2005. The Journal of Arachnology 33:197±204

HORIZONTAL AND VERTICAL DISTRIBUTION OF (ARANEAE) IN SUNFLOWERS

Stano PekaÂr: Research Institute of Crop Production, Drnovska 507, 161 06 Praha 6ÐRuzyneÏ, Czech Republic. E-mail: [email protected]

ABSTRACT. Sun¯owers are an increasingly important crop plant in the Czech Republic. The fauna of this crop has not been investigated yet. The aim of this study was to monitor the spider fauna of sun¯owers and to study the seasonal change in the spatial and vertical distribution of this fauna. For this purpose a small experimental area was used where spiders on each single leave of 50 sun¯ower plants were visually checked at monthly intervals from spring until autumn. The density of spiders increased during the season reaching a maximum of seven spiders/plant in the autumn shortly before harvest. The spatial distribution changed accordingly, being random in spring and early summer and normal or aggre- gated toward late summer. Two spider , bimaculata and Theridion impressum (Theridi- idae), dominated (96% of all individuals) throughout the season. These two species exhibited a different microhabitat preference: N. bimaculata individuals were found particularly on the lower sun¯ower leaves, T. impressum preferred higher leaves. The density of the spiders (per leaf) was independent of the density of two dominant pest species, aphids and leafhoppers. Keywords: Aphids, spatial distribution, agrobiocenosis, strati®cation, colonization

Although sun¯owers are considered the (L. Koch 1875), was found to prey on aphids second most important oilseed crop in the and other pests on sun¯ower (Singla 1999). world (Cobia & Zimmer 1978), in the Czech As the fauna of predators occurring on sun- Republic their importance was not recognized ¯owers has not been investigated in , until recently when the current production had the ®rst aim of this study was to monitor spi- not been able to cover the need of our food ders, particularly the change in their temporal industry (JiraÂtko et al. 1996). Since then the and spatial distribution in a sun¯ower plot. planted area has enlarged mainly in the south- Another aim was to observe the vertical dis- eastern part of the country where the warmer tribution of the most abundant species of spi- climate provides suitable conditions for a high ders on sun¯owers. Very little attention has production. been paid to the strati®cation of spider fauna In its native region, i.e. , the in agroecosystems (exceptions are He et al. sun¯ower has many pests (Charlet & Brewer 1995; Hao et al. 2000), obviously due to the 1998). Thus it thrives better in foreign coun- intensive effort required for such investigation tries because it has left a multitude of pests (Holland et al. 2004). and diseases behind. This is particularly true for Europe. In the Czech Republic the sun- METHODS ¯ower plants are attacked by only a few pests: The study was performed in Praha-RuzyneÏ, aphids, leafhoppers, moths and heteropterans the Czech Republic (50Њ06ЈN, 14Њ15ЈE, fau- (JiraÂtko et al. 1996). nistic grid no. 5951). The sun¯owers were The fauna of natural enemies of sun¯ower planted in April 2003 in rows 80 cm apart, at pests has been so far investigated only outside a distance of 30 cm from one seedling to an- Europe. It was found to be composed of var- other. The total area was about 2,000 m2.In ious heteropterans, lacewings, coccinellids, the middle of this area, an experimental plot ants and parasitoids (Lynch & Garner 1980; (4 m ϫ 7 m) including 50 plants was selected. Boica Junior et al. 1984; Men & Thakre The position (coordinates relative to the left 1998). Spiders were also among the most lower corner of the plot) of each plant within abundant and important predators (Seiler et al. the experimental plot was mapped. 1987; Royer & Walgenbach 1991). For ex- The investigation began in late May when ample, an araneid species, Neoscona nautica sun¯ower plants were 10 cm tall and termi-

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Table 1.ÐList of spiders recorded species on the sun¯owers during one season. Numbers are total records and the percentage from the total number.

Family/species Number % Araneidae (Walckenaer 1802) 11 0.70 Araneus sp. 1 0.06 Araniella sp. 4 0.20 acalypha (Walckenaer 1802) 1 0.06 Enoplognatha sp. 19 1.20 (Linnaeus 1767) 282 17.10 Theridion impressum L. Koch 1881 1301 79.20 Theridion varians Hahn 1833 2 0.11 pusilla (Sundevall 1830) 15 0.90 Thomisidae Xysticus sp. 6 0.40 Dictynidae Dictyna sp. 1 0.06 Total 1643 nated in September shortly before harvest. tribution of spiders in the study plot was stud- Plants in the selected plot were examined at ied using graphical spatial analysis. The monthly intervals, i.e. altogether ®ve times analysis projects a three-dimensional dataset during the season. On each examination date that includes two-dimensional coordinates of every single leaf (upper and lower surface) of each plant and the spider density for each each of 50 plants was visually inspected to plant on a two-dimensional plane. The gradi- record the number of spiders present. The ent of density is displayed as shades of gray leaves were gently inspected not to disturb with white color standing from 0 and black present spiders. The height of each plant was standing for the maximum density. The con- recorded on each date too. The spiders were tours of density were modelled using distance not sampled, only visually inspected in order weighted least-square method. Numbers rep- to record their change during the seasons. Fur- resent means Ϯ standard error throughout the ther, on each date 25 plants were selected out- text. side the experimental plot. On each plant one leaf was sampled in order to examine the RESULTS number of spiders, aphids (unidenti®ed), leaf- Horizontal distribution.ÐMore than 1600 hoppers (unidenti®ed) and other insects. All individual spiders were observed during the spiders were identi®ed to species, if possible, study (Table 1). The majority of spiders (99%) or to a . Juvenile theridiid spiders were were represented by theridiids. Two spider identi®ed using PekaÂr (1999). species, T. impressum L. Koch 1881 and Statistical analyses were performed using Neottiura bimaculata (Linnaeus 1767) (both STATISTICA (StatSoft). Distribution of spi- Theridiidae), accounted for 98% of all spiders, ders at each observation date was tested using with the former species making up 79% of the Kolmogorov-Smirnov test (KST) for normal- spider fauna. The density of spiders on sun- ity. Linear regression models (LM) were used ¯owers increased over the study season. On to study the relationship between density and 28 May 2003, there were 0.27 Ϯ 0.09 spiders the season and the relationship between prey per plant. On 25 June, the density increased and spider densities. Since the data did not to 1.49 Ϯ 0.26 and on 23 July it was 1.12 Ϯ follow a normal distribution, log-transforma- 0.20 individuals/plant. On 20 August, the den- tion was used prior to analysis. Horizontal dis- sity further increased to 6.78 Ϯ 0.68 and on PEKAÂ RÐHORIZONTAL AND VERTICAL DISTRIBUTION OF SPIDERS 199

Figure 1.ÐSeasonal change in the spatial distribution of spiders on the sun¯ower plot. The graph represents the study plot. The shades of gray identify spider density (per plant) on individual plants: the darker the shade the higher number of individuals. Contours of densities were modelled using least-square method. Data from 50 plants in one 4 m ϫ 7 m plot, inspected repeatedly.

17 September it was 6.98 Ϯ 0.76 spiders per analysis of each individual plant revealed that plant. The overall density thus increased fol- there was a change of density within the plot. lowing a linear model y ϭϪ0.48 ϩ 0.07*ϫ The highest increase (5.7 times on average) in (LM, R2 ϭ 0.91, P Ͻ 0.04). The average in- the density was recorded from July±August, crement was thus 3.5 spiders/plot/day. i.e. in the period following breeding when spi- Although the mean spider density of the en- der density increased on 88% of the plants. A tire plot increased during the season, detailed less pronounced increase was found from 200 THE JOURNAL OF ARACHNOLOGY

Figure 2.ÐSeasonal changes in the vertical distribution of spider density (mean Ϯ SE) on sun¯ower plants. Leaves are numbered from the bottom to the top of the plants and grouped into height categories of 5 leaves.

May±June (1.2 times) when the spider density and July the distribution was rather random increased on 49% of the plants. From June± (KST, P Ͻ 0.01). In August and September it July the average density decreased (0.37 approached a normal distribution (KST, P Ͼ times) on 41% of the plants. Finally, from Au- 0.10). But the analysis of the spatial distri- gust±September the average density also de- bution showed that the distribution was in fact creased (0.2 times) on 53% of the plants. aggregated toward the end of season with two The distribution of spiders changed during patches of high spider density on the margin the season as follows (Fig. 1): in May, June of the study plot (Fig. 1). PEKAÂ RÐHORIZONTAL AND VERTICAL DISTRIBUTION OF SPIDERS 201

Figure 3.ÐMean (Ϯ SE) density of N. bimaculata and T. impressum on sun¯ower leaves (numbered from the bottom to the top of the plants and grouped into height categories of 5 leaves). Data from July and August pooled.

Vertical distribution.ÐThe strati®cation studies it was dominated by theridiid spiders. of spiders did not change dramatically during Some differences were observed in compari- the season. Temporal analysis showed that the son with other crops, which presumably result spiders were always more abundant on the up- from the different plant structure. Large sun- per leaves, except for the terminals, which ¯ower leaves do not provide suitable attach- formed the ¯ower (Fig. 2). The distribution of ments for the webs of araneid spiders, which the two most abundant species, N. bimaculata are therefore more abundant on structurally and T. impressum, differed. While N. bima- more complex plants, such as soybean or rape. culata was mainly found in the lower parts of In North America, the sun¯ower was domi- the plants, T. impressum dominated the upper nated by other spider guilds: thomisid and sal- parts (Fig. 3). ticid spiders (Seiler et al. 1987). This is be- The vertical distribution of aphids on sun- cause the spider fauna of agroecosystems in ¯ower leaves is shown in Fig. 4. Unlike spi- North America is different from that in Eu- ders, aphids were more abundant on lower rope (Nyffeler & Sunderland 2003). than on upper leaves. The density of spiders Increase of spider density with the devel- (per leaf) was independent of the density of opment of crops was observed in many sea- aphids and/or leafhoppers (LM, P Ͼ 0.23). sonal crops including sun¯owers (Royer & DISCUSSION Walgenbach 1991; Duf®eld & Reddy 1997). Observed composition of spiders on sun- In this study it was caused by the in¯ux of ¯owers was similar to the canopy fauna of spiders, mainly theridiids, from neighboring corn, soybean or rape in Europe (e.g., Alder- habitats, which is taking place mainly in the weireldt 1989; Nyffeler 1982), i.e., in all these spring (Blandenier & FuÈrst 1997). The new 202 THE JOURNAL OF ARACHNOLOGY

Figure 4.ÐMean (Ϯ SE) density of spiders and aphids on sun¯ower leaves (numbered from the bottom to the top of the plants and grouped into height categories of 5 leaves). Data from July and August pooled. individuals settled randomly in the plot, in- the density is expected to be a function of dicated by their random distribution. In June plant size and complexity, thus smaller plants the spiders reached maturity and mated, fol- host fewer spiders than tall ones. In accor- lowed by a decline in spider density resulting dance with this, Liu et al. (2003) observed a from the death of males. In July they repro- maximum density of four spiders per cotton duced (PekaÂr 1999) and the newborn spider- plant, whereas Zhang et al. (1997) found a lings dispersed locally. As a result the distri- maximum of six spiders per corn plant. bution became aggregated. Such distribution The two principal species of theridiid spi- has been rarely documented for spiders in ders seem to utilize different strata for their agroecosystems (e.g., Yan 1988; Nyffeler & webs. Such dichotomous but syntopic web Breene 1992). Linyphiid spiders showed no placement may be a result of competition or evidence of spatial pattern (Thomas et al. site preference. In an experimental work on 1990; Holland et al. 2004) probably because the competition between two sympatric liny- of their high dispersal ability. A change from phiid spiders, Herberstein (1998) found that random to aggregated distribution as observed two species, Frontinellina frutetorum (C.L. in this study was found also by Cang et al. Koch 1834) and Neriene radiata (Walckenaer (1989). They recorded that a linyphiid spider 1842), compete for web space. As a result, (Sundevall 1830) they placed their webs in different strata when had a random distribution at low population occurring syntopically. No web displacement densities but aggregated at higher population was observed for the theridiid spiders. Neot- densities in cotton. tiura bimaculata was never found in the upper Spider densities vary not only temporally strata even on plants where T. impressum was but also between different crops. In general, absent. Thus it is possible that these two spe- PEKAÂ RÐHORIZONTAL AND VERTICAL DISTRIBUTION OF SPIDERS 203 cies have different microhabitat requirements Arachnology. (P.A. Selden, ed.). British Arach- and do not compete mutually for space. Sim- nological Society, Burnham Beeches, Bucks. ilar preference for a certain stratum has also Boica Junior, A.L., A.C. Bolonhezi & N.J. Paccini. been observed in other spider species (e.g. 1984. Survey of insect pests and their natural Kim et al. 1989). enemies on sun¯ower (Helianthus annuus L.), grown as ®rst and second crops in the Munici- In total the number of spiders was higher pality of Selviria, Mato Grosso do Sul. Anais da in the upper than in the lower stratum in this Sociedade Entomologica do Brasil 13:189±196. study. In contrast to this, Liu et al. (2003) Cang, H., Y.J. Zhang & Y.Y. Zhu. 1989. Studies on found that there were more spiders in the low- the spatial distribution pattern and sampling tech- er parts of cotton plants than in the upper niques of predators in cotton ®elds. Natural En- parts. Similar results were obtained from a emies of Insects 11:70±76. study on rice (Anwaru & Ibrahim 1995). But Charlet, L.D. & G.J. Brewer. 1998. Sun¯ower In- higher spider densities in the lower strata ob- sect pest management. University of Minnesota. served in these studies are due to the inclusion Available at http://ipmworld.umn.edu/chapters/ of epigeic spiders. Sun¯ower plants are not charlet.htm. Cobia, D.W. & D.E. Zimmer. 1978. Sun¯owers: used as foraging sites by epigeic spiders as the production and marketing. N. D. 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