Advertisement

Marine Biology

, Volume 156, Issue 7, pp 1359–1373 | Cite as

Eye development in southern calamary, Sepioteuthis australis, embryos and hatchlings

  • Anna Bozzano
  • Patricia M. Pankhurst
  • Natalie A. Moltschaniwskyj
  • Roger Villanueva
Original Paper

Abstract

Eye development, optical properties and photomechanical responses were examined in embryos and hatchlings of the southern calamary, Sepioteuthis australis. This species occurs in shallow coastal waters in Australia and New Zealand, and the egg masses were collected in October and December 2004 from Great Oyster Bay, Tasmania. At the earliest developmental stage the eye of the squid was comprised of a hemispherical cup of undifferentiated neural retina, while presumptive iris cell layers and lentigenic precursor cells enclosed a posterior eye chamber. Differentiation of the proximal and distal processes was observed in correspondence with the cornea development and lens crystallization, and occurred before differentiation of the neural retina, which was complete prior to hatching. Longer photoreceptor distal processes were first observed just prior to hatching in the dorsal-posterior retina. After hatching, this difference was much more evident and higher photoreceptor density was found in the central retina. This indicates that the eye of S. australis at this age uses different retina areas for different visual tasks. Optical sensitivity and resolution suggest that juvenile S. australis are diurnal. This study also found functional photomechanical responses of visual screening pigment migration and pupil constriction in S. australis embryos, although complete functionality of the pupil at this stage was uncertain. However, the pupils of squid aged 2 days closed almost completely under bright conditions, showing that photomechanical responses were highly developed in the juvenile squid. These findings indicate that squid embryos are able to perceive visual stimulation, suggesting an early reliance on vision for survival after hatching.

Keywords

Retina Neural Retina Central Retina Retinal Region Distal Process 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors are deeply grateful to Sue Reilly for her technical histological support at James Cook University. Keith Harrison, Stephen Leporati and Gretta Pecl (Tasmanian Aquaculture and Fisheries Institute) kindly provided unpublished data on the size of Octopus pallidus hatchlings shown in Table 3. We are grateful to the reviewers and the editor for their helpful suggestions and comments on the manuscript. The work undertaken by AB at the University of Tasmania and James Cook University was supported by a Postdoctoral Fellowship from the Spanish Ministry of Science (MECD). AB was also funded by the I3P framework of CSIC. Both sources of AB funds were co-financed by the European Social Foundation. RV was supported by the Spanish Researchers Mobility framework (MECD). PMP had a James Cook University Finfish Aquaculture and Emerging Species Research Advancement Program Grant. This work was supported by the University of Tasmania Merit Grants Scheme awarded to NAM. The experiments comply with the current laws of Australian Animal Welfare.

References

  1. Ali MA (1972) Action spectra of retinomotor and pupillary responses. Vision Res 12:1199. doi: https://doi.org/10.1016/0042-6989(72)90107-1 CrossRefGoogle Scholar
  2. Arnold JM (1965) Normal embryonic stages of the squid, Loligo pealii (Lesueur). Biol Bull 128:23–32. doi: https://doi.org/10.2307/1539386 CrossRefGoogle Scholar
  3. Blaxter JHS, Staines M (1970) Pure-cone retinae and retina-motor responses in larval teleosts. J Mar Biol Assoc UK 50:449–460CrossRefGoogle Scholar
  4. Boletzky SV (2003) Biology of early life stages in cephalopod molluscs. Adv Mar Biol 44:143–203. doi: https://doi.org/10.1016/S0065-2881(03)44003-0 CrossRefGoogle Scholar
  5. Bozzano A, Catalán IA (2002) Ontogenetic changes in the retinal topography of the European hake, Merluccius merluccius: implications for feeding and depth distribution. Mar Biol (Berl) 141:549–559. doi: https://doi.org/10.1007/s00227-002-0840-7 CrossRefGoogle Scholar
  6. Bozzano A, Collin SP (2000) Retinal ganglion cell topography in elasmobranchs. Brain Behav Evol 55:191–208. doi: https://doi.org/10.1159/000006652 CrossRefGoogle Scholar
  7. Budelmann B, Schipp R, Boletzky SV (1997) Cephalopoda. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 6A. Wiley-Liss, New York, pp 119–414Google Scholar
  8. Burnside B, Evans M, Fletcher RT, Chader GJ (1982) Induction of dark-adaptive retinomotor movement (cell elongation) in teleost retinal cones by cyclic adenosine 3′, 5′-monophosphate. J Gen Physiol 79:759–774. doi: https://doi.org/10.1085/jgp.79.5.759 CrossRefGoogle Scholar
  9. Chen DS, Van Dykhuizen G, Hodge J, Gilly WF (1996) Ontogeny of copepod predation in juvenile squid (Loligo opalescens). Biol Bull 190:69–81. doi: https://doi.org/10.2307/1542676 CrossRefGoogle Scholar
  10. Collin SP, Pettigrew JD (1988) Retinal topography in reef teleosts. II. Some species with prominent horizontal streak and high-density areae. Brain Behav Evol 31:283–295. doi: https://doi.org/10.1159/000116595 CrossRefGoogle Scholar
  11. Darmaillacq A-S, Lesimple C, Dickel L (2008) Embryonic visual learning in the cuttlefish, Sepia officinalis. Anim Behav 76:131–134. doi: https://doi.org/10.1016/j.anbehav.2008.02.006 CrossRefGoogle Scholar
  12. Daw NW, Pearlman AL (1974) Pigment migration and adaptation in the eye of the squid, Loligo pealei. J Gen Physiol 63:22–36. doi: https://doi.org/10.1085/jgp.63.1.22 CrossRefGoogle Scholar
  13. Douglas RH, Partridge JC, Marshall NJ (1998) The eyes of deep-sea fish I: lens pigmentation, tapeta and visual pigments. Prog Retin Eye Res 17:597–636. doi: https://doi.org/10.1016/S1350-9462(98)00002-0 CrossRefGoogle Scholar
  14. Douglas RH, Williamson R, Wagner H-J (2005) The pupillary response of cephalopods. J Exp Biol 208:261–265. doi: https://doi.org/10.1242/jeb.01395 CrossRefGoogle Scholar
  15. Evans BI, Browman HI (2004) Variation in the development of the fish retina. In: Govoni JJ (ed) Development of form and function in fishes and the question of larval adaptation. Am Fish Soc Symp 40:145–166Google Scholar
  16. Gleadall IA, Ohtsu K, Gleadall E, Tsukahara Y (1993) Screening-pigment migration in the octopus retina includes control by dopaminergic efferents. J Exp Biol 185:1–16Google Scholar
  17. Groeger G, Cotton PA, Williamson R (2005) Ontogenetic changes in the visual acuity of Sepia officinalis measured using the optomotor response. Can J Zool Rev Can Zool 83:274–279. doi: https://doi.org/10.1139/z05-011 CrossRefGoogle Scholar
  18. Haacke C, Heß M, Melzer RR, Gebhart H, Smola U (2001) Fine structure and development of the retina of the grenadier anchovy Coilia nasus (Engraulididae, Clupeiformes). J Morphol 248:41–55. doi: https://doi.org/10.1002/jmor.1019 CrossRefGoogle Scholar
  19. Hagins WA, Liebman PA (1962) Light-induced pigment migration in the squid retina. Biol Bull 123:498Google Scholar
  20. Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, CambridgeGoogle Scholar
  21. Hughes A (1977) The topography of vision in mammals of contrasting lifestyles: comparative optics and retinal organization. In: Austrum H, Joung R, Loewenstein WR, MacKay DM, Teuber HL (eds) Handbook of sensory physiology, vol VII/5. Springer, New York, pp 613–756Google Scholar
  22. Inada H (1996) Retinomotor response and retinal adaptation of Japanese common squid Todarodes pacificus at capture with jigs. Fish Sci 62:663–669CrossRefGoogle Scholar
  23. Johnsen S (2000) Transparent animals. Sci Am 280:80–89CrossRefGoogle Scholar
  24. Johnson C (2006) The digestive and visual development of the juvenile cephalopods Sepioteuthis australis and Euprymna tasmanica. Ph.D. thesis, University of TasmaniaGoogle Scholar
  25. Kier CK, Chamberlain SC (1990) Dual control for screening pigment movement in photoreceptors of the Limulus lateral eye: circadian efferent input and light. Vis Neurosci 4:237–255CrossRefGoogle Scholar
  26. Kvenseth AM, Pittman K, Helvik JV (1996) Eye development in Atlantic halibut (Hippoglossus hippoglossus): differentiation and development of the retina from early yolk sac stages through metamorphosis. Can J Fish Aquat Sci 53:2524–2532. doi: https://doi.org/10.1139/cjfas-53-11-2524 CrossRefGoogle Scholar
  27. Land MF (1981) Optics and vision in invertebrates. In: Autrum H (ed) Handbook of sensory physiology. Springer, Berlin, pp 471–592Google Scholar
  28. Land MF (1984) Molluscs. In: Ali MA (ed) Photoreception and vision in invertebrate. Plenum Press, New York, pp 699–725CrossRefGoogle Scholar
  29. Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press Inc, New YorkGoogle Scholar
  30. Lee PG, Turk PE, Yang WT, Hanlon RT (1994) Biological characteristics and biomedical applications of the squid Sepioteuthis lessoniana cultured through multiple generations. Biol Bull 186:328–341. doi: https://doi.org/10.2307/1542279 CrossRefGoogle Scholar
  31. Mäthger LM, Denton EJ (2001) Reflective properties of iridophores and fluorescent ‘eyespots’ in the loliginid squid Alloteuthis subulata and Loligo vulgaris. J Exp Biol 204:2103–2118PubMedGoogle Scholar
  32. Messenger JB (1981) Comparative physiology of vision in molluscs. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6C. Springer, Berlin, pp 93–200Google Scholar
  33. Moltschaniwskyj NA, Pecl GT (2003) Small-scale spatial and temporal patterns of egg production by the temperate loliginid squid Sepioteuthis australis. Mar Biol (Berl) 142:509–516CrossRefGoogle Scholar
  34. Moltschaniwskyj NA, Pecl GT (2007) Spawning aggregations of squid (Sepioteuthis australis) populations: a continuum of ‘microcohorts’. Rev Fish Biol Fish 17:183–195. doi: https://doi.org/10.1007/s11160-006-9025-7 CrossRefGoogle Scholar
  35. Moltschaniwskyj NA, Steer MA (2004) Spatial and seasonal variation in reproductive characteristics and spawning of southern calamary (Sepioteuthis australis): spreading the mortality risk. ICES J Mar Sci 61:921–927. doi: https://doi.org/10.1016/j.icesjms.2004.06.007 CrossRefGoogle Scholar
  36. Moltschaniwskyj NA, Hall K, Lipinski MR, Marian JEAR, Nishiguchi M, Sakai M, Shulman DJ, Sinclair B, Sinn DL, Staudinger M, Van Gelderen R, Villanueva R, Warnke K (2007) Ethical and welfare considerations when using cephalopods as experimental animals. Rev Fish Biol Fish 17:455–476. doi: https://doi.org/10.1007/s11160-007-9056-8 CrossRefGoogle Scholar
  37. Muntz WRA (1977) Pupillary response of cephalopods. Symp Zool Soc Lond 38:277–285Google Scholar
  38. Muntz WRA, Gwyther J (1988) Visual acuity in Octopus pallidus and Octopus australis. J Exp Biol 134:119–129Google Scholar
  39. Munz FW, McFarland WN (1977) Evolutionary adaptations of fishes to the photic environment. In: Crescitelli F (ed) Handbook of sensory physiology, vol VI/5. Springer, Berlin, pp 193–274Google Scholar
  40. Neave DA (1984) The development of visual acuity in larval plaice (Pleuronectes platessa L.) and turbot (Scophthalmus maximus L.). J Exp Mar Biol Ecol 78:167–175. doi: https://doi.org/10.1016/0022-0981(84)90077-7 CrossRefGoogle Scholar
  41. Nicol JAC (1989) The eyes of fishes. Oxford University Press, OxfordGoogle Scholar
  42. Nixon M, Mangold K (1998) The early life of Sepia officinalis, and the contrast with that of Octopus vulgaris (Cephalopoda). J Zool (Lond) 245:407–421. doi: https://doi.org/10.1111/j.1469-7998.1998.tb00115.x CrossRefGoogle Scholar
  43. Nixon M, Young JZ (2003) The brains and lives of cephalopods. Oxford University Press, OxfordGoogle Scholar
  44. Norman M (2000) Cephalopods. A world guide. Conch Books Press, HackenheimGoogle Scholar
  45. Packard A (1969) Visual acuity and eye growth in Octopus vulgaris (Lamarck). Monitore Zool Ital (N.S.) 3:19–32Google Scholar
  46. Packard A (1972) Cephalopods and fish: the limit of convergence. Biol Rev Camb Philos Soc 47:241–307. doi: https://doi.org/10.1111/j.1469-185X.1972.tb00975.x CrossRefGoogle Scholar
  47. Pankhurst PM, Eagar R (1996) Changes in visual morphology through life history stages of the New Zealand snapper, Pagrus auratus. N Z J Mar Freshw Res 30:79–90CrossRefGoogle Scholar
  48. Pankhurst PM, Pankhurst NW, Montgomery JC (1993) Comparison of behavioural and morphological measures of visual acuity during ontogeny in a teleost fish, Forterygion varium, Tripterygiidae (Forster, 1801). Brain Behav Evol 42:178–188. doi: https://doi.org/10.1159/000114151 CrossRefGoogle Scholar
  49. Pecl G (2001) Flexible reproductive strategies in tropical and temperate Sepioteuthis squids. Mar Biol (Berl) 138:93–101. doi: https://doi.org/10.1007/s002270000452 CrossRefGoogle Scholar
  50. Pecl GT (2004) The in situ relationships between season of hatching, growth and condition in the southern calamary, Sepioteuthis australis. Mar Freshw Res 55:429–438. doi: https://doi.org/10.1071/MF03150 CrossRefGoogle Scholar
  51. Pecl GT, Moltschaniwskyj NA (2006) Life history of a short-lived squid (Sepioteuthis australis): resource allocation as a function of size, growth, maturation, and hatching season. ICES J Mar Sci 63:995–1004Google Scholar
  52. Schaeffel F, Murphy CJ, Howland HC (1999) Accommodation in the cuttlefish (Sepia officinalis). J Exp Biol 202:3127–3134PubMedGoogle Scholar
  53. Sivak JG, West JA, Campbell MC (1994) Growth and optical development of the ocular lens of the squid (Sepioteuthis lessoniana). Vision Res 34:2177–2187. doi: https://doi.org/10.1016/0042-6989(94)90100-7 CrossRefGoogle Scholar
  54. Steer MA, Moltschaniwskyj NA, Gowland FC (2002) Temporal variability in embryonic development and mortality in the southern calamary Sepioteuthis australis: a field assessment. Mar Ecol Prog Ser 243:143–150. doi: https://doi.org/10.3354/meps243143 CrossRefGoogle Scholar
  55. Steer MA, Moltschaniwskyj NA, Jordan AR (2003a) Embryonic development of southern calamary (Sepioteuthis australis) within the constraints of an aggregated egg mass. Mar Freshw Res 54:217–226. doi: https://doi.org/10.1071/MF02107 CrossRefGoogle Scholar
  56. Steer MA, Pecl GT, Moltschaniwskyj NA (2003b) Are bigger calamary Sepioteuthis australis hatchlings more likely to survive? A study based on statolith dimensions. Mar Ecol Prog Ser 261:175–182. doi: https://doi.org/10.3354/meps261175 CrossRefGoogle Scholar
  57. Suzuki T, Takahashi H (1988) Response of the retina of flying squid Sthenoteuthis oualaniensis (Lesson) to light changes. Bull Fac Fish Hokkaido Univ 39:21–26Google Scholar
  58. Suzuki T, Inada H, Takahashi H (1985) Retinal adaptation of Japanese common squid Todarodes pacificus Steenstrup to light changes. Bull Fac Fish Hokkaido Univ 36:191–199Google Scholar
  59. Sweeney AM, Steven HDH, Johnsen S (2007) Comparative visual acuity of coleoid cephalopods. Integr Comp Biol 47:808–814. doi: https://doi.org/10.1093/icb/icm092 CrossRefGoogle Scholar
  60. Takayama T, Inada H, Watanabe T (1998) Retinomotor response and iris function of Neon Flying squid Ommastrephes bartrami to lighting. Nippon Suisan Gakkai Shi 64:631–635CrossRefGoogle Scholar
  61. Tasaki I, Nakaye T (1984) Rapid mechanical responses of the dark adapted squid retina to light pulses. Science 223:411–413. doi: https://doi.org/10.1126/science.6691153 CrossRefGoogle Scholar
  62. Villanueva R, Nozais C, Boletzky SV (1996) Swimming behaviour and food searching in planktonic Octopus vulgaris Cuvier from hatching to settlement. J Exp Mar Biol Ecol 208:169–184. doi: https://doi.org/10.1016/S0022-0981(96)02670-6 CrossRefGoogle Scholar
  63. Villanueva R, Moltschaniwskyj NA, Bozzano A (2007) Abiotic influences on embryo growth: statoliths as experimental tools in the squid early life history. Rev Fish Biol Fish 17:101–110. doi: https://doi.org/10.1007/s11160-006-9022-x CrossRefGoogle Scholar
  64. Warrant E (1999) Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation. Vision Res 39:1611–1630. doi: https://doi.org/10.1016/S0042-6989(98)00262-4 CrossRefGoogle Scholar
  65. Warrant E, Nilsson D-E (2006) Invertebrate vision. Cabridge University Press, New YorkGoogle Scholar
  66. Watanuki N, Kawamura G, Kaneuchi A, Iwashita T (2000) Role of vision in behaviour, visual field, and visual acuity of cuttlefish Sepia esculenta. Fish Sci 66:417–423. doi: https://doi.org/10.1046/j.1444-2906.2000.00068.x CrossRefGoogle Scholar
  67. Wentworth SL, Muntz WRA (1992) Development of the eye and optic lobe of Octopus. J Zool (Lond) 227:673–684CrossRefGoogle Scholar
  68. Yamamoto M, Takasu N, Uragami I (1985) Ontogeny of the visual system in the cuttlefish, Sepiella japonica.2. Intramembrane particles, histofluorescence, and electrical responses in the developing retina. J Comp Neurol 232:362–371. doi: https://doi.org/10.1002/cne.902320308 CrossRefGoogle Scholar
  69. Yoshida MK, Ohtsu K, Nakaye T (1976) Development of the cuttlefish retina. In: Yamada E, Mishima S (eds) The structure of the eye. Maruzen, Tokyo, pp 215–221Google Scholar
  70. Young JZ (1963) Light- and dark- adaptation in the eyes of some cephalopods. Proc Zool Soc Lond 140:255–272CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Anna Bozzano
    • 1
    • 3
  • Patricia M. Pankhurst
    • 2
  • Natalie A. Moltschaniwskyj
    • 3
  • Roger Villanueva
    • 1
    • 3
  1. 1.Institut de Ciències del Mar (CSIC)BarcelonaSpain
  2. 2.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia
  3. 3.National Centre for Marine Conservation and Resource Sustainability, Australian Maritime CollegeUniversity of TasmaniaLauncestonAustralia

Personalised recommendations