Fish and robot dancing together: Bluefin killifish females respond differently to the courtship of a robot with varying color morphs

Bioinspiration and Biomimetics

Volumn 9, Issue 3, 2014, Pages

  Phamduy, P ^a   Polverino, G ^a,b   Fuller, R C ^c   Porfiri, M ^a  

^a POLYTECHNIC UNIVERSITY   (United States)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

animal behavior; bioinspired design; courtship; ethorobotics; killifish; robotics

Indexed keywords

ASPECT RATIO; COLOR; FISH; ROBOTICS;

ANIMAL BEHAVIOR; BIO-INSPIRED DESIGNS; COURTSHIP; ETHOROBOTICS; KILLIFISH;

ROBOTS;

ANIMAL; BIOMIMETICS; COLOR; COURTSHIP; DEVICE FAILURE ANALYSIS; DEVICES; EQUIPMENT DESIGN; FEMALE; FUNDULIDAE; MALE; PHYSIOLOGY; PROCEDURES; ROBOTICS; SEXUAL BEHAVIOR;

ANIMALS; BIOMIMETICS; COLOR; COURTSHIP; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; FEMALE; FUNDULIDAE; MALE; ROBOTICS; SEXUAL BEHAVIOR, ANIMAL;

EID: 84907844815     PISSN: 17483182     EISSN: 17483190     Source Type: Journal    
DOI: 10.1088/1748-3182/9/3/036021     Document Type: Article

References (68)

1. Badyaev A V and Hill G E 2003 Avian sexual dichromatism in relation to phylogeny and ecology Annu. Rev. Ecol. Evol. S 34 27-49 (Pubitemid 38171412)
2. Messmer V, Jones G P, van Herwerden L and Munday P L 2005 Genetic and ecological characterisation of colour dimorphism in a coral reef fish Environ. Biol. Fish. 74 175-83 (Pubitemid 41618733)
3. Bell R C and Zamudio K R 2012 Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity Proc. R. Soc. B 279 4687-93
4. Amundsen T 2000 Why are female birds ornamented? Trends Ecol. Evol. 15 149-55 (Pubitemid 30151592)
5. Pilastro A, Benetton S and Bisazza A 2003 Female aggregation and male competition reduce costs of sexual harassment in the mosquitofish Gambusia holbrooki Anim. Behav. 65 1161-7 (Pubitemid 36914329)
6. Roulin A, Dijkstra C, Riols C and Ducrest A L 2001 Female-and male-specific signals of quality in the barn owl J. Evolution. Biol. 14 255-66 (Pubitemid 32333198)
7. Galeotti P, Rubolini D, Dunn P O and Fasola M 2003 Colour polymorphism in birds: causes and functions J. Evolution. Biol. 16 635-46 (Pubitemid 36832262)
8. Gray S M and McKinnon J S 2007 Linking color polymorphism maintenance and speciation Trends Ecol. Evol. 22 71-9 (Pubitemid 46123723)
9. Sinervo B, Miles D B, Frankino W A, Klukowski M and DeNardo D F 2000 Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards Horm. Behav. 38 222-33
10. Van Gossum H, Sherratt T N and Cordero-Rivera A 2008 The Evolution of Sex-limited Colour Polymorphisms. Dragonflies: Model Organisms for Ecological and Evolutionary Research (Oxford, UK: Oxford University Press)
11. Pryke S R, Astheimer L B, Griffith S C and Buttemer W A 2012 Covariation in life-history traits: differential effects of diet on condition, hormones, behavior, and reproduction in genetic finch morphs Amer. Nat. 179 375-90
12. McGhee K E, Fuller R C and Travis J 2007 Male competition and female choice interact to determine mating success in the bluefin killifish Behav. Ecol. 18 822-30 (Pubitemid 47357648)
13. Tibbetts E A and Dale J 2004 A socially enforced signal of quality in a paper wasp Nature 432 218-22 (Pubitemid 39545851)
14. de Heij M E, Gustafsson L and Brommer J E 2011 Experimental manipulation shows that the white wing patch in collared flycatchers is a male sexual ornament Ecol. Evol. 1 546-55
15. Sheldon B C, Andersson S, Griffith S C, Örnborg J and Sendecka J 1999 Ultraviolet colour variation influences blue tit sex ratios Nature 402 874-7 (Pubitemid 30017168)
16. Hoefler C D and Morris M R 1999 A technique for the temporary application and augmentation of pigment patterns in fish Ethology 105 431-8 (Pubitemid 29245294)
17. Houde E D 1997 Patterns and trends in larval-stage growth and mortality of teleost fish J. Fish Biol. 51 52-83 (Pubitemid 28073193)
18. Hancox D, Hoskin C J and Wilson R S 2010 Evening up the score: sexual selection favours both alternatives in the colour-polymorphic ornate rainbowfish Anim. Behav. 80 845-51
19. Beausoleil J M J, Doucet S M, Heath D D and Pitcher T E 2012 Spawning coloration, female choice and sperm competition in the redside dace Clinostomus elongatus Anim. Behav. 83 969-77
20. Tinbergen N 1948 Social releasers and the experimental method required for their study Wilson Bull. 60 6-51
21. Sevenster P 1949 Modderbaarsjes Lev. Nat. 52 184-9
22. Posner G S 1982 Variation in the aggressive behavior of Xiphophorous variatus (Pisces: Poeciliidae) with regard to group dynamics and response towards conspecific models (New York: New York University) 116
23. Rowland W J 1999 Studying visual cues in fish behavior: a review of ethological techniques Environ. Biol. Fish. 56 285-305 (Pubitemid 29523974)
24. Rosenthal G G and Evans C S 1998 Female preference for swords in Xiphophorus helleri reflects a bias for large apparent size Proc. Natl. Acad. Sci. 95 4431-6 (Pubitemid 28207929)
25. Künzler R and Bakker T C M 2001 Female preferences for single and combined traits in computer animated stickleback males Behav. Ecol. 12 681-5 (Pubitemid 34029709)
26. Karino K, Shimada Y, Kudo H and Sato A 2010 Relative importance of the area and intensity of the orange spots of male guppies Poecilia reticulata as mating traits preferred by females J. Fish Biol. 77 299-307
27. Abaid N, Spinello C, Laut J and Porfiri M 2012 Zebrafish (Danio rerio) responds to images animated by mathematical models of animal grouping Behav. Brain Res. 232 406-10
28. Polverino G, Liao J C and Porfiri M 2013 Mosquitofish (Gambusia affinis) preference and behavioral response to animated images of conspecifics altered in their color, aspect ratio, and swimming depth PLoS ONE 8 e54315
29. Saverino C and Gerlai R 2008 The social zebrafish: behavioral responses to conspecific, heterospecific, and computer animated fish Behav. Brain Res. 191 77-87
30. Seehausen O and van Alphen J J 1998 The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex) Behav. Ecol. Sociobiol. 42 1-8 (Pubitemid 28189726)
31. Swain D T, Couzin I D and Leonard N E 2012 Real-time feedback-controlled robotic fish for behavioral experiments with fish schools Proc. IEEE 100 150-63
32. Krause J, Winfield A F and Deneubourg J L 2011 Interactive robots in experimental biology Trends Ecol. Evol. 26 369-75
33. Kopman V, Laut J W, Polverino G and Porfiri M 2013 Closed-loop control of zebrafish response using a bioinspired robotic-fish in a preference test J. R. Soc. Interface 10 20120540
34. Polverino G and Porfiri M 2013 Mosquitofish (Gambusia affinis) responds differentially to a robotic fish of varying swimming depth and aspect ratio Behav. Brain Res. 250 133-8
35. Polverino G, Abaid N, Kopman V, Macrì S and Porfiri M 2012 Zebrafish response to robotic fish: preference experiments on isolated individuals and small shoals Bioinspir. Biomim. 7 036019
36. Marras S and Porfiri M 2012 Fish and robots swimming together: attraction towards the robot demands biomimetic locomotion J. R. Soc. Interface 9 1856-68
37. Polverino G and Porfiri M 2013 Zebrafish (Danio rerio) behavioural response to bioinspired robotic fish and mosquitofish (Gambusia affinis) Bioinspir. Biomim. 8 044001
38. Spinello C, Macrì S and Porfiri M 2013 Acute ethanol administration affects zebrafish preference for a biologically-inspired robot Alcohol 47 391-8
39. Abaid N, Marras S, Fitzgibbons C and Porfiri M 2013 Modulation of risk-taking behaviour in golden shiners (Notemigonus crysoleucas) using robotic fish Behav. Process. 100 9-12
40. Cianca V, Bartolini T, Porfiri M and Macri S 2013 A robotics-based behavioral paradigm to measure anxiety-related responses in zebrafish PLoS ONE 8 e69661
41. Aureli M, Fiorilli F and Porfiri M 2012 Portraits of self-organization in fish schools interacting with robots Physica D 241 908-20
42. Faria J J, Dyer J R G, Clement R O, Couzin I D, Holt N, Ward A J W, Waters D and Krause J 2010 A novel method for investigating the collective behaviour of fish: introducing 'Robofish' Behav. Ecol. Sociobiol. 64 1211-8
43. Rossi C, Coral W and Barrientos A 2012 Swimming Physiology of Fish: Towards Using Exercise for Farming a Fit Fish in Sustainable Aquaculture ed A P Palstra and J V Planas (New York: Springer)
44. Polverino G, Phamduy P and Porfiri M 2013 Fish and robots swimming together in a water tunnel: robot color and tail-beat frequency influence fish behavior PLoS ONE 8 e77589
45. Abaid N, Bartolini T, Macri S and Porfiri M 2012 Zebrafish responds differentially to a robotic fish of varying aspect ratio, tail beat frequency, noise, and color Behav. Brain Res. 233 545-53
46. Foster N R 1967 Comparative Studies on the Biology of Killifishes (Pisces, Cyprinodontidae) (Ithaca, NY: Cornell Univ.)
47. Fuller R C 2002 Lighting environment predicts the relative abundance of male colour morphs in bluefin killifish (Lucania goodei) populations Proc. R. Soc. B 269 1457-65 (Pubitemid 34810661)
48. Fuller R C and Travis J 2004 Genetics, lighting environment, and heritable responses to lighting environment affect male color morph expression in bluefin killifish Lucania goodei Evolution 58 1086-98 (Pubitemid 38673796)
49. Fuller R C and Johnson A M 2009 A test for negative frequency-dependent mating success as a function of male colour pattern in the bluefin killifish Biol. J. Linn. Soc. 98 489-500
50. Fuller R C and Noa L A 2010 Female mating preferences, lighting environment, and a test of the sensory bias hypothesis in the bluefin killifish Anim. Behav. 80 23-35
51. Fuller R C, Fleishman L J, Leal M, Travis J and Loew E 2003 Intraspecific variation in retinal cone distribution in the bluefin killifish Lucania goodei J. Comp. Physiol. A 189 609-16 (Pubitemid 37105902)
52. Butail S, Bartolini T and Porfiri M 2013 Collective response of zebrafish shoals to a free-swimming robotic fish PLoS ONE 8 e76123
53. Kalueff A V, Stewart A M and Gerlai R 2014 Zebrafish as an emerging model for studying complex brain disorders Trends Pharmacol. Sci. 35 63-75
54. Fuller R C 2001 Patterns in male breeding behaviors in the bluefin killifish, Lucania goodei: a field study (Cyprinodontiformes: Fundulidae) Copeia 2001 823-8 (Pubitemid 33146263)
55. Price A C, Weadick C J, Shim J and Rodd F H 2008 Pigments, patterns, and fish behavior Zebrafish 5 297-307
56. Tinbergen N 1953 The Herring Gull's World: a Study of the Social Behaviour of Birds (Oxford: Frederick A. Praeger)
57. McAlister W H 1958 The correlation of coloration with social rank in Gambusia hurtadoi Ecology 39 477-82
58. Molstad A J 2008 Development of Vision and the Effect of Spectral Environment on the Cone Photoreceptor Mosaic of the Bluefin Killifish Lucania goodei (Tallahassee, FL: Florida State University) 30
59. Cummings M E, Jordão J M, Cronin T W and Oliveira R F 2008 Visual ecology of the fiddler crab, Uca tangeri: effects of sex, viewer and background on conspicuousness Anim. Behav. 75 175-88 (Pubitemid 350298083)
60. Bybee S M, Yuan F, Ramstetter M D, Llorente-Bousquets J, Reed R D, Osorio D and Briscoe A D 2012 UV photoreceptors and UV-yellow wing pigments in Heliconius butterflies allow a color signal to serve both mimicry and intraspecific communication Amer. Nat. 179 38-51
61. Flamarique I N and Harosi F I 2000 Photoreceptors, visual pigments, and ellipsosomes in the killifish, Fundulus heteroclitus: a microspectrophotometric and histological study Visual Neurosci. 17 403-20 (Pubitemid 30451622)
62. Körner K E, Schlupp I, Plath M and Loew E R 2006 Spectral sensitivity of mollies: comparing surface-and cave-dwelling Atlantic mollies Poecilia mexicana J. Fish Biol. 69 54-65 (Pubitemid 44365985)
63. Watson C, Lubieniecki K, Loew E, Davidson W and Breden F 2010 Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail Xiphophorus helleri BMC Evol. Biol. 10 87
64. Cen L and Erturk A 2013 Bio-inspired aquatic robotics by untethered piezohydroelastic actuation Bioinspir. Biomim. 8 016006
65. Mojarrad M and Shahinpoor M 1997 Biomimetic robotic propulsion using polymeric artificial muscles Proc. IEEE Int. Conf. Robotics and Automation (Albuquerque, NM,) 2152-7
66. Chen Z, Sharata S and Tan X 2010 Modeling of biomimetic robotic fish propelled by an ionic polymer metal composite caudal fin IEEE ASME Trans. Mechatron. 15 448-59
67. Aureli M, Kopman V and Porfiri M 2010 Free-locomotion of underwater vehicles actuated by ionic polymer metal composites IEEE ASME Trans. Mechatron. 15 603-14
68. Yeom S W and Oh I K 2009 A biomimetic jellyfish robot based on ionic polymer metal composite actuators Smart Mater. Struct. 18 085002