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First published online April 17, 2009
Journal of Experimental Biology 212, 1377-1391 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.028506

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

Aaron N. Rice^* and Andrew H. Bass

Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA

View larger version (47K): [in this window] [in a new window]   Fig. 1. Representative hoot train of Batrachomoeus trispinosus. (A) Waveform (amplitude is in dimensionless arbitrary units) and (B) spectrogram (Hz) of 13 boatwhistle calls in a train of 36 s in duration. Box indicates the position of the individual call represented in C. (C) Power spectrum of an individual, representative hoot on an expanded time base, shown in the inset (scale bar represents 250 ms). (D) Close-up of boatwhistle waveform, showing fine-scale call structure. Sounds were recorded at 44.1 kHz.

View larger version (12K): [in this window] [in a new window]   Fig. 2. Temporal patterns in different B. trispinosus vocalizations. (A) Duration of individual boatwhistle hoots within a train versus the order in which they occur within the train. (B) Duration of individual grunts within a grunt train versus the order in which they occur within the train. The duration of calls decreases with increasing order within the train (i.e. later calls are shorter), while there is no correlation with interval duration within the train.

View larger version (34K): [in this window] [in a new window]   Fig. 3. (A) Waveform, (B) spectrogram and (C) power spectrum of a representative individual grunt of B. trispinosus. Sounds were recorded at 44.1 kHz.

View larger version (74K): [in this window] [in a new window]   Fig. 4. (A) Waveform and (B) spectrogram of a representative grunt train (composed of 45 individual grunts) of B. trispinosus. Boxes in A represent individual grunts within the train in C and E. (C) The waveform and (D) corresponding power spectrum of an individual grunt at the beginning of the grunt train. (E) Waveform of an individual grunt in the middle of the grunt train. Sounds were recorded at 44.1 kHz.

View larger version (63K): [in this window] [in a new window]   Fig. 5. Examples of two representative grunts exhibiting acoustic beats from B. trispinosus. (A) Waveform, (B) spectrogram, (C) power spectrum, (D) and waveform with expanded time base of a individual grunt. Box in A indicates enlarged section in D. Arrows in C represent peaks at 194, 2196, 2326 and 2498 Hz. (D) Waveform, (E) spectrogram, (F) power spectrum and (G) waveform with expanded time base of a second grunt, showing beat structure and clear harmonics. Box in E indicates enlarged section in H. Arrows in G represent peaks at 194, 2196, 2348 and 2520 Hz. For spectrograms (B,F) and power spectra (D,H), FFT size=1028 samples.

View larger version (14K): [in this window] [in a new window]   Fig. 6. (A) Diel patterns of calling frequency of different call types in B. trispinosus. Horizontal bar beneath x-axis labels indicates light cycle: open bar represents the period of ambient lights on, filled bar represents the period of ambient lights off (with only moonlight on). (B) Number of different call types over the lunar cycle in B. trispinosus.

View larger version (46K): [in this window] [in a new window]   Fig. 7. (A) Representative waveforms of different toadfish vocalizations. Horizontal scale bars represent 250 ms; amplitude of the different calls is not to scale. (B) Relative temporal position of the occurrence of the maximum amplitude in toadfish harmonic calls, for B. trispinosus (BT), Halobatrachus didactylus (HD), Opsanus beta (OB), O. phobetron (OP), O. tau (OT), and the growl and hum of Porichthys notatus (PN).

View larger version (19K): [in this window] [in a new window]   Fig. 8. Results from a principal coordinates analysis (PCo2 versus PCo1) of spectrographic cross-correlation (SPCC–PCo) (Cortopassi and Bradbury, 2000) of 166 vocalizations from six species of toadfishes. Sounds analyzed included harmonic hoots from the boatwhistle vocalizations of B. trispinosus (filled blue squares), H. didactylus (filled red circles), O. beta (open green circles), O. phobetron (open purple squares), O. tau (open blue triangles) and the hum of P. notatus (filled orange triangles). Due to their temporal similarity to toadfish boatwhistles, `growls' of P. notatus (filled yellow diamonds) were also analyzed.

View larger version (58K): [in this window] [in a new window]   Fig. 9. (A) Ventral view of a cleared and stained B. trispinosus specimen (6.6 cm standard length) showing the bilateral swimbladder. The skin and viscera of the abdominal cavity were removed and the swimbladder was left in place. Specimen was cleared and stained for cartilage (with Alcian Blue) and bone (with Alizarin Red) following the protocol of Song and Parenti (Song and Parenti, 1995). Scale bar represents 1 cm. The right pelvic and pectoral fins are labeled for reference orientation. (B) Ventral view of dissected swimbladders from a 9.9 cm standard length female, showing asymmetry between left and right bladders. Arrows indicate points of attachment, where the bladders are connected to each other by connective tissue. Scale bar represents 1 cm.

View larger version (54K): [in this window] [in a new window]   Fig. 10. Cross-section (70 µm thick sections) of swimbladder wall and intrinsic swimbladder muscle of B. trispinosus, stained with Methylene Blue from 7.1 cm standard length male (A) and 15.1 cm standard length male (B). The medial side of the swimbladder is to the left. Scale bar represents 1 mm for A and B. (C) High magnification view of junction of swimbladder wall and muscle from the area represented by the box in A. Medial side of the swimbladder is to the left. Scale bar represents 1 mm.

View larger version (14K): [in this window] [in a new window]   Fig. 11. Ontogenetic changes in swimbladder morphology of B. trispinosus males and females. (A) Length of left swimbladder versus standard length; (B) length of right swimbladder versus standard length; (C) left swimbladder width versus standard length; (D) right swimbladder width versus standard length. Solid lines represent regression lines of males (black) and females (gray). For all parameters measured, males were significantly different from females (ANCOVA, P<0.0001); females had longer swimbladders and wider swimbladder muscles than males, while males had wider swimbladders than females.

View larger version (35K): [in this window] [in a new window]   Fig. 12. Phylogenetic relationships of toadfishes generated from a maximum likelihood analysis of genes from available sequences (16S; 28S; cytochrome oxidase subunit I, COI; cytochrome b, CytB) in GenBank. Branch lengths are drawn proportional to the amount of character change. Bootstrap values are shown next to nodes. The gadid, Gadus morhua, was used as an outgroup for the Batrachoididae. Boxes around species names indicate taxa used in the comparative sound analysis, and a representative waveform of the species' call and swimbladder is shown for each taxon analyzed.

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