The family Herpestidae (cusimanses and mongooses) is a monophyletic radiation of carnivores with remarkable variation in microhabitat occupation and diel activity, but virtually nothing is known about how they use vision in the context of their behavioral ecology. In this paper, we measured the number and topographic distribution of neurons (rods, cones and retinal ganglion cells) and estimated the spatial resolving power of the eye of the diurnal, forest-dwelling Ansorge's cusimanse (Crossarchus ansorgei). Using retinal wholemounts and stereology, we found that rods are more numerous (42,500,000; 92%) than cones (3,900,000; 8%). Rod densities form a concentric and dorsotemporally asymmetric plateau that matches the location and shape of a bright yellow tapetum lucidum located within the dorsal aspect of the eye. Maximum rod density (340,300 cells/mm2) occurs within an elongated plateau below the optic disc that corresponds to a transitional region between the tapetum lucidum and the pigmented choroid. Cone densities form a temporal area with a peak density of 44,500 cells/mm2 embedded in a weak horizontal streak that matches the topographic distribution of retinal ganglion cells. Convergence ratios of cones to retinal ganglion cells vary from 50:1 in the far periphery to 3:1 in the temporal area. With a ganglion cell peak density of 13,400 cells/mm2 and an eye size of 11 mm in axial length, we estimated upper limits of spatial resolution of 7.5-8 cycles/degree, which is comparable to other carnivores such as hyenas. In conclusion, we suggest that the topographic retinal traits described for Ansorge's cusimanse conform to a presumed carnivore retinal blueprint but also show variations that reflect its specific ecological needs.

1.
Ahnelt PK, Kolb H (2000): The mammalian photoreceptor mosaic-adaptive design. Prog Retin Eye Res 19:711-777.
2.
Blake R, Cool SJ, Crawford M (1974): Visual resolution in the cat. Vision Res 14:1211-1217.
3.
Bruhn SL, Cepko CL (1996): Development of the pattern of photoreceptors in the chick retina. J Neuroci 16:1430-1439.
4.
Calderone JB, Reese BE, Jacobs GH (2003): Topography of photoreceptors and retinal ganglion cells in the spotted hyena (Crocuta crocuta). Brain Behav Evol 62:182-192.
5.
Coimbra JP, Collin SP, Hart NS (2014a): Topographic specializations in the retinal ganglion cell layer correlate with lateralized visual behavior, ecology, and evolution in cockatoos. J Comp Neurol 522:3363-3385.
6.
Coimbra JP, Collin SP, Hart NS (2014b): Topographic specializations in the retinal ganglion cell layer of Australian passerines. J Comp Neurol 522:3609-3628.
7.
Coimbra JP, Collin SP, Hart NS (2015): Variations in retinal photoreceptor topography and the organization of the rod-free zone reflect behavioral diversity in Australian passerines. J Comp Neurol 523:1073-1094.
8.
Coimbra JP, Hart NS, Collin SP, Manger PR (2013): Scene from above: retinal ganglion cell topography and spatial resolving power in the giraffe (Giraffa camelopardalis). J Comp Neurol 521:2042-2057.
9.
Coimbra JP, Marceliano MLV, Andrade-da-Costa BLS, Yamada ES (2006): The retina of tyrant flycatchers: topographic organization of neuronal density and size in the ganglion cell layer of the great kiskadee Pitangus sulphuratus and the rusty margined flycatcher Myiozetetes cayanensis (Aves: Tyrannidae). Brain Behav Evol 68:15-25.
10.
Coimbra JP, Trévia N, Marceliano MLV, Andrade-da-Costa BLS, Picanço-Diniz CW, Yamada ES (2009): Number and distribution of neurons in the retinal ganglion cell layer in relation to foraging behaviors of tyrant flycatchers. J Comp Neurol 514:66-73.
11.
Collin SP (1999): Behavioural ecology and retinal cell topography; in Archer SN, Djamogoz MBS, Loew ER, Partridge JC, Vellarga S (eds): Adaptive Mechanisms in the Ecology of Vision. London, Chapman and Hall, pp 509-535.
12.
Curcio CA, Packer O, Kalina RE (1987): A whole mount method for sequential analysis of photoreceptor and ganglion cell topography in a single retina. Vision Res 27:9-15.
13.
de Busserolles F, Fitzpatrick JL, Marshall NJ, Collin SP (2014a): The influence of photoreceptor size and distribution on optical sensitivity in the eyes of lanternfishes (Myctophidae). PloS One 9:e99957.
14.
de Busserolles F, Marshall NJ, Collin SP (2014b): Retinal ganglion cell distribution and spatial resolving power in deep-sea lanternfishes (Myctophidae). Brain Behav Evol 84:262-276.
15.
Gilchrist J, Jennings A, Veron G, Cavallini P (2009): Family Herpestidae (mongooses); in Wilson D, Mittermeier R (eds): Handbook of Mammals of the World. Barcelona, Lynx Edicions, vol 1, pp 210-235.
16.
Glaser EM, Wilson PD (1998): The coefficient of error of optical fractionator population size estimates: a computer simulation comparing three estimators. J Microsc 192:163-171.
17.
Gompper ME, Decker DM (1998): Nasua nasua. Mamm Species 580:1-9.
18.
Gundersen HJG (1977): Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J Microsc 11:219-223.
19.
Hall SE, Mitchell DE (1991): Grating acuity of cats measured with detection and discrimination tasks. Behav Brain Res 44:1-9.
20.
Hanke FD, Peichl L, Dehnhardt G (2009): Retinal ganglion cell topography in juvenile harbor seals (Phoca vitulina). Brain Behav Evol 74:102-109.
21.
Henderson Z (1985): Distribution of ganglion cells in the retina of adult pigmented ferret. Brain Res 358:221-228.
22.
Hendrickson AE (2009): Fovea: primate; in Squire L (ed): Encyclopedia of Neuroscience. Oxford, Academic Press, p 327-334.
23.
Hughes A (1975): A quantitative analysis of the cat retinal ganglion cell topography. J Comp Neurol 163:107-128.
24.
Hughes A (1977): The topography of vision in mammals of contrasting life style: comparative optics and retinal organization; in Crescitelli F (ed): Handbook of Sensory Physiology: The Visual System of Vertebrates. Berlin, Springer, vol 7/5, pp 613-756.
25.
Hughes A (1981a): Population magnitudes and distribution of the major modal classes of cat retinal ganglion cell as estimated from HRP filling and a systematic survey of the soma diameter spectra for classical neurones. J Comp Neurol 197:303-339.
26.
Hughes A (1981b): Cat retina and the sampling theorem; the relation of transient and sustained brisk-unit cut-off frequency to α and β-mode cell density. Exp Brain Res 42:196-202.
27.
Isayama T, O'Brien BJ, Ugalde I, Muller JF, Frenz A, Aurora V, Tsiaras W, Berson DM (2009): Morphology of retinal ganglion cells in the ferret (Mustela putorius furo). J Comp Neurol 517:459-480.
28.
Johnson GL (1901): Contributions to the comparative anatomy of the mammalian eye: chiefly based on ophthalmoscopic examination. Philos Trans R Soc Lond B 194:1-82.
29.
Kingdon J (2004): The Kingdon Pocket Guide to African Mammals. London, A&C Black.
30.
Kryger Z, Galli-Resta L, Jacobs G, Reese B (1998): The topography of rod and cone photoreceptors in the retina of the ground squirrel. Vis Neurosci 15:685-691.
31.
Lisney TJ, Iwaniuk AN, Kolominsky J, Bandet MV, Corfield JR, Wylie DR (2012): Interspecifc variation in eye shape and retinal topography in seven species of galliform bird (Aves: Galliformes: Phasianidae). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 198:717-731.
32.
Lisney TJ, Stecyk K, Kolominsky J, Graves GR, Wylie DR, Iwaniuk AN (2013a): Comparison of eye morphology and retinal topography in two species of new world vultures (Aves: Cathartidae). Anat Rec 296:1954-1970.
33.
Lisney TJ, Stecyk K, Kolominsky J, Schmidt BK, Corfield JR, Iwaniuk AN, Wylie DR (2013b): Ecomorphology of eye shape and retinal topography in waterfowl (Aves: Anseriformes: Anatidae) with different foraging modes. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 199:385-402.
34.
Marshall NJ (2000): Communication and camouflage with the same ‘bright' colours in reef fishes. Philos Trans R Soc Lond B Biol Sci 355:1243-1248.
35.
Mass AM, Supin AY (1992): Peak density, size and regional distribution of ganglion cells in the retina of the fur seal Callorhinus ursinus. Brain Behav Evol 39:69-76.
36.
Mass AM, Supin AY (2000): Ganglion cells density and retinal resolution in the sea otter, Enhydra lutris. Brain Behav Evol 55:111-119.
37.
Mass AM, Supin AY (2003): Retinal topography of the harp seal Pagophilus groenlandicus. Brain Behav Evol 62:212-222.
38.
Mass AM, Supin AY (2010): Retinal ganglion cell layer of the Caspian seal Pusa caspica: topography and localization of the high-resolution area. Brain Behav Evol 76:144-153.
39.
Miller PE, Murphy CJ (1995): Vision in dogs. J Am Vet Med Assoc 207:1623-1634.
40.
Müller B, Peichl L (1989): Topography of cones and rods in the tree shrew retina. J Comp Neurol 282:581-594.
41.
Newman AS, Marshall JN, Collin SP (2013): Visual eyes: a quantitative analysis of the photoreceptor layer in deep-sea sharks. Brain Behav Evol 82:237-249.
42.
Nyakatura K, Bininda-Emonds OR (2012): Updating the evolutionary history of Carnivora (Mammalia): a new species-level supertree complete with divergence time estimates. BMC Biol 10:12.
43.
Patou M-L, McLenachan PA, Morley CG, Couloux A, Jennings AP, Veron G (2009): Molecular phylogeny of the Herpestidae (Mammalia, Carnivora) with a special emphasis on the Asian Herpestes. Mol Phylogenet Evol 53:69-80.
44.
Peichl L (1992): Topography of ganglion cells in the dog and wolf retina. J Comp Neurol 324:603-620.
45.
Peichl L (2005): Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec 287:1001-1012.
46.
Peichl L, Němec P, Burda H (2004): Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae). Eur J Neurosci 19:1545-1558.
47.
Peichl L, Pohl B (2000): Cone types and cone/rod ratios in the crab-eating raccoon and coati (Procyonidae). Invest Ophthalmol Vis Sci 41:S494.
48.
Pettigrew JD, Dreher B, Hopkins CS, McCall MJ, Brown M (1988): Peak density and distribution of ganglion cells in the retinae of microchiropteran bats: implications for visual acuity. Brain Behav Evol 32:39-56.
49.
Reuter T, Peichl L (2008): Structure and function of the retina in aquatic tetrapods; in Thewissen JGM, Nummela S (eds): Sensory Evolution on the Threshold - Adaptations in Secondarily Aquatic Vertebrates. Oakland, University of California Press, pp 149-172.
50.
Rodieck RW (1973): The Vertebrate Retina: Principles of Structure and Function. San Francisco, Freeman.
51.
Silveira LC, Perry V, Yamada E (1993): The retinal ganglion cell distribution and the representation of the visual field in area 17 of the owl monkey, Aotus trivirgatus. Vis Neurosci 10:887-897.
52.
Silveira LC, Picanço-Diniz CW, Oswaldo-Cruz E (1989a): Distribution and size of ganglion cells in the retinae of large Amazon rodents. Vis Neurosci 2:221-235.
53.
Silveira LC, Picanço-Diniz C, Sampaio L, Oswaldo-Cruz E (1989b): Retinal ganglion cell distribution in the cebus monkey: a comparison with the cortical magnification factors. Vision Res 29:1471-1483.
54.
Slomianka L, West MJ (2005): Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 136:757-767.
55.
Snyder AW, Miller WH (1977): Photoreceptor diameter and spacing for highest resolving power. J Opt Soc Am 67:696-698.
56.
Steinberg RH, Reid M, Lacy PL (1973): The distribution of rods and cones in the retina of the cat (Felis domesticus). J Comp Neurol 148:229-248.
57.
Stone J (1965): A quantitative analysis of the distribution of ganglion cells in the cat's retina. J Comp Neurol 124:337-352.
58.
Stone J (1981): The Wholemount Handbook: A Guide to the Preparation and Analysis of Retinal Wholemounts. Sydney, Maitland Publications.
59.
Stone J (1983): Parallel Processing in the Visual System. New York, Plenum Press.
60.
Van Rompaey H, Colyn M (1992): Crossarchus ansorgei. Mamm Species 402:1-3.
61.
Wässle H (1971): Optical quality of the cat eye. Vision Res 11:995-1006.
62.
Wässle H (2004): Parallel processing in the mammalian retina. Nat Rev Neurosci 5:747-757.
63.
Wässle H, Boycott BB (1991): Functional architecture of the mammalian retina. Physiol Rev 71:447-480.
64.
Wässle H, Peichl L, Boycott BB (1981): Morphology and topography of on-and off-alpha cells in the cat retina. Proc R Soc Lond B Biol Sci 212:157-175.
65.
West MJ, Slomianka L, Gundersen HJG (1991): Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
66.
Williams DR, Coletta NJ (1987): Cone spacing and the visual resolution limit. J Opt Soc Am A 4:1514-1523.
67.
Wilson DE, Reeder DAM (2005): Mammal Species of the World: A Taxonomic and Geographic Reference, ed 3. Baltimore, The Johns Hopkins University Press, vol 1.
68.
Wong ROL, Wye-Dvorak J, Henry GH (1986): Morphology and distribution of neurons in the retinal ganglion cell layer of the adult tammar wallaby - Macropus eugenii. J Comp Neurol 253:1-12.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.