The complexity of site quality: multiple factors affect web tenure in an orb-web spider

Animal Behaviour 79 (2010) 1147e1155

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The complexity of site quality: multiple factors affect web tenure in an orb-web spider Clare C. Rittschof a, *, Kelly V. Ruggles b,1 a b

Department of Biology, University of Florida Institute of Human Nutrition, Columbia University

a r t i c l e i n f o Article history: Received 23 August 2009 Initial acceptance 3 December 2009 Final acceptance 2 February 2010 Available online 19 March 2010 MS. number: A09-00552R Keywords: context-dependent decision foraging decision habitat selection kleptoparasite male harassment multimodal signalling Nephila clavipes

Behavioural decisions involving foraging, mate choice and habitat selection are complex and difficult to evaluate experimentally. Web abandonment by orb spiders is a complex decision that is experimentally tractable. For females of the golden orb spider, Nephila clavipes, the web is a microhabitat that serves as a prey capture device, a mating site and a habitat for parasites. Thus, the web embodies the complexity of a bird territory or mammal home range, but is spatially compact and amenable to experimental manipulation. We used both field census data and field experimental manipulations to address the importance of prey capture rate, kleptoparasite load and male presence for web tenure (the time spent at a web site) in both mature and immature female N. clavipes. No factor explained variation in web tenure for immature females, although census data suggested that increased kleptoparasite load decreased web tenure. For mature females, increased male presence decreased web tenure, while increased prey capture rate, condition and body size all increased web tenure. Web tenure also decreased over the course of the season. Females integrate multiple cues to make web movement decisions. One of these cues is male presence, which detracts from the quality of a web site, suggesting that mate harassment might affect females' web movement decisions. Insight into this seemingly simple behaviour contributes to a growing understanding of how and when animals integrate multiple cues into behavioural decisions. Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

A behavioural decision is defined as the moment an animal unequivocally commits future time to a course of action (Brockmann et al. 1979). This course of action can affect the survival and ultimately the fitness of the individual. Complex decisions are those in which animals simultaneously evaluate the costs and benefits of multiple factors during the decision-making process. As a result, complex decisions are commonly plastic and context dependent. For example, combinations of visual, auditory, olfactory and acoustic cues allow females to assess male traits in a hierarchical manner and choose mates based on the features most relevant to the present environment (Bateson 1983; Dale & Slagsvold 1996; Qvarnstrom 2001; Candolin 2003). Foraging decisions too are complex because animals must respond to the profitability of a foraging site, the competition for the site and the presence of predators (Milinski & Heller 1978; Brown 1988; Stephens et al. 2007). Complex behavioural decisions can be difficult to assess using an experimental approach. One such case is habitat selection,

* Correspondence: C. C. Rittschof, Department of Biology, University of Florida, 220 Bartram Hall, P.O. Box 118525, Gainesville, FL 32611-8525, U.S.A. E-mail address: critter@ufl.edu (C.C. Rittschof). 1 K. V. Ruggles is at the Institute of Human Nutrition, Columbia University, 630 West 168th Street, Presbyterian Hospital, 15th Floor East, Suite 1512, New York, NY 10032, U.S.A.

where quantifying the factors that influence habitat choice is difficult because animal home ranges are relatively large and heterogeneous, focal species interact with multiple predators and competitors, and the density of conspecifics can be highly variable. As a result, most authors address decision complexity associated with habitat selection through correlational studies (e.g. Eterovick & Ferreira 2008; Pipia et al. 2008; Barri et al. 2009; Godvik et al. 2009). While these studies suggest factors of large effect, correlational studies do not provide a direct test of the importance of one or a combination of factors in habitat selection; experimental studies are needed to test these factors. In this study we use an experimental approach to examine the criteria for web site abandonment in the orb-web spider Nephila clavipes. Spiders' web relocation decisions provide an opportunity to experimentally address complex site movement decisions on a manageable spatial scale. For the golden orb-web spider, Nephila clavipes, the web is a complex microhabitat that serves as a prey capture device, a mating site and a habitat for competitors, predators and kleptoparasites. Females periodically change web sites throughout their lifetimes, and web tenure is highly variable, ranging from 1 day to many weeks. However, the cues females use to decide to leave a web site remain unclear (Rypstra 1981; Vollrath 1985; Vollrath & Houston 1986).

0003-3472/$38.00 Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2010.02.014

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Many factors could contribute to N. clavipes web site quality. Adequate temperature and solar radiation are important for juvenile growth and egg maturation in adult spiders (Li & Jackson 1996), and spiders avoid web sites at temperature extremes (Barghusen et al. 1997). Vegetation for structural support influences web site selection (Lubin et al. 1993; McNett & Rypstra 2000), and web destruction by wind or debris may cause relocation (Leclerc 1991; Chmiel et al. 2000). In addition to abiotic factors, predation risk may motivate site selection or abandonment (Hodge & Uetz 1992). Although it is likely that multiple factors affect site movement decisions in N. clavipes, studies of web movement have focused on prey capture rate as the most important influence on web tenure (e.g. Vollrath 1985; Vollrath & Houston 1986). These studies have found mixed support for the idea that female web tenure is positively correlated with prey capture rate. Vollrath (1985) found that females housed together in large artificial enclosures and provided with large amounts of food did not change webs, while females in low-food enclosures changed webs at least once during the study period. In contrast, Vollrath & Houston (1986) found no relationship between prey availability and web movement for females housed individually in containers where they were free to move and to construct new webs. Given these mixed results and the importance of prey capture for site movement decisions in other species (e.g. Uetz 1992), prey capture rate is one factor that needs to be considered in studies of web tenure. Another factor that generally influences habitat quality is the cost imposed by parasites and competitors (Tilman 1994; Poulin 1995; Thomas et al. 2005). Unusual among orb-web spiders, N. clavipes webs are almost always occupied by kleptoparasites. These kleptoparasites are small spiders in the genus Argyrodes that steal prey items from the web, thus lowering the resident's prey consumption rate. Although several studies have suggested a role for kleptoparasites in web movement in Nephila species (Robinson & Olazarri 1971; Robinson & Robinson 1973, 1976; Vollrath 1979), in N. clavipes, one study (Rypstra 1981) investigated the correlation between kleptoparasite load and female web movement decisions in a tropical population. With observational data, Rypstra (1981) found a negative correlation between the number of prey items consumed by the web owner and web relocation within the first 48 h of site residence. Rypstra's (1981) study showed that kleptoparasite presence is correlated with web movement behaviour in a short-term context, and thus kleptoparasites may also influence web movement after long-term web site residence that is more characteristic of N. clavipes. In addition, experimental studies that demonstrate a relationship between a kleptoparasite-mediated change in feeding rate and web tenure are needed to corroborate Rypstra's (1981) correlational study. In addition to kleptoparasitic spiders, adult male N. clavipes cohabit on both juvenile and adult female webs. These males fight with one another, court adult females for copulations, and sometimes feed off prey carcasses that a female is consuming (Christenson & Goist 1979). Males do not, however, scavenge prey items on the web. Even though males can occur on female webs in numbers as high as 16 (C. C. Rittschof, unpublished data), and they can stay on webs for weeks at a time (Cohn et al. 1988), no study has addressed the role of male presence in N. clavipes web movement decisions. Male presence could have a positive or negative effect on the timing of female web movement. The presence of multiple males on the web could entice a female to stay at the web site longer because it provides her the opportunity for mate choice. In many animal systems, females have developed pre- and postcopulatory mechanisms to find and select among multiple potential mates, and these choices affect female reproductive success (reviewed in Andersson & Simmons 2006). Precopulatory female choice has

been shown in other spider systems (e.g. Koh et al. 2009; Stoltz et al. 2009), raising the possibility that, in N. clavipes, females change web sites to increase their ability to attract males. Access to more than one male is especially important if females mate multiply to achieve maximal reproductive success. For example, if males vary in quality or degree of genetic compatibility with females, or if the environment is heterogeneous and multiple mating is necessary to produce a variety of offspring phenotypes, multiply mated females outperform singly mated females in terms of offspring survival and fitness (Zeh & Zeh 2001). If this is the case, female behaviour should optimize interactions with potential male mates (Arnqvist & Nilsson 2000). In contrast, interactions with males can carry costs because males harass females for copulations, attract predators and carry diseases (Daly 1978; Arnqvist 1989, 1992; Fowler & Partridge 1989; Sih et al. 1990; Arnqvist & Rowe 1995; Clutton-Brock & Parker 1995; Watson et al. 1998; Knell & Webberley 2004). For N. clavipes females, males could impose an energetic cost for both juvenile and adult females because males are known to feed alongside females. In addition, males might impose a harassment cost for adult females because males attempt to copulate with adult females while the female eats (Christenson et al. 1985). In this study, we addressed three factors that could affect web movement decisions in N. clavipes: prey capture rate, kleptoparasite load and male presence. We used two approaches for both immature and mature females; field censuses of natural populations and field experimental manipulations. This study is the first to address both the role of male presence and the use of multiple cues in site movement decisions of female orb-web spiders. Our findings may provide insight in other systems where habitats and home ranges are larger and less experimentally tractable. In addition, insight into the potential complexity of this seemingly simple decision contributes to a growing understanding of how and when animals integrate multiple cues into behavioural decisions. METHODS Nephila clavipes Web-building Behaviour Nephila clavipes females capture prey and mate during the day and night, but they travel between web sites only at night (Vollrath & Houston 1986). Once a site is found, the female builds a new web within hours. Nephila clavipes webs are semipermanent structures; although females repair their prey capture orb periodically (Higgins 1987), they do not regularly deconstruct and rebuild their webs like some other orb-web spiders (e.g. Adams 2000). Because of extended web tenure, in some populations, females are found in stable aggregations (Hodge & Uetz 1992). In our study population, very young juvenile spiders can be found in clusters with overlapping webs and shared anchor lines. However, as spiders become larger, they move away from each other. Groups of aggregated adult females are uncommon; spiders in close proximity occasionally take over each other's webs, displacing or cannibalizing the web owner (C. C. Rittschof, personal observation). Study Sites Census data were collected during summer 2007 on a private ranch in Jonesville, Florida, U.S.A. (29
390 1400 N, 82
3102300 W) 20 km west of Gainesville, Alachua County. The study area was a 400 m2 plot of oak forest with palmetto understory that was surrounded by forest on two sides, a hay field on one side and an open cow pasture on the other. This site was chosen because there is a high density of N. clavipes, and web movements were confined to the woodland, which allowed us to easily relocate females that

C.C. Rittschof, K.V. Ruggles / Animal Behaviour 79 (2010) 1147e1155

had moved. The manipulative experiments were conducted during summer 2008 at the Ordway-Swisher Biological Station in Melrose, Florida (Putnam County, 29
420 3200 N, 82
30 W) 30.7 km east of Gainesville. Nephila clavipes were found in mixed oak and pine forest habitats within the 3683 ha preserve. Census Data Collection Data were collected every 2 days between 0800 and 1200 hours from 26 June until 3 October 2007. Females included in the study had a minimum cephalothorax width of 1.4 mm (measured at the widest point using fibreglass dial callipers) and occupied a web no more than 2.5 m above the ground. Every female that met these criteria was numbered and uniquely marked on the abdomen with enamel paint (TestorsÒ, Rockford, IL, U.S.A.). All males present on the web were also given unique paint marks. Webs were marked with flagging tape where the anchor line met a branch. The first data entry for each female included her body size (cephalothorax width in mm at the widest point), reproductive state (whether the female was adult or juvenile), the number of legs the female was missing, the size of her web (maximal horizontal diameter of the prey capture orb), the number of prey carcasses present and the number of kleptoparasites in the web, the size of each male present and whether the males were missing legs, and web condition. Web condition was ranked as good if the web had an intact and wellmaintained prey capture surface, fair if the web had a full prey capture surface with holes or missing strands, and poor if the web was reduced with little or no prey capture surface. Each day of data collection, we recorded female leg number and the identity, size and leg number of each male present, as well as the number of prey carcasses and kleptoparasites, and the condition of the web. Prey carcasses were counted each day they were present because females occasionally feed off large carcasses for more than one day, but do not store remnants or other debris in the web. This method allowed us to account for the size of prey items in the analysis of prey capture rate (larger prey items were present longer and recorded more than once). However, larger prey items (e.g. cicadas, beetles and dragonflies) are less common than smaller prey items (e.g. flies and moths) (C. C. Rittschof, personal observation), and because females can consume small prey items quickly, our daily counts provided a conservative estimate of prey capture rate. Each time a female moulted we recorded her new cephalothorax width, reproductive state and web size. When a female abandoned her web, her new web site was marked if it was within the study area and data collection continued. All new females that immigrated into the study area were added to the study upon arrival. Analysis of Census Data Census data were analysed separately for immature and mature females. Because some females abandoned their webs and built new webs within the study area during the time frame of the census, measurements were calculated on a per-web basis. Using this method, some individuals (29 immature females, 6 mature females) appeared more than once in the data set. In these cases, only the first web for each female was included in the analysis. For each female we calculated web tenure, which is defined as the number of days between the first observation and the day the female completely abandoned her web site. Because females periodically reconstruct portions of their orb that have been damaged by prey or debris, a web was considered to be in the same site if it maintained at least one anchor line (silk that connects the web to the substrate) from the original web. Otherwise, if the female moved her web, the site was considered abandoned.

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For each female web included in the data analysis, we calculated the mean number of prey carcasses present per day (mean prey/ day), mean kleptoparasite load (mean kleptoparasites/day) and mean number of males present per day (mean males/day). The independent variables mean prey/day, mean males/day and mean kleptoparasites/day showed a pattern consistent with an underlying Poisson process, so each rate value was divided again by total web tenure to estimate the central tendency (Freund & Wilson 1997). The dependent variable, web tenure, was log transformed to normalize the distribution of the data. We constructed a generalized linear model with web tenure as the dependent variable, and mean prey/day/day, mean males/day/ day, mean kleptoparasites/day/day (hereafter prey rate, male rate and kleptoparasite rate, respectively), start date and female cephalothorax width as independent variables. We analysed the model using backwards elimination and specified a probability to leave of 0.15. Independent variables were removed one at a time until all variables remaining had a significance of P < 0.15. Experiments We conducted two separate experiments for mature and immature females. Because no study had addressed the role of male presence in site movement decisions, we manipulated male presence to test for a causal effect on web tenure for both female age groups. Because males are not as common on immature female webs as they are on mature webs, we added males to immature webs to test for effects of male presence. In addition, to test the common assumption that prey capture rate affects web tenure in spiders, in a second treatment we added prey to immature female webs. The immature female manipulations were conducted as a 2  2 factorial design (Fig. 1a). For mature females, because we were concerned about having a sufficient number of individuals for analysis, we conducted only a single treatment where we manipulated the presence of males. For this treatment, because males are common on mature female webs, we removed all males present (Fig. 1b). For both female age groups we accounted for the effects of kleptoparasite load by holding the number of kleptoparasites constant. At the beginning of both experiments, we recorded each female's body size, as well as the number of prey items, males and kleptoparasites present on each web. This record established the ‘baseline’ number of males and kleptoparasites for each female in the experiments. To hold the kleptoparasite load constant throughout the experiments, we maintained the number of kleptoparasites at or below the baseline number. To do this, we either removed new kleptoparasites that arrived daily, or left kleptoparasites unmanipulated if there were no new arrivals or if some kleptoparasites left the web. Kleptoparasites that were removed were released at least 10 m from the nearest treatment web. All females included in the experiments had webs no higher than 2.5 m from the ground, each female had eight legs, and webs of all females were in good condition. Females and their webs were marked in the same way as they were for census data collection. On each treatment day, we recorded the number of prey items, males and kleptoparasites present on the web before performing treatments. Finally, as a control for disturbance, all webs that did not require manipulation were plucked daily until the female left her resting position. Immature females We assessed the effects of increased male presence and increased prey capture rates on immature female web tenure from 26 June to 8 July 2008. On day 1 we randomly selected 96 females using the following criteria: (1) females were immature and

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(a) N=20

N=21

N=18

N=20

(b) N=73

N=67

Figure 1. Experimental design used to examine factors affecting web tenure in the orb-web spider Nephila clavipes. (a) For immature females, males and/or cricket prey were added to the webs daily, or webs were left unmanipulated in a full factorial design. (b) For mature females, all males on the web were removed daily or left unmanipulated. Initial male group size ranged from 0 to 5 males. There was no prey treatment for mature females. For both immature and mature female experiments, kleptoparasites were removed daily as necessary to maintain the number of kleptoparasites at or below the initial number present at the start of the experiment.

between 3.3 mm and 4.8 mm in size (2e3 instars from maturity), and (2) there were no conspecifics within a 1 m radius. Each female was assigned at random to either the manipulated or control for both the prey and male treatments in a full factorial design. Because each female was assigned to one prey treatment and one male treatment, there were four treatment combinations that started with 24 females in each combination. However, some webs were accidentally destroyed over the course of the study, decreasing the sample size for some treatment combinations (Fig. 1a). A thunderstorm prevented executing the treatments on day 1, making day 2 the first treatment day. On day 2, 94 webs were found, and females were still present on 81 of them. For females in the manipulated prey treatment group, we added one small cricket (2.2 mm head capsule width) to the web each day. The females in the control prey treatment group did not receive supplemental prey. For the manipulated male treatment group, we added males to the web to maintain the number of males at one more than the baseline number. Immature females started with either 0 males or 1 male on their webs. Thus, if a female started the experiment with 0 males on her web, we added one male on day 2 and kept one male on her web throughout the experiment. In some cases, males stayed on the web when added on day 2, and we did not have to add any for the remainder of the experiment. In other cases the male left and we

added a new male to the web each day. For females in the control male treatment group, we removed or added males to maintain the number of males at the baseline number for each female. Each web was treated for 10 days, or until the female abandoned the web. The 10-day length of the experiment was based on the upper quartile for immature female web tenures in the census data. Mature females We assessed the effects of male removal on the length of female web tenure in an experiment conducted during 23 Auguste6 September 2008. Females entered the experiment over a period of 5 days because daylight time constraints prevented starting all females at the same time. The experiment spanned 14 days from the first experimental day for the first cohort of females to enter the experiment. This time period was chosen based on the upper quartile of web tenure in the census data. We marked 140 mature females and their webs. In addition to taking the initial baseline measurements and body size measurements on the first day as we did for immature females, we included a measure of abdomen height, the maximum dorsaleventral distance across the abdomen. Corrected for body size, abdomen height is a measure of condition (Vincent & Lailvaux 2006). Each female was assigned to either the experimental malesremoved group or the control group (Fig. 1b). Some females attracted more males than others, so the baseline number of males found on female webs was variable (range 0e5 males). However, as a result of the natural distribution of males on female webs, group sizes of 3e5 were rare. To control for this initial variation in male presence, females with similar baseline male numbers were split as evenly as possible across the two treatment groups. Because the objective of this experiment was to evaluate the effect of male presence on female web movement, in our experimental group (males-removed) we removed all males present for each day of the experiment. Males were released at least 10 m from the nearest treatment web. For the control group, we did not add or remove males. The experiment continued until the female abandoned her web, or until the end of the experiment (14 days after treatment day 1). During the course of the study, three females left their webs to lay a clutch of eggs and then returned to their original web site after 1e2 days with deflated abdomens. Because these females chose to return to the same web site, their web tenure includes the time spent at the web site after they returned from their oviposition sites. Because many females abandon intact webs, we monitored abandoned webs for up to 3 days to ensure females did not return. Experimental Data Analysis Web tenure, measured as time until web abandonment, had a distribution that was very similar to a survivorship curve for a cohort of individuals over time (Fig. 2). For this reason, we used the Cox proportional hazards model from the SAS statistical package JMP (SAS Institute, Cary, NC, U.S.A.) to determine which experimental variables affect web tenure. The proportional hazards model uses a partial likelihood estimate to determine whether a model covariate (factor) increases or decreases the probability of web abandonment. A positive estimate value means that the covariate increases the likelihood that the female will abandon her web. In all analyses, we used a backwards elimination approach, removing the least significant covariate and reanalysing the model until the only covariates remaining had a significance value P < 0.15 for the partial likelihood ratio test (Allison 1995). For immature females, both male and prey treatments, as well as their interaction, were added to the model as covariates. For mature females, the male treatment was added. Because the start date

C.C. Rittschof, K.V. Ruggles / Animal Behaviour 79 (2010) 1147e1155

Males added Control

Proportion remaining

0.8

0.6

Immature females (N=128) Mature females (N=42)

0.4 Proportion of webs

1

1151

0.3

0.2

0.1 0.4 0 0.2

5

10

15

20 25 30 35 40 Web tenure (days)

45

50

55

Figure 3. Census web tenure distribution of immature and mature female Nephila clavipes, represented as a proportion of total webs in each age class (bin ¼ 5 days).

0

2

4

6 8 Time (days)

10

12

Figure 2. Web tenure in the orb-web spider Nephila clavipes, represented as a survivorship curve. This sample survivorship curve corresponds to the immature female experiment where males were added to the web or left unmanipulated in the control. The Cox proportional hazards analysis determined which covariates contributed to the shape of the survivorship curve.

varied among females in both experiments, the experimental start date was included as a covariate (Allison 1995). Other covariates were cephalothorax width, and, for mature females, condition. To address multiple hypotheses for web abandonment simultaneously, we incorporated additional covariates calculated from our data. The following measurements were calculated strictly, without any transformation: (1) the mean number of males found on each web per day (mean males/day) (2) the mean daily prey capture rate (mean prey/day) and (3) the mean number of kleptoparasites present each day before we removed new arrivals (mean kleptoparasites/day). Finally, to test for an interaction effect between kleptoparasite load and prey capture rate as shown by Rypstra (1981), we ran the analyses a second time replacing mean prey/day and mean kleptoparasites/day with ‘prey consumption rate’ as the covariate: prey consumption rate ¼ mean prey/day  0.25  mean kleptoparasites/ day. The prey consumption rate is an approximation of the number of prey consumed by N. clavipes per day after a portion of the prey caught is lost to kleptoparasitic spiders. The amount of prey lost is proportional, not equivalent, to the number of kleptoparasites present, because kleptoparasites are smaller than N. clavipes and they often feed on prey that the N. clavipes female has partially consumed (C. C. Rittschof, personal observation). Thus, for our estimate of the negative impact of kleptoparasites on N. clavipes prey consumption, we discounted the mean number of kleptoparasites present per day by one-fourth (for every four kleptoparasites present each day, one item of food per day is lost). This is a generous estimate of the effect of kleptoparasites on prey consumption in this population of N. clavipes (C. C. Rittschof, personal observation). RESULTS

factors with P < 0.15, explained a significant amount of variation in web tenure and yielded one significant factor: kleptoparasite rate (kleptoparasites/day/day) was negatively correlated with web tenure for immature females (slope ¼ 2.10, SE ¼ 0.484, F1,122 ¼ 18.9, P < 0.0001). Mature females Web tenure ranged from 1 to 53 days (median ¼ 7 days, 75% quartile ¼ 12.8 days; Fig. 3). Initially, the final model after backwards elimination yielded only one significant factor: prey rate (prey/day/day) was negatively correlated with web tenure. However, the significance of prey rate was strongly driven by one outlier, a female observed for 1 day that day caught two prey items. When we removed the outlier, the final model explained a significant amount of variation in web tenure, and yielded three significant factors: prey rate was negatively correlated with web tenure (slope ¼ 1.64, SE ¼ 0.741, F1,33 ¼ 4.9, P < 0.034); later in the season, web tenure was shorter (slope ¼ 0.02, SE ¼ 0.005, F1,33 ¼ 8.7, P < 0.006), and increased male rate (males/day/day) was negatively correlated with web tenure (slope ¼ 7.68, SE ¼ 2.143, F1,33 ¼ 12.9, P < 0.001). Experiments Immature females By day 10, 76% of the females abandoned their webs (N ¼ 78, three webs were accidentally destroyed). The prey-added and the males-added treatments significantly increased prey capture rate (mean prey/day: t77 ¼ 10.051, P < 0.0001) and number of males present (mean males/day: t77 ¼ 8.27, P < 0.0001), respectively, compared to the control treatments (Fig. 4). However, no covariates significantly affected web tenure, although the sample size of 78 had a power of 0.75 to detect a difference in web tenure of 2 days between treatment groups. The covariate that had the greatest effect was male treatment, which decreased web tenure (P ¼ 0.28 when all other covariates were eliminated). Finally, when the covariate prey consumption rate was substituted for mean prey/day and mean kleptoparasites/day, there was still no effect on web tenure.

Census Immature females Web tenure ranged from 0 to 49 days (median ¼ 6 days, 75% quartile ¼ 10.5 days; Fig. 3). The final model, which included the

Mature females Of the 140 webs, 95% were monitored for 12 or more days, and 74% of the females on these webs had abandoned their web site by day 14 of the experiment. The males-removed treatment did not

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C.C. Rittschof, K.V. Ruggles / Animal Behaviour 79 (2010) 1147e1155 Table 2 Covariate estimates in the proportional hazards model for the probability of web abandonment by Nephila clavipes in the mature female experiment, with prey consumption rate

2 (a) ∗

Mean prey/day

1.5

1

Estimate

P (if <0.15)

0.393 0.449 2.12 0.542

0.0164 0.0090 0.0001 0.0088

CW: cephalothorax width. The value ‘prey consumption rate’ combines the effects of mean prey/day and mean kleptoparasites/day to account for the effects of kleptoparasites on prey consumption. Significant values are shown in bold (P < 0.05).

0.5

0

males-removed treatment and individuals that were in the control group) and ran two separate proportional hazard analyses for web tenure starting only with the significant covariates from the combined analysis. When the control group and the malesremoved treatment group were analysed separately, mean males/ day was a highly significant covariate in the males-removed treatment group analysis, but not significant in the control treatment group analysis. Separating the control and treatment groups had other effects on the significant covariates from the analysis of the full data set (Table 3); condition remained the only other significant factor other than mean males/day, and only in the males-removed treatment group.

Control

Prey added

2 (b)

1.5 Mean males/day

Covariate Mean males/day Body size (CW, mm) Condition Prey consumption rate

∗

1 DISCUSSION

0.5

0

Males added Control Treatment

Figure 4. (a) Mean  SE number of prey captured/day by immature female Nephila clavipes in the prey-added group and the control group. (b) Mean  SE number of males/day on webs of immature female Nephila clavipes in the males-added group and the control group. *P < 0.0001.

significantly affect web tenure of mature females. Increased mean kleptoparasites/day was associated with a decrease in web tenure, although the effect was not significant. Increased mean prey/day, increased body size and increased condition were associated with a significant increase in web tenure, while increased mean males/ day corresponded to a decrease in web tenure (Table 1). Increased prey consumption rate (due to an increase in prey capture and/or decrease in kleptoparasites) corresponded to a significant increase in web tenure (Table 2). The significant negative effect of male presence (as measured as mean males/day) on web tenure was surprising because daily removal of all males did not affect web tenure (i.e. there was no males-removed treatment effect on web tenure). We performed an additional analysis to interpret this result. We split individuals by treatment (two separate groups: individuals that were part of the

Table 1 Covariate estimates in the proportional hazards model for the probability of web abandonment by Nephila clavipes in the mature female experiment Covariate

Estimate

P (if <0.15)

Mean kleptoparasites/day Mean prey/day Mean males/day Body size (CW, mm) Condition

0.095 1.31 0.410 0.407 1.91

0.1146 0.0125 0.0138 0.0187 0.0009

CW: cephalothorax width. Significant values are shown in bold (P < 0.05).

Census data showed that different factors were correlated with web tenure for immature and mature females: kleptoparasite presence was a significant factor for immature females while date, prey capture rate and male presence were significant factors for mature females. Experimental treatments for immature females tested for a causative effect of male presence and prey capture rate on web tenure while kleptoparasite load was controlled. There was no effect of the prey and male treatments on web tenure, and no other measured factor was significantly correlated with web tenure. For mature females, in order to ensure an adequate sample size, only male presence was experimentally manipulated while kleptoparasite presence was controlled. Although there was no treatment effect of male removal, multiple factors were correlated with web site movement decisions for mature females: prey capture rate, male presence, female condition, body size and date. These findings suggest that N. clavipes web movement decisions are complex and age specific.

Prey Capture Rate There were mixed results regarding the relationship between prey capture rate and web movement decisions in N. clavipes. Prey capture rate did not affect immature female web tenure. Prey capture rate of mature females was negatively correlated with web Table 3 Covariate estimates in the proportional hazards model for the probability of web abandonment by Nephila clavipes in the mature female experiment, separated by treatment group Covariate

Mean males/day Body size (CW, mm) Condition Prey consumption rate

Estimate

P (<0.15)

Males removed

Control

Males removed

Control

0.777 0.366 2.35 0.451

0.107 0.412 1.27 0.613

0.0004 0.1301 0.0214 0.1594

0.7042 0.0855 0.0972 0.0543

CW: cephalothorax width. Males removed and control groups were analysed separately. Significant values are shown in bold (P < 0.05).

C.C. Rittschof, K.V. Ruggles / Animal Behaviour 79 (2010) 1147e1155

tenure in the census, but was positively correlated with web tenure in the experiment. These opposite results suggest that prey capture rate has no causative role in site abandonment. High prey capture rates could have occurred at web sites chosen using other selection criteria. In widow spiders, Lubin et al. (1993) found that structural habitat features that provide support for webs, protection from predators and shelter from thermal extremes play a greater role in site selection than prey capture rate. In our study, general habitat features differed between the census and the experiment; web sites on boundaries between forests and open areas were common in our experiment but infrequent in the closed census plot. These boundary habitats are high in prey (Vollrath 1985), but they are also high in temperature and light exposure. Furthermore, the effect of date on web tenure in the mature female census suggests that temperature or daylength may influence site movement. This evidence, in addition to the null result of the prey-added treatment for immature females, leads us to conclude that high prey capture rates are a by-product of site selection based on other criteria. The overall lack of effect of prey capture rate on web tenure is surprising given the generalization that orb-web spider site selection is affected by web site profitability (Rypstra 1981; Janetos 1982; Vollrath 1985; Uetz 1992; Nakata & Ushimaru 1999). However, other studies have reported mixed results on the effect of prey capture rate on female web movement in N. clavipes (e.g. Vollrath 1985; Vollrath & Houston 1986). Furthermore, in spider species with prey capture patterns similar to N. clavipes (e.g. Tetragnatha elongata), female site movement strategy is not affected by female prey capture experience. Temporal variation in prey capture rate overwhelms a female's ability to detect variation in prey capture rate among web sites (Caraco & Gillespie 1986; Gillespie & Caraco 1987; Lubin et al. 1993). Instead, female foraging strategies reflect overall prey abundance within the larger habitat. Male Presence In the mature female census, male presence was negatively correlated with web tenure. In the mature female experiment, mean males/day was negatively correlated with web tenure. Separate analyses of the males-removed treatment group and the control group within the mature female experiment revealed that increased mean males/day was strongly associated with decreased web tenure, but only for females in the males-removed treatment group. One hypothesis for this effect could be that the malesremoved treatment changed the way in which females perceived or interacted with new male visitors. When males arrive at a web, they compete among themselves for the hub position close to the female (Christenson & Goist 1979). The hub male copulates with the female and prevents other males from mating with her (Christenson & Goist 1979; Cohn et al. 1988). In our studies, the number of unique males that arrive at a females' web site during a single tenure ranges from 0 to 16 (C. C. Rittschof, unpublished data). However, because of the presence of the hub male, most of these males never have the opportunity to court or mate with the female. Defence of the female by the hub male may decrease the level of female harassment from newly arrived males. Thus, as was the case in the males-removed treatment group, if all males including the hub male are removed every day, the process of competition among newly arrived males and attempted copulation with the female occurs daily. Our results support the hypothesis that male presence in the form of high encounter rates with new males and possibly high levels of harassment decrease female web tenure. Furthermore, there was no effect of male presence for immature females, presumably because males do not attempt to copulate with these females.

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Costs of female harassment by males are common in species like N. clavipes with a male-biased operational sex ratio, or in situations where multiple males attempt to mate with the female simultaneously (Clutton-Brock & Parker 1995). However, females should only respond to male harassment when costs of harassment are high. In some systems, females suffer a physical cost to mating when males are the larger sex. In others, male harassment prevents females from foraging successfully (Magurran & Seghers 1994; Chapman et al. 2003). In N. clavipes, more work remains to demonstrate whether hub male presence decreases female harassment, and if harassment carries a cost. Kleptoparasite Load Kleptoparasite load was not correlated with web tenure in the mature female census or in the immature or mature female experiment. Increased kleptoparasite load has often been proposed to affect host web tenure (Robinson & Olazarri 1971; Robinson & Robinson 1973, 1976; Vollrath 1979), but few studies have demonstrated negative effects of these parasites on their hosts (Rypstra 1981; Grostal & Walter 1997; Koh & Li 2002). In other species of Nephila, there are mixed results regarding the importance of kleptoparasite presence on web abandonment by hosts (Grostal & Walter 1997; Koh & Li 2002). Rypstra (1981) demonstrated a positive correlation between prey consumption rate (prey capture rate minus prey consumed by kleptoparasites) and web tenure in N. clavipes. Our results do not support this finding, possibly because of population differences. Rypstra's (1981) study population was tropical, with much higher prey capture rates. Furthermore, Rypstra (1981) documented prey thefts by Argyrodes at a higher rate than occurs in our population of N. clavipes (C. C. Rittschof, personal observation). In N. clavipes, kleptoparasite load is a function of web size and the degree of connectivity among neighbouring webs (Agnarsson 2003), and in our population there may be little effect of kleptoparasite presence on female web movement. Female Condition and Body Size Condition and body size were positively correlated with web tenure for mature females. Large abdomen size is in part a consequence of egg development (Ortlepp & Gosline 2008), and so the relationship between tenure and abdomen height could be because movement for gravid females is risky; this is the case in other species because gravid females are slow and clumsy compared to nongravid females (Magnhagen 1991; Rodewald & Foster 1998; Ghalambor et al. 2004; S. P. Lailvaux, personal communication). Because three females laid eggs during the course of our experiment, at least some of the females with large abdomens were gravid. However, it is also possible that large abdomen size was the result of recent consumption of a large prey item. In Stegodyphus lineatus, hungry females adopt a more risky web selection strategy compared to satiated females (Bilde et al. 2002). If N. clavipes females with large abdomens are satiated and in good condition, the risks associated with changing web sites may outweigh the benefits (Caraco & Gillespie 1986). Furthermore, females with smaller absolute body size that changed webs more often in our study might have done so because they matured in habitats with low prey abundance, and so they adopted a risky foraging strategy. Conclusions While our study addresses the relationship between web tenure and date, female size, age, condition, prey capture rate, kleptoparasite load and male presence, it excludes important variables that

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affect web tenure and web abandonment in other species. For example, web disturbance and destruction stimulate web relocation in spiders (Chmiel et al. 2000), and these factors could add variability to N. clavipes web tenure. Predator avoidance is another factor that could affect web movement decisions, particularly for immature N. clavipes. Many spiders aggregate (e.g. Rayor & Uetz 1990; Lloyd & Elgar 1997) or occupy protected sites (e.g. Lubin et al. 1993; Blamires et al. 2007) to decrease predation risk. Immature N. clavipes inhabit interior of wooded patches, whereas mature females inhabit forest edges, and immature webs are often clustered with overlapping orbs (C. C. Rittschof, personal observation). These web site features could reduce predation risk and influence site abandonment decisions especially for smaller females. Finally, the age of the orb web itself might affect its quality, and correspond to changes in prey capture rate, kleptoparasite load and male presence. Pollen, dust and rain decrease the stickiness of the prey capture spiral over time, which decreases prey capture efficiency (Opell & Schwend 2008). Chemicals present in the prey capture silk that are toxic to insect prey (Salles et al. 2006) and might serve as male or kleptoparasite attractants also degrade over time. In our study, females with shorter web tenures could have been females that changed web sites at a high rate and therefore had webs that were new and in good condition. If young webs are associated with high rates of prey capture, male presence and kleptoparasite load, these variables might be a consequence, not a cause, of short tenure. Despite the importance of other unmeasured factors, our study demonstrates that female web tenure is highly variable, and that female web movement decisions are complex and age dependent. We found little support for factors that are traditionally attributed to web movement decisions, including prey capture rate and kleptoparasite load. Overall, the factors driving web movement for immature females remain unclear. In contrast, our results suggest that female body size, condition and time of season influence web movement decisions for mature females. Furthermore, this study supports the novel hypothesis that web tenure for mature females is influenced by male presence and possibly male harassment for copulations. The conclusions about habitat selection and site quality drawn from this spider system have implications for other animal systems that share similar reproductive strategies, life history characteristics, or ecological niches. For example, costs of male harassment and female response to male harassment are common across diverse groups including insects, mammals and birds (CluttonBrock & Parker 1995; Fox 2002; Gay et al. 2009). The relationship between N. clavipes female web abandonment behaviour and male presence suggests that female survival and reproduction in a malebiased population may be a direct function of the presence of males themselves. Such is the case, for example, in the Ile Longue feral sheep, where female mortality is greatest during the summer when food resources are plentiful, but harassment by males is also at its peak (Reale et al. 1996). Spiders' web movement decisions warrant future study because the microhabitat of the web is a tractable model system for addressing the physiological and ecological factors that affect site movement decisions at large. This study adds to a growing body of literature that acknowledges the importance of understanding the plasticity and context-dependent nature of behavioural decisions. Acknowledgments We thank our field assistants Kristie Vetter and Jason Ziegler. We are also grateful to Mark Brenner and Susan Milbraith for the use of the Jonesville field site as well as the Ordway-Swisher Biological

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