Evolution, 60(12), 2006, pp. 2633–2642

HABITAT-SPECIFIC SENSORY-EXPLOITATIVE SIGNALS IN BIRDS: PROPENSITY OF DIPTERAN PREY TO CAUSE EVOLUTION OF PLUMAGE VARIATION IN FLUSH-PURSUIT INSECTIVORES PIOTR G. JABŁON´SKI,1,2,3,4 KELLY LASATER,5 RONALD L. MUMME,6,7 MARTA BOROWIEC,8,9 JAKUB P. CYGAN,10 JANICE PEREIRA,1,11 AND EWA SERGIEJ8 1 Arizona

Research Laboratories Division of Neurobiology, 611 Gould-Simpson Building, University of Arizona, Tucson, Arizona 85721 2 Centre for Ecological Research, Polish Academy of Sciences, Dziekanow Lesny, 05-092 Łomianki, Poland 3 Ewha Womans University, Department of Environmental Science and Engineering, College of Engineering, Seoul 120-750, Korea 4 E-mail: [email protected] 5 3823 Oxbow Village NW, Albuquerque, New Mexico, 87120 6 Department of Biology, Allegheny College, Meadville, Pennsylvania 16335-3902 7 E-mail: [email protected] 8 Department of Avian Ecology, Zoological Institute, University of Wroclaw, Sienkiewicza 21, 50-335 Wroclaw, Poland 9 E-mail: [email protected] 10 Institute of Zoology, Polish Academy of Sciences, Wilcza 64,00-679 Warszawa, Poland 11 Department of Entomology, University of Arizona, Tucson, Arizona 85721 Abstract. Sensory exploitation occurs when signals trigger behavioral reactions that diminish the receiver’s fitness. Research in this area focuses on the match between the signal’s form and the receiver’s sensitivity, but the effect of habitat on interspecific sensory exploitation is rarely addressed. Myioborus redstarts use conspicuous wing and tail displays of contrasting black-and-white plumage patches to flush dipteran insects, which are then pursued and captured in flight. Previous studies have shown that by increasing the distance at which insects perform an escape response, conspicuous visual displays improve the birds’ foraging performance. We tested the hypothesis that selection for a visual signal that maximizes prey escape distance under local habitat conditions can lead to the evolution of geographic variation in plumage pattern among Myioborus redstarts. Using models of foraging birds, we recorded the escape responses of Dipterous insects to a range of plumage patterns and background tones (from light to dark) to determine whether the plumage pattern that maximizes prey flushing is dependent upon that habitat (background) against which birds are viewed by their prey. Our results indicate that the effectiveness of a particular plumage pattern in flushing dipteran prey depends strongly on the background against which that plumage pattern is displayed, and darker habitat (background) conditions generally favor plumages with more extensive patches of white in the tail. However, the addition of white wing patches that imitate the plumage of the painted redstart (Myioborus pictus) generally increases insect escape responses but reduces the effect that tail pattern variation and background tone have on escape behavior. These experiments support the hypothesis that habitat-specific natural selection to enhance sensory exploitation of prey escape responses could produce geographic variation in plumage patterns of flush-pursuers. Key words.

Escape neurons, foraging, local adaptation, Myioborus, predator-prey, visual signaling. Received July 5, 2006.

Accepted August 22, 2006.

The evolution of signals may be affected by the environment (Endler 1992; Fleishman 1992; Marchetti 1993; Bradbury and Vehrencamp 1998), the sensory systems in the intended receivers (Dunning and Roeder 1965; Jackson and Wilcox 1990, 1993a,b; Fleishman 1992; Marchetti 1993; Ryan 1998; Wilczynski et al. 2001), and by sensory systems in organisms that are neither signalers nor the intended receivers of signals (Endler 1991; Simmons et al. 2001). Previous research in this area has typically characterized a signal as it is perceived by the receiver based on properties of the receiver’s sensory system. Only rarely is signal perception estimated from direct tests of the receiver’s behavioral responses in the relevant habitat conditions (e.g., Fleishman and Persons 2001). Signals that have evolved to match preexisting sensitivity of receivers through sensory drive/sensory bias/sensory trap or sensory exploitation (Endler 1992; Fleishman 1992; Marchetti 1993; Christy 1995; Semple and McComb 1996; Endler and Basolo 1998; Ryan 1998; Boughman 2002) are good candidates for such research. Our earlier studies on flush-pursuit foraging in birds

(Jabłon´ski 1999, 2001; Jabłon´ski and Strausfeld 2000, 2001; Mumme 2002; Galatowitsch and Mumme 2004; Jabłon´ski et al. 2006; Mumme at al. 2006) suggest that flush-pursuing birds and their prey could be used to study the combined effects of the receiver sensitivity and habitat properties on geographical variation of sensory-exploitative signals because they comprise a system with clear costs to receivers and with relatively well-understood neurobiological and adaptive bases for the receiver’s sensitivity and the signalers’ signals. Flush pursuers are avian predators that use conspicuous visual displays of contrasting plumage patterns to exploit insect escape behaviors (Root 1967; Harrison 1976; Fitzpatrick 1980; Robinson and Holmes 1982, 1984; Sherry 1984, 1985; Remsen and Robinson 1990; Sherry and Holmes 1997; Jabłon´ski 1999, 2001, 2002, 2003; Mumme 2002). The conspicuously displaying birds trigger activity in their prey’s descending neurons (P. G. Jabłon´ski, J. Talley, and N. J. Strausfeld, unpub1. ms.), causing prey to attempt escape earlier than would occur in responses to a more typical and less conspicuous insectivorous bird. This leads to escape flights

2633 䉷 2006 The Society for the Study of Evolution. All rights reserved.

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FIG. 1. Variability in tail-patch size and shape among Myioborus redstarts. (A) Tail of M. miniatus from Monteverde, Costa Rica. (B) Tail of M. torquatus from Monteverde, Costa Rica. (C) Tail and wing patches of M. pictus from Arizona. (D) Tail patches of M. pictus from Arizona. (E) Tail patch of M. pictus from Guatemala. (F) Tail patch of M. pictus from northern Mexico. (E) and (F) depict specimens from the British Museum of Natural History, London. (Photos A–D by P. G. Jabłon´ski; photos E and F by P. G. Jabłon´ski and S. I. Lee.)

or jumps elicited at larger distances to a moving predator (Jabłon´ski and Strausfeld 2000, 2001), which in turn leads to an increase of the number of insects pursued by birds (Jabłon´ski 1999; Mumme 2002). Although it is possible that capture success may decrease if displays stimulate escape responses at too great a distance (no data on this issue are available), conspicuous flush displays increase the frequency of parental feeding of nestlings (Mumme 2002), suggesting that any conceivable negative effects on capture success, if present, are outweighed by the positive effect of flush displays on the total number of insects available for pursuit. It has been proposed (Jabłon´ski 1999) that this sensory exploitation of insect escape responses is possible because the whole guild of common insectivorous predators, which are not flush pursuers but rather gleaners and peckers, exert selection pressures that maintain the prey’s sensitivity to approaching predator, a sensitivity that is exploited by the relatively infrequently encountered flush pursuers. Some of the flush pursuers, such as the Myioborus redstarts and the Rhipidura fantails, exhibit high inter- and intraspecific geographic variation in the pattern and extent of white plumage patches (Ford 1981; Blakers et al. 1984; Curson et al. 1994) that are conspicuously presented towards insect prey, including high numbers of Diptera (Cameron 1985; Barber et al. 2000). For example, the slate-throated redstart (M. miniatus), which is broadly distributed in Neotropical montane rainforests, displays high geographic variation in tail-patch size among subspecies (Galatowitsch and Mumme 2004; Mumme et al. 2006). Tail-patch size in the painted redstart (M. pictus) also changes from small in Guatemala (Fig. 1E) to large in northern Mexico and Arizona (Fig. 1C,F).

There is also geographic variation in tail-patch shape. The slate-throated redstart’s tail patch is formed by white tips of the outermost tail feathers, creating a more curved inner contour of the tail patch (Fig. 1A). This shape differs from that of the painted redstart or the collared redstart (M. torquatus: Fig. 1B), which have elongated white patches that extend laterally along the outermost two or three tail feathers. Unlike other Myioborus redstarts, the painted redstart possesses bright white wing patches that are displayed during flushpursuit foraging along with the contrasting tails (Fig. 1C). Using plumage manipulations, we have recently shown (Mumme et al. 2006) that geographic variation in tail-patch size in the slate-throated redstart reflects regional adaptation that enhances flush-pursuit performance by maximizing the number of insects flushed. According to one hypothesis (the prey-specific hypothesis; Mumme et al. 2006), differences in the prey species among geographical localities might have contributed to the evolution of geographic variation in the extent of white in the tail. However, the importance of the same prey taxon (Brachyceran Diptera) in the diet of such distantly related flush pursuers like Myioborus (Barber et al. 2000) and Rhipidura (Cameron 1985) and the documented similarities in anatomy of escape neurons among Brachyceran Diptera (King and Wyman 1980; Wyman et al. 1985; Bacon and Strausfeld 1986; Groenenberg and Strausfeld 1990; Milde and Strausfeld 1990; Jabłon´ski and Strausfeld 2001) are inconsistent with, but do not reject, the prey-specific hypothesis. According to another hypothesis (the habitat-specific hypothesis; Mumme et al. 2006), geographic variation in habitat conditions, which influence properties of the background against which insects view approaching birds, affects the

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flush-maximizing plumage pattern and contributes to the evolution of plumage pattern variability among flush pursuers. Habitats of Myioborus redstarts vary widely from light and sunny juniper-pine-oak woodlands of northern Mexico and Arizona to the dark montane tropical forests of South and Central America. Therefore, it is likely that the habitat-specific hypothesis may contribute importantly to the variation of plumage pattern in Myioborus flush pursuers. Here, we determine how size and shape of tail patches in Myioborus plumage and how the presence of contrasting patches in wings (as in the painted redstart) affect prey escape distance against light, intermediate, and dark backgrounds. From the results we propose predictions concerning the evolution and geographical variation of plumage pattern of flush pursuers in the framework of the habitat-specific hypothesis. MATERIALS

AND

METHODS

Study Areas The study was conducted in 2002–2004, during the months of April through August, in Cave Creek Canyon near the Southwestern Research Station (American Museum of National History) and in East Turkey Creek Canyon in the Chiricahua Mountains of Arizona USA (31⬚53.005⬘N, 109⬚12.334⬘W) at an elevation of 1650 m in a oak-juniper-pine woodland. The painted redstart is the only species of Myioborus that lives in the region. Additional experimental work was conducted in May–July, 2003–2004, at the Estacio´n Biolo´gica Monteverde in Monteverde, Costa Rica, where we have been studying a color-banded population of slate-throated redstarts since January 2000 (Mumme 2002; Mumme et al. 2006). Light Measurements of Bird Feathers and the Habitat To compare physical properties of habitats at Arizona and Costa Rica study sites, we determined brightness (in visible spectrum) of white and black tail feathers of the painted redstart and the slate-throated redstart against their foraging habitats at 49 sites in the juniper-oak-pine woodland of Arizona and 26 sites in the Costa Rican rainforest. We used a Canon (Tokyo) Rebel 2000 central-area partial (9.5% of picture area) light metering system in the shutter-priority AE program. We recorded what exposure times would have been required for a fan of three to five white and for a fan of three to five black tailfeathers located in front of the camera and for four points of the background against which the feathers were viewed. These sites were chosen to simulate foraging locations of birds. The measurements were conducted between 0800 and 1100 h in sunny weather. The fans of feathers filled the whole area used by the light measuring system. The camera was set at ISO 100 and f5.6. In the analysis we used the exposure times for white and black feathers paired with an average exposure time from the four habitat points at each site. Shorter exposure time corresponds with greater light levels, and longer exposure times indicate low light levels. We also conducted similar measurements for experimental models of foraging birds and artificial backgrounds, which are described below. We conducted spectrophotometric measurements at the Arizona and Costa Rica field sites using a USB2000 fiber optic

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spectrometer (Ocean Optics, Inc., Dunedin, FL) with OOIBase32 Software (Ocean Optics) and a portable Dell Notebook Inspiron 8100 (Dell Inc., Round Rock, TX). Spectral properties of light present in the locations of foraging birds in Arizona (N ⫽ 31 locations) and Costa Rica (N ⫽ 12) were represented as spectral distributions of relative (proportion of the maximum intensity observed at about 530 nm) intensity of light reflected by a white ceramic reference (white ceramic tile with reflectance spectrum gauged using correction from a comparison to the Ocean Optics standard: STAN-SSH). Reflectance spectra of white and black tail feathers of the painted redstart in Arizona (N ⫽ 7 white and N ⫽ 5 black feather coloration) and the slatethroated redstart in Costa Rica (N ⫽ 3 white and N ⫽ 3 black feather coloration) were measured in sun against dark background at the respective study sites using freshly collected feathers of each species in accordance with the standard methods (using transmission mode according to the OOIBase32 Spectrometer Operating Software Manual, Ocean Optics, Inc; www.OceanOptics.com). Contrasts between tailfeathers (white or black) and the habitat background were calculated according to the formula: [FeatherIntensity ⫺ MeanBackgroundIntensity] ⫼ [FeatherIntensity ⫹ MeanBackgroundIntensity] (Land and Nilsson 2002). The overall intensity of light (range 0–4000 units on the scope’s scale) reflected from the feathers and transmitted through feather structure (for bright backgrounds) was either a single measure at each location, or a mean from two or three such measurements (FeatherIntensity). The intensity of background light (MeanBackgroundIntensity) was an average from four to six measurements of the habitat against which the feathers were viewed at each location (N ⫽ 16 locations for white and black feathers of the painted redstart in AZ; N ⫽ 4 and N ⫽ 8 for black and white feathers, respectively, of the slatethroated redstart in Costa Rica). Experiments Using Idealized Bird Models Bird models To determine the effect of plumage pattern on escape behavior of prey, we tested insect responses to simple models of ‘‘idealized’’ Myioborus flush pursuers. Three series of models were created: one series represented the ‘‘corner’’ tail pattern similar to the slate-throated redstart (series miniatus; Fig. 2A). The remaining two series simulated the ‘‘edge’’ tail pattern similar to that found in the painted redstart (pictus models). These pictus models were presented either without (series pictus 1: Fig 2A) or with (series pictus 2: Fig. 2A) wing patches (6.3 cm2 total). Each series consisted of five models with varying extent of white in the tail ranging from none (model 0), very little white (model 1; about 1.7 cm2), lesser intermediate white (model 2; about 4.0 cm2), greater intermediate white (model 3; about 7.4 cm2), and extensive white (model 4; about 11.9 cm2). Model 3 in the pictus 2 series most closely approximated a typical painted redstart. Model 2 in the miniatus series approximated a typical slate-throated redstart from Costa Rica. By using models with a larger variation of white, which does not normally occur in Myioborus redstarts, we could determine whether a flushmaximizing (‘‘optimal’’) patch size exists. Models were constructed in accordance with Jabłon´ski and Strausfeld (2000) from stiff cardboard the size and two-di-

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FIG. 2. (A) Schematic representation of bird models used in experiments: (B) application of model approach toward an insect during the experiments and (C) details of the device to measure escape distances during the experiments.

mensional shape of a Myioborus redstart’s foraging display. The models were then painted with a base coat of flat black enamel paint (21211 Flat Black, Rustoleum, Inc., Vernon Hills, IL) and the tail and wing patches were painted with flat white enamel paint (7790 Flat White, Rustoleum, Inc). Models were attached at a 45⬚ angle to a 2-m rod that was rotated and advanced forward to simulate the hops and pivots of a foraging redstart (Fig. 2B, C). A second rod with 1 cm increments was used to measure the escape distance of the flies. The model approached an insect within a 45⬚ area from the center of the insects’ eye. The model on the end of the rod was extended through the slit in the backdrop to a starting position approximately 1 m from the fly. The model was alternatively rotated 90⬚ twice, then advanced forward approximately 10 cm. The moment a fly took flight, the model was stopped and the measuring rod was extended to the location where the fly had been and the distance was recorded. This procedure by Jabłon´ski and Strausfeld (2000) was subsequently used by Jabłon´ski and Strausfeld (2001), Galatowitsch and Mumme (2004), Jabłon´ski and McInerney (2005), Jabłon´ski and Lee (2006), and Mumme et al. (2006). We validated the use of these cardboard models by testing the response of flies at the Arizona study site to both a model painted redstart (model 3 in the pictus 2 series, Fig. 2A) and a natural looking and moving taxidermic mount of a painted redstart. The escape distance of flies in response to the cardboard models (20.6 ⫾ 4.9 cm; mean ⫾ SD) against natural habitats in Arizona did not differ (t58 ⫽ 0.53, P ⫽ 0.60) from

an escape distance in response to the taxidermic models (21.2 ⫾ 4.3 cm). Backgrounds Three background colors (white, black, and gray) were used to approximate two extremes of lighting conditions as well as an intermediate (gray) condition. To create the backgrounds, cloth of the appropriate color was stretched over a 1-m square wood frame with a vertical slit in the center to allow the model and rod to pass through (Fig. 2B). Effect of patch shape, size, and background on escape in Diptera (experiment 1) To determine the effect of tail-patch size and shape on prey escape reactions, we tested flies (Thricops, Muscidae, Brachycera, Diptera) under natural field conditions against white, gray, and black backgrounds with series miniatus, pictus 1, and pictus 2 models (Fig. 2; see Bird models for method of stimulus delivery) in shaded areas to prevent glare on the model. The order of models was random and the experimenter was unaware of which model was used. Each fly was tested once, and 21–73 flies/model/background were used. Effect of tail pattern and wing patch presence against natural backgrounds in Arizona (experiment 2) Would the conclusions from experiments against artificial backgrounds (exp. 1) also hold in the natural habitats of flush

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pursuers? To determine what effect the presence of wing patches has on the escape distance of Muscidae flies against natural habitat, we compared the pictus 1 and pictus 2 patch series using the natural background in relatively light habitats in the Chiricahua Mountains, Arizona. Each fly was tested once, and 25–37 flies were used for each model. Models of realistic M. miniatus in light and dark habitats (experiment 3) This experiment tested the hypothesis that dramatically different habitat background conditions of light and sunny Arizona versus dark and shady forests in Costa Rica should strongly affect the relationship between tail-patch size and escape distance in muscid flies, producing differences between Arizona and Costa Rica similar to the differences in the experiments using idealized models in artificial light and black backgrounds. We used natural variation, instead of the idealized expanded variation, of tail-patch size to obtain results directly relevant to adaptive explanations of geographic variation among subspecies of the slate-throated redstart. Models were prepared according to Galatowitsch and Mumme (2004) to imitate the natural extent of geographic tail patch variation in the slate-throated redstart: small patches in M. miniatus hellmayri, medium patches in M. m. comptus, and large patches in M. m. verticalis. Muscidae (Thricops sp. in Arizona and an unidentified species in Costa Rica) were tested according the methods described above. Each individual fly was tested only once. Muscidae in Costa Rica (n ⫽ 16–21 for each model) were tested in dark shady areas under forest canopy near canyon bottoms of the mountainous breeding area of the slate-throated redstart in Monteverde. Muscidae in Arizona (n ⫽ 45–53 for each model) were tested in areas near canyon bottoms in the territories of the painted redstart in the Chiricahua Mountains. Statistical Methods We used analysis of variance (ANOVA) to study the effect of independent variables (background tone, tail-patch size, or tail-patch shape) on escape distance. The escape distances were log-transformed (log(escape distance ⫹ 1 cm)) to remove correlation between mean and variance in the data (Zar 1999). Post-hoc comparisons were performed using Tukey test (Statistica ver. 4.5; StatSoft 1999). RESULTS Light Measurements of Feathers, Habitats, and Models Approximately tenfold differences in the exposure times for all measurements (feathers, models, and habitat backgrounds) between Costa Rica (Fig. 3C) and Arizona (Fig. 3A) show that Costa Rican habitats of the slate-throated redstart are much darker than the habitats of the painted redstart in Arizona. Independently of this difference in the absolute amount of light in the habitats, relative brightness of feathers in comparison with the average background against which they are viewed is different between Costa Rica and Arizona. Whereas 25% of exposure times for black feathers of the slate-throated redstart in Costa Rica fell below the level of the habitat light intensity (Fig. 3D: habitat light is at the level

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of lower quartile of feather brightness distribution), almost all of Arizona measurements of black feathers of the painted redstart were above the habitat level against which they were viewed (Fig. 3B: habitat light is at the level of minimum value for feathers). All exposure times for white feathers in Costa Rica were smaller than the local habitat, indicating that they would always contrast with the habitat (Fig. 3D). In Arizona, however, some of the exposure times of white feathers were longer than the local habitat’s exposure time, indicating that they might sometime be perceived as darker than the habitat against which they are viewed (Fig. 3B). These differences appear to be caused by larger and more numerous sunlit patches in the Arizonan than in the Costa Rican backgrounds against which the bird models, located in the shadow of tree crowns where redstarts typically forage, were viewed for the light measurements. Figure 3 also shows median exposure times for the models used in experiments 2–6 in Arizona, the medians for the three artificial backgrounds used in experiments 1–3 and 5 in Arizona, as well as the medians for cardboard bird models and the habitat in which experiment 3 was conducted in Costa Rica. Composition of light available in habitats of the two species showed the lowest intensity for UV light and the maximum intensity in the range of 500–560 nm (Fig. 4A,B). The reflectance of plumage of the two species was at the level of about 50–65% or at 0–5%, for white or black feathers, respectively, over most of the whole spectrum (Fig. 4C,D). Contrast between white feathers and the habitat background was higher in Costa Rica than in Arizona across the spectrum (Fig. 4E,F; upper lines). The opposite was observed for black feathers (Fig. 4E,F; lower lines). The models differed from the white feathers mainly in the narrow range of short waves. Experiments with Bird Models Effect of background, tail-patch size, tail-patch shape, and wing-patch presence (exp. 1) Background tone affected the relationship between tailpatch size and escape distance in the miniatus (Fig. 5A), pictus 1 (Fig. 5B), and pictus 2 (Fig. 5C) series (ANOVA two-way interactions F8,514 ⫽ 15.56, F8,557 ⫽ 9.21, and F8,541 ⫽ 5.53, respectively, all P ⬍ 0.0001). To estimate the effect tail-patch size and shape in the absence of wing patterns we compared insect responses to the models lacking wing patches, series miniatus and pictus 1 (Fig. 5A,B). There was a clear indication of a backgroundspecific optimal tail-patch size that maximizes escape distance for pictus 1 rather than for the miniatus models. First, the effect of background tone on the relationship between tail-patch size and escape distance was different for miniatus than for pictus 1 models (uniformly black model was not considered here: the three-way interaction F6,889 ⫽ 2.604, P ⫽ 0.017). Second, the relationship between tail-patch size and escape distance was different between miniatus (Fig. 5A) and pictus 1 models for black (two-way interaction F3,316 ⫽ 4.194, P ⫽ 0.006) and white (F3,371 ⫽ 4.245, P ⫽ 0.006), but not for gray (F3,202 ⫽ 2.130, P ⫽ 0.100) backgrounds, and Tukey comparisons that followed the two-way ANOVAs more clearly indicated presence of optimal tail-patch sizes for pictus 1 than for the miniatus models (Fig. 5A,B). For

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FIG. 3. Light measurements of habitats, plumage, and experimental models and backgrounds expressed in terms of exposure time for film speed of 100 ASA and aperture of f 5.6: (A) median (bar), upper and lower quartiles (box), and minimum and maximum value (line) of exposure times for white and black feathers of Myioborus pictus in its habitat in Arizona woodland in Chiricahua Mountains (n ⫽ 49); (B) relative difference in brightness between white and black feathers of M. pictus and the habitat in Arizona (n ⫽ 45); (C) exposure times for white and black feathers of M. miniatus and for its habitat in Costa Rican rainforest in Monteverde (n ⫽ 26). Note the difference in scale between (A) and (C). (D) Relative difference in brightness between white and black feathers of M. miniatus and the habitat against which the feathers are viewed in Costa Rica (n ⫽ 26). Black dots in (A) indicate medians for white (W) and black (B) color in experimental models (n ⫽ 16) and the artificial backgrounds used in experiments (n ⫽ 4–8). Black dots in (C) indicate medians for white (W) and black (B) color in experimental models and the background at experimental sites in Costa Rica (n ⫽ 3).

the black background, both miniatus and pictus 1 models with the largest tail patch maximized the escape distance. In this background, there was a more pronounced effect of patch addition to the display for patches imitating the shape of pictus series (difference between patch size 0 and 1; Fig. 5A,B). For white backgrounds, there was a significant effect of tail-patch size on escape distance in pictus 1 series only (F4,220 ⫽ 8.143, P ⫽ 0.000004; Fig. 5B), with the largest escape distance caused by tail-patch sizes 1 and 2. Finally, although the two series did not differ for gray background, a statistically significant peak of escape distance occurred only for pictus 1 models for tail-patch size somewhere between 1 and 3 (Fig. 5B). Taken together, these results indicate that the support for background-specific patch sizes that max-

imize escape distance was stronger for pictus 1 than for miniatus models. The effect of tail-patch size on escape distance depended on the presence of wing-patches (Fig. 5B,C; two-way interaction F4,1098 ⫽ 5.674, P ⫽ 0.0002), and this effect was independent of background tone (three-way interaction F4,1098 ⫽ 1.671, P ⫽ 0.101). Hence, the effect of tail-patch size on escape distance was more pronounced for pictus 1 (Fig. 5B) than for pictus 2 models (Fig. 5C) in all backgrounds (black, F4,387 ⫽ 3.150, P ⫽ 0.014; gray, F4,293 ⫽ 2.893, P ⫽ 0.023; white, F4,418 ⫽ 2.323, P ⫽ 0.056). For the white background, the maximum average escape distance (for tail-patch size 2) was significantly higher in pictus 1 than in pictus 2 models (Tukey test, P ⬍ 0.05; following the two-

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eral consequence of reducing the variation in escape distance in response to various tail-patch sizes, as in the artificial background experiments (Fig. 5). Models of realistic Myioborus miniatus in light and dark habitats (exp. 3) The difference in the shape of the curve (interaction term: F4,322 ⫽ 3.21, P ⫽ 0.024) between Costa Rica (Fig. 7, broken line) and Arizona (Fig. 7 solid line) was in the direction predicted from earlier experiments (Fig. 5): in the dark Costa Rican forests the maximal escape distance was triggered by models with larger patch size than in the light habitats of Arizona. DISCUSSION Habitat-Specific Selection of Tail-Patch Size

FIG. 4. Spectrophotometry of habitat and feathers of Myioborus pictus in Arizona and M. miniatus in Costa Rica: (A, B) distribution of intensity of light available in the habitats of Arizona (A; n ⫽ 31 sites) and Costa Rica (B; n ⫽ 12); (C, D) reflectance spectra of white (upper lines) and black (lower lines) plumage colors of M. pictus (C; means from n ⫽ 7 and n ⫽ 5 for whites and blacks, respectively) and M. miniatus (D; n ⫽ 3 and n ⫽ 3); (E, F) contrast of white (upper lines) and black (lower lines) feathers against habitats for M. pictus in Arizona (E; n ⫽ 16 and n ⫽ 16) and M. miniatus in Costa Rica (F; n ⫽ 8 and n ⫽ 4). Lines indicate average values and shaded areas in (A, B, E, F) indicate confidence intervals.

way ANOVA for white background), suggesting further that wing-patch presence decreases the escape distance. No such significant difference occurred for black or gray backgrounds. Taken together, these results show that wing-patch presence (in pictus 2 models) reduces the background-specific effect of tail-patch size on escape distance in flies. Effect of tail pattern and wing-patch presence against natural backgrounds in Arizona (exp. 2) To determine what effect the presence of wing patches has on the escape distance of Muscidae flies against natural habitat, we compared pictus 1 and pictus 2 patch series using the natural background in relatively light habitats in the Chiricahua Mountains. Escape distance in response to pictus 1 models depended on the tail-patch size (F3,100 ⫽ 4.36, P ⫽ 0.006), with tail patch 2 producing the largest escape distances (Fig. 6). The presence of the wing patch eliminated (interaction F3,222 ⫽ 2.98, P ⫽ 0.032) any significant effect of tail-patch size on escape distance (pictus 2, F3,122 ⫽ 0.86, P ⫽ 0.46). Hence, the addition of wing patches has the gen-

Artificial background tone simulated habitat lighting conditions and significantly influenced the plumage pattern and tail-patch size that maximizes prey flushing. In conditions with darker backgrounds, larger white patches become better for flushing insects, but against lighter backgrounds smaller patches fared better. This relationship was significantly more pronounced for models with the idealized pictus type of tailpatch shape than for the idealized miniatus tail-patch shape. Our previous studies have shown that effects of color pattern alterations in bird models on insect escape distance correspond to the effects of these plumage alterations on foraging success in birds (Jabłon´ski 1999; Mumme 2002; Mumme et al. 2006). Therefore, the existence of habitat-specific tailpatch size that maximizes flush distance of prey indicates that dipteran prey can generate habitat-specific natural selection for the size and shape of tail patches that maximize foraging performance in flush-pursuit birds. Although our results suggest that the patches along external tail edges (like the pictus 1 series) may be more susceptible to this selection, experiments using realistic miniatus models in the birds’ natural habitat (Galatowitsch and Mumme 2004) suggested a tail-patch size that maximizes the escape distance in this species. Models that have wing patches (pictus 2 series) produced little variation in escape distances in comparison to redstart models without wing patches (pictus 1 series). Therefore, when wing patches are absent in a flush pursuer, there should be a stronger background-specific selection for a certain tail-patch size that maximizes escape distance. The main experiments used dipterous insects from one locality (Arizona) and from one family only. Typically, the descending neurons believed to mediate escape responses in Diptera (the giant descending neuron cluster; King and Wyman 1980; Wyman et al. 1985; Bacon and Strausfeld 1986; Groenenberg and Strausfeld 1990; Milde and Strausfeld 1990; Jabłon´ski and Strausfeld 2001) are evolutionarily conserved, suggesting similar tuning properties among many different families. This evolutionary conservation among dipteran prey, together with similarity of the effect of tail-patch size on escape distance in Diptera and Homoptera at the same locality in Costa Rica (shown previously by Galatowitsch and Mumme 2004; Mumme et al. 2006), are all consistent

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FIG. 5. Effect of tail-patch size (none and sizes 1–4), tail-patch shape, background tone (black, gray, white), and the presence of wing patches on escape distance in Diptera (Muscidae; n ⫽ 21–73 for each patch size treatment) for models in the miniatus (A), pictus 1 (B), and pictus 2 (C) series. Within each background, the groups of homogenous means (Tukey post-hoc test, P ⬍ 0.05) are marked with letters in a different font format for each background: lowercase normal letters for black, lowercase italic letters for gray, and uppercase letters for white backgrounds. Means and standard errors are shown.

with the habitat-specific hypothesis. Comparison of escape distance as a function of tail-patch size in very dark habitat locations of Costa Rica (Fig. 7) with comparable data from average habitat locations (Galatowitsch and Mumme 2004; Mumme et al. 2006) is also consistent with the predictions from artificial background experiments (Fig. 5). This comparison shows that in average light conditions (Galatowitsch and Mumme 2004; Mumme et al. 2006) the tail-patch size that maximizes flushing is at the level characteristic for the local population of the slate-throated redstart (M. m. comp-

FIG. 6. Effect of tail-patch size (1–4) and presence (broken line; pictus 2 models) or absence (solid line; pictus 1 models) of wing patches on escape distance of Diptera (Muscidae) in response to redstart models in the pictus 1 and pictus 2 series in the natural habitat of painted redstarts in Arizona (n ⫽ 25–37 for each patchsize treatment). The groups of homogenous means (Tukey post-hoc test, P ⬍ 0.05) are marked with letters for the models lacking wing patches. Means and standard errors are shown.

tus), whereas in darker conditions the tail-patch size that maximizes escape distance is larger (Fig. 7). All this evidence is consistent with the habitat-specific hypothesis for the evolutionary explanation of plumage variation among flush pursuers. However, the effect of local prey-specific sensitivity on the evolution of differences among flush-pursuing birds (prey-specific hypothesis), especially in birds that consume a variety of arthropod prey (e.g., Sherry 1984, 1985), cannot be excluded. Our conclusions are based on experiments with cardboard models that had lower reflectance than white feathers in the UV range. However, this is the range of light that is the least available in the habitat that Myioborus redstarts occupy (Fig. 3A,B), and therefore the difference between models and feathers with regard to the white patch contrast against the habitat should be relatively minor, even for insects with UV-

FIG. 7. Effect of tail-patch size of models portraying natural variation in tail patch size of the slate-throated redstart (Myioborus miniatus) on the escape distance of Muscidae in natural habitats in Costa Rica (CR: broken line; n ⫽ 16–21 for each patch-size treatment) and Arizona (AZ: solid line; n ⫽ 45–53 for each patch-size treatment). Means and standard errors are shown.

SENSITIVITY OF PREY AND COLORS OF PREDATORS

sensitive vision. Accordingly, there was no difference in the escape distance between tests using cardboard models and taxidermic mounts. Therefore, we argue that the nature of the effects of habitat background and the white patch size and shape on flushing insects could be generalized from our results to the natural situation of foraging birds. Predictions of Evolutionary Trends among Flush Pursuers Diptera are important insect prey for at least two genera of flush pursuers (Myioborus: Jabłon´ski and Strausfeld 2000; Barber et. al. 2000; Rhipidura: Cameron 1985) and are the most responsive to the flush displays (Pereira 2005). We showed that their sensitivity can potentially create selection on an avian flush pursuer for a habitat-specific plumage pattern that maximizes the visual signal used to stimulate and flush potential prey. Plumage coloration in many birds (Price 2002; Roulin 2004), including flush pursuers (Caughley 1969; Craig 1972), strongly depends on genetics, and there is no reason to believe that the conspicuous plumage features of the Myioborus displays are different with this respect. Therefore, the habitat-specific selection acting on the genes that affect plumage coloration may lead to evolutionary diversification of these heritable plumage patterns. Although this selection may be in conflict with antipredatory trends toward better camouflage, presence of white patches in the plumage of Myioborus redstarts does not always lead to higher visual detection (Jabłon´ski 2004). Assuming evolution of plumage pattern for maximization of prey flushing according to the habitat-specific hypothesis, we predict (1) that flush pursuers in darker habitats evolve larger white tail patches, (2) that selection for a specific tailpatch size is stronger in more uniform light conditions in the foraging habitat, (3) that habitat-specific selection may be stronger when the tail patch extends along the lateral edges of the tail, and (4) that selection for a specific tail-patch size is strong in species lacking wing patches or other plumage patterns that are presented during flush displays. The last prediction also implies that tail-patch size among flush pursuers with conspicuous wing patches should be analyzed separately from flush pursuers without wing patches. The whole set of predictions relies on the assumption that larger escape distances result in a greater susceptibility of the prey to predation by redstarts. None of the previous field experiments provide evidence to question this assumption (Jabłon´ski 1999; Jabłon´ski and Strausfeld 2000, 2001; Mumme 2002; Galatowitsch and Mumme 2004; Mumme et al. 2006), which has been recently confirmed for Brachyceran Diptera (Pereira 2005). In summary, we have shown the potential for dipteran prey to cause habitat-specific evolution of sensory-exploitative signals in avian predators. Flush-pursuit foraging creates a unique possibility for studying how a clearly defined selective mechanism for enhanced foraging performance interacts with other factors that shape the diversity of plumage patterns among birds (Savalli 1995; Roulin 2004). ACKNOWLEDGMENTS Funding was provided by the National Science Foundation (grant no. 0133874 to PGJ and a Research Experience for

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Undergraduates supplement to this grant); Komitet Badan´ Naukowych KBN (grant no. 6PO4F06321 to PGJ and grant no. 3PO4F05225 to JPC); Kosciuszko Foundation Fellowships to PGJ and JPC; Association for the Study of Animal Behaviour grant to PGJ; the Committee for Research and Exploration of the National Geographic Society (grant 719402 to RLM); a fellowship from the Korean Science and Engineering Foundation International Program 2005–2006 to PGJ and SDL; and a private contribution by D. Utterback, who let us use his car. PGJ was hosted at the laboratory of N. J. Strausfeld for the duration of the study and at the laboratory of S. D. Lee for the duration of preparation of the final manuscript, while on unpaid leave from the Centre for Ecological Studies, Polish Academy of Sciences. We thank the director, W. Sherbrooke, and staff of the Southwestern Research Station (SWRS) of the American Museum of Natural History for housing and lodging and help in many matters regarding field experiments. Advice from N. J. Strausfeld, J. Douglass, and S. I. Lee is acknowledged. We thank field assistants M. Borowiec, L. Grove, C. Hall, A. Kirschel, A. Moors, T. Samper, J. Yerger and laboratory assistant, G. Gelsey. The help from the volunteers at the SWRS is acknowledged. We are grateful to M. Hidalgo of the Estacio´n Biolo´gica Monteverde (EBM) for housing and for allowing us to work on EBM properties. LITERATURE CITED Bacon, J. P., and N. J. Strausfeld. 1986. The dipteran giant fiber pathway: neurons and signals. J. Comp. Physiol. A 158:529–548. Barber, M. B., D. R. Barber, and P. G. Jabłon´ski. 2000. Painted redstart (Myioborus pictus). No. 258 in A. Poole and G. Gill, eds. The birds of North America. Academy of Natural Sciences, Philadelphia, PA, and The American Ornithologists’ Union, Washington, DC. Blakers, M., S. J. J. F. Davies, and P. N. Reilly. 1984. The atlas of Australian birds. Royal Australasian Ornithologists Union, Melbourne Univ. Press, Melbourne, Australia. Boughman, J. W. 2002. How sensory drive can promote speciation. Trends Ecol. Evol. 17:571–577. Bradbury, J. W., and S. L. Vehrencamp. 1998. Principles of animal communication. Sinauer Associates, Sunderland, MA. Cameron, E. 1985. Habitat usage and foraging behavior of three fantails (Rhipidura: Pachycephalidae). Pp. 177–191 in A. Keast, H. F. Recher, H. Ford and D. Saunders, eds. Birds of eucalyptus forests and woodlands: ecology, conservation, management. Royal Australian Ornithologists Union and Surrey Beatty and Sons, Sydney, Australia. Caughley, G. 1969. Genetics of melanism in the fantail, Rhipidura fuliginosa. Notornis 16:237–240. Christy, J. H. 1995. Mimicry, mate choice, and the sensory trap hypothesis. Am. Nat. 146:171–181. Craig, J. L. 1972. Investigation of the mechanism maintaining polymorphism in the New Zealand fantail, Rhipidura fuliginosa (Sparrman). Notornis 19:42–55. Curson, J., D. Quinn, and D. Beadle. 1994. Warblers of the Americas: an identification guide. Houghton Mifflin, Boston, MA. Dunning, D. C. and K. D. Roeder. 1965. Moth sounds and the insect catching behaviour of bats. Science 147:173–174. Endler, J. A. 1991. Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Visual Res. 31:587–608. ———. 1992. Signals, signal conditions, and the direction of evolution. Am. Nat. 139:S125–S153. Endler, J. A., and A. L. Basolo. 1998. Sensory ecology, receiver biases and sexual selection. Trends Ecol. Evol. 13:415–420.

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