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First published online May 18, 2006
Journal of Experimental Biology 209, 2085-2102 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02266
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In vivo cranial suture function and suture morphology in the extant fish Polypterus: implications for inferring skull function in living and fossil fish

Molly J. Markey1,*, Russell P. Main2 and Charles R. Marshall,1,2

1 Department of Earth and Planetary Sciences, Harvard University, USA
2 Department of Organismic and Evolutionary Biology, Harvard University, USA


Figure 1
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Fig. 1. Strain gauge placement in Polypterus endlicherii. Single-element strain gauges were bonded across the interfrontal (IF), interparietal (IP) and frontoparietal (FP) sutures. Strips of TeflonTM were placed along each suture before bonding the gauges to prevent gluing the suture shut. Due to space constraints, a single rosette gauge was glued to the left frontal bone (Fr), with the Ea component aligned with the FP gauge, and the Ec component parallel to the IF gauge. Pa, parietal; Eb, measured bone strain at 45° to Ea and Ec.

 

Figure 2
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Fig. 2. (A) Kinematics and sutural strains measured during three suction feeding events (Polypterus 1, trial 3, events 1-3; see Table S1 in supplementary material). Still frames of (B) mouth opening, (C) maximum gape and (D) mouth closing are shown for the first suction feeding event. The blue vertical lines indicate the timing of the gape cycle. All strain peaks appear to coincide with maximum gape, and only one peak is observed in each feeding event. The interparietal (IP) suture is loaded in compression, while the interfrontal (IF) and frontoparietal (FP) sutures are loaded in tension.

 

Figure 3
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Fig. 3. Most common strain patterns during suction and biting in Polypterus, mapped onto a three-dimensional reconstruction of the skull made from the microCT scan of fish no. 2. Lengths of vectors are proportional to the strains they represent (see scale bar). The percentages indicate how frequently each pattern is observed during suction and biting. Double-headed arrows indicate a shift in strain polarity within a single event. In spite of the variation in strain patterns in suction and biting, the interfrontal (IF) is consistently loaded in tension, while the interparietal (IP) is compressed. The frontoparietal (FP) suture may be loaded in tension or compression, or may shift from one to the other, within a single feeding event. The maximum (E1) and minimum (E2) principal strains on the left frontal bone are also shown.

 

Figure 4
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Fig. 4. Mean peak strains across the interfrontal (IF), interparietal (IP) and frontoparietal (FP) sutures, and maximum (E1) and minimum (E2) principal bone strains during suction and biting. Values are means ± 1 s.e.m. Filled symbols are strains measured in suction, and open symbols represent strains measured during biting. (circles, Polypterus 1; squares, Polypterus 2, triangles; Polypterus 3, diamonds; Polypterus 4). Black symbols are the mean of means for all four fish (± 1 s.e.m.). The most common strain pattern during suction is shown (inset). Mean peak IF, FP and IP strains are higher during suction than during biting. In addition, E1 is larger during suction than in biting, but there is no difference in the E2 in suction and biting.

 

Figure 5
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Fig. 5. Wide range of times at which peak suture and bone strains, and maximum gape, hyoid depression and head lifting, are achieved during biting (B) and suction (S) for all 52 feeding events included in this analysis. Peak hyoid depression and head lifting are given for suction only, because biting events do not exhibit distinct maxima of these variables. Mean timing values for each strain and kinematic peak are shown in yellow (mean ± s.d., N=4). For 8 individual trials, vertical paths show the times at which each strain and kinematic maximum were achieved. The red arrows indicate the first (left) and second (right) suction feeding events shown in Fig. 2. The blue arrows indicate the first (left) and second (right) biting events illustrated in Fig. 6. There was substantial variation in these timings between trials; however, the correlations between strain peak timing and the fish's kinematic activity were significant. If the temporal pattern of maximum strains and kinematics were identical in all suction or biting trials, then the vertical paths would all be parallel and located in the same region of the gape cycle, which they are not. Note that portions of the lines that represent suction events tend to track each other closely, as do portions of the biting events. This illustrates our finding that biting and suction events cause maximum skull and suture deformation at different points in the feeding cycle.

 

Figure 6
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Fig. 6. (A) Kinematic measurements and suture strains during three biting events (Polypterus 1, trial 3, events 10-12; see Table S1 in supplementary material). Still frames of (B) mouth opening, (C) maximum gape and (D) mouth closing are given for the first biting event. The blue vertical lines indicate timing of the gape cycle. Strains due to biting were much more variable that strains caused by suction, so this particular trace should not be considered representative of all the strain traces measured during biting. In this particular event, the interparietal (IP) and frontoparietal (FP) sutures experience shifts in strain polarity, while the interfrontal (IF) suture is consistently loaded in tension. Note that the angle of head lifting and the amount of hyoid depression do not change appreciably in these events, in contrast to suction feeding.

 

Figure 7
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Fig. 7. Correlating suture shape and function in Polypterus using microCT slices. Line drawings of each suture are provided to the right of the actual slice images. The interparietal (IP) suture, which is loaded in compression during suction and biting, is highly interdigitated in cross section. In contrast, the interfrontal (IF) suture has an abutting (i.e. flat-edged) morphology and is typically loaded in tension during suction and biting. The frontoparietal (FP) suture, however, is highly overlapping, and is loaded in tension or compression, and may experience a shift in strain polarity during suction and biting. Pa, parietal; Fr, frontal.

 

Figure 8
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Fig. 8. Dissection of Polypterus in lateral and ventral views, showing many of the muscles that act during the expansive and compressive phases of feeding. Expansive phase muscles are shown in pink, while compressive phase muscles are shown in blue. The position of the frontoparietal (FP) suture is indicated by the green arrow. Modified from Lauder (Lauder, 1980Go), with permission of the author. AMp, adductor mandibulae pterygoideus; AMt, adductor mandibulae temporalis; LAP, levator arcus palatini; AM2, adductor mandibulae, division 2; DO, dilator operculi; AOP, adductor operculi; EP, epaxialis; IH, interhyoideus; SH, sternohyoideus; BM, branchiomandibularis; IMp, intermandibularis posterior.

 





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