Effects of Light Adaptation on the Temporal Resolution of Deep-sea Crustaceans1

Abstract The effects of light adaptation on flicker fusion frequency were examined in the photoreceptors of 13 species of deep-sea crustaceans. Light adaptation produced a significant increase in the maximum critical flicker fusion frequency (CFFmax) in 7 species—all 6 species of euphausiids in the study, and 1 species of oplophorid (Group 1). This is the first example of an increase in temporal resolution due to light adaptation in a deep-sea species. In the other six species—2 oplophorids, 1 pandalid, 1 pasiphaeid, 1 penaeid and 1 sergestid (Group 2)—light adaptation had no effect, or resulted in a decrease in the flicker fusion frequency. The mean dark-adapted CFFmax of the Group 1 species was significantly higher, and the mean response latency significantly lower, than those of the Group 2 species. Possible explanations for these differences include the activity and bioluminescence mode of preferred prey items, as well as the retention of larval/juvenile adaptations in adult eyes.

[1]  Jacques Forest,et al.  Les crevettes profondes de l'Atlantique oriental tropical , 1973 .

[2]  E. Wolf,et al.  THE FLICKER RESPONSE CONTOUR FOR THE CRAYFISH. I , 1939, The Journal of general physiology.

[3]  A. Baker.  The Vertical Distribution of Euphausiids Near Fuerteventura, Canary Islands (‘Discovery’ Sond Cruise, 1965) , 1970, Journal of the Marine Biological Association of the United Kingdom.

[4]  C. Roger.  Recherches sur la situation trophique d'un groupe d'organismes pélagiques (Euphausiacea). I. Niveaux trophiques des espèces , 1973, Marine Biology.

[5]  Friedrich Zettler,et al.  Die Abhängigkeit des Übertragungsverhaltens von Frequenz und Adaptationszustand; gemessen am einzelnen Lichtrezeptor von Calliphora erythrocephala , 1969, Zeitschrift für vergleichende Physiologie.

[6]  S B Laughlin,et al.  Voltage‐activated potassium channels in blowfly photoreceptors and their role in light adaptation. , 1991, The Journal of physiology.

[7]  P. Froneman,et al.  Trophic positions of three euphausiid species from the Prince Edward Islands (Southern Ocean): implications for the pelagic food web structure , 2001 .

[8]  Evon M. O. Abu-Taieh,et al.  Comparative Study , 2020, Definitions.

[9]  F. Wong.  Nature of light-induced conductance changes in ventral photoreceptors of Limulus , 1978, Nature.

[10]  R. B. Pinter,et al.  Frequency and time domain properties of retinular cells of the desert locust (Schistocerca gregaria) and the house cricket (Acheta domesticus) , 1972, Journal of comparative physiology.

[11]  S. B. Laughlin,et al.  Fast and slow photoreceptors — a comparative study of the functional diversity of coding and conductances in the Diptera , 1993, Journal of Comparative Physiology A.

[12]  J. Mauchline,et al.  The biology of euphausiids , 1967 .

[13]  H. Autrum,et al.  Electrophysiological analysis of the visual systems in insects. , 1958, Experimental cell research.

[14]  M. Wiener,et al.  Animal eyes. , 1957, The American orthoptic journal.

[15]  T. Horikoshi,et al.  Comparison of stimulus-response (V-log I) functions in five types of lepidopteran compound eyes (46 species) , 2004, Journal of Comparative Physiology A.

[16]  Peter Herring,et al.  The Biology of the deep ocean , 2002 .

[17]  T. Frank.  Comparative Study of Temporal Resolution in the Visual Systems of Mesopelagic Crustaceans. , 1999, The Biological bulletin.

[18]  E. Gaten,et al.  Temporal resolution in the eyes of marine decapods from coastal and deep-sea habitats , 2000 .

[19]  Michael F. Land,et al.  Optics and Vision in Invertebrates , 1981 .

[20]  J. Case,et al.  Temporal adaptations in visual systems of deep-sea crustaceans , 1995 .

[21]  H. Autrum.  Die Belichtungspotentiale und das Sehen der Insekten (Untersuchungen an Calliphora und Dixippus) , 1950, Zeitschrift für vergleichende Physiologie.

[22]  R. Glantz,et al.  Motion detection and adaptation in crayfish photoreceptors. A spatiotemporal analysis of linear movement sensitivity , 1991, The Journal of general physiology.

[23]  E. Widder,et al.  Comparative study of the spectral sensitivities of mesopelagic crustaceans , 1999, Journal of Comparative Physiology A.

[24]  T. Cronin,et al.  A short-wavelength photoreceptor class in a deep-sea shrimp , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  E. Wolf,et al.  THE FLICKER RESPONSE CONTOUR FOR THE ISOPOD ASELLUS , 1939, The Journal of general physiology.

[26]  A. Hodgkin,et al.  Changes in time scale and sensitivity in the ommatidia of Limulus , 1964, The Journal of physiology.

[27]  V. Andersen,et al.  The diel migrations and vertical distributions of zooplankton and micronekton in the Northwestern Mediterranean Sea. 1. Euphausiids, mysids, decapods and fishes , 1992 .

[28]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[29]  F. Barth,et al.  VISION IN THE CTENID SPIDER CUPIENNIUS SALEI: SPECTRAL RANGE AND ABSOLUTE SENSITIVITY , 1993 .

[30]  A. Hodgkin,et al.  Changes in time scale and sensitivity in turtle photoreceptors , 1974, The Journal of physiology.

[31]  H. Autrum.  Light and Dark Adaptation in Invertebrates , 1981 .

[32]  J. Case,et al.  Visual Spectral Sensitivities of Bioluminescent Deep-sea Crustaceans , 1988 .

[33]  W. McFarland,et al.  The significance of spectral position in the rhodopsins of tropical marine fishes. , 1973, Vision research.

[34]  T. Frank,et al.  Temporal resolution in mesopelagic crustaceans. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  T. Hopkins,et al.  Structure and Trophic Ecology of a Low Latitude Midwater Decapod and Mysid Assemblage , 1994 .

[36]  A. Dubs,et al.  The dynamics of phototransduction in insects , 1984, Journal of Comparative Physiology A.

[37]  J. Childress.  Are there physiological and biochemical adaptations of metabolism in deep-sea animals? , 1995, Trends in ecology & evolution.

[38]  P. Herring,et al.  Regional morphological variations in the compound eyes of certain mesopelagic shrimps in relation to their habitat , 1992, Journal of the Marine Biological Association of the United Kingdom.

[39]  Simon B. Laughlin,et al.  The sensitivities of dragonfly photoreceptors and the voltage gain of transduction , 2004, Journal of comparative physiology.

[40]  W. H. Miller,et al.  Comparative Physiology and Evolution of Vision in Invertebrates , 2011, Handbook of Sensory Physiology.

[41]  S. Bäckström,et al.  The inhibitory effect of glutathione on some processes of animalization. , 1958 .

[42]  P. Herring.  BIOLUMINESCENCE IN THE CRUSTACEA , 1985 .

[43]  D. Ventura,et al.  Comparative study of temporal summation and response form in hymenopteran photoreceptors , 2004, Journal of Comparative Physiology A.

[44]  Roger C. Hardie,et al.  Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly , 1978, Journal of comparative physiology.

[45]  V. Hu.  Relationships between vertical migration and diet in four species of euphausiids 1 , 1978 .

[46]  J. Giske,et al.  Vertical distribution and trophic interactions of zooplankton and fish in Masfjorden, Norway , 1990 .

[47]  M. Barangé.  Vertical migration and habitat partitioning of six euphausiid species in the northern Benguela upwelling system , 1990 .

[48]  P. Herring,et al.  Morphology of the reflecting superposition eyes of larval oplophorid shrimps , 1995, Journal of morphology.

[49]  T. Hopkins,et al.  Trophic strategies of euphausiids in a low-latitude ecosystem , 1994 .

[50]  E. Wolf,et al.  THE FLICKER RESPONSE CONTOUR FOR THE CRAYFISH. I. , 1939 .

[51]  K. Naka,et al.  S‐potentials from colour units in the retina of fish (Cyprinidae) , 1966, The Journal of physiology.

[52]  F. Beyer.  Meganyctiphanes norvegica (M. sars) (Euphausiacea) a voracious predator on Calanus, other copepods, and ctenophores, in oslofjorden, southern Norway , 1992 .

[53]  E. Widder,et al.  Effects of a decrease in downwelling irradiance on the daytime vertical distribution patterns of zooplankton and micronekton , 2002 .

[54]  S B Laughlin,et al.  Matched filtering by a photoreceptor membrane , 1996, Vision Research.

[55]  S. Laughlin,et al.  Temperature and the temporal resolving power of fly photoreceptors , 2000, Journal of Comparative Physiology A.

[56]  J. Welsh,et al.  EYES OF DEEP SEA CRUSTACEANS: I. ACANTHEPHYRIDÆ , 1937 .

[57]  J. Cartes.  Day-night feeding by decapod crustaceans in a deep-water bottom community in the western Mediterranean , 1993, Journal of the Marine Biological Association of the United Kingdom.

[58]  B W Knight,et al.  Adapting bump model for ventral photoreceptors of Limulus , 1982, The Journal of general physiology.

[59]  J. Mauchline.  IX.—The Biology of the Euphausiid Crustacean, Meganyctiphanes norvegica (M. Sars). , 1959 .

[60]  R. Elofsson,et al.  The ontogenetic development of refracting superposition eyes in crustaceans: Transformation of optical design. , 1986, Tissue & cell.

[61]  K. Naka,et al.  S‐potentials from luminosity units in the retina of fish (Cyprinidae) , 1966, The Journal of physiology.

[62]  R. Glantz.  Light adaptation in the photoreceptor of the crayfish, Procambarus clarki. , 1968, Vision research.

[63]  P. Nival,et al.  The diel migrations and vertical distributions of zooplankton and micronekton in the Northwestern Mediterranean Sea. 2. Siphonophores, hydromedusae and pyrosomids , 1992 .

[64]  Rob R. de Ruyter van Steveninck,et al.  The metabolic cost of neural information , 1998, Nature Neuroscience.