Development of the Visual System in a Burrow-Nesting Seabird: Leach's Storm Petrel

Abstract

Little is known about the development of vision in wild birds. It is unknown, for example, whether the ability to see can be predicted by the level of prenatal growth or whether the eyes are open at hatching in a particular species. In this study, we investigated the growth of eyes, the formation of retinal ganglion cell topography, and the appearance of simple, visually guided behaviours in chicks of a small procellariiform seabird, Leach's storm petrel (Oceanodroma leucorhoa). This semi-precocial species, which has a well-developed sense of smell, nests in underground burrows where adults provision chicks for 6-8 weeks in the dark before fledging. Retinal ganglion cell topographic maps revealed that fine-tuning of cell distribution does not happen early in development, but rather that the ganglion cell layer continues to mature throughout provisioning and probably even after fledging. While the olfactory bulbs reached adult size around 7 weeks after hatching, the eyes and telencephalon continued to grow. Optokinetic head response and artificial burrow finding experiments indicated that chicks in the 2nd week after hatching lack even the most basic visually guided behaviours and are probably blind. Thus, vision in Leach's storm petrel chicks starts to function sometime around the 3rd week after hatching, well after the eyes have opened and the olfactory system is functional.

Is seabird light‐induced mortality explained by the visual system development?

“…Chicks of burrow‐nesting petrels spend most of their early life in the dark environment underground, only going out at night to practice flight motions during the end of the nestling period (Yoda, Shiozaki, Shirai, Matsumoto, & Yamamoto, ). Mitkus and colleagues have studied development of the visual system in a burrow‐nesting seabird—Leach's storm‐petrel ( Hydrobates leucorhous ) (Mitkus, Nevitt, & Kelber, ), a species affected by light pollution (Miles, Money, Luxmoore, & Furness, ). Leach's storm‐petrel chicks spend 6–8 weeks in dark underground burrows before fledging.…”

“…Their vision starts to function only around the third week post‐hatching, however the retina is still immature and continues to develop, reaching adult‐like state probably only sometime after fledging. In contrast, olfactory bulbs reach adult‐like size before fledging, and can be used to identify burrows 1 week after hatching (Mitkus et al, ).…”

“…Two factors responsible for poor vision in recently fledged petrels were presented (Mitkus et al, ). First, a trade‐off prioritizing olfaction over an energetically costly visual system.…”

Olfactory receptor subgenome and expression in a highly olfactory procellariiform seabird

“…The larger number of intact OR genes and smaller percentage of pseudogenized ORs 467 in Leach's storm-petrels than most waterbirds suggests enhanced olfactory capabilities, 468 consistent with the large olfactory bulb ratio in Procellariiformes (Corfield, et reliance on olfaction and good sense of smell may develop in Leach's storm-petrels being 488 raised in darkness, whereas Procellariiform species exposed to more light may depend less on 489 olfaction for homing and individual recognition (Mitkus, et al 2016;Mitkus, et al 2018). 490…”

“…Leach's storm-petrels can readily 554 perform odor discrimination tasks as chicks soon after hatching (O'Dwyer, et al 2008). A 555 recent study by Mitkus et al (2018) has shown that Leach's storm-petrel chicks are blind for 556 the first 2 to 3 weeks post hatching suggesting a heightened reliance on olfaction. In our 557 study, some of the most over-expressed genes we identified in chick compared to adult 558 olfactory conchae are those that involved in ossification and soft tissue development (Table 559 S5), such as the genes SPARC, PHOSPHO1, Smpd3, COL1A1, COL1A2, and COL11A1.…”