Abstract Recent decades have witnessed an intensified expansion of thermophilic organisms from southern into northern Europe. Argiope bruennichi, an orb-weaver spider species, is extending its range relatively fast and gradually becoming a common species in Europe. The aim of this study was to investigate how this relatively newly-come taxon is affecting another orb-weaver spider species and whether it demonstrates features of an invasive species. Interactions were examined between this species and another dominant species with similar body and web size, Araneus quadratus. The study areas were located in two adjacent regions in northeast Poland: the warmer Mazury Lake District and the colder Suwalki Lake District. The areas differed in both population density of the studied species as well as in climatic conditions. Six study sites were selected in each region. In the Mazury Lake District, A. bruennichi was more frequent than A. quadratus; this relationship was reversed in the Suwalki Lake District. We measured the height of the web hub above the ground and the height of the plants to which webs were fixed. Web location height was chosen as an indicator of the interaction. The results indicate that A. quadratus located its webs higher than A. bruennichi, regardless of species abundance and region. A. bruennichi does not exert a significant negative impact on A. quadratus web placement. The two species clearly prefer different heights, which in turn may determine the kind of prey they catch. Many spiders are able to coexist in the same habitats because they can exploit different space and food resources (Riechert and Cady 1983, Novak et al. 2010). Microhabitat requirements, food preferences (Austin 2002), the role of each species in the ecosystem (Hutchinson 1957), and its influence on the environment combine to define its niche (Peterson 2003, Entling et al. 2007). The ecological niche determines the expansion process of a population and knowledge about a niche’s properties enables predictions of the future direction of colonization (Peterson 2003). One of the many dimensions of an ecological niche is space (Soberón 2007). Large numbers of individuals may cause a spatial separation of niches which enables different species to coexist in the same biocenosis (Enders 1974). However, a high density of individuals may also limit the availability of suitable microhabitats for web construction and cause interactions among them (Heiling and Herberstein 1999). Low density of individuals, spatial separation, and use of a variety of food resources all favor coexistence owing to a low degree of competition (Uetz et al. 1978, Brown 1981, Wise 1981, Richardson and Hanks 2009, Tahir et al. 2012). Direct interspecific interactions are rare in web spider communities because of their passive hunting strategy (Tahir et al. 2012). Nevertheless, indirect interactions have been observed among Araneidae, Linyphiidae, and Theridiidae, due to changes of web positions that were found to be dependent on spider densities (Horton and Wise 1983, Herberstein 1998, Fasola 1999, Opatovsky et al. 2016). Spiders might also relocate their webs, independent of spider density, because the current location is prey-poor (Nakata and Ushimaru 1999). The height of web placement determines the type of potential prey resources in a given habitat (Riechert and Cady 1983, Hénaut et al. 2006, Richardson and Hanks 2009). The Palearctic spider Argiope bruennichi extended its range to the north during the 20th century. Particularly, rapid expansion took place during the 1990s and the following decade. Its original range covered areas around the Mediterranean and Black Sea, but the northern border of the range has now reached Fennoscandia (Ivinskis et al. 2009, Kumschick et al. 2011). Most likely, harsh climatic conditions occurring further north break the dispersion of this originally thermophilous species, in spite of its possibly shifted temperature niche (Krehenwinkel and Tautz 2013). Although A. bruennichi was noted in Fennoscandia (Bratli and Hansen 2004, Jonsson 2004, Terhivuo et al. 2011), the observations refer mostly to single individuals. Stable populations of the species occurred in the south of Sweden, a region characterized by a milder, moderate climate (Jonsson 2004). A. bruennichi became very frequent across most of the territory of Poland during the 1990s (Barabasz and Górz 1998). However, in the Suwalki Lake District, the density of the species is still lower (Wawer 2014), hence it can be treated as the periphery of an expanding range (Brown et al. 1996). Although A. bruennichi’s expansion is a natural phenomenon, it may be assumed that the gradual colonization of new areas could change interactions within local communities of orb-weaver spiders. Introduced species can cause significant changes to the ecosystem (Hann 1990, Jakob et al. 2011), but we do not know how natural range changes may affect the coexistence of orb-weavers, e.g., A. bruennichi and Araneus quadratus. Expansion may have an invasive context according to the IUCN definition; it may, e.g., destroy habitats and change the density of native species (Mack et al. 2000). Some authors argue that although the appearance of a new spider species in a given habitat does not always produce a negative effect, it can modify the behavior of coexisting species (Burger et al. 2001). The recent rapid expansion of A. bruennichi and its dominance in spider communities provides a rare opportunity to study the interaction between A. bruennichi and A. quadratus, a common species with a similar biology and habitat preferences (Crome 1956, Kajak 1965, Prószyński and Staręga 1971, Nyffeler and Benz 1989). If species’ spatial preferences overlap, then there is a probability that either one species will displace the other or that the species will compete over web sites. Similar studies (Nyffeler and Benz 1989, Rachwał 2006), have been conducted, but they did not consider the peripheral edge of the range, where the density of an expanding species may vary more than in the core range. We decided to investigate the relationship between A. quadratus and A. bruennichi in two regions which differed with respect to time of settlement and density A. bruennichi. We investigated web height above the ground as an indicator of the interaction between the two species. We ask whether web location heights diverge under stronger competition and whether the expansive A. bruennichi on the periphery of its range has an influence on the web placement of A. quadratus. Materials and Methods Spiders A. bruennichi (Scopoli, 1772) and A. quadratus (Clerck, 1757) occupy similar grassland habitats; mature body size is 6.9–8.3 mm and 7–11 mm in males and 9.9–22 mm and 10.5–20.5 in females; average web area is 489 and 445 cm2, respectively (Kajak 1965, Nyffeler and Benz 1978, 1989; Nentwig et al. 2017). Study Area Web location of A. bruennichi and A. quadratus was investigated in wastelands in the Suwalki Lake District. Study localities were selected in two adjacent regions differing in climatic conditions: the warmer Mazury Lake District (53°41′N, 21°54′E) and the cooler Suwalki Lake District (Suwalki Lake District) further north (54°18′N, 22°17′E) (Fig. 1). In these regions, A. bruennichi has been present for about 10 years. Field work was carried out in August 2012. We chose 12 study sites (six in each region): Mazury Lake District 1 (53°41′2″N, 21°54′29″E), Mazury Lake District 2 (53°41′2″N, 21°54′7″E), Mazury Lake District 3 (53°40′41″N, 21°52′6″E), Mazury Lake District 4 (53°41′5″N, 21°54′0″E), Mazury Lake District 5 (53°41′31″N, 21°54′41″E), Mazury Lake District 6 (53°41′37″N, 21°54′52″E); Suwalki Lake District 1 (54°18′29″N, 22°22′7″E), Suwalki Lake District 2 (54°18′42″N, 22°25′52″E), Suwalki Lake District 3 (54°18′48″N, 22°27′14″E), Suwalki Lake District 4 (54°16′40″N, 22°17′29″E), Suwalki Lake District 5 (54°16′38″N, 22°17′34″E), and Suwalki Lake District 6 (54°16′41″N, 22°17′42″E). The study sites were grasslands situated in agricultural wastelands. Fig. 1. View largeDownload slide Map of Europe and schematic map of Poland showing location of regions where the research was conducted: Mazury Lake District (MLD) and Suwalki Lake District (SLD). The map created in ArcGIS. Fig. 1. View largeDownload slide Map of Europe and schematic map of Poland showing location of regions where the research was conducted: Mazury Lake District (MLD) and Suwalki Lake District (SLD). The map created in ArcGIS. Webs A transect was set across each study site, and the number of webs were recorded along the transect. Its length varied depending on the site’s width (from 50 to 125 m). The webs of A. bruennichi and A. quadratus were recorded on the transect line. In the absence of a spider on its web, the species was determined based on web characteristics (e.g., stabilimentum) or, in the case of lack of stabilimentum, on specimens under the web. The height of each observed web was measured defined as the distance from the ground to the hub (the center of the web structure). We also measured the height of the two main plants to which the thread was fixed (web frame plants). Statistical Analysis We used a t-test to analyze differences in web height and plant height between species. A general linear model (GLM) with log-link function and normal error distribution was used with web height (cm) and web frame plant height (cm) as dependent variables’ species, region, and study site were set as independent variables. The chi-square test was used to compare the frequency of both species’ occurrences in the study sites. A Pearson correlation was used to examine the relationships between web frame plant height and height of web location and to determine whether it was correlated to region. The statistical significance was set at P ≤ 0.05. Software environment SAS 2013, for statistical computing and graphics, was used. Results In total, 504 webs were examined, including 258 in the Mazury Lake District and 246 in the Suwalki Lake District. Generally, A. bruennichi’s webs were less numerous than A. quadratus webs (39.8 and 60.2%, respectively) (Fig. 2). However, in the Mazury Lake District, A. bruennichi webs were more numerous (57.4%) than A. quadratus webs (42.6%), while in the Suwalki Lake District, A. quadratus webs were three times more numerous (78.4% webs) than those of A. bruennichi webs (21.6%). Frequency analysis showed significant differences in species proportion between the regions (χ2 = 65.9; df = 1; P < 0.001). Fig. 2. View largeDownload slide The percentage of webs of A. quadratus and A.bruennichi per 10-m transect at 12 sites in two regions: Mazury Lake District (MLD) and Suwalki Lake District (SLD). Fig. 2. View largeDownload slide The percentage of webs of A. quadratus and A.bruennichi per 10-m transect at 12 sites in two regions: Mazury Lake District (MLD) and Suwalki Lake District (SLD). Generally, web height differed significantly between species (t-test, t502=18.80; P < 0.0001), with A. bruennichi placing its webs about 26.6 cm lower than A. quadratus (Fig. 3). In the Mazury Lake District, A. bruennichi web’s heights ranged from 14.25 to 89.75 cm (mean 40.1 cm) above the ground while in the Suwalki Lake District, the webs were located higher (from 26.25 to 77.75 cm; mean 47.6 cm). A. quadratus located its webs at similar heights in both regions: from 27.25 to 102.75 cm (mean 68.1 cm) in the Mazury Lake District and from 38.75 to 116.75 cm (mean 69.1 cm) in the Suwalki Lake District. Statistically, there was no difference in the web height of A. bruennichi between the two regions (GLM F = 1.99; P = 0.16), and the same pattern was found for A. quadratus (GLM F = 0.56; P = 0.45). Fig. 3. View largeDownload slide Differences in average hub height of A. bruennichi (white) and A. quadratus (black) within the regions (MLD [Mazury Lake District], SLD [Suwalki Lake District]). The lower boundary of the box indicates the 25th percentile, the line within the box shows the median, and the upper boundary of the box indicates the 75th percentile. Whiskers indicate minimum and maximum values. Points outside the whiskers indicate extreme values. Fig. 3. View largeDownload slide Differences in average hub height of A. bruennichi (white) and A. quadratus (black) within the regions (MLD [Mazury Lake District], SLD [Suwalki Lake District]). The lower boundary of the box indicates the 25th percentile, the line within the box shows the median, and the upper boundary of the box indicates the 75th percentile. Whiskers indicate minimum and maximum values. Points outside the whiskers indicate extreme values. A. bruennichi chose lower plants for building webs than A. quadratus (t-test, t502=10.98; P < 0.0001) (Fig. 4). In addition, there was a significant correlation between web frame plant height and the height of web location for both study regions and both species (Pearson correlation r = 0.83, P < 0.0001): the higher the plants, the higher the webs were placed (Fig. 5). Web frame plant heights chosen by A. bruennichi were significantly different between sites both within the Suwalki Lake District (GLM F = 2.82; P = 0.03) and within the Mazury Lake District (GLM F = 22.5; P < 0.0001). The height of the plants preferred by A. quadratus varied between the sites in the Mazury Lake District (GLM F = 6.40; P < 0.0001) and in the Suwalki Lake District (GLM F = 4.99; P = 0.001). Moreover, frame plant heights chosen by A. bruennichi (GLM F = 13.60; P = 0.0003) and those chosen by A. quadratus (GLM F = 6.83; P = 0.0094) varied significantly between the regions: in the the Suwalki Lake District, the plants were significantly higher than in the Mazury Lake District. Fig. 4. View largeDownload slide The average height of the web frame plants chosen by A. bruennichi (white) and A. quadratus (black) in regions (MLD [Mazury Lake District], SLD [Suwałki Lake District]). The lower boundary of the box indicates the 25th percentile, the line within the box shows the median, and the upper boundary of the box indicates the 75th percentile. Whiskers indicate minimum and maximum values. Points outside the whiskers indicate extreme values. Fig. 4. View largeDownload slide The average height of the web frame plants chosen by A. bruennichi (white) and A. quadratus (black) in regions (MLD [Mazury Lake District], SLD [Suwałki Lake District]). The lower boundary of the box indicates the 25th percentile, the line within the box shows the median, and the upper boundary of the box indicates the 75th percentile. Whiskers indicate minimum and maximum values. Points outside the whiskers indicate extreme values. Fig. 5. View largeDownload slide Relationships between the height web location of A. bruennichi (white) and A. quadratus (black) and web frame plant height in the two regions (MLD [Mazury Lake District], SLD [Suwałki Lake District]). Fig. 5. View largeDownload slide Relationships between the height web location of A. bruennichi (white) and A. quadratus (black) and web frame plant height in the two regions (MLD [Mazury Lake District], SLD [Suwałki Lake District]). The number of A. bruennichi webs did not significantly affect the web height of the other species (GLM F = 3.24; P = 0.07), the number of A. quadratus webs also had no influence on the web height of A. bruennichi (GLM F = 3.50; P = 0.06). Discussion The frequency of species under study differed between the two regions: A. bruennichi was more numerous in the Mazury Lake District, but A. quadratus occurred more frequently in the the Suwalki Lake District. In the Mazury Lake District, we found more A. bruennichi webs, while in the Suwalki Lake District, this species occurred only occasionally. Similar abundance relationships between these two spider species were shown in a study conducted in 2009–2011: A. bruennichi dominated in the Mazury Lake District (0.7/m2), while A. quadratus dominated in the Suwalki Lake District (1.1/m2) (Wawer 2014). A comparison with earlier research conducted by Kajak (1960) in the 1950s on meadows showed that the density of A. quadratus (0.1/m2) was lower than in 2010 (Wawer 2014), and there were no A. bruennichi in north-eastern Poland. In general, the farther north, the more A. quadratus and the less A. bruennichi were seen. In both studied regions, A. bruennichi built its web about 27 cm lower than A. quadratus, whose webs were mainly found closer to the ground. Other studies have demonstrated even greater differences, such as 30 cm in Switzerland (Nyffeler and Benz 1989) and 38 cm in central Poland (Rachwał 2006). Perhaps, the small differences in observed web height and web location were dependent on the height of vegetation. Additionally, Nyffeler and Benz (1989) show that A. bruennichi overlaps in web height during part of the season with other species, including A. quadratus. So, these species compete at least during some parts of the season. In our study, A. quadratus showed conservative behavior in web building and placed their webs at a similar height in both the Mazury and Suwalki Lake Districts. The web heights of A. bruennichi also did not statistically differ in both regions. However, A. bruennichi was characterized by a plasticity in web ranges. The web range of this species was wider in the Mazury Lake District than in the Suwalki Lake District, where the web frame plants were higher (Fig. 4). We discovered a positive correlation between the web frame plant height and web height among both species. The location of a web is mainly determined by the structure of the vegetation and the availability of space (Colebourn 1974, Hatley and MacMahon 1980, Robinson 1981, Fasola and Mogavero 1995, McNett and Rypstra 2000, Bruggisser et al. 2012). Hence, the structure of the plants probably had an influence on the differences in A. bruennichi web range between the regions. The analysis showed that species abundance in studied species did not influence web height, as P-values were higher than 0.05. However, we suggest that results occurring on the periphery of the range point to a marked trend of interaction between the species. It is possible that the abundance of coexisting orb-weaver spiders may modify interactions between them. Some experiments have shown that the density of individuals affects web height of web distribution between linyphiids Frontinella frutetorum and Neriene radiata (Herberstein 1998) and between theridiid Enoplognatha gemina and linyphiid Alioranus pastoralis (Opatovsky et al. 2016). However, some studies did not show such effects; e.g., a reduction in the density of an American Argiope species did not significantly affect the position of webs constructed by other species (Horton and Wise 1983). Similarly, in Italy, Fasola (1999) did not find any competition between three dominant species (A. bruennichi, Araneus marmoreus, and Agelena labyrinthica) in web numbers or web positions. To summarize, the appearance of A. bruennichi and its domination did not influence A. quadratus web height in the study area. A. bruennichi may occupy free space in the environment without changing the strata preferences of A. quadratus. Valéry et al. (2008) argue that ‘invasive species’ expand rapidly, occupying areas and becoming numerous in communities. A. bruennichi has been defined as ‘invasive’ in a few publications, as a species with fast colonization (Ivinskis et al. 2009, Terhivuo et al. 2011, Krehenwinkel and Tautz 2013). This rapid expansion has also been observed in the last decade in north-eastern Poland (Wawer 2014). However, in the context of invasive species having a negative effect on the environment (Davis 2013, IUCN 2000), we did not observe any negative effect concerning the space niche of A. quadratus. Moreover, Taraschewski et al. (2005), though highlighting the major impact A. bruennichi had on reducing the number of insects, stated that it did not cause prey extinction. Due to different habitat preferences, the species probably also do not degrade smaller spider species, who typically prefer more compact vegetation (Gunnarsson 1992). Other authors have also noted that new species do not necessarily cause invasion (Moutou and Pastoret 2010). These data do not support the degradation of other spider species, although some cryptic effects might be in play. It is possible, that juveniles outcompete small spider species or other invertebrates, but so far, studies in this area have not been conducted. Acknowledgments We thank Magdalena Witek (MIZ PAS) and Marcin Zalewski (MIZ PAS) for helpful comments. We thank Miłosława Barkowska (University of Warsaw) and Artur Goławski (SUNSH) for help in statistical analyzes. We thank Barry K. Oliphant for linguistic corrections. The authors wish to express special thanks to Professor Anna Liana (MIZ PAS) for encouragement and support throughout studies. We are very grateful to reviewers for comments and suggestions that improved this manuscript. References Cited Austin, M. P. 2002. 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Environmental Entomology – Oxford University Press
Published: Feb 1, 2018
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