Bird Deborah J, Hamid Iman, Fox-Rosales Lester, Van Valkenburgh Blaire
Department of Ecology and Evolutionary Biology University of California Los Angeles Los Angeles CA USA.
Ecol Evol. 2020 Jun 23;10(14):6929-6953. doi: 10.1002/ece3.6343. eCollection 2020 Jul.
It is widely accepted that obligate aquatic mammals, specifically toothed whales, rely relatively little on olfaction. There is less agreement about the importance of smell among aquatic mammals with residual ties to land, such as pinnipeds and sea otters. Field observations of marine carnivorans stress their keen use of smell while on land or pack ice. Yet, one dimension of olfactory ecology is often overlooked: while underwater, aquatic carnivorans forage "noseblind," diving with nares closed, removed from airborne chemical cues. For this reason, we predicted marine carnivorans would have reduced olfactory anatomy relative to closely related terrestrial carnivorans. Moreover, because species that dive deeper and longer forage farther removed from surface scent cues, we predicted further reductions in their olfactory anatomy. To test these hypotheses, we looked to the cribriform plate (CP), a perforated bone in the posterior nasal chamber of mammals that serves as the only passageway for olfactory nerves crossing from the periphery to the olfactory bulb and thus covaries in size with relative olfactory innervation. Using CT scans and digital quantification, we compared CP morphology across Arctoidea, a clade at the interface of terrestrial and aquatic ecologies. We found that aquatic carnivoran species from two lineages that independently reinvaded marine environments (Pinnipedia and Mustelidae), have significantly reduced relative CP than terrestrial species. Furthermore, within these aquatic lineages, diving depth and duration were strongly correlated with CP loss, and the most extreme divers, elephant seals, displayed the greatest reductions. These observations suggest that CP reduction in carnivorans is an adaptive response to shifting selection pressures during secondary invasion of marine environments, particularly to foraging at great depths. Because the CP is fairly well preserved in the fossil record, using methods presented here to quantify CP morphology in extinct species could further clarify evolutionary patterns of olfactory loss across aquatic mammal lineages that have independently committed to life in water.
人们普遍认为，专性水生哺乳动物，特别是齿鲸，对嗅觉的依赖相对较小。对于与陆地仍有残余联系的水生哺乳动物，如鳍足类动物和海獭，嗅觉的重要性则存在较少的共识。对海洋食肉动物的实地观察强调了它们在陆地或浮冰上对嗅觉的敏锐运用。然而，嗅觉生态学的一个方面常常被忽视：在水下时，水生食肉动物觅食时“嗅觉失灵”，它们闭着鼻孔潜水，远离空气中的化学信号。因此，我们预测，相对于亲缘关系密切的陆生食肉动物，海洋食肉动物的嗅觉解剖结构会有所简化。此外，由于潜水更深、时间更长的物种觅食时远离水面的气味信号，我们预测它们的嗅觉解剖结构会进一步简化。为了验证这些假设，我们研究了筛状板（CP），它是哺乳动物后鼻腔中的一块多孔骨，是嗅觉神经从外周穿过到达嗅球的唯一通道，因此其大小与相对嗅觉神经支配程度相关。我们使用CT扫描和数字量化方法，比较了处于陆地和水生生态交界处的一个类群——熊超科动物的CP形态。我们发现，来自两个独立重新侵入海洋环境的谱系（鳍足类和鼬科）的水生食肉动物物种，其相对CP比陆生物种显著减小。此外，在这些水生谱系中，潜水深度和时间与CP缩小密切相关，而最极端的潜水者——海象，其CP缩小程度最大。这些观察结果表明，食肉动物的CP缩小是对海洋环境二次入侵期间选择压力变化的一种适应性反应，特别是对在深海觅食而言。由于CP在化石记录中保存得相当完好，使用本文介绍的方法量化已灭绝物种的CP形态，可能会进一步阐明独立适应水生生活的水生哺乳动物谱系中嗅觉丧失的进化模式。
