1425

The Journal of Experimental Biology 213, 1425-1435 © 2010. Published by The Company of Biologists Ltd doi:10.1242/jeb.039743

Background colour matching by a crab in the field: a community sensory ecology perspective

Jérémy Defrize1,*, Marc Théry2 and Jérôme Casas1 1Institut de Recherche sur la Biologie de l’Insecte, Université François Rabelais de Tours, CNRS UMR 6035, 37200 Tours, France and 2Département d’Ecologie et de Gestion de la Biodiversité, Muséum National d’Histoire Naturelle, CNRS UMR 7179, 91800 Brunoy, France *Author for correspondence ([email protected])

Accepted 13 January 2010

SUMMARY The question of whether a species matches the colour of its natural background in the perspective of the correct receiver is complex to address for several reasons; however, the answer to this question may provide invaluable support for functional interpretations of colour. In most cases, little is known about the identity and visual sensory abilities of the correct receiver and the precise location at which interactions take place in the field, in particular for mimetic systems. In this study, we focused on , a crab spider meeting the criteria for assessing crypsis better than many other models, and claimed to use colour changes for both aggressive and protective crypsis. We carried out a systematic field survey to quantitatively assess the exactness of background colour matching in M. vatia with respect to the visual system of many of its receivers within the community. We applied physiological models of bird, bee and blowfly colour vision, using flower and spider spectral reflectances measured with a spectroradiometer. We observed that crypsis at long distance is systematically achieved, exclusively through achromatic contrast, in both bee and bird visions. At short distance, M. vatia is mostly chromatically detectable, whatever the substrate, for bees and birds. However, can be either poorly discriminable or quite visible depending on the substrate for bees. Spiders are always chromatically undetectable for blowflies. We discuss the biological relevance of these results in both defensive and aggressive contexts of crypsis within a community sensory perspective. Supplementary material available online at http://jeb.biologists.org/cgi/content/full/213/9/1425/DC1 Key words: background colour matching, bee vision, mimetism, crab spider, Misumena vatia, crypsis, sensory ecology.

INTRODUCTION and colour discrimination thresholds have been studied in detail in Crypsis through background matching has been reported for a wide only a few species, including bird and bee species (Menzel and range of , including both vertebrates and invertebrates Backhaus, 1989; Vorobyev and Osorio, 1998; Hart et al., 2000). (Marshall, 2000; Ruxton et al., 2004; Mäthger et al., 2008; Stuart- Moreover, cryptic animals are rarely caught in the act of either Fox et al., 2008). Background matching is defined as a strategy catching prey (for cryptic predators) or escaping detection (for preventing detection by changing the colour and patterning of the cryptic prey). As a corollary, the location at which the interaction body to match those of the background (Stevens and Merilaita, occurs is known only imprecisely and is described in broad, generic 2009). Many species have been described as cryptic on the basis of terms (e.g. ‘rocks’, ‘grasses’). This may be problematic in cases in human vision but colour contrast, which involves both chromatic which the substrate colour and patterns vary over short distances and/or achromatic contrasts, has rarely been tested from the within the range of habitat use of the cryptic species. A survey of perspective of the usual receiver and in natural conditions (Stevens the literature shows that, unlike most background-matching species, and Merilaita, 2009). There are several reasons for this lack of data: crab spiders, including the species we will focus on, Misumena vatia (i) the correct prey and/or predators of the ‘cryptic’ organism may (Araneae, ), meet the criteria for addressing questions not yet be clearly identified, (ii) the assessment of chromatic and/or of this kind better than many other models (Théry et al., 2010). achromatic contrast(s) in the prey/predator visual system requires They are mainly sedentary and are found in large numbers on knowledge of the physiological basis of both types of contrasts in flowers. Moreover, one of the main prey of the crab spiders such the species concerned, particularly in terms of the number and nature as M. vatia, besides flower-visiting , is foraging bees (see of the different photoreceptor types. These physiological works must TableS1 and TableS2 in supplementary material), the colour vision be supplemented by (iii) behavioural studies, which are also required of which has been studied in detail. to determine not only whether true colour vision and colour blind Misumena vatia has been studied for more than a century, due mechanisms are used by an observer but also the colour to their amazing ability to be the same colour as the colour of some discrimination thresholds. True colour vision is the ability to of the flowers on which they hunt (Heckel, 1891; Weigel, 1941; discriminate between two lights of different spectral compositions, Insausti and Casas, 2008; Insausti and Casas, 2009) (reviewed in regardless of their relative intensity (Kelber et al., 2003), and colour Théry and Casas, 2009). This apparent colour matching is discrimination threshold is defined as the lowest contrast between particularly spectacular because it involves a change in the colour two stimuli that can be detected by an observer. Spectral sensitivities of the entire body from white to yellow (and back) over the space are known for a wide range of species but both true colour vision of a few days, depending on the colour of the flower (Weigel, 1941;

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1426 J. Defrize, M. Théry and J. Casas

Théry, 2007). It is widely assumed that this apparent flower Misumena vatia goes through seven juvenile instars, the first of matching is not only a form of aggressive against - which is spent in the egg sac (Gertsch, 1939). We captured spiders and -feeding prey but also a form of defensive mimicry, with a prosoma size ranging from 1mm (fourth juvenile instar) to especially against birds. This is an assumption, as exceedingly few 3mm (adults). Total size (prosoma + ) varied between bird attacks have been reported so far, despite intense sampling of 2.5mm and 12mm. Second and third instar spiders were not gut contents (Bristowe, 1971) and decades of long field work (Morse, captured, as their abdomen dimensions were smaller than the 2007). Studies with bee physiological vision models recently diameter of the optic sensor. We collected 75% (110/146) of the revealed that M. vatia can produce both chromatic and achromatic spiders studied on ‘white’ flowers whereas only 18% were caught contrasts well below the discrimination thresholds of their on ‘yellow’ flowers and 7% on ‘red’ and ‘blue’ flowers. This Hymenopteran prey (Chittka, 2001). At first sight, these results are heterogeneity did not result from a sampling bias. Indeed, large thus consistent with the above hypothesis of crypsis against prey. numbers of ‘yellow’-flowered species were carefully inspected However, chromatic and achromatic matching have been without the detection of M. vatia. Among these 146 spiders, 20 were quantitatively assessed in M. vatia on two flower species only found only once or twice on a specific flower species. We decided (Chaerophyllum temulum and Senecio vernalis) (Chittka, 2001) and that only flower species on which at least five spiders were found for two individual spiders only. Misumena vatia, however, has been would be included in the analysis. Thus, crypsis in the perspective detected on a much wider range of flower species in the field of the receivers was analysed on 126 spiders found on six flower (Heckel, 1891; Rabaud, 1923; Weigel, 1941). Moreover, crab species. Spiders hunting on Filipendula ulmaria Maximowicz 1879 spiders ambush numerous prey species (Fig.1), with different (‘Meadow sweet’) and Senecio sp. L. (‘Ragwort’) were collected visual abilities. from homogeneous patches, consisting of single flower species We therefore carried out a systematic field survey in a given whereas spiders found on Achillea millefolium L. (‘Common geographical region, using a statistical test, to produce a quantitative yarrow’), Heracleum sphondylium L. (‘Common hogweed’) and assessment of the exactness of the colour matching of M. vatia on Cleome spinosa L. (‘Spiny spiderflower’) were collected from all flower species on which spiders were observed, with respect to heterogeneous patches, consisting of at least two flower species. the visual system of not only their main putative predator, Leucanthemum vulgare Lamarck 1779 (‘Oxeye daisy’) was the only insectivorous birds, but also their main prey, bees and flies. plant species from which spiders were collected in both homogeneous and heterogeneous patches. Spiders were caught in MATERIALS AND METHODS eight different patches. The smallest patch had an area of 20m ϫ Spider and flower collection 20m. All of the spiders collected were found on the flower petals. Juvenile and adult female Misumena vatia Clerck 1757 crab spiders were collected from all of the flower species on which M. vatia was Spectroradiometric measurements observed at various sites in the surroundings of Tours (47°20Ј18ЉN, We measured the reflectance of both spiders and flowers with a 00°42Ј52ЉE), France, from April to October, in 2007 and 2008. All spectroradiometer (Avantes Avaspec 256, Eerbeek, The Netherlands) of the flowers of each patch were carefully inspected to prevent and a deuterium–halogen lamp (Avantes Avalight D/H-S) emitting sampling bias. Once caught, the spiders and the flowers on which light of wavelengths between 215nm and 1100nm. Reflectance was they were sitting were placed in a plastic box with a piece of damp expressed relative to a 99% (300–700nm) reflectance standard. A cotton wool and transferred to the laboratory. We measured the reference reading was taken, and dark current calibration was carried reflectance of the spiders and the flowers on the same day. We also out before taking the measurements for each spider and each flower. measured the length of the prosoma to test whether a relationship An optic fiber sensor 1.5mm in diameter and equipped with a quartz between the stage of development and the contrasts on the substrate window cut at a 45deg. angle was used. Spiders were anesthetised occurred in the field. with CO2 before recordings of the reflectance spectrum of the

Fig.1. Schematic representation of both multi-substrate and multi-receiver communities considered in this study. From left to right: Halictus sp. (solitary bees), Episyrphus sp. (Syrphid flies), (bees), Apis mellifera (bees), Lucilia sp. (blowfly) and blue tit (Passeriformes). The represented abstract flower colour types on which Misumena vatia can be found are at the bottom.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Background matching by a crab spider 1427 abdomen were taken (Fig.2A). Spiders and flowers were placed on to date. In the following, we present the colour computation in the a flat mounting stand for measurements. We assessed both chromatic bee visual system first, followed by the bird vision system. The and achromatic contrasts of each spider, by measuring the reflectance colour vision model, which is very different, is presented last. of the exact part of the flower on which M. vatia was found The quantum catch Q for a given spectrum in the respective (Fig.2B–D). We obtained three reflectance spectra for each abdomen photoreceptor i is calculated as: and for each flower. A mean reflectance spectrum was then 700 calculated for each spider and each flower. Qi = ∫ Ri (λ)S(λ)I(λ)dλ , (1) 300 Modelling chromatic and achromatic contrasts in both bee and bird visual systems where Ri is the spectral sensitivity function of the (UV), We measured the chromatic and achromatic contrasts created by Blue (B) and Green (G) receptors for trichromatic bees with M. vatia against its substrate using the physiological model sensitivity peaks at 340nm, 435nm and 540nm, respectively developed by Vorobyev and Osorio (Vorobyev and Osorio, 1998; (Peitsch et al., 1992). We used bee templates to obtain absorption Vorobyev et al., 2001). The model developed by Chittka (Chittka, curves (Stavenga et al., 1993). S() is the spectral reflection function 1992) has also been widely used for assessments of the chromatic of spiders or substrates, and I() is the illuminating daylight and achromatic contrasts of crab spiders against their substrates. spectrum (CIE D65). Here we assume that almost all visual However, the model of Vorobyev and Osorio (Vorobyev and Osorio, interactions occur in sunny daylight. 1998) has the advantage of including a powerful colour The colour distance S, in JND units, between each spider and discrimination threshold, as it includes the total receptor noise. Total its flower, for the trichromatic eyes of bees, is given by: receptor noise is the sum of photon (‘quantum’) noise and internal e2 (Δf −Δf )2 + e2 (Δf −Δf )2 + e2 (Δf −Δf )2 receptor (‘neural’) noise. Indeed, this physiological model, based (ΔS )2 = UV G B B G UV G UV B , (2) (e e )2 + (e e )2 + (e e )2 on the observation that the ability to discriminate between colours UV B UV G B G is limited by total receptor noise, has been shown to predict well the ability to discriminate between colours in animals, including where ei is the internal receptor noise for each receptor class i of primates, birds and the honeybee Apis mellifera. The chromatic and bees (UV, B, G) and fi is the natural log of the quantum catches achromatic contrasts between two spectra are measured in units of for receptor i (UV, B and G for bees) between spiders (Sp) and just noticeable difference (JND). A value of 1 JND between two flowers (F): spectra corresponds to the discrimination threshold under ideal fi  ln (QiSp / QiF). (3) conditions and under which two spectra are considered to be indistinguishable (Wyszecki and Stiles, 1982). The relationship Crab spider–prey interactions occur in conditions of high light between noise level and light intensity is however not linear intensity, and a large proportion of spiders were found on bright (Anderson and Laughlin, 2000; Vorobyev et al., 2001), and this ‘white’ and ‘yellow’ flowers. Internal receptor noise is thought to model does not incorporate physiological mechanisms that may predominate at high light intensity (Vorobyev et al., 2001). The affect colour discrimination such as spatial and temporal summation internal receptor noise ei, is calculated as: (Dyer and Neumeyer, 2005). Despite these shortcomings, Vorobyev and Osorio’s model remains the most efficient colour vision model ei / ͱi, (4)

100 Fig.2. Mean (±s.d.) reflectance spectra of A B Leucanthemum vulgare Misumena vatia analysed in this study (A), 80 and of the flower species used as substrate by M. vatia (B–D). Misumena 60 vatia

40 Achillea millefolium

20

0

100 C Filipendula ulmaria D Cleome spinosa Reflect a nce (%) 80

60

40 Heracleum Senecio sp. sphondylium 20

0 300 400 500 600 700 300 400 500 600 700 Wavelength (nm)

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1428 J. Defrize, M. Théry and J. Casas where  is the Weber fraction assigned to each receptor class [0.13 (Q) for the Green (G) receptor class between spider (Sp) and flower (Vorobyev and Osorio, 1998)] and i is the relative density of the (F). QGSp and QGF are the quantum catch (Q) for a spider (Sp) and receptor class i of bees. Within a honeybee eye, ommatidia do not a flower (F) spectrum, respectively, in the Green (G) receptor class contain similar sets of photoreceptors. Wakakuwa et al. indeed found of the bees. eG is the internal receptor noise of the Green (G) receptor three types of ommatidia containing either one UV, one B and six class of bees. G receptors (Type I), or two UV, one B and six G receptors (Type For bird colour vision, we used the spectral sensitivities of the II), or one UV, two B and six G receptors (Type III) (Wakakuwa tetrachromatic insectivorous blue tit Cyanistes caeruleus, taking into et al., 2005). They also revealed that the ratio of the Types I, II, III account visual pigment, oil droplet and ocular media transmittances was 44:43:10 (Wakakuwa et al., 2005). Moreover, Spaethe and (Hart et al., 2000; Hart, 2001). Spectral sensitivity functions were Briscoe showed that this heterogeneity also occurs in bumblebees taken directly from avian templates generously provided by Doris (Spaethe and Briscoe, 2005). We thus used the ratio of 1:0.471:4.412 Gomez. The presence of blue tits has been reported in the meadows for all bees (for UV, B and G receptors, respectively). This ratio around Tours (Théry et al., 2005). takes into account both the ommatidia heterogeneity and the ratio We measured the quantum catch (see Eqn1) for a given spectrum of Types I, II, III. in the ultraviolet sensitive (UVS), short-wavelength sensitive (SWS), Chromatic contrast is the dominant cue used by foraging bees medium-wavelength sensitive (MWS) and long-wavelength for the identification of flowers at short distance, when a flower sensitive (LWS) photoreceptors of blue tits, as we did for bees. subtends a visual angle of at least 15deg. (Giurfa et al., 1996). The colour distance S between each spider and flower for the However, at long distance, when a flower subtends a visual angle tetrachromatic eyes of birds is given by: between 5deg. and 15deg., honeybees and bumblebees use green 2 2 2 2 2 (S)  ((eUVSeSWS) (fLWS – fMWS) + (eUVSeMWS) (fLWS – fSWS) contrast for flower detection, looking for a difference between 2 2 2 + (eUVSeLWS) (fSWS – fMWS) + (eSWSeMWS) (fLWS background and target green receptor signals (Giurfa et al., 1996; 2 2 2 2 – fUVS) + (eSWSeLWS) (fMWS – fUVS) + (eMWSeLWS) Spaethe et al., 2001). 2 2 2 (fSWS – fUVS) ) / ((eUVSeSWSeMWS) + (eUVSeSWSeLWS) The green contrast between a spider and its flower can be 2 2 + (eUVSeMWSeLWS) + (eSWSeMWSeLWS) ), (6) calculated as: where ei is the internal receptor noise for each receptor class i of SG fG / eG  ln (QGSp / QGF) / eG , (5) birds (UVS, SWS, MWS and LWS) and fi is the natural log of the in which SG is the spectral sensitivity of the L-wavelength quantum catches for receptor i (UVS, SWS, MWS and LWS) photoreceptor of bees. fG is the natural log of the quantum catch between Sp and F (see Eqn3). The relative density of the receptor

–0.26 Fig.3. (A,C)Distribution of spider and flower colour loci on B the chromaticity diagram of bees (A) and birds (C). (B,D)Selected enlarged area. Each small coloured symbol –0.28 represents a spider found on a flower species (larger symbol). Pink circles indicate spiders found on Heracleum sphondylium, red squares indicate spiders found on –0.30 Filipendula ulmaria, green triangles indicate spiders found on Leucanthemum vulgare, blue circles indicate spiders found on Cleome spinosa, blue squares indicate spiders

Y –0.32 found on Achillea millefolium, yellow triangles indicate spiders found on Senecio sp. UVultraviolet, Bblue, –0.34 Ggreen. UVSultraviolet sensitive, SWSshort-wavelength A sensitive, MWSmedium-wavelength sensitive, and LWSlong-wavelength sensitive. –0.36

–0.38 0.1 0.2 0.3 0.4 0.5 0.6 0.7 X C D

1.0 –0.23 0.8 –0.24 0.6 –0.25 0.4

Z –0.26 0.2 Z –0.27 0 0.8 –0.2 0.4 –0.28 0.08 –0.4 0 –0.29 0.04 0.8 0.4 –0.4 X 0.1 0 –0.1 X 0 –0.2 0 Y –0.4 –0.8 Y –0.3 –0.4

THE JOURNAL OF EXPERIMENTAL BIOLOGY Background matching by a crab spider 1429 class i taken from Pareus caeruleus was 1, 1.92, 2.68 and 2.7 for (luminance max. – luminance min.) / (luminance max. + luminance UVS, SWS, MWS, LWS photoreceptors, respectively (Maier and min.) at which maximum contrast sensitivity occurs. In the starling, Bowmaker, 1993). We also achieved the calculations with different the maximum contrast sensitivity has a Michelson contrast value photoreceptor ratios [1, 2, 2, 4 (Schaefer et al., 2007); 1, 1, 1, 2 of 16% for 1.1cyclesdeg.–1 (Ghim and Hodos, 2006). We created (Lind and Kelber, 2009)] to assess how sensitive the results are to two spectral reflectance curves that display not only a Michelson this choice. contrast of 16% but also a LWS receptor contrast equal to 16%, For the receptor noise value in birds, we proceeded as Schaefer because Weber fraction are often calculated from LWS class cone et al. (Schaefer et al., 2007). Our reasoning was that not only (i) (Vorobyev et al., 1998). are the noise levels in avian photoreceptors still unclear (Lind We assumed that these two spectra computed with the ‘limiting and Kelber, 2009), but also that (ii) the absolute value of noise Weber fraction’ in Vorobyev and Osorio’s model (Vorobyev and varies quite a lot, depending on the viewing conditions (Ghim Osorio, 1998) should have an achromatic contrast equal to 1 JND. and Hodos, 2006; Schaefer et al., 2007; Harmening et al., 2009). Thus, by identifying the ‘Weber fraction’ that allows us to get an We thus performed calculations with several values of Weber achromatic contrast between these two spectra equal to 1 JND, we fraction. Increase of the Weber fraction results in a corresponding also identify the ‘limiting Weber fraction’ at which the maximum increase of the threshold value in JND. The lowest Weber contrast sensitivity occurs (16%). In this study, we used the fraction was estimated as 0.1 from behavioural data (Maier and maximum contrast sensitivity of the starling (16% at Bowmaker, 1993) and corresponds to a threshold of 1 JND. 1.1cyclesdeg.–1), as no such data exist for C. caeruleus. Because noise above 0.5 is physiologically implausible, we We estimated the most relevant range of ‘Weber fraction’ to use assumed that Weber fraction can increase up to 0.5, which by referring to contrast threshold values computed in the starling corresponds to a threshold of 5 JNDs. We assumed that spiders Sturnus vulgaris (Passeriformes) (Ghim and Hodos, 2006). with a contrast against their substrates higher than 5 JNDs can Following the same steps as above, we also calculated the Weber always be detected. fractions at the lowest (0.3cyclesdeg.–1) and highest (7cyclesdeg.–1) Birds use also achromatic contrast at long range (Osorio et al., spatial frequencies at which the lowest contrast sensitivities occur. 1999a; Osorio et al., 1999b), through double-cones. Thus, the We thus found a set of ‘Weber fractions’, ranging from 0.2 to 0.5, achromatic contrast between a spider and its substrate is then which is close to the range used by Schaefer et al. (Schaefer et al., measured as:

SDC fDC / eDC  ln (QDC–Sp / QDC–F) / eDC , (7) N = 13 56 34 6 8 9 in which SDC is the spectral sensitivity of the double-cone 25 A photoreceptors of birds. fDC is the natural log of the quantum catch for the double cone (DC) receptor class between spider (Sp) and flower 20 *** (F). QDC-Sp and QDC-F are the quantum catch (Q) for a spider (Sp) and a flower ( ) spectrum, respectively, in the double cone ( ) receptor F DC 15 class of the birds. eDC is the internal receptor noise of the double *** cone (DC) receptor class of birds. Chromatic and achromatic contrasts © 10 were calculated with Avicol software (Paris, France; available (JND u nit) upon request from D. Gomez at [email protected]) (Gomez *** ** and Théry, 2007). 5 ** *** We plotted the position of each flower and spider in the Chrom a tic di s crimin ab ility chromaticity diagram of both bees and birds, following the 0 calculation given in Kelber et al. (Kelber et al., 2003). Trichromatic 4 B bees have a two-dimensional chromaticity diagram (Fig.3A,B) n.s. whereas it is three-dimensional for tetrachromatic birds (Fig.3C,D). n.s. 3 We also performed a more complex analysis using an assumption n.s. about bird vision, which is natural but will need further testing. n.s. n.s. Studies have shown that the contrast threshold of birds is strongly 2 affected by viewing conditions, especially the spatial frequency of n.s. the stimuli (Ghim and Hodos, 2006; Harmening et al., 2009). Indeed, (JND u nit) contrast sensitivity functions display an inverted-U shape (Ghim 1 and Hodos, 2006; Harmening et al., 2009). In the case of the motionless M. vatia, each spatial frequency corresponds to a specific Achrom a tic di s crimin ab ility distance at which birds observe spiders. These studies thus provide 0 contrast threshold according to a wide range of distances. However, leome Achillea C contrast thresholds are given in ‘Michelson contrast’ values that ulmaria vulgare spinosa cannot be used in the model developed by Vorobyev et al. (Vorobyev Heracleum Filipendula millefolium Senecio sp. sphondylium et al., 2001). Using the method described below, we thus transformed Leucanthemum contrast threshold values into Weber fractions that can be integrated into the model developed by Vorobyev et al. (Vorobyev et al., 2001). Fig.4. Mean (±s.d.) chromatic (A) and achromatic (B) discriminability, We first determined the contrast discrimination threshold (the measured in just noticeable differences (JNDs), for Misumena vatia against different flower species for the trichromatic prey, bees. Horizontal broken inverse of contrast sensitivity) for each distance from a bird to a lines indicate the threshold for crypticity in the bee’s visual system. Note spider. Generally, the contrast discrimination threshold for a given the difference in scale on the Y-axis of the two graphs. n.s.non significant. spatial frequency corresponds to the lowest Michelson contrast **P<0.01, ***P<0.001.

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1430 J. Defrize, M. Théry and J. Casas

18 Fig.5. Individual chromatic discriminability 16 distribution, in just noticeable differences Misumena vatia against different 14 (JNDs), for Heracleum sphondylium Filipendula ulmaria flower species for bee vision. Vertical broken 12 lines indicate the threshold for crypticity in the 10 bee visual system. 8 6 4 2 0 18 16 14

a tion s Leucanthemum vulgare Achillea millefolium 12 10 8 6 4

N u m b er of o bs erv 2 0 18 16 14 12 Cleome spinosa Senecio sp. 10 8 6 4 2 0 04266 8 10 12 14 16 18 20 22 24 042 8 10 12 14 16 18 20 22 24 Chromatic discriminability (JND)

2007). On the basis of an 8mm size for spiders, we finally assessed The model consists of two subsystems made of the pairs R7p/R8p the distance of birds to spiders corresponding to each spatial and R7y/R8y, R7 and R8 being antagonistically connected in each frequency. one. The differences R7–R8 gives input to a threshold mechanism such that each subsystem can have one of the two values (+, –). Assessing chromatic contrast in the fly visual system Each combination of values (+/+, +/–, –/+, –/–) corresponds to a Classical colour vision models used for bees or birds do not fit the specific category. For each stimulus, we thus calculated the vision of flies, despite good knowledge of spectral sensitivities of differences ‘R7p–R8p’ and ‘R7y–R8y’. Two stimuli eliciting the several fly species (Horridge et al., 1975; Bernard and Stavenga, same combination of values are considered as similar for Lucilia 1979; Hardie, 1979; Hardie and Kirschfeld, 1983), and receptor noise sp. values of fly photoreceptors involved in the colour vision process The quantum catch for a given spectrum in the respective fly (Anderson and Laughlin, 2000). Indeed, whereas bees and birds photoreceptors is calculated as in Eqn1 (see above), and spectral display a continuous colour vision, Troje showed that the flower- sensitivities of Lucilia sp. are taken from Hardie and Kirschfeld visiting blowfly Lucilia sp. possesses a categorical colour vision (Hardie and Kirschfeld, 1983). We used templates fitted to Lucilia’s (Troje, 1993). For this species, the wavelength spectrum consists spectral sensitivities (Stavenga et al., 1993). We did not compute of four categories (UV, Blue, Yellow and Purple). Lucilia sp. the achromatic contrast for blowflies, as nothing is known about discriminated monochromatic lights belonging to different this aspect in flies. categories. However, no discrimination occurs within a category. Troje (Troje, 1993) proposed a colour opponent mechanism that Is perfect chromatic matching due to chance only? matches its result well. Despite the fact that this model needs to be We investigated whether perfect chromatic matching (JND<1) on further tested and improved, we use it because (i) it is, to our the whitish F. ulmaria (harbouring the largest number of spiders) knowledge, the single one available for any fly, (ii) it is based on was due to chance alone, by first calculating the chromatic behavioural experiments, and (iii) Lucilia sp. is a flower-visiting discriminability, against F. ulmaria, of the spiders found on other species that may suffer predation by crab spiders. flower species. We then compared the proportion of undetectable This model involves four types of central photoreceptors, spiders in the simulated spider–F. ulmaria pairs with the proportion named R7p, R7y, R8p and R8y, with a peak at 341nm, 362nm, of undetectable spiders actually found on F. ulmaria. We assumed 465nm and 537nm, respectively (Hardie and Kirschfeld, 1983). that if the observed matching was due to chance alone, the proportions

THE JOURNAL OF EXPERIMENTAL BIOLOGY Background matching by a crab spider 1431 of undetectable spiders would be similar in both sets of spiders. Thus, N = 13 5634 6 8 9 in this case, spiders hunting on flower species other than F. ulmaria 30 would have matched F. ulmaria petals equally well as spiders hunting A on F. ulmaria. A mean colour spectrum of F. ulmaria was used to 25 measure chromatic contrast in the two sets of spiders. The same protocol was tested with the whitish H. sphondylium, the flower 20 species harbouring the second largest number of spiders. 15

Statistical analysis (JND u nit) 10 We used various statistical tests to compare mean contrast values with chromatic and achromatic discrimination thresholds for bee 5 and bird colour visions. We first tested the normality of Chrom a tic di s crimin ab ility distributions, using the Shapiro test, and then performed one- 0 sample t-test for normally distributed variables and the non- 5 parametric rank sign test for variables with non-normal B distributions. We also assessed whether the proportions of perfect 4 chromatic matching between two distributions were similar using a normal approximation of the chi-squared test. All statistical 3 analyses were performed with R and Statistica (Statsoft France, France). 2 (JND u nit) RESULTS Chromatic and achromatic contrast values for bees 1 We observed no correlation between the stage of spider development Achrom a tic di s crimin ab ility and both the chromatic and achromatic contrast values (R20.0221, 0 P0.14 and R20.034, P0.10, respectively; N126). We analysed leome the chromatic and achromatic discriminabilities using first the mean Achillea C ulmaria vulgare spinosa contrast values. The mean chromatic contrast values are above the Heracleum Filipendula millefolium Senecio sp. sphondylium discrimination threshold (1 JND) (t-test, P<0.01 for H. sphondylium; Leucanthemum sign test, P<0.001 for F. ulmaria; sign test, P<0.001 for L. vulgare; t-test, P<0.01 for A. millefolium; t-test, P<0.001 for C. spinosa; sign Fig.6. Mean (±s.d.) chromatic (A) and achromatic (B) discriminability, test, P<0.001 for Senecio sp.) (Fig.4A). Mean achromatic measured in just noticeable differences (JNDs), for Misumena vatia against different flower species for a tetrachromatic passerine bird. JNDs of 1 to 5 discriminability values for the spiders did not significantly exceed represent the range of most likely threshold values obtained in the literature. the discriminability threshold value (1 JND) in honeybees (sign tests: P0.86, P0.17, P0.11, P0.74 for H. sphondylium, F. ulmaria, L. vulgare and Senecio sp., respectively; t-tests: P0.84, P0.13 for A. Chromatic and achromatic contrast values for birds millefolium, C. spinosa, respectively). Thus, M. vatia would not be Our results revealed that, at short distance, M. vatia can be always detected by the green receptor of bees at long range (Fig.4B). To chromatically detected on L. vulgare, A. millefolium, C. spinosa and sum up the results for mean contrast values, we show that spiders Senecio sp. by birds, as their mean chromatic contrasts are always appear detectable at short range but undetectable at long significantly higher than 5 JNDs (P<0.01, t-test for A. millefolium; distance for bees. P<0.001 t-tests for L. vulgare, C. spinosa, and for Senecio sp., sign If we consider individual chromatic contrast between pairs test). Spiders hunting on H. sphondylium and F. ulmaria will be (Fig.5), the situation is more complex than that described above on also detectable, except if receptor noise reaches values of 0.45 the basis of mean values. Spiders may be either perfectly cryptic (P0.051 for H. sphondylium, t-test and P0.13 for F. ulmaria, sign (undetectable spiders have values that are <1 JND) or poorly test) (Fig.6A). At long distance, we observed that M. vatia is discriminable (pairs with values between 1 and 4 JNDs) on H. achromatically undetectable whatever the flower species and the sphondylium (23% and 61%, respectively) or F. ulmaria (19% and value of noise. Indeed, mean achromatic contrasts did not differ 71%, respectively). On L. vulgare, A. millefolium, C. spinosa and significantly from 1 JND (Fig.6B). Senecio sp., respectively, 47%, 33%, 0%, 0% of pairs produce values Individual chromatic contrast values allowed us to confirm that between 1 and 4 JNDs but no perfect chromatic matching was on each flower, a high proportion of spiders are always chromatically observed. All spiders hunting on C. spinosa and Senecio sp. appear detectable (higher than 5 JNDs) (53%, 48%, 94%, 83%, 100% and quite visible (JND>4) for bees. 100% for H. sphondylium, F. ulmaria, L. vulgare, A. millefolium, A similar analysis with achromatic contrast distributions revealed C. spinosa and Senecio sp., respectively) (Fig.7). All of these low levels of variability in individual pairs (data not shown) and a conclusions remained valid when calculations are performed with larger proportion of spiders near the discrimination threshold of different photoreceptor ratios (1, 2, 2, 4 and 1, 1, 1, 2 for UVS, bees (0

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1432 J. Defrize, M. Théry and J. Casas

10 Fig.7. Individual chromatic discriminability distribution, in just noticeable differences (JNDs), for Misumena vatia Filipendula ulmaria 8 Heracleum sphondylium against different flower species for bird vision.

6

4

2

0 10 Leucanthemum vulgare Achillea millefolium 8 a tion s

6

4

2 N u m b er of o bs erv 0 10 Cleome spinosa Senecio sp. 8

6

4

2

0 0101520255 30 0 5 1015202530 Chromatic discriminability (JND) chromatic signal should be used, we observed that M. vatia is always At short distance, M. vatia is mostly chromatically detectable detectable. At the opposite, M. vatia is always achromatically whatever the substrate for bees and birds. However, spiders can be undetectable whatever the distance at which it is observed by birds, either poorly discriminable or quite visible depending on the especially at long distances when achromatic signals are most substrate for bees (Table1). Indeed, M. vatia hunts sometimes on relevant. flowers on which it yields a high chromatic contrast for bee vision whereas other flowers provide substrate on which perfect chromatic Chromatic contrast in the fly visual system crypsis can be achieved. The same trend was already suggested using Using the colour opponent model developed by Troje (Troje, 1993), Chittka’s model but with two spider individuals only (Chittka, 2001). we found that all spiders would appear cryptic for Lucilia sp., both We show that these perfect matchings (JND<1) result from a purely spiders and substrates being ranked as (+/+) in the fly vision (N126). random process, implying no particular local adaptation of the spiders to their flowers. This explains the small number of perfectly Proportions of perfect chromatic matching for simulated cryptic spiders observed in this study. A model proposed that spider–flower pairs in bee visual system colouration in a visually heterogeneous habitat can be optimised by We showed that perfect chromatic matching occurred in either finding a compromise in the degree of crypsis between assessments of the chromatic contrast of spiders found on different microhabitats or by increasing the degree of crypsis in one of the flower species against petals of F. ulmaria. The proportion of microhabitats at the expense of another (Merilaita et al., 2001). Here, matching did not differ significantly between spiders actually we noticed that it is unlikely that the resulting colouration of M. hunting on F. ulmaria and spiders initially found on the flowers vatia is a form of crypsis optimised for visually heterogeneous of other species and then randomly assorted to F. ulmaria (11/56 environments. Unlike for bees and passerine birds, chromatic and 12/70, respectively, d.f.124, P0.77). Similar proportions of crypsis seems to be always achieved for the blowfly Lucilia sp. In undetectable spiders were also obtained between spiders initially the following, we focus on both the chromatic and achromatic hunting on H. sphondylium in assessments of the chromatic contrasts elicited by M. vatia and discuss their biological relevance discriminability of spiders found on other flower species with in defensive and aggressive mimicry contexts. respect to those on H. sphondylium (3/13 and 20/113, respectively, d.f.124, P0.59). Is crypsis at long distance sufficient to avoid bird attacks? Our results suggest that the detectability of M. vatia through DISCUSSION chromatic signal varies according to the distance at which passerine We observed that crypsis at long distance is systematically achieved, birds forage. Misumena vatia appears chromatically visible at short exclusively through achromatic contrast, in both bee and bird visions. distance for insectivorous passerines on the substrate on which it

THE JOURNAL OF EXPERIMENTAL BIOLOGY Background matching by a crab spider 1433

14 Heracleum sphondylium Filipendula ulmaria Fig.8. Mean (±s.d.) chromatic (black squares) and 12 achromatic (grey circles) contrasts of spiders against different substrates in the perspective of birds, according 10 to different spatial frequencies. On the basis of 8mm- 8 long spiders, we also assessed the distance of birds to 6 spiders corresponding to each spatial frequency. A 4 logarithmic scale is used for the x-axis. 2 0 14 Leucanthemum vulgare Achillea millefolium 12 10 8

as t s (JND) 6 4 Contr 2 0 14 Cleome spinosa Senecio sp. 12 10 8 6 4 2 0 Spatial frequency 0.3 1 7.5 0.3 1 7.5 (cycles deg.–1) Distance (cm) 16 50 375 16 50 375 sits. Despite this chromatic conspicuousness, the predation pressure spectabilis (Heiling et al., 2005). However, there is a lack of from birds on M. vatia is very low. Indeed, Morse (Morse, 2007) knowledge about the role of the chromatic and achromatic crypsis has not recorded any case of bird predation in 30 years of intensive in the prey capture rate and survival rate against birds. Indeed, field research on crab spiders. Moreover, Bristowe’s (Bristowe, despite the growing number of studies using crab spider–prey 1971) records of over 10,000 spiders eaten by birds from sampling interactions, there is not yet any evidence, for any prey, that their stomach contents contain only four M. vatia, a very low decreasing chromatic and/or achromatic contrasts provides the spider number. Thus, these observations indicate that the lack of predation with a benefit in terms of predation efficiency (Gonçalves-Souza cannot be explained by vision at short distance. This raises the et al., 2008; Yokoi and Fujisaki, 2009; Brechbühl et al., 2010a; question whether bird attacks are low because birds are actually avoiding visible M. vatia or because protection is efficiently achieved through achromatic crypsis at long distance? Answering Table 1. Detectability of Misumena vatia according to the distance this question will require us not only to quantify the range of visual at which it is perceived for different visual observers angles at which chromatic signals are used but also to relate the Short distance Long distance foraging paths taken by birds in the vegetation to the positions of Chromatic Achromatic Chromatic Achromatic their prey. contrast contrast contrast contrast Mostly Are M. vatia under selection by prey for crypsis? Bees Undetectable Bees, when reaching a new patch, detect flowers first through the detectable achromatic signal (Spaethe et al., 2001), according to the visual angle at which chromatic vision may occur [>15deg. honeybees (Giurfa Blowfly Undetectable ? ? ? et al., 1996)] and their spatial resolution (2.8deg. ϫ 5.4deg. in honeybees; 5deg. in bumblebees) (Autrum and Wiedemann, 1962; Mostly Eheim and Wehner, 1972; Meyer-Rochow, 1981). However, within Blue tits Undetectable detectable a patch, bumblebees forage with a flight height ranging from 23mm to 50mm, depending on the flower diameter (Spaethe et al., 2001). Cross circles indicate no neurophysiological relevant situations. Question From these data, it is likely that both chromatic and achromatic marks indicate that there is a lack of study allowing us to fill in the boxes. contrasts elicited by spiders are noticed by prey. Distances are relative distances. However, for honeybees, calculations Other crab spider species have been reported to be either allow us to determine that an 8 cm-diameter flower would be identified chromatically cryptic on a substrate in the perspective of bees, as with chromatic signal until a distance of around 30 cm. For foraging for onustus (Théry and Casas, 2002; Théry et al., 2005), distances higher than 30 cm, honeybees will identify flowers with or achromatically cryptic, as for the Australian crab spider Thomisus achromatic (green) signal.

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1434 J. Defrize, M. Théry and J. Casas

Brechbühl et al., 2010b). These studies, however, revealed that the dependent of the receiver and the substrate on which M. vatia sits. way prey behave in response to a crab spider is not only species These results raise concerns about drawing conclusions based on specific but also individual specific. We discuss these aspects in human visual assessments. They also highlight the importance of turn. studying background matching, in the field, from the sensory Some species of solitary bees and syrphid flies have been ecology of all main receivers. For generalist predators, a visual reported to be deterred by the presence of M. vatia (Brechbühl et ecology community perspective seems mandatory before statements al., 2010b), Thomisus labefactus (Yokoi and Fujisaki, 2009), on adaptation of crypsis can be issued. This endeavour also leads Xysticus species (Brechbühl et al., 2010a) and an artificial to the identification of major gaps in our knowledge, such as the Misumenops argenteus (Gonçalves-Souza et al., 2008). Syrphid flies neuroethology of colour vision in flower-visiting flies, in particular Sphaerophoria spp., for instance, show a 100% flower rejection rate the abundant syrphid flies (Brechbühl et al., 2010b) and of the crab when flowers on which a spider sits are presented to them (Yokoi spiders themselves. and Fujisaki, 2009). However, the lack of information about levels of contrasts and the relative importance of chromatic cues in these ACKNOWLEDGEMENTS anti-predatory behaviours precludes us to conclude about any gain We thank Doris Gomez for providing Avicol© software. We would also like to thank Teresita Insausti and Sylvain Pincebourde for their constructive reviews and in being chromatically and achromatically cryptic. reviewers who provided valuable comments on the manuscript. This study was The evidence for selection for crypsis is also lacking when performed as part of the PhD work of J.D. at the University of Tours, under the discussed from the honeybee and bumblebee point of view, for supervision of J.C. which it is relatively easy to assess the degree of contrasts, and for which it has been shown that flower chromatic cues affect REFERENCES visitation rates (Lunau et al., 1996). In these species, predator- Anderson, J. C. and Laughlin, S. B. (2000). Photoreceptor performance and the co- ordination of achromatic and chromatic inputs in the fly visual system. Vision Res. avoidance learning has been shown to modulate the level of 40, 13-31. predator detection. While naive bumblebees Bombus terrestris Autrum, H. and Wiedemann, I. (1962). Versuche fiber den Strahlengang im Insektenauge (Appositionsauge). Z. Natforsch. 17, 480-482. visit white flowers harbouring a ‘white’ or ‘yellow’ artificial M. Bernard, G. D. and Stavenga, D. G. (1979). Spectral sensitivities of retinular cells vatia at the same rate, those having suffered several unsuccessful measured in intact, living flies by an optical method. J. Comp. Physiol. A 134, 95-107. Bhaskara, M. R., Brijesh, C. M., Ahmed, S. and Borges, R. M. (2009). Perception of spider attacks can increase inspection times and display false ultraviolet light by crab spiders and its role in selection of hunting sites. J. Comp. alarms (erroneous rejection of flowers without predators), both Physiol. A 195, 409-417. Brechbühl, R., Kropf, C. and Bacher, S. (2010a). Impact of flower dwelling crab decreasing their foraging efficiency (Ings and Chittka, 2008). spiders on plant mutualisms. Basic Appl. Ecol. 11, 76-82. Increased level of detection in bees suggests that crypsis could Brechbühl, R., Casas, J. and Bacher, S. (2010b). Ineffective crypsis in a crab spider: a prey community perspective. Proc. R. Soc. Lond., B, Biol. Sci. 277, 739-746. be beneficial. However, not only false alarms but also the fact Bristowe, W. S. (1971). The World of Spiders. London: Collins. that some bumblebees and honeybees decide to leave the patch Chittka, L. (1992). The colour hexagon: a chromaticity diagram based on of flowers after several spider attacks (Dukas and Morse, 2003; photoreceptor excitations as a generalized representation of colour opponency. J. Comp. Physiol. A 170, 533-543. Dukas and Morse, 2005), induce a loss of available prey, even Chittka, L. (2001). Camouflage of predatory crab spiders on flowers and the colour for poorly discriminable spiders. Moreover, recent field perception of bees (Aranida: Thomisidae / : Apidae). Entomol. Gen. 25, 181-187. experiments, which do not take into account the ‘learning state’ Dailey, T. B. and Scott, P. E. (2006). Spring nectar sources for solitary bees and flies of visiting bees, suggested that the selective pressure of learning in a landscape of deciduous forest and agricultural fields: production, variability, and consumption. J. Torrey Botan. Soc. 133, 535-547. on crypsis may be less important than expected. Indeed, the Dukas, R. and Morse, D. H. (2003). Crab spiders affect flower visitation by bees. number of honeybees and bumblebees visiting flowers with a Oikos 101, 157-163. Dukas, R. and Morse, D. H. (2005). Crab spiders show mixed effects on flower- highly chromatically contrasting M. vatia is similar to flowers visiting bees and no effect on plant fitness components. Ecoscience 12, 244-247. without spiders (Dukas and Morse, 2003) (Brechbühl et al., Dyer, A. G. and Neumeyer, C. (2005). Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). J. Comp. Physiol. A 191, 547-557. 2010b). Thus, the proportion of experienced bees efficiently Eheim, W. P. and Wehner, R. (1972). Die sehfelder der zentralen ommatidien in den avoiding crab spiders may be too low to significantly impact the appositionsaugen von Apis mellifera und Cataglyphis bicolor (Apidae, Formicidae; Hymenoptera). Kyberneticke 10, 168-179. encounter rate and to drive the spider colouration towards crypsis. Gertsch, W. J. (1939). A revision of the typical crab-spiders (Misumeninae) of America Why then do spiders choose flowers on which they yield a high north of Mexico. Bull. Am. Mus. Nat. Hist. 76, 277-442. Ghim, M. M. and Hodos, W. (2006). Spatial contrast sensitivity of birds. J. Comp. chromatic contrast? Misumena vatia will systematically produce Physiol. A 192, 523-534. high chromatic contrast on several floral reflectance types due to Giurfa, M., Vorobyev, M., Kevan, P. and Menzel, R. (1996). Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J. its inability to cover the entire flower colour spectrum, particularly Comp. Physiol. A 178, 699-709. the UV range (Herberstein et al., 2009). However, M. vatia can be Gomez, D. and Théry, M. (2007). Simultaneous crypsis and conspicuousness in color found hunting on UV-reflecting flowers, such as C. spinosa and patterns: comparative analysis of a neotropical rainforest bird community. Am. Nat. 169, 42-61. Senecio sp. Nothing is known about M. vatia’s spectral sensitivities Gonçalves-Souza, T., Omena, P. M., Souza, J. C. and Romero, G. Q. (2008). Trait- and whether a UV contrast may also act as an attractive stimulus mediated effects on flowers: artificial spiders deceive and decrease plant fitness. Ecology 89, 2407-2413. for honeybees, in a similar fashion as the UV-reflecting Australian Hardie, R. C. (1979). Electrophysiological analysis of fly retina. I: comparative crab spider T. spectabilis hunting on UV-absorbing flowers (Heiling properties of R1-6 and R7 and 8. J. Comp. Physiol. A 129, 19-33. Hardie, R. C. and Kirschfeld, K. (1983). Ultraviolet sensitivity of fly photoreceptors R7 et al., 2005; Bhaskara et al., 2009). Lunau et al. showed that bees and R8: evidence for a sensitizing function. Biophys. Struct. Mech. 9, 171-180. innately prefer flowers with strongly contrasting markings (Lunau Harmening, W. M., Nikolay, P., Orlowski, J. and Wagner, H. (2009). Spatial contrast sensitivity and grating acuity of barn owls. J. Vision 9, 1-12. et al., 1996). So, whether conspicuous colouration may be an Hart, N. S. (2001). Variations in cone photoreceptor abundance and the visual ecology alternative to crypsis on some substrates for an efficient predation of birds. J. Comp. Physiol. A 187, 685-697. Hart, N. S., Partridge, J. C., Cuthill, I. C. and Bennett, A. T. B. (2000). Visual is still unknown. pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). J. Comp. Physiol. A 186, 375-387. Conclusions Heckel, E. (1891). Sur le mimétisme de Thomisus onustus. Bull. Sc. Fr. Belg. 23, 347- This spider has been assumed to be chromatically cryptic for more 354. than a century. We show here, through a quantitative study carried Heiling, A. M., Cheng, K., Chittka, L., Goeth, A. and Herberstein, M. (2005). The role of UV in crab spider signals: effects on perception by prey and predator. J. Exp. out in the field, that the degree of chromatic contrast is quite Biol. 208, 3925-3931.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Background matching by a crab spider 1435

Herberstein, M. E., Heiling, A. M. and Cheng, K. (2009). Evidence for UV-based Robertson, I. C. and Maguire, D. K. (2005). Crab spiders deter insect visitations to sensory exploitation in Australian but not European crab spiders. Evol. Ecol. 23, 621- slickspot peppergrass flowers. Oikos 109, 577-582. 634. Ruxton, G. D., Sherratt, T. N. and Speed, M. P. (2004). Avoiding Attack: the Horridge, G. A., Mimura, K. and Tsukahara, Y. (1975). Fly photoreceptors. II. Evolutionary Ecology of Crypsis, Warning Signals, and Mimicry. Oxford: Oxford Spectral and polarized light sensitivity in the drone fly Eristalis. Proc. R. Soc. Lond., University Press. B, Biol. Sci. 190, 225-237. Schaefer, M. H., Schaefer, V. and Vorobyev, M. (2007). Are fruit colors adapted to Ings, T. C. and Chittka, L. (2008). Speed-accuracy tradeoffs and false alarms in bee consumer vision and birds equally efficient in detecting colorful signals? Am. Nat. responses to cryptic predators. Curr. Biol. 18, 1520-1524. 169, 159-169. Insausti, T. C. and Casas, J. (2008). The functional morphology of color changing in Schmalhofer, V. R. (2001). Tritrophic interactions in a pollination system: impacts of a spider: development of ommochrome pigment granules. J. Exp. Biol. 211, 780- species composition and size of flower patches on the hunting success of a flower- 789. dwelling spider. Oecologia 129, 292-303. Insausti, T. C. and Casas, J. (2009). Turnover of pigment granules: cyclic Spaethe, J. and Briscoe, A. D. (2005). Molecular characterization and expression of catabolism and anabolism of ommochromes within epidermal cells. Tissue Cell 41, the UV opsin in bumblebees: three ommatidial subtypes in the retina and a new 421-429. photoreceptor organ in the lamina. J. Exp. Biol. 208, 2347-2361. Kelber, A., Vorobyev, M. and Osorio, D. (2003). colour vision – behavioural Spaethe, J., Tautz, J. and Chittka, L. (2001). Visual constraints in foraging tests and physiological concepts. Biol. Rev. 78, 81-118. bumblebees: flower size and color affect search time and flight behavior. Proc. Natl. Lind, O. and Kelber, A. (2009). Avian colour vision: Effects of variation in receptor Acad. Sci. USA 98, 3898-3903. sensitivity and noise data on model predictions as compared to behavioural results. Stavenga, D. G., Smits, R. P. and Hoenders, B. J. (1993). Simple exponential Vision Res. 49, 1939-1947. functions describing the absorbance bands of visual pigment spectra. Vision Res. Lunau, K., Wacht, S. and Chittka, L. (1996). Colour choices of naïve bumble bees 33, 1011-1017. ant their implications for colour perception. J. Comp. Physiol. A 178, 477-489. Stevens, M. and Merilaita, S. (2009). Animal camouflage: current issues and new Maier, E. J. and Bowmaker, J. K. (1993). Colour vision in the passeriform bird, perspectives. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 364, 423-427. Leiothrix lutea: correlation of visual pigment absorbance and oil droplet transmission Stuart-Fox, D., Moussalli, A. and Whiting, M. J. (2008). Predator-specific with spectral sensitivity. J. Comp. Physiol. A 172, 295-301. camouflage in chameleons. Biol. Lett. 4, 326-329. Marshall, J. N. (2000). Communication and camouflage with the same ‘bright’ colours Théry, M. (2007). Colours of background reflected light and of the prey’s eye affect in reef . Philos. Trans. R. Soc. Lond., B, Biol. Sci. 355, 1243-1248. adaptive coloration in female crab spiders. Anim. Behav. 73, 797-804. Mäthger, L. M., Chiao, C. C., Barbosa, A. and Hanlon, R. T. (2008). Color matching Théry, M. and Casas, J. (2002). Predator and prey views of spider camouflage. on natural substrates in cuttlefish, Sepia officinalis. J. Comp. Physiol. A 194, 577- Nature415, 133. 585. Théry, M. and Casas, J. (2009). The multiple disguises of spiders: web colour and Menzel, R. and Backhaus, W. (1989). Color vision in honey bees: phenomena and decorations, body colour and movement. Philos. Trans. R. Soc. Lond., B, Biol. Sci. physiological mechanisms. In Facets of Vision (eds D. G. Stavenga and R. C. 364, 471-480. Hardie), pp. 281-297. Tokyo: Springer-Verlag. Théry, M., Debut, M., Gomez, D. and Casas, J. (2005). Specific color sensitivities of Merilaita, S., Lyytinen, A. and Mappes, J. (2001). Selection for cryptic coloration in a prey and predator explain camouflage in different visual systems. Behav. Ecol. 16, visually heterogeneous habitat. Proc. R. Soc. Lond., B. Biol. Sci. 268, 1925-1929. 25-29. Meyer-Rochow, V. B. (1981). Electrophysiologically determined spectral efficiencies of Théry, M., Insausti, T. C., Defrize, J. and Casas, J. (2010). The multiple disguises of the compound eye and the median ocellus in the bumblebee Bombus hortorum spiders. In Camouflage (ed. M. Stevens and S. Merilaita). Cambridge University tarhakimalainen (hymenoptera, Insecta). J. Comp. Physiol. A 139, 261-266. Press (in press). Morse, D. H. (1979). Prey capture by the crab spider Misumena calycina (Araneae: Troje, N. (1993). Spectral categories in the learning behaviour of blowflies. Zeitschrift Thomisidae). Oecologia 39, 309-319. für Naturforschung C. J. Biosc. 48, 96-104. Morse, D. H. (1981). Prey capture by the crab spider Misumena vatia (Clerck) Vorobyev, M. and Osorio, D. (1998). Receptor noise as a determinant of colour (Thomisidae) on three common native flowers. Am. Midl. Nat. 105, 358-367. thresholds. Proc. R. Soc. Lond., B, Biol. Sci. 265, 351-358. Morse, D. H. (1995). Changes in biomass of penultimate-instar crab spiders Misumena Vorobyev, M., Osorio, D., Bennett, A. T. D., Marshall, N. J. and Cuthill, I. C. vatia (Araneae, Thomisidae) hunting on flowers late in the summer. J. Arachnol. 23, (1998). Tetrachromacy, oil droplets and bird plumage colours. J. Comp. Physiol. A 85-90. 183, 621-633. Morse, D. H. (2007). Predator Upon a Flower: Life History and Fitness in a Crab Vorobyev, M., Brandt, R., Peitsch, D., Laughlin, S. B. and Menzel, R. (2001). Spider. Cambridge, MA: Harvard University Press. Colour thresholds and receptor noise: behaviour and physiology compared. Vision Osorio, D., Miklosi, A. and Gonda, Z. (1999a). Visual ecology and perception of Res. 41, 639-653. coloration patterns by domestic chicks. Evol. Ecol. 13, 673-689. Wakakuwa, M., Kurasawa, M., Giurfa, M. and Arikawa, K. (2005). Spectral Osorio, D., Vorobyev, M. and Jones, C. D. (1999b). Colour vision of domestic chicks. heterogeneity of honeybee ommatidia. Naturwiss. 92, 464-467. J. Exp. Biol. 202, 2951-2959. Weigel, G. (1941). Färbung und Farbwechsel der Krabbenspinne Misumena vatia (L.). Peitsch, D., Fietz, A., Hertel, H., de Souza, J., Ventura, D. F. and Menzel, R. Z. Vergl. Physiol. 29, 195-248. (1992). The spectral input systems of hymenopteran insects and their receptor- Wyszecki, G. and Stiles, W. S. (1982). Color Science, 2nd edn. New York: Wiley, based colour vision. J. Comp. Physiol. A 170, 23-40. New York. Rabaud, E. (1923). Recherches sur la variation chromatique et l’homochromie des Yokoi, T. and Fujisaki, K. (2009). Hesitation behaviour of Sphaerophoria arthropodes terrestres. Bull. Sc. Fr. Belg. 57, 1-69. spp. to avoid ambush by crab spiders. Naturwiss. 96, 195-200.

THE JOURNAL OF EXPERIMENTAL BIOLOGY