Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-16T19:52:11.168Z Has data issue: false hasContentIssue false

Early development of eye and retina in lanternfish larvae

Published online by Cambridge University Press:  06 September 2007

A. BOZZANO
Affiliation:
Institut de Ciències del Mar (CSIC), Barcelona, Spain
P.M. PANKHURST
Affiliation:
School of Marine Biology and Aquaculture, James Cook University, Townsville, Queensland, Australia
A. SABATÉS
Affiliation:
Institut de Ciències del Mar (CSIC), Barcelona, Spain

Abstract

The morphological characteristics of the eyes and the retinae of lanternfish larvae of Lampanyctus crocodilus, Benthosema glaciale, and Myctophum punctatum were analyzed in pre-flexion, flexion, and post-flexion stages. Pre-flexion larvae of L. crocodilus, the species with the shallowest depth distribution, had spherical eyes located antero-laterally on a strongly laterally-compressed head, suggesting a forward binocular visual field. B. glaciale and M. punctatum larvae live deeper in the water column and had eyes elongated in the dorsal-ventral plane. The eyes of B. glaciale were prominent, projecting slightly outward from a laterally-compressed head, suggesting a strongly laterally-directed visual field. M. punctaum had stalked elongated eyes projecting from a dorso-ventrally flattened head. The eyes can be freely rotated allowing lateral, anterior and dorsally-directed vision. A prominent choroidal gland was situated beneath the ventral portion of the eye in M. punctatum and B. glaciale, while a smaller gland was present in the dorsal and ventral portions of the eye of L. crocodilus. In pre-flexion stage larvae, the retina of all three species was differentiated with numerous rod photoreceptors in the peripheral retinal areas and fewer cone photoreceptors mainly distributed in the central retina. This distribution suggests concomitant enhancement of scotopic sensitivity in the vertical visual plane and improved photopic acuity in the lateral and forward visual directions. The concurrent development of cones and rods, as observed in the pre-flexion stage of myctophid larvae, is consistent with meeting the special demands of visual planktivory in sub-surface waters. During larval development a gradual increase of ROS length was also accompanied by a progressive loss of cones that were almost totally absent in post-flexion larvae. This can be interpreted as an adaptive response to an impending deep mesopelagic adult life.

Type
Research Article
Copyright
© 2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ali, M.A. & Klyne, M.A. (1985). Phylogeny and functional morphology of the vertebrate retina. In: Vertebrate Morphology, ed. Duncker/Fleiscer. pp. 633648. Stuttgart: Gustav Fisher Verlag.
Barnett, C.H. (1951). The structure and function of the choroidal gland of teleostean fish. Journal of Anatomy 85, 113119.Google Scholar
Blaxter, J.H.S. & Jones, M.P. (1967). The development of the retina and retinomotor responses in the herring. Journal of the Marine Biological Association of the United Kingdom 47, 677679.CrossRefGoogle Scholar
Blaxter, J.H.S. & Staines, M. (1970). Pure-cone retinae and retinomotor responses inlarval teleosts. Journal of the Marine Biological Association of the United Kingdom 50, 449460.CrossRefGoogle Scholar
Blaxter, J.H.S. (1965). The feeding of herring larvae and their ecology in relation to feeding. California Cooperative Oceanic Fisheries Investigations. http://www.calcofi.org/newhome/publications/CalCOFI_Reports/v10/pdfs/Vol_10_Blaxter.pdf
Blaxter, J.H.S. (1986). Development of sense organs and behavior of teleost larvae with special reference to feeding and predator avoidance. Transactions of the American Fisheries Society 115, 98114.Google Scholar
Blaxter, J.H.S. (1988). Sensory performance, behaviour, and ecology of fish. In Sensory Biology of Aquatic Animals, eds. Atema, J., Fay, R.R., Popper, A.N. & Tavolga, W.N., pp. 203232. New York: Springer-Verlag.
Cobcroft, J.M. & Pankhurst, P.M. (2003). Sensory organ development in cultured striped trumpeter larvae Latris lineata: Implications for feeding behaviour. Marine and Freshwater Research 54, 669684.CrossRefGoogle Scholar
Cobcroft, J.M. & Pankhurst, P.M. (2006). Visual field of cultured strimped trumpeter Latris lineata (Teleostei) larvae feeding on rotifer prey. Marine and Freshwater Behaviour and Physiology 39, 193208.CrossRefGoogle Scholar
Collin, S.P. (1988). The retinal structure of the shovel-nosed ray, Rhinobatos batillum (Rhinobatidae). Morphology and quantitative analysis of ganglion, amacrine and bipolar cell populations. Experimental Biology 47, 195207.Google Scholar
Collin, S.P. & Pettigrew, J.D. (1988). Retinal ganglion cell topography in teleosts: A comparison between Nissl stained material and retrograde labelling from the optic nerve. Journal of Comparative Neurology 276, 412422.CrossRefGoogle Scholar
Eastman, J.T. (1993). Antarctic Fish Biology: Evolution in a unique environment. San Diego: Academic Press.
Guma'a, S.A. (1982). Retinal development and retinomotor responses in perch, Perca fluviatilis L. Journal of Fish Biology 20, 611618.CrossRefGoogle Scholar
Hirt, B. & Wagner, H-J. (2005). The organization of the inner retina in a pure-rod deep-sea fish. Brain, Behavior and Evolution 65, 157167.CrossRefGoogle Scholar
Hobson, E.S. & Chess, J.R. (1986). Relationships among fishes and their prey in a nearshore sand community off southern California. Environmental Biology of Fish 17, 201226.CrossRefGoogle Scholar
Hopkins, T.L. & Gartner, J.J.V. (1992). Resource-partitioning and predation impact of a low-latitude myctophid community. Marine Biology 114, 185197.CrossRefGoogle Scholar
Job, S.D. & Bellwood, D.R. (1996). Visual acuity and feeding in larval P. biaculeatus. Journal of Fish Biology 48, 952963.Google Scholar
Job, S.D. & Bellwood, D.R. (2000). Light sensitivity in larval fish: Implications for vertical zonation in the pelagic zone. Limnology and Oceanography 45, 362371.CrossRefGoogle Scholar
Johnsen, S. (2000). Transparent animals. Scientific American February, 8089.CrossRefGoogle Scholar
Kawamura, G., Tsuda, R., Kumai, H. & Ohashi, S. (1984). The visual cell morphology of Pagrus major and its adaptive changes with shift from pelagic to benthic habitats. Bulletin of the Japanese society of Scientific Fisheries 50, 19751980.CrossRefGoogle Scholar
Kendall, Jr., A.W., Ahlstrom, E.H. & Moser, H.G. (1984). Early life history stages of fishes and their characters. In Ontogeny and systematic of fishes, eds. Moser, H.G., Richards, W.J., Cohen, D.M., Fahay, M.P., Kendall, A.W. & Richardson, S.L., pp. 1122. Lawrence, KS: Allen Press Inc.
Kotrschal, K., Adam, H., Brandstätter, R., Junger, H., Zaunreiter, M. & Goldschmid, A. (1990). Larval size constraints determine directional ontogenetic shift in the visual system of teleosts. Zeitschrift fuer Zoologische Systematik und Evolutionsforschung 28, 166182.Google Scholar
Lara, M.R. (2001). Morphology of the eye and visual acuities in the settlement-intervals of some coral reef fishes (Labridae, Scaridae). Environmental Biology of Fishes 62, 365378.CrossRefGoogle Scholar
Leis, J.M. (1991). The pelagic stage of reef fishes: The larval biology of coral reef fishes. In The Ecology of Fish on Coral Reefs, ed. Sale, P.F., pp. 183230. San Diego: Academic Press.CrossRef
Locket, N.A. (1977). Adaptations to deep-sea environment. In The Visual System in Vertebrates. Handbook of Sensory Physiology, Vol. 8, 5th edition, ed. Crescitelli, F., pp 67192. NewYork: Springer.CrossRef
Locket, N.A. (1980). Variation of architecture with size in the multiple-bank retina of a deep-sea teleost, Chaoliodus sloanei. Proceeding of the Royal Society of London B 208, 223242.CrossRefGoogle Scholar
Mack, A.F., Süssmann, C., Hirt, B. & Wagner, H.J. (2004). Displaced amacrine cells disappear from the ganglion cell layer in the central retina of adult fish during growth. Investigative Ophthalmology and Visual Science 45, 37493755.CrossRefGoogle Scholar
Margulies, D. (1997). Development of the visual system and inferred performance capabilities of larval and early juvenile scombrids. Marine and Freshwater Behaviour and Physiology 30, 7598.CrossRefGoogle Scholar
Matsuoka, M. (1999). Histological characteristics and development of the retina in the Japanese sardine Sardinopsis melanostictus. Fisheries Science 65, 224229.CrossRefGoogle Scholar
Miller, T.J., Crowder, L.B. & Rice, J.A. (1993). Ontogenetic changes in behavioural and histological measures of visual acuity in three species of fish. Environmental Biology of Fishes 37, 18.Google Scholar
Moku, M., Mori, K. & Watanabe, Y. (2004). Shrinkage in the body length of myctophid fish (Diaphus slender-type spp.) larvae with various preservatives Copeia 3, 647651.Google Scholar
Moku, M., Iishimaru, K. & Kawaguchi, K. (2001). Growth of larval and juvenile Diaphus theta (Pisces: Myctophidae) in the transitional waters of the western North Pacific. Ichthyological Research 48, 385390.CrossRefGoogle Scholar
Moser, H.G. & Ahlstrom, E.H. (1970). Development of lanternfishes (family Myctophidae) in the California Current. Part I. Species with narrow-eyed larvae. Bulletin of the Los Angeles County Museum of Natural History Science 7.
Moser, H.G. (1981). Morphological and functional aspects of marine fish larvae. In Marine Fish Larvae: Morphology, Ecology and Relation to Fisheries, ed. Lasker, R., pp. 8931. Seattle, WA: University of Washington Press.
Moser, H.G. & Ahlstrom, E.H. (1974). Role of larval stages in systematic investigations of marine teleosts: The Myctophidae, a case study. Fishery Bulletin 72, 391413.Google Scholar
Moser, H.G., Richards, W.J., Cohen, D.M., Fahay, M.P., Kendall, A.W. & Richardson, S.L. (1984). Ontogeny and Systematics of Fishes. Lawarence, KS: Allen Press Inc.
Neave, D.A. (1984). The development of the retinomotor reactions in larval plaice (Pleuronectes platessa, L.) and turbot (Scophthalmus maximum, L.). Journal Experimental Marine Biology and Ecology 76, 167175.Google Scholar
Nicol, J.A.C. (1989). The Eyes of Fishes. Oxford: Clarendon Press.
Nirenberg, S. & Meister, M. (1997). The light response of retinal ganglion cells is truncated by a displaced amacrine circuit. Neuron 18, 637650.CrossRefGoogle Scholar
O'Day, W.T. & Fernandez, H.R. (1976). Vision in the lanternfish Stenobrachius leucopsaurus (Myctophidae). Marine Biology 37, 187195.CrossRefGoogle Scholar
Olivar, M.P & Sabatés, A. (1997). Vertical distribution of fish larvae in the north-west Mediterranean Sea in spring. Marine Biology 129, 289300.CrossRefGoogle Scholar
Olivar, M.P., Rubíes, P. & Salat, J. (1992). Horizontal and vertical distribution patterns of ichthyoplankton under intense upwelling regimes off Namibia. South African Journal of Marine Science 12, 7182.CrossRefGoogle Scholar
Olivar, M.P., Sabatés A., Abelló P. & García M. (1998). Transitory hydrographic structures and distribution of fish larvae and neustonic crustaceans in the north-western Mediterranean. Oceanologica Acta 21, 95104.CrossRefGoogle Scholar
Omura, Y., Uematsu, K., Tachiki, H., Furukawa, K. & Satoh, H. (1997). Cone cells appear also in the retina of eel larvae. Fisheries Science 63, 10521053.CrossRefGoogle Scholar
Pankhurst, N.W. (1984). Retinal development in larval and juvenile European eel, Anguilla anguilla (L.). Canadian Journal of Zoology 62, 335343.CrossRefGoogle Scholar
Pankhurst, N.W. (1987). Intra- and interspecific changes in retinal morphology among mesopelagic and demersal teleosts from the slope water of New Zeland. Environmental Biology of Fishes 19, 269280.CrossRefGoogle Scholar
Pankhurst, P.M. & Eagar, R. (1996). Changes in visual morphology through life history stages of the New Zealand snapper, Pagrus auratus. New Zealand Journal of Marine and Freshwater Research 30, 7990.CrossRefGoogle Scholar
Pankhurst, P.M. & Hilder, P.E. (1998). Effect of light intensity on feeding of striped trumpeter Latris lineate larvae. Marine and Freshwater Research 49, 363368.CrossRefGoogle Scholar
Pankhurst, P.M. (1994). Age-related changes in the visual acuity of larvae of New Zealand snapper, Pagrus auratus. Journal of the Marine Biological Association of the United Kingdom 74, 337349.CrossRefGoogle Scholar
Pankhurst, P.M. (2007) Mechanoreception. In Fish Larvae Physiology, ed. Finn, R.N. Science Publisher Inc.
Pankhurst, P.M., Pankhurst, N.W. & Montgomery, J.C. (1993). Comparison of behavioural and morphological measures of visual acuity during ontogeny in the teleosts fish, Forsterygion varium, Tripterygiidae (Foster, 1801). Brain, Behaviour and Evolution 42, 178188.Google Scholar
Paxton, J.R. (1972). Osteology and relationships of the lanternfishes (Family Myctophidae). Bulletin of the Los Angeles City of the Musum of the Natural History Science 13, 81.Google Scholar
Poling, K.R. & Fuiman, L.A. (1998). Sensory development and its relation to habitat change in three species of scianidae. Brain Behavior and Evolution 52, 270284.CrossRefGoogle Scholar
Powers, M.K. & Raymond, P.A. (1990). Development of the visual system. In The Visual System of Fishes, eds. Douglas & R.H., Djamgoz M.B.A., pp. 419442. London, UK: Chapman and Hall.CrossRef
Rodríguez, A. & Gisbert, E. (2002). Eye development and the role of vision during Siberian sturgeon early ontogeny. Journal of Applied Ichthyology 18, 280285.CrossRefGoogle Scholar
Sabatés, A. (2004). Diel variability of fish larvae distribution during the winter mixing period in the NW Mediterranean. ICES Journal of Marine Science 61, 12431252.CrossRefGoogle Scholar
Sabatés, A. & Saiz, E. (2000). Intra- and interspecific variability in prey size and niche breadth of myctophiform fish larvae. Marine Ecology Progress Series 201, 261271.CrossRefGoogle Scholar
Sabatés, A., Bozzano, A. & Vallvey I. (2003). Feeding pattern and the visual light environment in myctophid fish larvae. Journal of Fish Biology 63, 14761490.CrossRefGoogle Scholar
Sameoto, D.D. (1988). Feeding of lanternfish Benthosema glaciale off the Nova Scotia shelf. Marine Ecology Progress Series 44, 113129.CrossRefGoogle Scholar
Sandy, J.M. & Blaxter, J.H.S. (1980). A study of retinal development in larval herring and sole. Journal of the Marine Biology Association of the United Kingdom 60, 5971.CrossRefGoogle Scholar
Sassa, C. & Kawaguchi, K. (2005). Larval feeding habits of Diaphus theta, Protomyctophum thompsoni and Tarletonbeania taylori (Pisces: Myctophidae) in the transition region of the western North Pacific. Marine Ecology Progress Series 298, 261276.CrossRefGoogle Scholar
Shand, J. (1997). Ontogenetic changes in retinal structure and visual acuity: a comparative study of coral-reef teleosts with differing post-settlement lifestyles. Environmental Biology of Fishes 49, 307322.CrossRefGoogle Scholar
Shand, J., Archer, M.A. & Collin, S.P. (1999a). Ontogenetic changes in the retinal photoreceptor mosaic in a fish, the black bream, Acanthopagrus butcheri. The Journal of Comparative Neurology 412, 203217.Google Scholar
Shand, J., Døving, K.B. & Collin, S.P. (1999b). Optics of the developing fish eye: Comparisons of Matthiessen's ratio and the focal length of the lens in the black bream Acanthopagrus butcheri. Vision Research 39, 10711078.Google Scholar
Wagner, H.J., Frohlich, E., Negishi, K. & Collin, S.P. (1998). The eyes of deep-sea fish. II. Functional morphology of the retina. Progress in Retinal and Eye Research 17, 637685.CrossRefGoogle Scholar
Weihs, D. & Moser, H.G. (1981). Stalked eyes as an adaptation towards more efficient foraging in marine fish larvae. Bulletin of Marine Science 3, 3136.Google Scholar