Does distance from the sea affect a soil microarthropod community?

Acta Oecologica 76 (2016) 39e46

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Original article

Does distance from the sea affect a soil microarthropod community? Haggai Wasserstrom, Yosef Steinberger* The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, 5290002, Israel

a r t i c l e i n f o

a b s t r a c t

Article history: Received 4 April 2016 Received in revised form 20 July 2016 Accepted 8 August 2016 Available online 17 August 2016

Coastal sand dunes are dynamic ecosystems characterized by strong abiotic gradients from the seashore inland. Due to significant differences in the abiotic parameters in such an environment, there is great interest in biotic adaptation in these habitats. The aim of the present study, which was conducted in the northern Sharon sand-dune area of Israel, was to illustrate the spatial changes of a soil microarthropod community along a gradient from the seashore inland. Soil samples were collected from the 0e10 cm depth at five locations at different distances, from the seashore inland. Samples were taken from the bare open spaces during the wet winter and dry summer seasons. The soil microarthropod community exhibited dependence both on seasonality and sampling location across the gradient. The community was more abundant during the wet winter seasons, with an increasing trend from the shore inland, while during the dry summers, such a trend was not observed and community density was lower. The dominant groups within soil Acari were Prostigmata and Endeostigmata, groups known to have many representatives with adaptation to xeric or psammic environments. In addition, mite diversity tended to be higher at the more distant locations from the seashore, and lower at the closer locations, a trend that appeared only during the wet winters. This study demonstrated the heterogeneity of a soil microarthropod community in a coastal dune field in a Mediterranean ecosystem, indicating that the gradient abiotic parameters also affect the abundance and composition of a soil microarthropod community in sand dunes. © 2016 Elsevier Masson SAS. All rights reserved.

Keywords: Acari Community Gradient Microarthropods Sandy soil ecosystem

1. Introduction Sand dunes are accumulations of sand created by wind, and they are mostly common in deserts, seashores, and rivers. They are widely distributed across the globe, as today, about 10% of the land area between 30
N and 30
S is covered by sand deserts (Sarnthein, 1978). Sand-dune ecosystems are characterized by harsh conditions and are low in nutrients (Hesp, 1991; Willis, 1963; Willis and Yemm, 1961), causing physical stress on biotic components that limits biomass accumulation below and above the ground. In contrast to the relatively stable nature of soils, sand-dune ecosystems are dynamic and usually in the process of successional changes (Foster and Tilman, 2000). Dune ecosystems represent the earliest stages in the development of soil (Jones et al., 2008). The most characteristic feature of coastal dunes is their connection to the seashore. This marine influence creates an environmental gradient across a coastal dunefield from the

* Corresponding author. E-mail address: [email protected] (Y. Steinberger). http://dx.doi.org/10.1016/j.actao.2016.08.005 1146-609X/© 2016 Elsevier Masson SAS. All rights reserved.

seashore inland due to physical stress caused by its proximity to the sea (McLachlan and Brown, 2006). The abiotic conditions are harshest near the shore due to winds that move sand particles and salt spray. Proceeding inland, the environmental conditions are more moderate, with a decrease in wind velocity and amount of salt spray (Hesp, 1988; Young, 1987), as well as a decrease in sandparticle transport rates (Goldsmith et al., 1990). Proceeding inland, these environmental features are assumed to cause a decrease in temperature extremes and alterations in the ratio between the coarse and finer particle fractions (Ranwell, 1972). These features affect the amount of organic matter, moisture levels, and sand movement, causing a decrease in pH, followed by changes in the composition of the plant community and its distribution (Kachi and Hirose, 1983; van der Valk, 1974; Wilson and Sykes, 1999). Due to the harsh environment, the number of terrestrial inhabitants adapted to survive in sand-dune habitats, mostly without natural shelter, is relatively low and dominated by arthropods, particularly insects that are considered typical of embryo and consolidated dunes. Arachnids are very common in sands (Almquist, 1969; Barnes, 1953; Cooke and Cotton, 1961), but usually the insects are the dominant inhabitants of sandy areas (Callan,

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H. Wasserstrom, Y. Steinberger / Acta Oecologica 76 (2016) 39e46

1964; Colombini et al., 2005; Ranwell, 1972; Russell, 2008; Spungis, 2002). Most of the research on arthropods focused on macroarthropods, while there is little information available on their smaller relatives e the microarthropods (Koehler et al., 1995; McLachlan and Brown, 2006), and much more research is needed. The biomass of the living organisms beneath the soil is almost 20 times larger than that of the humans living on it (Balogh, 1970), illustrating the richness of the world under our feet. On most beaches, sandy soil fauna is rich and diverse, and may have greater biomass than macrofauna, even though we can find 25 species in the soil on sandy beaches for every species of macrofauna above it (Armonies and Reise, 2000). However, very little is known about the sand dune mesofaunal communities (McLachlan, 1991). Soil microarthropods are one of the most important components of any terrestrial ecosystem (Santos et al., 1981; Steinberger and Wallwork, 1985) due to their role in controlling key functional processes, e.g., organic-matter decomposition and mineralization (Kaczmarek et al., 1995; Santos and Whitford, 1981; Wallwork, 1970; Whitford and Parker, 1989), soil formation (Persson, 1989), and nutrient cycling (Irmler, 1982; Powers et al., 1998). Many studies were conducted on soil microarthropodcommunity structure and composition in dry areas, but most of them were restricted to desert soils (Kamill et al., 1985; Steinberger, 1990; Steinberger and Whitford, 1985; Wallwork et al., 1985), without reference to sandy shore ecosystems. Information on the size and composition of mite populations in sandy shores was mostly restricted to cold and temperate climates (Kagainis and Eitminaviciute, 2011; Salmane, 1999, 2000), which are different in their features and soil biota from the dry Mediterranean region. While the gradient's effects on the flora and macrofauna of sand dunes, from the shore inland, have been studied in detail (Heykena, 1965; Isermann and Cordes, 1992; Jungerius, 1990; Rose, 1988; van Heerdt and Morzer-Bruyns, 1960; Willis, 1989), information on its effects on a soil microarthropod community is scarce, and limited to specific taxonomic groups in cold climates (Koehler et al., 1992, 1995). Moreover, these studies did not provide any information on the changes within this community during the different seasons of the year. Our aim in the present study was to examine the seasonal and spatial shifts in the soil microarthropod community's size and composition along a sand-duneeecosystem gradient, from the shore inland, on the eastern Mediterranean shore. In order to achieve this goal, we selected a study site that included a coastal sand-dune ecosystem consisting of shifting-to-semiestabilized dunes. Soil samples were collected at five sites along a 4 km transect, from the sea inland, during a two-year period. The samples were collected from bare, open areas, in order to minimize the effect of different microhabitats, created by the different flora at each location, as many studies showed significant differences in soil microarthropod communities among diverse plant species and bare soil (Noble et al., 1996; Steinberger et al., 1990). We hypothesize that microarthropod-community size and diversity will be determined by its distance from the seashore. The microarthropod community will increase and will be more diverse as it proceeds inland, due to the expected improvements in soil physical and biochemical conditions, e.g., lower salinity, increase in amounts of organic matter, and decrease in sand movement. 2. Materials and methods

rainfall of 580 mm, falling mainly during winter and early spring (November to February), and with maximum rainfall in December. The mean minimum daily temperature reaches 10.5
C in January, while the mean maximum daily temperature reaches 28.5
C in August. Winds in winter are intense and vary in their direction, while they are weaker in summer, with a stable regime. The sand dunes at this site vary from shifting to semi-stabilized and stabilized dunes, with vegetation cover dominated by shrubs and herbaceous annuals. According to Danin (Danin, 2005), this system is a unique Mediterranean ecosystem in which we can find the whole psammosere. 2.2. Soil sampling Soil samples were collected from the 0e10 cm depth at five locations (n ¼ 5) across a west-to-east transect, i.e., 100, 200, 1000, 2500, and 4100 m from the shore inland. The soil samples were collected from open spaces on four dates, i.e., 8/1/13 (winter 2012/ 13), 19/8/13 (summer 2013), 16/1/13 (winter 2013/14), and 21/8/14 (summer 2014). A total of 100 soil samples were collected during the study period. Each soil sample was immediately placed in an individual polyethylene bag and transported in an insulated cooler to the laboratory, where it was stored at 4
C. Stones, roots, and other organic debris were removed from the soils prior to physicochemical and biological analyses. 2.3. Soil analysis Subsamples from each replicate were analyzed for soil parameters. Soil moisture (SM) was determined gravimetrically by drying the soil samples at 105
C for 48 h and measuring the mass loss. Soil organic matter (OM) was detected by oxidation with dichromate in the presence of H2SO4 (Rowell, 1994). Salinity was measured by measuring electrical conductivity in a soil-water suspension (1:10 soil-water extract), and measured using an autoranging EC/temp meter (TH2400, EI-Hamma). pH was determined using a combined pH electrode in the filtered supernatant of a mixture of 20 g soil and 40 ml tap water. 2.4. Microarthropod extraction and identification A subsample of 150 g fresh soil was taken from each sample for microarthropod extraction within 48 h of field collection. Each subsample was placed separately in a modified Berlese-Tullgren funnel under standard 40 W light bulbs for 72 h for microarthropod extraction. The microarthropods were collected from the funnels, then counted and identified. A representative from each taxonomic unit was mounted on a slide and identified under a light microscope based on the available keys. Mites of the order Mesostigmata, suborders Prostigmata, Endeostigmata, and Oribatida, were identified to the family level using keys by Krantz and Walter (2009) and unpublished keys. Psocoptera (Insecta) and Collembola (Entognatha) were described at the order level. Acari feeding habits were determined for each family based on the feeding behavior reported in the literature (Krantz and Walter, 2009). Feeding behavior was divided into five groups: predators, algivores, fungivores, phytophages, and detritivores. When such information was not available, feeding habits were deduced based on that of closely related family.

2.1. Study site 2.5. Statistical analysis The study was conducted at the Caesarea coastal sand dunes located in the northern Sharon Plains, from the Mediterranean shore to four km inland, 32
480 N between 34
880 E and 34
930 E. The climate is sub-humid Mediterranean, with a multiannual mean

All data were subjected to statistical analysis of variance (ANOVA) using the statistical analysis system model (GLM). Duncan's multiple range tests were used to determine differences

D1 e 100 m, D2 e 200 m, D3 e 1000 m, D4 e 2500 m, and D5 e 4100 m e from the shore.

D5

0.12 0.027b^ 2.34b^ 7.72b^ 0.15 0.053a^ 1.95c^ 7.57c^

D4 D3

0.13 0.026b^ 2.1bc^ 7.55c^ 0.18 0.027b^ 2.44b^ 7.75ab^

D2 D1

0.18 0.03b^ 3.19a^ 7.79a^ 0.13ab* 0.028 3.05b* 7.72b* 0.13ab* 0.031 3.24b* 7.7b* 0.1b* 0.016 2.64b* 7.85a* 0.08b* 0.038 3.74ab* 7.74ab* 0.23a* 0.02 4.91a* 7.68b* 2.92ab' 0.017b' 2.6ab' 7.78ab' 3.66a' 0.129a' 2.42abc' 7.65b' 2.02b' 0.041b' 2.06c' 8.04a' 3.47a' 0.069ab' 2.3bc' 7.9ab' 3.28a' 0.023b' 2.86a' 7.68b' 2.29b 0.084a 11.29a 7.72b 2.46ab 0.037ab 10.25ab 7.71b 3.1a 0.006b 10.87ab 7.79a 2.5ab 0.013b 10.61ab 7.75ab 2.75ab 0.009b 10.22b 7.82a SM (%) OM (%) Salinity (mS/cm) pH

2014

D5 D4 D3 D2 D1

2013

D5 D4 D3 D2 D1

2013/14

D5 D4 D3

Soil microarthropods in general, and soil Acari in particular, were greatly affected by season, location, and the interplay between the two (Table 2). The microarthropod community recorded during the present study included 22 families of Acari: 12 prostigmatid, 5 endeostigmatid, 4 oribatid, and 1 mesostigmatid (see Supplementary Table A1), with members of Entognatha (Collembola) and Psocoptera. Acari were significantly more abundant during the winter seasons compared with the summer seasons (Fig. 1). During both winters, the highest numbers of microarthropods were found in the locations furthest from the seashore (D4 and D5), while the lowest density was found at the location closest the sea. These results were the opposite of the trend found during the first summer, where the largest populations were found at the two locations closest to the sea (D1 and D2), and they were significantly lower (p < 0.05) at the other three locations. Such a trend was not found during the second summer, and there were no significant differences between the overall microarthropod communities at the five locations. The most abundant groups within the Acari were Prostigmata and Endeostigmata (Fig. 1). Representatives of both groups were found at almost all five locations during the winter and summer seasons, and were significantly affected by seasonality, distance from sea, and the interaction between them (Table 2). Prostigmata was the most abundant mite group during the study period, and accounted for 47.5e87.5% of all mites (at each location) during the winter seasons, and 14.3e100% during the summer seasons (see

D2

3.2. Microarthropod community

D1

Soil moisture, organic matter, salinity, and pH values at the five locations during the four seasons are summarized in Table 1. Soil moisture (n ¼ 100) was found to be significantly affected by season and the interplay between season and location (Table 2). During both winters, soil moisture was higher at all locations compared with the summers, but there was no obvious trend observed at the different locations. Organic-matter levels in the soil samples were found to be relatively low during the study period, reaching 0.129% (Table 1), and were found to be significantly affected by season, location, and the interaction between the two (Table 2). Organic matter was found to be significantly higher (p < 0.05) during the second winter compared with the first at all locations except D5 e the most distant location from seashore. Soil salinity was found to be significantly higher (p < 0.05) during the first winter compared with the other seasons. However, in all the other seasons except for the first winter, the location closest to sea had the highest levels of salinity compared with the eastern locations (Table 1). In most cases, there was a decreasing trend in salinity proceeding inland, with an elevation at the most distant location from shore, except during the first winter, which showed no obvious trend. Similar to organic matter, salinity was significantly affected by season, location, and their combination (Table 2). pH was slightly alkaline during the study period, however, it was significantly affected by season, location, and the interaction between the two (Table 1).

2012/13

3.1. Soil abiotic characteristics

Summer

3. Results

41

Winter

between separate means. Differences at the p < 0.05 level were considered significant. These data were also subjected to redundancy discriminant analysis (RDA) using CANOCO for Windows 4.5, to explain the effects of environmental factors on the obtained results (ter Braak, 1995).

Table 1 Differences in the mean values of soil moisture, organic matter, salinity, and pH between soil samples (n ¼ 5) collected from five locations during winters 2012/13 and 2013/14 and summers 2013 and 2014. Values with the same letter are not significantly different (p > 0.05).

H. Wasserstrom, Y. Steinberger / Acta Oecologica 76 (2016) 39e46

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H. Wasserstrom, Y. Steinberger / Acta Oecologica 76 (2016) 39e46

Table 2 The effects of sampling season and location on abiotic and biotic soil parameters (n ¼ 100) during the study period. Season

Location

Season  Location

F-test

p-value

F-test

p-value

F-test

p-value

Soil moisture Organic matter Salinity pH

278.18 3.18 831.53 4.62

<0.0001 0.0285 <0.0001 0.005

1.55 3.99 5.21 4.16

NS 0.0053 0.0009 0.0041

3.43 2.58 2.79 3.07

0.0004 0.0061 0.0031 0.0013

Prostigmata Endeostigmata Oribatida Mesostigmata Entognatha Psocoptera Total Acari Total microarthropods Taxonomic richness H'

33.66 29.46 6.06 3.96 18.36 4.35 31.44 40.75 82.65 66.36

<0.0001 <0.0001 0.0157 0.0497 <0.0001 0.0069 <0.0001 <0.0001 <0.0001 <0.0001

15.01 5.9 4.2 2.1 8.99 0.95 11.28 14.66 11.64 6.55

<0.0001 0.0003 0.0037 0.0259 <0.0001 NS <0.0001 <0.0001 <0.0001 <0.0001

8.21 2.35 4.2 2.1 3.81 0.58 5.16 6.75 5.68 3.56

<0.0001 0.0121 0.0037 0.0259 0.0001 NS <0.0001 <0.0001 <0.0001 <0.0001

Supplementary Table A1). During the winter seasons, there was a clear trend of lower densities at the locations closest to the sea and higher densities at the locations furthest from the sea. During the first summer sampling period, the biggest prostigmatid communities were found at the sampling locations closest to the seashore. Eupodidae and Tydeidae were the most abundant Prostigmata families, and were abundant at almost all locations during both

winters. These families are diverse groups and can feed on many food sources, e.g., fungi, algae, and mesofauna (Walter and Proctor, 2013). Endeostigmatids, which feed mostly on algae and fungi (Walter, 1988), were more abundant during the wet winters compared with the dry summers, when they were hardly found, especially during the second summer. During both winters, they were most abundant at the D4 location and least abundant at the location closest to the seashore (D1). Endeostigmatid abundance did not exhibit a similar trend during the summers. Both oribatids and mesostigmatids exhibited seasonal differences and locational differences (Table 2). During the first year, i.e., winter 2012/13 and summer 2013, oribatid mites were hardly abundant, while during the second year, they were found in most of the samples (Fig. 1). Mesostigmatids were found only during the wet winters, with 267 individuals per m2 at the fourth location (D4) during winter 2012/13, and 1067 individuals per m2 at the second location (D2) and 401 individuals per m2 at the most distant location from the sea (D5) during winter 2013/14. Entognatha was the most abundant hexapoda group during both winters, and exhibited significant differences in abundance according to location and season (Table 2). Its lowest densities were found at the closest location to the sea (D1), whereas the highest densities were found in the soil samples collected at the distant locations from the seashore (D4 and D5). This microarthropod group was not present in the soil samples during the dry summer seasons. On the other hand, during the summers, the most abundant hexapoda group was Psocoptera, which was found at almost all

Fig. 1. Spatial and temporal variations in the mean abundance of the dominant microarthropod groups in soil samples (n ¼ 5) collected from five locations during winter 2012/13 (A), winter 2013/14 (B), summer 2013 (C), and summer 2014 (D). The letters represent statistically significant differences (p < 0.05) between the locations in the same season. Distances from the shore: D1 e 100 m; D2 e 200 m; D3 e 1000 m; D4 e 2500 m; and D5 e 4100 m.

H. Wasserstrom, Y. Steinberger / Acta Oecologica 76 (2016) 39e46

43

sampling locations during both summers (Fig. 1). During the first summer season, there were no differences in the psocopteran communities between the different locations, while during the second summer, they were more abundant in the locations closest to the seashore. 3.3. Taxonomic richness and diversity Taxonomic richness was greatly affected by seasonality (Table 2); it was significantly higher (p < 0.05) in the winter seasons compared with the summer seasons (Table 3). The numbers of taxa were also affected by the location across the gradient. During the winter seasons, there was an increasing trend in taxonomic richness proceeding inland, except at D3, with the lowest values found close to sea (in D1), and the highest at the eastern locations (D4 and D5). During the summer season of 2013, there was a decreasing trend in taxonomic richness related to the distance from seashore, while no obvious trend was observed in the second summer. Diversity (Shannon's index) was significantly affected by season and location (Table 2). Similar to taxonomic richness, the highest diversity values were obtained during the winters and were lowest during summers. During both winters, the lowest diversity was at the location closest to the sea, while the highest was at one of the most distant locations (D5 during winter 2012/13 and D4 during winter 2013/14). Fig. 2. Redundancy analysis (RDA) showing the relationship between the different microarthropod groups and environmental variables at the different locations during two winters. SM e soil moisture; OM e organic matter; prosti e Prostigmata, ori e Oribatida, meso e Mesostigmata, endeo e Endeostigmata, entog e Entognatha, psoco e Psocoptera, micro e total microarthropods. Distances from the shore: D1 e 100 m; D2 e 200 m; D3 e 1000 m; D4 e 2500 m; and D5 e 4100 m.

3.4. The relationship between environmental parameters and the microarthropod community During the wet winter seasons, there was a distinctive difference between the locations far away from the sea (D4 and D5) and the closer ones (D1, D2, and D3) (Fig. 2). The dominant microarthropod groups, i.e., Prostigmata, Endeostigmata, and Entognatha, were compatible with the conditions at the most distant locations from seashore (D4 and D5), and correlated with soil organic-matter content, even though these locations are not similar in their communities. Furthermore, oribatid mites were more compatible with the conditions of the location closest to seashore, while Psocoptera preferred neither, with an affinity to salinity. During the dry summers, the opposite was true, the furthest locations from the sea (D3, D4, and D5) were similar to each other, and were different from the closest ones (D1 and D2) (Fig. 3). All microarthropod groups (except for endeostigmatids) preferred the locations closer to the seashore, while the psocopterans were found to show a positive relation to soil salinity levels.

are considered to be harsh and unstable habitats (McLachlan and Brown, 2006). Coastal sand dune ecosystems are known for their unique physicochemical characteristics that are the result of the proximity to the sea. Their additional abiotic components amplify the harshness of the sandy soil environment. In order to be able to determine alterations of soil microarthropod community components in such a harsh environment, a gradient across a coastal dunefield from the shore inland, which affects the various organisms living in such an ecosystem (McLachlan and Brown, 2006; Rajaniemi and Allison, 2009), was investigated. Walker et al. (1981) and Tisdall and Oades (1982) demonstrated that erosion rates, soil moisture, organic-matter inputs, and exposure to weathering over time, influence the development of soil structure and community stabilization. We investigated whether the distance from the sea affects the soil microarthropod community during the wet winter and dry summer seasons. The results of our study showed that the sampling sites along the seashore inland affect both biotic and abiotic parameters, and are strongly related to seasonality. According to McLachlan and Brown (2006), the salinity gradient found in the present study during the dry summers was mild, mainly due to rapid leaching, which leads to a decrease in

4. Discussion Sand is an unstable foundation, with low thermal conductivity that results in considerable heating and drying of the soil surface, but the temperatures become moderate a few centimeters under the sand surface. The coarse texture of the sand allows fast infiltration and drainage of water, and therefore, movable sand dunes

Table 3 Taxonomic richness (TR) and Shannon's diversity index (H') of Acari along the transect during the two winters and summers of the study period. Values with the same letter are not significantly different (p > 0.05). TR

Winter 2012/13 Winter 2013/14 Summer 2013 Summer 2014

H'

D1

D2

D3

D4

D5

D1

D2

D3

D4

D5

3.4c 1.6C 2.0a 0.2

7.2abc 9.8AB 2.4a 1.2

5.0bc 7.0B 0.6b 0.4

9.0ab 13.2A 0.6b 0.2

9.4a 10.8AB 0.2b 0.8

0.84c 0.82B 0.59ab

1.5abc 1.92A 0.76a 0.58

1.39bc 1.7A 0b

1.94ab 2.34A 0b

2.05a 1.8A 0b 0.35

D1 e 100 m; D2 e 200 m; D3 e 1000 m; D4 e 2500 m; and D5 e 4100 m e from the shore.

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H. Wasserstrom, Y. Steinberger / Acta Oecologica 76 (2016) 39e46

Fig. 3. Redundancy analysis (RDA) showing the relationship between the different microarthropod groups and environmental variables at the different locations during two summers. SM e soil moisture; OM e organic matter; prosti e Prostigmata, ori e Oribatida, meso e Mesostigmata, endeo e Endeostigmata, entog e Entognatha, psoco e Psocoptera, micro e total microarthropods. Distances from the shore: D1 e 100 m; D2 e 200 m; D3 e 1000 m; D4 e 2500 m; and D5 e 4100 m.

sodium chloride levels in the upper layers in the sand system. Microarthropod abundance was found to be greatly affected by season, and reached higher numbers during the wet winters compared with the dry summers due to the significantly higher levels of soil moisture in the winters. This was similar to the finding of Wasserstrom et al. (2016), who studied an arid ecosystem. During the winter seasons, there was an increasing trend in microarthropod-community density, which was found to be correlated with soil organic-matter content, which is known to affect this community (Loots and Ryke, 1967; Wasserstrom et al., 2016). Furthermore, the highest number of microarthropods was found at the D4 location during the second winter, where there was also the greatest amount of soil organic matter documented during the study period. We attributed this elevation in organic-matter content to the extensive increase in algae activity beneath the surface in all samples collected only at this location (D4), at a depth of 0.5e2 cm under the surface. Another possible contributor to this increasing trend in the microarthropod community is the wind, which is known to influence the distribution of fungi and nematodes in sand dunes (de Rooij-van der Goes et al., 1997). The winds during the winters at the Israeli Mediterranean coast are intensive and significantly stronger compared with the rest of the seasons (Levin et al., 2006). These winds become weaker with distance proceeding inland. The winds move sand particles and, therefore, the sand transport gets weaker as one moves from the seashore towards land (Goldsmith et al., 1990), and the sand dune surface becomes more stable. The winds might also be the cause of the very low amounts of organic matter measured at most of the locations (except for D5 e the most distant location from seashore) during the first winter. During the days before the first winter sampling, very strong winds were recorded at the study site (Israel Meteorological Service, 2016). Since organic matter is sparse in this environment and accumulates mostly in the top layer of the sand dune, these winds could transport a significant amount of sand and organic matter

(Whitford and Sobhy, 1999) from the top layer, proceeding inland. During both dry summers, we did not find as obvious a trend of microarthropod density as during the winters. Microarthropod densities were very low, probably due to the interplay of low soil moisture and high temperatures, known to influence the abundance of this community. Both soil moisture and temperature were among the most important parameters influencing soil microarthropods (Huhta and Hanninen, 2001; Kardol et al., 2011; MacKay et al., 1986; Tsiafouli et al., 2005), especially in xeric environments, where high temperatures and low soil moisture limit their numbers and activity, and also affect their movement in the soil toward the deeper layers (Steinberger and Wallwork, 1985), since these layers are less exposed to the harsh conditions above the surface, i.e., wind and radiation. Despite the subhumid Mediterranean climate of the study site, this ecosystem has became a xeric habitat (Kutiel, 2001) due to its nature and the environmental conditions during most of the year (except for the winter rainy season). Therefore, soil moisture and temperature is of crucial important for the soil biota in general, and the soil microarthropods living in this environment in particular. The relatively high densities found at the two locations closest to the sea during the first summer might be the result of the slightly higher soil moisture at these locations, although no significant differences were found between the locations. Prostigmata was the dominant Acari group during the study period, and was more abundant than the second dominant group of mites e Endeostigmata. This can be attributed to the very low organic-matter content in these sand dunes, as shown in research studies conducted in the Negev Desert (Steinberger, 1990; Steinberger and Wallwork, 1985). Our findings are similar to the community composition found in other psammic sites by Russell and Alberti (2011), who found endeostigmatid and prostigmatid mites to be the two dominant groups in continental sand dunes in Germany. In contrast to the findings of Koehler et al. (1995) and Salmane (2000), who studied microarthropods in coastal sand dunes, we hardly found any mesostigmatid mites in the present research, due to the differences between the climates in which these studies were conducted. Their studies were conducted in colder and wetter climates, while this study was conducted in a Mediterranean ecosystem, which is hotter and dryer and, therefore, more suitable for predatory mites from the Prostigmata, known to be the dominant predator group in xeric environments (Noble et al., 1996; Steinberger, 1990). This fact also explained the low microarthropod densities found in the current study compared with other studies conducted in various sand dunes (Koehler et al., 1995; Russell and Alberti, 2011; Salmane, 2000). Moreover, Prostigmata was represented by several families known to have psammophilous species, e.g., Tydeidae, Caligonellidae, and Linotetranidae. Endeostigmatid mites, which were represented by several families, were also very abundant in these sand dunes, which is not surprising because these mites are very abundant in sandy soils and all of these families are known to have psammophilic species (Russell, 2000; Russell and Alberti, 2011). One of the more common endeostigmatid mites in these sand dunes, Nanorchestidae, is known to be dominant in warm and dry environments and sand dunes (Russell and Alberti, 2011). Nematalycidae is also known to occur in sandy soils and is distributed world-wide (Haupt and Coineau, 1999; Russell, 2000). This is possibly due to their morphological adaptations to psammophilic life (Haupt and Coineau, 1999). Oribatida were found in small numbers, probably due to the small amounts of organic matter and the arid nature of this ecosystem. Entognatha were very common during both winters due to wetter and colder conditions, which they prefer, and were absent during the dry summers. In contrast, Psocoptera were found almost exclusively during the dry summers, where the conditions

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were more suitable for them, as found by Wasserstrom et al. (2016). Taxonomic richness exhibited different trends between the seasons and was highly associated with the wetter and cooler winters, where it reached its maximum values. There was an increasing gradient in taxonomic richness during both winters, where the lowest numbers were found at the two locations closest to the seashore and the highest values were found at the two most distant locations. Similar to this trend, Acari diversity, which was expressed as Shannon's index, was also lower closer to the seashore and reached its highest values at the more inland locations. These results are similar to the gradients of increasing abundance and diversity in coastal dunes that were found for insects (Boomsma and Van Loon, 1982) and spiders (Duffey, 1968; Lowrie, 1948). However, in the current study, such gradients were found only during the wet winters and not during the dry summers. On the contrary, during the first summer, an opposite gradient in taxonomic richness was found, with the highest richness obtained at the locations in proximity to the seashore, as we saw in the case of mite abundance. The results of this study show the variations in a soil microarthropod community along a transect from the seashore inland. We shed some light on this community from the unique Caesarea sand dune ecosystem in the eastern Mediterranean Sea, which was never explored before, and, until now, there has been little knowledge about sand dune microarthropod communities in a Mediterranean climate. Although there was no clear pattern of change in the composition of this community along the transect, there was a change in abundance, i.e., an increasing trend proceeding inland. This trend was clear during the wet winter, while during the dry summer, this community was hardly found in the upper soil layer as a result of the arid nature of this sand dune ecosystem. The lack of a clear changing pattern in the mite community composition is probably due to the fact that the samples were taken from bare areas that had low soil organic-matter content. Moreover, there were no significant changes in the geochemical components of the sand dunes along the transect (Ravikovitch, 1981) and the dunes were not fully stabilized. Salinity had little effect on the community's components, probably due to the fact that many of them have adapted to arid sandy conditions that allow them to tolerate higher salinity conditions. Despite the above, differences in abundance were still found. This shows that distance from the sea and the different abiotic components in a coastal sand dune ecosystem affect the soil microarthropod community, and these differences cannot be attributed to the effect of the different plant species along the transect, creating different microhabitats. This effect is mostly noticeable during the wet winter seasons, when conditions allow the soil microarthropod community to prosper and reach its highest densities in this unique ecosystem. As all samples were taken from less successionally developed locations, we found many families with psammophilous species along the whole transect.

5. Conclusions We showed that there is a limited influence of distance from the sea on the microarthropod community, and other environmental parameters, such as soil moisture and temperature, also play a role in determining the extent of this influence. Our findings regarding the microarthropod community in such a unique ecosystem in the Mediterranean area, emphasize the significance of sand-dune ecosystems and their soil biota, which contributes to their stabilization and resilience and, therefore, these fragile ecosystems should be preserved and protected from anthropogenic threats to eradicate them.

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Acknowledgments We would like to thank Dr. Stanislav Pen-Mouratov and Ms. Rachel Wasserstrom for their assistance during the study period. We also thank Ms. Sharon Victor for her comments and for preparing the manuscript for publication. This research was partly supported by the Israel Taxonomy Initiative (ITI), which was not involved in the research, preparation of the article, or the decision to submit the article for publication. This research is part of the PhD thesis of Haggai Wasserstrom. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.actao.2016.08.005. References Almquist, S., 1969. Seasonal growth of some dune-living spiders. Oikos 20, 392e408. Armonies, W., Reise, K., 2000. Faunal diversity across a sandy shore. Mar. Ecol. Prog. Ser. 196, 49e57. Balogh, J., 1970. Biogeographical aaspects of soil ecology. In: Phillipson, J. (Ed.), Methods of Study in Soil Ecology. UNESCO Publications, Paris, pp. 33e38. Barnes, R.D., 1953. The ecological distribution of spiders in non-forest maritime communities at Beaufort, North Carolina. Ecol. Monogr. 23, 315e337. Boomsma, J.J., Van Loon, A.J., 1982. Structure and diversity of ant communities in successive coastal dune valleys. J. Animal Ecol. 51, 957e974. Callan, E.M., 1964. Ecology of sand dunes with special reference to the insect communities. In: Davis, J.H. (Ed.), Ecological Studies in Southern Africa. W. Junk, The Hague. Colombini, I., Bouslama, M.F., El Gtari, M., Fallaci, M., Scapini, F., Chelazzi, L., 2005. Study of the community structure of terrestrial arthropods of a Mediterranean sandy beach ecosystem of Morocco. Ecosystemes cotiers sensibles de la Mediterrane: cas dulittoral de Ecosystemes cotiers sensibles de la Mediterrane: cas du littoral de Smir. Trav. Inst. Sci. Ser. Gen. 4, 43e54. Cooke, J.A.L., Cotton, M.J., 1961. Some observations on the ecology of spiders occurring on sand dunes at Whiteford Burrows, Gower Peninsula, Glamorgan. Entomologist's Mon. Mag. 97, 183e187. Danin, A., 2005. The sandy areas of Caesarea, a rare situation of alpha and beta diversity linked by plant succession. Israel J. Plant Sci. 53, 247e252. de Rooij-van der Goes, P.C.E.M., Van Dijk, C., Van der Putten, W.H., Jungerius, P.D., 1997. Effects of sand movement by wind on nematodes and soil-borne fungi in coastal foredunes. J. Coast. Conservation 3, 133e142. Duffey, E., 1968. An ecological analysis of spider fauna of sand dunes. J. Animal Ecol. 37, 641e674. Foster, B.L., Tilman, D., 2000. Dynamic and static views of succession: testing the descriptive power of the chronosequence approach. Plant Ecol. 146, 1e10. Goldsmith, V., Rosen, P., Gertner, Y., 1990. Eolian transport measurements, winds, and comparison with theoretical transport in Israeli coastal dunes. In: Nordstrom, K.F., Psuty, N.P., Carter, R.W.G. (Eds.), Coastal Dunes: Form and Process. John Wiley & Sons, Brisbane, pp. 79e101. Haupt, J., Coineau, Y., 1999. Ultrastructure and functional morphology of a nematalycid mite (Acari : actinotrichida : Endostigmata : Nematalycidae): adaptations to mesopsammal life. Acta Zool-Stockholm 80, 97e111. Hesp, P., 1988. Surfzone, beach, and foredune interactions on the Australian south east coast. J. Coast. Res. Special Issue 3, 15e25. Hesp, P.A., 1991. Ecological processes and plant adaptations on coastal dunes. J. Arid Environ. 21, 165e191. Heykena, A., 1965. Vegetationstypen der Kustendunen an der ostlichen und sudlichen Nordsee. In: Raabe, E.W. (Ed.), Mitt. d. AG F. Floristik in Schl-Holst. und Hamburg. Kiel Arbeitsgemeinschaft f. Floristik in Schleswig-Holstein u, Hamburg, p. 13. Huhta, V., Hanninen, S.M., 2001. Effects of temperature and moisture fluctuations on an experimental soil microarthropod community. Pedobiologia 45, 279e286. Irmler, U., 1982. Litterfall and nitrogen turnover in an Amazonian blackwater inundation forest. Plant Soil 67, 355e358. Isermann, M., Cordes, H., 1992. Changes in dune vegetation on spiekeroog (east Friesian Islands) over a 30 year period. In: Carter, R.W.G., Curtis, T.G.F., SheehySkeffington, M.J. (Eds.), Coastal Dunes. Balkema, Rotterdam, Brookfield, pp. 201e209. Israel Meteorological Service, 2016. The Meteorological Service Data Base [accessed 6/7/2016]. Hebrew. Available from: https://ims.data.gov.il/ims/1. Jones, M.L.M., Sowerby, A., Williams, D.L., Jones, R.E., 2008. Factors controlling soil development in sand dunes: evidence from a coastal dune soil chronosequence. Plant Soil 307, 219e234. Jungerius, P.D., 1990. The characteristics of dune soils. In: Bakker, T.W., Jungerius, P.D., Klijn, J.A. (Eds.), Catena Suppl. 18. Catena Verlag, Cremlingen,

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