Adaptive auditory plasticity for social communication in the plainfin midshipman fish (Porichthys notatus)

Abstract

Acoustic communication plays an important role in the social behaviours of vocal teleost fishes in the family Batrachoididae (midshipman and toad fishes). The midshipman and toadfishes have become good models for investigating the neural and endocrine mechanisms of auditory perception and vocal production shared by all vertebrates (Bass and Lu 2006), in part, because the reproductive success of these batrachoidid fishes is highly dependent on acoustic communication. Recent neuroethological studies of acoustic communication in the plainfin midshipman fish (Porichthys notatus) have provided strong evidence for the related reproductive-state and steroid-dependent modulation of hearing sensitivity in this species that leads to enhanced coupling of sender and receiver in this communication system (Sisneros and Bass 2003; Sisneros et al. 2004a). The plainfin midshipman fish is a vocal marine teleost fish found along the west coast of the USA. During the late spring and summer, midshipman fish migrate from deep water into the rocky intertidal zone to court and spawn. Midshipman fish are known to have three adult reproductive morphs that include female and two male morphs known as type I and II. Type I or ‘singing’ males acoustically court females with their seasonal advertisement calls or ‘hums’, which is a multiharmonic acoustic signal with a fundamental frequency (F0) that ranges from 90 to 100Hz (Brantley and Bass 1994). The dominant harmonics of the hum range up to 400Hz and can contain as much or more spectral energy than the F0. These harmonics have been hypothesized to be important for the detection and localization of the advertisement signal during the reproductive season (Sisneros and Bass 2003). Type II males or ‘sneaker’ males use an alternative reproductive tactic that does not require them to build nests or acoustically court females. Instead type II males satellite and/or ‘sneak’ spawn in the nests of type I males to steal fertilizations from ‘singing’ males when they are actively courting females. Females rely heavily on their auditory sense to detect and locate advertising males that produce the multiharmonic hums during the breeding season and will often exhibit robust phonotaxis to a synthesized hum (and even to a low frequency tone near the F0 of the male’s advertisement call). Previous work showed that the frequency sensitivity of the auditory afferents that innervated the saccule, the main organ of hearing in the midshipman, changed seasonally with reproductive state such that reproductive females were better suited than nonreproductive females to encode the dominant harmonics of the male’s advertisement call (Sisneros and Bass 2003). An investigation of the seasonal periodicity of reproduction