The Various Ways in Which Birds Blink

Simple Summary

While our blink simply involves lowering the upper eyelid, with little involvement of the lower lid, birds have various ways of blinking depending on the species and the circumstances. Like us, they have upper and lower eyelids, though the upper lid only moves down in parrots, owls, pigeons, and a few others. The lower lid rises with drowsiness and when the bird is preening. Birds blink when they turn their heads using a ‘third eyelid’, the nictitating membrane which moves horizontally from the inner part to the outer part of the eye. The closest cousins of birds, crocodiles, blink with their lower lids and nictitating membranes but not their upper lids. As crocodiles have changed very little since they first appeared, it seems likely that their way of blinking is similar to that of the common ancestor of birds and crocodiles, the archosaur. So, upper lid blinking in birds probably came later than lower eyelid and nictitating membrane blinking. The orders of bird which have upper lid blinking are not closely related, so this type of blink is likely to be an example of convergent evolution where distantly related species evolve similar traits to adapt to similar needs. Blinking evolved as a way of keeping the cornea moist when fish first left the sea and is an as yet neglected marker of vertebrate evolution.

Abstract

There has, to date, been no systematic study of the various ways in which birds blink. Digital video recordings were made, and studied using still frames, of 524 bird species, mainly in zoos but also in the wild. Videos on 106 species from various sites on the internet were studied, some of which we had also videoed, giving a total of 591 (out of a possible 10,000) species from all 43 orders and 125 (out of a possible 249) families. Digital video recordings were also made of 15 (out of a possible 24) species of crocodile. Three types of blink were observed in birds: (1) Nictitating membrane blinks were rapid and brief (phasic) and occurred mainly on head movement. (2) Upper lid blinks were seen in parrots, owls, pigeons and some others. These were also rapid and brief and accompanied nictitating membrane blinks. (3) Lower lid blinks were slow and sustained (tonic) and occurred with drowsiness and preening. Nictitating membrane blinks and lower lid blinks were seen in crocodiles but not upper lid blinks. Globe retraction, where the eyeball is pulled into the orbit of the skull during a blink, was seen in crocodiles but not birds. Phasic blinks remove debris and moisten the cornea, essential for allowing oxygen to diffuse into the cornea, which has no blood supply. Tonic blinks are probably mainly protective. The orders of birds which have upper lid blinking are not closely related and this feature is probably the result of convergent evolution.

1. Introduction

Blinking is of importance in an evolutionary context as it was one of the key factors which allowed fish to leave the sea and assume a terrestrial lifestyle. Most fish do not blink. They have no need to, for oxygen dissolved in water can diffuse into the epithelium on the surface of the cornea. The cornea is transparent and contains no blood vessels. Blood vessels would pose a barrier to light reaching the retina. Fish venturing from water onto land faced the problem that when the cornea dries out, atmospheric oxygen is no longer able to diffuse into the cornea (this is why the corneas of unconscious, unblinking patients in intensive care units swell and become opaque if moisture is not frequently applied to their eyes). Blinking, sweeping moisture over the cornea with eyelids, allows atmospheric oxygen to dissolve in the fluid and diffuse into the cornea.

In mudskippers, fish which spend much of their time out of water, sea water in a cup below the stalk on which the eye sits moistens the globes when the eye retracts [1]. In longer established terrestrial vertebrates, lacrimal and Harderian glands provide tears. In birds, tears are mainly produced by the Harderian gland [2] and reach the cornea through a duct which opens into the base of the nictitating membrane. As well as moistening the cornea, tears from the Harderian gland contain antibodies which protect against infection. In humans, cats and dogs, where three layers in the tear film are described, an outer layer of mucin slows the rate of evaporation of tears and lubricates the movement of the eyelids [3,4].

Video has proved to be a useful clinical tool for observing gait, eye movement and involuntary movements [5,6] and was used in this study to investigate how birds blink. Blinking in humans can be a reflex (for example, the corneal reflex), voluntary or spontaneous [7]. While spontaneous blinking in humans is a relatively simple process, the upper lid briefly falling and rising about twelve times a minute [8], birds have more than one type of spontaneous blink, and not all species blink in the same way.

In one of the earliest accounts, Owen [9] noted that, like non-avian reptiles, birds have three eyelids. The upper and lower lids move in the vertical plane. The third, the nictitating membrane, is drawn horizontally or obliquely across the cornea by the combined action of the quadratus membranae nictitantis and pyramidalis membranae nictitantis muscles which lie behind the eyeball [10].

Owen [9] observed that the lower eyelid rises in sleep. Owls and nightjars blink with their upper lids. The upper eyelid is elevated by levator palpebrae superioris and the upper and lower eyelids are brought together by the action of orbicularis oculi. In an anatomical study, Stibbe [11] contrasted the nictitating membrane blink of birds with that of mammals. In the latter, the membrane is not actively drawn across the eye by the contraction of muscles. Rather, it lies in a state of elastic tension out of sight on the medial side of the globe, springing across when the eyeball retracts by the action of the retractor bulbi muscle. In birds, the muscles required for globe retraction, and in most birds for eye movements, have become vestigial—capable of causing only low-amplitude eye movement of the type, for example, which causes saccadic oscillation [12]. This evolved presumably to lighten the load for flight.

In cats and dogs, globe retraction only occurs during blinking with both eyelids, so the membrane is not usually seen. Blount [13] measured the inter-blink interval in a wide range of mammals, some reptiles and amphibia, and in four species of birds. In an eagle owl, often the blinks involving the eyelids or nictitating membrane were unilateral. Of relevance to the present study, it was noted that in a parrot, the lower lid was much slower to return to its resting position than the upper lid. Most fish do not have functioning eyelids and Blount surmised that blinking evolved in air-breathing animals as a means of preventing desiccation of the cornea by exposure to air. Mowrer [14] proposed that blinking during head movements, which are rapid and frequent in birds as they have to compensate for their lack of eye movements, might prevent blurred images reaching the retina. During rapid head turns, images traverse the retina at a rate beyond the capacity of the retinal photoreceptors to respond adequately [15]. Yorzinski [16] has more recently proposed that blinking during a gaze shift, a time when visual information is already limited, may minimise additional information loss. Kirsten and Kirsten [17] measured the spontaneous blink rates of 25 species of birds. They also noted a correlation between blinks and head turns. Nocturnal species such as owls had a lower blink rate than diurnal species. Curio [18] coined the terms ‘tonic’ and ‘phasic’ blinks to distinguish slow prolonged blinks from rapid brief ones. In the tonic blinks of many orders (Anseriformes, Accipitriformes, Falconiformes, Galliformes, Charadriiformes, Columbiformes and the Oscines suborder of Passeriformes), the lower lid rises during sleep. In Psittaciformes and Trochili (hummingbirds), the upper lid descends in sleep and in Strigiformes and Caprimulgiformes, both lids are involved. He commented that ‘such information is lacking for most orders, or the handbooks provide wrong or conflicting information’.

The purpose of the present study was to take up Curio’s challenge and increase our understanding of the way that birds blink across the avian orders. To do this, we aimed to video or obtain videos of representative numbers of species from every order of birds to test the following hypotheses: Do all birds have the same type of blink? Is the blink type related to activities such as head turns, drowsiness, nocturnality, preening or ground feeding/pecking? Where a blink type is confined to certain species of bird, can this be related to phylogeny? How does blinking in birds compare with blinking in their closest cousins, Crocodilia?

The following predictions were made: Such has been the evolutionary flowering of birds and the myriad environments to which they have adapted, not all birds will have the same types of blink. Blinking in birds will differ from blinking in crocodilians, which have changed little since they first emerged.

2. Materials and Methods

Birds were videoed throughout the year from 2015–2021 using a Panasonic Lumix DMC FZ2500 digital single-lens reflex camera and a Sony FDR–AX53 camcorder. The zoom on these cameras allowed close-up views of the eyes even when the bird was more than 5 metres away. There was no intervention such as making a noise, gesticulating or using flash photography. Most filming was carried out at 25 frames/second and in some settings, for example, to see saccadic oscillation, at 100 frames/second. If they remained in view, birds were videoed for at least a minute. When the opportunity arose, the same bird might be videoed repeatedly. Wild birds were studied in Sydney, Australia, and to a small extent in the UK and the Netherlands. Captive birds and other animals were filmed at zoos in Australia: Taronga and Featherdale Park in Sydney, the Reptile Park in Gosford and zoos in Canberra, Melbourne, Adelaide, Launceston and Queensland (Australia Zoo, Lone Pine and Currumbin); Singapore: the Jurong Bird Park; UK: London Zoo, Whipsnade, Barnes Wetlands, Torquay, Woburn Abbey, Bristol, Crocodiles of the World in Carterton, Oxfordshire and the Suffolk Owl Sanctuary; Ireland: Dublin; Belgium: Pairi Daiza Zoo; France: ZooParc de Beauval; Netherlands: Rotterdam Zoo, the Avifauna Park; USA: Bronx Zoo in New York, San Diego Zoo; South Africa: Pretoria, Hout Bay and Stellenbosch; New Zealand: Auckland; Greece: Athens. Sampling was opportunistic depending on which species the zoos happened to have. Common species were often videoed multiple times and no major differences were ever observed between blinks in different individuals of the same species. Rare species might be videoed only once.

Digital video files were analysed using Movavi Video Editing software [Versions 12.1 to 15.4.1] (which is easy to use and not overly expensive), made in Novosibirsk, Russia, with a Dell laptop (XPS 15 9560), made in Longhua, China, and later a MacBook Pro (2.6 GHz Processor and 16 GB memory), US Apple Company, manufactured in China. Video files could be viewed frame by frame in order to follow the position of the eyelids and nictitating membrane during the course of a blink. The software has a facility for taking still pictures. Examples are shown in Figure 1, Figure 2, Figure 3, Figure 4, Figure 5, Figure 6, Figure 7, Figure 8, Figure 9, Figure 10, Figure 11, Figure 12, Figure 13, Figure 14, Figure 15 and Figure 16. In order to obtain a more complete representation across the orders, videos from a further 106 species from the internet were studied. These were played back at a quarter speed, providing clear information on the positions of the eyelids and nictitating membrane during the course of the blink. Still photos were not taken. The identities of species were confirmed using the Cornell University site Birds of the World (https://birdsoftheworld.org).

Videoing birds was not without its challenges. Stationary birds tended to preen themselves, obscuring the eyes, or to fall asleep. With birds with laterally situated eyes, usually only one eye could be seen at a time. This was not the case with the frontally oriented eyes of raptors. Nictitating membrane blinks were mainly associated with head movements and in small birds, such as finches (Fringillidae), honeyeaters (Meliphagidae) and fairywrens (Maluridae), these were so rapid that any blinking which might have occurred was often obscured by movement blur. It was sometimes hard to detect the movement of transparent nictitating membranes, particularly across a dark iris. This was the case in a number of species of the order Anseriformes. For the purposes of this study, no time limit was set on how long a blink could last, but for most species, blinks rarely lasted longer than a second or two, and most were much briefer.

3. Results

3.1. Birds

Video recordings were made on 591 bird species, which included 43 orders and 125 families (see

Table A1. Upper lid blinks in avian species, F: number of species within a family; S: number of species studied; A/B: A our video/B internet video; FUL: full upper lid blink; Y: yes; “_“: not seen; PUL: partial upper lid blink.

Order	Family	Species	Common Name	F	S	A/B	FUL	PUL
Accipitriformes	Accipitridae	Accipiter novaehollandiae	Grey goshawk	249	28	A		Y
		Aquila audax	Wedge-tailed eagle			A
		Aquila rapax	Tawny eagle			A
		Aviceda subcristata	Pacific baza			A
		Buteo buteo	Common buzzard			A
		Buteo rufofuscus	Jackal buzzard			A
		Buteo trizonatus	Forest buzzard			A
		Elanus coeruleus	Black-winged kite			A
		Gypohierax angolensis	Palm-nut vulture			A
		Gyps africanus	White-backed vulture			A
		Gyps fulvus	Griffon vulture			A
		Haliaeetus leucocephalus	Bald eagle			A
		Haliaeetus leucogaster	White-bellied sea eagle			A
		Haliastur indus	Brahminy kite			A		Y
		Haliastur sphenurus	Whistling kite			A		Y
		Hamirostra melanosternon	Black-breasted buzzard			A
		Hieraaetus morphnoides	Little eagle			A
		Hieraaetus wahlbergi	Wahlberg’s eagle			A
		Hieraaetus morphnoides	Little eagle			A
		Ictinaetus malaiensis	Black eagle			A
		Melierax canorus	Pale chanting goshawk			A
		Milvus migrans	Black kite			A
		Nisaetus nanus	Wallace’s hawk-eagle			A
		Parabuteo unicinctus	Harris’ hawk			A
		Polyboroides typus	African harrier hawk			A
		Polemaetus bellicosus	Martial eagle			A
		Stephanoaetus coronatus	Crowned eagle			A
		Terathopius ecaudatus	Bateleur			A
		Trigonoceps occipitalis	White-headed vulture			A
	Sagittariidae	Sagittarius serpentarius	Secretary bird	1	1	A
Cathartiformes	Cathartidae	Gymnogyps californianus	California condor	7	5	A
		Cathartes aura	Turkey vulture			A		Y
		Vultur gryphus	Andean condor			A
		Coragyps atratus	Black vulture			A
		Sarcoramphus papa	King vulture			A
	Pandionidae	Pandion haliaetus	Western osprey	1	1	A		Y
Anseriformes	Anatidae	Aix galericulata	Mandarin duck	174	48	A
		Aix sponsa	Wood duck			A		Y
		Alopochen aegyptiaca	Egyptian goose			A
		Anas castanea	Chestnut teal			A
		Anas georgica	Yellow-billed pintail			A		_
		Anas platyrhynchos	Mallard			A
		Anas superciliosa	Pacific black duck			A
		Anas undulata	Yellow-billed duck			A
		Anser anser	Graylag goose			A
		Anser cygnoides	Swan goose			A		_
		Anser indicus	Bar-headed goose			A		_
		Asarcornis scutulata	White-winged duck			A		_
		Aythya affinis	Lesser scaup			A		_
		Aythya australis	Hardhead			A
		Aythya fuligula	Tufted duck			A
		Aythya nyroca	Ferruginous duck			A		_
		Aythya valisineria	Canvasback			A		_
		Branta canadensis	Canada goose			A
		Branta leucopsis	Barnacle goose			A		_
		Branta sandvicensis	Nene			A		_
		Bucephala albeola	Bufflehead			A		_
		Cairina moschata	Muscovy duck			A
		Callonetta leucophrys	Ringed teal			A
		Cereopsis novaehollandiae	Cape Barren goose			A
		Chenonetta jubata	Australian wood duck			A
		Cygnus atratus	Black swan			A
		Cygnus cygnus	Whooper swan			A
		Cygnus olor	Mute swan			A		_
		Dendrocygna arcuata	Wandering whistling duck			A
		Dendrocygna bicolor	Fulvous whistling duck			A		Y
		Dendrocygna eytoni	Plumed whistling duck			A		_
		Dendrocygna viduata	White-faced whistling duck			A		_
		Lophodytes cucullatus	Hooded merganser			A		_
		Hymenolaimus malacorhynchos	Blue duck or whio			A
		Mergellus albellus	Smew			A		_
		Mergus merganser	Common merganser			A
		Mergus serrator	Red-breasted merganser			A		_
		Neochen jubata	Orinoco goose			A		_
		Nettapus auritus	African pygmy goose			A
		Netta rufina	Red-crested pochard			A
		Oxyura australis	Blue-billed duck			A
		Radjah radjah	Radjah shelduck			A
		Sarkidiornis sylvicola	Comb duck			A		_
		Somateria fischeri	Spectacled eider			A		Y
		Somateria mollissima	Common eider			A		_
		Spatula hottentota	Hottentot teal			A
		Tadorna ferruginea	Ruddy shelduck			A
		Tadorna variegata	Paradise shelduck			A		_
	Anseranatidae	Anseranas semipalmata	Magpie goose	1	1	A
	Anhimidae	Chauna torquata	Southern screamer	3	1	A
Apterygiformes	Apterygidae	Apteryx australis	Kiwi	5	1	B		_
Bucerotiformes	Bucerotidae	Berenicornis comatus	White-crowned hornbill	59	11	A
		Buceros bicornis	Great hornbill			A
		Buceros hydrocorax	Rufous hornbill			A
		Buceros rhinoceros	Rhinoceros hornbill			A
		Bycanistes brevis	Silvery-cheeked hornbill			A
		Horizocerus albocristatus	White-crested hornbill			A
		Lophoceros fasciatus	African pied hornbill			A
		Lophoceros nasutus	African grey hornbill			A
		Rhyticeros plicatus	Blyth’s (Papuan) hornbill			A
		Rhyticeros undulatus	Wreathed hornbill			A
		Tockus deckeni	Von der Decken’s hornbill			A
	Bucorvidae	Bucorvus leadbeateri	Southern ground hornbill	2	2	A
		Rhabdotorrhinus exarhatus	Sulawesi hornbill			A
	Upupidae	Upupa epops	Eurasian hoopoe	2	1	A/B
	Phoeniculidae	Phoeniculus purpureus	Green wood hoopoe	8	1	A/B
Caprimulgiformes	Aegothelidae	Aegotheles cristatus	Australian owlet nightjar	9	1	B	Y
	Apodidae	Aeronautes saxatalis	White-throated swift	12	2	B	Y
		Apus apus	Common swift			B	Y
	Hemiprocnidae	Hemiprocnae comata	Whiskered treeswift	4	1	B	Y
	Caprimulgidae	Caprimulgus europaeus	European nightjar	96	2	B	Y
		Lyncornis macrotis	Great eared nightjar			B	Y
	Nyctibiidae	Nyctibius grandis	Great potoo	7	1	B	Y
	Trochilidae	Calypte anna	Anna’s hummingbird	363	4	B	Y
		Calypte costae	Costa’s hummingbird			B	Y
		Mellisuga helenae	Bee hummingbird			B	Y
		Selasphorus sasin	Allen’s hummingbird			B	Y
Cariamiformes	Cariamidae	Cariama cristata	Red-legged seriema	2	1	A
Casuariiformes	Casuariidae	Dromaius novaehollandiae	Emu	4	2	A
		Casuarius casuarius	Southern cassowary			A
Charadriiformes	Turnicidae	Turnix castanotus	Chestnut-backed buttonquail	18	3	A/B	Y
		Turnix melanogaster	Black-breasted buttonquail			A	Y
		Turnix varius	Painted buttonquail			A	Y
	Haematopodidae	Haematopus fuliginosus)	Sooty oystercatcher	12	4	A	_
		Haematopus longirostris	Pied oystercatcher			A
		Haematopus moquini	African oyster catcher			A	_
		Haematopus ostralegus	Eurasian oystercatcher			A
	Burhinidae	Burhinus capensis	Spotted thick-knee	10	3	A/B		Y
		Burhinus grallarius	Bush stone-curlew			A		Y
		Esacus magnirostris	Beach stone-curlew			A		Y
	Laridae	Chroicocephalus hartlaubii)	Hartlaub’s gull	99	14	A/B
		Chroicocephalus novaehollandiae	Silver gull			A/B		Y
		Chroicocephalus ridibundus	Black-headed gull			A/B
		Rissa tridactyla	Black-legged kittiwake			A/B		Y
		Gygis alba	White tern			A/B		_
		Hydroprogne caspia	Caspian tern			B		_
		Larosterna inca	Inca tern			A
		Larus argentatus	European herring gull			A
		Larus marinus	Great black-backed gull			A
		Larus pacificus	Pacific gull			A/B
		Larus dominicanus	Kelp gull			A
		Rhinchops niger	Black skimmer			B
		Sterna striata	White-fronted tern			A		_
		Thalasseus bergii	Greater crested tern			A
	Scolopacidae	Numenius madagascariensis	Far Eastern curlew	97	4	A/B		_
		Tringa nebularia	Common greenshank			A	Y
		Calidris canutus	Red knot			A/B	Y
		Tringa totanus	Common redshank			A	Y
	Recurvirostridae	Himantopus himantopus	Black-winged stilt	9	3	A		Y
		Recurvirostra avosetta	Pied avocet			A	Y
		Recurvirostra novaehollandiae	Red-necked avocet			A	Y
	Alcidae	Fratercula cirrhata	Tufted puffin	25	2	A	Y	Y
		Uria aalge	Common guillemot			A		Y
	Charadriidae	Charadrius mongolus	Lesser sand plover	68	7	A/B		Y
		Elseyornis melanops	Black-fronted dotterel			A/B		_
		Vanellus miles	Masked lapwing			A		Y
		Vanellus spinosus	Spur-winged lapwing			A		_
		Vanellus tricolor	Banded lapwing			A		Y
		Pluvialis fulva	Pacific golden plover			A		Y
		Thinornis cucullatus	Hooded plover			A		_
	Jacanidae	Irediparra gallinacea	Comb-crested jacana	8	1	A		Y
Ciconiiformes	Ciconiidae	Ciconia stormi	Storm’s stork	20	12	A		Y
		Ciconia abdimii	Abdim’s stork			A		Y
		Ciconia ciconia	White stork			A		Y
		Ciconia episcopus	Woolly-necked stork			A		Y
		Ciconia nigra	Black stork			A		Y
		Ciconia stormi	Storm’s stork			A		Y
		Ephippiorhynchus asiaticus	Black-necked stork			A		Y
		Ephippiorhynchus senegalensis	Saddle-billed stork			A		Y
		Leptoptilos crumenifer	Marabou stork			A		Y
		Mycteria cinerea	Milky stork			A		Y
		Mycteria leucocephala	Painted stork			A		Y
		Mycteria ibis	Yellow-billed stork			A		Y
Coliiformes	Coliidae	Colius colius	White-backed mousebird	6	2	B		Y
		Uroclius indicus	Red-faced mousebird			B		Y
Columbiformes	Columbidae	Caloenas nicobarica	Nicobar pigeon	353	37	A	Y
		Chalcophaps indica	Common emerald dove			A	Y
		Columba arquatrix	African olive pigeon			A	Y
		Columba guinea	Speckled pigeon			A	Y
		Columba leucomela	White-headed pigeon			A	Y
		Columba livia domestica	Domestic pigeon			A	Y
		Columba palumbus	Common wood pigeon			A	Y
		Ducula aenea	Green imperial pigeon			A	Y
		Ducula bicolor	Pied imperial pigeon			A	Y
		Ducula spilorrhoa	Torresian imperial pigeon			A	Y
		Gallicolumba crinigera	Mindanao bleeding-heart			A/B	Y
		Gallicolumba tristigmata bimaculata	Sulawesi ground dove			A	Y
		Geopelia cuneata	Diamond dove			A	Y
		Geopelia humeralis	Bar-shouldered dove			A	Y
		Geopelia striata	Zebra dove			A	Y
		Geophaps plumifera	Spinifex pigeon			A	Y
		Geophaps scripta	Squatter pigeon			A	Y
		Genus macropygia	Cuckoo dove			A	Y
		Goura victoria	Victoria crowned pigeon			A	Y
		Hemiphaga novaeseelandiae	Kererū			A	Y
		Leucosarcia melanoleuca	Wonga pigeon			A	Y
		Lopholaimus antarcticus	Topknot pigeon			A	Y
		Macropygia phasianella	Brown cuckoo-dove			A	Y
		Ocyphaps lophotes	Crested pigeon			A	Y
		Otidiphaps nobilis	Pheasant pigeon			A/B	Y
		Pampusana jobiensis	White-bibbed ground dove			A	Y
		Phaps elegans	Brush bronzewing			A	Y
		Phaps histrionica	Flock bronzewing			A/B	Y
		Ptilinopus magnificus	Wompoo fruit dove			A	Y
		Ptilinopus regina	Rose-crowned fruit dove			A	Y
		Ptilinopus superbus	Superb fruit dove			A	Y
		Streptopelia decipiens	African mourning dove			A	Y
		Spilopelia chinensis	Spotted dove			A/B	Y
		Spilopelia senegalensis	Laughing dove			A/B	Y
		Streptopelia risoria	Barbary dove			A	Y
		Zenaida macroura	Mourning dove			A	Y
Coraciiformes	Meropidae	Merops albicollis	White-throated bee-eater	31	4	A
		Merops bullockoides	White-fronted bee-eater			A
		Merops nubicus	Northern carmine bee-eater			A/B
		Merops ornatus	Rainbow bee-eater			A/B
	Alcedinidae	Dacelo leachii	Blue-winged kookaburra	117	7	A
		Dacelo novaeguineae	Laughing kookaburra			A
		Halcyon coromanda	Ruddy kingfisher			A
		Todiramphus chloris	Collared kingfisher			A
		Todiramphus cinnamominus	Guam kingfisher			A
		Todiramphus macleayii	Forest kingfisher			A
		Todiramphus sanctus	Sacred kingfisher			A
	Coraciidae	Coracias cyanogaster	Blue-bellied roller	13	2	A
		Eurystomus orientalis	Oriental dollarbird			A
Cuculiformes	Cuculidae	Cuculus canoris	Common cuckoo	147	9	B
		Centropus phasianinus	Pheasant coucal			A
		Centropus sinensis	Greater coucal			B
		Crotophaga major	Greater ani			B
		Dromococcyx pavoninus	Pavonine cuckoo			B
		Dromococcyx phasianellus	Pheasant cuckoo			B
		Guira guira	Guira cuckoo			A
		Morococcyx erythropygus	Lesser ground-cuckoo			B
		Scythrops novaehollandiae	Channel-billed cuckoo			A
Eurypygiformes	Eurypygidae	Eurypyga helias	Sunbittern	1	1	A/B
	Rhinichetidae	Rhinochetus jubatus	Kagu	1	0	B	_
Falconiformes	Falconidae	Caracara plancus	Crested caracara	65	7	A/B
		Falco cenchroides	Nankeen kestrel			A
		Falco columbarius	Merlin			A/B
		Falco rupicolus	Rock kestrel			A
		Falco subbuteo	Eurasian hobby			A
		Phalcoboenus australis	Striated caracara			A
		Phalcoboenus megalopterus	Mountain caracara			A
Galbuliformes	Bucconidae	Malacoptila fusca	White-chested Puffbird	37	1	B
	Galbulidae	Galbula ruficauda	Rufus tailed jacamar	18	1	B
Galliformes	Cracidae	Pauxi pauxi	Helmeted curassow	57	2	A
		Nothocrax urumutum	Nocturnal curassow			A
	Numididae	Acryllium vulturinum	Vulturine guineafowl	8	2	A
		Numida meleagris	Helmeted guineafowl			A
	Phasianidae	Afropavo congensis	Congo peafowl	186	22	A		Y
		Arborophila atrogularis	White-cheeked partridge			A/B		Y
		Alectoris chukar	Chukar partridge			A
		Argusianus argus	Great argus			A
		Chrysolophus amherstiae	Lady Amherst’s pheasant			A
		Chrysolophus pictus	Golden pheasant			A
		Coturnix japonica	Japanese quail			A/B		Y
		Gallus gallus domesticus	Chicken			A		Y
		genus Meleagris	Turkey			A
		Lophophorus impejanus	Himalayan monal			A		Y
		Lophura bulweri	Bulwer’s pheasant			A/B
		Lophura diardi	Siamese fireback			A		Y
		Lophura nycthemera	Silver pheasant			A
		Pavo cristatus	Indian peafowl			A		Y
		Pavo muticus	Green peafowl			A
		Phasianus colchicus	Common pheasant			A		Y
		Polyplectron inopinatum	Mountain peacock-pheasant			A		Y
		Polyplectron napoleonis	Palawan peacock-pheasant			A
		Rollulus rouloul	Crested partridge			A/B
		Synoicus chinensis	King quail			A		Y
		Synoicus ypsilophorus	Brown quail			A		Y
		Tragopan temminckii	Temminck’s tragopan			A
	Odontophoridae	Colinus virginianus	Northern bobwhite	33	2	A		Y
		Ptilopachus petrosus	Stone partridge			A/B		Y
	Megapodiidae	Alectura lathami	Australian brushturkey	21	3	A
		Leipoa ocellata	Malleefowl			A
		Megapodius reinwardt	Orange-footed scrubfowl			A		Y
Gaviiformes	Gaviidae	Gavia immer	Common loon	5	1	B
Gruiformes	Gruidae	Antigone rubicunda	Brolga	15	5	A
		Antigone vipio	White-naped crane			A
		Balearica regulorum	Grey-crowned crane			A
		Grus japonensis	Red-crowned crane			A		Y
		Grus paradisea	Blue crane			A
	Psophiidae	Psophia crepitans	Grey-winged trumpeter	3	1	A
	Rallidae	Eulabeornis castaneoventris	Chestnut rail	159	8	A/B
		Fulica atra	Eurasian coot			A
		Gallinula tenebrosa	Dusky moorhen			A
		Hypotaenidia philippensis	Buff-banded rail			A
		Porphyrio hochstetteri	Takahē			A
		Porphyrio melanotus	Australasian swamphen			A
		Tribonyx mortierii	Tasmanian nativehen			A
		Tribonyx ventralis	Black-tailed nativehen			A
Leptosomiformes	Leptosomidae	Leptosomus discolor	Cuckoo roller	1	1	B
Mesitornithiformes	Mesitornithidae	Monias benschi	Subdesert mesite	3	1	B
Musophagiformes	Musophagidae	Crinifer piscator	Western plantain-eater	23	6	A
		Tauraco erythrolophus	Red-crested turaco			A
		Tauraco rossae	Lady Ross’s turaco			A		Y
		Menelikornis leucotis	White-cheeked turaco			A
		Tauraco persa	Guinea turaco			A
		Tauraco violaceus	Violet turaco			A		Y
Opisthocomiformes	Opisthocomidae	Opisthocomus hoazin	Hoatzin	1	1	B
Otidiformes	Otididae	Ardeotis australis	Australian bustard	26	1	A		Y
Passeriformes	Acanthizidae	Sericornis frontalis	White-browed scrubwren	66	2	A		_
		Acanthiza pusilla	Brown thornbill			A
	Acrocephalidae	Acrocephalus australis	Australian reed warbler	59	1	A		_
	Artamidae	Alauda arvensis	Eurasian skylark	24	10	A		Y
		Artamus cyanopterus	Dusky woodswallow			A		_
		Artamus leucorynchus	White-breasted woodswallow			A
		Artamus superciliosus	White-browed woodswallow			A
		Cracticus nigrogularis	Pied butcherbird			A		Y
		Cracticus torquatus	Grey butcherbird			A
		Melloria quoyi	Black butcherbird			A
		Gymnorhina tibicen	Australian magpie			A
		Strepera graculina	Pied currawong			A
		Strepera versicolor	Grey currawong			A/B
	Callaeidae	Callaeas wilsoni	North Island kōkako	5	1	B
	Campephagidae	Coracina novaehollandiae	Black-faced cuckooshrike	89	2	A		Y
		Coracina papuensis	White-bellied cuckooshrike			A
	Cisticolidae	Cisticola exilis	Golden-headed cisticola	162	1	A/B
	Corcoracidae	Genus Corcoracidae	White-winged chough	2	2	B
		Struthidea cinerea	Apostlebird			A
	Corvidae	Coloeus monedula	Western jackdaw	128	13	A
		Corvus albicollis	White-necked raven			A
		Corvus albus	Pied crow			A/B
		Corvus capensis	Black crow			A		Y
		Corvus corax	Common raven			A		Y
		Corvus corone	Carrion crow			A
		Corvus coronoides	Australian raven			A		Y
		Corvus frugilegus	Rook			A
		Corvus splendens	Indian house crow			A/B
		Cyanopica cyanus	Azure-winged magpie			A
		Pica pica	Common magpie			A
		Temnurus temnurus	Ratchet-tailed treepie			A
		Urocissa erythroryncha	Red-billed blue magpie			A
	Cotingidae	Rupicola peruvianus	Andean cock-of-the-rock	65	1	A
	Estrildidae	Bathilda ruficauda	Star finch	138	14	A/B		Y
		Chloebia gouldiae	Gouldian finch			A	Y
		Coccopygia quartinia	Yellow-bellied waxbill			A	_
		Erythrura trichroa	Blue-faced parrotfinch			A/B	Y
		Estrilda astrild	Common waxbill			A	Y
		Lonchura castaneothorax	Chestnut-breasted mannikin			A/B	Y
		Neochmia phaeton	Crimson finch			A	Y
		Neochmia temporalis	Red-browed finch			A	Y
		Ortygospiza atricollis atricollis	Black-faced quailfinch			A/B	Y
		Padda oryzivora	Java sparrow			A	Y
		Poephila cincta	Black-throated finch			A/B	Y
		Poephila personata	Masked finch			A/B	Y
		Stagonopleura guttata	Diamond firetail			A/B	Y
		Taeniopygia guttata	Zebra finch			A/B	Y
	Fringillidae	Euphonia violacea	Violaceous euphonia	229	1	A/B
	Hirundinidae	Hirundo neoxena	Welcome swallow	86	1	A/B
	Irenidae	Irena puella	Asian fairy-bluebird	2	1	A
	Leiothrichidae	Garrulax bicolor	Sumatran laughing thrush	143	3	A
		Leiothrix lutea	Red-billed leiothrix			A		Y
		Pterorhinus courtoisi	Blue-crowned laughing thrush			A
	Maluridae	Malurus coronatus	Purple-crowned fairywren	32	4	A
		Malurus cyaneus	Superb fairywren			A/B		_
		Malurus lamberti	Variegated fairywren			A/B		Y
		Malurus splendens	Splendid fairywren			A/B		_
	Meliphagidae	Acanthagenys rufogularis	Spiny-cheeked honeyeater	189	15	A
		Anthochaera carunculata	Red wattlebird			A
		Anthochaera chrysoptera	Little wattlebird			A
		Anthochaera paradoxa	Yellow wattlebird			A		_
		Anthochaera phrygia	Regent honeyeater			A
		Anthornis melanura	New Zealand bellbird			A
		Entomyzon cyanotis	Blue-faced honeyeater			A
		Lichenostomus melanops	Yellow-tufted honeyeater			A
		Manorina melanocephala	Noisy miner			A
		Manorina melanophrys	Bell miner			A
		Meliphaga lewinii	Lewin’s honeyeater			A/B		Y
		Philemon citreogularis	Little friarbird			A
		Philemon corniculatus	Noisy friarbird			A
		Phylidonyris novaehollandiae	New Holland honeyeater			A/B
		Plectorhyncha lanceolata	Striped honeyeater			A		_
	Menuridae	Menura novaehollandiae	Superb lyrebird	2	1	A/B
	Momotidae	Momotus coeruliceps	Blue-crowned motmot	14	1	A		Y
	Monarchidae	Grallina cyanoleuca	Magpie-lark	100	1	A
	Motacillidae	Anthus novaeseelandiae	Australasian pipit	69	1	A		Y
	Muscicapidae	Copsychus malabaricus	White-rumped shama	345	1	A
	Nectariniidae	Chalcomitra adelberti	Buff-throated sunbird	143	4	A
		Cinnyris chalybeus	Southern double-collared sunbird			A		_
		Cinnyris coccinigastrus	Splendid sunbird			A
		Cinnyris jugularis	Olive-backed sunbird			A/B		_
	Oreoicidae	Oreoica gutturalis	Crested bellbird	3	1	A		Y
	Oriolidae	Oriolus auratus	African golden oriole	38	5	A		Y
		Oriolus chinensis	Black-naped oriole			A		Y
		Oriolus sagittatus	Olive-backed oriole			A		Y
		Sphecotheres vieilloti	Australasian figbird			A
		Sphecotheres viridis	Green figbird			A
	Pachycephalidae	Colluricincla harmonica	Grey shrike-thrush	63	3	A
		Pachycephala pectoralis	Australian golden whistler			A
		Pachycephala rufiventris	Rufous whistler			A
	Paradisaeidae	Paradisaea minor	Lesser bird-of-paradise	42	2	A/B
		Paradisaea apoda	Greater bird-of-paradise			A		Y
	Passeridae	Passer domesticus	House sparrow	43	2	A		Y
		Passer melanurus	Cape sparrow			A		Y
	Petroicidae	Eopsaltria australis	Eastern yellow robin	49	1	A
	Pittidae	Pitta versicolor	Noisy pitta	46		A
	Ploceidae	Euplectes franciscanus	Northern red bishop	123	4	A
		Foudia madagascariensis	Red fody			A/B
		Ploceus castaneiceps	Taveta weaver			A		_
		Ploceus cucullatus	Village weaver			A/B
	Pomatostomidae	Pomatostomus superciliosus	White-browed babbler	5	1	A/B
	Prunellidae	Prunella modularis	Dunnock	12	1	A/B		_
	Psophophidae	Psophodes occidentalis	Chiming wedgebill	5	2	A
		Psophodes olivaceus	Eastern whipbird			A/B
	Ptilonorhynchidae	Ailuroedus crassirostris	Green catbird	27	3	A
		Ptilonorhynchus violaceus)	Satin bowerbird			A
		Sericulus chrysocephalus	Regent bowerbird			A
	Pycnonotidae	Pycnonotus cafer	Red-vented bulbul	151	1	A/B
		Pycnonotus jocosus	Red-whiskered bulbul			A/B
	Rhipiduridae	Rhipidura albiscapa	Grey fantail	54	2	A
		Rhipidura leucophrys	Willy wagtail			A
	Sturnidae	Acridotheres fuscus	Jungle myna	125	13	A		Y
		Acridotheres tristis	Indian myna			A		Y
		Aplonis metallica	Metallic starling			A
		Cinnyricinclus leucogaster	Violet-backed starling			A		Y
		Gracula religiosa	Common hill myna			A
		Lamprotornis bicolor	African pied starling			A
		Lamprotornis iris	Emerald starling			A
		Lamprotornis regius	Golden-breasted starling			A		Y
		Lamprotornis superbus	Superb starling			A/B
		Leucopsar rothschildi	Bali myna			A		Y
		Mino dumontii	Yellow-faced myna			A		Y
		Onychognathus morio	Red-winged starling			A
		Sturnus vulgaris	Common starling			A
	Thraupidae	Paroaria coronata	Red-crested cardinal	382	4	A		Y
		Ramphocelus carbo	Silver-beaked tanager			A
		Ramphocelus bresilius	Brazilian tanager			A/B		_
		Tachyphonus rufus	White-lined tanager			A
	Troglodytidae	Troglodytes troglodytes	Eurasian wren	86	1	B	Y
	Turdidae	Geokichla citrina	Orange-headed thrush	175	3	A		Y
		Turdus merula	Eurasian blackbird			A		Y
		Turdus philomelos	Song thrush			A
	Zosteropidae	Zosterops lateralis	Silvereye	143	1	A
Pelecaniformes	Ardeidae	Ardea alba	Great egret	68	11	A		Y
		Ardea cinerea	Grey heron			A		Y
		Ardea melanocephala	Black-headed heron			A		Y
		Ardea purpurea	Purple heron			A/B		Y
		Bubulcus ibis	Cattle egret			A		Y
		Egretta garzetta	Little egret			A		Y
		Egretta novaehollandiae	White-faced heron			A		Y
		Egretta picata	Pied heron			A		Y
		Egretta sacra	Pacific reef heron			A
		Nycticorax caledonicus	Nankeen night heron			A
		Nycticorax nycticorax	Black-crowned night heron			A
	Pelecanidae	Pelecanus conspicillatus	Australian pelican	8	5	A		Y
		Pelecanus crispus	Dalmatian pelican			A		Y
		Pelecanus occidentalis	Brown pelican			A		Y
		Pelecanus onocrotalus	Great white pelican			A		Y
		Pelecanus thagus	Peruvian pelican			A/B		Y
	Scopidae	Scopus umbretta	Hamerkop	1	1	A
	Threskiorthithidae	Bostrychia hagedash	Hadada ibis	36	11	A
		Eudocimus ruber	Scarlet ibis			A
		Geronticus calvus	Southern bald ibis			A/B
		Geronticus eremita	Northern bald ibis			A		Y
		Platalea ajaja	Roseate spoonbill			A/B		Y
		Platalea alba	African spoonbill			A		Y
		Platalea regia	Royal spoonbill			A		Y
		Plegadis falcinellus	Glossy ibis			A
		Theristicus caudatus	Buff-necked ibis			A
		Theristicus melanopis	Black-faced ibis			A
		Threskiornis molucca	Australian white ibis			A		Y
Phoenicopteriformes	Phoenicopteridae	Phoenicopterus chilensis	Chilean flamingo	6	3	A
		Phoenicopterus roseus	Greater flamingo			A
		Phoenicopterus ruber	American flamingo			A
Phaethontiformes	Phaethontidae	Phaethon aethereus	Query red-billed tropic bird	3	1	B
Piciformes	Ramphastidae	Ramphastos toco	Toco toucan	36	7	A/B
	Ramphastidae	Ramphastos tucanus	Red-billed toucan			A/B
	Ramphastidae	Aulacorhynchus haematopygus	Crimson-rumped toucanet			B
	Ramphastidae	Aulacorhynchus caeruleogularis	Blue-throated toucanet			B
	Ramphastidae	Pteroglossus castanotis	Chestnut-eared araçari			B
	Ramphastidae	Pteroglossus frantzii	Fiery-billed aracari			B/B
	Ramphastidae	Pteroglossus beauharnaisii	Curl-crested aracari			B
	Lybiidae	Lybius dubius	Bearded barbet	41	2	A/B		Y
		Trachyphonus erythrocephalus	Red-and-yellow barbet			A/Y		Y
	Picidae	Dryocopus pileatus	Pileated woodpecker	233	11	B	Y
		Dryocopus martius	Black woodpecker			B	Y
		Geococcyx velox	Lesser roadrunner			B
		Jinx torquilla	Eurasian wryneck			B	Y
		Melanerpes formicivorus	Acorn woodpecker			B	Y
		Mulleripicus fulvus	Ash woodpecker			B	Y
		Piculus chrysochloros	Golden-green woodpecker			B	Y
		Picus viridis	Eurasian green woodpecker			A/B	Y
		Picumnus innominatus	Speckled piculet			B	Y
Podargiformes	Podargidae	Podargus strigoides	Tawny frogmouth	16	1	A	Y
Podicipediformes	Podicipedidae	Tachybaptus novaehollandiae	Australasian grebe	22	3	A
		Podiceps grisegena	Red-necked grebe			B
		Podiceps nigricollis	Eared grebe			B
Procellariiformes	Diomedeidae	Diomedea exulans	Wandering albatross	15	1	B		Y
Psittaciformes	Cacatuidae	Cacatua galerita	Sulphur-crested cockatoo	21	10	A	Y
		Cacatua sanguinea	Little corella			A	Y
		Cacatua tenuirostris	Long-billed corella			A	Y
		Callocephalon fimbriatum	Gang-gang cockatoo			A	Y
		Calyptorhynchus banksii	Red-tailed black cockatoo			A	Y
		Eolophus roseicapilla	Galah			A	Y
		Lophochroa leadbeateri	Major Mitchell’s cockatoo			A	Y
	Cacatuidae	Nymphicus hollandicus	Cockatiel			A	Y
		Zanda funerea	Yellow-tailed black cockatoo			A	Y
		Zanda baudinii	Baudin’s black cockatoo			A	Y
	Psittacidae	Amazona aestiva	Turquoise-fronted amazon	175	12	A	Y
		Ara ararauna	Blue-and-gold macaw			A	Y
		Ara chloropterus	Red-and-green macaw			A	Y
		Aratinga jandaya	Jandaya parakeet			A	Y
		Aratinga nenday	Nanday parakeet			A	Y
		Aratinga solstitialis	Sun parakeet			A	Y
		Melopsittacus undulatus	Budgerigar			A	Y
		Myiopsitta monachus	Monk parakeet			A	Y
		Genus Amazona	Amazon parrot			A/B	Y
		Psittacula krameri	Rose-ringed parakeet			A	Y
		Psittacus erithacus	African grey parrot			A	Y
		Pyrrhura molinae	Green-cheeked parakeet			A	Y
	Psittaculidae	Agapornis personatus	Yellow-collared lovebird	190	36	A	Y
		Alisterus scapularis	Australian king parrot			A	Y
		Aprosmictus erythropterus	Red-winged parrot			A	Y
		Barnardius zonarius	Australian ringneck			A	Y
		Coracopsis barklyi	Seychelles black parrot			A	Y
		Cyclopsitta diophthalma	Double-eyed fig parrot			A	Y
		Genus Cyanoramphus	Kakariki parrot			A	Y
		Eclectus roratus	Eclectus parrot			A	Y
		Glossopsitta concinna	Musk lorikeet			A	Y
		Lorius chlorocercus	Yellow-bibbed lory			A	Y
		Lorius garrulus	Chattering lory			A	Y
		Lorius lory	Black-capped lory			A	Y
		Neophema chrysostoma	Blue-winged parrot			A	Y
		Neophema pulchella	Turquoise parrot			A	Y
		Neophema splendida	Scarlet-chested parrot			A	Y
		Neopsephotus bourkii	Bourke’s parrot			A	Y
		Northiella narethae	Naretha bluebonnet			A	Y
		Platycercus elegans	Crimson rosella			A	Y
		Platycercus eximius	Eastern rosella			A	Y
		Polytelis alexandrae	Princess parrot			A	Y
		Psephotus haematonotus	Red-rumped parrot			A	Y
		Trichoglossus chlorolepidotus	Scaly-breasted lorikeet			A	Y
		Trichoglossus moluccanus	Rainbow lorikeet			A	Y
		Platycercus adscitus	Pale-headed rosella			A	Y
		Platycercus caledonicus	Green rosella			A	Y
		Polytelis anthopeplus	Regent parrot			A	Y
		Polytelis swainsonii	Superb parrot			A	Y
		Pseudeos fuscata	Dusky lory			A	Y
		Psittacula alexandri	Red-breasted parakeet			A	Y
		Psittacula cyanocephala	Plum-headed parakeet			A	Y
		Psittacula eupatria	Alexandrine parakeet			A	Y
		Psittacula krameri	Rose-ringed parakeet			A	Y
		Psitteuteles versicolor	Varied lorikeet			A	Y
		Trichoglossus chlorolepidotus	Scaly-breasted lorikeet			A	Y
		Trichoglossus moluccanus	Rainbow lorikeet			A	Y
		Trichoglossus rubritorquis	Red-collared lorikeet			A	Y
	Strigopidae	Nestor meridionalis	Kākā	4	2	A	Y
		Nestor notabilis	Kea			A	Y
Pterocliformes	Pteroclidae	Pterocles orientalis	Black-bellied sandgrouse	16	1	B	Y
Rheiformes	Rheidae	Rhea americana	Greater rhea	2	2	A/B
		Rhea pennata	Darwin’s rhea			A/B
Sphenisciformes	Spheniscidae	Spheniscus demersus	African penguin	18	6	A
		Aptenodytes patagonicus	King penguin			A
		Eudyptes chrysocome	Southern rockhopper			A/B
		Eudyptes chrysolophus	Macaroni penguin			A/B
		Eudyptula minor	Little penguin			A
		Spheniscus humboldti	Humboldt penguin			A
Steatornithiformes	Steatornithidae	Steatoris caripensis	Oilbird			B		Y
Strigiformes	Strigidae	Athene cunicularia	Burrowing owl	228	24	A	Y
		Athene noctua	Little owl			A	Y
		Bubo africanus	Spotted eagle-owl			A	Y
		Bubo bengalensis	Indian eagle-owl			A/B	Y
		Bubo bubo	Eurasian eagle-owl			A	Y
		Bubo capensis	Cape eagle-owl			A	Y
		Bubo lacteus	Verreaux’s eagle-owl			A	Y
		Bubo scandiacus	Snowy owl			A	Y
		Bubo virginianus	Great horned owl			A	Y
		Glaucidium perlatum	Pearl-spotted owlet			A	Y
		Ketupa ketupu	Buffy fish owl			A	Y
		Ninox boobook	Australian boobook			A	Y
		Ninox connivens	Barking owl			A	Y
		Ninox novaeseelandiae	Morepork			A	Y
		Ninox rufa	Rufous owl			A/B	Y
		Ninox strenua	Powerful owl			A	Y
		Ptilopsis granti	Southern white-faced owl			A	Y
		Strix aluco	Tawny owl			A	Y
		Strix leptogrammica	Brown wood owl			A	Y
		Strix nebulosa	Great grey owl			A	Y
		Strix seloputo	Spotted wood owl			A	Y
		Strix uralensis	Ural owl			A	Y
		Strix woodfordii	African wood owl			A/B	Y
		Surnia ulula	Northern hawk owl			A	Y
	Tytonidae	Tyto alba	Barn owl	18	5	A	Y
		Tyto longimembris	Eastern grass owl			A	Y
		Tyto multipunctata	Lesser sooty owl			A/B	Y
		Tyto novaehollandiae	Masked owl			A	Y
Struthioniformes	Struthionidae	Struthio camelus	Common ostrich	2	1	A
Suliformes	Sulidae	Morus capensis	Cape gannet	10	1	A
	Phalacrocoracidae	Phalacrocorax capensis	Cape cormorant	40	5	A
		Phalacrocorax neglectus	Bank cormorant			A
		Phalacrocorax punctatus	Spotted shag or pārekareka			A
		Phalacrocorax sulcirostris	Little black cormorant			A
		Phalacrocorax varius	Australian pied cormorant			A
	Anhingidae	Anhinga novaehollandiae	Australian darter	4	1	A
Tinamiformes	Tinamidae	Eudromia elegans	Elegant crested tinamou	46	1	A/B		Y
Trogoniformes	Trogonidae	Trogon bairdii	Baird’s trogon	43	1	B		Y

). No blinking occurred during the period of observation (i.e., the bird flew away) in 67 species. Three types of blink were observed:

3.2. Nictitating Membrane Blinks

Here, the membrane travelled across the cornea from the inner (medial) to the outer (lateral) canthus (Figure 1).

Nictitating membrane blinks were usually frequent, rapid, brief and coincided with head movement. They also occurred with the head still. In the few species with preserved eye movements, nictitating membrane blinks also coincided with these (Figure 2).

Eye-movement-related nictitating membrane blinks were seen in Bucerotiformes and some species of Anseriformes, Ciconiiformes, Cuculiformes, Otidiformes, Passeriformes and Sphenisciformes. Eye movements were most noticeable in birds with large, long bills like hornbills (Bucerotidae), storks (Ciconiidae) and pelicans (Pelicanidae) but also in parrots (Psittaciformes) with large, short bills.

Nictitating membrane blinks were seen in the following orders: Accipitriformes, Anseriformes, Bucerotiformes, Cariamiformes, Casuariiformes, Cathartiformes, Ciconiiformes, Coraciiformes, Cuculiformes, Eurypygiformes, Falconiformes, Galliformes, Gruiformes, Musophagiformes, Otidiformes, Pelecaniformes, Phoenicopteriformes, Piciformes, Sphenisciformes, Suliformes and Tinamiformes.

In some species, the nictitating membrane blink was accompanied by a partial upper lid blink with slight lowering of the medial (nasal) side of the upper eyelid (Figure 3). In these species, the upper lid never covered the pupil. Partial upper lid blinks were seen in many species of Ciconiiformes, Galliformes and Pelecaniformes and a few species of Accipitriformes, Charadriiformes and Musophagiformes.

Birds with minimal eye movements, and even in those with easily observable eye movements, surveyed the landscape around them by frequent, rapid, brief head movements, akin to the saccadic (rapid, fixed velocity, voluntary) eye movements of humans [19]. Most, but not all, head movements were accompanied by nictitating membrane blinks.

Nictitating membrane blinks could be unilateral (‘winks’) or bilateral—asynchronous or synchronous. In larger species with less opaque membranes, arcades of blood vessels became visible during the course of a blink (Figure 4).

Nictitating membrane blinks were observed in 376 of 524 species which blinked (Table A1, and

Table 1. Number of species with each of the three types of blink and the total number of species videoed where a blink occurred.

Blink Type	Number of Species	Number Videoed
Nictitating membrane	376	524
Upper lid	166	524
Lower lid	77	524

) and could not be seen in 91 species which had a blink of another sort (in some of these cases, the quality of the video was good enough to see eyelid movement but not nictitating membrane movement). In 70 species, the membrane was transparent. This was the case in 21/22 species of Anseriformes, 3/3 species of Phoenicopteriformes, 3/3 of the family Spheniscidae (order Sphenisciformes), 5/5 of Suliformes and in some species within Charadriformes, Columbiformes, Galliformes, Pelecaniformes and Strigiformes. While most of the species with transparent nictitating membrane were aquatic, there were many notable exceptions, including owls (Strigiformes). In 9/13 species of Bucerotiformes, nictitating membrane blinks were associated with eye movements.

More prolonged nictitating membrane blinks were associated with irregular rapid bobbing of the eye. This was described by Pettigrew [12] as saccadic oscillation. The shaking of the pecten, a highly vascular structure protruding into the vitreous humour, increases the release of oxygen and nutrients into the vitreous humour. These diffuse into the retina which, unlike the human eye, does not have its own blood supply [20]. Saccadic oscillation was seen most clearly in birds with large eyes such as the stone curlew. It was not seen with the naked eye—it requires 100 fps video capture.

3.3. Upper Eyelid Blinks

Here, there was downward (ventral) movement of the upper eyelid accompanied by horizontal movement of the nictitating membrane from the inner (medial) to outer (lateral) canthus (Figure 5), although the upper eyelid often obscured this (Figure 6).

As with ‘pure’ nictitating membrane blinks, upper lid blinks were usually rapid, brief and coincided with head movement. Occasionally, they were observed with the head still. The movements of the upper lid and nictitating membrane appeared to be linked during a blink, neither occurring alone, but their movements were not necessarily synchronous, one starting or finishing before or after the other.

Upper lid blinking was observed in 166 of 524 species which blinked (Table 1 and Table A1) and in 43 of these, accompanying movement of the nictitating membrane could be seen. Upper lid blinking was seen in 30/36 species of Columbiformes, in all 60 species of Psittaciformes, all 11 species of Caprimulgiformes and in 24/28 species of Strigiformes. In other orders, the proportion of upper blinks was lower: 7/40 species of Charadriiformes and 18/131 species of Passeriformes (8/14 of the family Estrildidae). In no case did a nictitating membrane blink occur without an accompanying upper lid blink in species displaying upper lid blinks.

In some species, the upper lid was made prominent by being a different colour from the rest of the head e.g., Caloenas nicobarica and Momotus coeruliceps, which have white upper lids.

3.4. Lower Eyelid Blinks

A total of 77 species (out of 524 species which blinked, Table 1 and Table A1) across most orders of bird were observed while preening (Figure 7) and 98 during drowsiness (Figure 8). These had lower lid blinks in which the lower lid rose, usually slowly and in a sustained manner. Before sleep, the lower lid would rise and fall repeatedly, before eventually remaining elevated. Often, the nictitating membrane could be seen making a pass as the lower lid rose (Figure 9), but it did not usually stay out for the entire duration of the lower lid blink, unlike upper lid blinks.

The lower lid in some species (e.g., Radjah radjah, Columba guinea) was paper thin, presumably allowing some light to enter the pupil. In others it was of a different colour to the rest of the head, making it prominent (e.g., Hypotaenidia philippensis). Rarely, species used the nictitating membrane rather than the lower lid during preening (e.g., Scopus umbrette).

In addition to the three types of blink, two further behaviours involving blinking were noted:

3.5. Pecking

Domestic hens (Gallus gallus domesticus) were observed pecking lichen off an old corrugated-iron panel. Their bills had been worn down. What was noticeable was that with every peck, a nictitating membrane blink occurred as the bill reached a certain distance from the target. In pigeons (Columbiformes), each peck was accompanied by an upper and lower lid blink (Figure 10). The type of blink seen with pecking varied with the species:

Lower lid blink on pecking: Numenius madagascariensis, Alectoris chukar, Phasianus colchicus, Colinus virginianus, Nymphicus hollandicus.

Upper lid blink on pecking: Turnix melanogaster, Geopelia cuneata, Geopelia striata, Ocyphaps lophotes, Spilopelia chinensis, Spilopelia senegalensis, Streptopelia risorii, Nymphicus hollandicus.

Upper and lower lids involved in pecking: Pluvialis fulva, Columba livia domestica, Columba palumbus, Coturnix japonica, Taeniopygia guttata, Barnardius zonarius, Platycercus eximius, Psephotus haematonotus.

3.6. Synergic Upper and Lower Eyelid Moment

A curious phenomenon seen mainly in Columbiformes, Psittaciformes and Strigiformes in states of drowsiness involved the upper lid slowly descending until it reached the lower lid in its resting position. The lower lid would then slowly rise, the upper lid rising at the same pace so that the eye remained closed. The two lids would then rise and fall together in unison, until the eye eventually opened (Figure 11).

Sometimes, the bird would squint, the lids coming together leaving a small gap or slit through which the pupil could be seen (Figure 12, Figure 13 and Figure 14)

Sometimes, the nictitating membrane was visible during a squint (Figure 15).

3.7. Crocodilia

Videos were made of 15 species of Crocodilia from 3 families (

Table A2. Types of blink in crocodilia, NMBl: nictitating membrane blink; Gl R: globe retraction; LLBl: lower lid blink; Y: yes.

Order	Family	Species	Common Name	NMBl, Gl R	NMBl	NMBl, LLBl, Gl R	LLBl, Gl R	NMBl, LLBl
Crocodilia
	Alligatoridae
		Alligator mississippiensis	American alligator		Y	Y	Y
		Caiman latirostris	Broad-snouted caiman			Y
		Melanosuchus niger	Black caiman			Y
		Paleosuchus palpebrosus	Cuvier’s dwarf caiman			Y
		Paleosuchus trigonatus	Schneider’s dwarf caiman	Y
	Crocodylidae
		Crocodylus hombifer	Cuban crocodile			Y
		Crocodylus johnstoni	Freshwater crocodile	Y		Y	Y
		Crocodylus mindorensis	Philippine crocodile	Y
		Crocodylus niloticus	Nile crocodile			Y
		Crocodylus porosus	Saltwater crocodile	Y	Y	Y
		Crocodylus siamensis	Siamese crocodile			Y
		Mecistops cataphractus	West African slender-snouted crocodile		Y	Y	Y
		Osteolaemus tetraspis tetraspis	West African dwarf crocodile				Y
	Gavialidae
		Gavialis gangeticus	Gharial		Y			Y
		Tomistoma schlegelii	Tomistoma			Y

). This was a more time-consuming exercise than with birds, as many minutes could pass between blinks. Nictitating membrane blinks were seen in 15 species, 3 with visible globe retraction, 4 with no evident globe retraction (Figure 16) and 11 associated with globe retraction and elevation of the lower lid (Figure 17). In five species, there was lower lid elevation and globe retraction without visible movement of the nictitating membrane. In no case was there upper lid blinking, though in some cases the upper lid sank a little into the orbit as the globe retracted.

Figure 16. Nictitating membrane blink in an American Alligator (Alligator mississippiensis). Sequence: (a): pre-blink, edge of nictitating membrane visible at inner fornix; (b): nictitating membrane half covers the cornea; (c): nictitating membrane covers the cornea. No change in diameter of palpebral fissure, so no evidence of globe retraction.

Figure 16. Nictitating membrane blink in an American Alligator (Alligator mississippiensis). Sequence: (a): pre-blink, edge of nictitating membrane visible at inner fornix; (b): nictitating membrane half covers the cornea; (c): nictitating membrane covers the cornea. No change in diameter of palpebral fissure, so no evidence of globe retraction.

4. Discussion

The present study confirms the observation of Curio [18] that blinking in birds appears to be of two types, phasic and tonic.

Phasic blinks were frequent, rapid and brief and involved the nictitating membrane and, in some species, the upper lid as well. They occurred during head movement associated with a shift in gaze [16]. Not every shift in gaze was accompanied by a blink, and some blinks, even flurries of blinks, were observed with the head still. Phasic blinks spread tears from the Harderian gland over the surface of the cornea. Debris on the surface of the cornea is also swept towards the medial canthus. Tear fluid drains into puncti on the inner end of the upper and lower eyelid and into the lacrimal duct, and thence to the anterior/cranial nasal cavity.

Tonic blinks were infrequent, slow and sustained, occurring with drowsiness and during preening and involving the nictitating membrane and lower lid. They appear to have the function of protecting the eye from feathers and ‘feather dust’ during preening (and from the bill of other birds preening them). The lower lid would rise and fall as a prelude to sleep and then remain raised during sleep. This protects the eye from exposure and foreign material and shuts out light. That said, it was not uncommon to find that the lower eyelids were paper thin when closed. Tonic blinks are likely to be less effective than phasic blinks in distributing tear fluid and removing debris as they occur less frequently.

During prolonged blinks and during sleep, the cornea is no longer exposed to atmospheric oxygen. In humans, gas exchange continues during sleep by virtue of the rich supply of capillaries on the conjunctival side of the eyelids [21]. If these are also present in birds, gas exchange might be impaired when the nictitating membrane comes between the cornea and the eyelids. It may be significant therefore that the nictitating membrane appears to have a rich arcade of blood vessels.

Involvement of the lower lid in tonic blinks is seen in frogs, turtles, lizards (personal observations), crocodiles as well as birds. This may hark back to the time when fish leaving the sea adopted an amphibious lifestyle. Half-submerged in water, elevation of the lower lid protects the eye from floating debris. In crocodiles, a ‘submergence reflex’, where the lower eyelid elevates and the external auditory meatus closes as the water level rises, has been described [22].

Of particular interest is the finding that in some orders and families of birds, phasic blinks involve not only the nictitating membrane but also the upper lid. It is likely that this feature evolved after the emergence of nictitating membrane blinks, as Crocodilia only blink with their nictitating membranes and lower lids. With birds, Crocodilia are the only living descendants of archosaurs, a group of diapsid amniotes which once included dinosaurs and pterosaurs. While birds have evolved over the last 165–150 million years into 10,000 or so extant species ranging greatly in size, shape and habitat [23], Crocodilia have evolved into only 23 extant species and have changed little since they first appeared [24]. Upper lid blinks were not found in Paleognathae (ratites and tinamous) or Galloanserae (land fowl and waterfowl), only in the Neoaves clade which underwent a rapid expansion following the Cretaceous–Paleogene mass extinction [25].

Upper eyelid blinks were seen mainly in four orders: Columbiformes, Strigiformes, Psicattiformes and Caprimulgimorphae. The question arises, what were the factors which led to this? Have they perhaps evolved from a common ancestor which blinked with its upper eyelids? According to a recent genomic analysis of clade genotypes [25], these four orders are not closely related (

Table A3. Phylogeny of avian blink. Non-coding topology for Neoaves adapted from Braun and Kimball [25]. Clade I: core landbirds or Telluraves; Clade II: core waterbirds or Aequornithes; Clade III: Phaethontimorphae; Clade IV: Otidimorphae; Clade V: Strisores; Clade VI: Columbimorphes; Clade VII: Mirandornithes. : Present.

Clade	Order	Most or All Families with Full Upper Lid Blinks	Some Families with Full Upper Lid Blinks	Families with Full Upper Lid Blinks	Some Families with Partial Upper Lid Blinks	Families with Partial Upper Lid Blinks
I	Passerines			Estrildidae, Troglodytidae
I	Parrots
I	Falcons
I	Seriemas
I	Rollers
I	Woodpeckers
I	Hornbills
I	Trogons
I	Cuckoo-roller
I	Mousebirds
I	Owls
I	Hawks and eagles
I	New World vultures
II	Pelicans
II	Cormorants
II	Storks
II	Penguins
II	Tubenoses
II	Loons
III	Sunbittern
III	Tropicbirds
V	Hummingbirds
V	Swifts
V	Owlet-Nightjars
V	Frogmouths
V	Oilbird
V	Potoos
V	Nightjars
	Shorebirds					Turnicidae
	Cranes and rails
IV	Turacos
IV	Bustards
IV	Cuckoos
VI	Doves
VI	Mesites
VI	Sandgrouse
VII	Flamingos
VII	Grebes
	Landfowl			Phasianidae
	Waterfowl
	Tinamous
	Emu and cassowaries
	Kiwis
	Rheas
	Ostriches
	Crocodilians (OUTGROUP)

). Columbiformes are classified within Columbaves which includes turacos, which do not blink with their upper eyelids. Strigiformes lie between Accipitriformes and Coraciimorphae, neither of which blink with their upper eyelids. Psicattiformes are classed with Australaves, a group which includes falcons, which do not blink with their upper eyelids. Caprimulgimorphae is an order which includes swifts and hummingbirds. In short, no clear pattern of genetic association emerges. Further evidence that upper lid blinking is not related to clade genotypes comes from the finding that even within orders such as Passeriformes and Charadriiformes, which mostly blink with their nictitating membranes, there were families which blinked with their upper lids.

No clear association was apparent between upper lid blinking and nocturnality. Of the orders with upper lid blinks, Strigiformes is the only one which is almost exclusively nocturnal (the exceptions being the northern hawk-owl, Surnia ulula, and the burrowing owl, Athena cunicularia). Within the order of Caprimulgiformes, nightjars (Caprimulgidae) are nocturnal but swifts (Apodidae) and hummingbirds (Trochilidae) are not. Columbiformes and Psittaciformes are diurnal.

These findings suggest that upper lid blinking is the result of convergent evolution. So, what might have been the factors which favoured upper lid blinking? Movement of objects in air tends to be of a higher velocity than in water and therefore more potentially injurious. Birds cannot retract their eyes, and it is retraction in other classes of animal which provides the most protection from blunt mechanical injury [26]. While the lower lid can cover the eye, it tends to move slowly. The rapidly moving upper lids and nictitating membranes might provide reflex closure of the eyes in response to a visual threat (menace reflex) [27], touching of the feather-equivalent of eyelashes by potentially damaging objects like twigs or leaves (lash response) [28] or touching the cornea (corneal reflex) [7].

This begs the question, are birds which blink with their upper lids at greater risk of eye injury than other birds? This may be the case in ground-feeding birds like pigeons (Columbidae) and quails (Phasianidae) which peck for seeds in undergrowth and foliage. A common finding was of blinking with every peck but this could involve the nictitating membrane, upper lid, lower lid or both, depending on the species. Protection during blinking does not depend on having a mobile upper lid. In the case of owls and nightjars, catching live prey capable of injuring their eyes at night may put them at greater risk than other raptors which hunt during the day when visibility is better. But the lower lid and nictitating membrane could also provide this protection. A paper by Ostheim and colleagues [29] raised another possibility. The amount of light focused on the retina by the cornea and lens is related to the size of the pupil. Ostheim and colleagues [29] showed that, in the case of pigeons, the eyelids may also play a role under certain conditions. They found that during pecking, pigeons do not close their eyes completely. The effect of this is to turn the round aperture of the pupil into a narrow horizontal slit, thereby increasing the depth of field [30]. This would result in sharper retinal images of the target, even at close range. For this to occur, upper and lower lids need to come together synergistically. Such behaviour was observed in pigeons, parrots and owls, albeit with drowsiness.

It is hard to know what to make of the many species of bird with partial upper lid blinks—where the inner part of the upper lid lowered a little during a nictitating membrane blink. It did not appear to be produced by eye movement. Perhaps, in these species, upper lid blinks are in the process of evolving into existence—or perhaps out of existence?

Birds and crocodilians both blink with their nictitating membranes to lubricate and clear debris from the cornea. Crocodilia and aquatic birds, such as cormorants (Phalacrocoracidae), may protect their eyes while submerged without losing all vision, using their nictitating membranes, though this has not been established. Certainly, there is a preponderance of transparent nictitating membranes in birds which forage aquatically. Under water, the cornea and nictitating membrane contribute little to refraction of light entering the eye as the cornea is thin and the refractive indices of water and aqueous humour in the anterior chamber of the eye are similar [31]. Birds protect their eyes during sleep and preening by raising the lower eyelids, which are often quite flimsy. By contrast, Crocodilia protect their eyes from injury by retracting the eyeballs deep into the orbits. In saltwater crocodiles, this causes the thickly armored, hinged, upper eyelids to fold like a trapdoor to cover over the orbits. The lower eyelids are also raised. Having larger prey than birds, the requirements of Crocodilia for protection of the eyes are likely to be more stringent than is the case for most birds. In the evolutionary balancing act of reducing body weight while increasing visual acuity, birds have mostly abandoned extraocular muscles which move the eyes and retract them, while increasing the size of the eyes relative to their body mass.

5. Conclusions

Birds (and Crocodilia) have two types of blink: rapid brief (phasic) nictitating membrane blinks; and slow sustained (tonic) lower eyelid blinks. In some avian orders, and in some families within others, phasic nictitating membrane blinks are accompanied by upper eyelid blinks.

Phasic blinks occur on head turn and pecking, tonic blinks on preening and with drowsiness. Nocturnality does not particularly predispose to any blink type.

Upper lid blinking cannot readily be related to phylogeny. The orders where it occurs in every species are not closely related. This type of blinking is probably the result of convergent evolution.