Intraspecific phenotypic variation in functional traits of a generalist predator in an agricultural landscape

Agriculture, Ecosystems and Environment 278 (2019) 35–42

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Intraspecific phenotypic variation in functional traits of a generalist predator in an agricultural landscape

T

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Radek Michalko , Viktoriya Dvoryankina Department of Forest Ecology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemědělská 3, Brno 613 00, Czech Republic

A R T I C LE I N FO

A B S T R A C T

Keywords: Biocontrol Edge-effect Individual specialization Seminatural habitat Trophic niche Spider

Seminatural habitats adjacent to crops often increase density and diversity of pests’ natural enemies in crops. However, there is no research investigating the effect of seminatural habitats on the intraspecific variation in functional traits of the pests’ natural enemies in agricultural landscapes, despite its significant impact on pest control. Here, we investigated whether there is intraspecific variation in functional traits of a potential biocontrol agent, the generalist spider Philodromus cespitum, depending on the location in an agricultural landscape. We compared size, capture rate, and fundamental trophic niche of P. cespitum along five transects (60 m) each consisting of three plots: hedgerow adjacent to an apple orchard, orchard edge, and orchard centre. The individuals from the orchard centers were larger than the individuals from orchard edges and hedgerows. Large individuals from the orchard centers had higher capture rate than large individuals from hedgerows but in small individuals it was the opposite. The adult females from the centers had a wider trophic niche than those from hedgerows, indicating higher foraging opportunism. The individuals from orchard edges had moderate phenotype in both trophic traits. The individuals from the orchard edges were also the most heterogeneous in body size and capture rate. The results show a clear edge effect which means that the hedgerows influenced the intraspecific functional composition in the orchard. As the intraspecific variation can interact with the species’ densities in influencing pest control, ignoring the intraspecific variation in the agricultural landscape and crops may lead to an inaccurate inference about the biocontrol services provided by spiders.

1. Introduction Seminatural habitats adjacent to crops increase density and diversity of pests’ natural enemies in crops (Rusch et al., 2010). So far, research focused only on the effects of seminatural habitats on density and interspecific diversity of natural enemies in crops (Landis et al., 2000; Rusch et al., 2010; Blitzer et al., 2012; Murphy et al., 2016; Tscharntke et al., 2016). To our knowledge, there is no research investigating the effect of seminatural habitats on the intraspecific variation in functional traits (i.e., traits affecting ecosystem functioning, such as capture rate and prey preferences of a predator [Fountain-Jones et al., 2015]) of pests’ natural enemies in agricultural landscape despite its significant impact on ecological dynamics (Okuyama, 2008; Bolnick et al., 2011; Sih et al., 2012). Such research may help explain why seminatural habitats sometimes fail to improve natural pest control (Tscharntke et al., 2016; Birkhofer et al., 2018). Intraspecific variation in functional traits (e.g.; in body size, foraging behaviour) in a population of a natural enemy can alter the intensity of interspecific interactions as larger or more aggressive

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individuals have higher capture rates (Maupin and Riechert, 2001; Pekár et al., 2015). Further, the intraspecific variation can completely restructure the food-web architecture. Individuals can prefer different prey and so alter the connections in the food-web networks (Araújo and Gonzaga, 2007; Cucherousset et al., 2011; Rhoades et al., 2018). Individuals can also differ in their position in the food web as they can consume prey from different trophic levels due to differences in size as well as behaviour (Wise, 2006; Michalko and Pekár, 2017; Michalko and Řežucha, 2018). Consequently, the intraspecific variation in functional traits of natural enemies can cascade throughout the whole community and can alter the pest suppression in a context-dependent manner (Royauté and Pruitt, 2015; Michalko and Pekár, 2017; Start and Gilbert, 2017). For example, individuals of a large top predator spider differed in prey preferences between a psyllid pest and a smaller spider (i.e. spider at lower trophic level, mesopredator). Some individuals preferred psylla over mesopredator spiders while others did not have any preferences. The distinct prey preferences of the individuals were associated with their foraging aggressiveness (i.e. no. of killed prey / time). Aggressive individuals (individuals with consistently high killing

Corresponding author. E-mail address: [email protected] (R. Michalko).

https://doi.org/10.1016/j.agee.2019.03.018 Received 30 September 2018; Received in revised form 15 March 2019; Accepted 17 March 2019 0167-8809/ © 2019 Elsevier B.V. All rights reserved.

Agriculture, Ecosystems and Environment 278 (2019) 35–42

R. Michalko and V. Dvoryankina

and Sisk, 2004; Birkhofer et al., 2018) may cause to intraspecific functional composition to gradually change from edge to the centre (Fig. 1A). The edges can also generate interactions that are not present in the semi-natural habitats or crop centres (Wimp et al., 2011). This can form other types of selection pressure, which can further modify the intraspecific functional composition (Riechert and Hedrick, 1993; Michalko and Řežucha, 2018; Lapiedra et al., 2018). Consequently, intraspecific functional composition may not change gradually in one direction but may shift abruptly from patch to patch (Fig. 1B). By contrast, strong spillover from the adjacent seminatural habitats and from the surrounding landscape may homogenize the population across seminatural habitats and crops (Holt et al., 2005). Some generalist predators freely move from seminatural habitats to deep inside the crops and back (Bommarco and Fagan, 2002; Birkhofer et al., 2018). Moreover, local populations can be affected by the processes operating at a spatial scale of the surrounding landscape rather than by local processes (Lemessa et al., 2015; Lefebvre et al., 2016). Therefore, there may be no intraspecific variation among patches at such small spatial scale (Fig. 1C). Here we investigated the presence of intraspecific phenotypic variation in functional traits in the cursorial spider Philodromus cespitum (Walckenaer, 1802) (Araneae, Philodromidae). P. cespitum is a dominant spider species in fruit orchards of Central Europe (Bogya et al., 1999; Korenko and Pekár, 2010) and is abundant also in the surrounding hedgerows (Michalko and Pekár, 2015a). Philodromids have been shown to supress psyllid pests in pear orchards (Michalko et al., 2017), aphids in apple orchards (Lefebvre et al., 2017), and dipteran pests in olive orchards (Picchi et al., 2016). We investigated the difference in body size, functional response, and fundamental trophic niche as these functional traits are among the key characteristics determining the predator-prey interactions. Body size can, among others, determine the vulnerability to other natural enemies (Rypstra and Samu, 2005), capture rate (Pekár et al., 2015), trophic niche (Sanders et al., 2015), and also the degree of trait-mediated effect (Persons and Rypstra, 2001). The capture rate and prey preference both affect the per capita predation pressure of a generalist predator on pests (Morozov

rates due to overkilling) did not have any preferences between the pest or mesopredator and were non-selective. In contrast, the timid individuals (individuals with consistently low killing rates) preferred the pest over mesopredator and were selective. The predator community with an aggressive non-selective top predator suppressed the pest more when the top predator to mesopredator abundance ratio was high. In contrast, the predator community with a timid selective top predator was more effective when the ratio was low (Michalko and Pekár, 2017). Therefore, we need to investigate how seminatural habitats affect intraspecific functional composition in order to improve our ability to predict their effect on pest suppression. The different conditions occurring in the crops and the adjacent seminatural habitats (e.g., resource availability, predation pressure, pesticides) can produce distinct selection pressures selecting for certain phenotypes (Wolf and Weissing, 2010; Montiglio and Royauté, 2014). For example, the seminatural habitats can host higher prey density and diversity than the crops (Rusch et al., 2010). The prey rich environment of seminatural habitats can select for a phenotype that effectively reduces foraging costs, i.e. a timid and selective phenotype that reduces predation risk and forages optimally by avoiding non-profitable prey (Riechert, 1991; Riechert and Hedrick, 1993). In contrast, the prey poor environment in crops can select for an aggressive and non-selective phenotype that forages opportunistically on everything that they can overcome (Riechert, 1991; Riechert and Hedrick, 1993). Moreover, the seminatural habitats that offer a high amount and diversity of prey could enable generalist predators to select such a diet that improves their fitness and increases their size (Toft, 2013). Therefore, the seminatural habitats may host, on average, timid / selective / large individuals in comparison to aggressive / non-selective / small individuals in the crops. Edge effects generally occur at the interface between seminatural habitats and crops (Ries and Sisk, 2004; Rand et al., 2006). The edge effect may result in different intraspecific functional composition (i.e. distribution of functional trait values) not only between crops and seminatural habitats but also between crop patches located in the central areas and at the edges. The gradually decreasing prey availability and the spillover of generalist predators across the edge (Ries

Fig. 1. Three theoretical scenarios (A–C) of how prey availability (orange triangle), movement intensity (width of arrows), and a unique biotic interaction (grey background) may influence intraspecific phenotypic variation in body size (size of points) and foraging aggressiveness (colour of points) of spiders in the patches (the black ovals) in an agricultural landscape. In the panel (A) the main selection pressure driving the phenotypic variation is prey availability that declines from hedgerows towards orchard centre. As low prey availability reduces body size (Toft, 2013) and selects for higher foraging aggressiveness (Riechert and Hedrick, 1993) the mean body size may gradually decline and mean foraging aggressiveness may gradually increase from hedgerows towards centre. In the panel (B) the edge between hedgerows and orchard can generate unique interactions such as predation on spiders by birds (depicted by grey background; Wimp et al., 2011). The predation pressure by birds might overcome the selection pressure of prey availability. The predation by birds selects for smaller body size and lower foraging aggressiveness (Riechert and Hedrick, 1993; Gunnarsson, 1990). Consequently, the distribution of body size and foraging aggressiveness change abruptly from hedges towards orchard centres. Generally, the movement of spiders in an agricultural landscape is stronger from the hedges towards the crop centres than oppositely (depicted as arrows of different width Birkhofer et al., 2018). In the panels (A,B) the movement among patches is relatively weak so the selection pressures are the dominating force in structuring the phenotypic composition in the patches. But in the panel (C) the movement is so high that it overrides the selection pressures. Consequently, the movement homogenizes the distribution of phenotypes among patches (Holt et al., 2005). 36

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the experiments in plastic jars of surface area 96 cm2 (height: 3.5 cm, d =7 cm). The experiments were conducted under room temperature (23 ± 1 °C) and under natural photoperiod. The individuals within each plot were assigned to prey density randomly without replacement. We recorded the number of flies killed every 8 h during the following 24 h. During each check we replaced the killed flies by live ones to ensure constant prey densities.

and Petrovskii, 2013). We expected that (i) there would be significant intraspecific variation in the studied functional traits among patches located in the hedgerows, at the orchard edges, and in the orchard centres. We also expected that (ii) the patches in seminatural habitats would host larger individuals, but with a lower capture rate and a narrower fundamental trophic niche when controlled for size. This is because hedgerows host more prey for philodromids than the orchard (Korenko and Pekár, 2010; Michalko and Pekár, 2015a,2015b). The prey-poor environment selects for opportunistic and aggressive behaviour while the resource rich environment selects for the opposite (Riechert, 1991; Riechert and Hedrick, 1993; Maupin and Riechert, 2001). Further, we expected that (iii) functional composition will gradually change along transects due to dispersal and gradual changes in prey availability (Ries and Sisk, 2004; Fig. 1A).

2.3. Prey acceptance To investigate whether the philodromids from different locations differ in their fundamental trophic niches (here used as a description of prey accepted in the laboratory) we conducted experiments on prey acceptance. We used only adult females from the experiments on functional response (N = 58) but not all of them. To minimize spatial autocorrelation, we pooled the females within each location and selected them randomly. We aimed to investigate whether there are differences in the trophic niches among the individuals from the three locations rather than their overall trophic niches. Therefore, we offered three prey types to the females that represent a gradient in prey-ranks (highly, moderately, and least preferred) by philodromids at the population-level (Michalko and Pekár, 2015b). But the individuals can rank these prey types differently (Michalko and Pekár, 2017). Therefore, we expected that the potential differences would show up by differential preying on less preferred prey types. The prey types were: Diptera (D. hydei; preferred, mean body length =1.9 mm ± SD = 0.18), Heteroptera (larva of Lygus sp.; less preferred, mean body length =1.9 mm ± SD = 0.18), and Araneae (Xysticus sp.; least preferred, mean body length =1.9 mm ± SD = 0.17) (Michalko and Pekár, 2015b). These prey types are part of the natural diet of P. cespitum in the studied area (Michalko and Pekár, 2015b). Each female was offered from one to all three prey types. We offered the prey types to the females in random order without replacement. Therefore, the design was a type of incomplete blocks design. There were 12–21 replicates per prey type / location. Prey item was classified as accepted if a female began to consume it within 15 min after the first contact, otherwise it was classified as refused. If the prey item was refused, it was replaced by another prey type immediately. If the prey was accepted, a female was left to consume it and another prey item of different type was offered after 3 days. The body size (from head to the end of abdomen without appendages) of accepted as well as refused prey was measured to an accuracy of 0.1 mm.

2. Methods 2.1. Study site and sampling We collected P. cespitum in a commercial apple orchard (79 ha) in Brno, Czech Republic (49°09’38’’N, 16°33’38’’E) and the semi-natural habitats that were directly adjacent to, or contained within, the orchard (Fig. S1) from 1st June – 15th June 2018. We specifically aimed to investigate whether intraspecific variation can occur over such a short distance, i.e. patch scale within an orchard. Therefore, we collected the philodromids on five transects in one large orchard rather than on several orchards to eliminate other potential sources of variability such as management, type of surrounding seminatural habitats, and other landscape characteristics. The apple orchard was under integrated pest management with application of pesticides. The seminatural habitats were 2–5 m wide strips of hedgerows dominated mostly by scrubs, namely Rosa sp., Crataegus sp., and Prunus spinosa L. P. cespitum is a dominant spider species in the orchard and the surrounding hedgerows. However, the hedgerows host more prey for the philodromids, and the philodromids are more abundant in the hedgerows (Korenko and Pekár, 2010; Michalko and Pekár, 2015a,b). We selected 5 transects that were randomly placed in the orchard but situated in such a way that they did not overlap (Fig. 1S). The mean distance between two neighbouring transects was 640 m (range 280–940 m). Each transect consisted of three plots: 1) hedgerow directly adjacent to the orchard, 2) orchard edge (5–10 m from the hedgerow), and 3) orchard centre (50–60 m from the hedgerow). Thus, plots within each transect were spatially closer to each other than to any other patch from a different transect. As we aimed for the individual based approach, we collected a pre-determined number of individuals. In each plot we collected 10 individuals of P. cespitum, but due to mortality the number of individuals varied between 7–10 per plot. We collected the philodromids by beating. Each individual was placed in a separate vial and transferred to the laboratory. In the laboratory, we sorted the philodromids according to their stage (adult female, adult male, and juveniles). We measured the width of the cephalothorax under a stereomicroscope with a precision of 0.1 mm. The philodromids were identified according to Bryja et al. (2005).

2.4. Statistical analyses We performed all analyses within the R environment (R Development Core Team, 2018). We compared the mean body size by use of linear mixed effect models (LME) using the R package ‘nlme’ (Pinheiro et al., 2015). The fixed effects of the initial model were location (hedgerow, orchard edge, orchard centre), stage (female, male, juvenile), and their interaction. We determined the appropriate structure of random effects by building three competing models and selected the appropriate model using AIC assuming that Δ AIC ≥ 3 signifies substantial difference (Zuur et al., 2015). The structure of random effects in the three competing models were 1) plot nested within transect, 2) plot, and 3) transect. The random effects in the final model were represented by the transect. We compared the body size variability among the locations by the Levene’s test of homogeneity of variance. We compared the distribution of life stages (i.e. adult females : adult males : juveniles) with Chi-square test. We summed all individuals within each life stage across the locations. We used generalized estimating equations (GEE) from the R package ‘geepack’ (Højsgaard et al., 2006) as an extension of GLM for autocorrelated data to compare the functional responses among the philodromids. To deal with the repeated measurements performed on an individual we computed the mean no. of captured flies per individual.

2.2. Functional response With each individual, we conducted an experiment on functional response three days after its collection. As we aimed to maintain the general state of the philodromids from the field, we purposely did not feed them during this period. We investigated the functional response of P. cespitum to laboratory reared Drosophila hydei Sturtevant, 1921 (Drosophilidae). Each spider was exposed to one of the 10 densities of flies. The densities were 1–17, starting with 1, 2, 3 individuals and then increasing by steps of 2 individuals (i.e. 5, 7, 9 individuals etc.). We conducted 11–15 replicates per prey density (N = 138). We performed 37

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significantly different from the orchard centres (Levene’s test, F1,95 = 1.0, P = 0.321, Fig. 2B). The variability in body size was also higher in the orchard centres than in the hedgerows (Levene’s test, F1,90 = 4.3, P = 0.041, Fig. 2B).

Table 1 The results of the generalized estimating equations investigating the factors that influence the functional response of Philodromus cespitum to Drosophila hydei. Significant results are in bold. Term

d.f.

X2

P-value

Location

2 1

0.2 195.1

0.905 < 0.001

1 2 1

10.6 11.1 0.9

0.001 0.004 0.343

2

0.8

0.666

2

0.9

0.653

3.2. Functional response to prey density 1 Density

Size Location : Size 1 : Density

Size

Location : Location :

1 Density 1 : Density

Size

The number of killed flies increased with their density (GEE-g, P < 0.001; Tables 1 and 2, Fig. 3). The location influenced how the capture rate increased with predator body size (GEE-g, P = 0.003; Table 1 and 2, Fig. 3). For philodromids from the orchard centers the number of killed flies increased significantly with predator body size (contrasts, P < 0.001), however for spiders from the edges and hedgerows the number of killed flies increased only marginally with size (contrasts, P = 0.053 and P = 0.054, respectively). The variability of the parameter estimate around the effect of body size was larger by an order of magnitude in the philodromids from the edges than the other two locations (Table 2). Consequently, the effect of body size differed significantly between spiders from the hedgerows and the orchard centers (contrasts, P = 0.001), while the effect of body size of philodromids from the edges did not differ significantly from either location (contrasts, P > 0.219).

Individuals (N = 2) that did not prey were not included in the analyses. The statistical cluster was then represented by a transect and we expected “exchangeable” correlation structure among individuals. There was no additional spatial autocorrelation in the residuals of the model. We modelled the functional response of philodromids to be of type II (i.e. asymptotic) using the Holling (1965) disk equation as: Ne = aNT / (1 + aNTh), where Ne, a, N, T, and Th are number of killed prey, search efficiency, prey density, total time, and handling time respectively. We expected the type II response as the philodromids have been shown to have this response to Drosophila flies in a simple environment repeatedly (e.g. Řezáč et al., 2010; Michalko and Košulič, 2016). We used its linearized form and fitted it by GEE with gamma error structure and inverse link (GEE-g) and the prey density was inversely transformed (Pekár and Brabec, 2016). As the functional response of philodromids can be influenced by their size (Michalko and Košulič, 2016), we also added the effect of body size into the initial model (Table 1). To compare functional responses of philodromids, we incorporated the effect of location into the model with all possible two-fold and three-fold interactions (Table 1). We used GEE also to compare the trophic niche of the philodromids. GEE had binomial error structure and logit link (GEE-b) as the data had Bernoulli’s distribution (Pekár and Brabec, 2018). The individual represented the statistical cluster and we expected “exchangeable” correlation structure as there were only a few (1–3) measurements per cluster (Pekár and Brabec, 2018). There was no additional spatial autocorrelation in the residuals of the model. The explanatory variables were location, prey type, prey to predator size ratio, and all their twofold and the three-fold interactions (Table 3). The terms were excluded according to the rule of marginality and their significance (Pekár and Brabec, 2016). To compare the niche width, we computed the mean 50% acceptance threshold of prey to predator size ratio across the three prey types. We computed the 50% acceptance threshold for each prey type using the following formula: −α / β, where α and β are the estimated intercept and slope, respectively, from the binomial GEE regression type of analysis (Pekár and Brabec, 2016).

3.3. Prey acceptance The probability of prey acceptance was additively influenced by the location, prey type, and size ratio (GEE-b, P < 0.030; Table 3 and 4, Fig. 4). The highest acceptance rate was observed for the philodromids from the orchard centers, but it was significantly different only from spiders from the hedgerows (P = 0.048). The acceptance probability of spiders from the orchard edges was moderate and statistically did not differ from the other two locations (contrasts, P > 0.111). The philodromids accepted mostly flies followed by heteropterans, and spiders, and the acceptance probability decreased with increasing prey to predator size ratio (Fig. 4). The mean prey to predator size ratio for 50% acceptance probability was 2.14, 2.28, and 2.8 for the individuals from the hedgerows, orchard edges, and orchard centers, respectively. 4. Discussion In this study we aimed to investigate whether the distinct conditions in the hedgerows and apple orchard can produce distinct body size, capture rate, and trophic niche in a generalist spider predator Philodromus cespitum in an agricultural landscape. The individuals from hedgerows and orchard edges were smaller than the individuals from the central areas. The capture rate showed an interesting pattern as the small individuals from hedgerows had a higher capture rate than small individuals from the orchard centers but for large individuals it was the opposite. The adult females from the hedgerows had lower prey acceptance rate than females from the orchard centers and narrower trophic niche. The individuals from orchard edges had an intermediate phenotype in the trophic functional traits but not statistically different from individuals from the other two locations. We will further discuss the potential causes and consequences of the intraspecific variation.

3. Results 3.1. Body Size and life stage

4.1. Body size The distribution of life stages did not differ among the locations (χ24 = 4.3, P = 0.372). Body size differed among the locations (LME, F2,131 = 13.0, P < 0.001, Fig. 2A). All stages were largest in the orchard centres (contrasts, P < 0.004). Although the philodromids were slightly smaller at the orchard edges than in the semi-natural habitats, it was not statistically significant (contrasts, P = 0.175). The size variation differed among the locations (Levene’s test, F2,138 = 3.2, P = 0.045, Fig. 2B). The largest variation was at the orchard edges, where the variance was significantly larger than in the hedgerows (Levene’s test, F1,89 = 6.5, P = 0.012, Fig. 2B) but not

The individuals from hedgerows and orchard edges were smaller than the individuals from the central areas of the orchard, which is in contrast with the predictions. We expected the opposite as the hedgerows are more prey rich than the orchard centers (Korenko and Pekár, 2010; Michalko and Pekár, 2015a; Michalko and Pekár, 2015b), which would enable the philodromids to grow larger (Toft, 2013). The observed pattern can be explained by several non-exclusive mechanisms. Firstly, the hedgerows may host not only more prey but also more enemies such as birds which likely prey in parts of the orchards closer 38

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Fig. 2. Mean body size comparison among individuals of the spider Philodromus cespitum at different life stages (A) and overall body size distribution (B) in three locations in an apple orchard. The points and lines in the panel (A) are the estimated means and CI95%, respectively. Table 2 Parameter estimates (SE) of the generalized estimating equations with Gamma error structure and inverse link investigating the factors that influence the functional response of Philodromus cespitum to Drosophila hydei. The equation for parameter substitution is displayed to get the model fit in Fig. 4. m.s = marginally significant (P = 0.054). Different superscript is used for statistical significance (P < 0.05). Location Hedgerow Orchard edge Orchard center

α 0.20 (0.061) 0.41 (0.191) 0.45 (0.104)

β

γ

0.97 (0.039) 0.97 (0.039) 0.97 (0.039)

−0.06 (0.030) −0.18 (0.100) m.s.; −0.20 (0.052)b

Table 3 The results of binomial generalized estimating equations investigating the factors that influence the acceptance probability of three prey types by the spider Philodromus cespitum. Significant results are in bold. Term

d.f.

X2

P-value

Location Prey Size.Ratio Location : Prey Location : Size.ratio Prey : Size.Ratio Location : Prey : Size.Ratio

2 2 1 4 2 2 4

7.1 12.9 15.6 3.1 4.6 1.4 8.7

0.029 0.002 < 0.001 0.545 0.099 0.491 0.07

Equation m.s.,a

y=

a,b

Prey density αPrey density + β + γPreydensity * size

Table 4 Parameter estimation (SE) from the binomial generalized estimating equations investigating the factors that influence the acceptance probability of three prey types by the spider Philodromus cespitum. The parameters are shown in the treatment parametrization where Diptera act as the intercept. Location

Diptera

Heteroptera

Araneae

Size ratio

Hedgerow Orchard edge Orchard center

5.19 (1.130) 5.46 (0.954) 6.47 (1.136)

−0.10 (0.720)

−2.68 (0.639)

−1.99 (0.504)

intensifies intraguild predation in spiders (Finke and Denno, 2006; Rickers et al., 2006; Korenko and Pekár, 2010). The susceptibility to intraguild predation including cannibalism decreases with increasing size (Rypstra and Samu, 2005; Michalko and Pekár, 2015b) and the intense intraguild predation might therefore select for larger body size. Thus, intraguild predation might dominate in the orchard centers, while bird predation might dominate in the hedgerows and orchard edges. Moreover, the resource poor environment of the central areas might select for larger body size because larger individuals are more resistant to starvation (Gunnarsson, 1987). The larger size might be explained also by dispersal as larger individuals can be more mobile at the field-

to hedgerows (Heikkinen et al., 2004). Bird predation affects larger spiders more than smaller ones (Askenmo et al., 1977; Gunnarsson, 1990). The larger size in central areas might be explained by intraguild predation among spiders. Spiders are the most abundant invertebrate generalist predators in the trees of the studied orchard (Korenko and Pekár, 2010). The central areas of orchard are prey poor and the vegetation structure is relatively simple in comparison to the hedgerows. The resource poor and structurally simple environment strongly

Fig. 3. The comparison of functional responses of individuals of Philodromus cespitum, collected at three locations of an apple orchard, to flies Drosophila hydei (A). (B) The relationship between body size and capture rate at two different prey densities of individuals of P. cespitum collected in three locations of an apple orchard. The parameter estimate is shown in Table 4.

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Fig. 4. Prey acceptance probability of three prey types by the spider Philodromus cespitum from three locations in the apple orchard depending on the prey to predator size ratio (body length : carapace width). The three prey types were Diptera (A), Heteroptera (B), and Araneae (C).

The results have important implications because they show that the seminatural habitats and crops can host not only different species composition but also can differ in intraspecific functional composition. Moreover, the presence of seminatural habitats can influence the intraspecific functional composition directly in the crops. To our knowledge, this has not been shown so far. A few previous studies have, indeed, demonstrated that the presence of seminatural habitats in the agricultural landscape and/or adjacent to the crops can alter the functional role of generalist predators by means of diet composition (Diehl et al., 2013; Birkhofer et al., 2016; Mader et al., 2016). However, they focus on a predator-community’s wide response, at whole-field spatial scales. The functional differences might be then explained by various factors affecting the predator-prey interactions. Our results complement these studies and show that the altered function can be caused by changes in behaviour of the generalist predators. Moreover, the intraspecific variation occurred at a relatively small spatial scale (< 60 m) and was not eliminated by dispersal. The intraspecific functional composition can further interact with the density of other community members and also alter their functional traits (Bolnick et al., 2011; DiRienzo et al., 2013; Royauté and Pruitt, 2015; Michalko and Pekár, 2017). This may affect the pest suppression differently than predicted by models based only on densities and species’ mean traits across patches (Chatterjee et al., 2009; Bolnick et al., 2011). The impact of the adjacent seminatural habitats on intraspecific functional variation in crops likely interacts with similar factors as in the case with the community composition and species’ densities. Further studies should therefore investigate how this may be influenced by the dispersal ability of a species (e.g., Wu et al., 2017), the size of the seminatural habitats (e.g., Diehl et al., 2013), and the type of crop management applied (e.g. Birkhofer et al., 2016).

scale and therefore reach parts farther away from the source area (Ness et al., 2004). 4.2. Capture rate and trophic niche We expected that the relatively prey-poor environment of the orchard centers will select for higher capture rate and wider trophic niche of P. cespitum in comparison to the prey-rich hedgerows. This hypothesis was supported only partially as only the large individuals behaved according to the expectations. The higher capture rate in large individuals corresponds with other studies that show that spider populations from areas with more intense agricultural management have higher capture rate (Royauté et al., 2014; Petcharad et al., 2018). In contrast to the expectation, the small individuals from the orchard centers had lower capture rate than the small individuals from the hedgerows. This pattern may be explained again by more intense intraguild predation in orchard centers than hedgerows. The small individuals that are prone to the intraguild predation may trade-off foraging for safety (Stephens et al., 2007). The strong intraguild predation could be evinced by the larger philodromids and / or Anyphaena accentuata (Walckenaer, 1802) (Anypahenidae) which are the dominant top predators in the trees of the studied orchard and have been found to prey on each other (Korenko and Pekár, 2010; Michalko and Pekár, 2015b; Petráková et al., 2016). Indeed, the adult philodromid females from orchard centres had higher capture rates and also preyed upon a larger range of spider body size than the females from hedgerows and were therefore more dangerous for smaller spiders. 4.3. Edge-effect in intraspecific variation We expected that there would be a continuous change in the studied functional traits. This hypothesis was supported as the individuals from the orchard edges had a moderate phenotype that was not statistically different from the other two locations which did differ significantly from one another. However, the body size and the parameter estimates for capture rate had the highest variability at the orchard edges, which indicates that the individuals were also the most heterogeneous. There are at least two possible explanations for the observed pattern. First, there might be a gradual change in conditions, and the counteracting selection pressures (e.g., prey shortage vs. predation) might become more balanced towards the orchard edges (Wolf et al., 2007). Second, the conditions at the edges might not differ from the hedgerows nor from the orchard central areas, but, the movement of philodromids from the hedgerows to the orchard and from the orchard to the hedgerows (e.g., Birkhofer et al., 2018) might create a more heterogeneous sub-population at the orchard edges (Wolf and Weissing, 2010).

5. Conclusions In conclusion, the results show that the intraspecific functional composition of population of the spider Philodromus cespitum differed between the apple orchard and the adjacent hedgerows. The intraspecific variation can therefore arise at relatively small spatial scales (60 m) without being erased by dispersal. Moreover, the interface between seminatural habitats and crops formed an edge effect, which means that the hedgerows affected the intraspecific behavioural and morphological composition of philodromids in the orchard. The seminatural habitats can therefore affect not only the densities of natural enemies in crops but also their functional traits. As the intraspecific variation interacts with the species’ densities in determining natural pest control (Michalko and Pekár, 2017; Start and Gilbert, 2017), ignoring the impact of seminatural habitats on the intraspecific variation 40

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may lead to an inaccurate inference about the biocontrol services provided by spiders.

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