E. Curio, On how birds protect their eyes: division of labour between the upper lid,lower lid and the nictitating membrane, J ORNITHOL, 142(3), 2001, pp. 257-272
Birds close their eyes during sleep in various taxon-specific ways. Either
the lower lid moves up as in the majority of species including the Anseres,
Accipitres. Falconiformes, Galli, Charadrioidea, Columbiformes, and Oscine
s; or the upper lid moves down (Psittaciformes, Trochili), or both lids clo
se the eye as in Strigiformes and Caprimulgi. Such information is absent fo
r most orders, or the handbooks provide wrong or conflicting information. B
eside the tonic, sleep-related eye closure, birds move one or both lids in
a phasic, usually swift mode when awake. These frequent lid movements are t
ypified by their different co-ordination and function. Photographic and obs
ervational evidence strongly suggests mechanical protection of the eye as a
novel function (where this had not been proposed previously). When an impa
ct from any object is imminent from in front of or above the head, the uppe
r lid shuts in pigeons, owls and oscines, and with water splashing, the low
er lid as well (Cinclus). The most convincing evidence for mechanical prote
ction comes from the deployment of the upper lid during the picking up of s
piny insect prey as compared to easy-to-swallow berries, when both lids sta
y at rest (Gallicolumba).
A new function is also attributed to the beating of the nictitating membran
e (Membrana nictitans). Traditionally viewed as a cleaning device it also s
erves to protect the eye from mechanical impact, and it also can be tuned t
o the side from where danger is threatening, though by and large there is a
dearth of information from avian taxa. The non-visually elicited action of
the membrane seems always to be bilateral (Falco, Harpia). The very stimul
i eliciting the blinking of a lid can, in different species, trigger the be
at of the membrane, and can cause it to move tonically (Falco). The membran
e beats at a rate difficult to measure since many of its beats coincide wit
h the blinking of the upper lid and thus remain hidden (Otus). This coincid
ence is difficult to account for by any function discussed so far, as are t
he many hidden beats during tonic eye closure with the lids (Passer).
The hypothesis according to which the action of the membrane is filtering o
ut undesirable retinal stimulation during e.g. rapid head movements is dism
issed on four different grounds. The increase of the membrane activity duri
ng predator alarm (Ficedula) is functionally unaccounted for.
In a fashion unique among birds, the Blue Nuthatch (Sitta azurea) protects
its eyes by contracting the naked skin surrounding the eye, thereby minimiz
ing the exposure of the cornea during foraging along the underside of branc
hes. a continual rain of bark particles and debris jeopardizes unimpeded vi
sion.
Secondarily, one or both lids or the nictitating membrane have taken on the
function of optic signals by virtue of contrasting feather colour or color
ation. The phasic ('flashing') signal movements involved are directed at th
e pair mate (Cinclus, Corvidae, Cepphus), predators (Anas) or at unknown pa
rties (Ficedula).