Do Fireflies Detect the Color of Their Bioluminescent Flash?
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Colors of the Night: Do fireflies detect the color of their bioluminescent flash? Abner B. Lall Department of Biology, Howard University, Washington, DC 2. Von Uexküll’s Functional Cycle Perpetual Field Receptor Central Receptor Inner Perpetual Cue World of Object Bearer (Releaser) the Central Effector Subject Functional Cue Bearer (Effector) Motor Field 3. Illuminated lanterns of Photinus pyralis and Photuris versicolor 4. Bioluminescence emissions of different species of North American lampyrids 550 560 570 580 1.0 0.8 Relative 0.6 Intensity 0.4 0.2 0.0 500 550 600 650 700 Wavelength [nm] 5. Peak emission of bioluminescence (BL) of North American lampyrids as a function of the time for the initiation of flashing activity 8 6 Early-flashing or Frequency 4 vespertine 2 0 14 12 Late -flashing 10 or nocturnal 8 Frequency 6 4 2 0 550 560 570 580 Peak Wavelength [nm] 6. Fireflies have large spherical scotopic eyes Photo by Prof. J. Lloyd Photo by Prof. J. Lloyd 7. Hemisected scotopic compound eye of Photinus pyralis Photo by Prof. M. Järvilehto 8. Superposition eye has a large aperture to summate photons coming through off-axis facets to a point giving an erect image 9. Electroretinograms (ERGs) of negative polarity recorded from the corneal surface by long duration stimuli differ in the short from the long wavelengths across the spectrum 10. Determination of electroretinographic visual spectral sensitivity of the eye 11. Narrow bimodal ERG [S(λ)] functions in vespertine Photinus collustrans & P. marginellus with attenuation of sensitivity in the green region 0 0 Photinus Photinus collustrans marginellus Log Relative Sensitivity 1 1 2 2 100 1.0 (560) (563) 80 Bioluminescence 0.8 emission 60 0.6 Relative Sensitivity Photon 40 0.4 Intensity 20 0.2 0 0 350 450 550 650 350 450 550 650 Wavelength [nm] 12. Longitudinal section through the rhabdomeric region showing orange screening pigment that causes attentuation of sensitivity in the green in P. pyralis Photo by Prof. M. Järvilehto 13. In Situ MSP absorbance of orange screening pigments as cut-off filters for sunlight reflection from green foliage in vespertine species 1.0 0.8 P. scintillans 525 0.6 –N = 21 0.4 •N = 3 0.2 0 1.0 P. macdermotti 0.8 510 N = 18 0.6 0.4 0.2 Absorbance 0 1.0 P. collustrans 0.8 512 –N = 18 0.6 •N = 10 0.4 0.2 0 1.0 P. pyralis 0.8 517 0.6 –N = 18 0.4 •N = 19 0.2 0 400 450 500 550 600 650 700 Wavelength [nm] 14. Dovetailing between species BL and S(λ) functions in six vespertine species with marked attenuation of sensitivity in the green Photinus 560 Photinus 564 Photinus 578 1.0 collustrans marginellus scintillans 1.0 0.8 0.8 0.6 0.6 0.4 0.4 0.2 0.2 0 0 562 564 569 Bicellonycha Photinus Photinus 1.0 wickershamorum pyralis macdermotti 1.0 0.8 0.8 0.6 0.6 Relative Sensitivity Relative 0.4 0.4 0.2 0.2 Relative Intensity PhotonRelative 0 0 350 400 450 500 550 600 650 700 350 400 450 500 550 600 650 700 350 400 450 500 550 600 650 700 Wavelength [nm] 15. Broad ERG S(λ) functions in nocturnal firefly Photuris versicolor 0 + 1 DA Log Relative 0.3 mV Quantal 2 Sensitivity 3 4.0 mV 4 100 80 Relative 60 Sensitivity BL Emission 40 20 0 300 350 400 450 500 550 600 650 700 Wavelength [nm] 16. Broad ERG S(λ) maxima and BL emission of nocturnal firefly Photuris lucicrescens 0 Log Relative 1 Quantal Sensitivity Dorsal, n=5 2 0 Log Relative 1 Ventral, n=7 Quantal Sensitivity 2 100 100 80 80 ERG Relative Relative 60 60 Photon Sensitivity 40 40 Intensity 20 BL Emission 20 0 0 300 350 400 450 500 550 600 650 700 Wavelength [nm] 17. Broad ERG S(λ) functions in nocturnal fireflies Photuris versicolor & P. lucicrescens 18. Chromatic adaptation with orange filter (A) and with intense monochromatic lights (B) show the presence of three: near-uv, blue and green types of receptors 19. Differential monochromatic adaptation uncovers blue, green, and near-uv receptors 20. Near–uv and blue sensitivity in dorsal frontal region 21. Longitudinal section through the rhabdomeric segment in Photuris (Horridge, 1969) 22. Intracellular receptor potential from single retinular cells in Photinus pyralis Intracellular + ERG 40 30 20 mV Intracellular 10 0 ERG -10 0 200 400 ms 23. Narrow yellow spectral sensitivity of the receptor potential in single retinular cells of Photinus pyralis 1.0 0.8 0.6 Relative Sensitivity 0.4 0.2 0 300 350 400 450 500 550 600 650 Wavelength [nm] 24. Single tiered cartridge consisting of 6 large proximal R1-6 (yellow/green), one distal R7 (UV) and one basal R8 (blue) retinular cells 25. Comparison of the action spectrum of the female response with single cell S(λ) function and the BL emission in vespertine Photinus pyralis 100 100 Female Behavioral Threshold 80 80 60 60 Relative Relative Sensitivity 40 40 Photon Intensity 20 20 Bioluminescence Single cell 0 0 400 450 500 550 600 650 700 Wavelength [nm] 26. Action spectrum of the inhibition of the female response in Photinus pyralis -10.50 -10.75 -11.00 -11.25 -11.50 -11.75 LogPhoton/s/cm2 -12.00 -12.25 -12.50 380 400 420 440 460 480 500 Wavelength -nm 27. Results 1. The female fireflies did not respond to test flashes (500 ms every 4 s) at 420, 440, 458 and 480 nm. 2. Bright blue adapting light at 420, 440, 460 and 480 nm inhibited the female response to 548 nm test flash. 3. The response inhibition persisted even after the adaptation light was turned off. 4. For females to consistently respond to 548 nm test flash, the females had to be primed after blue adaptation. 5. The action spectrum of the inhibition is in the short wavelength part of the spectrum and corresponds to the blue spectral mechanism isolated by chromatic adaptation. 28. Conclusions 1. Fireflies possess three receptors: near-uv, blue and yellow/green. 2. Yellow/green receptor is the transducer for the BL signal. 3. The stimulation of the blue receptor results in an inhibition of the female response in P. pyralis. 4. The presence of blue-green antagonist system is the hallmark of processing color information in insects. 5. It is proposed that the yellow/green receptors put an excitation (+) input, and the blue receptors put an inhibitory (-) input to the neurons of the visual centers in the firefly brain. 29. Conclusions continue 5. The evidence for the presence of a blue-green antagonist chromatic mechanism exists in glow- worm Lampyris noctiluca (Booth et al. 2004). 6. The presence of color vision in dim starlight has been shown in nocturnal hawkmoth, Deilephila elpenor (Kelber et al. 2002). 7. We propose that fireflies functioning in dimly lighted environments possess color vision. 30. Research Collaborators SPECTROSCOPY Professor Howard H. Seliger William H. Biggley Johns Hopkins University ECOLOGY & BEHAVIOR Professor James E. Lloyd, University of Florida STRUCTURE Professor Matti Järvilehto, University of Oulo, Finland MICROSPECTROPHOTOMETRY Professor Thomas W. Cronin, University of Maryland Professor G. K. Strothers, Pennsylvania State University ELECTROPHYSIOLOGY Professor Matti Weckström, University of Oulu, Finland STUDENTS : Egbert T. Lord, Ph. D., Howard University Karen M. Worthy, M. A., Howard University Phillip Chapados, B.S. Johns Hopkins University .