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Retinal ultrastructure may mediate polarization sensitivity in larvae of the Sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae)

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Abstract

A number of invertebrates are known to be sensitive to the polarization of light and use this trait in orientation, communication, or prey detection. In these animals polarization sensitivity tends to originate in rhabdomeric photoreceptors that are more or less uniformly straight and parallel. Typically, polarization sensitivity is based on paired sets of photoreceptors with orthogonal orientation of their rhabdomeres. Sunburst diving beetle larvae are active swimmers and highly visual hunters which could potentially profit from polarization sensitivity. These larvae, like those of most Dytiscids, have a cluster of six lens eyes or stemmata (designated E1 through E6) on each side of the head capsule. We examined the ultrastructure of the photoreceptor cells of the principal eyes (E1 and E2) of first instar larvae to determine whether their rhabdomeric organization could support polarization sensitivity. A detailed electron microscopical study shows that the proximal retinas of E1 and E2 are in fact composed of photoreceptors with predominantly parallel microvilli and that neighboring rhabdomeres are oriented approximately perpendicularly to one another. A similar organization is observed in the medial retina of E1, but not in the distal retinas of E1&2. Our findings suggest that T. marmoratus larvae might be able to analyze polarized light. If so, this could be used by freshly hatched larvae to find water or within the water to break the camouflage of common prey items such as mosquito larvae. Physiological and behavioral tests are planned to determine whether larvae of T. marmoratus can actually detect and exploit polarization signals.

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References

  • Bernard GD, Wehner R (1977) Functional similarities between polarization vision and color vision. Vision Res 17:1019–1028

    Article  PubMed  CAS  Google Scholar 

  • Boal JG, Shashar N, Grable MM, Vaughan KH, Loew ER, Hanlon RT (2004) Behavioral evidence for intraspecific signaling with achromatic and polarized light by cuttlefish (Mollusca: Cephalopoda). Behaviour 141:837–861

    Article  Google Scholar 

  • Brown PK, Brown PS (1958) Visual pigments of the Octopus and cuttlefish. Nature 182:1288–1290

    Article  PubMed  CAS  Google Scholar 

  • Buschbeck EK, Sbita SJ, Morgan RC (2007) Scanning behavior by larvae of the predacious diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae) enlarges visual field prior to prey capture. J Comp Physiol A 193:973–982

    Article  Google Scholar 

  • Chiou TH, Kleinlogel S, Cronin T, Caldwell R, Loeffler B, Siddiqi A, Goldizen A, Marshall J (2008) Circular polarization vision in a stomatopod crustacean. Curr Biol 18:429–434

    Article  PubMed  CAS  Google Scholar 

  • Cronin TW (2006) Invertebrate vision in water. In: Warrant E, Nilsson D-E (eds) Invertebrate colour vision. Cambridge University Press, Cambridge, pp 211–249

    Google Scholar 

  • Eguchi E, Waterman TH (1968) Cellular basis for polarized light perception in the spider crab, Libinia. Cell Tissue Res 84:87–101

    CAS  Google Scholar 

  • Evans AV (2006) Field guide to beetles of California. University of California Press, Berkeley

    Google Scholar 

  • Glas HW (1977) Models for unambiguous e-vector navigation in the bee. J Comp Physiol A 113:129–159

    Article  Google Scholar 

  • Goldsmith TH (1975) The polarization sensitivity–dichroic absorption paradox in arthropod photoreceptors. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin, pp 392–409

    Google Scholar 

  • Goldsmith TH (1977) Membrane adaptations of visual photoreceptors for the analysis of plane-polarized light. In: Castellani A (ed) Research in photobiology. Plenum Press, New York, pp 651–658

    Google Scholar 

  • Horváth G (1995) Reflection polarization patterns at flat water surfaces and their relevance for insect polarization vision. J Theor Biol 175:27–37

    Article  PubMed  Google Scholar 

  • Horváth G, Varjú D (2004) Polarized light in animal vision: polarization patterns in nature. Springer, Berlin

    Google Scholar 

  • Johnsen S (2005) Visual ecology on the high seas. Mar Ecol Prog Ser 287:281–285

    Google Scholar 

  • Labhart T (1980) Specialized photoreceptors at the dorsal rim of the honeybee’s compound eye: polarizational and angular sensitivity. J Comp Physiol A 141:19–30

    Article  Google Scholar 

  • Lerner A, Meltser N, Sapir N, Erlick C, Shashar N, Broza M (2008) Reflected polarization guides chironomid females to oviposition sites. J Exp Biol 211:3536–3543

    Article  PubMed  Google Scholar 

  • Lythgoe JN, Hemmings CC (1967) Polarized light and underwater vision. Nature 213:893–894

    Article  PubMed  CAS  Google Scholar 

  • Maksimovic S, Cook TA, Buschbeck EK (2009) Spatial distribution of opsin-encoding mRNAs in the tiered larval retinas of the sunburst diving beetle Thermonectus marmoratus (Coleoptera: Dytiscidae). J Exp Biol 212:3781–3794

    Article  PubMed  CAS  Google Scholar 

  • Mandapaka K, Morgan RC, Buschbeck EK (2006) Twenty-eight retinas but only twelve eyes: an anatomical analysis of the larval visual system of the diving beetle Thermonectus marmoratus (Coleoptera: Dytiscidae). J Comp Neurol 497:166–181

    Article  PubMed  Google Scholar 

  • Marshall NJ, Messenger JB (1996) Colour-blind camouflage. Nature 382:408–409

    Article  CAS  Google Scholar 

  • Marshall J, Cronin TW, Shashar N, Land M (1999) Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication. Curr Biol 9:755–758

    Article  PubMed  CAS  Google Scholar 

  • Mäthger LM, Hanlon RT (2006) Anatomical basis for camouflaged polarized light communication in squid. Biol Lett 2:494–496

    Article  PubMed  Google Scholar 

  • Morgan RC (1992) Natural history, captive management and the display of the sunburst diving beetle Thermonectus marmoratus. AAZPA/CAZPA Annual Conference, pp 457–464

  • Morgan RC (1995) Sunburst diving beetle Thermonectus marmoratus biology, husbandry and display. Invertebrate Captivity, pp 50–57

  • Novales-Flamarique I, Hawryshyn CW (1997) Is the use of underwater polarized light by fish restricted to crepuscular time periods? Vision Res 37:975–989

    Article  PubMed  CAS  Google Scholar 

  • Rossel S (1993) Navigation by bees using polarized skylight. Comp Biochem Physiol 104:695–708

    Article  Google Scholar 

  • Rossel S, Wehner R (1982) The bee’s map of the e-vector pattern in the sky. PNAS 79:4451–4455

    Article  PubMed  CAS  Google Scholar 

  • Schwind R (1984) The plunge reaction of the backswimmer Notonecta glauca. J Comp Physiol A 155:319–321

    Article  Google Scholar 

  • Schwind R (1991) Polarization vision in water insects and insects living on a moist substrate. J Comp Physiol A 169:531–540

    Article  Google Scholar 

  • Shashar N, Hanlon RT (1997) Squids (Loligo pealei and Euprymna scolopes) can exhibit polarized light patterns produced by their skin. Biol Bull 193:207–208

    Google Scholar 

  • Shashar N, Hanlon RT, Petz AD (1998) Polarization vision helps detect transparent prey. Nature 393:222–223

    Article  CAS  Google Scholar 

  • Shashar N, Hagan R, Boal JG, Hanlon RT (2000) Cuttlefish use polarization sensitivity in predation on silvery fish. Vision Res 40:71–75

    Article  PubMed  CAS  Google Scholar 

  • Smola U, Tscharntke H (1979) Twisted rhabdomeres in the dipteran eye. J Comp Physiol 133:291–297

    Article  Google Scholar 

  • Smola U, Wunderer H (1981) Fly rhabdomeres twist invivo. J Comp Physiol 142:43–49

    Article  Google Scholar 

  • Snyder AW, McIntyre P (1975) Polarisation sensitivity of twisted fused rhabdoms. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin, pp 388–391

    Google Scholar 

  • Strausfeld NJ, Seyan HS (1985) Convergence of visual, haltere, and prosternal inputs at neck motor neuron of Calliphora erythrocephala. Cell Tissue Res 240:601–615

    Article  Google Scholar 

  • Tuchin VV (2007) Tissue optics: light scattering methods and instruments for medical diagnosis. Society of Photo-Optical Instrumentation Engineers

  • Velasco J, Millan VH (1998) Feeding habits of two large insects from a desert stream: Abedus herberti (Hemiptera: Belostomatidae) and Thermonectus marmoratus (Coleoptera: Dytiscidae). Aquat Insects 20:85–96

    Article  Google Scholar 

  • von Frisch K (1949) Polarisation des Himmelslicht als orientierender Faktor bei den Tänzen der Bienen. Experientia 5:142–148

    Article  PubMed  CAS  Google Scholar 

  • von Frisch K, Lindauer M (1956) The “language” and orientation of the honey bee. Annu Rev Entomol 1:45–58

    Article  Google Scholar 

  • Waterman TH (1975) The optics of polarization sensitivity. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin, pp 339–371

    Google Scholar 

  • Wehner R (2001) Polarization vision–a uniform sensory capacity? J Exp Biol 204:2589–2596

    PubMed  CAS  Google Scholar 

  • Wehner R, Bernard GD (1993) Photoreceptor twist–a solution to the false-color problem. PNAS 90:4132–4135

    Article  PubMed  CAS  Google Scholar 

  • Wehner R, Labhart T (2006) Polarisation vision. In: Warrant E, Nilsson D-E (eds) Invertebrate vision. Cambridge University Press, Cambridge, pp 291–348

    Google Scholar 

  • Wehner R, Strasser S (1985) The POL area of the honey bee’s eye: behavioral evidence. Physiol Entomol 10:337–349

    Article  Google Scholar 

  • Wehner R, Bernard GD, Geiger E (1975) Twisted and non-twisted rhabdoms and their significance for polarization detection in the bee. J Comp Physiol 104:225–245

    Article  Google Scholar 

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Acknowledgments

The Insectarium of the Cincinnati Zoo and Botanical Garden provided the initial culture of Sunburst Diving Beetles. We are grateful to Dr. Birgit Ehmer and Karunyakanth Mandapaka for their technical assistance. We also thank two anonymous reviewers for valuable feedback, Shannon Werner for editing the final version of the manuscript, and the Vontz Center for Molecular Studies for the use of their equipment. This research was funded by the National Science Foundation (IOB-545978).

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Authors and Affiliations

  1. Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA

    Nadine Stecher & Elke K. Buschbeck

  2. Insectarium, Cincinnati Zoo and Botanical Garden, 3400 Vine Street, Cincinnati, OH, 45220-1399, USA

    Randy Morgan

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  1. Nadine Stecher
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  2. Randy Morgan
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  3. Elke K. Buschbeck
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Correspondence to Elke K. Buschbeck.

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Communicated by T. Bartolomaeus.

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Stecher, N., Morgan, R. & Buschbeck, E.K. Retinal ultrastructure may mediate polarization sensitivity in larvae of the Sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae). Zoomorphology 129, 141–152 (2010). https://doi.org/10.1007/s00435-010-0107-7

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  • DOI: https://doi.org/10.1007/s00435-010-0107-7

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