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First published online November 19, 2007
Journal of Experimental Biology 210, 4104-4122 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.007930
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Phylogenetic comparative analysis of electric communication signals in ghost knifefishes (Gymnotiformes: Apteronotidae)

Cameron R. Turner1,2,*, Maksymilian Derylo3,4, C. David de Santana5,6, José A. Alves-Gomes5 and G. Troy Smith1,2,7

1 Department of Biology, Indiana University, Bloomington, IN 47405, USA
2 Center for the Integrative Study of Animal Behavior (CISAB), Indiana University, Bloomington, IN 47405, USA
3 CISAB Research Experience for Undergraduates Program, Indiana University, Bloomington, IN 47405, USA
4 Dominican University, River Forest, IL 60305, USA
5 Laboratório de Fisiologia Comportamental (LFC), Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, AM 69083-000, Brazil
6 Smithsonian Institution, National Museum of Natural History, Division of Fishes, Washington, DC 20560, USA
7 Program in Neuroscience, Indiana University, Bloomington, IN 47405, USA


Figure 1
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Fig. 1. Signal parameter measurements. (A) EOD frequency trace (top) and head-to-tail EOD waveform (voltage) trace (bottom). (B) Power spectrum (8192 points, Hanning window) of an EOD recording showing fundamental (F1), second (F2) and third (F3) harmonic frequencies. (C) EOD frequency trace (top), head-to-tail EOD waveform (voltage) trace (middle), and root-mean-square (RMS) EOD amplitude trace (bottom) for a single chirp. Points used to measure signal parameters are indicated with crosses and/or arrows. See Table 1 for details on how duration and FM parameters were calculated from these points. (D) EOD frequency trace (top) and head-to-tail EOD waveform (voltage) trace (bottom) for a chirp with extreme and prolonged reduction of EOD amplitude. Broken red line indicates where EOD frequency was not measurable (i.e. when RMS EOD amplitude dropped below 15% of baseline). Estimates of EODf were fixed at this frequency until RMS EOD amplitude returned to at least 15% of its baseline.

 

Figure 2
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Fig. 2. Phylogenies used for comparative analyses. (A) Modified from the preliminary phylogeny of de Santana (C.D.d.S., unpublished data). de Santana's phylogeny is a majority consensus from 597 most parsimonious trees in a maximum parsimony analysis of 103 morphological characters. (B) Modified from Crampton and Albert (Crampton and Albert, 2006Go). Scale bar applies to branch lengths. Note that we use the older name Sternarchogiton porcinum whereas this species is referred to as `Apteronotus' porcinum in Crampton and Albert (Crampton and Albert, 2006Go). Note differences between the two phylogenies in the placement of S. terminalis, S. nattereri and S. porcinum and in the relationship between A. albifrons and A. leptorhynchus.

 

Figure 3
Figure 3
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Fig. 3. Photographs and species-typical electrocommunication signals of 15 apteronotid taxa. (A) Photograph of the head, not shown to scale. (B) A 3 ms section of head-to-tail EOD waveform with peak-to-peak amplitude normalized for all taxa. (C) EOD frequency trace (top) and head-to-tail EOD waveform (voltage) trace (bottom) of characteristic chirps in each species. Amplitude reductions during chirps are apparent from the amplitude envelope of the waveform trace in some species. Axes are the same as in Fig. 1A. Axis scales are identical within column C across all panels to allow direct comparison of chirp FM and duration. Red bars show positive start and stop times, respectively. Orange bars show the negative stop time. (D) Additional examples of chirps for each species shown as in C. Note the different frequency scale in D compared with C. The frequency axis scales are identical across panels within column D, but time scales vary as indicated. (E) Scatter plot of positive FM and duration showing all EODMs recorded in each taxon. Chirps are shown as red squares, GFRs as blue circles. The chirps identified in columns C and D are colored yellow and labeled. The purple line illustrates the linear function used to distinguish chirps from GFRs when necessary (see Materials and methods for details). Note that the duration axis is logarithmic, and thus the linear functions appear curved. Axis scales are identical across all panels within column E.

 

Figure 4
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Fig. 4. EOD frequency trace of chirp `bursts' from S. terminalis. (A) Entire burst. (B) The red-boxed portion of the burst in A is shown on an expanded time scale. Note the plateau-like elevation of the baseline EODf and the clustering of chirps within the burst.

 

Figure 5
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Fig. 5. EOD frequency trace of a `rasp' from Brazilian P. hasemani. (A) Entire rasp. (B) The red-boxed portion of the rasp in A is shown on an expanded time scale.

 

Figure 6
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Fig. 6. Discriminant function analysis (DFA) of EOD, chirp and GFR parameters. Scatter plots of first versus second (A) and first versus third (B) canonical roots from a DFA based on all signal parameters reveal the ability of these roots to segregate apteronotid species. Each data point represents a single fish, and species are color-coded as indicated. Some species (e.g. P. hasemani and A. leptorhynchus in A, and `A.' bonapartii and P. gimbeli in B) were well-segregated. Other species (e.g. S. terminalis and S. cf. roseni) overlapped considerably. (C) Performance of DFAs based on all signal parameters, EOD parameters only, chirp parameters only, or GFR parameters only in correctly classifying the species of individuals in leave-one-of-each-species-out cross-validations (see Materials and methods). The broken black line represents performance predicted based on chance alone. All DFAs correctly classified individuals at rates exceeding chance, but DFAs based on EODs and chirps performed better than those based on GFRs.

 

Figure 7
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Fig. 7. Correlations between signal parameters. Raw species means are shown with the correlation calculated using TIPS model (large {alpha}; non-phylogenetic). (A) Correlation between chirp undershoot FM and chirp–FM slope. More negative values indicate larger undershoots (y-axis) and faster returns to baseline EODf (x-axis). (B) Correlation between chirp FM and chirp %AM. Larger values on the x-axis indicate greater reduction in EOD amplitude during chirps. Letters on each data point indicate species as follows: A, S. cf. curvirostris; B, S. cf. roseni; C, S. terminalis; D, P. hasemani (Peru); E, P. hasemani (Brazil); F, A. albifrons; G, A. leptorhynchus; H, `A.' bonapartii; I, `A.' n. sp. B; J, S. nattereri; K, S. porcinum; L, P. gimbeli (Peru); M, P. gimbeli (Brazil); N, A. devenanzii; O, A. balaenops.

 

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© The Company of Biologists Ltd 2007