Visual cues used in directing predatory strikes by the jumping spider Yllenus arenarius (Araneae, Salticidae)

Animal Behaviour 120 (2016) 51e59

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Visual cues used in directing predatory strikes by the jumping spider Yllenus arenarius (Araneae, Salticidae) Maciej Bartos*, Piotr Minias
d
z, Poland Department of Biodiversity Studies and Bioeducation, University of Ło

a r t i c l e i n f o Article history: Received 5 May 2016 Initial acceptance 30 May 2016 Final acceptance 4 July 2016 MS. number: 16-00401 Keywords: deflection details false head jumping spider motion perception Salticidae visual cues Yllenus arenarius

Salticids are known for their complex predatory behaviour, which is based on the analysis of visual information from their prey, but the role of cues used in different predatory tasks is poorly known. We investigated which cues are used to identify the preferred target on the prey's body, examining the reactions of the euryphagous salticid Yllenus arenarius to various virtual prey presented on a miniature screen. We manipulated the number of head-indicating details (ranging from prey with four details, including a head spot, antennae, legs and wings, to prey lacking any details), the position of these details in relation to motion direction (in the leading versus in the trailing part of the body), the local motion of legs and the presence of horizontal motion. When all cues pointed to the same body end the spiders identified the preferred target almost unerringly regardless of the number of details. Movement alone, movement combined with a different number of details in the leading part, local motion of legs and head spot alone on motionless prey elicited the same reactions. When the cues provided contradictory information (motion direction and details pointing to opposite body ends) the spiders struck the trailing end more often the more details were placed there, and they visually inspected body ends of their prey before attack. These results indicate that the spiders used the direction of the prey's motion and the complexity of head-indicating details when making decisions related to strike targeting. These findings elucidate the role of motion and the complexity of details forming ‘false heads’, an antipredator adaptation assumed to redirect predatory strikes on prey from various animal groups. We demonstrate that in stationary prey even very simple patterns efficiently redirect predatory strikes. We provide the first experimental evidence of the effectiveness of ‘false head’ complexity in moving prey. © 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

The decision about which part of the prey's body a predator should strike may significantly affect predatory success and the predator's survival, particularly if the prey is comparatively large or dangerous. Accurate target identification enables the predator to strike areas that allow its fangs, claws or venom to act upon the sensitive organs of the prey (the major parts of the CNS, including locomotor ganglia or muscles that move legs and wings) and grasp the prey firmly while staying away from its defences (jaws, stings, defensive secretions). A predator that fails to identify the preferred target may not only lose the prey but also be injured or even become a meal itself. There is extensive evidence that predators bias their initial strikes to certain body parts. In various taxonomic groups as diverse as toads (Ingle & McKinley, 1978), mantids (Kral & Prete, 2004), wasps (Steiner, 1986) and spiders (Foelix, 1996; Pollard, 1990), including salticids (Bartos, 2002a; Cutler, 1980;

* Correspondence: M. Bartos, Department of Biodiversity Studies
d

d
Bioeducation, University of Ło z, Banacha 1/3, 90-237 Ło z, Poland. E-mail address: [email protected] (M. Bartos).

and

Edwards, 2008; Edwards & Jackson, 1993; Freed, 1984; Harland & Jackson, 2006) the strikes are directed at the anterior region of the body, where in bilateral animals the major vulnerable organs are located. However, it is unclear how the predators identify this preferred target. The anterior part of the body can be visually identified based on parameters related to the motion of prey (speed, motion direction, orientation of the object in relation to its motion direction and local motion of appendages) and the prey's appearance. Well-studied visual predators, such as toads, mantids and salticids have been demonstrated to rely on motion-related cues while discriminating between prey and nonprey (Bednarski, Taylor, & Jakob, 2012; Ewert, 2004; Kral & Prete, 2004). It is, however, not only moving prey that is captured. A number of visual predators also capture stationary prey. For example, highly specialized salticids routinely identify and capture motionless prey (reviewed in Jackson & Tarsitano, 1993) precisely targeting a specific body area (Nelson, Jackson, & Sune, 2005). Stalking and precise attacks on motionless prey have also been reported among nonspecialized salticids (reviewed in Forster,

http://dx.doi.org/10.1016/j.anbehav.2016.07.021 0003-3472/© 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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1982, 1985). Hence, there must be some cues not related to motion that enable predators to recognize prey orientation. Extreme specialists, such as Portia and Evarcha culicivora, rely heavily on details (e.g. eyes, antennae, legs) that can potentially indicate prey orientation, but no studies have been conducted to ascertain whether these details are used when targeting strikes (Harland & Jackson, 2000, 2002; Nelson & Jackson, 2012a, 2012b). Besides, the majority of salticids prey upon a wide range of arthropods which typically possess a variety of cephalic and caudal appendages with different forms, complexity, colours and local motion patterns; therefore, some more general cues rather than highly specific details seem to be more important in the identification of their preferred target. Salticids have exceptional eyesight due to their complex visual system consisting of eight eyes spaced around the carapace. However, it is a pair of large, forward-facing ‘principal eyes’ that is responsible for discerning image details (Land & Nilsson, 2012; Williams & McIntyre, 1980), colour vision (Blest, Hardie, McIntyre, & Williams, 1981; Peaslee & Wilson, 1989) and estimating distance (Nagata et al., 2012). These eyes have very high spatial acuities (down to 0.04
; Harland, Li, & Jackson, 2012), but within a very narrow horizontal visual field of 2e5
enlarged to about 60
by the ability of the whole eye tubes to move (Land, 1969b). Six relatively small ‘secondary eyes’ positioned along the sides of the carapace have wide visual fields and function primarily as movement detectors (Land, 1972, 1985) with the exception of the forward-facing anterior-lateral eyes, which possess higher visual acuities than the rest (Eakin & Brandenburger, 1971; Land, 1985) and play a role in the initial categorization of moving objects (Zurek & Nelson, 2012), the initiation of an approach to prey and during prey capture (Forster, 1979; Harland et al., 2012; Zurek, Taylor, Evans, & Nelson, 2010). To examine how euryphagous visual predators identify a preferred target we used Yllenus arenarius, a salticid with a diverse natural diet consisting of over 50 species of insects and spiders (Bartos, 2004, 2011). These spiders preferentially strike the prey in the anterior areas of their bodies (mainly thoraxes) with posterior strikes being exceptional (Bartos, 2002a, M. Bartos, personal observation; Fig. 1). The spider uses a conditional predatory strategy with distinct prey-specific predatory techniques reported in just-emerged spiderlings (Bartos, 2008; Bartos & Szczepko, 2012), which suggests that both predatory techniques and visual cues used in prey identification are preprogrammed. In this study we examined predatory decisions related to attack targeting in Y. arenarius. Our primary goal was to test which of the cues carrying information about the orientation of the prey's body, such as the global motion of the prey, the complexity of headindicating details, the position of these details and the local motion of legs, are used by the salticids in targeting predatory strikes. A secondary goal was to examine how the predators make decisions when different cues provide contradictory information about the preferred target, a situation naturally occurring in prey possessing ‘false heads’. The use of virtual prey with headindicating details in the trailing part of the body gave us the

opportunity to test whether ‘false heads’ are an effective antipredator adaptation in moving prey or only in stationary prey. METHODS Subjects and Housing The spiders used in this study were freshly emerged juveniles (mean body length: 1.71 ± 0.11 [SD] mm) of Y. arenarius collected from an inland dune in Central Poland (Kwilno, 51
590 N, 19
300 E, Zgierz County). In total, we collected 986 spiders. Collecting was carried out during the first 2 weeks of June, when the spiders left their nests built under the surface of sand (Bartos, 2002b). The search for the spiders started 2 weeks before the expected time of hatching and was based on the knowledge of the spider's biology and life cycle (Bartos, 2005). The spiders were caged individually, used within 2 days in tests and released afterwards in the areas of the dune separated from those where the spiders were collected. Each individual was used only once in the tests. We tested the responses of Y. arenarius to video images of virtual prey possessing different features of their natural prey. We used a method of displaying video playback on a miniature screen, which has proved to be a very successful tool to study visual object recognition in spiders for more than two decades (Dolev & Nelson, 2014; Harland & Jackson, 2002; Nelson & Jackson, 2006, 2012b; Peckmezian & Taylor, 2015). To ascertain whether the virtual prey images were realistic models of the spiders' natural prey we compared the responses of the spiders to two live prey groups: thrips (Thysanoptera) and flies (Diptera), which were the natural prey used to design the virtual prey cues, and to one virtual prey: H þ 4M, which was the most complex virtual prey resembling the natural prey we tested (Fig. 2). About 30% of the spiders (N ¼ 300) from the initial group collected for the experiments approached and attempted to capture the virtual prey or natural prey and only data from these recordings were included in the analyses. Virtual Prey Tests Stimuli consisted of videos of different images created using Macromedia Flash 8 in greyscale (Fig. 2). The images differed with respect to five cues: the presence of head-indicating details (present versus absent), the number of details (zero, one, two, three or four details), the position of details (either on the leading part of the body, marked with ‘þ’, or on the trailing part of the body, marked with ‘’), the local motion of legs (marked with ‘M’) and the presence of horizontal motion (horizontal motion marked with ‘H’ versus lack of horizontal motion marked with ‘V’). Our aim was to compare the reactions of spiders to images that moved along the anteroposterior axis (horizontally) with those without such a motion. However, as motionless images were ignored by the spiders, we used vertical motion imitating a prey raising its body (one bout of up and down movement by 0.5 times the body height every 3 s) in order to attract the spider's attention. The velocity of images

Figure 1. The initial strikes of Y. arenarius on different natural prey captured in the field: (a) fly, (b) wasp, (c) antlion larva. Photo: M. Bartos.

M. Bartos, P. Minias / Animal Behaviour 120 (2016) 51e59

53

Type of global

Position

Number

Local motion

Virtual prey

Virtual prey

motion

of details

of details

of legs

image

acronym

Horizontal (H)

Leading end (+)

4

Yes (M)

H+4M

Horizontal (H)

Leading end (+)

4

No

H+4

Horizontal (H)

Leading end (+)

3

No

H+3

Horizontal (H)

Leading end (+)

2

No

H+2

Horizontal (H)

Leading end (+)

1

No

H+1

Horizontal (H)

No details

0

No

H0

Horizontal (H)

Trailing end (–)

1

No

H–1

Horizontal (H)

Trailing end (–)

2

No

H–2

Horizontal (H)

Trailing end (–)

3

No

H–3

Horizontal (H)

Trailing end (–)

4

No

H–4

Horizontal (H)

Trailing end (–)

4

Yes (M)

H–4M

Vertical (V)

No details

0

No

V0

Vertical (V)

Left (L)

1

No

VL1

Vertical (V)

Right (R)

1

No

VR1

Figure 2. The characteristics of the virtual prey used in the experiments.

moving horizontally was set to 1.05 mm/s. These parameters were selected to maximize the attention of the spiders. Stimuli were based on the characteristics of Chirothrips manicatus (Thysanoptera), hereafter called thrips and Drosophila melanogaster (Diptera), hereafter called flies, which are readily preyed upon by juvenile Y. arenarius in the field and in the laboratory (Bartos, 2004, 2011). The body length to height ratio of the virtual prey was set to 10/1. The body length on the screen was 3.89 mm, which was within the preferred prey size range of juvenile Y. arenarius (Bartos, 2011). The bodies of the virtual prey were elongated ovals with a grey interior and a thin, black outline. The head spot was a black oval (height/width ¼ 1.2) of the same height as the body. The wings were elongated ovals (length/ width ¼ 5.2) with thin black margins, no internal veins, lying flat on the body. Instead of using the minute wings and legs of thrips as a template to draw these details, we used the more visible wings of D. melanogaster, insects readily accepted as prey by salticids (Jackson, 1974). Leg movements in H þ 4M and H  4M prey were based on the movement of fruit fly legs. Legs and antennae were black lines without internal details. The distance between the bottom edge of the body and the substrate in horizontally moving prey was the same in all images irrespective of whether they were with or without legs. Virtual prey images were drawn and subsequently animated using Macromedia Flash 8. To check their visibility and unambiguity the recordings were displayed on the screen of the arena, recorded (using a Canon XL1s camera with Canon 100 mm macro lens) from the perspective that the spiders could see them and assessed with the human eye. The arena used in the experimental set-up (Fig. 3) was a white cardboard cuboid (100 mm high) with an isosceles trapezium as the bottom (250 mm long trapezium legs, 200 mm long wide base, 100 mm long narrow base) and without the top. The screen was made of fine grained matt glass (unmarked type) and mounted in the narrowest wall of the arena. A sheet of white cardboard with a square hole (30  10 mm) cut inside was placed in front of the screen to mask the unnecessary stimuli from behind the screen. As a result, only the rectangular area of the screen was visible for the spider. The cardboard sides of the screen wall folded inwards to cover the corners and evenly disperse the light to avoid distracting

Computer recording behaviour Camera

Computer playing animation

Projector Reducing lens and filters Screen Starting point

Figure 3. The arena (an open-top cuboid with opaque walls) and the projecting equipment used to present Y. arenarius with virtual prey images.

the tested spiders. The bottom of the arena was filled with dry dune sand, which is the natural substrate for Y. arenarius and which was successfully used in earlier studies with the spiders (Bartos, 2008; Bartos & Szczepko, 2012). Near the screen wall the sand surface was level with the bottom of the screen and from that level it gently sloped (at an angle of approximately 10
) to the back of the arena. The starting point, where the tube with the spider was placed at the beginning of the test, was situated 25 mm in front of the screen (equal to about 15 body lengths of the spider). The point was marked with a strip of a millimetre scale glued to a nonflexible tape attached to the rear wall of the arena. The arena was lit with a 100 W incandescent light bulb placed 0.5 m above the surface of the sand. Rendered movies (swf format) were projected (1400  1050 pixels) on to a screen using a SHARP XR-10X-L data projector. The screen was situated about 100 mm from the projector lens and

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M. Bartos, P. Minias / Animal Behaviour 120 (2016) 51e59

slightly higher than the lens. The projector displayed images at an angle of about 10
upwards, which along with the level of sand rising by 10
towards the screen in the arena let the spiders see the animated image on the screen, but made it difficult to see the lamp of the projector, which could possibly distract the spider's attention. Any defocus that resulted from the angle of display was reduced with the vertical keystone effect of the projector. The brightness of the image was controlled by using neutral-density filters placed between the screen and the projector. The size of the image from the projector was initially large and it was subsequently reduced by using a lens placed between the projector and the screen. This approach, also used in other studies (Dolev & Nelson, 2014; Harland & Jackson, 2002; Nelson & Jackson, 2006, 2012b), enabled the display of life-size images in high resolution, which are more realistic for salticids, animals known for their high visual acuities (Land & Nilsson, 2012). The projector was connected to a PC clone computer with Macromedia Flash Player 8, which played the animations. A CCD camera placed 0.5 m above the sand surface and connected to the video card (Matrox Marvel G450 eTV) of another PC clone computer recorded the spider and at the same time the virtual prey on the screen. During the tests the spider was observed on the monitor and was unable to see the experimenter. Testing was carried out between 0900 and 1600 hours (laboratory photoperiod 12:12 h light:dark, lights on at 0700 hours). The laboratory was lit with fluorescent tube ceiling lights located 2 m above the arena. At the beginning of the test the spider was placed in the arena within an opaque plastic tube (80 mm long, inner diameter 8 mm). One side of the tube was sealed with a plug. The tube was placed on the sand and positioned parallel to the screen so that the spider could not see the screen after the plug's removal. This tube position allowed the recording of the moment when the spider faced the screen. The opening of the tube was placed at the starting point in the middle of the arena. In successive trials the tube was directed towards the right or left (the direction was chosen at random). After the plug was removed, the spider could leave the tube. The trial was excluded from the analyses if the spider did not leave the tube within 10 min after plug removal, if the spider jumped out of the tube during plug removal (or jumped afterwards) or if the spider left the arena without noticing the virtual prey. The playback projection started before the spider was released, as the timing of playback initiation may influence the spider's decision (Clark & Uetz, 1992). In the experiments with horizontal motion the virtual prey moved from one side of the screen to the other, disappearing off the screen for 5 s. After this time the virtual prey entered the screen from the same side and moved in the opposite direction. The prey that did not move horizontally (V0, VL1, VR1) performed up and down movements played in a loop. To remove draglines and chemical cues from the spiders used in the previous experiment the surface of sand was brushed between the tests, and a 5 mm thick surface of sand was removed. Next, the arena was refilled with new sand and evened with a wooden tile to the original level. After each test the screen was wiped with a piece of cotton dipped in 95% ethanol and the screen was allowed to dry between trials. No individual was used in more than one test of any one type. Natural Prey Tests In the tests we used C. manicatus and D. melanogaster. The flies were obtained from a laboratory culture. Thrips were collected in the field by sweep netting dune grass on the day of the experiment or the day before then held individually in test tubes. Each prey specimen was randomly chosen for the test. Flies and thrips offered to a spider were within the size range of ±20% of the spider's body length. The virtual prey (H þ 4M) used for the comparison with flies

and thrips was about twice as long. We decided to choose an elongated body for the virtual prey so that we could clearly see which part of the body was attacked and whether the spider performed fronterear observation (i.e. whether or not it alternately oriented towards the two body ends of its prey). We found that the spiders chose similar targets to attack and performed fronterear observation with similar frequency in all three prey groups. The test arena was a white cardboard cylinder (height: 150 mm; diameter: 200 mm) with a 10 mm thick layer of sand on the bottom. The sand was obtained from the same dune where the spiders were collected. An incandescent light bulb (100 W) was placed above the arena, about 500 mm from the sand surface. A CCD camera with a macro lens was positioned above the centre of the arena, about 0.5 m from the surface of the sand. The camera was connected to the video card (Matrox Marvel G450 eTV) of a PC clone computer. The spiders' behaviour was observed on the computer screen. During the test no spider was able to see the experimenter. Laboratory lighting and the time of testing were the same as in the experiments with the virtual prey. At the beginning of the test the spider was placed within the arena, and after 1 min a prey item was introduced 80 mm from the spider. The prey was dropped approximately 30
e40
to the left or right from the spider's anteroposterior axis (position chosen at random) to allow the experimenter to record the moment when the predator faced the prey. To decrease the probability of escape from the arena, before the experiment the prey was kept for 15 min in a refrigerator (5
C), introduced to the arena and left with the spider until the attack or for 5 min. When the spider or the prey climbed the walls of the arena or when the prey escaped the test was aborted and the spider was excluded from successive tests. After each test the surface of sand was brushed, the surface layer was removed and the arena was refilled with sand to a fixed level. No individual was used in more than one test of any one type. Behavioural Analyses Video recordings were analysed frame-by-frame using Lightworks 11.0.3 (www.lwks.com). After calibration with a high-quality scale the distances were measured on the screen in Corel Draw 8.0 using the x- and y-coordinates of the position of the cursor (to the nearest 0.1 mm). We noted whether or not the spider performed fronterear observation, manifested by swivelling the body, which resulted in the spider alternately directing its principal eyes towards the anterior and the posterior ends of the prey's body. In the experiments with virtual prey we determined the point that was stabbed by the spider on the displayed image of the virtual prey, and in the experiments with natural prey we determined the point that was attacked on the body of the prey (hereafter called the target of attack). The target of attack was measured as the distance between the leading edge of the prey's body and the point between the principal eyes of the spider in the frame where the spider stabbed the prey. If the prey did not move horizontally (V0, VL1 and VR1) we measured the distance between the left edge of the body and the point between the spider's principal eyes in the frame where the spider stabbed the prey. For each virtual prey the attacks on the leading and trailing halves of the body were noted (henceforth referred to as ‘attacks on the leading part of the body’ and ‘attacks on the trailing part of the body’, respectively). Statistical Analyses In the analysis of moving prey we used logistic regression with binomial error to test for the effects of the number of details, the position of details, their interaction, the effects of the local motion

M. Bartos, P. Minias / Animal Behaviour 120 (2016) 51e59

of legs and the interaction between the local motion and the position of details on the occurrence of attack on the leading versus trailing parts of the body and for the occurrence of fronterear observation. Nonsignificant (P  0.05) variables were removed using a method of backward removal. The significance of particular effects was assessed with the Wald statistic (W). The strength of the overall association between the predictors in the model was estimated using Nagelkerke's R2 (Nagelkerke, 1991). Logistic regression coefficients (b) and standard errors (b, SE) were used to assess the character and strength of significant relationships. Effect sizes are quoted as odds ratios (OR) with 95% confidence intervals (CI). Since the group of virtual prey lacking any head-indicating details (H0) could not be included in the logistic regression analysis due to limitations in the model structure, we used the G test to compare the responses of spiders to this kind of prey with prey possessing details in the leading part of the body (all categories combined). The G test was also used to test the responses of spiders to virtual prey (H þ 4M) and natural prey (thrips, flies), as well as to test the frequency of fronterear observation in the virtual prey lacking horizontal motion (V0, VL1, VR1). Binomial tests were used to check the distribution of strikes on prey that did not move horizontally (V0, VL1, VR1). All values are presented as means ± SD. All analyses were performed using STATISTICA 10.0 software (Statsoft, Tulsa, OK, U.S.A.). Ethical Note We followed the ASAB/ABS guidelines for the ethical treatment of animals. After the study all spiders were released in the area where they had been collected. RESULTS

55

P ¼ 0.010; Fig. 4). The odds of attacking the trailing part equipped with head-indicating details increased 1.6-fold (CI: 1.1e2.2) with each additional detail. The local motion of legs (b ¼ 1.81 ± 2.57, W ¼ 0.49, P ¼ 0.481) and the interaction between the local motion and the position of details (b ¼ 0.43 ± 0.32, W ¼ 1.80, P ¼ 0.180) were nonsignificant and excluded from the model. The reduced model fitted the data well (c21 ¼ 61.35, P < 0.0001, Nagelkerke R2 ¼ 0.39). Horizontal Motion Present, No Details To test whether motion direction is a sufficient cue for proper targeting of an attack when head-indicating details are absent we compared the frequency of attacks on the virtual prey lacking any details (H0) with the virtual prey possessing details in the leading part of the body. We found that the spiders attacked the leading part in all these prey with similar frequency (Fig. 4) regardless of the presence or absence of details in the leading part (G1 ¼ 0.64, P ¼ 0.423). No Horizontal Motion, Head Spot Present Spiders attacking the prey that did not move horizontally (N ¼ 10) jumped upon the body end with the head spot (binomial test, null expectation 1:1: P < 0.001) regardless of whether the spot was on the left (VL1) or on the right end of the body (VR1). The strikes were distributed within the 4% and 16% range of the relative body length on either side of the body. No Horizontal Motion, No Head Spot

The spiders used in the experiments with the virtual prey showed a normal sequence of predatory behaviours observed with the natural prey. The spiders oriented towards prey images, approached with short pauses, during which some spiders performed fronterear observation, and finally jumped, attacking the virtual prey displayed on the screen.

To exclude the possibility that the spiders perceived only the head spot without seeing the whole body we tested a group of spiders (N ¼ 8) against the virtual prey lacking any details (V0). In seven instances the spiders attacked either the left or right end of the body (within 25%-long sections on either side of the body). One spider struck within the remaining 50% area in the body centre. The tendency for targeting body ends was statistically significant (binomial test, null expectation 1:1: P < 0.04).

Target of Attack

FronteRear Observation

The spiders directed all strikes to the ends but not to the centre of the body, regardless of the presence of horizontal motion, the position of details, the number of details and the local motion of legs. All horizontally moving virtual prey were struck within 2e16% and 82e95% of the relative body length. The target of attack on the most complex virtual prey with details in the leading part of the body, H þ 4M (N ¼ 20), and on the natural prey, thrips (N ¼ 26) and flies (N ¼ 28), was similar (G2 ¼ 0.99, P ¼ 0.611).

Fronterear observation was common when head-indicating details occurred in the trailing part of the body, but rare when the same details occurred in the leading part, when there were no details or when the prey was natural. There were no differences in the frequency of fronterear observation between the most complex virtual prey with details in the leading part (H þ 4M) and the natural prey used to design this virtual prey (thrips and flies; G2 ¼ 0.99, P ¼ 0.611). Fronterear observation occurred once when the spiders approached H þ 4M (N ¼ 20) and once when they approached thrips (N ¼ 26), but it was absent when the spiders approached flies (N ¼ 28).

Horizontal Motion Present, Details Present We found that in horizontally moving prey both the position (b ¼ 2.63 ± 0.66, W ¼ 16.04, P < 0.001) and the interaction between the position and the number of details (b ¼ 0.22 ± 0.09, W ¼ 6.76, P ¼ 0.009) significantly predicted which body part (leading versus trailing) the individuals would strike (Fig. 4). When details (regardless of their number) occurred in the leading part of the body the odds of attacking precisely this part were 14 times larger (CI: 3.8e51.0) than the odds of attacking the trailing part of the body. In the leading part the number of details did not affect the choice of target (b ¼ 0.19 ± 0.53, W ¼ 0.13, P ¼ 0.714), while the increasing number of details in the trailing part elicited more frequent attacks in the trailing part (b ¼ 0.45 ± 0.17, W ¼ 6.63,

Horizontal Motion Present, Details Present Only the position of details affected the frequency of fronterear observation (b ¼ 3.25 ± 0.63, W ¼ 27.01, P < 0.0001; Fig. 5). When details were present in the trailing part of the body, the odds of occurrence of fronterear observation were 23 times larger (CI: 8.1e69.8) than in the situation when details were present in the leading part of the body. The number of details (b ¼ 0.13 ± 0.15, W ¼ 0.74, P ¼ 0.389), the local motion of legs (b ¼ 1.28 ± 2.72, W ¼ 0.22, P ¼ 0.638), the interaction between the number and the position of details (b ¼ 0.16 ± 0.52, W ¼ 0.09, P ¼ 0.760) and the

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M. Bartos, P. Minias / Animal Behaviour 120 (2016) 51e59

100

N=20

N=17

N=21

N=19

N=22

N=23

N=24

N=23

N=18

N=19

N=22

H+4M

H+4

H+3

H+2

H+1

H0

H–0

H–2

H–3

H–4

H–4M

Attacks (%)

80 60 40 20 0

Prey type Figure 4. Attacks on the leading (grey bars) and on the trailing (black bars) parts of the body of the virtual prey possessing a different number of details in the leading parts (H þ 4M, H þ 4, H þ 3, H þ 2 and H þ 1), in the trailing parts (H  1, H  2, H  3, H  4 and H  4M) and the virtual prey lacking details (H0). The leading parts of the body are the left ends of the pictograms. In H þ 4M and H  4M the legs moved; in other prey the legs were still. N is the number of spiders that attacked the prey.

Front–rear observation (%)

100

N=20

N=17

N=21

N=19

N=22

N=23

N=24

N=23

N=18

N=19

N=22

H+4M

H+4

H+3

H+2

H+1

H0

H–0

H–2

H–3

H–4

H–4M

80 60 40 20 0

Prey type Figure 5. Fronterear observation elicited in response to virtual prey possessing details in the leading parts of the body (H þ 4M, H þ 4, H þ 3, H þ 2 and H þ 1), in the trailing parts of the body (H  1, H  2, H  3, H  4 and H  4M) and to virtual prey lacking details (H0). The leading parts of the body are the left ends of the pictograms. The remaining (unplotted) percentage depicts the lack of fronterear observation. In H þ 4M and H  4M the legs moved; in other prey the legs were still. N is the number of spiders that attacked the prey.

interaction between the local motion and the position of details (b ¼ 0.36 ± 0.34, W ¼ 1.13, P ¼ 0.289) were nonsignificant. The reduced model fitted the data well (c21 ¼ 63.30, P < 0.0001, Nagelkerke R2 ¼ 0.38). Horizontal Motion Present, No Details To test whether the lack of details affects how the spiders inspect the prey before the strike we compared the frequency of fronterear observation of the virtual prey lacking any details (H0) with that of the virtual prey possessing details in the leading parts of their bodies. Fronterear observation occurred with a similar low frequency in both groups (G1 ¼ 0.01 ± 1.14, P ¼ 0.952; Fig. 5). No Horizontal Motion, Head Spot Present Versus Absent Fronterear observation was observed in one of 10 spiders that approached VL1 and VR1 prey with head spots and in two of eight spotless prey (V0), which resulted in the lack of differences related to the presence of the head spot (G1 ¼ 0.36, P ¼ 0.548).

DISCUSSION In this study we demonstrated that Y. arenarius used both the direction of motion and the head-indicating details when identifying the position of their preferred target. When one of the cues was missing, the spiders based their decisions on the other cue. For example, while attacking the virtual prey that did not move horizontally, the spiders used the position of the head spot, and while attacking the virtual prey that lacked details, the spiders used only motion direction. When all cues provided coherent information, as in the experiments with H þ 4M, H þ 4, H þ 3, H þ 2 and H þ 1 virtual prey, the decisions based on the simple cues were the same as those based on the more complex patterns. In all these cases the spiders occasionally used fronterear observation, which suggests that they did not search for additional cues. It seems that as long as the perceived cues provided simple, but coherent information the spiders did not attempt to verify it. It is likely that making decisions about the target of attack based on patchy cues may be common in nature, e.g. when predators cannot see the whole prey because it is partially concealed or because a more thorough visual inspection may increase the risk of the prey escaping.

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We demonstrated that motion direction was a salient cue, sufficient to identify a preferred target even when configurational cues were missing. The spiders struck the same parts of the body when details were present in the leading part and when details were lacking. Moreover, the distributions of all the strikes on these virtual prey were very similar. These findings suggest that the details were not necessary to precisely identify the preferred area, which supports the role of motion direction as an important indicator of body orientation. Motion was already known to be an essential cue used by predators; however, until now its role was resolved only in the early stages of predation (during prey detection and discrimination between prey and nonprey), but not in other predatory tasks (Bednarski et al., 2012; Ingle & McKinley, 1978; Kral & Prete, 2004; Prete, Hurd, Branstrator, & Johnson, 2002; Yamawaki, 1998, 2000, 2003). There have been numerous observations of predators responding to various shapes that are rough approximations of their natural prey, but only if these objects were moving. For example, toads, mantids and salticids attempted to capture horizontally moving, elongated rectangles lacking any details as if they were valid prey (Bednarski et al., 2012; Ewert, 2004; Kral & Prete, 2004). Moreover, various authors have reported that moving objects of different shapes, often not resembling salticid prey at all, including squares, circles, triangles, crosses, spheres of different sizes and small balls of paper, were approached and captured by nonspecialized salticids (Bednarski et al., 2012; Dill, 1975; Drees, 1952; Forster, 1979; Heil, 1936; Zurek et al., 2010). All these findings stress the role of motion in prey detection, but apart from this function, global motion also provides information about the orientation of the moving animal and the position of its head and tail and is thus an important cue for a predator before the strike. Bilateral animals typically move head on, which is a result of cephalization with all its consequences pertaining to the position of mouthparts, sensory and locomotor structures. Therefore, motion direction seems to be typically a credible indicator of prey orientation indicating the position of the head and tail areas. It seems, however, that global motion may not always provide credible information about the actual body orientation. There is a range of circumstances when animals move backwards (at least for short distances) withdrawing or performing alternate forward and backward movements, e.g. digging a nesting hole, tearing out a piece of food from a larger part, interacting with conspecifics, or in other activities. These examples suggest that prey details may also be salient cues in targeting predatory strikes, and when the prey is still, they become the only cues indicating body orientation of the observed prey. We demonstrated that prey details provide salticids with another salient cue about the target of strike. We have also shown that more complex biologically relevant details are viewed by the spiders as a more likely target than a simpler pattern. This study provides evidence that prey details are used by nonspecialized salticids, while previous studies have stressed the reliance on details only in specialized salticids, such as Portia and E. culicivora (Harland & Jackson, 2000, 2002; Nelson & Jackson, 2012a, 2012b). In contrast to these specialized salticids relying heavily on prey details, the nonspecialized salticids have generally been portrayed as limited in their use of details (Bednarski et al., 2012; Freed, 1984; but see ; Drees, 1952) and they have been likened to predators that rapidly classify objects as prey, such as toads and mantids (Bednarski et al., 2012). The most convincing arguments supporting this assumption come from a recent study in which the authors tried to ascertain the use of details by Phidippus audax (Bednarski et al., 2012). The spiders were presented with manipulated videos depicting a moving cricket, a motionless cricket, a snapshot of a cricket that moved across the screen with the same global motion pattern as the natural cricket and a rectangle of the same size and

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colour. One of the major findings was that the spiders were unable to distinguish between the moving snapshot of a cricket and the moving rectangle that lacked the interior detail. The result remained unchanged after applying aversive conditioning to train the spider to avoid a favoured stimulus. Apparently these findings seem to be at odds with our results, which suggest that the ability of Y. arenarius, a salticid similar in many aspects to P. audax, to rely on details is different to that of P. audax. There are, however, two important differences between the experiments, which point to the possible causes of these distinct findings. First, in the study with P. audax the average velocity of the object was 20 times higher than the velocity used in this study with Y. arenarius. Therefore, it seems likely that the responses of P. audax were mediated by the lowerresolution anterior-lateral eyes typically used by salticids during the orientation, chasing and attacking of quickly moving prey (Land, 1985; Zurek & Nelson, 2012; Zurek et al., 2010), while the responses of Y. arenarius were possibly mediated by the highresolution principal eyes used during the approach to slowly moving or motionless prey (Harland et al., 2012; Land, 1969a; Williams & McIntyre, 1980). Lastly, the differences between the studies may also result from the different predatory tasks being completed by the spiders in the two studies. Phidippus audax was used to discriminating between prey and nonprey, which requires reliance on motion and on the proportions of the observed object, as suggested by the studies on toads and mantids (Ewert, 2004; Kral & Prete, 2004). Using Y. arenarius we analysed a different predatory task, namely one that required precise identification of a particular region on the body of the prey, and we found that, among other cues, the task can be completed using head-indicating details. Therefore, our findings suggest that, at least some nonspecialized salticids are not entirely limited in their use of details, but they may rely on some prey details only during particular predatory tasks and not others. The spiders used both motion direction and details, but it seems that the cues were treated differently, with motion direction having a greater weight than at least some of the details. This unequal weighting might be accounted for by the different propensities to strike opposite body parts in the prey lacking details and the prey with details in the trailing body parts, where the increasing number of strikes in the trailing part resulted from the growing complexity of head-indicating details in that part. More complex patterns with three or four details in the trailing part and moving legs elicited a similar number of strikes in that part of the body in comparison to the cue from motion direction pointing to the opposite body end, while a head spot alone located on the trailing body end attracted about 20% of strikes. Interestingly, the most complex pattern with a head spot, antennae, wings and legs did not significantly outweigh the cue from motion direction pointing to the opposite body end. However, whether this was the result of the higher weight of motion direction, the lower weight of particular details or the fact that the tested details were not as realistic as in the natural prey cannot be answered in this study. Interestingly, another generalist salticid, Hypoblemum albovittatum showed significantly shorter decision times and a stronger preference for detailed ‘realistic’ images of flies over the abstract images (Dolev & Nelson, 2016), which may suggest that the degree of complexity of the details we used and their limited ‘realism’ might have influenced the decisions of Y. arenarius. Our study also has implications for understanding the role of details forming ‘false heads’ in motionless and moving prey, as some virtual prey we used were equipped with cephalic and thoracic details in the posterior body ends. Until now the complexity of different structures and markings forming ‘false heads’ have only been tested in motionless prey (reviewed in Ruxton, Sherratt, & Speed, 2004), particularly in various motionless

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butterfly lures possessing ‘false heads’ or those where such ‘false heads’ were artificially added. For example, in one study, blue jays, Cyanocitta cristata, were presented with experimentally modified dead cabbage butterflies, Pieris rapae, differing with respect to the presence of wing tails, eyespots and lines converging in the anal angle of the butterfly hindwing. The birds biased their attacks to the hind area of the wing, where the ‘false head’ pattern occurred (Wourms & Wasserman, 1985). A number of other studies have stressed the role of ‘false heads’ as antipredator adaptations, but no study has dealt with the question of whether complex ‘false heads’ lose their protective value when the prey animals are in motion (Ruxton et al., 2004). Only one study reports that when the background closely matches the coloration of a quickly moving fake stoat, even a single contrasting spot on the tip of its tail can redirect the attack of a hawk (Powell, 1982), which suggests that in some circumstances deflection can be an adaptive antipredator strategy also for moving prey. Our study provides the first experimental evidence of the efficacy of ‘false head’ details, stressing the role of ‘false head’ complexity in redirecting a predator's attack on moving prey. Horizontal motion significantly reduced the efficacy of even the most complex ‘false heads’ that we used, while the lack of such motion turned even a single head spot into an effective deflecting structure attracting all predatory strikes. This suggests that deflection should be more effective and possibly more common among animals that tend to remain stationary (at least at the moments when they become particularly vulnerable to attack, while feeding or resting) rather than among those that actively move about. This assumption seems to gain some support from the occurrence of deflection in different ecological groups, as it is the most widespread phenomenon reported in nectar-drinking, sapdrinking or other herbivorous insects, mainly butterflies: lycaenids and satyrids (Robbins, 1980, 1981; Van Someren, 1992; Wickler, 1968), riodinids (DeVries, 1997), nymphalids (Lyytinen, Brakefield, €m, & Mappes, 2004; Lyytinen, Brakefield, & Mappes, Lindstro 2003; Tonner, Novotny, Leps, & Komarek, 1993) and leafhoppers (Edmunds, 1974). It is far less common among other taxa, particularly those that locomote a lot (Ruxton et al., 2004). It has been claimed that the occurrence of deflection in the animal kingdom is highly underestimated (Ruxton et al., 2004). Taking into account the results of this study, particularly the observation that even a single head spot may effectively deflect a predatory attack, it seems likely that various deflective structures or markings not so obvious to the human eye may be much more widespread than those already reported. The efficacy of the relatively crude patterns we used to elicit predatory strikes also suggests that, if Y. arenarius, an efficient visual hunter, can be easily misled about where to strike, it is very likely that predators with much lower visual acuities may be deceived by prey with simple ‘false heads’. Acknowledgments We thank Zbigniew Wojciechowski for stimulating discussions throughout this project and two anonymous referees for helpful comments. We also thank Jerzy Krysiak for his help designing the displaying module of the experimental set-up and Bartłomiej Dana, Michel Mabiki, Paulina Karwalska and Wioleta Gruszka for technical assistance. The work was supported in part by the University
d
of Ło z and by the Polish Ministry of Scientific Research and Information Technology grant (SCSR 6P04F07215) to M.B. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.anbehav.2016.07.021.

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