Introduction

Predators use a wide range of tactics to catch prey, from sit-and-wait tactics, where the predator waits for prey to approach (e.g., snakes such as Gloydius shedaoensis that ambush their prey; Shine and Sun 2003), to active tactics, where the predator approaches the prey (e.g., cougars, Puma concolor, that stalk and chase their prey; Husseman et al. 2003). While some predators will use one tactic against all, or most, of their prey (e.g., crab spiders that ambush pollinating insects on flowers, Morse 1981; Heiling et al. 2005), others may flexibly alternate between tactics according to the type of prey, the environment or circumstances during the hunt. Flexible use of predatory tactics has been observed in a wide variety of taxa, including mammals (e.g., harbour seals, Phoca vitulina; Bowen et al. 2002), birds (e.g., loggerhead shrikes, Lanus ludovicianus; Yosef and Grubb 1993), reptiles (e.g., snakes, Natrix maura; Patterson and Davies 1982), fish (e.g., brook charr, Salvelinus fontinalis; Grant and Noakes 1987) and spiders (e.g., the jumping spider Portia fimbriata; Jackson and Blest 1982; Jackson 1995). A predator that hunts dangerous prey may use specialised, prey-specific tactics. For example, whiptail lizards simply catch and eat harmless crickets, but vigorously shake and throw dangerous scorpion prey before eating it (O’Connell and Formanowicz 1998).

Spiders are dangerous prey to the insects that hunt them, as the spider is both prey and potential predator. Descriptions of the predatory tactics used by araneophagic (‘spider-eating’) insects are limited to only a few studies. Several species of parasitic wasp use the tactic of flying into spider webs, forcing the spiders to drop from their webs to the ground where they may be more easily captured (Sceliphron caementarium (Blackledge and Pickett 2000) and Pison morosum (Laing 1988)). Chalybion caeruleum, another parasitic wasp, uses aggressive mimicry to lure Argiope spiders within attacking range (Blackledge and Pickett 2000). However, these wasps have each only been observed using the one predatory tactic against their spider prey.

Stenolemus assassin bugs are also predators of web-building spiders. Whilst little is known of the predatory tactics used by Stenolemus species studied to date, they appear to have very narrow prey ranges. For example, Stenolemus lanipes has been reported hunting the tangle-web spider Achaearanea tepidariorum (Hodge 1984) and Stenolemus edwardsii has been reported to hunt spiderlings of the common house spider Ixeuticus robustus (Badumna insignis) although it will feed on other small spiders when these are unavailable (Hickman 1969). In sharp contrast to reports for these species, Stenolemus bituberus has a wide prey range, and uses two distinct predatory tactics, ‘stalking’ and ‘luring’ (Wignall and Taylor 2008). When stalking spiders, S. bituberus slowly approach the spider until within attacking range. When luring spiders, S. bituberus manipulate the silk of the webs, generating vibrations that attract the resident spider into range. We present in this paper one of the first studies of how alternative predatory tactics are used by an araneophagic insect while hunting different prey spiders.

Materials and methods

Stenolemus bituberus and prey spiders (juveniles and adults of both) were collected from trees and buildings on Macquarie University campus (Sydney, Australia), and when possible were returned after testing. Juvenile S. bituberus cannot fly and are unlikely to move far, if at all, from the location where they were collected. As we did not visit trees more than once during each instar, it is unlikely that individual S. bituberus were tested more than once within an instar, although some individuals may have been re-tested at later instars. The spider species we collected were Achaearanea extridium (n = 50) and Achaearanea sp. (n = 52) (Theridiidae), Badumna longinqua (n = 54) (Desidae), Pholcus phalangioides (n = 50) (Pholcidae) and a species belonging to an unidentified genus from the family Uloboridae (n = 53). These spiders represent circa 90% of the genera that S. bituberus have been observed hunting in the field (Wignall and Taylor 2008).

Spiders were collected 2–5 days before testing, and were placed in wooden frames (200 × 200 × 30 mm) to build webs. Frames closely resembled those of Jackson et al. (2002). They had a removable clear acrylic screen at the front, to which spiders could not attach their web (removed for tests), and a wooden screen at the back. Frames were cleaned with a damp cloth between tests and were set up outdoors under shade to maintain natural light, temperature and humidity.

On the morning of each test, S. bituberus were collected from the field and photographed under standard magnification through an Olympus SZX12 microscope using a ProgResC10 digital camera and proprietary software (Jenoptik L.O.S., Germany). Pronotum length and abdomen width were measured from images using UTHSCSA ImageTool v3.00 software. Condition was defined as residuals from the regression of pronotum length on abdomen width (see Jakob et al. 1996; Taylor et al. 2000). The relative size of the spider was calculated as body length of the spider divided by the body length of S. bituberus.

All tests were started in either early morning (6–10 a.m.) or late afternoon (5–7 p.m.), the most active periods of S. bituberus in nature (A. Wignall, personal observations). We randomly assigned each individual S. bituberus to a spider species. To transfer S. bituberus to the frame, we carefully removed the piece of paper on which it stood from the maintenance vial and placed it on the base of the frame. Observations started once S. bituberus placed a tarsus on the frame. Tests were aborted if S. bituberus failed to begin hunting (i.e., failed to contact a silk thread with a tarsus or antenna) within 1 h.

We recorded the predatory behaviour of S. bituberus and the responses of the spiders. Tests ran until: (1) S. bituberus caught the spider; (2) the spider caught S. bituberus; (3) the spider ran away (i.e., left the frame) or (4) S. bituberus abandoned the hunt (i.e., left the frame or no activity for 90 min). For each hunt, we assessed whether the luring tactic was used or whether S. bituberus relied only on stalking. We report the p-values for whole models of statistical tests, then all subsequent p-values less than 0.1 for individual predictors.

Results

Stepwise logistic regression was used to investigate factors that might influence whether an S. bituberus initiated hunting. Factors initially included in the model were spider species, spider size (relative to assassin bug size) and S. bituberus condition (whole model chi-square 21.57, df = 6, p < 0.01). Of these, the only factor that significantly influenced pursuit tendency was spider species (G 4 = 26.33, p < 0.01), with pairwise Fisher’s exact tests showing that S. bituberus were more likely to initiate hunts against Achaearanea sp. than against any other species (p ≤ 0.05 for all comparisons; Fig. 1a). Stenolemus bituberus were also more likely to initiate hunts against A. extridium and P. phalangioides than against Uloboridae sp. (p < 0.01 for both comparisons).

Fig. 1
figure 1

For each spider species (sample sizes indicated above bars), a proportion of S. bituberus initiating hunts; b proportion of each of the four possible outcomes of a hunt; and c proportion of S. bituberus using either the luring or stalking tactic

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We considered whether hunt outcome varied among the spider species hunted, excluding Uloboridae sp. for which all S. bituberus abandoned their hunts (Fig. 1b). Hunts had significantly different outcomes for different spider species (Fisher’s exact test, test statistic = 30.46, p < 0.01). Pairwise Fisher’s exact tests revealed all comparisons to be significant (all p < 0.05) except for between A. extridium and B. longinqua (p = 0.89; Fig. 1b). There was a strong tendency for S. bituberus to abandon hunts against A. extridium, B. longinqua and Uloboriidae sp., high probability of being killed in hunts against P. phalangioides, and high probability of success in hunts against Achaearanea sp. (Fig. 1b).

Stepwise logistic regression was used to assess the influence of spider species (excluding Uloboridae sp. due to small sample sizes), spider relative size and S. bituberus’ condition on the predatory tactic adopted (whole model chi-square = 12.63, df = 6, p = 0.05). Of these, only spider species influenced predatory tactic (G 3 = 9.08, p = 0.03). Pairwise Fisher’s exact tests showed that S. bituberus were more likely to use the luring tactic against A. extridium and Achaearanea sp. and more likely to rely on stalking alone against P. phalangioides (both p < 0.05; Fig. 1c).

Stepwise polytomous logistic regression was used to analyse factors associated with the outcome of hunts against Achaearanea sp. The other spider species were excluded from this analysis as small sample sizes for some of the outcomes introduced instability in the models. Factors included in the model were spider relative size, S. bituberus’ condition and the distance at which the hunt began (whole model chi-square = 14.36, df = 6, p = 0.03). We found that S. bituberus were more likely to catch spiders rather than abandon the hunt if they were large relative to the spider (G 3 = 8.70, p = 0.03) or if they were in poor condition (G 3 = 8.25, p = 0.04) (Fig. 2). The probability of any of the four possible outcomes of the hunt was not affected by the tactic used (chi-square = 0.86, df = 3, p = 0.84). The duration of successful hunts did not vary with the relative size of the spider or with S. bituberus’ condition (whole model F 2, 16 = 0.93, p = 0.42).

Fig. 2
figure 2

Influence of a spider relative size (calculated as body length of the spider divided by the body length of S. bituberus) and b S. bituberus’ condition (defined as the residuals from a regression of pronotum length on abdomen width) on the outcome of hunts of Achaearanea sp

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Discussion

The predatory behaviour of S. bituberus assassin bugs varied with prey spider species. In particular, hunts were initiated more often against A. extridium and Achaearanea sp. than against the other spider species. This is consistent with field observations indicating that spiders from the genus Achaearanea are among their main prey (Wignall and Taylor 2008). Other Stenolemus assassin bugs also prey on Achaearanea spiders, these being the sole reported prey of S. lanipes (Hodge 1984). S. bituberus appears to differ from other studied Stenolemus in preying on spiders and spiderlings from many different genera (and families), although it is possible that more detailed investigation would reveal wider prey ranges than those reported to date for other Stenolemus species.

S. bituberus select their predatory tactic according to spider species, with luring used more often against each of the Achaearanea species than against P. phalangioides. Prey-specificity of predatory tactic may be related to differences in aggressiveness of each spider species, and hence differences in the probability of counter-attack. Both P. phalangioides and spiders from the genus Achaearanea are known to throw silk at prey snared by their webs (Jackson et al. 1990; Hajer and Hrubá 2007). However, P. phalangioides are also web-invading aggressive mimics (Jackson and Brassington 1987) and we observed more individuals of this species counter-attacking and killing S. bituberus than spiders from the genus Achaearanea (see Fig. 1b). In other studies, we have found P. phalangioides to be much more prone to rapidly approach and attack artificial vibratory stimuli compared with Achaearanea species (A. Wignall, unpublished data). Hence, S. bituberus may reduce the risk of detection and counter-attack by stalking rather than luring P. phalangioides. Alternatively, S. bituberus may be better able to attack the body of P. phalangioides when stalking. When luring P. phalangioides, attacking the body may be more difficult due to this species’ long legs with which it can throw silk at the assassin bug from a distance. A still further hypothesis may be that S. bituberus alters predatory tactic, not to reduce risk, but to increase the probability of capturing the spider. However, we found no evidence to suggest that, for hunts against Achaearanea sp. at least, the predatory tactic affects capture rate.

Although the relative tendencies varied among prey species, S. bituberus did use both stalking and luring tactics against each spider species tested. Interestingly, neither spider size nor S. bituberus’ condition influenced the tactic used. For example, prey size affects the risk posed by prey, and as a result the predatory tactic adopted, in Nephila orb-weaving spiders (Higgins 2007). However, while predatory tactic was not affected, S. bituberus did tend to abandon more hunts against larger spiders (see Fig. 2), indicating that spider size may still be a factor in the assessment of risk.

Generally, predators capture small prey more easily than large prey (e.g., Husseman et al. 2003). Indeed, predators are usually larger than their prey (e.g., Magalhães et al. 2005). In our experiments, S. bituberus were more likely to capture smaller Achaearanea sp. and were more likely to abandon hunts against larger spiders. These results suggest both that larger spiders are more dangerous and that S. bituberus can discern spider size, perhaps visually, chemically or using seismic cues transmitted through the web.Size-dependent risk of counter-attack on predators has been reported in several species, including a phytodsiid predator Typhlodromus bambusae whose nymphs are more vulnerable than adults to counter-attack from prey spider mites (Schizotetranychus celarius) (Saito 1986).

The condition of S. bituberus also influenced the outcome of hunts against Achaearanea sp. Stenolemus bituberus that were in poor condition were more likely to persist and capture the spider, whereas those that were in better condition were more likely to abandon the hunt (Fig. 2). Optimal foraging theory predicts that as the quality of the environment improves, predators become more selective of prey (e.g., Osenberg and Mittelbach 1989). Stenolemus bituberus with better body condition are likely to have been collected from better quality sites, and hence may be more selective of the spiders they persist in hunting. Alternatively, S. bituberus in poorer condition may be more likely to risk hunting dangerous prey, as has been observed in other species that will take risky prey when starved (e.g., Gillette et al. 2000).