UV vision and photoreception

UV vision has been documented in a variety of terrestrial organisms including insects, birds, amphibians, reptiles, and mammals [53-55]. It is therefore not surprising that many aquatic organisms also perceive light in the UV spectrum. Most UV photoreceptors in aquatic organisms have been described in fish species; however, UV photoreceptors have also been reported in bacteria and algae as well as some species of protozoans, annelids, cnidarians, and crustaceans (Table 1).

14.4.1 Relation to habitat and age

Many UV photoreceptors have a maximum absorbance peak in the UV-A range but UV-B photoreceptors have been documented in some species (Table 1). One explanation for the rarity of UV-B vision is that UV-B radiation is potentially more damaging to the eye. For instance, cataracts are reported to occur in several fish species inhabiting shallow waters [56]. Seeing in the UV-A may therefore be less detrimental to the eye; however, prolonged exposure to UV-A radiation may also be potentially damaging, albeit less than UV-B. In addition, since eyes are photon-, not energy-counters, seeing in the UV-A provides more light than in the UV-B. However, visible light provides more photons than UV, making UV vision a curious trait (See section 14.4.2).

Some authors have suggested that UV photoreceptors vary with habitat such that peak absorbance correlates with wavelengths present in their photic environment [57-59]. In some cases, species such as the rudd Scardinius erythroph-thalmus [60] and the brown trout, Salmo trutta [61], display seasonal changes in spectral sensitivity that correspond to seasonal changes in the photic environment associated with daylength and temperature. Most of these shifts are in the longer wavelengths with shorter wavelength sensitivity remaining the same [62]. Behavior shifts are also suggested to contribute to shifts in spectral sensitivity, such as foraging at the surface during summer months and in deeper strata during winter months [60].

UV photoreceptors in some fish species not only vary with habitat but with age as well. Many fish species, such as Lepomis gibbosus, Perca flavescens, and Salmo sp., possess UV photoreceptors as larvae but lose them with maturity [63,64]. This loss of UV photoreception coincides with a habitat shift from the surface waters to more demersal waters in addition to a change in diet from small to larger zooplankton prey and/or fish [63-65]. In some species of salmonoids, however, UV photoreceptors disappear during earlier life history stages and reappear in adults. For example, ultraviolet cones and UV sensitivity in the sockeye salmon, Oncorhynchus nerka, diminished during smoltification and reappeared at the late juvenile or adult stage [66]. The author also noted that the arrangement of the UV cones in the retina of the adult sockeye salmon was similar to those of saltwater salmon, 0. tshawytsha and 0. keta, collected while migrating back to natal streams or spawning in streams. This suggests that UV photoreceptors may assist in navigation during migrations. Goldfish and species of cyprinids retain their UV photoreceptors as adults. These species experience little to no change in habitat or diet and therefore a change in the spectral sensitivity of their photoreceptors would not be expected. Ontogenetic changes in spectral sensitivity among aquatic species other than fish are less well known.

14.4.2 Adaptive significance

The adaptive role of UV vision is not completely understood. In some organisms, UV photoreceptors assist in navigation and orientation, associated with the e-vector of the polarized light field [67,68], while in others they have been demonstrated to enhance color discrimination [55,69]. Recognition and communication between conspecifics and mates at UV wavelengths has been speculated in species of coral reef fish [20,27], Recently, the epithelial mucus of several marine fish species was found to contain UV-absorbing compounds, which may be seen by fish with UV vision [70], Consequently, it is suggested that one fish may see another as "tanned" or "untanned", potentially playing an important role in visual communication.

UV photoreceptors are also thought to help in the detection of prey during visual foraging by enhancing prey contrast [20,63,64]. Planktonic prey, such as Daphnia and Diaptomus, absorb solar radiation in the near-UV [71]. Because of this, these zooplankton may appear darker than their surrounding background. In addition, planktonic prey also scatter light and may appear lighter or darker depending on the direction of illumination, shape, and refractive index differences (Figure 5) [71]. Larvae of the phantom midge Chaoborus trivittatus reflect blue light greater than longer wavelength red light and it is predicted that the reflectance curve will shift towards shorter wavelengths as the angle of incidence increases [72]. These differences in reflectance were hypothesized to reduce visibility to visual feeding fish and therefore reduce mortality. This would be true for fish without UV photoreceptors, but increased reflectance at shorter wavelengths may increase visibility to foragers with UV vision.

Laboratory experiments have demonstrated that larval fish do feed better in

Table 1. Survey of the distribution of UV photoreceptors among aquatic organisms. (This list is not all-inclusive.) Microspectrophotometry is abbreviated as MSP.

Organism

Method

Wavelength of maximum response or absoption (nm)

Reference

Bacteria

Mutant, Escherichia coli

behavior

396-450

[89]

Purple eubacterium, Ecotothiorhodospira halophila

behavior

N/A

[90]

Saltwater bacterium, Halobacterium halbium

behavior

280, 370

[91]

Phytoplankton

Cyanobacterium, Chologloeopsis

physiology, MAAs induction

310

[76]

Green alga rhizoid, Bryopsis plumosa

physiology, MAAs induction

260, 310

[92]

Protozoans

Ciliates

Chlamydodon mnemosyne

behavior

360

[93]

Blepharisma japonicum

behavior

N/A

[33]

Annelids

Alciopid worm, Torrea Candida

electrophysiology

400

[77]

Cnidarians

Sea anemone, Anthopleura xanthogrammica

behavior

360

[91]

Molluscs

Giant clam, Tridacna sp.

electrophysiology

360

[94]

Crustaceans

Cladoceran, Daphnia magna

behavior

348

[75]

Harpacticoid copepod, Tigriopus californicus

behavior

N/A

[44]

Ectoparasitic copepod, Lepeophtheirus salmonis

behavior

352-400

[95]

Crayfish, Procambarus clarkia

MSP

440

[53]

Mantis Shrimp, Pseudosquilla ciliate

MSP

400

[96]

Deep sea oplophroid shrimp

Systellaspis debilis

behavior

410

[35]

Janicella spinacauda

electrophysiology

370

Oplophorus spinosus

Oplophorus gracilirostris

Estuarine intertidal crabs

Sesarma reticulatum

S. cinereum

Pinnotheres ostreum

Prawn, Palaemonetes vulgaris

Spiny lobster, Panulirus argus

Horseshoe crab, Limulus polyphemus

Fishes

Clupeomorpha

Northern anchovy, Engraulis mordax

Ostariophysi

Minnow, Phoxinus laevis

Roach, Rutilus rutilus

Goldfish, Carassius auratus

Carp, Cyprnus carpio

Danio, Danio aequipinnatus

Eastern Golden Shiner, Notemigonus crysoleucas

Rudd, Scardinius erythrophthalmus

Japanese dace, Tribolodon hakonensis

Salmoniformes

Rainbow trout, Oncorhynchus mykiss Brown trout, Salmo trutta Atlantic salmon, Salmo salar Sockeye salmon, Oncorhynchus nerka Acanthopterygii Guppy, Poecilia latipinna Guppy, P. reticulata Sunfish, Lepomis spp. Yellow perch, Perca flavescens Atlantic Silverside, Menidia menidia Killifish, Fundulus heteroclitus California topsmelt, Atherinops affinis electrophysiology electrophysiology behavior behavior behavior electrophysiology MSP, electrophysiology electrophysiology

operant conditioning MSP

heart-rate conditioning

MSP, behavior electophysiology

heart-rate conditioning

MSP, electrophysiology

MSP MSP MSP MSP MSP MSP MSP

400

[97]

400

[97]

360

[98]

360

[98]

360

[98]

390

[99]

370

[100]

360

[101]

358, 365

[102]

response down to 365

[103]

355-360

[104]

365

[105]

377

[106]

358

[107]

355

[27]

355-360

[108]

350-370

[109]

390

[110]

355

[65]

360

[111]

N/A

[66]

412

[112]

411

[112]

360 370

E. Loe

385

[113]

365

[114]

363

115}

355

Organism

Method

Wavelength of maximum response or absoption (nm)

Reference

Grunion, Leuresthes tenuis

MSP

355

[116]

Kelp greenling, Hexagrammos decagrammus

MSP

350, 358

[102]

White spotted greenling, H. steilen

MSP

364

[102]

Lingcod, Ophiodon elongates

MSP

359

[102]

Puget Sound sculpin, Artedius meanyi

MSP

363, 375

[102]

Cabezon, Scorpaenichthys marmorutus

MSP

364

[102]

Rock prickleback, Xiphister mucosus

MSP

364

[102]

Dwarf wrymouth, Lyconectes aleutensis

MSP

355

[102]

Wolf-eel, Anarrhichthys oceliatus

MSP

378

[102]

Pacific sandfish, Trichodon trichodon

MSP

359

[102]

Atlantic halibut, Hippoglossus hippoglossus

in situ hybridization

N/A

[117]

Cichlid, Metriaclima zebra

MSP

368

[118]

Damselfish, Dascyllus albisella

MSP

>400

[119]

Pomacentridae,

Dascyllus trimaculatus

Pomacentrus coelestris

Chromis punctipinnis

MSP

360

[120]

Reptiles

Red-eared terrapin, Pseudemys scripta elegans

electrophysiology

360

[121]

Caspian terrapin, Mauremys caspica

electrophysiology

360

Figure 5. UV images taken with a UV video camera sensitive between 320 nm and 410 nm. (A) Image taken in Oneida Lake, NY, USA showing Daphnia sp. in silhouette against the brighter skylight. Freshwater copepods Diaptomus siscilis are also shown and appear darker because they contain a dense, UV-absorbing (orange) pigment. (B) Image of Daphnia sp. showing UV scatter 90° from the direction of artificial UV illumination from a xenon light source. [Photos provided by E.R. Loew and W.N. McFarland.]

Figure 5. UV images taken with a UV video camera sensitive between 320 nm and 410 nm. (A) Image taken in Oneida Lake, NY, USA showing Daphnia sp. in silhouette against the brighter skylight. Freshwater copepods Diaptomus siscilis are also shown and appear darker because they contain a dense, UV-absorbing (orange) pigment. (B) Image of Daphnia sp. showing UV scatter 90° from the direction of artificial UV illumination from a xenon light source. [Photos provided by E.R. Loew and W.N. McFarland.]

the presence of UV-A wavelengths [63,64] and can feed under monochromatic UV-A [63]. However, recent experiments with trout suggest that UV photoreceptors do not enhance foraging under natural levels of solar radiation [73]. In field experiments conducted in Patagonia, Argentina (41°08'S, 71°25'W) with rainbow trout, Oncorhynchus mykiss, the removal of UV wavelengths from solar radiation had no effect on the number of prey eaten or on prey preference. These experiments were run outdoors between 1000-1300 h local time. It is not known if a difference would have been noticed during crepusclular periods when relative UV levels are higher and planktivory is more challenging.

It has been suggested that increased absorbance in prey species in the UV range due to photoprotective pigments increases visibility to predators, especially in transparent organisms. Transparent organisms occupying the epipelagic zone in the Northwest Atlantic Ocean were found to be more UV absorbent than those occupying the deeper mesopelagic zone, while visible transparency was similar for organisms inhabiting both regions [74]. However, absorbance was greatest in the UV-B range not in the UV-A range where UV vision occurs. In addition, species with high UV-absorption tended to be less transparent in the visible range. For both these reasons, the effects of UV absorption on UV visibility were predicted to be slight in comparison to potential photoprotection.

UV photoreceptors have also been identified in several zooplankton prey, such as the cladoceran Daphnia magna [75]. It is possible that these UV photoreceptors may also serve a means of predator avoidance. However, this hypothesis has yet to be fully tested.

The presence of both UV photoreception and negative phototaxis in some species suggest that UV photoreceptors may help animals to avoid depths at which levels of damaging solar radiation are high. Indeed, it is not known if organisms can sense the UV damage they are incurring and respond appropriately without the aid of UV photoreceptors. In the cyanobacterium Cholog-loeopsis, a UV-B photoreceptor is linked to the production of the photoprotective compound shinorine, a mycosporine-like amino acid [76]. Induction efficiency of shinorine was greatest when organisms are exposed to UV-B at 310 nm.

Curiously, UV vision is also noted in some mesopelagic and benthic organisms where little to no UVR is present. One explanation for UV vision at these depths is that many deep-sea fishes and some crustaceans possess photophores, light emitting organs with maximum emission in the blue, that may be used to communicate information between conspecifics and/or predators and prey. UV photoreceptors in these species have significant blue sensitivity, and the emissions of the photophores correlate well with the maximum transmission of the water as well as with the maximum sensitivity of the visual pigments [59]. These organisms are also known to be vertical migrators and it is suggested that UV photoreceptors may be used to detect varying ratios of shorter to longer wavelengths that would occur at sunrise and sunset, which could trigger the organisms to ascend and descend if enough solar radiation were available [35]. In the alciopid worm, Torrea Candida, it is suggested that UV photoreceptors are used as a depth gauge [77].

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