Anatomical, histological and computed tomography comparisons of the eye and adnexa of crab-eating fox (Cerdocyon thous) to domestic dogs

Autoři: Nayone Lima Lantyer-Araujo aff001;  Danielle Nascimento Silva aff001;  Alessandra Estrela-Lima aff002;  Caterina Muramoto aff002;  Fernanda de Azevedo Libório aff003;  Érica Augusta da Silva aff001;  Arianne Pontes Oriá aff002
Působiště autorů: Post-Graduate Program in Animal Science in the Tropics, School of Veterinary Medicine and Zootechny, Federal University of Bahia (UFBA), Salvador, Bahia, Brazil aff001;  Department of Veterinary Anatomy, Pathology and Clinics, School of Veterinary Medicine and Zootechny, UFBA, Salvador, Bahia, Brazil aff002;  Screening Center for Wild Animals, Brazilian Institute of the Environment and Renewable Natural Resources, Salvador, Bahia, Brazil aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


An understanding of species' morphological and physiological parameters is crucial to developing conservation strategies for wild animals kept in human care. Detailed information is lacking for crab-eating fox (Cerdocyon thous) eyes and adnexa. Therefore, the aim of this study was to describe anatomical, histological and computed tomography (CT) features of the eye and adnexa in crab-eating fox, compared to domestic dogs. CT of the eye and adnexa of one live animal and a frozen specimen was performed for anatomical identification. In addition, the heads of five animals of each species were fixed in 10% buffered formalin for gross anatomical description of the eye and adnexa using topographic dissection and exenteration techniques. All steps were photographed and features such as location, shape, and distances and relationships between structures were described. For histological evaluation, two eyes of each species were fixed in 10% buffered formalin, processed by routine paraffin inclusion technique and stained with hematoxylin and eosin. The CT scan was difficult to evaluate, mainly that of the frozen head, which did not provide good definition of the soft tissues; nevertheless, it demonstrated the potential for structure visualization and description. The gross anatomical and histological evaluations showed the presence of eyelashes on the upper eyelid and of upper and lower lacrimal points, an incomplete orbit with supraorbital ligament, slightly exposed sclera with discretely pigmented limbus and pigmentation throughout the conjunctiva, and a slit-shaped pupil. Hematoxylin and eosin staining demonstrated structural similarities between the crab-eating fox and domestic dog. Thus, the possibility of using the domestic dog as a study model for the preventive and therapeutic management of wild dogs kept in human care is demonstrated.

Klíčová slova:

Computed axial tomography – Dogs – Domestic animals – Eye muscles – Eyes – Pets and companion animals – Animal ocular anatomy


1. Ramos VA Jr, Pessutti C, Chieregatto CAFS. Guia de identificação dos canídeos silvestres brasileiros. Sorocaba: JoyJoy Studio Ltda.–Comunicação Ambiental; 2003.

2. Wozencraft WC. Order Carnivora. In: Wilson DE, Reeder DM, editors. Mammal species of the world: a taxonomic and geographic reference. 3rd ed. Washington DC: Smithsonian Institution Press; 2005. pp. 532–628.

3. Courtenay O, Maffei L. Cerdocyon thous. In: IUCN 2010. IUCN Red List of Threatened Species. 2008. Version 2010.4. [cited 2015 Jul 17]. Available from:

4. Convention on international trade in endangered species of wild fauna and flora (CITES). Appendices I, II and III. Geneva: International Environment House; 2014.

5. Beisiegel BM, Lemos FG, Azevedo FC, Queirolo D, Jorge RSP. Avaliação do risco de extinção do cachorro-do-mato Cerdocyon thous (Linnaeus, 1766) no Brasil. Biodiversidade Brasileira. 2013; 3(1): 138–145.

6. Daszak P, Cunningham AA, Hyatt AD. Emerging infectious diseases of wildlife–threats to biodiversity and Human Health. Science. 2000; 287: 443–449. doi: 10.1126/science.287.5452.443 10642539

7. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, Kamal M, et al. Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature. 2005; 438(8): 803–819. doi: 10.1038/nature04338 16341006

8. Souza NP, Almeida ABPF, Freitas TPT, Paz RCR, Dutra V, Nakazato L, et al. Leishmania (Leishmania) infantum chagasi in wild canids kept in captivity in the State of Mato Grosso. Rev Soc Bras Med Trop. 2010;43(3):333–335. doi: 10.1590/s0037-86822010000300024 20563507

9. Almeida AP, Souza TD, Marcili A, Labruna MB. Novel Ehrlichia and Hepatozoon Agents Infecting the Crab-Eating Fox (Cerdocyon thous) in Southeastern Brazil. J Med Entomol. 2013; 50(3): 640–646. doi: 10.1603/me12272 23802461

10. Catenacci LS, Griese J, Silva RC, Langoni H. Toxoplasma gondii and Leishmania spp. infection in captive crab-eating foxes, Cerdocyon thous (Carnivora, Canidae) from Brazil. Vet Parasitol. 2010; 169: 190–192. doi: 10.1016/j.vetpar.2009.12.019 20060648

11. Curi NHA, Coelho CM, Malta MCC, Magni EMV, Sábato MAL, Araújo AS, et al. Pathogens of wild maned wolves (Chrysocyon brachyurus) in Brazil. J Wildl Dis. 2012; 48(4): 1052–1056. doi: 10.7589/2011-10-304 23060508

12. McIness EF, Burroughs REJ, Duncan NM. Possible vaccine-induced canine distemper in a South American Bush Dog (Speothos venaticus). J Wildl Dis. 1992; 28(4): 614–617. doi: 10.7589/0090-3558-28.4.614 1474661

13. Kern TJ, Colitz CMH. Exotic animal ophthalmology. In: Gelatt KN, Gilger BC, Kern TJ, editors. Veterinary Ophthalmology. 5th ed. Iowa: John Wiley & Sons; 2013. Chapter 33, pp. 1750–1819.

14. Park SA, Taylor KT, Zwingenberger AL, Reilly CM, Toupadakis CA, Marfurt CF, et al. Gross anatomy and morphometric evaluation of the canine lacrimal and third eyelid glands. Vet Ophthalmol. 2016; 19(3): 230–236. doi: 10.1111/vop.12288 26076886

15. Montiani-Ferreira F, Truppel J, Tramontin MH, Vilani RGD, Lange RR. The capybara eye: clinical tests, anatomic and biometric features. Vet Ophthalmol. 2008; 11(6): 386–394. doi: 10.1111/j.1463-5224.2008.00663.x 19046280

16. Sarma K. Morphological and craniometrical studies on the skull of kagani goat (Capra hircus) of Jammu region. Int J Morphol. 2006; 24: 449–455. doi: 10.4067/S0717-95022006000400025

17. Silva DN, Oriá AP, Araujo NL, Martins-Filho E, Muramoto C, Liborio FA, et al. Morphological study of the eye and adnexa in capuchin monkeys (Sapajus sp.). PLoS ONE. 2017; 12(12): e0186569. doi: 10.1371/journal.pone.0186569 29206882

18. Banzato T, Selleri P, Veladiano IA, Martin A, Zanetti E, Zotti A. Comparative evaluation of the cadaveric, radiographic and computed tomographic anatomy of the heads of green iguana (Iguana iguana), common tegu (Tupinambis merianae) and bearded dragon (Pogona vitticeps). BMC Vet Res. 2012; 8(53): 1–11. doi: 10.1186/1746-6148-8-53 22578088

19. Souza NM, Maggs DJ, Park SA, Puchalski SM, Reilly CM, Paul-Murphy J, et al. Gross, histologic, and micro-computed tomographic anatomy of the lacrimal system of snakes. Vet Ophthalmol. 2015; 18(Suppl. 1): 15–22. doi: 10.1111/vop.12184 24862081

20. Bolzan AA, Brunelli ATJ, Castro MB, Souza MA, Souza JL, Laus JL. Conjunctival impression cytology in dogs. Vet Ophthalmol. 2005; 8(6): 401–405. doi: 10.1111/j.1463-5224.2005.00414.x 16359363

21. Maggs DJ. Diseases of the conjunctiva. In: Maggs D, Miller P, Ofri R, editors. Slatter’s fundamentals of veterinary ophthalmology. 6th ed. Missouri: Elsevier; 2017. Chapter 7, pp. 140–158.

22. Perazzi A, Bonsembiante F, Gelain ME, Patruno M, Eorio ED, Migliorati A, et al. Cytology of the healthy canine and feline ocular surface: comparison between cytobrush and impression technique. Vet Clin Pathol. 2017; 46(1): 164–171. doi: 10.1111/vcp.12450 28117903

23. Cullen CL. Normal ocular features, conjunctival microflora and intraocular pressure in the Canadian beaver (Castor canadensis). Vet Ophthalmol. 2003; 6(4): 279–284. doi: 10.1111/j.1463-5224.2003.00307.x 14641823

24. Nichols B. Conjunctiva. Microscopy Res Technique. 1996; 33: 296–319. doi: 10.1002/(SICI)1097-0029(19960301)33:4<296::AID-JEMT2>3.0.CO;2-O

25. Moore CP, Wilsman NJ, Nordheim EV, Majors LJ, Collier LL. Density and distribution of canine conjunctival goblet cells. Invest Ophthalmol Vis Sci. 1987; 28: 1925–1932. 3679745

26. Martins BC, Oriá AP, Souza ALG, Campos CF, Almeida DE, Duarte RA, et al. Ophthalmic patterns of captive brown brocket deer (Mazama gouazoubira). J Zoo Wildl Med. 2007; 38(4): 526–532. doi: 10.1638/MS05-084.1 18229857

27. Gasser K, Fuchs-Baumgartinger A, Tichy A, Nell B. Investigations on the conjunctival goblet cells and on the characteristics of glands associated with the eye in the guinea pig. Vet Ophthalmol. 2011; 14(1): 26–40. doi: 10.1111/j.1463-5224.2010.00836.x 21199277

28. Sebbag L, Reilly CM, Eid R, Maggs DJ. Goblet cell density and distribution in cats with clinically and histologically normal conjunctiva. Vet Ophthalmol. 2016; 19(Suppl. 1): 38–43. doi: 10.1111/vop.12343 26799820

29. World Association of Veterinary Anatomists (WAVA). Nomina Anatomica Veterinaria. 6th ed. Vienna: International Committee of Veterinary Gross Anatomical Nomenclature; 2017. p. 149.

30. Lee AG, Johnson MC, Policeni BA, Smoker WRK. Imaging for neuro-ophthalmic and orbital disease–a review. Clin Exp Ophthalmol. 2009; 37: 30–53. doi: 10.1111/j.1442-9071.2008.01822.x 19016810

31. Deemer JL. Inflection in inactive lateral rectus muscle: evidence suggesting focal mechanical effects of connective tissues. Invest Ophthalmol Vis Sci. 2008; 49(11): 4858–4864. doi: 10.1167/iovs.08-2069 18599563

32. Murphy CJ, Samuelson DA, Pollock RV. The eye. In: Evans HE, de Lahunta A, editors. Miller’s Anatomy of the Dog. 4th ed. Philadelphia: WB Saunders Co.; 2012. p. 765.

33. Sires BS, Saari JC, Garwin GG, Hurst JS, Van Kuijk FJGM. The color difference in orbital fat. Arch Ophthalmol. 2001; 119: 868–871. doi: 10.1001/archopht.119.6.868 11405838

34. Udhay P, Noronha OV, Mohan RE. Helical computed tomographic dacryocystography and its role in the diagnosis and management of lacrimal drainage system blocks and medial canthal masses. Indian J Ophthalmol. 2008; 56(1): 31–37. doi: 10.4103/0301-4738.37593 18158401

35. Schlueter C, Budras KD, Ludewig E, Mayrhofer E, Koenig HE, Walter A, et al. CT and anatomical study of the relationship between head conformation and the nasolacrimal drainage system. J Feline Med Surg. 2009; 11: 891–900. doi: 10.1016/j.jfms.2009.09.010 19857852

36. Rached PA, Canola JC, Schluter C, Laus JL, Oechtering G, Almeida DE, et al. Computed tomographic-dacryocystography (CT-DCG) of the normal canine nasolacrimal drainage system with three-dimensional reconstruction. Vet Ophthalmol. 2011; 14(3):174–179. doi: 10.1111/j.1463-5224.2010.00861.x 21521441

37. Zwingenberger AL, Park SA, Murphy CJ. Computed tomographic imaging characteristics of the normal canine lacrimal glands. BMC Vet Res. 2014; 10(116): 1–6. doi: 10.1186/1746-6148-10-116 24886364

38. Pinard CL, Weiss ML, Brightman AH, Fenwick BW, Davidson HJ. Normal anatomical and histochemical characteristics of the lacrimal glands in the American bison and cattle. Anat Histol Embryol. 2003; 32: 257–262. 12969024

39. Alsafy MAM. Comparative morphological studies on the lacrimal apparatus of one humped camel, goat, and donkey. J Appl Biol Sci. 2010; 4(1): 49–53. doi: 10.3923/jbs.2010.224.230

40. Cabral VP, Laus JL, Dagli MLZ, Pereira GT, Talieri LC, Monteiro ER, et al. Canine lacrimal and third eyelid superficial glands’ macroscopic and morphometric characteristics. Ciênc Rural. 2005; 35(2): 391–397.

41. El-Naseery NI, El-Behery EI, El-Ghazali HM, El-Hady E. The structural characterization of the lacrimal gland in the adult dog (Canis familiaris). Benha Vet Med J. 2016; 31(2): 106–116. doi: 10.1590/S0103-84782005000200023

42. Martinez PA, Marti DA, Molina WF, Bidau CJ. Bergmann’s rule across the equator: a case study in Cerdocyon thous (Canidae). J Anim Ecol. 2013; 82: 997–1008. doi: 10.1111/1365-2656.12076 23550718

43. Schmitt E, Wallace S. Shape change and variation in the cranial morphology of wild canids (Canis lupus, Canis latrans, Canis rufus) compared to domestic dogs (Canis familiaris) using geometric morphometrics. Int J Osteoarchaeol. 2014; 24: 42–50. doi: 10.1002/oa.1306

44. Salguero R, Johnson V, Williams D, Hartley C, Holmes M, Dennis R, et al. CT dimentions, volume and densities of normal canine eyes. Vet Rec. 2015; 176 (15): 386. doi: 10.1136/vr.102940 25690914

45. Samuelson DA. Ophthalmic Anatomy. In: Gelatt KN, Gilger BC, Kern TJ, editors. Veterinary Ophthalmology. 5th ed. Iowa: John Wiley & Sons; 2013. Chapter 2, pp. 39–170.

46. Brischoux F, Pizzatto L, Shine R. Insights into the adaptive significance of vertical pupil shape in snakes. J Evol Biol. 2010; 23: 1878–1885. doi: 10.1111/j.1420-9101.2010.02046.x 20629855

47. Banks MS, Sprague WW, Schmoll J, Parnell JAQ, Love GD. Why do animal eyes have pupils of different shapes? LifeScience. 2015; 1: 1–9. doi: 10.1126/sciadv.1500391 26601232

48. Malmström T, Kröger RHH. Pupil shapes and lens optics in the eyes of terrestrial vertebrates. J Exp Biol. 2006; 209: 18–25. doi: 10.1242/jeb.01959 16354774

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden