All the better to see you with

Giant and colossal squid have bigger eyes than any other living animals. A paper published in Current Biology last month asks why it is that they do when other animals get by with smaller eyes. Intriguingly, they suggest that it might be sperm whale predation that has driven both body and eye size in these massive invertebrates. Unfortunately, I think the authors tackle the problem from and adaptationist perspective and do not give alternative hypotheses due consideration.

A kraken fights with a leviathan in a diorama at the Museum of Natural History (image Wikimedia Commons)

Eyes are metabolically expensive organs to build and to maintain. So it's interesting that they are so prevalent in the deep sea where sunlight is weak or never reaches. But, in the deep, animals and other organisms make their own light. Indeed, it has been estimated that 80 - 90% of creatures in the deep sea are bioluminescent. Clearly then, making and detecting light are important for life below the sun's influence. But, most animals get away with eyes much smaller than those of giant and colossal squid.

Generally speaking, big eyes are more sensitive and provide better spatial resolution. But, the amount of light reaching the retina is dependent on the ratio of focal length (the distance between lens and retina) and pupil diameter (camera mavens will recognise this ratio as the f/stop value). In some cases smaller eyes can be more sensitive because they have a shorter focal length. With longer focal length, larger eyes have greater acuity and can increase sensitivity by increasing pupil size.

The paper examines just how much visual performance in the sea improves with increasing eye size and what visual strategies giant eyes are best suited for. They take into account the focal length and pupil size plus a raft of other factors such as the transmission of light in water and background illumination. They find that giant eyes are best suited to detecting the distant shapes of large moving objects illuminated by small bioluminescent organisms disturbed by the object's passage.

The authors argue that the only objects that are both large enough and important enough for giant and colossal squid to detect at distance are hunting sperm whales. The bioluminesence stimulated by moving whales would allow giant and colossal squid to see them at about 120 meters away. Unfortunately for the squid, this is inside the distance at which the whales would detect them with their sonar. The authors argue, therefore, that the squid must use their ability to detect whales at this distance to prepare for a coordinated escape response.

The authors, I'm sure, would acknowledge that their study is speculative and important questions remain. For instance, the maximum recorded sprint speed of hunting whales is about  9 ms^-1, which would give a giant squid more than 10 seconds of advanced warning of a whale closing at speed. Giant and colossal squid are unlikely to be strong enough swimmers to flee beyond sonar range, leaving them the only option of evasive maneuvers. Surely smaller eyes and shorter detection distances would still leave them ample time to prepare to outmaneuver the whale.

The authors rule out the possibility that giant and colossal squid use their eyes to detect prey because huge eyes offer only marginally better performance than much smaller eyes. However, they only consider individual prey items and looking at the published studies on the diet of giant squid, many of their prey species are schooling fish (e.g. Macruronus novaezelandiae, Micromesistius poutassou and Trachurus trachurus) and squid (e.g. Nototodarus sloanii, Ommastrephes bartramii and Todarodes sagittatus). Although detecting individuals of these species might not favour the evolution of giant eyes, schools of prey could easily reach sperm whale size and would also trigger bioluminescence as they move. 

On moonless nights fishermen at the surface are able to use the pattern of bioluminesence stimulated by schools of fish to distinguish among several species. It's possible that giant and colossal squid could use patterns of bioluminescence to determine whether it's being stimulated by prey or non-prey species or, of course, a hunting whale. Longer prey detection distances would seem to be a highly advantageous trait for fueling the fast growth rate of giant squid (reaching 150 - 250 kg in about 5 years).

In making their argument that the eye size of giant and colossal squid is unusually large, the authors contrast them with several other extant whales and fish. None of these extant species, though, are visual predators that hunt at great depth. The authors do also compare to the extinct ichthyosaurs, which had eyes of similar size and were probably visual predators that hunted at depth. They suggest that this is because ichthyosaurs had a similar need to detect the bioluminesence stimulated by large moving objects, perhaps pliosaurs or other ichthyosaurs.

None of these comparisons are truly fair, even the ecologically similar ichthyosaurs, because they don't take into account allometric scaling effects. When making trait comparisons among lineages you should always examine the trait within lineages. It is entirely plausible that the eyes of giant and colossal squid are large simply because they're scaled up versions of those in species with smaller body size. The authors claim that giant and colossal squid eyes are unusually large even for squid, but the paper they cite in support of this point only examines changes in eye size in a single species as it grows.

The problem with looking at the relationship between eye size and body size within a single species of cephalopod is that eye size as a proportion of body size decreases as they age. This is almost certainly not e case when you examine the relationship between body size and eye size among species. As in cephalopods, eye size in vertebrates generally decreases as a proportion of body size as individuals grow. But, eye size increases as you move from species with smaller body size to species with larger body size. Unfortunately, no such among species relationship has been published for cephalopods.

In a crude attempt to get an idea of the scaling relationship in squid, I searched the literature for reports of eye size that could be linked to a length measurement. I was able to find data in three species (Dosidicus gigas, Loligo opalescens and Illex illecebrosus), but eye size as a proportion of mantel length in giant and colossal squid was within the range of these species. Although my "analysis" should be taken with some salt (e.g. some values were estimated from graphs), it seems that giant and colossal squid eyes are not unusually large when their body size is taken into account.

Although I have strong doubts that the eyes of giant and colossal squid were selected for detecting hunting sperm whales, this study does provide some interesting information about the performance of eyes in the sea. Because deep-sea squid and their predators are so hard to observe, we really only have recourse to mathematical models to determine the selective pressures on predators and prey. But, we should never ever start with the assumption that the trait of interest is adaptive and then look for explanations.

Nilsson, D., Warrant, E., Johnsen, S., Hanlon, R., & Shashar, N. (2012). A Unique Advantage for Giant Eyes in Giant Squid Current Biology, 22 (8), 683-688 

DOI: 10.1016/j.cub.2012.02.031