Ethology 110, 397—411 (2004) 2004 Blackwell Verlag, Berlin ISSN 0179–1613
Difference in Web Construction Behavior at Newly Occupied Web Sites Between Two Cyclosa Species Kensuke Nakata* & Atushi Ushimaru *Tokyo Keizai University, Minamimachi 1-7-34, Kokubunji, Tokyo; Center for Ecological Research, Kyoto University, Kamitanakami Hiranocho, Otsu, Shiga, Japan Abstract Animals make decisions based on subjective assessments of their environment. To determine their future foraging activities, animals probably assess food availability from past foraging experiences. Thus, foraging also functions as a way for animals to collect information, with the uncertainty of an assessment decreasing as foraging activity increases. This suggests that different needs for a correct assessment may affect the investment made in foraging activities. Orb-web spiders sometimes relocate their webs and relocation rate differs among species. After web relocation, several spider species have been reported to construct the first webs at newly occupied web sites using less silk than usual, possibly to avoid the risk of an overinvestment at sites where food availability has not been determined. Nevertheless, they may pay a cost, because of inadequate decisionmaking, if webs constructed with less silk convey less information and increase the uncertainty of an assessment. We expect that stronger site tenacity necessitates a greater requirement for correct assessment of web site and the degree to which spiders reduce the amount of web silk in the first web after web relocation is smaller in species that use the same site longer. To test this hypothesis, we examined web construction in two orb-web spiders, Cyclosa octotuberculata and C. argenteoalba. At the same time we found that these two species exhibit different web-site tenacity, as C. octotuberculata does not relocate its webs as frequently as does C. argenteoalba. After artificially induced web relocation, C. argenteoalba constructed webs that were initially smaller and contained only about 2/3 of the silk in control webs that were constructed at the original site. In contrast, C. octotuberculata did not exhibit such decreases in web size or in the amount of web silk used. This result is consistent with our hypothesis. Corresponding author: Kensuke Nakata, Tokyo Keizai University, Minamimachi 1-7-34, Kokubunji, Tokyo, 185-8502, Japan. E-mail:
[email protected]
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Introduction Animals live in heterogeneous environments where ecological characteristics vary among sites. Most species adjust their behavior to the site that they are currently using, and decisions are based on subjective assessments of the site made by each individual (Giraldeau 1997). During foraging, animals invest both time and energy to obtain food. To adjust their investment in foraging activity, they must assess the food availability (Stephens & Krebs 1986) and the risk of predation (Lima & Dill 1990) at the foraging site. For each individual, the most direct and reliable information regarding food availability likely comes from its past foraging experience. The effects of foraging experience on subsequent decision-making have been demonstrated in both vertebrate (e.g. Nishimura 1988; Bowers & Adams-Manson 1993) and invertebrate foragers (e.g. Dukas & Real 1993). Thus, foraging functions not only as an activity to obtain food, but also as a way to sample food availability for future decision-making. Because the information obtained from foraging is subject to stochastic errors, an assessment of food availability carries an element of uncertainty, which may cause animals to make inappropriate decisions. However, uncertainty will decrease with increased foraging, or sampling intensity. This suggests that different needs for appropriate decision-making may affect animalsÕ investment in foraging activities. Orb-web spiders are ideal subjects with which to examine this hypothesis for the following four reasons: (1) Orb webs are used to capture prey, and the foraging investment of each spider is easily estimated as the total length of silk in each web. (2) The shape and size of a web are a direct result of decisions made by each spider (Vollrath 1992). Most spiders renew their webs daily, during which time they adjust the web size, shape, spiral density, and the amount of silk invested. The daily web construction activities are based on the spidersÕ foraging experience (Herberstein et al. 1998; Venner et al. 2000) and other factors, such as reproductive state (Sherman 1994), available space (Krink & Vollrath 2000), or prey type (Sandoval 1994; Schneider & Vollrath 1998). (3) Spiders have to pay the cost of foraging (i.e. the cost of web construction) before obtaining any food. This is different from mobile forager, such as a bird. Mobile foragers update their knowledge about food availability at the current site during a foraging bout. Their foraging investments are often measured through the Ôgiving-upÕ time, and are affected by both prior experience and the ongoing foraging process (e.g. Iwasa et al. 1981). This requires the controlling of foraging events, during a foraging bout in an experiment using mobile foragers, which is not always essential for experiments using sedentary foragers. (4) Orb-web spiders are not completely sedentary, and sometimes change the site of their web. Occurrence of web relocation is affected by numerous variables including prey availability (Vollrath 1985; Nakata & Ushimaru 1999; Chmiel et al. 2000), web destruction (Hodge 1987; Chmiel et al. 2000), conspecific interactions (Smallwood 1993), risk-averse responses to prey-rich habitats (Gillespie & Caraco 1987), and environmental changes such as increased temperature or humidity (Cherrett 1964). Average residence time at one web site differs between species and ranges from a few days
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to more than 10 d (Shelly 1984; Hodge 1987; Smallwood 1993; Nakata & Ushimaru 1999). Interspecific variation in web-site tenacity among species may result in differences in the needs of a correct habitat assessment. A correct assessment of the current site will lead to an appropriate decision about how much spiders should invest into foraging per web constructed in the future. The appropriate decision will enhance the spider’s foraging efficiency, and will be more beneficial if a spider uses the same site repeatedly for long time. Therefore, correct assessment is considered more important for spiders that exhibit strong site tenacity than for spiders that change web sites frequently. Because spiders obtain information about their environment from vibrations transmitted through web silk (Suter 1978), spider species with strong site tenacity may invest more into web construction than species that frequently changes web site. However, because the size and shape of spider webs are species-specific, we could not compare webs directly between species to address this. Instead, we focused on the decrease in the amount of web silk used in a new web after relocation to a different site, a result found in our previous study (Nakata & Ushimaru 1999). In Cyclosa argenteoalba, we found that following relocation to a new site the amount of silk used in the construction of the first web was smaller than the amount used to build a second web. Similar observations have been made in Araneus diadematus (Zschokke & Vollrath 2000). During web relocation, spiders generally search randomly for new sites (Riechert & Gillespie 1986), and settle in sites that they have not previously occupied. They have to construct a web with no previous foraging experience at the new site, and constructing the first web with less silk may reduce the risk of over-investment at sites where food availability is unknown (Vollrath 1992). Nevertheless, costs associates with inadequate decision-making may arise, if the webs constructed with less silk convey less information. Spider species with strong site tenacity may suffer from inadequate decision-making for longer than do spiders that relocate their webs frequently. The purpose of this study is to test a hypothesis that the degree to which spiders reduce the amount of silk in the first web after relocation is smaller in the species that relocate their web less frequently. Subject species are Cyclosa octotuberculata and C. argenteoalba. We examined natural web relocation frequencies in both sympatric species. We induced web relocation in both species experimentally, and measured several parameters of their webs. Then, we compared the effects of web relocation on investment in subsequent web construction for the two species. We discuss the results with respect to the difference in the web relocation frequency of the two species. Methods C. argenteoalba and C. octotuberculata are common species in Japan. They are often sympatric, and the size ranges of their prey overlap (Miyashita 1997). Both are diurnal species that construct vertical orb webs at sunrise and consume sticky spirals and most of the radial threads during the following night. Normally,
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web renewal occurs daily. Both species decorate their webs with debris, including the remnants of prey and exoskeletons after molting, but the manner of decoration differs. Cyclosa octotuberculata hangs a thread of debris vertically from the top to the bottom of the web through the hub. The spider sits on the debris, where it is camouflaged and inconspicuous to the human eye. The thread of debris does not seem to affect foraging success of the web owner (Baba 2003). In the reproductive season, female spiders hang their egg sacs along the thread of debris. In contrast, C. argenteoalba hangs a cluster of debris in the lower half of its web, and sits on the hub, away from the debris, where it is easily seen. Females do not hang egg sacs on their web, but lay eggs on nearby vegetation. The two species also differ in their treatment of debris when webs are relocated. Cyclosa octotuberculata moves the debris to the new site, whereas C. argenteoalba abandons it. The study site was located in a bamboo forest in Kyo-Tanabe, Japan (3448¢N, 13545¢E), where C. argenteoalba and C. octotuberculata coexist, although the former is more abundant than the latter. Experiments were conducted in late Jul. 2000, when adult C. argenteoalba females were found. At this time, however, most C. octotuberculata were juveniles. Therefore, we conducted an additional experiment with adult C. octotuberculata females to test the effect of developmental stage (i.e. juvenile vs. adult) in late Jun. 2001 at Mt. Inasa, Nagasaki, Japan (3244¢N, 12951¢E). For adult C. octotuberculata, we marked spiders individually on the gaster with different dot pattern using red paints. We did not mark C. argenteoalba and juvenile C. octotuberculata. We examined the web site tenacity of 30 C. argenteoalba, 51 juvenile C. octotuberculata and 26 adult C. octotuberculata over the course of 2 d. We marked the locations of webs by recording the attachment points of the frame threads, and then on the following day we examined whether the webs had been relocated. When the frame threads of an inhabited web remained attached to the same points as on the previous day, we considered web relocation not to have occurred. We regarded all other cases as web relocations, including the case when spiders changed only one attachment point. This was because in Kyo-Tanabe, the frame thread length of C. argenteoalba webs constructed between bamboos was often 3–4 m, and the location of the hub sometimes shifted more than 50 cm when a single attachment point was changed (pers. obs.) Apart from measuring web relocation rate, we also conducted a web relocation experiment spanning 3 d. On the first day, in Kyo-Tanabe, we established manipulation and control areas for both adult C. argenteoalba and juvenile C. octotuberculata, and marked the locations of all webs in both areas. Nineteen C. argenteoalba and 24 C. octotuberculata were found in the manipulation area, and 26 C. argenteoalba and 22 C. octotuberculata were found in the control area. In the manipulation area, we cut one or two frame threads of all the webs to induce web relocation. Care was taken to ensure that the silk of collapsed webs remained on the intact frame threads so that the spiders could consume the web by the next day. On the day following web destruction, we found that 19 C. argenteoalba and 13 C. octotuberculata in the manipulation area had constructed
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webs at new sites where webs had not been observed on the previous day. We used these spiders as manipulated groups to test the effect of web relocation following web construction. In the manipulation area, no spiders constructed their webs at the same site on the day after manipulation. In the control area, 20 C. argenteoalba and 16 C. octotuberculata spun new webs at the same sites as on the previous day. At Mt. Inasa, we assigned 12 adult C. octotuberculata to a manipulated group and 14 individuals to a control group. We marked the locations of all webs and cut the frame threads of webs in the manipulated group on the first day. The next day, 11 individuals from the manipulated group had moved their webs to different sites. In the control group, 13 individuals constructed their webs at the same site as on the previous day. One spider in each group disappeared from the study area. In both experiments, we measured web parameters on the second and third days, i.e. we measured the first and the second webs at the newly occupied web site (hereafter, we refer to these as the first and the second webs). Spiders that changed their web sites on the third day were excluded from the analysis. Consequently, we obtained data from 13 manipulated and 16 control spiders for C. argenteoalba, 12 manipulated and 15 controls for juvenile C. octotuberculata, and 11 manipulated and 13 controls for adult C. octotuberculata. It is believed that available space for web construction limits spider population (Rypstra 1983). If this was also the case in Cyclosa, manipulated spiders might not be able to find an appropriate new space for a web of the usual size, and might construct smaller webs instead. Then, web size would be kept small for consecutive web constructions at the same site. The measurement for the second webs was conducted to examine this possibility. We used total thread length (TTL) to estimate the level of investment in web construction. To calculate these values, we measured seven web parameters: the vertical and horizontal diameters of the outermost and innermost sticky spiral loop, the number of sticky spirals in the vertical and horizontal directions, and the number of radials (RA). We averaged the diameter of the outermost (Dout) and innermost (Din) spirals and the number of spirals (SP) across the vertical and horizontal directions. Calculation was done using formulas below: TTL ¼ p
Dout þ Din SP Dout þ RA 2 2 2
The TTL is the sum of capture threads and radial thread length. The formula to calculate capture thread length was adopted from Venner et al. (2001). Radial thread length was calculated as the number of radials multiplied by the average radius. The TTL is a function of web size and density of sticky spirals. Spiders may decrease TTL by constructing a web of smaller size, placing sticky spirals more sparsely, or both. When the decrease in TTL is only because of sparser spirals, it might be interpreted that spiders adjusts their webs to change target prey type (Sandoval 1994; Schneider & Vollrath 1998) and not to avoid the risk of an over-
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investment. To examine this possibility, we also calculated catching area (CA) and spiral density (SD) using formulas:
CA ¼ p
SD ¼
D2out D2in 4
SP 2 Dout Din
Catching area was calculated using the Ellipse-Hub formula of Herberstein & Tso (2000). Analysis
We calculated the correlation coefficients among three web parameters (TTL, CA, and SD). We used Bonferroni’s correction to test statistical significance, as three coefficients (TTL–CA, TTL–SD and CA–SD) were examined simultaneously. Next, we compared the effect of manipulation on TTL between adult and juvenile C. octotuberculata. We conducted a three-way repeated-measures anova with age (juvenile vs. adult) and treatment (control vs. manipulated) as betweensubjects factors and web-day (the first vs. the second webs) as a within-subjects factor. We also tested the effect of manipulation between adult C. argenteoalba and adult C. octotuberculata in similar way, in which we used species instead of age as a between-subjects factor. When significant species (or age) · treatment · web-day interaction was detected, we conducted post hoc comparison between control and manipulated groups for each species (or age) and web day by t-test with a Bonferroni’s correction. As we made four comparisons simultaneously, we multiplied the p-value from each t-test by four to examine statistical significance. We also tested the effect of manipulation on CA and SD between adult C. argenteoalba and adult C. octotuberculata using three-way repeatedmeasures anova and the t-test with a Bonferroni’s correction in a similar way. All data were log-transformed before each test. Results The results of our web-site tenacity investigation showed that C. argenteoalbaÕs daily web relocation rate was significantly higher than juvenile C. octotuberculata (p ¼ 0.037, Fisher’s exact probability test) (Table 1). It was also higher than adult C. octotuberculata (Table 1), and the difference between C. argenteoalba and adult C. octotuberculata was marginally significant (p ¼ 0.0564, Fisher’s exact probability test). The correlation coefficients between TTL and CA were significant for all combinations of species (and age), treatment and web-day. By contrast, only one correlation coefficient between SD and TTL or CA was significant (Table 2).
Abandon
Moves to new web site
6–7
10–14
Species
C. argenteoalba
C. octotuberculata Adult
0.059 (3/51)
0.038 (1/26)
0.233 (7/30)
Web relocation rate (per day)
c
m
c
m
c
m
Treatment
1964.3 (640.5) 1837.2 (630.0) 387.0 (112.9) 347.8 (89.8)
2073.0 (569.7) 3285.1 (557.9)
TTL (cm)
First webs
459.4 (152.0) 422.2 (148.0) 30.5 (13.4) 30.0 (8.1)
190.8 (54.1) 271.6 (60.4)
CA (cm2)
3.06 (0.30) 3.16 (0.65) 9.65 (2.67) 8.21 (2.06)
8.31 (1.23) 9.61 (1.88)
SD
2064.8 (750.2) 2006.3 (453.9) 432.8 (149.5) 318.7 (84.6)
3230.1 (650.6) 3571.0 (811.1)
TTL (cm)
Second webs
466.0 (185.9) 467.7 (147.5) 35.3 (16.0) 26.9 (6.5)
248.3 (53.7) 299.2 (75.9)
CA (cm2)
In first and second webs columns, average web parameters were indicated with SD (standard deviation) in parenthesis. m, manipulation group; c, control group; TTL, total thread length; CA, catching area; SD, spiral density.
Juvenile
Treatment of debris thread at web relocation
Size range of adult female (mm)
3.18 (0.40) 3.18 (0.73) 9.11 (2.00) 8.23 (1.65)
10.00 (1.17) 9.26 (1.37)
SD
Table 1: Difference in web relocation behaviors and results of experiment between two Cyclosa spiders. Numerals in parenthesis in web relocation rate column indicate the number of relocating spiders/the number of spiders examined
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Table 2: Correlation coefficients among web parameters Correlation coefficients Species C. argenteoalba First webs Second webs
TTL– Treatment df CA p m c m c
C. octotuberculata Adult First webs m c Second webs m c Juvenile First webs m c Second webs m c
TTL– SD p
CA– SD
p
11 14 11 14
0.86 0.59 0.91 0.87
0.999
9 11 9 11
0.97 0.85 0.97 0.73
0.999 )0.13 >0.999 0.17 >0.999 )0.50 0.246
10 13 10 13
0.74 0.67 0.92 0.80
0.019* 0.04 >0.999 )0.64 0.074 0.018* 0.56 0.088 )0.23 >0.999 0.999 )0.60 0.122 0.999
Significant at *5 and ***0.1% level. p-values are after Bonferroni’s correction (i.e. multiplying raw p-values by three). m, manipulation group; c, control group; TTL, total thread length; CA, catching area; SD, spiral density.
While average TTL of adult C. octotuberculata is about five times longer than that of juvenile (Table 1), three-way repeated-measures anova did not revealed any effect of manipulation, web-day, and interaction terms on TTLs of juvenile and adult C. octotuberculata (Table 3). On the contrary, significant species · treatment · web-day interaction was detected in anova of TTLs of the first and the second web for adult C. argenteoalba and C. octotuberculata (Table 4; Fig. 1). Experimental manipulation affects TTL of the C. argenteoalbaÕs first web: in C. argenteoalba, mean TTL of the first web in the manipulated group was about 2/3 that of the control group, and the difference was statistically significant (t ¼ )5.801, Bonferroni-corrected p < 0.001, df ¼ 27), (p-values for all t-tests hereafter are indicated as Bonferroni-corrected p) while no significant difference was detected in C. octotuberculata (t ¼ )0.517, p > 0.999, df ¼ 22). For the second web, there was no significant difference between manipulated and control groups in both species (C. argenteoalba, t ¼ )1.076, p > 0.999, df ¼ 27; C. octotuberculata, t ¼ 0.049, p > 0.999, df ¼ 22). For manipulated groups in both species, variance in TTL was larger for the second webs than the first webs (Table 1), but difference was not statistically significant (F ¼ 0.767 and 0.729, p ¼ 0.653 and 0.626, for C. argenteoalba and C. octotuberculata, respectively). The three-way anovas of the CA and SD also revealed significant species · treatment · web-day
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Table 3: anova table for comparisons of total thread length between adult and juvenile Cyclosa octoruberculata Source Between-subjects Age Treatment Age · treatment Individual ⁄ age · treatment Within-subjects Web-day Web-day · age Web-day · treatment Web-day · age · treatment Residual Total
Partial SS
df
MS
F
p
69.725 0.335 0.150 8.299
1 1 1 47
69.725 0.335 0.150 0.177
394.88 1.90 0.85
