Avian ophthalmic peculiarities

Particularidades oftálmicas em aves

Clarissa Machado de Carvalho Ana Carolina da Veiga Rodarte-Almeida Marcelo Ismar Silva Santana Paula Diniz Galera About the authors

ABSTRACT:

Morphology and physiology of bird eyes are similar to mammals; although, there are peculiarities that should be considered for a correct interpretation of an ophthalmic examination. While the ophthalmology of domestic species is already well established, there are gaps to be filled regarding birds, particularly due to the large number of existing species. This literature review consists of a brief contribution regarding peculiarities of anatomy, physiology, and ophthalmic semiotechnique of the avian eye.

Key words:
anatomy; eye physiology; intraocular pressure; ophthalmic examination; tear test; wild animals

RESUMO:

A morfologia e a fisiologia dos olhos das aves são similares àquelas de mamíferos, mas existem particularidades que devem ser consideradas para a correta interpretação do exame oftálmico. Enquanto a oftalmologia de espécies domésticas já é bem estabelecida, ainda há diversas lacunas no que tange às aves, particularmente devido ao grande número de espécies existentes. Este trabalho objetiva realizar uma revisão bibliográfica abrangendo anatomia, fisiologia e semiologia oftálmica de aves.

Palavras-chave:
animais selvagens; anatomia; exame oftálmico; fisiologia ocular; teste lacrimal; pressão intraocular

INTRODUCTION:

Birds’ vision is highly specialized, being adapted to their lifestyle, habitat, and physical activities. Their visual acuity is excellent and color vision is well developed (CUTHILL et al., 2000CUTHILL, I.C. et al. Ultraviolet vision in birds. Advances in the Study of Behavior, v.29, p.159-214, 2000. Available from: <Available from: https://sciencedirect.com/science/article/pii/S0065345408601059 >. Accessed: May 13, 2017. doi: 10.1016/S0065-3454(08)60105-9.
https://sciencedirect.com/science/artic...
; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
). It is believed that most birds, except for some nocturnal species, are able to detect light in the ultraviolet spectrum (CUTHILL et al., 2000), an ability that plays an important role in camouflage and orientation, as well as inter- and intraspecific communication based on reflection of ultraviolet light in the plumage (CUTHILL et al., 2000; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; WILLIAMS, 2012).

While the ophthalmology of mammalian domestic species is already well established, it is noted that there are still several gaps to be filled regarding domestic and wild birds, particularly due to the large number of existing species. This literature review consists of a brief contribution to the anatomy, physiology, and ophthalmic semiotechnique of the avian eye.

Eyelids and ocular adnexa

Birds have upper and lower eyelids and a nictitating membrane (or third eyelid). The lower eyelid is usually more mobile than the upper eyelid, and capable of covering most of the eyeball during blinking (MURPHY, 1993MURPHY, CJ. Ocular lesions in birds of prey. In: Zoo and Wildlife Medicine, 3 rd edition (ed. Fowler ME). Philadelphia, W.B. Saunders. 1993. 211-221.; WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; MONTIANI-FERREIRA, 2001MONTIANI-FERREIRA F. Ophthalmology. In: FOWLER M.E. & CUBAS Z.S. (Eds). Biology Medicine, and Surgery of South American Wild Animals, 1 ed Ames: Iowa State University Press (UI), 2001. p.437-456.). Eyelids have a fibroelastic tarsal plate without the presence of meibomian glands (MURPHY, 1993MURPHY, CJ. Ocular lesions in birds of prey. In: Zoo and Wildlife Medicine, 3 rd edition (ed. Fowler ME). Philadelphia, W.B. Saunders. 1993. 211-221.; WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
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). In both eyelids, near the edges, there are modified eyelashes called filoplumes, for protection and tactile function (MURPHY, 1993MURPHY, CJ. Ocular lesions in birds of prey. In: Zoo and Wildlife Medicine, 3 rd edition (ed. Fowler ME). Philadelphia, W.B. Saunders. 1993. 211-221.; HARRIS et al., 2008HARRIS, M.C. et al. Ophthalmic examination findings in a colony of Screech owls (Megascops asio). Veterinary ophthalmology, v.11, n.3, p.186-92, 2008. Available from: < Available from: https://dx.doi.org/10.1111/j.1463-5224.2008.00618.x >. Accessed: Jan. 27, 2017. doi: 10.1111/j.1463-5224.2008.00618.x.
https://dx.doi.org/10.1111/j.1463-5224.2...
; BALDOTTO, 2012BALDOTTO, S.B. Investigações sobre oftalmologia de animais de companhia não convencionais, com ênfase na soroprevalência do Encephalitozoon cuniculi.2012. Dissertação (Mestrado em Ciências Agrárias) - Universidade Federal do Paraná. Available from: <Available from: https://acervodigital.ufpr.br/handle/1884/29691 >. Accessed: May 13, 2017.
https://acervodigital.ufpr.br/handle/18...
).

Muscles of the eyeball are thin and undeveloped, being one of the reasons why ocular mobility is limited (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
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). That is compensated by the movement of the head, which can rotate up to 270° (SICK, 1993SICK, H. Order Strigiformes. In: SICK, H. Birds in Brazil: a natural history. Princeton University Press, Princeton, USA, 1993. p.286-298.). There are four straight muscles, two oblique muscles, the pyramidal muscle and a square muscle (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
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).

Nictitating membrane is well developed and highly mobile (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
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), and may be thin, almost transparent, or thicker and white, with interspecific variation (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; HARRIS et al., 2008HARRIS, M.C. et al. Ophthalmic examination findings in a colony of Screech owls (Megascops asio). Veterinary ophthalmology, v.11, n.3, p.186-92, 2008. Available from: < Available from: https://dx.doi.org/10.1111/j.1463-5224.2008.00618.x >. Accessed: Jan. 27, 2017. doi: 10.1111/j.1463-5224.2008.00618.x.
https://dx.doi.org/10.1111/j.1463-5224.2...
; BALDOTTO, 2012BALDOTTO, S.B. Investigações sobre oftalmologia de animais de companhia não convencionais, com ênfase na soroprevalência do Encephalitozoon cuniculi.2012. Dissertação (Mestrado em Ciências Agrárias) - Universidade Federal do Paraná. Available from: <Available from: https://acervodigital.ufpr.br/handle/1884/29691 >. Accessed: May 13, 2017.
https://acervodigital.ufpr.br/handle/18...
; RODARTE-ALMEIDA et al., 2013RODARTE-ALMEIDA, A.C.V. et al. O olho da coruja-orelhuda: observações morfológicas, biométricas e valores de referência para testes de diagnóstico oftálmico. Pesquisa Veterinária Brasileira, v.33, n.10, p.1275-1289, 2013. Available from: < Available from: https://scielo.br/pdf/pvb/v33n10/14.pdf >. Accessed: Jan. 27, 2017. doi: 10.1590/S0100-736X2013001000014.
https://scielo.br/pdf/pvb/v33n10/14.pdf...
; MEEKINS et al., 2015MEEKINS, J.M. et al. Ophthalmic diagnostic tests and ocular findings in a flock of captive american flamingos (Phoenicopterus ruber ruber). Journal of Avian Medicine and Surgery, n.29, v.2, p.95-105, 2015. Available from: < Available from: https://bioone.org/doi/abs/10.1647/2014-021 >. Accessed: Feb. 23, 2017. doi: 10.1647/2014-021.
https://bioone.org/doi/abs/10.1647/2014-...
). It is usually positioned dorsonasally in the conjunctival sac, between the upper eyelid and the eyeball, moving in a ventrotemporal direction (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; HARRIS et al., 2008HARRIS, M.C. et al. Ophthalmic examination findings in a colony of Screech owls (Megascops asio). Veterinary ophthalmology, v.11, n.3, p.186-92, 2008. Available from: < Available from: https://dx.doi.org/10.1111/j.1463-5224.2008.00618.x >. Accessed: Jan. 27, 2017. doi: 10.1111/j.1463-5224.2008.00618.x.
https://dx.doi.org/10.1111/j.1463-5224.2...
). However, in some species, such as the caracara (Caracara plancus), it is found in the palpebral rim of the nasal corner, moving in a nasotemporal direction (BALDOTTO, 2012BALDOTTO, S.B. Investigações sobre oftalmologia de animais de companhia não convencionais, com ênfase na soroprevalência do Encephalitozoon cuniculi.2012. Dissertação (Mestrado em Ciências Agrárias) - Universidade Federal do Paraná. Available from: <Available from: https://acervodigital.ufpr.br/handle/1884/29691 >. Accessed: May 13, 2017.
https://acervodigital.ufpr.br/handle/18...
). This movement is due to contraction of the pyramidal muscle, located in the retrobulbar space, which originates from the posterior region of the sclera, surrounding the optic nerve (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; KERN & COLITZ, 2013KERN, T.J.; COLITZ, C.M.H. Exotic animal ophthalmology. In: GELATT, K.N. et al. Veterinary ophthalmology , Hoboken: Wiley-Blackwell, 2012. Cap. 33, p.1750-1819.), and the square muscle, also located in the posterior region (KERN & COLITZ, 2013KERN, T.J.; COLITZ, C.M.H. Exotic animal ophthalmology. In: GELATT, K.N. et al. Veterinary ophthalmology , Hoboken: Wiley-Blackwell, 2012. Cap. 33, p.1750-1819.).

There is no gland in the third eyelid, and the lacrimal gland is situated in the inferotemporal section of the eyeball (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
), being absent in penguins and owls (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
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). Despite its name, the lacrimal gland plays a secondary role on bird’s tear production (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
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). The harderian gland is the main source of tears in birds, and it lies in the retrobulbar region, adjacent to the sclera, near the base of the third eyelid (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
). The duct comes out from this gland and opens into the conjunctival sac, between the eyeball and third eyelid (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
) and two lacrimal points drain the secretions into the nasolacrimal duct (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; BALDOTTO, 2012BALDOTTO, S.B. Investigações sobre oftalmologia de animais de companhia não convencionais, com ênfase na soroprevalência do Encephalitozoon cuniculi.2012. Dissertação (Mestrado em Ciências Agrárias) - Universidade Federal do Paraná. Available from: <Available from: https://acervodigital.ufpr.br/handle/1884/29691 >. Accessed: May 13, 2017.
https://acervodigital.ufpr.br/handle/18...
). There are no Meibomian glands (KERN & COLITZ, 2013).

Tear production can be measured in birds. The Schirmer tear test (STT) strip has a width of 0.5cm, which makes it difficult to insert it into the conjunctival sac of birds which have a smaller palpebral fissure (LANGE et al., 2014LANGE, R.R. et al. Reference values for the production of the aqueous fraction of the tear film measured by the standardized endodontic absorbent paper point test in different exotic and laboratory animal species. Veterinary Ophthalmology, v.17, n.1, p.41-45, 2014. Available from: < Available from: https://dx.doi.org/10.1111/vop.12038 >. Accessed: Jan. 27, 2017. doi: 10.1111/vop.12038.
https://dx.doi.org/10.1111/vop.12038...
). Consequently, the wetting of the strip’s length cannot be determined in such case (SMITH et al., 2015SMITH, S.P., et al. Evaluation of the phenol red thread tear test in Falconiformes. Journal of Avian Medicine and Surgery, v.29, n.1, p.25-29, 2015. Available from: < Available from: https://bioone.org/doi/abs/10.1647/2008-050 >. Accessed: Feb. 27, 2017. doi: 10.1647/2008-050.
https://bioone.org/doi/abs/10.1647/2008-...
). KORBEL & LEITENSTORFER (1998KORBEL, R.; LEITENSTORFER, P. The modified Schirmer tear test in birds - a method for checking lacrimal gland function. Tierärztliche Praxis. Ausgabe K, Kleintiere/Heimtiere, v.26, n.4, p.284-294, 1998. Available from: <Available from: https://ncbi.nlm.nih.gov/pubmed/9710937 >. Accessed: Jan. 27, 2017.
https://ncbi.nlm.nih.gov/pubmed/9710937...
) suggested cutting the filter paper lengthwise to reduce its width by half, allowing insertion into the conjunctival sac. However, due to the possibility of error in cutting the tapes, the measurement may not be accurate (SMITH et al., 2015SMITH, S.P., et al. Evaluation of the phenol red thread tear test in Falconiformes. Journal of Avian Medicine and Surgery, v.29, n.1, p.25-29, 2015. Available from: < Available from: https://bioone.org/doi/abs/10.1647/2008-050 >. Accessed: Feb. 27, 2017. doi: 10.1647/2008-050.
https://bioone.org/doi/abs/10.1647/2008-...
). In larger birds, there are studies standardizing STT reference values, described in table 1.

Table 1
Reference values for Schirmer tear test (mean ± standard deviation mm/min) and phenol red thread test (mean ± standard).

An alternative is to use the phenol red string test, which could be a less stressful method for birds, requiring only 15s (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; SMITH et al., 2015SMITH, S.P., et al. Evaluation of the phenol red thread tear test in Falconiformes. Journal of Avian Medicine and Surgery, v.29, n.1, p.25-29, 2015. Available from: < Available from: https://bioone.org/doi/abs/10.1647/2008-050 >. Accessed: Feb. 27, 2017. doi: 10.1647/2008-050.
https://bioone.org/doi/abs/10.1647/2008-...
). There are normal values reported for several species, as described in table 1. If bird species values are unknown, healthy cage mates can provide values comparable to physiological ones (WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
).

LANGE et al. (2012LANGE, R.R. et al. Measurement of tear production in black tufted marmosets (Callithrix penicillata) using three different methods: modified Schirmer’s I, phenol red thread and standardized endodontic absorbent paper points. Veterinary Ophthalmology, v.15, n.6, p.376-82, 2012. Available from: <Available from: https://doi.org/10.1111/j.1463-5224.2012.00998.x >. Accessed: Jan. 27, 2017. doi: 10.1111/j.1463-5224.2012.00998.x.
https://doi.org/10.1111/j.1463-5224.2012...
) have suggested the use of endodontic absorbent paper points to measure tear production because they have good absorptive properties, are sterile and have a standardized size, being a practical and easy to use alternative. In addition, its small size provides the possibility of insertion into the conjunctival sac of small species (LANGE et al., 2014LANGE, R.R. et al. Reference values for the production of the aqueous fraction of the tear film measured by the standardized endodontic absorbent paper point test in different exotic and laboratory animal species. Veterinary Ophthalmology, v.17, n.1, p.41-45, 2014. Available from: < Available from: https://dx.doi.org/10.1111/vop.12038 >. Accessed: Jan. 27, 2017. doi: 10.1111/vop.12038.
https://dx.doi.org/10.1111/vop.12038...
). There are reference values (mean ± standard deviation) for canary (Sicalis flaveola) (5.10±0.26mm/min), chestnut-bellied seed finch (Sporophila angolensis) (4.11±0.34mm/min) (LANGE et al. 2014LANGE, R.R. et al. Reference values for the production of the aqueous fraction of the tear film measured by the standardized endodontic absorbent paper point test in different exotic and laboratory animal species. Veterinary Ophthalmology, v.17, n.1, p.41-45, 2014. Available from: < Available from: https://dx.doi.org/10.1111/vop.12038 >. Accessed: Jan. 27, 2017. doi: 10.1111/vop.12038.
https://dx.doi.org/10.1111/vop.12038...
), Lear’s macaw (Ara leari) (13.37±1.22mm/min), blue-and-yellow macaw (Ara ararauna) (16.74±1.38mm/min) (MONÇÃO-SILVA et al., 2016MONÇÃO-SILVA, R.M. et al. Ophthalmic parameters of blue-and-yellow macaws (Ara ararauna) and Lear’s macaws (Anodorhynchus leari). Avian Biology Research, n.9, v.4, p.240-49, 2016. Available from: <Available from: https://doi.org/10.3184/175815516X14725499175746 >. Accessed: Feb. 27, 2017. doi: 10.3184/175815516X14725499175746.
https://doi.org/10.3184/175815516X147254...
), Caatinga parakeets (Eupsittula cactorum) (8.74±2.0mm/min) and yellow-chevroned parakeet (Brotogeris chiriri) (5.89±1.48mm/min) (OLIVEIRA et al. 2017OLIVEIRA, M.M.S. et al. Reference values for selected ophthalmic diagnostic tests in the caatinga parakeet (Eupsitulla cactorum) and yellow-chevroned parakeet (Brotogeris chiriri). Avian Biology Research, v.10, n.4, p.211-217, 2017. Available from: <Available from: https://doi.org/10.3184/175815617X14951979279286 >. Accessed: Jan. 10, 2018. doi: 10.3184/175815617X14951979279286.
https://doi.org/10.3184/175815617X149519...
).

Orbit and paranasal sinuses

In most birds, the supraorbital margin is formed by the frontal bone, while the infraorbital margin is constituted of the suborbital ligament, constituted of fasciae. In Psittaciformes, there is a bone, the suborbital arch. Cranial edge of the orbit is bordered by the lacrimal bone and the caudal edge by the laterosphenoidal bone (PAUL-MURPHY et al., 1990PAUL MURPHY, J. R. et al. Psittacine skull radiography. Veterinary Radiology, v.31, n.4, p.218-24, 1990. Available from: < Available from: https://onlinelibrary.wiley.com/doi/10.1111/j.1740-8261.1990.tb01818.x/abstract >. Accessed: Apr. 25, 2017. doi: 10.1111/j.1740-8261.1990.tb01818.x.
https://onlinelibrary.wiley.com/doi/10.1...
). Predators show a short orbital process of the lacrimal bone, which protrudes from the middle third of the supraorbital margin, directed dorsolaterally and which provides a fixation area for the orbital fascia, protecting the eyeball in the orbit (PYCRAFT, 1903PYCRAFT, W.P. I. A contribution towards our knowledge of the morphology of the owls. II . Osteology. Transactions of the Linnean Society of London, v.9, n.1, p.1-46, 1903. Available from: <Available from: https://onlinelibrary.wiley.com/doi/10.1111/j.1096-3642.1903.tb00445.x/abstract >. Accessed: Jan. 27, 2017. doi: 10.1111/j.1096-3642.1903.tb00445.x.
https://onlinelibrary.wiley.com/doi/10.1...
). The striped owl has a well-developed post-orbital process that constitutes the lateral border of the orbital cavity (RODARTE-ALMEIDA et al., 2013RODARTE-ALMEIDA, A.C.V. et al. O olho da coruja-orelhuda: observações morfológicas, biométricas e valores de referência para testes de diagnóstico oftálmico. Pesquisa Veterinária Brasileira, v.33, n.10, p.1275-1289, 2013. Available from: < Available from: https://scielo.br/pdf/pvb/v33n10/14.pdf >. Accessed: Jan. 27, 2017. doi: 10.1590/S0100-736X2013001000014.
https://scielo.br/pdf/pvb/v33n10/14.pdf...
).

The sesamoid bone of the sclera, whose function is to redirect the path of the tendon of the third eyelid pyramidal muscle, was described for the first time by MAHECHA & OLIVEIRA (1999MAHECHA, G.A.; OLIVEIRA, C. An additional bone in the sclera of the eyes of owls and the Common Potoo (Nictibius griseus) and its role in the contraction of the nictitating membrane. Acta Anatomica, v.163, n.4, p.201-11, 1998. Available from: < Available from: https://ncbi.nlm.nih.gov/pubmed/10072568 >. Accessed: Jan. 27, 2017. doi: 10.1159/000046499.
https://ncbi.nlm.nih.gov/pubmed/10072568...
) in Strigiformes, showing different dimensions and shapes in the different species studied. In the striped owls, this bone was found to be ventral to the ring of scleral ossicles (RODARTE-ALMEIDA et al., 2013RODARTE-ALMEIDA, A.C.V. et al. O olho da coruja-orelhuda: observações morfológicas, biométricas e valores de referência para testes de diagnóstico oftálmico. Pesquisa Veterinária Brasileira, v.33, n.10, p.1275-1289, 2013. Available from: < Available from: https://scielo.br/pdf/pvb/v33n10/14.pdf >. Accessed: Jan. 27, 2017. doi: 10.1590/S0100-736X2013001000014.
https://scielo.br/pdf/pvb/v33n10/14.pdf...
).

The infraorbital sinus and part of the cervical air sac system are located in several groups of birds, lateral to the eyeball, on the nasal and rostroventral sides. The sinus may be connected to pneumatized sections of cranial bones, which spread to the upper parts of the beak, jaw and orbit (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
). The most important feature of the orbit is the proximity of the eyeball to the cervicocephalic diverticulum of the infraorbital sinus. Increase of this diverticulum in cases of sinusitis or other diseases of the upper respiratory tract can lead to a series of ophthalmic conditions due to their proximity to the orbit, such as periorbital swelling, orbital compression, conjunctivitis, exophthalmia or intraocular inflammation (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; KERN & COLITZ, 2013; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
).

Ocular bulb

The eyeball of birds is large in comparison to the size of the skull, occupying up to 50% or more of the cranial volume, being its posterior segment larger than the anterior segment (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; KERN & COLITZ, 2013). The orbits are separated by the interorbital septum, a broad and thin bony structure (PYCRAFT, 1903PYCRAFT, W.P. I. A contribution towards our knowledge of the morphology of the owls. II . Osteology. Transactions of the Linnean Society of London, v.9, n.1, p.1-46, 1903. Available from: <Available from: https://onlinelibrary.wiley.com/doi/10.1111/j.1096-3642.1903.tb00445.x/abstract >. Accessed: Jan. 27, 2017. doi: 10.1111/j.1096-3642.1903.tb00445.x.
https://onlinelibrary.wiley.com/doi/10.1...
; BAUMEL et al., 1993BAUMEL J.J. et al. Handbook of avian anatomy: nomina anatomica avium. 2nd edition. Cambridge: Nutall Ornithological Club, 1993.).

Bone elements that support the sclera are present in several species of vertebrates, and birds possess scleral ossicles (FRANZ-ODENDAAL & HALL, 2006FRANZ-ODENDAAL, T.A.; HALL, BK. Skeletal elements within teleost eyes and a discussion of their homology. Journal of Morphology, v.267, n.11, p.1326-37, 2006. Available from: < Available from: https://ncbi.nlm.nih.gov/pubmed/17051547 >. Accessed: Jan. 27, 2017. doi: 10.1002/jmor.10479.
https://ncbi.nlm.nih.gov/pubmed/17051547...
). These are located in the eye, caudal to the limbus and usually form a ring, without connecting to the other elements of the skull (FRANZ-ODENDAAL & HALL, 2006FRANZ-ODENDAAL, T.A.; HALL, BK. Skeletal elements within teleost eyes and a discussion of their homology. Journal of Morphology, v.267, n.11, p.1326-37, 2006. Available from: < Available from: https://ncbi.nlm.nih.gov/pubmed/17051547 >. Accessed: Jan. 27, 2017. doi: 10.1002/jmor.10479.
https://ncbi.nlm.nih.gov/pubmed/17051547...
). Its posterior extremities form a continuous border with the cartilaginous lamina of the sclera (RODARTE-ALMEIDA et al., 2013RODARTE-ALMEIDA, A.C.V. et al. O olho da coruja-orelhuda: observações morfológicas, biométricas e valores de referência para testes de diagnóstico oftálmico. Pesquisa Veterinária Brasileira, v.33, n.10, p.1275-1289, 2013. Available from: < Available from: https://scielo.br/pdf/pvb/v33n10/14.pdf >. Accessed: Jan. 27, 2017. doi: 10.1590/S0100-736X2013001000014.
https://scielo.br/pdf/pvb/v33n10/14.pdf...
). The shape of the scleral ossicles varies between birds, and can be flattened, slightly convex or concave, dictating the general shape of the ocular bulb (BAUMEL et al., 1993BAUMEL J.J. et al. Handbook of avian anatomy: nomina anatomica avium. 2nd edition. Cambridge: Nutall Ornithological Club, 1993.; FRANZ-ODENDAAL & HALL, 2006FRANZ-ODENDAAL, T.A.; HALL, BK. Skeletal elements within teleost eyes and a discussion of their homology. Journal of Morphology, v.267, n.11, p.1326-37, 2006. Available from: < Available from: https://ncbi.nlm.nih.gov/pubmed/17051547 >. Accessed: Jan. 27, 2017. doi: 10.1002/jmor.10479.
https://ncbi.nlm.nih.gov/pubmed/17051547...
; LIMA et al., 2009LIMA F.C. et al. Anatomy of the scleral ossicles in brazilian birds. Brazilian Journal of Morphological Science, v.26, n.3-4, p.165-169, 2009. Available from: < Available from: https://jms.org.br/v26n3-4/07 >. Accessed: Jan. 27, 2017.
https://jms.org.br/v26n3-4/07...
). Two main functions of the ossicles have been described: protecting and supporting the eyeball, minimizing deformation during flight or diving, as well as assisting the ciliary muscles in visual accommodation (WALLS, 1942 apud FRANZ-ODENDAAL & HALL, 2006). The positioning of the ossicles does not vary between species, but the number and shape of the ossicles do (FRANZ-ODENDAAL & HALL, 2006)FRANZ-ODENDAAL, T.A.; HALL, BK. Skeletal elements within teleost eyes and a discussion of their homology. Journal of Morphology, v.267, n.11, p.1326-37, 2006. Available from: < Available from: https://ncbi.nlm.nih.gov/pubmed/17051547 >. Accessed: Jan. 27, 2017. doi: 10.1002/jmor.10479.
https://ncbi.nlm.nih.gov/pubmed/17051547...
. LIMA et al. (2009)LIMA F.C. et al. Anatomy of the scleral ossicles in brazilian birds. Brazilian Journal of Morphological Science, v.26, n.3-4, p.165-169, 2009. Available from: < Available from: https://jms.org.br/v26n3-4/07 >. Accessed: Jan. 27, 2017.
https://jms.org.br/v26n3-4/07...
carried out a study with 208 birds of 18 different orders, in which the anatomy of the ossicles of these birds was described; shape and arrangement and number of plates were different between species, with intra and interspecific numeric variation and also between the eyes of the same individual. RODARTE-ALMEIDA et al. (2013) RODARTE-ALMEIDA, A.C.V. et al. O olho da coruja-orelhuda: observações morfológicas, biométricas e valores de referência para testes de diagnóstico oftálmico. Pesquisa Veterinária Brasileira, v.33, n.10, p.1275-1289, 2013. Available from: < Available from: https://scielo.br/pdf/pvb/v33n10/14.pdf >. Accessed: Jan. 27, 2017. doi: 10.1590/S0100-736X2013001000014.
https://scielo.br/pdf/pvb/v33n10/14.pdf...
also reported intraspecific and individual variation in striped owls.

There are three typical eyeball formats in birds: flat, globose, and tubular (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
). In the flat eyeball, there is a short anteroposterior axis on the ciliary region, that is flat or partially concave, convex cornea and posterior hemispheric segment (present in parrots and passerines) (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; BAYÓN et al., 2007). In the globose form, the ciliary region protrudes further into the posterior pole, with a concave shape (found in diurnal birds of prey, crows, etc.) (BAYÓN et al., 2007). In the tubular eyeball, the intermediate segment is concave and extends posteriorly, forming a tube before joining the posterior segment (present in nocturnal birds; BAYÓN et al., 2007).

It is possible to measure the intraocular pressure of birds with applanation tonometer (Tonopen®), which requires the instillation of topical anesthetic on the surface of the cornea 10 to 15s before the measurement, or a rebound tonometer (Tonovet®, Tonovet Plus®), that doesn’t require topical anesthesia (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
). Tip of the rebound tonometer can be used on corneas around 3 mm thick, while the applanation tonometer tip requires a cornea with at least twice that thickness (WILLIAMS, 2012). So, it’s advised to notice that smaller birds may require the use of rebound tonometer in order to obtain their intraocular pressure, since readings with applanation tonometers provide non-reliable readings (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
). In a study conducted with the Tonopen® in 275 birds of 39 species, the values varied between 9.2 and 16.3mmHg (WILLIS & WILKIE, 1999). Other reference values for applanation and rebound tonometry are described in tables 2 and 3, respectively. Papers regarding the use of TonoVet Plus for birds, stablishing reference values, weren’t reported.

Table 2
Reference values for applanation tonometry (mean ± standard deviation mmHg).
Table 3
Reference values for rebound tonometry (mean ± standard deviation mmHg).

Anterior pole

Cornea of most bird species is thinner than that of mammals (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
), except for some diurnal birds of prey and waterfowl (WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
). It has five layers, with Bowman’s membrane below the epithelium (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; MONÇÃO-SILVA et al., 2016MONÇÃO-SILVA, R.M. et al. Ophthalmic parameters of blue-and-yellow macaws (Ara ararauna) and Lear’s macaws (Anodorhynchus leari). Avian Biology Research, n.9, v.4, p.240-49, 2016. Available from: <Available from: https://doi.org/10.3184/175815516X14725499175746 >. Accessed: Feb. 27, 2017. doi: 10.3184/175815516X14725499175746.
https://doi.org/10.3184/175815516X147254...
).

The iris color may vary according to the species, and there may also be intraspecific alteration, depending on the amount and types of pigments, degree of vascularization, age, sex and diet (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; BORTOLOTTI et al., 2003BORTOLOTTI, G.R. et al. Iris colour of american kestrels varies with age, sex, and exposure to PCBs. Physiological and Biochemical Zoology, v.76, n.1, p.99-104, 2003. Available from: <Available from: https://doi.org/10.1086/345485 >. Accessed Jan. 27, 2017.
https://doi.org/10.1086/345485...
; KERN & COLITZ, 2013; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
; RODARTE-ALMEIDA et al., 2013RODARTE-ALMEIDA, A.C.V. et al. O olho da coruja-orelhuda: observações morfológicas, biométricas e valores de referência para testes de diagnóstico oftálmico. Pesquisa Veterinária Brasileira, v.33, n.10, p.1275-1289, 2013. Available from: < Available from: https://scielo.br/pdf/pvb/v33n10/14.pdf >. Accessed: Jan. 27, 2017. doi: 10.1590/S0100-736X2013001000014.
https://scielo.br/pdf/pvb/v33n10/14.pdf...
), exposure to polychlorinated biphenyls (BORTOLOTTI et al., 2003) and reproductive season (O’CONNELL et al., 2017O’CONNELL, K.M. et al. Ophthalmic diagnostic testing and examination findings in a colony of captive brown pelicans (Pelecanus occidentalis). Veterinary Ophthalmology, v.20, n.3, p.196-204, 2017. Available from: < Available from: https://onlinelibrary.wiley.com/doi/10.1111/vop.12389/full >. Accessed: Nov. 06, 2018. doi: 10.1111/vop.12389.
https://onlinelibrary.wiley.com/doi/10.1...
). There is a wide range of colors that can be observed, from brown to yellow to blue (BORTOLOTTI et al., 2003; BALDOTTO, 2012BALDOTTO, S.B. Investigações sobre oftalmologia de animais de companhia não convencionais, com ênfase na soroprevalência do Encephalitozoon cuniculi.2012. Dissertação (Mestrado em Ciências Agrárias) - Universidade Federal do Paraná. Available from: <Available from: https://acervodigital.ufpr.br/handle/1884/29691 >. Accessed: May 13, 2017.
https://acervodigital.ufpr.br/handle/18...
; WILLIAMS, 2012; RODARTE-ALMEIDA et al., 2013; MEEKINS et al., 2015MEEKINS, J.M. et al. Ophthalmic diagnostic tests and ocular findings in a flock of captive american flamingos (Phoenicopterus ruber ruber). Journal of Avian Medicine and Surgery, n.29, v.2, p.95-105, 2015. Available from: < Available from: https://bioone.org/doi/abs/10.1647/2014-021 >. Accessed: Feb. 23, 2017. doi: 10.1647/2014-021.
https://bioone.org/doi/abs/10.1647/2014-...
).

The musculature of the bird iris is composed mainly of striated muscle fibers, which allow the voluntary contraction of the pupil, which makes it difficult to evaluate the pupillary light reflex (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
). The use of topical or intracameral neuroblockers for pharmacological dilation of the pupil, such as non-depolarizing muscle relaxants, is mandatory (BAYÓN et al., 2007; WILLIAMS, 2012). Induction of mydriasis with the use of topical rocuronium bromide is reported in the common buzzard (Buteo buteo), little owl (Athene noctua) (BARSOTTI et al., 2010aBARSOTTI, G. et al. Bilateral mydriasis in common buzzards (Buteo buteo) and little owls (Athene noctua) induced by concurrent topical administration of rocuronium bromide. Veterinary Ophthalmology, v.13, s.1, p.35-40, 2010a. Available from: < Available from: https://onlinelibrary.wiley.com/doi/10.1111/j.1463-5224.2010.00808.x/full >. Accessed: Feb. 23, 2017. doi: 10.1111/j.1463-5224.2010.00808.x.
https://onlinelibrary.wiley.com/doi/10.1...
), tawny owl (Strix aluco) (BARSOTTI et al., 2010bBARSOTTI, G. et al. Mydriatic effect of topically applied rocuronium bromide in tawny owls (Strix aluco): comparison between two protocols. Veterinary Ophthalmology, v.13, s.1, p.9-13, 2010b. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/20840085 >. Accessed: Feb. 23, 2017. doi: 10.1111/j.1463-5224.2010.00773.x.
https://www.ncbi.nlm.nih.gov/pubmed/2084...
) and European kestrel (Falco tinnunculus) (BARSOTTI et al., 2012) without adverse side effects.

Discrete anisocoria may be normal in stress situations and is commonly described in birds (MONTIANI-FERREIRA, 2001MONTIANI-FERREIRA F. Ophthalmology. In: FOWLER M.E. & CUBAS Z.S. (Eds). Biology Medicine, and Surgery of South American Wild Animals, 1 ed Ames: Iowa State University Press (UI), 2001. p.437-456.; HARRIS et al., 2008HARRIS, M.C. et al. Ophthalmic examination findings in a colony of Screech owls (Megascops asio). Veterinary ophthalmology, v.11, n.3, p.186-92, 2008. Available from: < Available from: https://dx.doi.org/10.1111/j.1463-5224.2008.00618.x >. Accessed: Jan. 27, 2017. doi: 10.1111/j.1463-5224.2008.00618.x.
https://dx.doi.org/10.1111/j.1463-5224.2...
). There is direct (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; HARRIS et al., 2008) and consensual pupillary light reflex; although, difficult to observe routinely (LI & HOWLAND, 1999).

Iridocorneal angle in birds is well developed, and it can be observed that the trabecular meshwork extends through the iris stroma (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; RODARTE-ALMEIDA et al., 2013RODARTE-ALMEIDA, A.C.V. et al. O olho da coruja-orelhuda: observações morfológicas, biométricas e valores de referência para testes de diagnóstico oftálmico. Pesquisa Veterinária Brasileira, v.33, n.10, p.1275-1289, 2013. Available from: < Available from: https://scielo.br/pdf/pvb/v33n10/14.pdf >. Accessed: Jan. 27, 2017. doi: 10.1590/S0100-736X2013001000014.
https://scielo.br/pdf/pvb/v33n10/14.pdf...
). The lateral extension of the anterior chamber is broad, continuing posteriorly, between the ciliary body and the sclera, being referred to as the cilioscleral sinus (EVANS & MARTIN, 1993EVANS, H.E.; MARTIN, G.R. Organa sensuum. In: Baumel J.J. (Ed.). Handbook of avian anatomy: nomina anatomica avium, Cambridge, Massachusetts: The Nuttal Ornithological Club, 1993. p.585-611.). This sinus is crossed by a large network of elastic fibers that make up pectinate ligaments with wide openings, called spaces of iridocorneal angle or spaces of Fontana (EVANS & MARTIN, 1993). RODARTE-ALMEIDA et al. (2013) described these ligaments as well-developed in owls and with extensive trabecular meshwork, especially in the temporal region of the eye, making it possible to observe the spaces of iridocorneal angle without use of lens for gonioscopy in the unarmed eye of young birds.

Birds have excellent visual accommodation capacity, a process of changing the focal length of the lens by means of altering the corneal curvature associated with anterior movement and lens deformation (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; KERN & COLITZ, 2013; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
). Lens is transparent and has a variable shape, being almost spherical in nocturnal birds and anteriorly flat in diurnal species (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; BAYÓN et al., 2007). Under the peripheral region of the lens there is a modified fibrous annular pad (WILLIS & WILKIE, 1999; WILLIAMS, 2012) that allows attachment between the lens and ciliary body, and consequently with the muscles responsible for accommodation, which are called Brucke’s and Crampton’s muscles (BAYÓN et al., 2007; KERN & COLITZ, 2013; WILLIAMS, 2012).

Crampton’s muscle originates in the sclera, below the scleral ossicles, and contracts to flatten the cornea along its periphery and bulges the center, increasing refractive power (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; KERN & COLITZ, 2013; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
). Brucke’s muscle pulls the ciliary body forward, decreasing the tension applied to the annular pad by the tenacular ligament of the ciliary body (BAYÓN et al., 2007; KERN & COLITZ, 2013; WILLIAMS, 2012). Deformation of the lens is also caused by the pressure of the circumferential muscle of the iris, which bulges the central portion of the lens, increasing its refractive power (WILLIAMS, 2012). Density of this muscle differs between species and is well developed in diving birds, where it is necessary to compensate for the lack of refraction of the cornea underwater (WILLIAMS, 2012).

Posterior pole

The retina is atapetal and avascular, being nourished primarily by the choroid (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; KERN & COLITZ, 2013; RUGGERI et al., 2010RUGGERI, M. et al. Retinal structure of birds of prey revealed by ultra-high resolution spectral-domain optical coherence tomography. Investigative ophthalmology & visual science, v.51, n.11, p.57-89, 2010. Available from: < Available from: https://ncbi.nlm.nih.gov/pmc/articles/PMC3061512/ >. Accessed: Jan. 27, 2017. doi: 10.1167/iovs.10-5633.
https://ncbi.nlm.nih.gov/pmc/articles/PM...
). The vascularization and pigmentation of the choroid determine its coloration, usually gray or reddish, and it is possible to visualize the choroidal vessels in some species (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; KERN & COLITZ, 2013; RODARTE-ALMEIDA et al., 2013RODARTE-ALMEIDA, A.C.V. et al. O olho da coruja-orelhuda: observações morfológicas, biométricas e valores de referência para testes de diagnóstico oftálmico. Pesquisa Veterinária Brasileira, v.33, n.10, p.1275-1289, 2013. Available from: < Available from: https://scielo.br/pdf/pvb/v33n10/14.pdf >. Accessed: Jan. 27, 2017. doi: 10.1590/S0100-736X2013001000014.
https://scielo.br/pdf/pvb/v33n10/14.pdf...
).

The type of photoreceptors and their density varies according to the visual ecology of the species, but usually rods and cones are present (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; CUTHILL et al., 2000CUTHILL, I.C. et al. Ultraviolet vision in birds. Advances in the Study of Behavior, v.29, p.159-214, 2000. Available from: <Available from: https://sciencedirect.com/science/article/pii/S0065345408601059 >. Accessed: May 13, 2017. doi: 10.1016/S0065-3454(08)60105-9.
https://sciencedirect.com/science/artic...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
). Some species present double cones and have oil droplets (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; CUTHILL et al., 2000) with a high content of carotenoids, which function is to filter the ultraviolet radiation that reaches the photoreceptors (CUTHILL et al., 2000). Generally, there is a region with a high density of cones, the area centralis (WILLIS & WILKIE, 1999).

In some birds, there is a fovea, a region of retinal depression where there is a dense arrangement of cones and a thinning of the layers of the retina, which allows more intense light stimulation in this region (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
). According to the number of foveas, birds can be classified as afoveal, monofoveal and bifoveal (BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
). Poultry have an a foveal retina and an areas centralis, having lower visual acuity compared to other birds (MONTIANI-FERREIRA, 2001MONTIANI-FERREIRA F. Ophthalmology. In: FOWLER M.E. & CUBAS Z.S. (Eds). Biology Medicine, and Surgery of South American Wild Animals, 1 ed Ames: Iowa State University Press (UI), 2001. p.437-456.). The monofoveal retinas have a central fovea (most birds) or temporal fovea (nocturnal predators, swallows), with or without an area centralis around the fovea (MURPHY, 1993MURPHY, CJ. Ocular lesions in birds of prey. In: Zoo and Wildlife Medicine, 3 rd edition (ed. Fowler ME). Philadelphia, W.B. Saunders. 1993. 211-221.; OROSZ, 2007OROSZ, S.E. The special senses of birds. In: Coles B.H. (Ed.) Essentials of avian medicine and surgery, 3rd ed. Oxford, UK: Blackwell Publishing. 2007. p.22-39. ; RUGGERI et al., 2010RUGGERI, M. et al. Retinal structure of birds of prey revealed by ultra-high resolution spectral-domain optical coherence tomography. Investigative ophthalmology & visual science, v.51, n.11, p.57-89, 2010. Available from: < Available from: https://ncbi.nlm.nih.gov/pmc/articles/PMC3061512/ >. Accessed: Jan. 27, 2017. doi: 10.1167/iovs.10-5633.
https://ncbi.nlm.nih.gov/pmc/articles/PM...
). In the bifoveal retinas, there is a main central fovea and an auxiliary one, with or without area centralis between the foveas (passerines, diurnal predators and other birds that hunt during flight) (MURPHY, 1993; MONTIANI-FERREIRA, 2001; BAYÓN et al., 2007; OROSZ, 2007; RUGGERI et al., 2010).

The pecten (pecten oculi) is a tissue projection that emerges from the choroid towards the vitreous body, located above the optic disc and reported in almost all birds. It is pigmented, with blackish coloration, and highly vascularized (WILLIS & WILKIE, 1999LI, T.; HOWLAND, H.C. A true neuronal consensual pupillary reflex in chicks. Vision Research, v.39, n.5, p.897-900, 1999. Available from: <Available from: https://doi.org/10.1016/S0042-6989(98)00197-7 >. Accessed: Jan. 27, 2017. doi: 10.1016/S0042-6989(98)00197-7.
https://doi.org/10.1016/S0042-6989(98)00...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; RUGGERI et al., 2010RUGGERI, M. et al. Retinal structure of birds of prey revealed by ultra-high resolution spectral-domain optical coherence tomography. Investigative ophthalmology & visual science, v.51, n.11, p.57-89, 2010. Available from: < Available from: https://ncbi.nlm.nih.gov/pmc/articles/PMC3061512/ >. Accessed: Jan. 27, 2017. doi: 10.1167/iovs.10-5633.
https://ncbi.nlm.nih.gov/pmc/articles/PM...
). It is assumed that the pecten has the primary function of retinal nutrition and maintenance of intraocular pressure (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; FERREIRA et al., 2016FERREIRA, T.A. et al. Hemodynamics of the pectinis oculi artery in American pekin duck (Anas platyrhynchos domestica). Veterinary ophthalmology, v.19, n.5, p.409-13.2016 Available from: <Available from: https://ncbi.nlm.nih.gov/pubmed/26398920 >. Accessed: Feb. 23, 2017. doi: 10.1111/vop.12316.
https://ncbi.nlm.nih.gov/pubmed/26398920...
). FERREIRA et al. (2016) FERREIRA, T.A. et al. Hemodynamics of the pectinis oculi artery in American pekin duck (Anas platyrhynchos domestica). Veterinary ophthalmology, v.19, n.5, p.409-13.2016 Available from: <Available from: https://ncbi.nlm.nih.gov/pubmed/26398920 >. Accessed: Feb. 23, 2017. doi: 10.1111/vop.12316.
https://ncbi.nlm.nih.gov/pubmed/26398920...
used vascular Doppler ultrasonography to determine blood flow parameters of the pecten in ducks, with results suggestive of high metabolic activity in the pecten, indicating possible nutritional functions, production of aqueous humor and regulation of intraocular pressure.

The pecten is morphologically classified according to its shape and number of folds: conical, found in kiwis (Apterix australis); in the form of wing or flag, reported in ostriches (Struthio camelus) and rheas (Rhea americana); and folded or pleated, reported in all other species (KERN & COLITZ, 2013). The optic disc is long and oval, but it cannot be observed by ophthalmoscopy, since it is located below the pecten, which obstructs its visualization (WILLIS & WILKIE, 1999WILLIS, A.M.; WILKIE, D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery, p.160-166, 1999. Available from: < Available from: https://jstor.org/stable/30130679 >. Accessed: Jan. 31, 2017.
https://jstor.org/stable/30130679...
; BAYÓN et al., 2007BAYÓN, A. et al. Avian ophthalmology. European Journal of Companion Animal Practice, v.17, n.3, p.253-266, 2007. Available from: <Available from: https://kruuse.com/da-DK/VidenOm/~/media/Files/ALL/Avian%20ophthalmology.ashx >. Accessed: Jan. 27, 2017.
https://kruuse.com/da-DK/VidenOm/~/medi...
; WILLIAMS, 2012WILLIAMS, D.L. The avian eye. In: WILLIAMS, D.L. Ophthalmology of Exotic Pets, John Wiley & Sons, Ltd, 2012. p.119-58. Available from: <Available from: https://doi.org/10.1002/9781118709627.ch9 >. Accessed: Feb. 27, 2017. doi: 10.1002/9781118709627.ch9.
https://doi.org/10.1002/9781118709627.ch...
).

CONCLUSION:

The field of avian ophthalmology is broad and needs constant research and updates in order to start to fill the gaps. As noted, the numerous features inherent to the avian eye make it essential to investigate and report the reference values and peculiarities in the different genus and, sometimes, species. It is necessary to know the anatomical and physiological characteristics of the birds to adapt materials and procedures and to be able to correctly interpret the findings of physical and complementary examinations.

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  • CR-2017-0904.R3

Publication Dates

  • Publication in this collection
    2018

History

  • Received
    13 Dec 2017
  • Accepted
    31 Oct 2018
  • Reviewed
    22 Nov 2018
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