Behavioral Ecology and Sociobiology

, Volume 66, Issue 12, pp 1569–1576

Functional values of stabilimenta in a wasp spider, Argiope bruennichi: support for the prey-attraction hypothesis

Authors

    • Division of Life SciencesUniversity of Incheon
  • Kyeonghye Kim
    • Kim and Chang Intellectual Property Law Firm
  • Jae C. Choe
    • Division of EcoScienceEwha Womans University
Original Paper

DOI: 10.1007/s00265-012-1410-8

Cite this article as:
Kim, K.W., Kim, K. & Choe, J.C. Behav Ecol Sociobiol (2012) 66: 1569. doi:10.1007/s00265-012-1410-8

Abstract

Many orb-weaving spiders decorate their webs with conspicuous ultraviolet (UV)-reflective stabilimenta. The prey-attraction hypothesis suggests that stabilimenta are visually attractive to prey and thus may increase the spiders’ foraging success. However, previous studies on the function of stabilimenta have produced conflicting results in Argiope species. Using a combination of field and laboratory studies, we examined whether the linear stabilimentum of Argiope bruennichi contributes to prey interception. We recorded prey interceptions in 53 webs with stabilimenta and 37 equally-sized webs without stabilimenta, classifying captured prey according to their taxonomical group and size. On average, 6.2 ± 4.7 prey items were intercepted in webs with stabilimenta, while 3.2 ± 2.9 items were intercepted in webs without stabilimenta. The effects of stabilimenta on foraging success appear to be due to increased interception of UV-sensitive insect pollinators, including 20 families of Diptera, Hymenoptera, Coleoptera, and Lepidoptera. The mean number of UV-sensitive prey was 4.4 ± 3.6 in webs with stabilimenta compared with 1.8 ± 2.1 in webs without stabilimenta. Webs with and without stabilimenta did not differ in the mean number of UV-nonsensitive prey captured. The linear stabilimentum showed strong positive effects on the interception of large prey: webs with stabilimenta captured more than twice as many large prey (≥5 mm) than webs without stabilimenta, whereas there was only a slight difference in the interception rates for small prey (<5 mm). Comparisons among different Argiope species suggest that the stabilimentum may have different adaptive functions in different species or ecological contexts.

Keywords

StabilimentumPrey-attraction hypothesisArgiope bruennichi

Introduction

Many orb web-weaving spiders (Araneae: Araneidae, Tetragnathidae, Uloboridae) decorate their webs with species-typical structures called stabilimenta (Simon 1895; Herberstein et al. 2000; Bruce 2006). A stabilimentum is a conspicuous white silk structure that reflects much more ultraviolet (UV) light than other spider silks in the web (Craig and Bernard 1990). This is surprising, given that web-building spiders’ silk generally has low UV-reflectance, presumably to reduce the visibility of webs to insect prey (Blackledge and Wenzel 2000).

Researchers have proposed many hypotheses concerning the function of the stabilimentum. The stabilimentum has been proposed to mechanically stabilize and strengthen the orb web (Robinson and Robinson 1970), camouflage the spider by obscuring its outline (Schoener and Spiller 1992; Eberhard 2003), prevent web damage by larger animals (Eisner and Nowicki 1983), increase foraging success by attracting more prey to the web (Craig and Bernard 1990; Tso 1998), help with thermoregulation by providing a sunshade for spiders foraging in high-temperature sites (Humphreys 1992), protect the spider from predatory attacks via concealment or by increasing the apparent size of the spider (Eberhard 1973; Lubin 1975), serve as a platform for molting (Simon 1895; Robinson and Robinson 1978; Nentwig and Heimer 1987), function as guides to lead males to females for mating (Crome and Crome 1961), or imitate gaps in vegetation produced by the sun and sky, natural sources of UV light (Craig and Bernard 1990).

A few hypotheses concerning the functional values of the stabilimentum have been tested directly by experimental manipulations, but the results have been contradictory or unclear and differ depending on the spider species examined (Herberstein et al. 2000; Bruce 2006; Walter and Elgar 2012). A recent and well-received hypothesis, the “prey-attraction hypothesis,” suggests that the stabilimentum may function to increase foraging success by attracting more prey to webs (Craig and Bernard 1990; Tso 1998; Watanabe 1999). Stabilimenta might increase the foraging success of web-building spiders, because web decorations may attract insect pollinators seeking flower nectar by reflecting UV light similar to UV-reflecting flowers.

A possible evolutionary mechanism by which such functions could evolve is offered by the sensory exploitation hypothesis, which was initially proposed to explain how sexual selection by female choice operates (Ryan 1998). This hypothesis predicts that preexisting biases in the receiver’s sensory system (for example, attraction to specific colors of food, specific sounds, etc.) may incidentally affect decisions that an animal makes when dealing with other behavioral challenges. Decorating the web with a stabilimentum, accordingly, might be an example of the exploitation of a preexisting sensory bias in a prey animal toward UV-reflective surfaces that allows orb-weaving spiders to profit via increased foraging success (Bruce et al. 2001).

The results of several studies of spiders in the Araneid genus Argiope have offered support for the prey-attraction hypothesis (e.g., Argiope trifasciata, Tso 1996; Argiope aetherea, Elgar et al. 1996; Argiope appensa, Hauber 1998; Argiope aurantia, Tso 1998; Argiope keyserlingi, Herberstein 2000, Bruce et al. 2001; Argiope versicolor, Li 2005; Argiope savignyi, Gálvez 2009), while other studies involving spiders in the same genus, and in some case the same species, have yielded results that do not support the prey-attraction hypothesis (e.g., A. trifasciata, Blackledge 1998; A. aurantia, Blackledge 1998, Blackledge and Wenzel 2000; A. bruennichi, Prokop and Grygláková 2005; A. appensa, Adamat et al. 2011).

Most researchers testing the prey-attraction function of stabilimenta have measured the average number of flying insects intercepted in webs with and without stabilimenta in the laboratory or in the field. However, a number of methodological problems with these studies have been noted (Bruce 2006). Webs with stabilimenta are often smaller than webs without stabilimenta (Hauber 1998; Bruce et al. 2004; but see Prokop and Grygláková 2005), and some researchers did not control for the effects of web size when assessing the effects of stabilimenta on prey capture rates (Bruce 2006). Previous studies have also failed to differentiate between prey species sensitive to UV light (hereafter referred to as UV-sensitive prey) and UV-nonsensitive species when counting the number of prey items intercepted in the webs. Previous studies have also generally not considered the energy content of prey captured in different types of webs (one large prey item captured in one type of web could contain more nutrients than several small prey items captured in a web of a different type) or the effects of the sites on which webs were built (webs with stabilimenta may occur in sites with a different prey density or the spider may consider the natural background when designing its web; Bruce 2006). Past experience in prey capture could also influence web design (Herberstein et al. 2000; Venner et al. 2000; Adamat et al. 2011).

In this study, we examine the prey-attraction function of stabilimenta in Argiope bruennichi which is abundant in paddy fields, wetlands, and shrub areas in South Korea. We hypothesized that webs with stabilimentum would capture more UV-sensitive prey that webs without stabilimentum. Using a combination of field and laboratory studies, we compared prey interception rates between webs with stabilimenta and webs without stabilimenta while carefully controlling for the effects of potentially confounding variables. We measured the web structure and classified prey intercepted in the webs by taxonomy and size.

Materials and method

Study species

A. bruennichi (Scopoli 1772) (Araneidae), also known as the wasp spider, is a panpalearctic orb web-building spider. Individuals reach maturity and reproduce in August and September. Females (2.0–2.5 cm) are much larger than males (0.8–1.2 cm), and show clear yellow and black bands on their abdomen like many other members of the genus Argiope.

The female spider builds a spiral orb web at dawn or dusk, usually in long grass with small shrubs a little above ground level. After they finish building the orb spirals, A. bruennichi individuals decorate their webs with stabilimenta placed in a vertical linear pattern through the center of the web (Fig. 1). A stabilimentum is made using a densely woven zigzag stitch and consists of two parts: an upper stabilimentum and a lower stabilimentum. A. bruennichi do not always decorate their webs, and the number and size of silk bands placed on their webs vary on a daily basis. Therefore, spiders can be found on webs without stabilimenta, on webs with one-armed stabilimenta consisting of a lower part or an upper part only, or on webs with both the upper and lower parts of the stabilimentum. Stabilimenta are constructed from the same silk used by orb-web spiders to wrap prey, which originates from the aciniform and piriform glands (Walter et al. 2008).
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Fig. 1

Web of A. bruennichi built in a square wooden frame (500 × 500 × 150 mm). The spider decorates its web with stabilimenta placed in a vertical linear pattern through the center of the web

Collection and rearing

We collected adult female A. bruennichi along a paddy field in Hwa-seong, Kyung-gi, South Korea (126°50′ N 37°11′ E; altitude: 30–70 m) during August and September and immediately transported them to the laboratory. We placed each individual in a square wooden frame (500 × 500 × 150 mm) custom-designed for orb-web spiders with removable front and back glass covers. The spiders were kept in laboratory environments at 25 ± 1 °C and 100 lx illumination with a 12:12 h light/dark cycle. We humidified the inner sides of the cage twice per day with a spray, and provided the females with juvenile crickets, Teleogryllus emma.

Web measurement

The spiders built their webs overnight in the laboratory. After removing the front and back glass covers from the cage, we photographed the webs with a black velvet background to measure the following parameters: web area, stabilimentum area, radial length, number of spirals, and mesh size (Fig. 1).

To minimize possible influences of web size on prey capture rates (Prokop and Grygláková 2005), we selected webs with stabilimenta and webs of similar size without stabilimenta for our experiments. For webs with stabilimenta, we only included webs that had both an upper and a lower stabilimentum. We excluded webs built by females that had produced an egg sac, because physiology of the spider may influence the decoration characteristics (Walter and Elgar 2012).

To estimate web size, we measured the outermost and innermost diameters of each web from the sticky spirals (Fig. 2). Web area was then calculated as: web area = π × 1/2 outermost diameter × 1/2 innermost diameter. As the stabilimentum of A. bruennichi is a ladder-form, stabilimentum area was calculated as length × (upper width + lower width of the stabilimentum) / 2. Mean radius length was calculated from the lengths of the maximum and minimum radii. The number of spirals was measured as the number of sticky silk circles from the center of the web to the outermost radius. The mesh size (average distance between spirals) was calculated as (maximum radius / (number of spirals at that area − 2) + minimum radius / (number of spirals at that area – 2))/2.
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Fig. 2

Illustration of the web measurement in A. bruennichi. I and O: innermost diameter and outermost diameter of a web, R and R′: maximum and minimum radii, U and L: upper and lower width of a stabilimentum, M: mesh size

Field data collection

We removed the glass covers from the cages and installed the cages containing the webs built in the laboratory on the ground surface in the field site (an artificial pond bounded by weeds). We placed similar numbers of webs with and without stabilimenta in alternating order at 150 (±15)-cm intervals along the edge of the artificial pond. Field data collection was conducted on 10 clear days in September after cloudy days and rainy days were excluded because of difficulties of the field work and prey species variability.

We observed prey interceptions by the webs during trials lasting 5 h each, beginning between 0930 and 1000 hours. We collected all prey struggling within the webs immediately and stored them in ethanol for later identification. We identified all prey to the family level and categorized prey body size as “small prey” (<5 mm) or “large prey” (≥5 mm).

Data analysis

Basically, we used nonparametric statistics in StatView 5.0 (2005). We present, however, the data mean and standard deviation instead of medians and inter-quartile ranges. We compared the number of prey intercepted in webs with and without stabilimenta using Mann–Whitney U tests. We then compared rates of prey interception for different taxonomic groups of prey using Wilcoxon signed-rank tests. We used regression analysis with ANOVA to examine the relationships between the number of prey intercepted and stabilimentum area, web area, number of spirals, and mean radius length. We used the Mann–Whitney U test to compare web structures (web area, mean length of radii, number of spirals, and mesh size) and the mean numbers of small and large prey intercepted between webs with and without stabilimenta.

Results

We investigated prey interceptions for 53 webs with stabilimenta and 37 webs without stabilimenta. A total of 450 prey animals were captured: 331 in webs with stabilimenta and 119 in webs without stabilimenta. The mean number of prey captured per web was 5.0 ± 4.3 (n = 90).

The prey interception was affected by the presence of a stabilimentum. On average, 6.2 ± 4.7 prey animals were intercepted in a single web with stabilimentum, while 3.2 ± 2.9 were intercepted in a web without stabilimentum (Fig. 3a; Mann–Whitney U test: n1 = 53, n2 = 37, z = 4.059, p < 0.0001).
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Fig. 3

Comparison between webs with stabilimenta and webs without stabilimenta. a The number of prey interceptions per web; b the number of UV-sensitive prey; c the number of UV-nonsensitive prey. The median and 5th, 25th, 75th, and 95th percentiles are shown in the box plots

There was a significant difference in the interception of UV-sensitive prey between webs with stabilimenta and webs without stabilimenta. An average of 4.4 ± 3.6 UV-sensitive prey were captured in webs with stabilimenta, compared with 1.8 ± 2.1 captured in webs without stabilimenta (Fig. 3b; Mann–Whitney U test: n1 = 53, n2 = 37, z = 4.576, p < 0.0001). There was no difference in interception rates for UV-nonsensitive prey species in webs with and without stabilimenta (Fig. 3c; Mann–Whitney U test: n1 = 53, n2 = 37, z = 0.221, p = 0.8248): a mean of 1.8 ± 2.9 prey were intercepted in webs with stabilimenta and 1.4 ± 1.6 in webs without stabilimenta.

Classification of the prey

The 450 prey animals intercepted in the webs belonged to 29 family groups (Table 1). Insects in Dipteran families were the most commonly captured prey, comprising 50.7 % (228 preys) of the total prey intercepted.
Table 1

Classification of prey intercepted in the web of A. bruennichi. Ninety webs were observed in total including 53 webs with stabilimenta and 37 webs without stabilimenta

Prey classification

Total number of prey items intercepted

Mean number of prey per web

With stabilimentum

Without stabilimentum

Diptera

 Tipulidae: crane flies etc.

10

0.17

0.03

 Chironomidae: nonbiting midges etc.

146

2.13

0.89

 Muscidae: house flies etc.

15

0.23

0.08

 Drosophilidae: fruit flies etc.

43

0.66

0.22

 Culicidae: mosquitoes etc.

7

0.11

0.03

 Syrphidae: hoverflies etc.

7

0.13

0.00

Hymenoptera

 Andrenidae: mining Bees etc.

2

0.02

0.03

 Apidae: honey bees etc.

3

0.04

0.03

 Ichneumonidae: ichneumon wasps etc.

29

0.32

0.32

 Formicidae: ants etc.

4

0.04

0.05

 Vespidae: paper wasps etc.

3

0.06

0.00

 Braconidae: parasitoid wasps etc.

1

0.02

0.00

 Sphecidae: digger wasps etc.

1

0.02

0.00

 Pompilidae: spider wasps etc.

1

0.02

0.00

Coleoptera

 Chrysomelidae: leaf beetles etc.

6

0.11

0.00

 Scarabaeidae: scarab beetles etc.

3

0.02

0.05

 Staphylinidae: rove beetles etc.

1

0.00

0.03

Lepidoptera

 Pyralidae: snout moths etc.

5

0.09

0.00

 Arctiidae: tiger moths etc.

1

0.02

0.00

 Lycaenidae: gossamer-winged butterflies etc.

1

0.00

0.03

Homoptera

 Cicadellidae: leafhoppers etc.

1

0.00

0.03

 Aphidoidea: aphids etc.

41

0.47

0.43

 Delphacidae: planthoppers etc.

37

0.42

0.41

Hemiptera

 Pentatomidae: stink bugs etc.

11

0.15

0.08

Orthoptera

 Gryllidae: true crickets etc.

5

0.06

0.05

 Tetrigidae: grouse locusts etc.

46

0.66

0.30

 Tettigoniidae: katydids etc.

1

0.02

0.00

Acarina: mites etc.

11

0.17

0.05

Unclassified prey

8

0.09

0.08

Diptera, Hymenoptera, Coleoptera, and Lepidoptera were classified as UV-sensitive, while Homoptera, Hemiptera, Orthoptera, Acarina classified as UV-nonsensitive prey (Ioannides and Horridge 1975; Silberglied 1979; Wakakuwa et al. 2007)

Comparison of the number of prey intercepted in webs with and without stabilimenta paired by family showed different patterns in different taxonomic groups. Prey belonging to the 20 families of Diptera, Hymenoptera, Coleoptera, and Lepidoptera (Table 1) were significantly more likely to be captured by webs with stabilimenta than webs without stabilimenta: mean capture rate = 0.21 ± 0.48 items/web in webs with stabilimenta vs. 0.09 ± 0.21 items/web in webs without stabilimenta (Wilcoxon signed-rank test: n1 = n2 = 20, p < 0.01). On the other hand, there was no significant difference in interception rates for the eight families belonging to Homoptera, Hemiptera, and Orthoptera: 0.24 ± 0.24 items/web in webs with stabilimenta vs. 0.17 ± 0.18 in webs without stabilimenta (Wilcoxon signed-rank test: n1 = n2 =8, p > 0.05).

Stabilimentum area vs. prey interception

The mean stabilimentum area for webs with stabilimenta was 3.0 ± 1.4 cm2 (n = 53). The area of the stabilimentum was a significant predictor of the rate of prey interception (Fig. 4). When the area of stabilimentum increased, more prey were intercepted in the web (ANOVA test for regression analysis: F1,51 = 6.922, R2=0.12, p = 0.0112).
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Fig. 4

The number of prey intercepted plotted against stabilimentum area

Web structure

As we deliberately chose webs of similar size with stabilimenta and without stabilimenta for our field experiments before the webs were installed in the field site, there was no significant difference in the web area between webs with and without stabilimenta (Table 2). The mean length of radii and mesh size also did not differ in webs with and without stabilimenta (Table 2). However, webs with stabilimenta had more spirals on average than webs without stabilimenta (Table 2). When the number of spirals increased, the rate of prey interception increased both in webs with stabilimentum (ANOVA test for regression analysis: F1,51 = 7.400, R2 = 0.127, p = 0.0089) and without stabilimentum (F1,35 = 9.356, R2 = 0.211, p = 0.0042).
Table 2

Comparison of web structures between webs with stabilimenta and webs without stabilimenta in A. bruennichi (mean ± SD)

Web structural variable

Webs with stabilimenta (n = 53)

Webs without stabilimenta (n = 37)

Mann–Whitney U test

Web area (cm2)

669.6 ± 303.8

600.6 ± 278.8

z = 0.964, p = 0.3353

Mean length of radii (cm)

14.3 ± 3.4

13.9 ± 3.4

z = 0.521, p = 0.6026

Number of spirals

35.7 ± 11.3

26.5 ± 8.4

z = 4.034, p < 0.0001

Mesh size (cm)

0.44 ± 0.10

0.48 ± 0.11

z = 1.415, p = 0.1572

We grouped the data for webs with and without stabilimenta to examine the influence of the web structure on the number of prey intercepted. The number of prey intercepted was significantly positively related to the web area (ANOVA for regression analysis: F1,88 = 26.024, R2 = 0.228, p < 0.0001; Fig. 5a), the number of spirals (F1,88 = 24.598, R2 = 0.218, p < 0.0001; Fig. 5b), and the mean radius length (F1,88 = 19.249, R2 = 0.179, p < 0.001; Fig. 5c). On the other hand, the mesh size was not related to the number of prey intercepted (F1,88 = 2.710, p = 0.1033).
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Fig. 5

The number of prey intercepted plotted against web area (a), the number of spirals (b), and mean radius length (c); webs with and without stabilimenta were grouped together for these analyses

Prey size

Prey items of different sizes were intercepted at different rates. A total of 197 small (<5 mm) and 253 large (≥5 mm) prey were captured. The proportion of large prey intercepted in a single web was 0.41 ± 0.28 and small, 0.59 ± 0.28. Larger prey items were captured more than twice as frequently in webs with stabilimenta than webs without stabilimenta (Table 3, p < 0.0001). Differences were slight in capture rates for small-sized prey in webs with and without stabilimenta (Table 3). Only 22 (4.9 %) out of 450 prey captured were >10 mm in size, consisting of 16 prey in 53 webs with stabilimentum and 6 prey in 37 webs without stabilimentum. Difference in interception of prey larger than 10 mm was not statistically approved (p = 0.2169).
Table 3

The number of small (<5 mm) and large (≥5 mm) prey intercepted per web with vs. without a stabilimentum (mean ± SD)

Prey

Web

 

with stabilimentum (n = 53)

without stabilimentum (n = 37)

Mann–Whitney U test

Small

2.6 ± 3.0

1.6 ± 1.8

z = 1.911, p = 0.0560

Large

3.6 ± 2.4

1.6 ± 1.7

z = 4.481, p < 0.0001

Discussion

Our results support the prey-attraction hypothesis for the function of the stabilimentum in A. bruennichi. More prey items were intercepted in webs with stabilimenta than in equally sized webs without stabilimenta. The stabilimentum increased spider foraging success via an enhanced rate of interception of UV-sensitive insect pollinators, including 20 families of Diptera, Hymenoptera, Coleoptera, and Lepidoptera. Our results are in line with the results done in A. trifasciata (Tso 1996), A. aetherea (Elgar et al. 1996), A. appensa (Hauber 1998), A. aurantia (Tso 1998), A. keyserlingi (Herberstein 2000; Bruce et al. 2001), A. versicolor (Li 2005), and A. savignyi (Gálvez 2009).

Results of our study are, however, different from those of a study done in A. bruennichi in grassland habitat in Slovakia (49°28′ N, 19°23′ E; Prokop and Grygláková 2005). Prokop and Grygláková (2005) measured the number of prey captured every 30 min for 6 h in 31 webs with stabilimenta and 12 webs without stabilimenta. They did not find a difference in prey capture rates between webs with and without stabilimenta. These differences observed in the same species might be due to behavioral differences between populations in Slovakia (Central Europe) and South Korea (East Asia) isolated by distance and other geographic barriers over the long term. Alternatively, the result may be explained by differences in the characteristics of insect prey between the two field sites. Prokop and Grygláková (2005) reported that more than 40 % (webs with stabilimenta, 45 %; webs without stabilimenta, 43 %) of insects captured were Orthopterans, while Diptera comprised 50.7 % of the total number of prey intercepted in our study.

As noted by Prokop and Grygláková (2005), stabilimentum building might be more beneficial in grasshopper-poor habitats where flies constitute a greater part of spiders’ potential prey. Another possible element is that the difference in results may be due to methodological differences. Prey interceptions were observed at intervals of 30 min in the study of Prokop and Grygláková (2005). Small flying insects could be quickly devoured in place by the spider and thus go unreported, which might produce a bias in the results. Moreover, the study of Prokop and Grygláková’s (2005) only included 12 webs without stabilimenta. This small sample size might make it difficult to statistically detect real differences in prey capture rates between webs with and without stabilimenta.

In this study, we propose another advantage resulting from the building of stabilimenta by orb-weaving spiders. The stabilimentum of A. bruennichi had a strong effect on rates of capture for larger prey items: webs with stabilimenta captured more than twice as many large (≥5 mm) prey than webs without stabilimenta, while there was only a slight difference in capture rates for small (<5 mm) prey. Previous studies have largely neglected to consider the energy content of the prey. The stabilimentum may also mechanically stabilize and strengthen the orb web (Robinson and Robinson 1970). Spiders decorating their webs with stabilimenta at higher frequencies might expect to accumulate more energy by capturing larger flying insects, eventually resulting in higher growth rates (Li 2005).

The Araneid spider-genus Argiope is cosmopolitan with 76 currently known species. Argiope spiders show high diversity in their stabilimentum design both between and within species (Seah and Li 2002; Walter and Elgar 2012). Furthermore, different species and populations decorate their webs with stabilimenta at different frequencies, and individuals alter their decorating behavior on a daily basis (Bruce 2006; we observed such variability within individuals even when the spiders built webs in the laboratory.) Comparisons among different Argiope species suggest the possibility that the adaptive importance of stabilimentum usage may vary across species and ecological contexts.

There are many potential functions of stabilimenta. The evolutionary origin of this trait in the genus Argiope may have to be separated from its contemporary role (Walter and Elgar 2012). Whereas the original function of stabilimenta in A. bruennichi is probably not the prey-attraction, this study demonstrates that their presence enhances prey capture, at least in some ecological circumstances.

Acknowledgments

For help in data collection and field research support, we thank Byunghyuk Kim, Sanha Kim, Seungtae Kim, and Hyojeong Kim. We are also grateful to Susan Lappan for helpful comments on the manuscript. This work was supported by Korea Research Foundation Grant funded by the Korean Government (KRF-2008-331-C00270), the Ewha Global Top 5 Grant 2011 of Ewha Womans University, and the University of Incheon Research Grant (2011).

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