Does Vibrissal Innervation Patterns and Investment Predict Hydrodynamic Trail Following Behavior of Harbor Seals (Phoca vitulina)?

Abstract

Our understanding of vibrissal function in pinnipeds is poor due to the lack of comparative morphological, neurobiological, and psychophysical performance data. In contrast, the function of terrestrial mammalian vibrissae is better studied. Pinnipeds have the largest vibrissae of all mammals, and phocids may have the most modified vibrissae. The tactile performance for pinniped vibrissae is well known for harbor seals (Phoca vitulina). Harbor seals display at least two types of tactile behavior involving their mystacial vibrissae: a fine discriminatory capability using active touch and hydrodynamic trail following (the ability to detect and follow turbulent trails). This study investigated innervation patterns of harbor seal follicle‐sinus complexes (F‐SCs) to test the hypothesis that the whiskers used in hydrodynamic trail following possess increased innervation investment compared to other phocids. Therefore, the most lateral vibrissae from five harbor seals were histologically processed so that morphometric measurements and axon counts could be collected. Vibrissae from one harbor seal were immunolabeled with anti‐protein gene product (PGP 9.5) to document the pattern of deep vibrissal nerve innervation of the F‐SCs. Overall, harbor seals showed an innervation pattern (axons/F‐SC and axons/muzzle) similar to other phocids. The ventrolateral vibrissae, involved in hydrodynamic trail following, have greater axon density in harbor seals than harp seals, suggesting harbor seal F‐SC innervation patterns could explain their performance at trail following. The combination of microstructural, innervation investment, and behavioral data provides a foundation for functional inference regarding this tactile behavior in harbor seals and also facilitates future comparative work for other pinniped species. Anat Rec, 302:1837–1845, 2019. © 2019 American Association for Anatomy

Ecomorphology reveals Euler spiral of mammalian whiskers

“…Damping will occur within the follicle and will depend on the follicle anatomy, blood supply, and surrounding muscles, which all might be under active, or passive, control (Hartmann, Johnson, Towal, & Assad, 2003; Hyvärinen, 1989; Mitchinson et al, 2004). The arrangement of mechanoreceptors within follicles will also vary from species to species (Ebara et al, 2002; Hyvärinen, 1989; Jones & Marshall, 2019; Marshall, Amin, Kovacs, & Lydersen, 2006; Sprowls & Marshall, 2019), so exactly how and where whisker deflections and vibrations are detected will vary between species. It is evident that there is much to learn about whiskers; further studies could usefully explore relationships between morphological variation and evolutionary adaptations, in particular with respect to the “whisker specialists,” including aquatic and scansorial mammals.…”

“…Whisker morphology can vary between species, for example, many phocids have undulating, beaded whiskers (Ginter et al, 2012; Ginter, Fish, & Marshall, 2010; Hanke et al, 2010; Rinehart, Shyam, & Zhang, 2017), and aquatic mammals are thought to have more innervated whiskers than terrestrial species (Dehnhardt & Mauck, 2008; Mattson & Marshall, 2016; Mcgovern, Marshall, & Davis, 2015; Miersch et al, 2011; Rice, Mance, & Munger, 1986). Some aquatic species use their whiskers for both, touch and hydrodynamic sensing, such as California sea lions ( Zalophus californianus ; Gläser, Wieskotten, Otter, Dehnhardt, & Hanke, 2011; Milne & Grant, 2014) and Harbour seals ( Phoca vitulina ; Dehnhardt, Mauck, & Bleckmann, 1998; Grant, Wieskotten, Wengst, Prescott, & Dehnhardt, 2013), which may indicate functional differences between aquatic and terrestrial whiskers (Jones & Marshall, 2019; Sprowls & Marshall, 2019). Yet, while whisker shape and function are likely to differ between species, especially between aquatic and terrestrial species, the difficulty in comparing whisker shape quantitatively means that whisker morphology has not been explored across a wide range of mammalian species before.…”

“…. Some aquatic species use their whiskers for both, touch and hydrodynamic sensing, such as California sea lions (Zalophus californianus; Gläser, Wieskotten, Otter, Dehnhardt, & Hanke, 2011;Milne & Grant, 2014) and Harbour seals (Phoca vitulina; Dehnhardt, Mauck, & Bleckmann, 1998;Grant, Wieskotten, Wengst, Prescott, & Dehnhardt, 2013), which may indicate functional differences between aquatic and terrestrial whiskers (Jones & Marshall, 2019;Sprowls & Marshall, 2019). Yet, while whisker shape and function are likely to differ between species, especially between aquatic and terrestrial species, the difficulty in comparing whisker shape quantitatively means that whisker morphology has not been explored across a wide range of mammalian species before.…”

Creating underwater vision through wavy whiskers: a review of the flow-sensing mechanisms and biomimetic potential of seal whiskers

“…While an in-depth discussion of the innervation patterns of seal whiskers is outside the scope of the present article, the reader is referred to publications that studied the FSC microstructure of various seal species in great detail (e.g. in bearded seals [29], northern elephant seals [30] and harbour seals [31]) and discussed the consequences of a highly innervated FSC for the enhanced foraging abilities of seals.…”

Comparing vibrissal morphology and infraorbital foramen area in pinnipeds

“…As well as having morphological specializations, pinniped vibrissae are also particularly sensitive (Hyvärinen, 1989;Jones & Marshall, 2019;Marshall, Amin, Kovacs, & Lydersen, 2006;Mattson & Marshall, 2016;Smodlaka, Galex, Palmer, Borovac, & Khamas, 2017;Sprowls & Marshall, 2019), further supporting the importance of vibrissal sensing in pinnipeds. The deep vibrissal nerve, which is a branch of the infraorbital nerve (ION), contains 10 times more nerve fibers in pinnipeds, than in terrestrial mammals (Hyvärinen, 1989;Hyvärinen, Palviainen, Strandberg, & Holopainen, 2009).…”