Puffin vision is tuned to the exacting task of taking small prey items in winter, not fish in summer. This may render them vulnerable to collisions underwater.
The visual fields of Common Guillemots Uria aalge and Atlantic Puffins Fratercula arctica: foraging, vigilance and collision vulnerability. Martin, G.R. & Wanless, S. 2015. IBIS. DOI: 10.1111/ibi.12297
The principal tasks that have shaped the vision of birds are foraging and predator detection. We investigated vision in two closely related species, expecting to find that they had very similar visual fields. But we were in for a surprise.
The main perceptual challenges of foraging are accurate bill placement and accurate timing of bill contact with a food item. The bill has to be opened at exactly the right time in order to seize a prey item. These tasks can be controlled by the way the image of an object expands as it is approached and this means that the bill must be placed within the binocular field of view. Birds which do not require accurate bill placement for feeding have eyes which sit high in the head and allow all round vision for the detection of predators, but in most birds the eyes are slightly forward to provide the cues for accurate bill placement.
Subtle differences in visual fields have been found even in closely related species and these differences reflect very fine tuning of vision to quite nuanced differences in the tasks of foraging. Among ducks, for example, there are differences in visual fields between those species whose foraging can be completed without visual guidance (e.g. Northern Shovellers Anas clypeata) and those which are selective grazers (e.g. Eurasian Wigeons A. penelope) (Guillemain et al. 2002). Among Ibises visual fields differ according to whether the birds forage in water and soft substrates or take items from the surface in dry habitats (Martin & Portugal 2011).
As part of a project to build up a comparative data base on the vision of birds which forage in different ways (Martin 2014), we have now investigated visual fields in two species of auks; Atlantic Puffins Fratercula arctica and Common Guillemots Uria aalge. Both species are well known for feeding almost exclusively on small shoaling fish, and during the breeding season it is easy to observe them carrying fish back to their nests.
I carried out the work with Sarah Wanless on the Isle of May, where Sarah has been investigating seabird ecology for many years.
We predicted that both of these auks would have similar visual fields which would also be similar to those of other birds that take evasive prey by lunging at individual items. In such birds the binocular field is typically rather narrow (between 20-30 ° wide) and extending vertically by about 100 ° or more. The bill is positioned somewhere near or just below the centre of the binocular region (Martin 2014). For example, this kind of visual field occurs in Great Cormorants Phalacrocorax carbo which take evasive prey at close range underwater (White et al. 2007).
Our measurements presented us with a surprise. We were only half right. The Guillemots did follow our prediction; their binocular region is long and thin with the bill tip projecting below the centre. But the Puffins were quite different. Their visual field is very much like that of an owl or a passerine bird. It is broad, in fact its maximum width of 49 ° is just about the same as that of a Tawny Owl Strix aluco, and slightly less than those of passerines, which have the broadest binocular fields of all birds (Troscianko et al. 2012). Also, in Puffins, the region of maximum binocular width is angled forwards and upwards and in fact we showed that the eyes themselves are angled slightly upwards above the horizontal, something which is readily seen in the photographs (Figure 1).
Why should these two species of Auks be so different? They apparently face the same kind of perceptual challenges when foraging, both take small fish of approximately the same size and in similar circumstances. How can the perceptual tasks of their foraging be so different that they have resulted in the evolution of such different vision?
The answers seems to lie in what the birds do when we no longer see them, when they leave the coastal habitat and head out to sea for the winter months. At this time Puffins either switch or broaden their diets.
Mike Harris and collaborators have recently shown (Harris et al. 2015) that outside of the breeding season Puffins take a much wider range of food items than during the summer. Winter items include small crustacea, polychaetes and squid, as well as fish. We suggest that these prey items present a much more exacting challenge, and suggest that they are detected in silhouette from below using the broader part of the binocular field, with the bill swung upwards to grab it once it has been detected. Guillemots, as far as we know, prey upon small fish all year and so for them the challenges of foraging do not change.
The role of dietary changes and different foraging techniques within the annual cycle have already been shown to influence the vision of shorebirds which probe in the winter and take more surface prey in the summer (Martin & Piersma 2009).
There is, however, a twist to this story. Our visual field measurements were done in air. When a bird dives its visual fields shrink in both width and height. This is because in water the cornea can no longer act as a lens. It has been shown that the magnitude of this effect can be quite dramatic in penguins (Martin & Young 1984), in Humboldt Penguins Spheniscus humboldtii it nearly abolishes binocular vision in the direction of the bill, even though the field is broad in air. It is highly likely that an effect of similar magnitude would apply in Puffins and leave them with a binocular field of about 30 ° wide and only 60 ° vertically, projecting upwards. This reduced field could still play a crucial role in foraging for the smaller items that lie above and ahead of the bird.
In both Guillemots and Puffins such visual field shrinkage would leave them virtually without visual coverage straight ahead. This is likely to result in these birds being particularly vulnerable to collision with objects that lie ahead.
This is not a problem when diving in the open sea but it could render these birds particularly vulnerable to collisions with human artefacts which intrude into the open water column. Perhaps the major structure of a turbine is not a hazard, but certainly smaller ancillary objects, such as cables and pipes would be difficult to detect. This is the case for birds which are prone to colliding with power lines and wind turbines (Martin 2011; Martin et al. 2012). This reduced forward visual coverage would also mean that these birds are particularly vulnerable to being caught in fishing nets. Indeed Guillemots are the bird species most prone to be victims of gillnet bycatch (Zydelis et al. 2013). This vulnerability has been in part attributed to the poor visual resolution of these birds, especially at the low light levels in which they forage (Martin & Crawford 2015) – read Rory Crawford’s BOU Blog about bird vision and bycatch in gillnets. To this we can now add the possibility that Guillemots and Puffins will have minimal visual coverage of what lies ahead of them when underwater.
References and further reading
Guillemain, M., Martin, G.R., & Fritz, H. 2002. Feeding methods, visual fields and vigilance in dabbling ducks (Anatidae). Functional Ecology, 16, 522-529. View
Harris, M., Leopold, M.F., Jensen, J.-K., Meesters, E.H., & Wanless, S. 2015. The winter diet of the Atlantic Puffin Fratercula arctica around the Faroe Islands. Ibis, 157, 468-479. View
Martin, G.R. & Piersma, T. 2009. Vision and touch in relation to foraging and predator detection: insighful contrasts between a plover and a sandpiper. Proceedings of the Royal Society of London. Series B: Biological Sciences, 276, 437-445. View
Martin, G.R. 2011. Understanding bird collisions with man-made objects: a sensory ecology approach. Ibis, 153, 239-254. View
Martin, G.R. 2014. The subtlety of simple eyes: the tuning of visual fields to perceptual challenges in birds. Philosophical Transactions of the Royal Society B-Biological Sciences, 369, (1636) doi.org/10.1098/rstb.2013.0040. View
Martin, G.R. & Crawford, R. 2015. Reducing bycatch in gillnets: A sensory ecology perspective. Global Ecology and Conservation, 3, 28-50. View
Martin, G.R. & Portugal, S.J. 2011. Differences in foraging ecology determine variation in visual field in ibises and spoonbills (Threskiornithidae). Ibis, 153, 662-671. View
Martin, G.R., Portugal, S.J., & Murn, C.P. 2012. Visual fields, foraging and collision vulnerability in Gyps vultures. Ibis, 154, 626-631. View
Martin, G.R. & Young, S.R. 1984. The eye of the Humboldt Penguin, Spheniscus humboldti: visual fields and schematic optics. Proceedings of the Royal Society of London. Series B: Biological Sciences, 223, 197-222. View
Troscianko, J., von Bayern, A.M.P., Chappell, J., Rutz, C., & Martin, G.R. 2012. Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows. Nature Communications, 3:1110 DOI: 10.1038/ncomms2111. View
White, C.R., Day, N., Butler, P.J., & Martin, G.R. 2007. Vision and Foraging in Cormorants: more like Herons than Hawks? PLoSOne, i2(7): e639.doi:10.1371/journal.pone.0000639. View
Zydelis, R., Small, C., & French, G. 2013. The incidental catch of seabirds in gillnet fisheries: A global review. Biological Conservation, 162, 76-88. View
All images © Graham Martin
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