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Seeing double: visual physiology of double-retina eye ontogeny in stomatopod crustaceans

Journal of Comparative Physiology A volume 201, pages 331–339 (2015)Cite this article

Abstract

Stomatopod eye development is unusual among crustaceans. Just prior to metamorphosis, an adult retina and associated neuro-processing structures emerge adjacent to the existing material in the larval compound eye. Depending on the species, the duration of this double-retina eye can range from a few hours to several days. Although this developmental process occurs in all stomatopod species observed to date, the retinal physiology and extent to which each retina contributes to the animal’s visual sensitivity during this transition phase is unknown. We investigated the visual physiology of stomatopod double retinas using microspectrophotometry and electroretinogram recordings from different developmental stages of the Western Atlantic species Squilla empusa. Though microspectrophotometry data were inconclusive, we found robust ERG responses in both larval and adult retinas at all sampled time points indicating that the adult retina responds to light from the very onset of its emergence. We also found evidence of an increase in the response dynamics with ontogeny as well as an increase in sensitivity of retinal tissue during the double-retina phase relative to single retinas. These data provide an initial investigation into the ontogeny of vision during stomatopod double-retina eye development.

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References

  • Ahyong ST, Haug JT, Haug C (2014) Stomatopoda. In: Martin JW, Oleson J, Høeg J (eds) Atlas of crustacean larvae. Johns Hopkins University Press, pp 185

  • Arikawa K, Kawamata K, Suzuki T, Eguchi E (1987) Daily change of structure, function and rhodopsin content in the compound eye of the crab Hemigrapsus sanguineus. J Comp Physiol A 161:1–15

    Article  Google Scholar 

  • Arikawa K, Morikawa Y, Suzuki T, Eguchi E (1988) Intrinsic control of rhabdom size and rhodopsin content in crab compound eye by circadian biological clock. Cell Mol Life Sci 44:219–220

    Article  CAS  Google Scholar 

  • Bok MJ, Porter ML, Place AR, Cronin TW (2014) Biological sunscreens tune polychromatic ultraviolet vision in mantis shrimp. Curr Biol 24:1636–1642

    Article  CAS  PubMed  Google Scholar 

  • Chamberlain SC, Barlow RB (2003) Transient membrane shedding in Limulus photoreceptors: Control mechanisms under natural lighting. J Neurosci 4:2792–2810

    Google Scholar 

  • Chapman RM, Lall AB (1967) Electroretinogram characteristics and the spectral mechanisms of the median ocellus and the lateral eye in Limulus polyphemus. J Gen Physiol 50:2267–2287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cohen JH, Cronin TW, Lessios N, Forward RB (2010) Visual physiology underlying orientation and diel behavior in the sand beach amphipod Talorchestia longicornis. J Exp Biol 213:3843–3851

    Article  PubMed  Google Scholar 

  • Cronin T (1985) The visual pigment of a stomatopod crustacean, Squilla empusa. J Comp Physiol A 156:679–687

    Article  CAS  Google Scholar 

  • Cronin TW (1992) Visual rhythms in stomatopod crustaceans observed in the pseudopupil. Biol Bull 182:278–287

    Article  Google Scholar 

  • Cronin T, Jinks R (2001) Ontogeny of vision in marine crustaceans. Am Zool 41:1098–1107

    Article  Google Scholar 

  • Cronin T, Marshall N (1989) Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans. J Comp Physiol A 166:1–16

    Article  Google Scholar 

  • Cronin TW, Marshall N, Caldwell R, Pales D (1995) Compound eyes and ocular pigments of crustacean larvae (Stomatopoda and Decapoda, Brachyura). Mar Freshw Behav Phy 26:219–231

    Article  Google Scholar 

  • Deruntz P, Palevody C, Lambin M (1994) Effect of dark rearing on the eyes of Gryllus birnaculatus crickets. J Exp Zool 268:421–427

    Article  Google Scholar 

  • Douglass J, Forward R (1989) The ontogeny of facultative superposition optics in a shrimp eye: hatching through metamorphosis. Cell Tissue Res 258:289–300

    Article  Google Scholar 

  • Feller KD, Cronin TW, Ahyong ST, Porter ML (2013) Morphological and molecular description of the late-stage larvae of Alima Leach, 1817 (Crustacea: Stoamtopoda) from Lizard Island. Australia. Zootaxa 37221(1):22–32

    Article  Google Scholar 

  • Fincham A (1984) Ontogeny and optics of the eyes of the common prawn Palaemon (Palaemon) serratus (Pennant, 1777). Zool J Linn Soc-Lond 81:89–113

    Article  Google Scholar 

  • Gaten E (1998) Optics and phylogeny: is there an insight? The evolution of superposition eyes in the Decapoda (Crustacea). Contrib Zool 67:223–236

    Google Scholar 

  • Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG (2000) In search of the visual pigment template. Vis Neurosci 17:509–528

    Article  CAS  Google Scholar 

  • Jinks RN, Markley TL, Taylor EE, Perovich G, Dittel AI, Epifanio CE, Cronin TW (2002) Adaptive visual metamorphosis in a deep-sea hydrothermal vent crab. Nature 420:68–70

    Article  CAS  PubMed  Google Scholar 

  • Loew ER (1982) A field-portable microspectrophotometer. Meth Enzymol 81:647–655

    Article  CAS  Google Scholar 

  • Marshall J, Oberwinkler J (1999) Ultraviolet vision: the colourful world of the mantis shrimp. Nature 401:873–874

    Article  CAS  PubMed  Google Scholar 

  • Marshall N, Land M, King C, Cronin T (1991a) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarized light. Philos Trans Biol Sci 334:33–56

    Article  Google Scholar 

  • Marshall N, Land M, King C, Cronin T (1991b) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). II. Colour pigments in the eyes of stomatopod crustaceans: Polychromatic vision by serial and lateral filtering. Philos Trans Biol Sci 334:57–84

    Article  Google Scholar 

  • Marshall J, Cronin T, Kleinlogel S (2007) Stomatopod eye structure and function: a review. Arthropod Struct Dev 36:420–488

    Article  PubMed  Google Scholar 

  • Meyer-Rochow V (1975) Larval and adult eye of the western rock lobster (Panulirus longipes). Cell Tissue Res 162:439–457

    Article  CAS  PubMed  Google Scholar 

  • Meyer-Rochow V, Keskinen E (2003) Post-embryonic photoreceptor development and dark/light adaption in the stick insect Carausius morosus (Phasmida, Phasmatidae). Appl Entomol Zool 38:1–11

    Article  Google Scholar 

  • Morgan S, Provenzano A (1979) Development of pelagic larvae and postlarva of Squilla empusa (Crustacea, Stomatopoda), with an assessment of larval characters within the squillidae. Fish Bull 77:61–90

    Google Scholar 

  • Nilsson D (1983) Evolutionary links between apposition and superposition optics in crustacean eyes. Nature 302:818–821

    Article  Google Scholar 

  • Nilsson D, Hallberg E, Elofsson R (1986) The ontogenetic development of refracting superposition eyes in crustaceans: transformation of optical design. Tissue Cell 18:509–519

    Article  CAS  PubMed  Google Scholar 

  • Porter ML, Zhang Y, Desai S, Caldwell RL, Cronin TW (2010) Evolution of anatomical and physiological specialization in the compound eyes of stomatopod crustaceans. J Exp Biol 213:3473–3486

    Article  CAS  PubMed  Google Scholar 

  • Schiff H, Dore B, Boido M (2007) Morphology of adaptation and morphogenesis in stomatopod eyes. Ital J Zool 74(2):123–134

    Article  Google Scholar 

  • Stowe S (1980) Spectral sensitivity and retinal pigment movement in the crab Leptograpsus variegatus (Fabricius). J Exp Biol 87:73–98

    CAS  PubMed  Google Scholar 

  • Trevino DL, Larimer JL (1969) The spectral sensitivity and flicker response of the eye of the stomatopod. Squilla empusa say. Comp Biochem Physiol 31(6):987–991

    Article  Google Scholar 

  • Williams B, Greenwood J, Jillett J (1985) Seasonality and duration of the developmental stages of Heterosquilla tricarinata (Claus, 1871) (Crustacea: Stomatopoda) and the replacement of the larval eye at metamorphosis. Bull Mar Sci 36:104–114

    Google Scholar 

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Acknowledgments

We thank Dr. Richard Forward for his expert advice regarding S. empusa larvae as well as the use of his laboratory facilities at the Duke University Marine Laboratory (Beaufort, North Carolina, USA). Thank you to Dr. Ellis Loew (Cornell University, Ithaca, New York, USA) for the use of his field portable MSP system and Dr. Tsyr-Huei Chiou for his advice regarding his preliminary methods with conducting stomatopod larval ERGs. Also, thank you to Mary Willard and Margaret Blake for assistance with field collections and ERG data acquisition. We minimized the number of animals used in these experiments as well as dispatched individuals on ice immediately after recording. This work was funded by a Grant-In-Aid of Research from the Society of Integrative and Comparative Biology, the United States Air Force Office of Scientific Research [FA9550-12-1-0321], and the University of Delaware Research Foundation [12A0075].

Conflict of interest

There are no conflicts of interest to declare by the authors regarding this work.

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Authors and Affiliations

  1. University of Maryland Baltimore County, 1000 Hilltop Circle, Baltimore, MD, 21250, USA

    Kathryn D. Feller & Thomas W. Cronin

  2. College of Earth, Ocean and Environment, School of Marine Science and Policy, University of Delaware, 700 Pilottown Road, Lewes, DE, 19958, USA

    Jonathan H. Cohen

Authors
  1. Kathryn D. Feller
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  2. Jonathan H. Cohen
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  3. Thomas W. Cronin
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Correspondence to Kathryn D. Feller.

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Feller, K.D., Cohen, J.H. & Cronin, T.W. Seeing double: visual physiology of double-retina eye ontogeny in stomatopod crustaceans. J Comp Physiol A 201, 331–339 (2015). https://doi.org/10.1007/s00359-014-0967-2

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  • DOI: https://doi.org/10.1007/s00359-014-0967-2

Keywords

  • Squilla empusa
  • Vision
  • Ontogeny
  • Electroretinogram
  • Microspectrophotometry