An important and repeated claim (Abramson 2003; Bailey 2020) concerning Turner’s work is that he may have discovered honey bee color vision, which would be attributed incorrectly to the Austrian physiologist and Nobel-Prize winner Karl von Frisch. Turner published a series of experiments on the capacity of bees to see colors in 1910 (Turner 1910), while von Frisch’s classical paper on this topic was published 4 years later (Frisch 1914). Before this publication, von Frisch advertised his findings in short communications (e.g., Frisch 1913) but without providing a precise account of his experiments, which were described in detail for the first time in 1914 (Frisch 1914).
Color vision is defined as the capacity to distinguish colored surfaces based on their different chromatic contents, independently of intensity differences (Wyszecki and Stiles 1982). Before von Frisch, several scientists suggested that bees may see colors (e.g., Lubbock 1883; Forel 1901; Lovell 1910). Yet, none of them provided the precise experimental evidence showing this capacity as in all cases the demonstration that color choice was independent of differences in intensity was absent. Von Frisch, on the contrary, provided this demonstration using achromatic gray cardboards of variable intensity, which he opposed to the specific color cardboards to which his bees were trained (Figure 4a). He showed that bees learned to associate different color cardboards with a reward of sucrose solution, and that in choosing a rewarded color, they distinguished it from different levels of achromatic gray cardboards, some of which displayed an intensity similar to that of the color trained (Figure 4a). He used 16 colored cardboards varying from violet to red and purple (as seen by humans). This method proved that bees could see the majority of his cardboards as colored surfaces, except in the case of red, which was confused with a black cardboard (Frisch 1914). Later, Kühn extended the demonstration of bee color vision to the ultraviolet range using spectral lights produced by a mercury lamp. In this way, it was demonstrated that bees can see and discriminate colors in the range of 300 nm (ultraviolet) to orange-reddish (650 nm) (Kühn 1924).
The physiological basis for this capacity is the presence of three types of spectral photoreceptors in the bee retina, which set the basis for their trichromatic color vision (Daumer 1956). Their sensitivity peaks are located at 344 nm in the short-wave (ultra violet) region of the spectrum (S receptor), 436 nm in the middle-wave (blue) region (M receptor), and 544 nm in the long-wave (green) region of the spectrum (L receptor), respectively (Autrum and Zwehl 1964; Menzel and Blakers 1976) (Figure 4b).
Four years before the appearance of von Frisch’s massive work on honey bee color vision in 1914 (188 pages and 24 figures) (Frisch 1914), Turner published a brief account termed Experiments on Color Vision of the Honey Bee (22 pages, 3 drawings) (Turner 1910) where he explicitly addressed the question of whether honey bees are able to see and distinguish colors. He defined this question as “a matter of much theoretical importance for the correct interpretation of the relations of insects to flowers” (Turner 1910). The article summarized 32 brief experiments and observations performed in the field during 6 days (July 12 to 18, 1910).
Turner used artificial stimuli (Figure 5), which he placed among blossoms of Melilotus sp., where he detected many bees foraging at a time (Turner 1910). In all cases, he baited the stimuli with honey to attract the bees. He performed three series of experiments, varying the type of stimuli used to train the bees: cardboard discs, cardboard cones (or cornucopia), and cardboard boxes with a small opening, which allowed bees to enter to collect the honey (Figure 5).
The stimuli that were rewarded with honey were made unfortunately of red cardboard. Although we do not have the spectral reflection curve of the red he used, the choice of human red made them probably achromatic to the bees. At that time, Turner could not know that bees are blind to red colors. Although there is no question that bees can see such stimuli (Chittka and Waser 1997; Reisenman and Giurfa 2008), and that they can be trained to achromatic (e.g., black) discs and patterns (Giurfa and Menzel 1997), it is probable that in his experiment he was scrutinizing achromatic vision rather than true color vision. In some experiments, he presented blue or green non-rewarded alternatives to prove that bees remained truthful to the red rewarded stimuli but without proper controls it is difficult to prove that bees were choosing to avoid a non-rewarded chromatic (blue, green) stimulus rather than choosing a rewarded achromatic (red) stimulus.
His experiments showed, in any case, that bees used both visual and olfactory cues in their choice behavior. They approached the stimuli attracted by visual cues (red surface, shape), but in the absence of honey odor and, eventually, scent marks (Free 1987), they rejected them, until their enhanced appetitive motivation moved them to accept it. This shows that in most of Turner’s experiments, not only visual cues but also olfactory ones were determinant.
To sum up, Turner did not demonstrate color vision in bees before von Frisch. The choice of red as the rewarded color in all his experiments was unfortunate, but the most important point is the absence of demonstration, available in von Frisch’s work, that visual-stimulus choice was unaffected by variations in the achromatic dimension of stimulus intensity. Had he opposed his red stimuli to black (or dark gray) ones, he may have discovered—as von Frisch did (Frisch 1914)—that bees confused them, and thus that what he was observing was not a case of true color vision. Interestingly, Turner was aware of this problem; he explicitly wrote, when discussing his findings, “whether this is a true color vision or simply a greyness discrimination is no easy question to answer.” Yet, he preferred to conclude that his findings revealed true color vision based on the observation that bees preferred the red stimuli both under the sunshine and under the shadow. Clearly, he knew that it was necessary to control this aspect but he did not perform such a control, probably because the experiments were done under naturalistic conditions and during a very short period.
There are, nevertheless, other merits in Turner’s work, which refer to the way in which he conceived the behavior of the bees. He explained the choice of his artificial stimuli in terms of “meaning acquisition” and even stated that “those things [the stimuli] had acquired a meaning; those strange red things had come to mean ‘honey bearers’, and those strange green things and strange blue things had come to mean ‘not-honey bearers’.” This account reminds the Pavlovian notion of conditioned stimuli (CS) being associated with unconditioned stimuli (US) (Pavlov 1927) and with the principle of stimulus substitution stating that the CS acquires the value of the original US as a result of conditioning (García-Hoz 2014). In this way, Turner anticipated fundamental principles of associative-learning theories. Such elaboration was absent in von Frisch’s work.