J. Zool., Lond. (2000) 252, 187±195 # 2000 The Zoological Society of London Printed in the United Kingdom

Variation of eye size in butter¯ies: inter- and intraspeci®c patterns

Ronald L. Rutowski Department of Biology, State University, Tempe, AZ 85287-1501, U.S.A. E-mail: [email protected] (Accepted 6 October 1999)

Abstract Differences in behaviour, such as the mate-locating tactic, may favour the evolution of interspeci®c and intersexual differences in the structure of the visual system. This notion was tested by examining the relationships between eye size, body size, sex and mate-locating tactic in 16 of butter¯ies. The 16 species were grouped in eight phylogenetically close pairs that differed in the mate-locating tactic displayed by the males. Eye size was characterized by eye surface area, which was estimated from a set of linear eye measurements made on 10 individuals of each sex in each species. The major ®ndings were that eye surface area was positively correlated with body size both among and within species, males have larger eyes relative to their body size than females, and after controlling for body size and phylogeny, interspeci®c differences in the mate-locating tactic of males does not explain interspeci®c variation in the size of male eyes or in the magnitude of sexual difference in eye size. The optical and behavioural consequences of variation in eye size with body size and sex will await a better understanding of how eye structure varies with size within and between species.

Key words: eye size, butter¯ies, , body size, mate-locating tactic

INTRODUCTION trolled for phylogeny) revealed that diurnal and visually hunting species have consistently larger eyes with more In , the shape and size of the compound eye ommatidia, greater binocular overlap and more well- in¯uences many features of the visual ®eld including its de®ned frontolateral acute zones than species that hunt dimensions, acuity and sensitivity. For example, the nocturnally using non-visual cues (Bauer & Kredler, ¯atter the surface of an eye, the ¯atter the array of facet 1993). lenses that gather light for the underlying photorecep- At the intersexual level, the eyes of male are tors and the smaller the angle between the optical axes typically larger and morphologically more complex than of adjacent facets. This means that the region of the those of females (e.g. Beersma, Stavenga & Kuiper, 1977; visual ®eld examined by a ¯attened part of the eye is Zeil, 1983). This sexual dimorphism is generally inter- more densely sampled and so is seen with greater acuity preted as the adaptive result of the critical role of the (Land, 1997). As for eye size, the area of the cornea will visual system in males in detecting mates and acquiring set limits on the relationship between the number and matings (Thornhill & Alcock, 1983; Land, 1989, 1990, size of facet lens (i.e. a larger eye can have more facets, 1997). For instance, male blow¯ies chase females at high larger facets, or both than a small eye), which will in speeds during courtship. This behaviour favours males turn determine the size of the visual ®eld, its overall with regions of the eye that are both morphologically acuity and the sensitivity of the eye. and neurally specialized for the in-¯ight tracking of An adaptationist's logic leads to the expectation that rapidly moving objects. Not surprisingly, male blow¯ies interspeci®c and intersexual differences in the character- have larger eyes than females with morphological istics of the compound eye which affect the visual ®eld modi®cations that enhance visual system resolution and should re¯ect differences in behaviour, life style and sensitivity in the frontal region (Land & Eckert, 1985). habitat preferences that make different demands on the In butter¯ies, males search for females visually and, visual system. This prediction has been well supported like blow¯ies, engage in rapid pursuit ¯ights when they (Horridge, 1977; Wehner, 1981; Land, 1989, 1990, 1997; ®nd them (Rutowski, 1991). In contrast, after mating, Warrant & McIntyre, 1992, 1993). As a relevant females ¯y about searching for non-moving oviposition example of interspeci®c differences, a comparative study sites using visual (Rausher, 1978; Prokopy & Owens, of 27 species of predaceous carabid beetles (not con- 1983) and chemical cues (Dempster, 1992). Given these 188 R. L. Rutowski

Table 1. The species pairs, their taxonomic af®liations, the mean HFL and EESA (from the 10 individuals of each sex), and their categorization with respect to male mate-locating tactic. Superspeci®c is based on Scott (1986). The letter in parentheses following each binomen is used to indicate this species in Fig. 3

HFL (mm) EESA (mm2) Subfamily Family (tribe) Species ,<,

Hesperidae Hesperiinae venatus (A) 2.27 2.30 2.33 2.83 Perch (Dennis & Williams, 1987) Thymelicus lineola (B) 3.76 3.6 1.8 2.25 Patrol (Pivnick & McNeill, 1985) Papilionidae Papilioninae Papilio machaon (D) 5.64 5.48 5.38 5.92 Perch (Wickman, 1992a) (Papilionini) Papilio rutulus (E) 5.85 5.55 6.02 6.89 Patrol (Scott, 1975; R. L. Rutowski, pers. obs.) Lycaenidae Lycaeninae Polyommatus icarus (F) 1.88 1.92 1.01 1.26 Perch (Lundgren, 1977) (Polyommatini) Celastrina argiolus (G) 1.68 1.72 0.8 1.03 Patrol (Wickman, 1992a; R. L. Rutowski, pers obs.) Nymphalinae cinxia (H) 3.4 3.14 2.01 2.47 Perch (Wickman, 1992a) (Melitaeini) Melitaea diamina (I) 2.93 2.8 1.54 2.0 Patrol (Wickman, 1992a) Nymphalidae Nymphalinae Mellicta athalia (J) 3.1 2.9 1.74 2.22 Patrol (Wickman, 1992a) Eurodryas aurinia (M) 2.93 2.73 1.27 1.67 Perch (Wickman, 1992a) Nymphalidae Nymphalinae Issoria lathonia (N) 3.91 3.7 2.89 3.74 Perch (Wickman, 1992a) (Argynnini) Argynnis paphia (O) 5.17 5.04 4.89 5.78 Patrol (Magnus, 1950)

Nymphalidae Satyrinae Pararge aegeria (P) 2.82 2.61 1.7 2.03 Perch (Davies, 1978; Wickman & Wiklund, 1983) Aphantopus hyperantus (Q) 3.0 2.76 1.4 1.87 Patrol (Wickman, 1992a) Satyridae Satyrinae Coenonympha pamphilus (R) 2.78 2.4 0.91 1.26 Perch (Wickman, 1992b) Coenonympha tullia (T) 2.95 2.63 1.04 1.49 Patrol (Wickman, 1992b) sexual differences in behaviour selection should favour have dramatic frontal acute zones (Sherk, 1978). Hence, eyes in male butter¯ies that are larger than those of I predict that male perchers should have larger eyes females. Larger eyes have either more facets, larger than male patrollers. Moreover, perching is unlike any facets or both, any of which will enhance the probability behaviour seen in female butter¯ies, while patrolling is of detection, recognition and tracking of small moving similar in many respects to the search for oviposition objects. Consistent with this expectation, Yagi & sites displayed by females. I predict, then, that the Koyama (1963) reported that male butter¯ies have sexual difference in eye size in perchers will be greater larger eyes than females, but they did not rigorously than that in patrollers. control for the sexual differences in body size that are Here, I extend Yagi & Koyama's (1963) observations common in this group or phylogeny (Rutowski, 1997). and test these predictions by examining species and However, does the speci®c tactic used by males to sexual differences in eye size among a group of 16 species search for mates affect eye structure? Male butter¯ies of butter¯ies that differ in male mate-locating tactics. use two main tactics to locate females: patrolling and Unlike previous comparative studies, an effort was made perching (for review, see Scott, 1974; Rutowski, 1991). here to control explicitly for body size and phylogeny. When males patrol, they ¯y about the environment This test was modelled after Wickman's (1992a) study searching for females mostly at sources and that demonstrates a relationship between male mate- oviposition sites. When males perch, they remain sta- locating behaviour and wing size and shape in butter¯ies. tionary and wait for females to pass nearby. Females Again, the predictions examined were as follows. that pass nearby are seen and rapidly approached and (1) Within species, males should have larger eyes than courted. These two classes of strategies are expected to females regardless of the mate-locating tactic typical for make different sorts of demands on a male's visual the species. system. Perchers, I argue, should bene®t more from a (2) Males that use a perching tactic to locate mates large visual ®eld and one that is relatively high in acuity should have larger eyes than males that use a patrolling throughout to maximize the distance at which passing tactic. females, males and predators can be detected over a (3) The sexual difference in eye size should be larger in large range of arrival directions. A large and acute perchers than patrollers. visual ®eld can be achieved through having many large facets. In contrast, mobile patrollers will often be able to approach conspeci®cs closely at foodplants and MATERIALS AND METHODS oviposition sites and so may have high acuity more restricted to the forward facing part of the eye. In line The species and their behaviour with these expectations, dragon¯ies that perch when hunting have more uniform facet diameters across the Comparative tests of selectionist hypotheses about the eye than those that patrol while hunting, which tend to effects of behaviour on the evolution of morphology are Eye size in butter¯ies 189

Table 2. The eye and leg dimensions that were measured and used to calculate estimated eye surface area (EESA). All eye dimension are illustrated in Fig. 1

Name Abbreviation Description

Eye height EH Distance from top of eye to bottom of eye along a line parallel to the posterior margin of the eye Eye radius 1 ER1 Distance from ventral corner of eye to apparent edge of eye along a line parallel to the posterior margin of the eye; as viewed from below Eye radius 2 ER2 Distance from ventral corner of eye to apparent edge of eye along line parallel to median margin of the eye; as viewed from below Eye radius 3 ER3 Distance from ventral corner of eye to apparent edge of eye along a line that bisects the angle formed by the median and posterior margins of the eye; as viewed from below Eye span ES Greatest distance between the posterior margin of the eye and the medial margin of the eye as viewed from below the head Hind femur length HFL Length of the femur of the hindleg from its insertion into the trochanter to its distal end more rigorous if the effects of ancestry are controlled Estimation of eye surface area (Felsenstein, 1985; Harvey & Pagel, 1991). In this study, phylogeny was controlled for by examining the relation- To estimate eye surface area for an individual, it was ship between eye size and behaviour in 8 matched pairs assumed that the shape of a butter¯y's eye can be of species. Within each pair, the species differed in male approximated by the shape of part of a sphere or mate-searching tactic but were relatively recently spheroid. This assumption allowed the use of 5 linear diverged behaviourally and morphologically from a measurements (Fig. 1) and mensuration formulae to common ancestor as indicated by the phylogeny used by estimate the surface area of a single eye as follows. First, Wickman (1992a) and by taxonomy. Within pairs, both the eye height (EH) and the mean (MER) of the 3 eye species were in at least the same subfamily and some- radii (ERs 1, 2, and 3) was used to determine if the eye times in the same genus (Table 1). The mate-locating best approximated a sphere (EH = 2*MER), or an tactics used by a species was determined either from oblate (EH < 2*MER) or prolate (EH > 2*MER) literature accounts or from ®rst-hand observations spheroid. This determined the appropriate surface area (Table 1). Males of some species display both mate- formula to use in calculating the surface area of a sphere locating strategies (e.g. Pararge aegeria, Davies, 1978; or spheroid of these dimensions (Hodgeman, 1960). Wickman & Wiklund, 1983; Coenonympha pamphilus, Second, ER1, ER2 and ES were used to calculate the Wickman, 1985a); because these males experience selec- angle formed by ER1 and ER2 using standard trigono- tion pressures arising in the context of perching, like metric formulae. This angle was described as a fraction Wickman (1992a), I placed these species in the percher of 3608 and used to characterize the proportion of a category. sphere or spheroid surface area represented by the eye surface. The product of this fraction and the surface area calculation produced an estimate of eye surface The specimens area (EESA) in mm2. To evaluate the accuracy of this procedure, EESA Morphological measurements were made on specimens was compared to actual surface area measurements for of all species except Papilio rutulus in the collection of a nymphalid butter¯y not in this group ( the Swedish Museum of Natural History in Stockholm leilia) (Fig. 2). Direct measures of surface area were (Naturhistoriska Riksmuseet). I studied P. rutulus speci- made from corneal spreads as described in Wallace mens from the Hasbrouck Collection at Arizona & Rutowski (2000). The estimated and actual eye State University. Ten males and 10 females of each surface areas were signi®cantly positively correlated species were examined. When the series permitted, for males (r2 = 0.427, n = 14, P < 0.01), females specimens were used that were from a restricted geogra- (r2 = 0.667, n = 13, P < 0.0006), and both sexes phical area (e.g. SkaÊne) and collected only at 1 time of combined (r2 = 0.645, n = 27, P < 0.000001). The slope the year (e.g. May±July). of the combined data set was very close to 1 (0.98) but EESA was c. 5% below the actual eye surface area. Eye and body size measurements

A set of 6 measurements was made on each specimen Statistical analysis (Table 2, Fig. 1). These included a measure of body size (hind femur length, HFL) and several eye measurements Estimated eye surface areas and data on hind femur that I used to estimate eye surface area. All measure- length were log transformed before being statistically ments were made using an ocular micrometer on a analysed to normalize their distribution and to adjust dissecting microscope. for scale effects. In addition, estimates of eye surface 190 R. L. Rutowski

Fig. 1. Eye measurements made from below (left) and from the side (right). ER, eye radius; ES eye span; EH, eye height (see also Table 2).

3.8 of individuals de®ned by sex and species (Table 3). ) 2 Males EESA was signi®cantly positively correlated with HFL 3.6 2 Females in all specimens (r = 0.729, n =320, P < 0.001), and 3.4 there were signi®cant differences between categories in the location of the curves (P < 0.029). However, the 3.2 interaction between HFL and category in explaining EESA was not signi®cant, which indicates that the 3 slopes across all groups were homogeneous (P > 0.069). 2.8 Based on these results, all subsequent analyses testing for differences among species pairs, sexes and male 2.6 tactics either incorporated HFL as a covariate or used Estimated eye surface area (mm 2.4 the residuals describing the departure of each individual 2.5 2.7 2.9 3.1 3.3 3.5 3.7 from the regression line shown in Fig. 3. Measured eye surface area (mm2) There are two standouts in Fig. 3. First, both males Fig. 2. Direct measures of eye surface area as compared with and females of the Ochlodes venatus had eyes EESA for Asterocampa leilia. Upper solid line, that expected if that, compared to the other species, were relatively large the estimates matched perfectly the measured values of eye compared to their HFL. The feature that causes this surface areas; lower solid line, the regression line calculated species to be so different is not sex speci®c nor found in from the data, which indicates that the estimation procedure the other skipper examined. Perusal of the raw data slightly underestimates eye surface area. suggests that O. venatus has a small HFL relative to other measures of its size including forewing length. The second standout group is the Coenonympha females area were square-root transformed to reduce them to 1 which are well below the regression line. dimension. The slope of the regression line for males was 0.769 and for females was 0.762. This suggests that in butter- ¯ies, eye surface area shows a slight negative allometry RESULTS with body size. To test the prediction that males have larger eyes than Figure 3 shows that for all 320 specimens taken together females, an ANOVA was run with sex and species as there is a positive correlation between EESA and HFL. independent categorical variables and HFL as a An analysis of variance (ANOVA) was run to see if covariate (Table 4). Body size was controlled because in there were signi®cant differences in the relationship most butter¯ies females are larger than males (Rutowski, between HFL and EESA for the 32 possible categories 1997). The ANOVA revealed a signi®cant effect of sex Eye size in butter¯ies 191

0.5

All: r2 = 0.729,P <0.001

0.4

0.3

0.2 (eye surface area)) √ Log ( 0.1

0

–0.1 0.1 0.20.3 0.4 0.5 0.6 0.7 0.8 Log (hind femur length) Fig. 3. Transformed values of EESA and HFL plotted against one another for all specimens measured. Letters, species identity of the individual plotted as indicated in Table 1. Upper case letters, males; lower case letters, females. Solid line, least squares regression line that best ®ts the total data set.

Table 3. ANOVA results analysing the effect of body size on Table 4. Results of ANOVA examining sexual differences in EESA and the differences between categories. Each category EESA. The results show that with HFL as a signi®cant represents a speci®c sex and species of butter¯y (e.g. females of covariate, EESA varies signi®cantly with both sex and species. Coenonympha pamphilus). The results show a signi®cant effect However, the signi®cant sex6species interaction indicates that of body size on EESA, signi®cant differences in EESA among the sexual dimorphism in EESA is not uniform among species. categories, and that there is no signi®cant interaction between See text for details the effect of body size and category on EESA. See text for details Source SS d.f. MS F-ratio P

Source SS d.f. MS F-ratio P HFL 0.061 1 0.061 245.9 < 0.001 Sex 0.260 1 0.260 1052.5 < 0.001 HFL 0.040 1 0.040 148.6 < 0.001 Species 0.990 15 0.066 267 < 0.001 Category 0.013 31 < 0.001 1.59 0.029 Species6Sex 0.038 15 0.003 10.1 < 0.001 Category6HFL 0.012 31 < 0.001 1.44 0.069 Error 0.068 256 < 0.001 Error 0.071 287 < 0.001 on EESA, and in all species the adjusted least squares This analysis revealed signi®cant differences within mean EESA for males was larger than that for females. pairs of species in the EESA of males. Moveover, there There was also a signi®cant effect of species, which was a signi®cant effect of strategy on EESA but because indicates that some species have relatively larger eyes the pair6strategy interaction was signi®cant, the effect than others. The interaction between species and sex of strategy is dif®cult to interpret. Consistent with this was also signi®cant, which indicates that the extent to signi®cant interaction, the direction of the differences which male eyes are larger than those of females varies between males within matched pairs showed no clear signi®cantly among species. trend (see Table 6). To test the prediction that males in perchers have Finally, the prediction that the sexual difference in larger eyes than males in patrollers, an ANOVA was EESA is greater in patrollers than perchers was run with matched pair and strategy as independent evaluated as follows. The mean residuals for males and categorical variables and HFL as a covariate (Table 5). females of each species were extracted. Within each 192 R. L. Rutowski

Table 5. Results of ANOVA examining the effect of mate- Table 6. Analysis of how, within the phylogenetically locating strategy on EESA in males. With HFL incorporated a matched pairs, male mate-location strategy affects the magni- covariate in the analysis, EESA varies signi®cantly among the tude of differences in size-adjusted eye size between the sexes. phylogenetically matched pairs and with strategy. However, See text for details because of the signi®cant strategy6pair interaction the direc- tion of the effect of strategy within matched pairs is not Mean residual consistent as shown in Table 6 Pair Strategy Males Females Difference Source SS d.f. MS F-ratio P Ochlodes venatus (A) Perch 0.162 0.124 0.072 HFL 0.032 1 0.032 142.735 < 0.001 Thymelicus lineata (B) Patrol 70.037 70.109 0.038 Pair 0.102 7 0.015 65.675 < 0.001 Papilio machaon (D) Perch 0.041 0.011 0.03 Strategy 0.006 1 0.006 28.307 < 0.001 Papilio rutulus (E) Patrol 0.069 0.022 0.047 Strategy6pair 0.117 7 0.017 75.422 < 0.001 Polyommatus Perch 0.044 0.006 0.038 Error 0.039 143 < 0.001 icarus (F) Celastrina argiolus (G) Patrol 0.037 70.011 0.048 Melitaea cinxia (H) Perch 0.031 70.039 0.07 Melitaea diamina (I) Patrol 0.023 70.049 0.072 species, the sexual difference in mean residuals was Mellicta athalia (J) Perch 70.008 70.091 0.083 calculated to get a measure of the magnitude of sexual Eurodryas aurinia (M) Patrol 0.034 70.043 0.077 dimorphism in EESA adjusted for body size. Within Issoria lathonia (N) Perch 0.068 70.005 0.073 each phylogenetically matched pair the magnitude of Argynnis paphia (O) Patrol 0.062 0.018 0.044 this sexual difference between patrollers and perchers Pararge aegeria (P) Perch 0.049 70.014 0.063 Aphantopus Patrol 0.013 70.077 0.09 was compared (Table 6). The expectation according to hyperantus (Q) the original hypothesis was that within each pair this Coenonympha Perch 70.028 70.147 0.119 sexual difference should be greater in perchers than in pamphilus (R) patrollers. A paired t-test was used to determine if the Coenonympha Patrol 70.02 70.135 0.115 expected trend existed in the direction of these tullia (T) differences. The prediction was not supported (t = 0.894, P > 0.2, 6 d.f.). that the evolution of visually guided behaviours is constrained in small species compared to larger species. DISCUSSION In particular, small species may be constrained to tactics that reliably place males very close to where females are Eye size varies with body size likely to be or appear, for example, by close-range visual inspection of larval foodplants for newly emerged The results con®rm a previous report (Yagi & Koyama, females. Within species, large males may have an advan- 1963) that larger butter¯ies have larger eyes both among tage in visually mediated competition for mates. Also, if and within species. This means that eye performance is small eyes have small facets to maintain acuity while probably related to body size, but exactly how requires sacri®cing sensitivity, they may be disadvantageous in an understanding of how facet number, facet size and low illuminance environments compared to large eyes. eye shape interact with eye size (e.g. Zollikofer, Wehner, Interestingly, the owl butter¯ies, which are among the & Fukushi, 1995). Yagi & Koyama (1963) found that largest butter¯ies in the world, are known have crepus- among about 80 species of including cular activity patterns (Srygley, 1994; Freitas et al., butter¯ies, skippers and moths, larger species typically 1995). To date, however, there have been no studies have larger facets and that, in males and females of two examining size-related patterns of variation in behaviour pierid butter¯ies, individuals with larger eyes also had that might suggest such effects arising from size-related larger facets. Facet size above the minimum needed to variation in sensory system performance in butter¯ies or limit diffraction problems is related to the light other insects. capturing ability of each ommatidia, and so larger eyes should be more sensitive and better able to discriminate signals from background noise (Warrant & McIntyre, Males have larger eyes than females 1992, 1993). On the other hand, if facet number also increases with eye size, larger eyes may have, depending As predicted, in all 16 species, males have eyes that, on the radius of curvature of the eye, a larger visual even with body size controlled, are up to 30% larger in ®eld, higher overall resolution, or both. Hence, both surface area than those of females. Because females are within and among species, larger butter¯ies should, often larger in body size than males, the absolute because of their larger eye size, have greater overall difference in eye size may typically be even greater. visual sensitivity, larger visual ®elds, higher acuity, or There are two points to be made from this result. First, some combination of these. given the diversity of butter¯ies examined, this is prob- Both patterns of facet variation could in¯uence the ably the ancestral condition in butter¯ies and perhaps evolution of behaviour. Interspeci®c, size-related varia- all Lepidoptera given that sexual differences in eye size tion in the performance of a visual system may mean are also found in many moths (Yagi & Koyama, 1963). Eye size in butter¯ies 193

Second, the sexual difference in eye size means that eye size, Sherk (1978) found more pronounced acute males invest relatively more in the production and zones in the eyes of dragon¯ies that patrol when maintenance of their visual system than do females. hunting for prey compared to those that perch when This supports the view that sexual differences in beha- hunting. Also, eye size does not take into account viour put different demands on the visual systems of potential behaviourally related variation in the architec- males and females favouring divergence in the structure ture of those parts of the retina and central nervous of their eyes. The larger eyes of males are most probably system that gather and analyse visual information, such a product of sexual selection on males favouring indivi- as that found in butter¯ies (Swihart, 1967; Bernard & duals with large eyes in the context of mate detection Remington, 1991) and other insects (Zeil, 1983; and tracking during chases (Thornhill & Alcock, 1983; Strausfeld, 1991). Also, although their eyes show the Zeil, 1983). same general pattern of variation in size with body size Because they have eyes with a larger surface area than and sex, skippers have superposition eyes while, the rest females, males may have either more facets, larger have apposition eyes (Horridge, Giddings & Stange, facets, or both. Wallace & Rutowski (2000) show that in 1972). The implications of this variation in eye structure a nymphalid, Asterocampa leilia, males have no more for patterns of variation in eye size are not clear. facets than females but their facets are larger, especially Second, generalizations about differences in the visual in the frontal and dorsal frontal region of the eye. problems faced by patrollers and perchers may have However, again the precise consequences for vision been too simple and ignored ecological factors and cannot be predicted without knowing if there are sexual subtle behavioural differences within strategies that differences in the radius of curvature of the surface of might need to be considered to make correct predic- the eye. If there is no sexual difference in how the radius tions. For example, there is interspeci®c variation in of curvature of the eye changes over the surface of the how exactly males position themselves at perch sites eye, then larger facets mean that each eye in males has a used in mate location. Some perch on or near the larger visual ®eld with greater overall sensitivity and ground with the visual system directed upward ability to distinguish optical signals from background (Wickman, 1985) while others perch on tree trunks noise. However, if there are sexual differences in the facing down (Asterocampa , D. Rice, pers. comm.) radius of curvature regionally or overall, these differ- These differences in perch preferences as well as prob- ences must be understood to evaluate the effect of able differences in the typical ¯ight paths of passing sexual differences in facet size on vision. Males often females mean a general prediction that applies to all have a larger radius of curvature (= more ¯attened perchers may not be realistic. surface), especially in certain eye regions, than females, Third, the design of the test may have been ¯awed. and so have more acute vision at least regionally (Land Behavioural categorization of the species relied on (1) & Eckert, 1985; Land, 1997). Such regional specializa- published accounts of mate-locating tactics that are tions are especially likely in those parts of the eye that sometimes only weakly documented, and (2) placing are used in mate detection, tracking and recognition by males with alternate tactics into perchers. Inaccuracies males (Land, 1997). More information is needed on in behavioural categorization could have obscured real these aspects of butter¯ies before the details of sexual differences in eye structure between males that use differences in eye size in butter¯ies can be understood different tactics. Also, the imperfect correlation from either a proximate or an ultimate perspective. between measured and estimated eye surface areas (see Methods) could mean that the estimation technique was able to detect real differences between perchers and Comparison of perchers and patrollers patrollers. Finally, given the roles that the eyes play in many Contrary to the predictions made in the introduction, other aspects of the lives of these , the selection males that perch do not have larger eyes than males that pressures arising in the context of mate detection might patrol, and the sexual dimorphism in eye size is not be overridden by stronger selection pressures acting on greater in perching species than in patrolling species. eye design in contexts such as overall illuminance levels, There are several possible reasons why these predictions tracking mates and the detection of predators and adult were not met. food resources. First, there may be differences in the structure of the None the less, this study suggests three promising visual system between patrollers and perchers, but, as areas of research that should improve our under- the discussion up to this point makes clear, because the standing of how mate-locating tactics and visual system potential effects of variation in eye size on variation in structure and performance interact at both proximate visual system performance may be diverse, useful and ultimate levels of analysis. One is the study of general statements about the visual ®eld characteristics regional variation in the structure of the butter¯y eye of individuals with small vs large eyes are tenuous at and how it affects the structure of the male's visual ®eld best. For example, eye size alone does not measure and, in turn, his behaviour. Information of this sort is interspeci®c differences in the regional specialization of largely lacking for butter¯ies (for review, see Land, 1997) the eyes that might re¯ect interspeci®c variation in but can be obtained using established techniques (Land behaviour. Although he did not discuss differences in & Eckert, 1985). The second potentially interesting 194 R. L. Rutowski area for research is to gather more information on the Land, M. F. (1989). Variations in the structure and design of actual performance and placement of the visual system compound eyes. In Facets of vision: 90±111. Stavenga, D. G. & by males engaged in mate-location in the ®eld. The third Hardie, R. C. (Eds). Berlin: Springer Verlag. Land, M. F. (1990). The design of compound eyes In: Vision: is the relationship between visual ®eld structure and coding and ef®ciency. Blakemore, C. (Ed.). Cambridge: Cam- body size both within and between species. bridge University Press. Land, M. F. (1997). Visual acuity in insects. Ann. Rev. Entomol. 42: 147±177. Acknowledgements Land, M. F. & Eckert, H. (1985). Maps of the acute zones of ¯y eyes. J. comp. Physiol. 156: 525±538. The Department of Zoology, University of Stockholm, Lundgren, L. (1977). The role of intra- and interspeci®c male:male interactions in Polyommatus icarus Rott and some other species and especially Dr P.-O. Wickman and Professor of blues (Lycaenidae). J. Res. Lepid. 16: 249±264. Christer Wiklund provided generous material and intel- Magnus, D. B. E. (1950). Beobachtungen zur Balz und Eiablage lectual support during this study. The Swedish Museum des Kaisermantels Argynnis paphia L. (Lep., Nymphalidae). of Natural History provided access to specimens. Finan- Z. Tierpsychol. 7: 435±449. cial support for this research was provided by the Pivnick, K. A. & McNeill, J. N. (1985). Mate location and mating Swedish National Research Council and the U.S. behaviour of Thymelicus lineola (Lepidoptera: Hesperiidae). 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