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The Eyes of Lanternfishes (Myctophidae, Teleostei)

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The Eyes of Lanternfishes (Myctophidae, Teleostei) RESEARCH ARTICLE The Eyes of Lanternfishes (Myctophidae, Teleostei): Novel Ocular Specializations for Vision in Dim Light Fanny de Busserolles,1 N. Justin Marshall,2 and Shaun P. Collin1 1Neuroecology Group, School of Animal Biology and the Oceans Institute, The University of Western Australia, Crawley, Western Australia 6012, Australia 2Sensory Neurobiology Group, Queensland Brain Institute, University of Queensland, St. Lucia, Queensland 4072, Australia Lanternfishes are one of the most abundant groups of mes- region (typically central retina) composed of modified pig- opelagic fishes in the world’s oceans and play a critical role ment epithelial cells, which we hypothesize to be the rem- in biomass vertical turnover. Despite their importance, very nant of a more pronounced visual specialization important little is known about their physiology or how they use their in larval stages. The second specialization is an aggregation sensory systems to survive in the extreme conditions of of extracellular microtubular-like structures found within the deep sea. In this study, we provide a comprehensive the sclerad region of the inner nuclear layer of the retina. description of the general morphology of the myctophid We hypothesize that the marked interspecific differences eye, based on analysis of 53 different species, to under- in the hypertrophy of these microtubular-like structures stand better their visual capabilities. Results confirm that may be related to inherent differences in visual function. A myctophids possess several visual adaptations for dim- general interspecific variability in other parts of the eye is light conditions, including enlarged eyes, an aphakic gap, a also revealed and examined in this study. The contribution tapetum lucidum, and a pure rod retina with high densities of both ecology and phylogeny to the evolution of ocular of long photoreceptors. Two novel retinal specializations specializations and vision in dim light are discussed. were also discovered. The first specialization is a fundal J. Comp. Neurol. 522:1618–1640, 2014. pigmentation in adult eyes, found within an isolated retinal VC 2013 Wiley Periodicals, Inc. INDEXING TERMS: Myctophids; visual adaptations; retina; microtubular-like structures; fundal pigmentation; visual ecology The lanternfishes belong to the Myctophidae, a More precisely, information about their visual system monophyletic family of deep-sea teleost fishes belong- and how their eyes have adapted to see in dim light and ing to the order Myctophiformes (Paxton, 1972; for viewing bioluminescent emissions are very sparse. To Stiassny, 1996). The family is divided into two subfami- date, the most comprehensive studies on lanternfish lies, the Myctophinae and Lampanyctinae, seven tribes, vision are from Bozzano et al. (2007) and Turner et al. and 33 genera and is represented by about 250 spe- (2009), who focus mainly on the photoreceptors and the cies (Hulley and Paxton, 2013). All species are luminous spectral sensitivity of their visual pigments. Bozzano et al. and possess ventral and ventrolateral photophores (2007) studied several larval stages in three different lan- (except for Taaningichthys paurolychnus) arranged in ternfish species and found a predominance of rods with species-specific patterns and often possess additional luminous organs and tissue over the head and body (Paxton, 1972). Myctophids are one of the most abun- Grant sponsor: Research Council (to S.P.C.); Grant sponsor: Deep- Australia Linkage Grant (to N.J.M., S.P.C.); Grant sponsor: West dant groups of mesopelagic fishes in the oceans and Australian State Government; Grant sponsor: Scholarship for Interna- play a major role in the marine ecosystem by transfer- tional Research Fees (SIRF to F.d.B.); Grant sponsor: University Inter- national Stipend (UIS) at the University of Western Australia (to ring energy to the deeper layers of the ocean through F.d.B.). their vertical migration behaviors (Moku et al., 2000; *CORRESPONDENCE TO: Fanny de Busserolles, Neuroecology Group Cherel et al., 2010). Despite their critical role, very little (M317), School of Animal Biology and the Oceans Institute, The University of Western Australia, Crawley, Western Australia 6012, Australia. is known about their physiology or how they use their E-mail: [email protected]. sensory systems to survive in the extreme conditions of Received March 10, 2013; Revised October 14, 2013; the mesopelagic zone of the deep sea (200–1,000 m). Accepted October 15, 2013. DOI 10.1002/cne.23495 Published online November 8, 2013 in Wiley Online Library VC 2013 Wiley Periodicals, Inc. (wileyonlinelibrary.com) 1618 The Journal of Comparative Neurology | Research in Systems Neuroscience 522:1618–1640 (2014) The eyes of lanternfishes increases in outer segment length during development Cape Ferguson) under the following collection permits: but, surprisingly, also cones, although cone numbers Coral Sea waters (CSCZ-SR-20091001-01), Common- steadily decreased, being lost in all postlarval stages wealth waters (AU-COM2009051), GBRMPA (G09/ (Bozzano et al., 2007). Turner at al. (2009) studied the 32237.1) and Queensland Fisheries (133805; Marshall, spectral sensitivity of the rod visual pigment in 58 differ- AEC No. SNG/080/09/ARC), and in the Peru-Chile ent species of myctophids using visual pigment extract trench (FS Sonne, sampling permits obtained by the spectrophotometry. Most of the Myctophidae were single Chief Scientist, University of T€ubingen). For all speci- pigment species with only four species (Cerastocopelus mens, sampling was carried out following the guidelines warmingii, Hygophum proximum, Myctophum aurolaterna- of the NH&MRC Australian Code of Practice, under a tum, M. nitidulum), belonging to both subfamilies, pos- University of Western Australia Animal Ethics protocol sessing two visual pigments. The wavelength of maximum (RA/3/100/917). Additional specimens from Western absorption (kmax) of these pigments falls between 480 Australian waters, the western Mediterranean Sea, and and 492 nm (Partridge et al., 1992; Douglas and Par- the Bay of Biscay were acquired through collaborators tridge, 1997; Douglas et al., 1998; Hasegawa et al., (de Busserolles et al., 2013). Only large juveniles and 2008; Turner et al., 2009), which is well-adapted to visu- adults were analyzed in this study. Most of the samples alization of blue-green bioluminescent light, the light most are registered as voucher specimens at the Australian commonly emitted by deep-sea organisms. Museum in Sydney, Australia, but further taxonomic Some older studies on myctophids have investigated analyses have to be carried out for five of our study retinal structure and the sampling of the visual environ- species to confirm identification positively (Lampanyctus ment. However, these data have been compiled from very vadulus, Myctophum spinosum, Nannobrachium cf. nig- few species, which all reveal that lanternfishes, like many rum, Symbolophorus cf. boops, Triphoturus oculeus, de other mesopelagic fishes (Marshall, 1954; Munk, 1966; Busserolles et al., 2013). Arnott et al., 1970; Munk and Frederiksen, 1974; Locket, Two species were photographed with a digital cam- 1977; Somiya, 1980, 1982; Wagner et al., 1998), appear era and/or a stereomicroscope to show the position to have evolved eyes designed to enhance sensitivity with and relative size of the eyes in the head, the extent of the presence of an aphakic gap (Tarletonbeania crenularis, the binocular overlap, and the location of both photo- Lawry, 1974), a pure rod retina (Lampanyctus crocodilus, phores and luminous organs. Observations, dissection, Vilter, 1951; Lampanyctodes sp., Pankhurst, 1987; Steno- and morphometric analyses were performed aboard brachius leucopsarus,O’DayandFernandez,1976),a ship and on fresh specimens, whenever possible. For tapetum lucidum (Stenobrachius leucopsarus,O’Dayand each individual, the standard length and rostrocaudal Fernandez, 1976), high photoreceptor densities (Lampa- eye diameter were measured with digital callipers (to a nyctus crocodilus,Vilter,1951;Lampanyctodes sp., Pan- precision of 0.1 mm) prior to dissection and fixation. khurst, 1987; Stenobrachius leucopsarus,O’Dayand The position of the aphakic gap, when present, was Fernandez, 1976), and a ratherunspecializedretinawith noted (and ascribed to falling within the dorsal, nasal, poor acuity (Lampanyctus macdonaldi, Myctophum puncta- ventral, or temporal quadrants of the eye) and photo- tum,CollinandPartridge,1996;Wagneretal.,1998). graphed using an Olympus stereomicroscope SZX10 In this study, we provide a comprehensive description mounted with a Canon digital camera. Once the eyes of the general morphology of the myctophid eye, based had been enucleated, the cornea and lens were dis- on analysis of several different species, to understand sected free of the eyecup, and the color, extent, and their visual capabilities better. One of the characteristics integrity of the tapetum lucidum were assessed before of the Myctophidae is their great interspecific variability photographing the fundus with the Olympus stereomi- in ecology and behavior (depth distribution, Karnella, croscope SZX10 and Canon digital camera. The appear- 1987; migration pattern, Watanabe et al., 1999; lumi- ance of the tapetum can change dramatically nous organs, Edwards and Herring, 1977), so a diverse depending on the light conditions and freshness of the range of ocular specializations may also be expected. specimen. As a consequence, only the
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