Photon Hunting in the Twilight Zone: Visual Features of Mesopelagic Bioluminescent Sharks

The mesopelagic zone is a visual scene continuum in which organisms have developed various strategies to optimize photon capture. Here, we used light microscopy, stereology-assisted retinal topographic mapping, spectrophotometry and microspectrophotometry to investigate the visual ecology of deep-sea bioluminescent sharks [four etmopterid species (Etmopterus lucifer, E. splendidus, E. spinax and Trigonognathus kabeyai) and one dalatiid species (Squaliolus aliae)]. We highlighted a novel structure, a translucent area present in the upper eye orbit of Etmopteridae, which might be part of a reference system for counterillumination adjustment or acts as a spectral filter for camouflage breaking, as well as several ocular specialisations such as aphakic gaps and semicircular tapeta previously unknown in elasmobranchs. All species showed pure rod hexagonal mosaics with a high topographic diversity. Retinal specialisations, formed by shallow cell density gradients, may aid in prey detection and reflect lifestyle differences; pelagic species display areae centrales while benthopelagic and benthic species display wide and narrow horizontal streaks, respectively. One species (E. lucifer) displays two areae within its horizontal streak that likely allows detection of conspecifics' elongated bioluminescent flank markings. Ganglion cell topography reveals less variation with all species showing a temporal area for acute frontal binocular vision. This area is dorsally extended in T. kabeyai, allowing this species to adjust the strike of its peculiar jaws in the ventro-frontal visual field. Etmopterus lucifer showed an additional nasal area matching a high rod density area. Peak spectral sensitivities of the rod visual pigments (λmax) fall within the range 484–491 nm, allowing these sharks to detect a high proportion of photons present in their habitat. Comparisons with previously published data reveal ocular differences between bioluminescent and non-bioluminescent deep-sea sharks. In particular, bioluminescent sharks possess higher rod densities, which might provide them with improved temporal resolution particularly useful for bioluminescent communication during social interactions.

海洋中层带（mesopelagic zone）是一类视觉场景连续体，其内的生物体已演化出多种策略以优化光子捕获效率。本研究借助光学显微镜、体视学辅助视网膜地形测绘、分光光度法与显微分光光度法，对深海发光鲨鱼的视觉生态学展开了系统性探究，共涉及4种灯笼棘鲛科（Etmopteridae）物种：亮乌鲨*Etmopterus lucifer*、华丽乌鲨*E. splendidus*、棘乌鲨*E. spinax*与三角齿鲛*Trigonognathus kabeyai*，以及1种铠鲨科（Dalatiidae）物种：异鳞鲛*Squaliolus aliae*。
本研究揭示了一种全新的眼部结构：灯笼棘鲛科物种的眼球上颌区域存在半透明区域，该结构或可作为反照明（counterillumination）调节的参考系统，或充当破伪装的光谱滤光器；同时还发现了板鳃亚纲（elasmobranchs）此前未被报道的多种眼部特化结构，包括无晶状体间隙（aphakic gaps）与半圆形反光膜（semicircular tapeta）。
所有受试物种均拥有由纯视杆细胞构成的六边形镶嵌视网膜结构，且地形分布多样性极高。由浅表层细胞密度梯度形成的视网膜特化区域，或有助于猎物探测，并可反映物种的生活方式差异：远洋性物种具备中央凹（areae centrales），而底栖浮游性与底栖性物种则分别拥有宽阔与狭窄的水平视觉带。其中亮乌鲨（*E. lucifer*）的水平视觉带内存在两个中央凹区域，这或许使其能够精准识别同类修长的发光侧翼标记。
神经节细胞的地形分布变异度较低，所有受试物种均拥有用于实现敏锐正面双目视觉的颞侧区（temporal area）。该区域在三角齿鲛（*T. kabeyai*）中向背侧延伸，使其能够在腹正面视觉域内调整其特化颌部的攻击动作。亮乌鲨还额外拥有一个鼻侧区（nasal area），该区域与高视杆细胞密度区域相匹配。
视杆细胞视觉色素的峰值光谱灵敏度（λmax）介于484~491 nm之间，使这些鲨鱼能够探测到其栖息环境中绝大多数的入射光子。
与既往发表的研究数据对比显示，发光与非发光深海鲨鱼在眼部结构上存在显著差异：具体而言，发光鲨鱼拥有更高的视杆细胞密度，这或许能为其带来更优的时间分辨率，尤其适用于社交互动过程中的发光通信行为。