Intra‐ and Intersexual swim bladder dimorphisms in the plainfin midshipman fish (Porichthys notatus): Implications of swim bladder proximity to the inner ear for sound pressure detection

Abstract

The plainfin midshipman fish, Porichthys notatus, is a nocturnal marine teleost that uses social acoustic signals for communication during the breeding season. Nesting type I males produce multiharmonic advertisement calls by contracting their swim bladder sonic muscles to attract females for courtship and spawning while subsequently attracting cuckholding type II males. Here, we report intra- and intersexual dimorphisms of the swim bladder in a vocal teleost fish and detail the swim bladder dimorphisms in the three sexual phenotypes (females, type I and II males) of plainfin midshipman fish. Micro-computerized tomography revealed that females and type II males have prominent, horn-like rostral swim bladder extensions that project toward the inner ear end organs (saccule, lagena, and utricle). The rostral swim bladder extensions were longer, and the distance between these swim bladder extensions and each inner-ear end organ type was significantly shorter in both females and type II males compared to that in type I males. Our results revealed that the normalized swim bladder length of females and type II males was longer than that in type I males while there was no difference in normalized swim bladder width among the three sexual phenotypes. We predict that these intrasexual and intersexual differences in swim bladder morphology among midshipman sexual phenotypes will afford greater sound pressure sensitivity and higher frequency detection in females and type II males and facilitate the detection and localization of conspecifics in shallow water environments, like those in which midshipman breed and nest.

Auditory evoked potentials of the plainfin midshipman fish (Porichthys notatus): Implications for directional hearing

“…Coombs and Popper, 1979;Ramcharitar et al, 2006), which is supported by recent saccular potential measurements (Colleye et al 2019). We note that 'type II' male midshipman, an alternative male morph not considered further in the present report, also possess rostral swim bladder extensions and exhibit seasonally enhanced auditory sensitivity (see Mohr et al, 2017;Bhandiwad et al, 2017).…”

“…Ladich and Fay, 2013). While two fundamentally different modes of hearing (inertial acceleration and sound pressure reception) may still be identified, caveats against the reductionist dichotomy of hearing 'specialists' and 'generalists' (Popper and Fay, 2011) are underscored in the case of midshipman, wherein swim bladder-inner ear coupling varies both inter-and intra-sexually (Mohr et al, 2017). The AEP technique has been previously applied to assay contributions of the swim bladder in several species, with higher AEP thresholds following swim bladder deflation demonstrated in some species (such as the goldfish, Carassius auratus, a well-studied otophysan), but not others (such as O. tau) (Yan et al, 2000).…”

“…These changes are accompanied by an increase in auditory hair cell number within the saccular sensory macula (Coffin et al, 2012). Additionally, the swim bladder of the female midshipman exhibits rostral extensions ('horns') that terminate near the otic capsule (Bass and Marchaterre, 1989;Mohr et al, 2017). Such extensions, also present in certain other teleost species, are hypothesized to impart sound pressure sensitivity via mechanical coupling of the swim bladder and inner ear, akin to that provided by Weberian ossicles in otophysan species (e.g.…”

Lagenar potentials of the vocal plainfin midshipman fish, Porichthys notatus

“…While plainfin midshipman do not possess such hearing specializations, like Weberian ossicles, they do have swim bladder adaptations that may allow them to potentially detect sound pressure indirectly. A recent study by Mohr et al (2017) demonstrated that midshipman possess intra - and intersexual dimorphisms of the swim bladder that may facilitate pressure detection. Like other batrachoidid fishes, midshipman have a U -shaped swim bladder; how-ever, females and type II males have rostral extensions or “horns” that project close to the saccule and lagena, while the swim bladder of type I males does not have the distinct horns.…”

Testing ontogenetic patterns of sexual size dimorphism against expectations of the expensive tissue hypothesis, an intraspecific example using oyster toadfish (Opsanus tau)

“…Other species of Batrachoidiformes, such as members of the genus Porichthys (Midshipman), have been found to be sexually dimorphic in swim bladder size (Mohr et al., ). Given that Porichthys and Opsanus share common ancestry at least 30 million years ago (Near et al., ), it is likely that the changes in ontogenetic slope found in our study may represent an axis of Batrachoidiform diversification that vastly predates the origin of Opsanus tau .…”