Perception of Ultraviolet Light by Crab Spiders and Its Role in Selection of Hunting Sites
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J Comp Physiol A (2009) 195:409–417 DOI 10.1007/s00359-009-0419-6 ORIGINAL PAPER Perception of ultraviolet light by crab spiders and its role in selection of hunting sites Ramachandra M. Bhaskara Æ C. M. Brijesh Æ Saveer Ahmed Æ Renee M. Borges Received: 22 November 2008 / Revised: 19 January 2009 / Accepted: 23 January 2009 / Published online: 24 February 2009 Ó Springer-Verlag 2009 Abstract The perception of ultraviolet (UV) light by spi- 1995; Briscoe and Chittka 2001). Among invertebrates, UV ders has so far been only demonstrated in salticids. Crab sensitivity is an ancient trait and is known in many insects spiders (Thomisidae) hunt mostly on flowers and need to find including honeybees (Briscoe and Chittka 2001; Kevan appropriate hunting sites. Previous studies have shown that et al. 2001). The importance of visual signals or cues, some crab spiders that reflect UV light use UV contrast to especially in the UV range, in either legitimate communi- enhance prey capture. The high UV contrast can be obtained cation or sensory exploitation has been of considerable either by modulation of body colouration or active selection interest in both invertebrates and vertebrates (Endler 1993). of appropriate backgrounds for foraging. We show that crab The role of UV in mate choice has been demonstrated in spiders (Thomisus sp.) hunting on Spathiphyllum plants use taxa as diverse as butterflies (Papke et al. 2007), jumping chromatic contrast, especially UV contrast, to make them- spiders (Lim et al. 2007, 2008), birds (Cuthill et al. 2000; selves attractive to hymenopteran prey. Apart from that, they Hausmann et al. 2003), and reptiles (Fleishman et al. are able to achieve high UV contrast by active selection of 1993). The perception of UV also plays a prominent role in non-UV reflecting surfaces when given a choice of UV- predator–prey interactions in varied taxa (Chittka 2001; reflecting and non-UV reflecting surfaces in the absence of Franks and Noble 2004;Ha˚stad et al. 2005) including the odour cues. Honeybees (Apis cerana) approached Spathi- selection of hunting sites in jumping spiders (Li and Lim phyllum plants bearing crab spiders on which the spiders 2005). Therefore UV perception could have important were high UV-contrast targets with greater frequency than impacts on predator–prey interactions in other spider taxa those plants on which the UV contrast of the spiders was low. also, such as in crab spiders (Thomisidae). However, the Thus, crab spiders can perceive UV and may use it to choose perception of UV by spiders has only been shown in sal- appropriate backgrounds to enhance prey capture, by ticids (De Voe 1975; Lim and Li 2006) to date, although exploiting the attraction of prey such as honeybees to UV. UV receptors have been found in ctenids (Walla et al. 1996). Whether thomisids can perceive UV has not been Keywords Chromatic contrast Á Sensory ecology Á demonstrated. Sensory exploitation Á Sensory trap Á Visual ecology Crab spiders are usually ambush predators on flowers, and attack butterflies, bees and other floral visitors (Lovell 1915). They can influence pollinator visitation to flowers Introduction (Dukas and Morse 2005) by exploiting the sensory biases of prey (Heiling et al. 2006). In keeping with their sit-and- Many animals are sensitive to ultraviolet (UV) light. This wait life style, some thomisids spend considerable amounts seems to occur in almost all taxonomic groups (Tove´e of time well camouflaged on flowers, blending with their backgrounds (Chittka 2001). Some of them even change colour to match their background (Oxford and Gillespie & R. M. Bhaskara Á C. M. Brijesh Á S. Ahmed Á R. M. Borges ( ) 1998). To date there exist reports of two strategies used by Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560 012, India crab spiders to ambush hymenopteran prey. The European e-mail: [email protected] crab spider Thomisus onustus appears cryptic to prey as 123 410 J Comp Physiol A (2009) 195:409–417 well as their own predators, i.e. birds, by merging with the of the Indian Institute of Science, Bangalore, India background (The´ry and Casas 2002; The´ry et al. 2005). On (12°580N and 77°350E). These exotic aroids are planted in the other hand, the high chromatic contrast, especially UV dense clumps within flower beds. We classified the contrast, of the Australian crab spider Thomisus spectabilis development of the Spathiphyllum inflorescence into five (Heiling et al. 2003; Heiling and Herberstein 2004) and of stages (Fig. 1a). Misumena vatia (Greco and Kevan 1994) is effective in Phase A A small bud is present at the end of the attracting prey and may thus exploit the UV sensitivity of peduncle; the spathe is not yet opened their hymenopteran prey (Heiling et al. 2003). The choice Phase B The spathe is open and bright white in colour, of hunting site by spiders could be a hard-wired pheno- but the flowers are not yet developed menon or a consequence of learning. Crab spiders could Phase C The flowers are mature, the anthers have use visual, olfactory and/or tactile cues to find hunting sites dehisced, and pollen can be observed adhering (Morse 1988; Aldrich and Barros 1995; Chien and Morse to the spadix (i.e. cone) 1998; Heiling et al. 2004). Their foraging decisions could Phase D The flowers are pollinated, the cone appears also be affected by past experiences and floral condition dark and the spathe is turning green (Morse 2000a, b). While the effectiveness of chromatic Phase E The spathe and cone are completely green and contrast, especially of the UV component, has been dem- fruit formation is complete onstrated in thomisid–prey interactions (Heiling et al. 2003, 2005a, b, 2006; Heiling and Herberstein 2004), Throughout this paper, cone refers to the inflorescence whether crab spiders can perceive UV and can use this of the plant, while the word spathe (unless specified) may information in choosing backgrounds that would allow be used to refer to the cone ? leaf-like parabolic structure, themselves to be maximally detected against the back- as when referring to B or C spathes, for example. Spiders ground and also make themselves highly attractive to prey hunt only on the cones. is not known. To determine if white crab spiders (Thomisus sp.) In this paper we investigate the visual ecology of the preferentially select spathes of a particular phase as hunting crab spider Thomisus sp. on Spathiphyllum plants. These grounds, we collected observational data on the natural plants have spadix inflorescences which are sites with a presence of adult crab spiders on the cones of the five high frequency of hymenopteran and dipteran prey visits. phases of spathes. We also recorded the abundance of We study the effect of spathe development and corre- spathes in these phases. Observations were made over three sponding changes in visual parameters of the 24-h periods, with individual inflorescences in a patch inflorescence on the utilisation of inflorescences as hunt- being examined for the presence of spiders at three-hourly ing sites by crab spiders. We specifically examine the role intervals. of spectral reflectance differences between the spider and inflorescences in aiding spider choice of a hunting site Spectral reflectance of spiders and Spathiphyllum using the spectral sensitivities of the honeybee (Apis mellifera) as a generic prey taxon. We show by a choice The spectral reflectances (300–700 nm) of Spathiphyllum experiment that crab spiders can perceive the difference and crab spiders (Thomisus sp.) were measured using a between a UV-reflecting and a non-UV reflecting back- S2000 Ocean Optics spectrometer with a DT-MINI deu- ground and preferentially select the background that will terium-tungsten-halogen light source attached to a generate maximum contrast. We further demonstrate that computer running OOIBase32TM spectrometer operating honeybees (A. cerana) approach with greater frequency software (Ocean Optics, Dunedin, FL, USA). Relative those Spathiphyllum surfaces bearing crab spiders where reflectance spectra were recorded using an Ocean Optics the spiders have high UV-contrast compared to those with WS-1 white barium sulphate standard. Measurements lower UV-contrast, thus clearly revealing the adaptive were taken from cone, inner and outer surfaces of significance of the background selection strategy of the spathes, pedicel and leaf of the Spathiphyllum for each of spiders. the five phases; however, only values for the cones are reported here since spiders hunt only on this part, and move to the leaf-like portion only after prey capture Materials and methods (Fig. 1b). Adult crab spiders occupying B and C spathes of Spathiphyllum plants were collected for measurements. Study site and animals Reflectance spectra of spiders were recorded from pro- soma and opisthosoma separately. Ten replicates were We studied white crab spiders Thomisus sp. present on recorded for spiders and for each phase of the Spathi- Spathiphyllum (Araceae) inflorescences within the campus phyllum plants. 123 J Comp Physiol A (2009) 195:409–417 411 Flowers Spathe just Bud mature. opened. a stage. Anthers Flowers b Spathe dehisced. not immature. opened. Pollinated. Fruit Spathe and formed. cone Green turning spathe. green. A B C D E 5cm 1cm c d 100 45 80 60 40 Reflectance (%) 20 Chromatography paper Chromatography paper + Fool-a-bird 0 300 400 500 600 700 800 Wavelength (nm) Fig. 1 a Phases of spathe development (A–E) in Spathiphyllum; spectra of the UV-reflecting surface (chromatography paper) and non- classification based on external morphology and colouration. b White UV reflecting surface (chromatography paper ? Fool-a-bird) after crab spider (Thomisus sp.) preying on A. cerana on Spathiphyllum c lamination showing the decrease in the UV reflectance of the Sketch of the experimental set-up for the choice tests.