Abstract
Cubomedusae (box jellyfish) possess a remarkable visual system with 24 eyes distributed in four sensory structures termed rhopalia. Each rhopalium is equipped with six eyes: two pairs of pigment cup eyes and two unpaired lens eyes. Each eye type probably captures specific features of the visual environment. To investigate whether multiple types of photoreceptor cells are present in the rhopalium, and whether the different eye types possess different types of photoreceptors, we have used immunohistochemistry with a range of vertebrate opsin antibodies to label the photoreceptors, and electroretinograms (ERG) to determine their spectral sensitivity. All photoreceptor cells of the two lens eyes of the box jellyfish Tripedalia cystophora and Carybdea marsupialis displayed immunoreactivity for an antibody directed against the zebrafish ultraviolet (UV) opsin, but not against any of eight other rhodopsin or cone opsin antibodies tested. In neither of the two species were the pigment cup eyes immunoreactive for any of the opsin antibodies. ERG analysis of the Carybdea lower lens eyes demonstrated a single spectral sensitivity maximum at 485 nm suggesting the presence of a single opsin type. Our data demonstrate that the lens eyes of box jellyfish utilize a single opsin and are thus color-blind, and that there is probably a different photopigment in the pigment cup eyes. The results support our hypothesis that the lens eyes and the pigment cup eyes of box jellyfish are involved in different and specific visual tasks.
Similar content being viewed by others
References
Coates MM, Garm A, Theobald JC, Thompson SH, Nilsson D-E (2006) The spectral sensitivity of the lens eyes of a box jellyfish, Tripedalia cystophora (Conant). J Exp Biol 209:3758–3765
de Couet HG, Tanimura T (1987) Monoclonal antibodies provide evidence that rhodopsin in the outer rhabdomeres of Drosophila melanogaster is not glycosylated. Eur J Cell Biol 44:50–66
Foster RG, Garzia-Fernandez JM, Provencio I, DeGrip WJ (1993) Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. J Comp Physiol [A] 172:33–45
Garm A, Coates MM, Gad R, Seymour J, Nilsson D-E (2007a) The lens eyes of the box jellyfish Tripedalia cystophora and Chiropsalmus sp. are slow and color-blind. J Comp Physiol [A] 193:547–557
Garm A, O’Connor M, Parkefelt L, Nilsson D-E (2007b) Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie. J Exp Biol 210:3616–3623
Garm A, Andersson F, Nilsson D-E (2008) Unique structure and optics of the lesser eyes of the box jellyfish Tripedalia cystophora. Vision Res, in press
Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528
Janssen JJM (1991) The rod visual pigment rhodopsin: in vitro expression and site specific mutagenesis. PhD Thesis, University of Nijmegen, The Netherlands
Land MF, Nilsson D-E (2006) General-purpose and special-purpose visual systems. In: Warrant EJ, Nilsson D-E (eds) Invertebrate vision. Cambridge University Press, Cambridge, pp 167–210
Laska G, Hündgen M (1982) Morphologie und Ultrastruktur der Lichtsinnesorgane von Tripedalia cystophora Conant (Cnidaria, Cubozoa). Zool Jb Anat 108:107–123
Martin VJ (2004) Photoreceptors of cubozoan jellyfish. Hydrobiologia 530/531:135–144
Nilsson D-E, Coates M, Gislén L, Skogh C, Garm A (2005) Advanced optics in a jellyfish eye. Nature 435:201–205
Plachetzki DC, Degnan BM, Oakley TH (2007) The origins of novel protein interactions during animal opsin evolution. PLoS ONE 2:e1054
Santillo S, Orlando P, De Petrocellis L, Cristino L, Guglielmotti V, Musio C (2006) Evolving visual pigments: hints from the opsin-based proteins in a phylogenetically old “eyeless” invertebrate. BioSystems 86:3–17
Satterlie RA (1979) Central control of swimming in the cubomedusan jellyfish Carybdea rastonii. J Comp Physiol 133:257–267
Satterlie RA (2002) Neuronal control of swimming in jellyfish: a comparative story. Can J Zool 80:1654–1669
Schalken JJ (1987) The visual pigment rhodopsin: immunohistochemical aspects and induction of experimental autoimmune uveoretinitis. PhD Thesis, University of Nijmegen, The Netherlands
Skogh C, Garm A, Nilsson D-E, Ekström P (2006) The bilaterally symmetric rhopalial nervous system of box jellyfish. J Morphol 267:1391–1405
Suga H, Schmid V, Gehring WJ (2008) Evolution and functional diversity of jellyfish opsins. Curr Biol 18:51–55
Szél A, Tákacs L, Monistori E, Diamantstein T, Vigh-Teichmann I, Röhlich P (1986) Monoclonal antibody recognizing cone visual pigment. Exp Eye Res 43:871–883
Vihtelic TS, Doro CJ, Hyde DR (1999) Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins. Vis Neurosci 16:571–585
Weber C (1982a) Electrical activities of a type of electroretinogram recorded from the ocellus of a jellyfish, Polyorchis penicillatus (Hydromedusae). J Exp Zool 223:231–243
Weber C (1982b) Electrical activity in response to light of the ocellus of the hydromedusan, Sarsia tubulosa. Biol Bull 162:413–422
Yamasu T, Yoshida M (1976) Fine structure of the complex ocelli of a cubomedusan, Tamoya bursaria Haeckel. Cell Tissue Res 170:325–339
Acknowledgements
The authors wish to thank Eva Landgren, Carina Rasmussen, and Rita Wallén for expert technical assistance. This study was supported by the Swedish Research Council (D.-E. Nilsson, #621-2005-2909) and the Carlsberg Foundation (A. Garm; #2005-1-74).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ekström, P., Garm, A., Pålsson, J. et al. Immunohistochemical evidence for multiple photosystems in box jellyfish. Cell Tissue Res 333, 115–124 (2008). https://doi.org/10.1007/s00441-008-0614-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-008-0614-8