Do Male and Female Cowbirds See Their World Differently? Implications for Sex Differences in the Sensory System of an Avian Brood Parasite

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Fernández Juricic, Esteban ^a   Ojeda, Agustin ^b   Deisher, Marcella ^a   Burry, Brianna ^a   Baumhardt, Patrice ^a   Stark, Amy ^a   Elmore, Amanda G ^a   Ensminger, Amanda L ^a  

^a PURDUE UNIVERSITY   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; BIRD; BODY MASS; BROOD PARASITE; CONTROLLED STUDY; EYE DIMENSION; FEMALE; GATHERING BEHAVIOR; GAZE; HEAD MOVEMENT; INFORMATION PROCESSING; MALE; MOLOTHRUS ATER; NONHUMAN; ORGAN SIZE; PHOTORECEPTOR; SEX DIFFERENCE; VISION; VISUAL INFORMATION;

ANIMALS; BODY WEIGHT; EYE; FEMALE; HEAD MOVEMENTS; LINEAR MODELS; MALE; NESTING BEHAVIOR; ORGAN SIZE; PARASITES; PASSERIFORMES; PHOTORECEPTOR CELLS, VERTEBRATE; SEX CHARACTERISTICS;

AVES; MOLOTHRUS; MOLOTHRUS ATER;

EID: 84875452152     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058985     Document Type: Article

References (74)

1. Bradbury JW, Vehrencamp SL (2011) Principles of animal communication. 2nd Edition. Sunderland MA: Sinauer Associates.
2. Wilczynski W, Ryan MJ, (2010) The behavioral neuroscience of anuran social signal processing. Current Opinion in Neurobiology 20: 754-763.
3. Knudsen DP, Gentner TQ, (2010) Mechanisms of song perception in oscine birds. Brain & Language 115: 59-68.
4. Dangles O, Irschick DJ, Chittka L, Casas J, (2009) Variability in sensory ecology: Expanding the bridge between physiology and evolutionary biology. Quarterly Review of Biology 84: 51-74.
5. Nava SS, Conway MA, Martins EP, (2009) Sex-specific visual performance: females lizards outperform males in motion detection. Biology Letters 5: 732-734.
6. Cummings ME, Bernal XE, Reynaga R, Rand AS, Ryan MJ, (2008) Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females. Journal of Experimental Biology 211: 1203-1210.
7. Doty RL, Cameron EL, (2009) Sex differences and reproductive hormone influences on human odor perception. Physiology & Behavior 97: 213-228.
8. Muchlinski MN, Docherty BA, Alport LJ, Burrows AM, Smith TD, et al. (2011) Behavioral and ecological consequences of sex-based differences in gustatory anatomy in Cebus paella. Anatomical Record, 294, 2179-2192.
9. Nava SS, Moreno L, Wang D, (2012) Receiver sex differences in visual response to dynamic motion signals in Sceloporus lizards. Behavioral Ecology and Sociobiology 66: 1357-1362.
10. Martins EP, Ord TJ, Davenport SW, (2005) Combining motions into complex displays: playbacks with a robotic lizard. Behavioral Ecology and Sociobiology 58: 351-360.
11. Hebets EA, Papaj DR, (2005) Complex signal function: developing a framework of testable hypotheses. Behavioral Ecology and Sociobiology 57: 197-214.
12. Tomasi D, Chang L, Caparelli EC, Ernst T, (2008) Sex differences in sensory gating of the thalamus during auditory interference of visual attention tasks. Neuroscience 151: 1006-1015.
13. Lowther PE (1993) Brown-headed Cowbird (Molothrus ater). The Birds of North America Online (ed A. Poole) Cornell Lab of Ornithology. Available: http://bna.birds.cornell.edu/bna/species/047. Accessed March 2012.
14. Gall MD, Lucas JR, (2010) Sex differences in auditory filters of brown-headed cowbirds (Molothrus ater). Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology. 196: 559-567.
15. Fernández-Juricic E, Beauchamp G, Treminio R, Hoover M, (2011a) Making heads turn: association between head movements during vigilance and perceived predation risk in brown-headed cowbird flocks. Animal Behaviour. 82: 573-577.
16. Hart NS, (2001a) The visual ecology of avian photoreceptors. Progression in Retinal and Eye Research. 20: 675-703.
17. Martin GR, Osorio D, (2008) Vision in birds. The senses: a comprehensive reference (eds AI Basbaum, A Kaneko, GM Shepherd, G Westheimer). San Diego: Academic Press. 1: 25-52.
18. von Campenhausen M, Kirschfeld K, (1998) Spectral sensitivity of the accessory optic system of the pigeon. Journal of Comparative Physiology A. 183: 1-6.
19. Osorio D, Miklosi A, Gonda Z, (1999a) Visual ecology and perception of coloration patterns by domestic chicks. Evolutionary Ecology. 13: 673-689.
20. Osorio D, Vorobyev M, Jones CD, (1999b) Colour vision in chicks. Journal of Experimental Biology. 202: 2951-2959.
21. Goldsmith TH, Butler BK, (2005) Color vision of the budgerigar (Melopsittacus undulatus): hue matches, tetrachromacy, and intensity discrimination. Journal of Comparative Physiology A. 191: 933-951.
22. Dolan T, Fernández-Juricic E, (2010) Retinal ganglion cell topography of five species of ground foraging birds. Brain, Behavior and Evolution. 75: 111-121.
23. Blackwell BF, Fernández-Juricic E, Seamans TW, Dolan T, (2009) Avian visual system configuration and behavioural response to object approach. Animal Behaviour. 77: 673-684.
24. Rossi EA, Roorda A, (2010) The relationship between visual resolution and cone spacing in the human fovea. Nature Neuroscience. 13: 156-157.
25. Aloimonos JY, Weiss I, Bandopadhay A, (1987) Active vision. International Journal of Computer Vision. 1: 333-356.
26. Maldonado PE, Maturana H, Varela FJ, (1988) Frontal and lateral visual system in birds. Brain, Behavior, and Evolution. 32: 57-62.
27. Shay O, van der Willigen RF, Wagner H, Katsman I, Rivlin E, (2006) On the barn owl's visual pre-attack behavior: I. Structure of head movements and motion patterns. Journal of Comparative Physiology. 192: 927-940.
28. Dawkins MS, Woodington A, (2000) Pattern recognition and active vision in chickens. Nature. 403: 652-655.
29. Dawkins MS, (2002) What are birds looking at? Head movements and eye use in chickens. Animal Behaviour. 63: 991-998.
30. Fernández-Juricic E, (2012) Sensory basis of vigilance behavior in birds: synthesis and future prospects. Behavioural Processes. 89: 143-152.
31. Rauschecker JP, Kniepert U, (1995) Auditory localization behavior in visually deprived cats. European Journal of Neuroscience. 6: 149-160.
32. Lessard N, Pare M, Lepore F, Lassonde W, (1998) Early blind human subjects localize sound sources better than sighted subjects. Nature. 395: 278-280.
33. Niven JE, Laughlin SB, (2008) Energy limitation as a selective pressure on the evolution of sensory systems. Journal of Experimental Biology. 211: 1792-1804.
34. Uchiyama M, Demura S, (2008) Low visual acuity is associated with the decrease in postural sway. Tohoku Journal of Experimental Medicine. 216: 277-285.
35. Hart NS, Lisney TJ, Collin SP, (2006) Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity. Journal of Experimental Biology. 209: 4776-4787.
36. Ullmann JFP, Moore BA, Temple SE, Fernández-Juricic E, Collin SP, (2012) The retinal wholemount technique: a window to understanding the brain and behaviour. Brain, Behavior and Evolution. 79: 26-44.
37. Meyer DBC, (1977) The avian eye and its adaptations. The visual system of vertebrates; handbook of sensory physiology (ed F Crescitelli). New York: Springer VII/5: 549-612.
38. Vorobyev M, (2003) Coloured oil droplets enhance colour discrimination. Proceedings of the Royal Society B. 270: 1255-1261.
39. Hart NS, Hunt DM, (2007) Avian visual pigments: characteristics, spectral tuning, and evolution. American Naturalist. 169: S7-S26.
40. Müller B, Peichl L, (1989) Topography of cones and rods in the tree shrew retina. Journal of Comparative Neurology. 282: 581-594.
41. Hart NS, (2001b) Variations in cone photoreceptor abundance and the visual ecology of birds. Journal of Comparative Physiology A. 187: 685-698.
42. Evans JE, Cuthill IC, Bennett ADT, (2006) The effect of flicker from fluorescent lights on mate choice in captive birds. Animal Behaviour. 72: 393-400.
43. Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sunderland, MA: Sinauer Associates Inc.
44. Montgomerie R (2006). Analyzing colors. Bird coloration: mechanisms and measurements (eds GE Hill & KJ McGraw). Cambridge: Harvard University Press.
45. Hart NS, Partridge JC, Cuthill IC, (2000) Retinal asymmetry in birds. Current Biology. 10: 115-117.
46. Sherry DF, Forbes MRL, Khurgel M, Ivy GO, (1993) Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird. Proceedings of the National Academy of Sciences. 90: 7839-7843.
47. Day LB, Guerra M, Schlinger BA, Rothstein SI, (2008) Sex differences in the effects of captivity on hippocampus size in brown-headed cowbirds (Molothrus ater obscurus). Behavioral Neuroscience. 122: 527-534.
48. Reboreda JC, Clayton NS, Kacelnik A, (1996) Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport. 7: 505-508.
49. Hauber ME, Clayton NS, Kacelnik A, Reboreda JC, DeVoogd TJ, (1999) Sexual dimorphism and species differences in HVC volumes of cowbirds. Behavioral Neuroscience. 113: 1095-1099.
50. McIlwain JT (1996) An introduction to the biology of vision. New York: Cambridge University Press.
51. Dowling JE (2012) The retina: an approachable part of the brain. Cambridge, Massachusetts: The Belknap Press of Harvard University Press.
52. 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, Behavior, and Evolution. 32: 39-56.
53. Williams DR, Coletta NJ, (1987) Cone spacing and the visual resolution limit. Journal of the Optical Society of America A. 4: 1514-1523.
54. Jägle H, Heine J, Kurtenbach A, (2006) L:M-cone ratio estimates of the outer and inner retina and its impact on sex differences in ERG amplitudes. Doc. Ophthalmol. 113: 105-113.
55. Gunther KL, Dobkins KR, (2002) Individual differences in chromatic (red/green) contrast sensitivity are constrained by the relative number of L- versus M-cones in the eye. Vision Research. 42: 1367-1378.
56. Sabbah S, Lamela Laria R, Gray SM, Hawryshyn CW, (2010) Functional diversity in the color vision of cichlid fishes. BMC Biology. 8: 133.
57. Land MF, (1999) Motion and vision: why birds move their eyes. Journal of Comparative Physiology A. 185: 341-352.
58. Land MF, Tatler BW (2009) Looking and acting: vision and eye movements in natural behavior. Oxford: Oxford University Press.
59. Jaeger RG, Wise SE, (1991) A reexamination of the male salamander 'sexy faeces hypothesis'. Journal of Herpetology. 25: 370-373.
60. Dawley EM, (1992) Sexual dimorphism in a chemosensory system: the role of the vomeronasal organ in salamander reproductive behavior. Copeia. 1992: 113-120.
61. Kram YA, Mantey S, Corbo JC, (2010) Avian Cone Photoreceptors Tile the Retina as Five Independent, Self-Organizing Mosaics. PLoS ONE. 5: e8992.
62. Lisney TJ, Ekesten B, Tauson R, Hastad O, Odeen A, (2012) Using electroretinograms to assess flicker fusion frequency in domestic hens Gallus gallus domesticus. Vision Research. 62: 125-133.
63. Fernández-Juricic E, Gall MD, Dolan T, O'Rourke C, Thomas S, et al. (2011b) Visual systems and vigilance behaviour of two ground-foraging avian prey species: white-crowned sparrows and California towhees. Animal Behaviour. 81: 705-713.
64. Clotfelter ED, (1998) What cues do brown-headed cowbirds use to locate red-winged blackbird host nests? Animal Behaviour. 55: 1181-1189.
65. Cooper BG, Goller F, (2004) Multimodal signals: enhancement and constraint of song motor patterns by visual display. Science. 303: 544-546.
66. O'Loghlen AL, Rothstein SI, (2003) Female preference for the songs of older males and the maintenance of dialects in brown-headed cowbirds (Molothrus ater). Behavioral Ecology and Sociobiology. 53: 102-109.
67. O'Loghlen AL, Rothstein SI, (2010a) Male visual displays enhance female sexual responsiveness to song in brown-headed cowbirds (Molothrus ater). Condor. 112: 615-621.
68. O'Loghlen AL, Rothstein SI, (2012) When less is best: female brown-headed cowbirds prefer less intense male displays. PLoS ONE. 7: e36130.
69. Rothstein SI, Yokel DA, Fleischer RC, (1988) The agonistic and sexual functions of vocalizations of male brown-headed cowbirds, Molothrus ater. Animal Behaviour. 36: 73-86.
70. Gloag R, Fiorini VD, Reboreda JC, Kacelnik A, (2012) Brood parasite eggs enhance egg survivorship in a multiply parasitized host. Proceedings of the Royal Society of London B. 279: 1831-1839.
71. O'Loghlen AL, Rothstein SI, (2010b) Multimodal signaling in a songbird: male audiovisual displays vary significantly by social context in brown-headed cowbirds. Animal Behaviour. 79: 1285-1292.
72. Rothstein SI, Yokel DA, Fleischer RC, (1986) Social dominance, mating and spacing systems, female fecundity, and vocal dialects in captive and free ranging brown-headed cowbirds. Current Ornithology. 34: 127-185.
73. West MJ, King AP, (1988) Female visual displays affect the development of male song in the cowbird. Nature. 334: 244-246.
74. Martin GR, Wilson KJ, Wild JM, Parsons S, Kubke MF, et al. (2007) Kiwi forego vision in the guidance of their nocturnal activities. PLoS ONE. 2(2): e198 doi:10.1371/journal.pone.0000198.