Assessment of trophic ecomorphology in non-alligatoroid crocodylians and its adaptive and taxonomic implications

Abstract

Although the establishment of trophic ecomorphology in living crocodylians can contribute to estimating feeding habits of extinct large aquatic reptiles, assessment of ecomorphological traits other than the snout shape has scarcely been conducted in crocodylians. Here, I tested the validity of the proposed trophic ecomorphological traits in crocodylians by examining the correlation between those traits and the snout shape (an established trophic ecomorphology), using 10 non-alligatoroid crocodylian species with a wide range of snout shape. I then compared the ontogenetic scaling of trophic ecomorphology to discuss its adaptive and taxonomic significance. The results demonstrated that degree of heterodonty, tooth spacing, size of supratemporal fenestra (STF), ventral extension of pterygoid flange and length of lower jaw symphysis are significantly correlated with snout shape by both non-phylogenetic and phylogenetic regression analyses. Gavialis gangeticus falls outside of 95% prediction intervals for the relationships of some traits and the snout shape, suggesting that piscivorous specialization involves the deviation from the typical transformation axis of skull characters. The comparative snout shape ontogeny revealed a universal trend of snout widening through growth in the sampled crocodylians, implying the existence of a shared size-dependent biomechanical constraint in non-alligatoroid crocodylians. Growth patterns of other traits indicated that G. gangeticus shows atypical trends for degree of heterodonty, size of STF, and symphysis length, whereas the same trends are shared for tooth spacing and ventral extension of pterygoid flange among non-alligatoroid crocodylians. These suggest that some characters are ontogenetically labile in response to prey preference shifts through growth, but other characters are in keeping with the conserved biomechanics among non-alligatoroid crocodylians. Some important taxonomic characters such as the occlusal pattern are likely correlated with ontogeny and trophic ecomorphology rather than are constrained by phylogenetic relationships, and careful reassessment of such characters might be necessary for better reconstructing the morphological phylogeny of crocodylians.

Keywords: allometry; crocodylian; occlusal pattern; piscivory; trophic ecomorphology.

Figure 1

A time‐calibrated molecular phylogeny of 10 sampled crocodylian species (based on Oaks, 2011).

Figure 2

(A) Rostral landmarks and semi‐landmarks used in this analysis. Seven landmarks (white markers) are taken at: 1: anterior end of rostrum; 2, 3: both lateral edges of premaxillary–maxillary contact; 4, 5: both lateral edges of maxillary alveolus #5; 6, 7: both lateral edges of rostrum at the level of posterior end of last maxillary alveolus. A total of 38 semi‐landmarks (gray markers) are taken on the outline of six palatal outline segments. (B) Measurement of lower jaw symphysis length. (C) Nineteen post‐rostral landmarks taken at: 1: orbit‐prefrontal‐lacrimal contact; 2: orbit‐lacrimal‐jugal contact; 3: orbit‐prefrontal‐frontal contact; 4: orbit‐frontal‐postorbital contact; 5: anteroventral end of postorbital bar; 6: posteroventral end of postorbital bar; 7: anterodorsal end of postorbital bar; 8: posterodorsal end of postorbital bar; 9: infratemporal fenestra‐jugal‐quadratojugal contact; 10: lateral edge of skull table at postorbital‐squamosal contact; 11: supratemporal fenestra (STF)‐postorbital‐squamosal contact; 12: triple junction of frontal‐parietal‐postorbital; 13: STF‐parietal‐postorbital contact; 14: STF‐parietal‐squamosal contact; 15: frontal‐parietal contact on midline; 16: supraoccipital‐parietal contact on midline; 17: posterior edge of skull table at parietal‐squamosal contact; 18: posteromedial corner of quadrate jaw joint; 19; posterior end of quadrate‐quadratojugal contact. (D) Landmarks and semi‐landmarks for calculating area of STF. Four landmarks (white markers) are taken at: 1: anterior edge of STF at postorbital‐parietal contact; 2: lateral edge of STF at postorbital‐squamosal contact; 3: medial‐most point of STF along parietal; 4: posterior edge of STF at parietal‐squamosal contact. A total of 12 semi‐landmarks (gray markers) are taken on the outline of STF to calculate the STF area including its smooth floor. (E) Measurements of pterygoid flange depth (PFD) and basioccipital tubera width.

Figure 3

(A,B,D–G) Bivariate plots of snout shape (RW1 score) and proposed ecomorphological variables for individuals within 2.1 ≤ log(CS) ≤ 2.4. Ordinary least squares (OLS) regression lines are fit on the plots. (C) Bivariate plot of mean species RW1 score and mode species maxillary tooth count for individuals within 2.1 ≤ log(CS) ≤ 2.4. CV, coefficient of variation. Dashed lines are 95% prediction intervals (PIs).

Figure 4

Bivariate plot of log(CS) and snout shape (RW1 scores). Area with gray gradient represents the estimated range of log(CS) breakpoints of snout shape for six species (C. acutus, C. niloticus, C. palustris, C. porosus, G. gangeticus and T. schlegelii), and the dashed line is their mean.

Figure 5

Log(CS) breakpoints of snout shape growth trajectories in six species estimated by piecewise linear model fitting. Individuals with log(CS) ≥ 2.0 were used for this analysis. Dots are the estimated values, and bars represent their 95% confidence intervals (CIs).

Figure 6

(A–G) Bivariate plots of log(CS) and ecomorphological variables. Reduced major axis (RMA) regression lines are fit on the plots (A,B,D–G).

Figure 7

Significant snout shape changes across the skull growth phases II and III. (A) C. acutus (from top: FMNH 20159; FMNH 59070). (B) C. intermedius (from top: FMNH 75659; SMF 28139). (C) C. niloticus (from top: IRSNB 5007; IRSNB 5012). (D) C. palustris (from top: BMNH 1848.2.5.9; BMNH 1868.4.9.11). (E) C. porosus (from top: FMNH 63744; FMNH 14071). (F) G. gangeticus (from top: YPM R10514; ZSM 28.1912). (G) T. schlegelii (from top: BMNH 1899.1.31.1; ZSM 395.1907). Ca, C. acutus; Ci, C. intermedius; Cni, C. niloticus; Cpa, C. palustris; Cpo, C. porosus; Gg, G. gangeticus; Ts, T. schlegelii. All scale bars are 10 cm.

Figure 8

Effect of size ranges on snout shape disparity tested by the empirical dataset. Ten individuals from each 10 species were randomly subsampled (10 000 replicates) without replacement, and the snout shape (RW1 scores) variance of 10 species was calculated for series of size ranges (2.0 ≤ log(CS) ≤ x, 2.30 ≤ x ≤ 2.60), where x sequentially changes by 0.01. The means and 95% confidence intervals of the variance for the series of size ranges were shown by a line chart. The subsampling and variance calculation were performed using the software r.

Figure 9

Comparative growth of snout shape (right palate) in sampled crocodylians. (A) C. palustris (from top: ZSM 523.1911; ZSM 542.1911; BMNH 1897.12.31.1). (B) C. acutus (from top: USNM 52336; FMNH 11038; USNM 268760). (C) T. schlegelii (from top: ZSM 202.1907; SMF 28135; ZSM 375.1907). (D) G. gangeticus (from top: BMNH 46.1.7.3; ZSM 29.1912; BMNH 1974.3009). All scale bars are 5 cm.

Figure 10

Comparison of occipital part of skulls in sampled crocodylians. (A) C. palustris (from left: ZSM 523.1911; ZSM 517.1911; BMNH 1897.12.31.1). (B) C. acutus (from left: AMNH 15182; AMNH 43299; USNM 268760). (C) T. schlegelii (from left: ZSM 202.1907; SMF 28135; ZSM 375.1907). (D) G. gangeticus (from left: BMNH 1896.7.7.4; ZSM 29.1912; AMNH 7138). All scale bars are 5 cm.

Figure 11

Occlusal pits left on palates. (A) T. schlegelii (BMNH 94.2.21.1). (B) Voay robustus (AMNH 3101). (C) Crocodylus rhombifer (AMNH 6181). Arrows indicate occlusal pits placed medial to maxillary tooth row. M5, maxillary alveolus #5; SOF, suborbital fenestra. All scale bars are 10 cm.

Figure 12

A pit between premaxilla and maxilla for reception of the fourth dentary tooth (C. palustris: BMNH 1852.5.9.45). The arrow indicates the pit. Scale bar: 5 cm.

Figure 13

Basioccipital region of the skull in C. palustris (BMNH 1897.12.31.1). Scale bar: 3 cm.