Novel vocal repertoire and paired swimbladders of the three-spined toadfish,Batrachomoeus trispinosus: insights into the diversity of the Batrachoididae

Abstract

SUMMARYToadfishes (Teleostei: Batrachoididae) are one of the best-studied groups for understanding vocal communication in fishes. However, sounds have only been recorded from a low proportion of taxa within the family. Here, we used quantitative bioacoustic, morphological and phylogenetic methods to characterize vocal behavior and mechanisms in the three-spined toadfish, Batrachomoeus trispinosus. B. trispinosus produced two types of sound: long-duration 'hoots' and short-duration 'grunts' that were multiharmonic, amplitude and frequency modulated, with a dominant frequency below 1 kHz. Grunts and hoots formed four major classes of calls. Hoots were typically produced in succession as trains, while grunts occurred either singly or as grunt trains. Aside from hoot trains, grunts and grunt trains, a fourth class of calls consisted of single grunts with acoustic beats, apparently not previously reported for individuals from any teleost taxon. Beats typically had a predominant frequency around 2 kHz with a beat frequency around 300 Hz. Vocalizations also exhibited diel and lunar periodicities. Spectrographic crosscorrelation and principal coordinates analysis of hoots from five other toadfish species revealed that B. trispinosus hoots were distinct. Unlike any other reported fish, B. trispinosus had a bilaterally divided swimbladder, forming two separate swimbladders. Phylogenetic analysis suggested B. trispinosus was a relatively basal batrachoidid, and the swimbladder and acoustic beats were independently derived. The swimbladder in B. trispinosus demonstrates that toadfishes have undergone a diversification of peripheral sonic mechanisms, which may be responsible for the concomitant innovations in vocal communication, namely the individual production of acoustic beats as reported in some tetrapods. Supplementary material available online at

Novel underwater soundscape: acoustic repertoire of plainfin midshipman fish

“…Third, building upon recent reports of the Lusitanian toadfish, Halobatrachus didactylus (Amorim, 2006;Vasconcelos et al, 2012), the three-spined toadfish, Batrachomoeus trispinosus (Rice and Bass, 2009;Rice et al, 2011), and two toadfish species from Belize, Sanopus astrifer and Batrachoides gilbert (see Mosharo and Lobel, 2012), the current study begins to reveal the breadth of intraspecific and interspecific diversity in the spectro-temporal properties of toadfish calls beyond that of species within the genus Opsanus that have predominated the literature for nearly six decades (see below). Fourth, together with our earlier studies of the three-spined toadfish (Rice and Bass, 2009;Rice et al, 2011), we looked in detail at the structure of individual sounds themselves. This includes an in-depth analysis of growls, the least studied but acoustically most variable in structure of midshipman sounds and perhaps toadfish sounds in general (see further discussion in the following section).…”

“…Boatwhistles have been the most extensively reported, and along with hum and hoot analogs are now documented for eight species of toadfishes (reviewed in Amorim, 2006;Mosharo and Lobel, 2012;Rice and Bass, 2009). Grunt-like calls are typical of toadfishes and many fish species (Amorim, 2006;Bass and McKibben, 2003;Fine and Thorson, 2008;Ladich and Myrberg, 2006;Myrberg and Lugli, 2006).…”

Melatonin action in a midbrain vocal-acoustic network

“…Field and captive studies of fish vocal behavior report robust daily periodicity, with activity peaking during nighttime in most species identified, including closely related toadfish species (Locascio and Mann, 2008;Rice and Bass, 2009). Directly complementing behavioral studies, in vivo neurophysiology in midshipman demonstrates a nocturnal increase in vocal network excitability, measured in increased duration and decreased stimulation threshold of midbrainevoked fictive calls (Rubow and Bass, 2009).…”

†Zappaichthys harzhauseri, gen. et sp. nov., a new Miocene toadfish (Teleostei, Batrachoidiformes) from the Paratethys (St. Margarethen in Burgenland, Austria), with comments on the fossil record of batrachoidiform fishes

“…Monod (1960) listed several putative diagnostic features of the batrachoidiforms, and, subsequently, Lauder and Liem (1983) proposed two synapomorphies, endopterygoid unossified and the possession of a dorsal fin with a short spinous portion and a long-based rayed portion, apparently defining the group. More recently, Wiley and Johnson (2010) proposed nine robust synapomorphies for the batrachoidiformes, including larvae with enormous yolk sac bearing an adhesive disc on its ventral surface [see also Breder and Rosen (1966) and Greenfield et al (2008)]; crowded configuration of dorsal-fin spine-pterygiophore complex (see also Monod, 1960); first epineural hypertrophied, robust, and ligamentously bound to the medial surface of the cleithrum; possession of five pectoral-fin radials, the uppermost unossified in some genera, the lowermost the largest and with a condylar association with the coracoid (see also Monod, 1960); supracleithrum with condylar articulation with posttemporal; parietals absent [however, according to Siebenrock (1901), Regan (1912), Monod (1960), Le Danois (1961), Rosen and Patterson (1969), and Lauder and Liem (1983), the parietals are present in batrachoidiform fishes, apparently fused with the epioccipitals and, in certain cases, with the epioccipitals and supraoccipital]; pelvic fin with a very short spine and two rays; mesethmoid unossified (see also Gosline, 1970); swimbladder with distinctive configuration [see, e.g., Collette and Russo (1981) and Rice and Bass (2009)…”

“…As emphasized by Rice and Bass (2009), little is known about the anatomy, evolutionary history, ecology, and behavior of batrachoidiform fishes outside of some European and North American taxa (see, e.g., Siebenrock, 1901;Gill, 1907;Pankratz, 1928Pankratz, , 1930Monod, 1960;Le Danois, 1961;Isaacson, 1964;Schwartz, 1974). The main exception is the 1046 papers on the physiology and other aspects of the biology of the oyster toadfish, Opsanus tau, listed by Schwartz and White (1996) and three previous bibliographies of this species.…”