J Insect Behav (2013) 26:283–303 DOI 10.1007/s10905-012-9335-7
Web-Building Flexibility Differs in Two Spatially Constrained Orb Spiders Thomas Hesselberg
Revised: 12 May 2012 / Accepted: 21 May 2012 / Published online: 5 June 2012 # Springer Science+Business Media, LLC 2012
Abstract Shelter and trap-building animals that compete for limited space and/or face costly relocations benefit from being flexible in their construction behavior. Orb spiders are good examples of this and their easily quantifiable two-dimensional webs allow us to analyze the behavioral adaptations and costs in terms of higher error levels or less precision resulting from building webs in sub-optimal conditions. Here I study behavioral flexibility in spatially constrained spiders by analyzing a wide range of web parameters including measures that indicate errors during web-building. I compare the geometry of laboratory webs of two orb spiders, Cyclosa caroli and Eustala illicita, built in differently shaped experimental frames and report two major findings. i) The two species differ in their ability to build webs in constrained spaces. ii) E. illicita adjusted a range of parameters including shape, area utilization and mesh height in response to spatial constraints, but kept other parameters constant, most notably the length of anchor threads and the shape of the auxiliary spiral. I furthermore found that constrained spiders did not make significantly more errors during web-building than when they had amble space available. Keywords Web-building behavior . behavioral flexibility . orb web geometry . area optimization . Araneidae
Introduction The ability to adapt specific behaviours in response to novel stimuli is known as behavioural plasticity or flexibility. Examples from vertebrates are plentiful and T. Hesselberg Smithsonian Tropical Research Institute, Apartado, 0843-03092 Balboa, Ancón, Republic of Panamá Present Address: T. Hesselberg (*) Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK e-mail:
[email protected]
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ranges from foraging innovation in guppies (Laland and Reader 1999) via opening of automatic doors by sparrows (Breitwisch and Breitwisch 1991) to opportunistic tool use in crows and primates (Kacelnik 2009; Seed and Byrne 2010). Recently it has become clear that many invertebrates, despite their more limited brain capacity, have a flexibility in at least some of their behaviours that is comparable to that of vertebrates (Chittka and Niven 2009). For instance, honeybees compensate for wing damage by adjusting their foraging behaviour to maintain a high food delivery to the hive (Dukas and Dukas 2011) and jumping spiders use trial-and-error to adjust their predatory strategy to fool the sensory system of their prey (Jackson and Wilcox 1993; Nelson and Jackson 2011). However, while the ability to adjust behaviour according to changes in the environment is important for all animals, it is particularly important to shelter and trap-building animals that either face intense competition for available space or suffer high costs of relocation (Hansell and Ruxton 2008). Thus behavioral flexibility is widespread among animal ‘architects’, especially in birds (Hansell 2000). For example, the hang nests of the Baltimore oriole differ in shape, entrance orientation, and how they are attached to the substrate depending on local twig structure (Hansell and Ruxton 2008), while bowerbirds apparently have few innate building rules, but have to learn from practice and from conspecifics how to build the species-specific bowers that are used to attract mates (Madden 2008). Examples are also known from invertebrates including caddisflies that build differently structured cases depending on locally available material (Williams and Penak 1980) and paper wasps show flexibility in repairing and rebuilding their nests and improves it with practice (Downing 1992). This study focuses on another group of well-known invertebrate ‘architects’; the spiders. Orb spiders in particular are good examples of trap-building animals expected to adapt their traps to their surroundings as experimental evidence from the golden orb web spider, Nephila clavipes, suggests they face a high predation risk when relocating their webs (Vollrath 1985). In addition, orb spiders are well-suited for studies of behavioral flexibility since their webs are in effect records of foraging behavior with a highly structured two-dimensional geometry that allows detailed analysis (Vollrath and Selden 2007). Although spiders construct orb webs by executing a string of fixed behavioral sequences and do not seem to improve web-building with age, experience or size (Mayer 1953; Reed et al. 1970; Witt et al. 1972; Eberhard 2007; Hesselberg 2010; Eberhard 2011), they do nonetheless show behavioral flexibility in a range of natural situations. For instance spiders adapt the size of their webs to match their available reserves of sticky and non-sticky silk (Eberhard 1988) and in windy conditions they reduce mesh height and web size and increase the strength of the structural silk threads to minimize the risk of wind damage to the web (Vollrath et al. 1997; Liao et al. 2009). Equally impressive, however, is their ability to adapt the shape and detailed geometry of their webs to their spatial surroundings while retaining the characteristics of the orb web (i.e. the hub, radii, frame and capture spiral). Araneus diadematus dramatically alters the shape of its web to match vertically or horizontally oblong frames, while simultaneously changing a wide range of parameters including mesh height (Vollrath et al. 1997; Krink and Vollrath 2000). Other members of the orb spider family Araneidae such as Argiope argentata and Telaprocera maudae show a similar degree of behavioral flexibility in response to spatial constraints (Ades 1986; Harmer and Herberstein 2009) and an extreme example is
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found in Leucauge argyra from the family Tetragnatidae, which readily build orb webs in pipes with a span of only 7 % of their normal web size (Barrantes and Eberhard 2012). However, it is currently not known how widespread the ability to adjust webs to available space is in web-building spiders or how species-specific differences in the ability are influenced by the general ecology and habitat of the spiders. Here, I look at the ability of two species of Araneidae from a neotropical forest to build webs in differently shaped frames in the laboratory. I chose two species that readily build webs in the laboratory and differ in their micro-habitat: Webs of Eustala illicita are found within Acacia collinsii trees in close proximity to ant-patrolled branches (Hesselberg and Triana 2010) and Cyclosa caroli primarily spans its web between the understory vegetation (Craig 1989). The aim of the study was twofold. First to test if differences in micro-habitat correlates with differences in behavioral flexibility and second to examine if constrained web contained more errors than normal webs, which could suggest their construction proved more difficult for the spiders. I utilized a wide range of web-parameters, including the majority of those that were shown in previous studies to be of interest such as shape, area utilization and mesh height as well as additional parameters such as the proportion of oversized space and the scatter around the radial angle and length regression both associated with errors and behavioral imprecision (Krink and Vollrath 1999; Hesselberg 2010; Eberhard 2011; Eberhard and Hesselberg 2012).
Methods Spiders I collected late instar females of Eustala illicita (Cambridge 1889) on Acacia collinsii trees in Parque Natural Metropilitano, a dry tropical forest in Panama City, Panama (8°59′ N, 79°32′ E). Late instar females of Cyclosa caroli (Hentz 1850) were collected from the Parque Natural Metropolitano and Cerro Ancon (8°57′ N, 79°32′ E), an urban forest fragment in Panama City, Panama. Care was taken to collect only wellfed (i.e. without a shrunken abdomen) spiders with all legs intact. Voucher specimens of both species were deposited in the Invertebrate Museum at the University of Panamá, Republic of Panama. Field Measurements To compare webs in the field with subsequent laboratory webs of the same individuals, I measured the webs of a subsection of the collected spiders in the field prior to removing the spiders. After spraying the webs with a plant mister to make them more visible, I measured the length of the upper vertical radius (ru), the vertical (dv) and horizontal (dh) capture spiral diameter, and the total length of all anchor threads with a ruler (Fig. 1a). From these measurements I estimated web shape, web asymmetry and the anchor thread – web diameter ratio using equations given below. Finally, I measured the vertical diameter of the hub and free zone (Hv) in order to estimate the capture spiral area from the Ellipse – Hub equation – Acap ¼ ðdv =2Þðdh =2Þp ðHv =2Þ2 p (Herberstein and Tso 2000).
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Fig. 1 Orb-web parameters. a Schematic drawing of a Eustala illicita web. The light grey regions show oversized spaces and the dark grey region shows the free sector. In addition, the vertical height of the hub (Hv), the horizontal (dh) and vertical diameters (dv) of the capture spiral, the upper (ru) and retreat radius (rr) of the capture spiral and a few of the anchor-threads are high-lighted in the drawing. The inserts show the inter-radial angle (θ) and the mesh height (Mh). b The same schematic drawing as in A, but now showing the four web sectors; the upper sector (UP) covered by the angles 315-45°, the compressed sector at the side of the spider’s retreat (RETREAT) between 45° and 135°, the lower sector (DOWN) between 135° and 225° and finally the non-compressed sector opposite the retreat sector (NON-RETREAT) between 225° and 315°
Experimental Conditions Immediately after capture, spiders were brought to the laboratory (23–26°C, 45–60 % rH) and placed individually in standard quadratic Perspex frames stacked like books on a bookshelf separated by Vaseline smeared Perspex sheets. The sizes of the standard frames (30 cm×30 cm×5 cm for E. illicita and 20 cm×20 cm×5 cm for C. caroli) were chosen based on size measurements of webs in the field (see Table 1). Spiders were allowed at least a week to acclimatize to laboratory conditions during which frames were sprayed with water daily and spiders with webs were fed two fruit flies every second day after which the capture spirals of their webs were collapsed by cutting the anchor threads with a soldering iron leaving the silk in the frames for the spiders to recycle (Peakall 1971). Only spiders that built three or more webs during the acclimatization period were used in the experiments. The last web built during the acclimatization period was photographed with a digital Nikon camera in custommade black box with 8 W fluorescent light from the side and 14 W from below after which spiders were given water and two fruit flies before being transferred to an experimental frame. An equal number of spiders of both species were randomly assigned to one of four experimental groups. i) Control group. Spiders in this group were transferred to frames with the same dimensions as the standard frame in which they had built webs during acclimatization. ii) Vertical group. Spiders were transferred to frames with half the width of the standard frame (i.e. 15 cm×30 cm×5 cm for E. illicita and 10 cm× 20 cm×5 cm for C. caroli). iii) Horizontal group. Spiders were transferred to frames with half the height of the standard frame (i.e. 30 cm×15 cm×5 cm for E. illicita and 20 cm×10 cm×5 cm for C. caroli). iv) Small group. Spiders were transferred to frames with half the height and width of the standard frame (i.e. 15 cm×15 cm×5 cm for E. illicita and 10 cm×10 cm×5 cm for C. caroli). Spiders were kept in the experimental frames for three days and inspected and given water on a daily basis. Where a web was built, it was photographed and then cut with a soldering iron as
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Table 1 A comparison between field and laboratory webs of Cyclosa caroli and Eustala illicita Field web
Laboratory web1)
T-test
P
Cyclosa caroli Number of webs
16
16
Mean of web diameter (cm)2)
14.4±1.1
9.9±0.5
3.74
Capture spiral area (cm2)
163±27
77±7
3.14
0.007*
Vertical asymmetry
0.01±0.04
−0.07±0.02
2.47
0.026
−0.09±0.03
−0.03±0.01
−1.81
0.092
4.4±0.3
4.5±0.5
−0.20
0.850
Shape Anchor thread ratio
0.002*
Eustala illicita Number of webs
16
16
Mean web diameter (cm)2)
21.7±1.2
19.4±0.7
2.32
0.035
Capture spiral area (cm2)
362±41
321±23
1.18
0.256
Vertical asymmetry
−0.40±0.06
−0.53±0.03
1.97
0.067
Shape
−0.09±0.03
−0.04±0.02
−1.49
0.158
1.7±0.3
1.6±0.2
0.44
0.675
Anchor thread ratio Mean ± standard error of the mean
* Indicates that there are significant differences after the sequential bonferroni adjustment 1) The pre-experimental webs (see materials and methods) were used as laboratory webs 2) The mean web diameter is the average of the horizontal and vertical diameter of the capture spiral
described above. On day two, spiders that had a web were fed two fruit flies after the web was photographed, but before it was cut. In some cases, spiders built webs that were attached to the separation sheets or in other ways got damaged during handling, so that no photograph could be obtained. These webs were included in the building frequency data, but not in any other analyses. Only the first web built in the experimental frame was analyzed in detail. Web Analysis To look at adaptations to space limitations in different parts of the web, I divided the web into the following four 90° sectors (Fig. 1b). The upper sector of the web (UP). The side of the web in which the signal thread and the retreat was found (RETREAT). In webs without a signal thread where the spider was found in the hub, the side associated with the shortest horizontal radius was designated as the RETREAT sector. The lower sector of the web (DOWN). The side opposite to the Retreat sector (NON-RETREAT). I then analysed the digital photographs using ImageJ (v1.41, National Institute of Health, USA) and extracted the following parameters (Fig. 1a): 1) Vertical (dv) and horizontal diameter (dh) of the capture spiral. 2) Distances from the hub centre to outer capture spiral in the UP sector (upper vertical radius, ru) and to the outer capture spiral in the RETREAT sector (smaller horizontal radius, rr). 3) The area of the capture spiral.
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4) 5) 6) 7)
The vertical diameter (Hv) and the area of the hub and the free zone. The number of radii in total and in each of the four web sectors (R). The length of the entire radius and the inter-radial angle (θ). The number of turns of the capture spiral (N) counted along the central radii in each of the four web sectors. The number of oversized spaces (O). Oversized spaces were defined as spiral sectors where the distance between adjacent spiral turns (i.e. mesh height) was 1.5 times as large as the average of the neighboring inner and outer meshheights along the same radius. The area of the free sector. The combined length of all the anchor threads connecting the web frame to the experimental frame. The second auxiliary spiral turn spacing was measured as the distance between the first and the second full turn of the auxiliary spiral along the central radii in each of the four web sectors. The auxiliary spiral loops were found by connecting the small white dotted remains of the auxiliary spiral in the finished web (Fig. 3; Foelix 1996).
8)
9) 10) 11)
From the measured parameters, I derived the following additional parameters: 1) Vertical asymmetry in the web between the upper and lower part was calculated from (ru – rl)/(ru +rl), where rl is the lower radius found from rl 0dv – ru, while the horizontal asymmetry was calculated from (rr – rn)/(rr +rn), where rn is the radius of the non-retreat side found from rn 0dh – rr. Both equations give a value from −1 to 1, where 0 indicates a perfectly symmetric web. 2) The shape of the web was calculated from (dh – dv)/(dh +dv), which again gives a value from −1 to 1, where 0 indicates a perfectly round web. 3) Mean mesh height in the whole web and in each of the four web sectors was estimated from the mesh height (distance from hub to last spiral turn/(N-1)) along the central radii in each of the four web sectors (Fig. 1a). 4) The oversized space ratio was calculated from O/(N×R) for each of the four sectors. 5) Area utilization was found as the ratio of the capture spiral area to the total area available in the experimental frame. 6) The anchor thread ratio was calculated as the ratio of the total length of all anchor threads to the mean diameter of the capture spiral (i.e. (dv +dh)/2). 7) The scatter around the linear regression line of the radius length and inter-radial angle relationship. A regression line was calculated for each web sector of the combined data from each experimental group for the original webs in the standard frames and the subsequent webs in experimental frames from which the sum of squares of the residuals was found. As the number of radii varies among webs, the sum of squares of the residuals was divided by this number. 8) The relative area of the free sector was found as the ratio of the free sector to total capture area. Statistics The two tailed t-test for matched samples were used to compare web-parameters between field webs of collected spiders and their subsequent webs built in the
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laboratory. A two-way ANOVA was used to compare web-building frequency between the two species. Homogeneity tests were performed and, if necessary to ensure equal variances, the data was arcsin transformed. To compare E. illicita webs in experimental frames across experimental groups, I first compared the response (experimental web – standard web) across the experimental groups with a one-way ANOVA or, in cases where the web sector was included as an additional parameter, a three-way mixed design ANOVA was used to compare the repeated measures web sectors and web type (both within-subject factors) across experimental groups (between-subject factor). In situations when the Mauchly’s Test showed that the assumption of sphericity was violated, I used the Greenhouse-Geisser correction. For post-hoc tests, I either tested for pair-wise differences within each experimental group with a two-tailed t-test for matched samples between web type and web sector or applied a Tukey Post-hoc test for experimental group. Finally, I compared the slope of the regression lines of the inter-radial angle vs. length relationship in the standard and experimental web following Zar (1996). All statistical tests were performed with PASW (Version 18.0, SPSS Inc, 2009) with an initial significance level of 5 %. However, since multiple statistical tests were performed on the same data-sets, a separate sequential Bonferroni adjustment was made on each data-set to minimise type I errors (Rice 1989).
Results The sizes of the standard frames were based on a preliminary survey of webs in the field. However, I also conducted a detailed comparison between field and laboratory webs for the two species (Table 1), since a recent study on a temperate orb spider found significant differences between webs from the field and the laboratory for a range of parameters (Sensenig et al. 2010). E. illicta webs showed only minor differences as expected from a previous study (Hesselberg and Triana 2010) (Table 1). In contrast, C. caroli webs from the laboratory had significantly smaller diameters and less overall capture spiral areas than webs from the field, although other parameters remained similar (Table 1). Web-Building Performance Out of 45 E. illicita females, 40 adapted successfully to the laboratory conditions and were included in the experiments, whereas this was only the case for 23 out of 53C. caroli females. The remaining spiders died, molted, laid eggs or built webs too infrequently. The numbers of E. illicita spiders that built at least one web during the 3-day experimental period out of the total assigned to each group were 9/11 in the Control group, 8/9 in the Horizontal group, 10/10 in the Vertical group and 10/10 in the Small group. The similar numbers for C. caroli were 5/5 in the Control group, 1/5 in the Horizontal group, 3/7 in the Vertical group and 1/6 in the Small group. Both species had a similar web-building frequency (i.e. the number of webs built during the 3-day experimental period out of the total maximum number of webs) in the Control group of 60–70 %, but there was a significant difference in how the two species responded to the experimental frames (Fig. 2; Two-way ANOVA: F1,63 026.3,
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Fig. 2 The mean web-building frequency during the first 3 days after the spiders were transferred to experimental frames (see methods and materials for a description of the frames). The black bars show building frequencies of Eustala illicita and the grey bars of Cyclosa caroli. The error bars represent the standard errors of the means
P00.00004). E. illicita had a constant web-building frequency across all experimental groups (One-way ANOVA: F3,39 00.1, P00.94), while C. caroli had a significantly lower web-building frequency in the Horizontal, Vertical and Small groups than in the Control group (One-way ANOVA: F3,22 06.5, P00.003). A Tukey post hoc test revealed that the three former groups, with a web-building frequency of around 7 % – 19 %, were not statistical different from each other (Fig. 2). It was obvious from a visual inspection that the majority of E. illicita spiders matched the shape of their webs to the experimental frames (Fig. 3), whereas the few C. caroli webs in experimental frames appeared not to match the shape of the frame as well as E. illicita webs (Fig. 4). Spatially Constrained E. illicita Webs The responses in overall web parameters to the experimental frames are shown in Fig. 5. No significant differences between webs in standard frames and subsequent webs in experimental frames were found in either horizontal or vertical asymmetry
Fig. 3 Photograph of webs of Eustala illicita in experimental frames. The black spiral shows the auxiliary spiral drawn by connecting the white remains of silk, from when the spider cut the auxiliary spiral, present on the radii in the finished web. The white bars in the lower right corner represent a length of 5 cm. a Control frame. b Vertical frame. c Horizontal frame. d Small frame. e The dimensions of the frames in cm
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Fig. 4 Photograph of webs of Cyclosa caroli in experimental frames. The white bars in the lower right corner represent a length of 5 cm. a. Control frame. b. Vertical frame. c. Horizontal frame. Note that this web shows damage in the lower half. d. Small frame. e. The dimensions of the frames in cm
(Fig. 5a, b, Table 2). The shape of the webs, however, changed dramatically in both the horizontal and the vertical frames to match frame shape (Figs. 3 and 5c, Table 2). There were no significant changes in the area of the free sector relative to the total capture spiral area (Fig. 5d, Table 2), but the relative size of the free sector decreased in all frames, especially in the Small group. This was caused primarily by an increase in webs without a free sector from 1/10 webs in the standard frames to 4/10 in the experimental Small frames. The similar values for the other experimental groups were 1/6 to 2/6 for the Control group, 2/9 and 2/9 for the Vertical group and finally 0/8 and 0/8 for the Horizontal group. Spiders used the same proportion of the available space in the two elongated frames as they used in the standard frames, and used an even higher proportion of the available space in the Small group (Fig. 5e, Table 2). Finally, no changes to the ratio of the combined length of all anchor threads to the mean capture spiral diameter were found, although a slight decrease was detected for webs in Horizontal and Small frames (Fig. 5f, Table 2).
Fig. 5 Differences in web parameters between webs built by Eustala illicita in standard (dark grey) and experimental frames (light grey) for the four experimental groups. a Vertical asymmetry of the web. b Horizontal asymmetry of the web. c Shape of the web. d The area of the free sector relative to capture spiral area. e. The percentage of available area in the frame taken up by the capture spiral. f. The ratio of the length of all anchor threads to the mean diameter of the web. The error bars indicate the standard errors of the means. The star (*) indicates that there were significant statistical differences after the sequential Bonferroni adjustment. Sample size and statistical test results can be found in Table 2
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Table 2 Response of transfer to experimental frames in general web parameters for Eustala illicita N
Response1)
Statistics2)
Control
6
−0.012±0.046
T00.26
0.807
Vertical
9
−0.040±0.085
T00.47
0.653
Horizontal
8
0.020±0.050
T0−0.40
0.703
Small
10
0.087±0.051
T01.70
0.122
F00.84
0.490 0.094
p
Vertical asymmetry
Across
3)
Horizontal asymmetry Control
5
0.092±0.420
T0−2.19
Vertical
9
−0.463±0.057
T00.81
0.440
Horizontal
8
0.009±0.030
T0−0.28
0.785
Small
7
−0.154±0.089
Across
3)
T01.73
0.135
F02.50
0.083
Shape Control
6
−0.015±0.033
T00.46
0.663
Vertical
9
−0.213±0.027
T08.03
