In their recent Journal of Experimental Biology paper on mottle camouflage patterns of cuttlefish and the visual background stimuli that evoke them, Chiao et al. state that ‘the mottle body pattern works by the principle of background matching’ (p. 188) (Chiao et al., 2010). ‘Mottle’ and ‘disruptive’ patterns doubtless contribute to camouflage in the animal kingdom – see Hugh B. Cott's classic Adaptive Colouration in Animals [referenced in Chiao et al. (Chiao et al., 2010)] – and the main contribution of Chiao et al.'s recent paper is to have classified the patterns worn by young cuttlefish during experiments with artificial backgrounds [figures 4–7 in Chiao et al. (Chiao et al., 2010)] according to granularity characteristics.
However, the fact is that none of the small cuttlefishes in the 19 photographs of experiments designed to test their statement is ‘matching’ the background. All stand out because average reflectance (albedo) of the body surface is different from average background reflectance; the one instance where the cuttlefish comes close to tone matching on a background critically darker than the others [figure 6A and supplementary figure S3 in Chiao et al. (Chiao et al., 2010)] is explained in terms of a ‘key’ switch from ‘mottle’ to ‘disruptive’. The terms ‘tone matching’ and ‘brightness contrast’ – universal phenomena – appear nowhere in the paper.
The cephalopod chromatophore system effecting camouflage has been widely explored in the past. Its structure is modular. Generation of brightness contrast ‘mottles’ of given granularity involving lateral inhibition is one kind of brain function with known location [for an account of the results of brain lesion experiments, see Packard (Packard, 1995a) and figure 10 in Packard (Packard, 1995b)]; neuromuscular gain controls for neutral density screens that modulate tone matching is another. The octopus in the middle and lower photographs of figure 3 in Packard (Packard, 1988) illustrates this functional separation so instructively that I (we) have reproduced them several times in the last 40 years. Text alongside the three photographs summarizes the matching principles.
Movie 1 in supplementary material (sub-adult Sepia officinalis from the Bay of Naples filmed against a plain unchanging background) comprises the same separation of functions in a cuttlefish under experimental conditions (exposure to CO2-bubbled seawater). The ‘mottle’ ‘template’ of Chiao et al. (Chaio et al., 2010) remains the same until near the end of the 20 s movie – i.e. spatial frequency (granularity) settings (but not energy levels) are unaltered. The screening function changes rapidly and over the extremes of its range – incidentally also turning the animal from ‘mottle’ to ‘uniform’.
Although not stated by Chiao et al. (Chiao et al., 2010), the set of chromatophores producing these dramatic changes from light to dark and back, and responsible for tone matching in the normal animal, is the same as (or currently indistinguishable from) the ‘small splotches of expanded dark chromatophores’ [said to be ‘roughly equal’ in ‘number and size’ to the light ‘splotches’ (p. 189)] in the static detail of the cuttlefish skin [figure 2A in Chiao et al. (Chiao et al., 2010)]. They are functionally the same as those creating the ‘chronic general mottle’ (or ‘trellis’) of the octopus. They contribute (1) to brightness contrast in the high-frequency band of the ‘mottle’ or ‘stipple’ and (2) to overall grey level in the lowest frequency band (body-wide dimension) through spatial recruitment of screening chromatophores (compare middle image with top and bottom images in Fig. 1), and not as described on p. 188 of Chiao et al. (Chiao et al., 2010).
Full descriptions may be found in my previous papers [pp. 94–95 of Packard (Packard, 1988); pp.114–119 of Packard (Packard, 1995b)]. [The general mechanism illustrated in Fig. 1 was explained previously as ‘variations in the state of contraction of chromatophores’ that produce ‘changes in the proportion of light and dark on the network of patches and grooves from one moment to the next’ (Packard and Sanders, 1971). NB The citations to my other work (Packard, 1982; Packard, 1995a) by Chiao et al. (Chiao et al., 2010) are without relevance.]
So why did Chiao et al. apparently miss the failure of the system to match the albedo in experiments with artificial backgrounds [figures 4–7 in Chiao et al. (Chiao et al., 2010)], and why did it fail?
The Chiao et al. paper makes a false distinction between ‘morphological’ and ‘functional’ approaches (p. 187). What is termed ‘morphological analysis’ is in fact pictorial analysis. We are thus two steps removed from the natural; experimenters' attention is directed elsewhere. Visuo-motor relationships may well be operating outside the normal dynamic range; why were 1000 lx light levels chosen for the photographs and not altered during experiments? 1.07 and 1.03 klx (p. 190), unlikely even in the shallows of its natural habitat, may be enough to blind the tone-matching function of European Sepia officinalis. Choosing a procedure in which ‘each animal image was cut out from its context’ (p. 192) and reporting total energy spectra for ‘background’ pixels and relative energy spectra for ‘animals’ [see figures 4–7 in Chiao et al. (Chiao et al., 2010)] may help to account for not noticing the lack of matching.
In conclusion, the experiments reported by Chiao et al. are too static. They do not reflect the dynamic nature of cephalopod camouflage nor its literature. Moreover, there are dozens of simple interventions for testing whether or not screens and mottles are functionally different – e.g. altered illumination, electronic flash, anaesthetics (such as CO2 or alcohol). Information is easy enough to come by, with better communication between experimental subject and participant observer – what I call ‘letting the animal tell its own story’ – and also between one side of the Atlantic and the shores of the Mediterranean. [NB Previous written and illustrated accounts of cephalopod body patterns over the last century have been exhaustively catalogued (Borrelli et al. 2006).]
