Light perception in two strictly subterranean rodents: life in the dark or blue?

. 2010 Jul 28 ; 5 (7) : e11810. [epub] 20100728

Jazyk angličtina Země Spojené státy americké Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid20676369

BACKGROUND: The African mole-rats (Bathyergidae, Rodentia) are strictly subterranean, congenitally microphthalmic rodents that are hardly ever exposed to environmental light. Because of the lack of an overt behavioural reaction to light, they have long been considered to be blind. However, recent anatomical studies have suggested retention of basic visual capabilities. In this study, we employed behavioural tests to find out if two mole-rat species are able to discriminate between light and dark, if they are able to discriminate colours and, finally, if the presence of light in burrows provokes plugging behaviour, which is assumed to have a primarily anti-predatory function. METHODOLOGY/PRINCIPAL FINDING: We used a binary choice test to show that the silvery mole-rat Heliophobius argenteocinereus and the giant mole-rat Fukomys mechowii exhibit a clear photoavoidance response to full-spectrum ("white"), blue and green-yellow light, but no significant reaction to ultraviolet or red light during nest building. The mole-rats thus retain dark/light discrimination capabilities and a capacity to perceive short to medium-wavelength light in the photopic range of intensities. These findings further suggest that the mole-rat S opsin has its absorption maximum in the violet/blue part of the spectrum. The assay did not yield conclusive evidence regarding colour discrimination. To test the putative role of vision in bathyergid anti-predatory behaviour, we examined the reaction of mole-rats to the incidence of light in an artificial burrow system. The presence of light in the burrow effectively induced plugging of the illuminated tunnel. CONCLUSION/SIGNIFICANCE: Our findings suggest that the photopic vision is conserved and that low acuity residual vision plays an important role in predator avoidance and tunnel maintenance in the African mole-rats.

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Dusenbery DB. New York: W.H. Freeman & Co; 1992. Sensory ecology: how organisms acquire and respond to information.558

Land MF, Nilsson D-E. Oxford: Oxford University Press; 2002. Animal Eyes.244

Nevo E. Oxford: Oxford University Press; 1999. Mosaic evolution of subterranean mammals: Regression, progression and global convergence.413

Lacey EA, Patton JL, Cameron GN. Chicago: University of Chicago Press; 2000. Life underground: the biology of subterranean rodents.457

Begall S, Burda H, Schleich CE. Heidelberg: Springer; 2007. Subterranean rodents: News from underground.398

Cooper HM, Herbin M, Nevo E. Visual system of a naturally microphthalmic mammal - the blind mole rat, Spalax ehrenbergi. J Comp Neurol. 1993;328:313–350. PubMed

Němec P, Cveková P, Burda H, Benada O, Peichl L. Visual systems and the role of vision in subterranean rodents: Diversity of retinal properties and visual system designs. In: Begall S, Burda H, Schleich CE, editors. Subterranean rodents: News from underground. Heidelberg: Springer; 2007. pp. 129–160.

Němec P, Cveková P, Benada O, Wielkopolska E, Olkowicz S, et al. The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): retina, subcortical visual nuclei and primary visual cortex. Brain Res Bull. 2008;75:356–364. PubMed

Bennett NC, Faulkes CG. Cambridge: Cambridge University Press; 2000. African mole-rats: ecology and eusociality.287

Cernuda-Cernuda R, Garcia-Fernandez JM, Gordijn MCM, Bovee-Geurts PHM, DeGrip WJ. The eye of the African mole-rat Cryptomys anselli: to see or not to see? Eur Neurosci. 2003;17:709–720. PubMed

Peichl L, Němec P, Burda H. Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae). Eur J Neurosci. 2004;19:1545–1558. PubMed

Hetling JR, Baig-Silva MS, Comer CM, Pardue MT, Samaan DY, et al. Features of visual function in the naked mole-rat Heterocephalus glaber. J Comp Physiol A. 2005;191:317–330. PubMed

Nikitina NV, Maughan-Brown B, O'Riain MJ, Kidson SH. Postnatal development of the eye in the naked mole rat (Heterocephalus glaber). Anat Rec A Discov Mol Cell Evol Biol. 2004;277A:317–337. PubMed

Mills SL, Catania KC. Identification of retinal neurons in a regressive rodent eye (the naked mole-rat). Visual Neurosci. 2004;21:107–117. PubMed PMC

Zhao HB, Ru BH, Teeling EC, Faulkes CG, Zhang SY, et al. Rhodopsin molecular evolution in mammals inhabiting low light environments. PLoS One. 2009;4(12):e8326. doi: 10.1371/journal.pone.0008326. PubMed DOI PMC

Solovei I, Kreysing M, Lanctot C, Kosem S, Peichl L, et al. Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell. 2009;137:356–368. PubMed

Negroni J, Bennett NC, Cooper HA. Organization of the circadian system in the subterranean mole-rat, Cryptomys hottentotus (Bathyergidae). Brain Res. 2003;967:48–62. PubMed

Němec P, Burda H, Peichl L. Subcortical visual system of the African mole-rat Cryptomys anselli: to see or not to see? Eur J Neurosci. 2004;20:757–768. PubMed

Crish SD, Dengler-Crish CM, Catania KC. Central visual system of the naked mole-rat (Heterocephalus glaber). Anat Rec A Discov Mol Cell Evol Biol. 2006;288A:205–212. PubMed

Eloff G. Functional and structural degeneration of the eye of the south African rodent mole, Cryptomys bigalkei and Bathyergus maritimus. S Afr J Sci. 1958;54:292–302.

Burda H, Bruns V, Muller M. Nevo E, Reig O, editors. Sensory adaptations in subterranean mammals. Evolution of subterranean mammals at the organismal and molecular levels. 1990. pp. 269–293. PubMed

Wegner RE, Begall S, Burda H. Light perception in ‘blind’ subterranean Zambian mole-rats. Anim Behav. 2006;72:1021–1024.

Rado R, Bronchti G, Wollberg Z, Terkel J. Sensitivity to light of the blind mole rat - behavioral and neuroanatomical study. Isr J Zool. 1992;38:323–331.

Lund RD, Lund JS. Visual system of mole Talpa europaea. Exp Neurol. 1965;13:302–316. PubMed

Lund RD, Lund JS. Central visual pathways and their functional significance in mole (Talpa europaea). J Zool. 1966;149:95–101.

Johannesson-Gross K. Brightness discrimination of the mole (Talpa Europaea L) in learning experiments applying a modified tube-maze method. Mamm Biol. 1988;53:193–201.

Carmona FD, Glosmann M, Ou J, Jimenez R, Collinson JM. Retinal development and function in a ‘blind’ mole. Proc R Soc B. 2010;277(1687):1513–1522. PubMed PMC

Sanyal S, Jansen HG, Degrip WJ, Nevo E, Dejong WW. The eye of the blind mole-rat, Spalax ehrenbergi - rudiment with hidden function. Invest Ophth Vis Sci. 1990;31:1398–1404. PubMed

Cernuda-Cernuda R, DeGrip WJ, Cooper HM, Nevo E, Garcia-Fernandez JM. The retina of Spalax ehrenbergi: Novel histologic features supportive of a modified photosensory role. Invest Ophth Vis Sci. 2002;43:2374–2383. PubMed

Carmona FD, Jimenez R, Collinson JM. The molecular basis of defective lens development in the Iberian mole. BMC Biol. 2008;6:44. PubMed PMC

Hood DC, Finkelstein MA. Sensitivity to light. In: Boff KR, Kaufman L, Thomas JP, editors. Handbook of perception and human performance 1. New York: Wiley; 1986.

Lyubarsky AL, Daniele LL, Pugh EN. From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG. Vision Res. 2004;44:3235–3251. PubMed

Pennesi ME, Lyubarsky AL, Pugh EN. Extreme responsiveness of the pupil of the dark-adapted mouse to steady retinal illumination. Invest Ophth Vis Sci. 1998;39:2148–2156. PubMed

Deans MR, Volgyi B, Goodenough DA, Bloomfield SA, Paul DL. Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron. 2002;36:703–712. PubMed PMC

Nakatani K, Tamura T, Yau KW. Light adaptation in retinal rods of the rabbit and 2 other nonprimate mammals. J Gen Physiol. 1991;97:413–435. PubMed PMC

Soucy E, Wang YS, Nirenberg S, Nathans J, Meister M. A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron. 1998;21:481–493. PubMed

Jeon CJ, Strettoi E, Masland RH. The major cell populations of the mouse retina. J Neurosci. 1998;18:8936–8946. PubMed PMC

Jacobs GH. The distribution and nature of color vision among the mammals. Biol Rev Camb Philos Soc. 1993;68:413–471. PubMed

Jacobs GH. Evolution of colour vision in mammals. Phil Trans R Soc B. 2009;364:2957–2967. PubMed PMC

Peichl L. Diversity of mammalian photoreceptor properties: Adaptations to habitat and lifestyle? Anat Rec A Discov Mol Cell Evol Biol. 2005;287A:1001–1012. PubMed

Hunt DM, Carvalho LS, Cowing JA, Parry JWL, Wilkie SE, et al. Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochem Photobiol. 2007;83:303–310. PubMed

Jacobs GH, Williams GA, Fenwick JA. Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse. Vision Res. 2004;44:1615–1622. PubMed

Applebury ML, Antoch MP, Baxter LC, Chun LLY, Falk JD, et al. The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning. Neuron. 2000;27:513–523. PubMed

Ahnelt PK, Kolb H. The mammalian photoreceptor mosaic-adaptive design. Prog Retin Eye Res. 2000;19:711–777. PubMed

Lovegrove BG, Papenfus ME. Circadian activity rhythms in the solitary cape mole-rat (Georychus capensis, Bathyergidae) with some evidence of splitting. Physiol Behav. 1995;58:679–685. PubMed

Riccio AP, Goldman BD. Circadian rhythms of locomotor activity in naked mole-rats (Heterocephalus glaber). Physiol Behav. 2000;71:1–13. PubMed

Oosthuizen MK, Cooper HM, Bennett NC. Circadian rhythms of locomotor activity in solitary and social species of African mole-rats (Family: Bathyergidae). J Biol Rhythm. 2003;18:481–490. PubMed

Hart L, Bennett NC, Malpaux B, Chimimba CT, Oosthuizen MK. The chronobiology of the natal mole-rat, Cryptomys hottentotus natalensis. Physiol Behav. 2004;82:563–569. PubMed

Vasicek CA, Oosthuizen MK, Cooper HM, Bennett NC. Circadian rhythms of locomotor activity in the subterranean Mashona mole rat, Cryptomys darlingi. Physiol Behav. 2005;84:181–191. PubMed

Schottner K, Oosthuizen MK, Broekman M, Bennett NC. Circadian rhythms of locomotor activity in the Lesotho mole-rat, Cryptomys hottentotus subspecies from Sani Pass, South Africa. Physiol Behav. 2006;89:205–212. PubMed

de Vries JL, Oosthuizen MK, Sichilima AM, Bennett NC. Circadian rhythms of locomotor activity in Ansell's mole-rat: are mole-rat's clocks ticking? J Zool. 2008;276:343–349.

Šumbera R, Burda H, Chitaukali WN, Kubová J. Silvery mole-rats (Heliophobius argenteocinereus, Bathyergidae) change their burrow architecture seasonally. Naturwissenschaften. 2003;90:370–373. PubMed

Šklíba J, Šumbera R, Chitaukali WN, Burda H. Home-range dynamics in a solitary subterranean rodent. Ethology. 2009;115:217–226.

Šklíba J, Šumbera R, Chitaukali WN, Burda H. Determinants of daily activity patterns in a free-living afrotropical solitary subterranean rodent. J Mammal. 2007;88:1009–1016.

Öelschlager HHA, Nakamura M, Herzog M, Burda H. Visual system labeled by c-Fos immunohistochemistry after light exposure in the ‘blind’ subterranean Zambian mole-rat (Cryptomys anselli). Brain Behav Evolut. 2000;55:209–220. PubMed

Oosthuizen MK, Bennett NC, Cooper HM. Fos expression in the suprachiasmatic nucleus in response to light stimulation in a solitary and social species of African mole-rat (family Bathyergidae). Neuroscience. 2005;133:555–560. PubMed

Patzenhauerová H, Bryja J, Šumbera R. Kinship structure and mating system in a solitary subterranean rodent, the silvery mole-rat. Behav Ecol Sociobiol. 2010;64:757–767.

McFarland WN, Munz FW. The visible spectrum during twilight and its implications to vision. In: Evans GC, Bainbridge R, Rackham O, editors. Light as an ecological factor II. Oxford: Blackwell Scientific Publications; 1975. pp. 249–270.

David-Gray ZK, Bellingham J, Munoz M, Avivi A, Nevo E, et al. Adaptive loss of ultraviolet-sensitive/violet-sensitive (UVS/VS) cone opsin in the blind mole rat (Spalax ehrenbergi). Eur J Neurosci. 2002;16:1186–1194. PubMed

Peichl L, Chavez AE, Ocampo A, Mena W, Bozinovic F, et al. Eye and vision in the subterranean rodent cururo (Spalacopus cyanus, Octodontidae). J Comp Neurol. 2005;486:197–208. PubMed

Williams GA, Calderone JB, Jacobs GH. Photoreceptors and photopigments in a subterranean rodent, the pocket gopher (Thomomys bottae). J Comp Physiol A. 2005;191:125–134. PubMed

Glosmann M, Steiner M, Peichl L, Ahnelt PK. Cone photoreceptors and potential UV vision in a subterranean insectivore, the European mole. J Vision. 2008;8(4):23, 1–12. PubMed

Lukáts A, Szabo A, Rohlich P, Vigh B, Szel A. Photopigment coexpression in mammals: comparative and developmental aspects. Histol Histopathol. 2005;20:551–574. PubMed

Šklíba J, Šumbera R, Chitaukali WN. Reactions to disturbances in the context of antipredatory behaviour in a solitary subterranean rodent. J Ethol. 2008;26:249–254.

Werner SJ, Nolte DL, Provenza FD. Proximal cues of pocket gopher burrow plugging behavior: Influence of light, burrow openings, and temperature. Physiol Behav. 2005;85:340–345. PubMed

Kawalika M, Burda H. Giant mole-rats, Fukomys mechowii, 13 years on the stage. In: Begall S, Burda H, Schleich CE, editors. Subterranean Rodents: News from Underground. Heidelberg: Springer; 2007. pp. 205–219.

Šumbera R, Chitaukali WN, Burda H. Biology of the silvery mole-rat (Heliophobius argenteocinereus). Why study a neglected subterranean rodent species? In: Begall S, Burda H, Schleich CE, editors. Subterranean Rodents: News from Underground. Heidelberg: Springer; 2007. pp. 221–236.

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