil arthropods is around 20 °C and lower values result in a significant decline of organism activity, which, in turn, affects arthropod growth and abundance. On the other hand, the correspondence between high temperature and high arthropod density and richness is not always reported for the Mediterranean environment in the scientific literature. In fact, Doblas-Miranda et al. (2007) found higher arthropod abundances and higher species richness during the cold-rainy period. In addition, in environments different from the Mediterranean, soil arthropod communities display a period of explosive growth with the arrival of the rainy season and with increasing soil moisture content (Ferguson, 2001; Raghubanshi et al., 1990; Reddy et al., 1994; Wiwatwitaya and Takeda, 2005; Zhu et al., 2010) or under warm-wet conditions (Harte et al., 1996). Further investigations are needed to clarify the effects of climatic conditions on soil arthropod communities in a Mediterranean context. Community taxa composition varied between the two seasons, with Acarina more abundant during warm-dry conditions and Collembola more abundant during cold-wet conditions (Figs. 3 and 4). These differences can be due to the organism life cycle that is partially dependent on the different climatic conditions. Several authors (Cortet and Poinsot-Balaguer, 1998; Kardol et al., 2011; Zhu et al., 2010) found that Acarina density was generally higher in warm conditions, while collembolan abundance was higher in cold-wet conditions. The high Collembola abundance found after a rainy period could be due to higher fungal biomass (Hawkes et al., 2011) that represents Collembolan main food source (Hopkin, 1997). The relative abundances of the other less abundant taxa found in the investigated area did not significantly differ between the different climatic conditions (Fig. 3). However, among the rare taxa, Chilopoda abundance strictly depended on soil water and organic matter content as confirmed by the reported

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Richness (n° taxa/site)

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40000 30000 20000 10000 0 16 12 8 4

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Organic matter (% d.w.)

Fig. 5. Relationships between different biological parameters describing soil arthropods communities in urban soils sampled in downtown Naples with selected soil parameters, including total Cu and Pb concentrations (Cutot, Pbtot), the summed metal concentrations expressed as toxic units (ΣTUtot) and soil organic matter content. Data are shown for both samplings performed in September 2010 and April 2011 (black and white spots, respectively).

significant correlations. Therefore, Chilopoda, more than the other rare taxa, were sensitive to soil moisture content. In urban areas, besides seasonality and climatic conditions, soil pollution and resource availability also affect arthropod distribution. In our study, the soil arthropod community showed linear responses to organic matter content and metal contamination level, confirming the central role of these two parameters in influencing the organisms (Fig. 5). However, arthropod responses to abiotic properties strongly differed between the two samplings, indicating that seasonal climatic variations may alter the responses of organisms to the different abiotic properties. In the soils with the highest and the lowest metal contamination level (RS2, MW2 and UP), arthropod abundance, richness, QBS and Acarina abundances showed the strongest decrease in spring, whereas the soils with moderate metal contamination (RS1 and MW1) showed no differences in arthropod abundance between the seasons (Figs. 2a, 5). This finding may suggest that the high and low polluted soils present an arthropod community dominated by few species well adapted to extreme conditions, whereas the moderately polluted soils may have an arthropod community more homogenous and therefore more tolerant to fluctuating conditions. The negative effects of metal

pollution on arthropods seemed to be mainly due to Pb rather than to Cu, as the biological parameters showed a linear negative relationship with soil Pb but less with Cu concentrations. Pb is a non-essential metal and its accumulation in body organisms can cause more damage than essential elements such as Cu. The differences detected between the seasons in the several arthropod community parameters were confirmed by the values of the biological index calculations. In the present study the values of the considered indices, except for the Simpson index, differed between the sampling times (Table 2). This confirms that sampling time is fundamental in considering the responses of soil organisms to different environmental conditions. Conclusions regarding the ecological effects of metal pollution therefore may be different depending on the sampling season. This disagrees with our hypothesis that community structure would be shaped by long-term exposure to metal pollution, and therefore should not differ depending on the time of sampling. In conclusion, the present study demonstrates that seasonal variations in climatic conditions affect soil arthropod community structure more in urban soils with low and high pollution than in moderately polluted soils, in which arthropod community structure seems to be

L. Santorufo et al. / Geoderma 226–227 (2014) 47–53

weakly affected by the sampling time. Therefore, seasonal variations should be taken into account when metal pollution effects on soil arthropod communities are investigated.

Acknowledgements The experimental work for this study was performed at VU University, Amsterdam, The Netherlands during a PhD visiting period. The authors wish to thank Matty Berg for helping in taxa identification and RudoVerweij for his valuable help in the experimental work.

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