Step 1 : Measure ( or Compute ) Light Step 2 : Compute Cone Quantal Catches

A key to understanding animal behavior is knowledge of the sensory information animals extract from their environment. For visually motivated tasks, the information animals obtain through their eyes is often assumed to be essentially the same as that perceived by humans. However, known differences in structure and processing among the visual systems of different animals clearly indicate that the world seen by each is different. A well-characterized difference between human and other animal visual systems is the number of types and spectral sensitivities of their photoreceptors. We are developing a technique, functional substitution, that exploits knowledge of these differences to portray for human subjects, colors as they would appear through the photoreceptors of another animal. In a specific application, we ask human subjects to rank hues of male threespine stickleback (Ggasterosteus aculeatus) throats viewed through stickleback photopigments. We compare these ranks to ranks of the same throat hues viewed through normal human photoreceptors. We find essentially no difference between the two sets of rankings. This suggests that any differences in human and stickleback rankings of such hues would result from differences in post-receptoral neural processing. Using a previously developed model of stickleback neural processing, we established another ranking of the hues which was again essentially the same as the rankings produced by the human subjects. A growing literature indicates that stickleback do rank such hues in the evaluation of males as potential mates or threats. Although our results do not demonstrate that humans and stickleback use the same mechanisms to assess color, our experiments significantly failed to show that stickleback and human rankings of throat hues should be different. Nevertheless, a comparison of all these rankings to ranks derived from subjective color scoring suggests that color scoring may utilize other cues and should thus be used cautiously. Introduction A pair of animals exposed to identical stimuli may perceive those stimuli quite differently. There are several causes for such disparate perceptions. For instance, there may be differences in the anatomical structures directing energy to the sensory receptors, differences in the types and number of those receptors, and/or differences in the neural processing of the receptors’ outputs. A challenge for biologists interested in understanding why animals behave as they do is the impenetrability of each animal’s Umwelt, or perceptual world (Uexküll 1957). To discern the causes of behavior, it is sometimes necessary to determine how the sensory capabilities of study species differ from those of humans, and to interpret the way these differences affect perception of, and ultimately responses to, the surrounding environment (Hughes 1999). Nowhere is the need for such determinations more apparent than in the study of vision (e.g. Bennett et al. 1994, Vorobyev et al. 1997; Fleishman et al. 1998; Fleishman & Endler 2000; Vorobyev et al. 2001; Kelber et al. 2003). Nevertheless, potential differences in perceptual capabilities are often assumed (or hoped) to be minimal in research on visual signaling, and human perceptual categories are sometimes used as the sole descriptors of stimuli (e.g. McRobert & Bradner 1998; Kilner & Davies 1998; Saino et al. 2003; Duckworth et al. 2003). Given the number of factors that sculpt perceptions, the presumption that human perception is an adequate substitute for that of another animal is dangerous at best. How can we know when human observers can be used fruitfully as surrogates for study subjects while investigating animal biology? One way to address the question is to design experiments that take advantage of known differences between human and non-human sensory capabilities and to quantify the effects of those differences. Improvements in technology used to display visual information have enabled us to simulate particular aspects of the perceptions of other animals. For instance, we can present synthetic stimuli that generate in human subjects the same sensory neuronal activity that occurs in study animals perceiving natural stimuli. Such simulations may improve understanding of how animals process the information in physical stimuli to make decisions resulting in overt behavior. Here we use this method to explore color perception of the threespine stickleback, (Gasterosteus aculeatus) a species that is rapidly becoming a model system for the study of evolution in general (Foster & Bell 1994; Schluter 2000; McKinnon & Rundle 2002; Foster & Baker 2004), and of communication systems and behavioral evolution in particular (e.g. Tinbergen 1951; Rowland 1994; Foster 1995; Foster et al. 1998; Olson & Owens 1998; Huntingford 2003). A feature of the threespine stickleback that has generated particular interest is the male nuptial signal. Although males exhibit mosaic nuptial coloration usually including -in human perceptual terms -a blue eye, red-orange throat, and a blue-green back (Rowland 1994; Bakker & Mundwiler 1994; McLennan 1996), it is the red element of the signal that has drawn the most attention. This signal has been argued to attract females, to serve as an index of male condition, to inhibit territorial intrusions by adjacent males, and most recently, to function in assortative mating between members of stickleback species pairs (e.g. Rowland 1994 for review; Rowland et al. 1995a,b; Baube et al. 1995; Baube 1997; McLennan 1996; Boughman 2001; Smith et al. 2004). The sensory system of isolated freshwater populations of the threespine stickleback has also been suggested to evolve in response to environmental conditions, specifically as a consequence of signal masking by humic acids. Where humic acids make water opaque, stickleback male throats typically appear black rather than red (Reimchen 1989; McDonald et al. 1995; McKinnon 1995; Scott & Foster 2001), and there is evidence of a parallel shift in the visual system (Boughman 2001). Within populations, male stickleback can exhibit considerable variation in the extent (area of fish and degree of color saturation) of the nuptial signal. This variation may be used by females as a criterion for mate choice, although the relationship has proven complex (e.g. Milinski & Bakker 1990; Bakker & Mundwiler 1994; Rowland 1994; Bolyard & Rowland 1996; Candolin 1999). Some of the complexity may be due to the way in which the development of the red coloration has been measured. The degree of redness (frequently referred to as ‘brightness of red coloration’ or just ‘brightness’ in the stickleback literature) has generally been assessed only through human judgements (e.g., Bakker 1986; McLennan & McPhail 1989; Milinski & Bakker 1990; Bakker & Milinski 1991). More recently, researchers have attempted to utilize objective means to assess coloration using spectrometric measurements of slide photographs (Wedekind et al. 1998) or digital photography (Candolin 1999, 2000; Braithewaite & Barber 2000). These methods rely indirectly upon the human visual system because both color film and the pixels of digital cameras record only the information that a standard human observer would extract upon viewing a captured scene. Consequently the methods may remove any effects of differences among human observers in the perception of stickleback colors, but they do not circumvent the more important potential effects of differences between human and stickleback perceptions of stickleback colors. Colorimeters and cameras can produce objective determinations of whether or not one stickleback throat is ‘redder’ than another. However, these redness values are not necessarily any more relevant to stickleback perceptions than are more direct human assessments (please note the distinction between photometers or colorimeters, and spectrometers or spectroradiometers; colorimeters and photometers are designed specifically with concern for human vision). In the threespine stickleback literature, human assessments have been justified by a supposed similarity between the absorption spectra of human photopigments and the absorption spectra of stickleback photopigments (Frischknecht 1993; McKinnon 1995; Kunzler & Bakker 2001). However, as shown in Fig. 1, there are potentially significant differences between human and stickleback pigments. Here we explore the effect of these pigment differences on the relative rankings of ‘redness’ of male stickleback throats.