Diet of Mesozoic toothed birds (Longipterygidae) inferred from quantitative analysis of extant avian diet proxies - PubMed (original) (raw)

Diet of Mesozoic toothed birds (Longipterygidae) inferred from quantitative analysis of extant avian diet proxies

Case Vincent Miller et al. BMC Biol. 2022.

Abstract

Background: Birds are key indicator species in extant ecosystems, and thus we would expect extinct birds to provide insights into the nature of ancient ecosystems. However, many aspects of extinct bird ecology, particularly their diet, remain obscure. One group of particular interest is the bizarre toothed and long-snouted longipterygid birds. Longipterygidae is the most well-understood family of enantiornithine birds, the dominant birds of the Cretaceous period. However, as with most Mesozoic birds, their diet remains entirely speculative.

Results: To improve our understanding of longipterygids, we investigated four proxies in extant birds to determine diagnostic traits for birds with a given diet: body mass, claw morphometrics, jaw mechanical advantage, and jaw strength via finite element analysis. Body mass of birds tended to correspond to the size of their main food source, with both carnivores and herbivores splitting into two subsets by mass: invertivores or vertivores for carnivores, and granivores + nectarivores or folivores + frugivores for herbivores. Using claw morphometrics, we successfully distinguished ground birds, non-raptorial perching birds, and raptorial birds from one another. We were unable to replicate past results isolating subtypes of raptorial behaviour. Mechanical advantage was able to distinguish herbivorous diets with particularly high values of functional indices, and so is useful for identifying these specific diets in fossil taxa, but overall did a poor job of reflecting diet. Finite element analysis effectively separated birds with hard and/or tough diets from those eating foods which are neither, though could not distinguish hard and tough diets from one another. We reconstructed each of these proxies in longipterygids as well, and after synthesising the four lines of evidence, we find all members of the family but Shengjingornis (whose diet remains inconclusive) most likely to be invertivores or generalist feeders, with raptorial behaviour likely in Longipteryx and Rapaxavis.

Conclusions: This study provides a 20% increase in quantitatively supported fossil bird diets, triples the number of diets reconstructed in enantiornithine species, and serves as an important first step in quantitatively investigating the origins of the trophic diversity of living birds. These findings are consistent with past hypotheses that Mesozoic birds occupied low trophic levels.

Keywords: Aves; Avialae; Birds; Body mass; Cretaceous; Diet; Finite element analysis; Jehol Biota; Mechanical advantage; Morphometrics.

© 2022. The Author(s).

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1

Fig. 1

Reconstructions of longipterygid skulls. Reconstructions are of Longipteryx morphotypes with large teeth (A) and small teeth (B), Longirostravis (C), Rapaxavis (D), and Shanweiniao (E). Colours of different bones indicate which specimen that bone is based on. All sclerotic rings are based on BMNHC Ph-930B. Quadratojugal morphology is unknown in any taxon so is drawn in a dotted line. See the “Methods” section for more details on reconstruction. Scale bars are based on DNHM-D2889 (A), IVPP V12552 (B), IVPP V11309 (C), DNHM D2522 (D), and DNHM D1878/2 (E)

Fig. 2

Fig. 2

Measurements taken to calculate mechanical advantage and functional indices in this study. All are mapped onto the outline of a skull of Falco peregrinus. Measurements are of anterior jaw-opening mechanical advantage AMA (A), posterior jaw-opening mechanical advantage PMA (B), jaw-opening mechanical advantage OMA (C), relative articular offset AO (D), relative maximum cranial height MCH (E), and relative average cranial height ACH (F). Outlevers are drawn in blue, inlevers in red, and skull length in green. Lines of action of m. adductor mandibulae (A, B) and attachment of m. depressor mandibulae (C) are indicated by a dashed pink line. The crosshatched region in F indicates an area measurement. Line drawing based on specimen CM S-14309

Fig. 3

Fig. 3

Violin plots of bird body mass, organised by more inclusive diets and the whole range of diets considered. A, B Bird masses grouped by broad categories of diet, “inclusive diet”, excluding (A) and including (B) semi-specialists. C, D Bird masses grouped by the main diet categories in this paper, excluding (C) and including (D) semi-specialists. In C, FrugivoreH is represented by a single taxon, thus is a point. Dromaius novaehollandiae is excluded from all graphs as an outlier. Inclusive diets with the same letters above them do not have significantly different average masses in phylogenetic HSD at the p = 0.05 level (Table 2). Diet abbreviations: FrugivoreH hard frugivore, FrugivoreS soft frugivore, GranivoreS swallowing granivore, GranivoreH husking granivore, InvertivoreH hard invertivore, InvertivoreM medium invertivore, InvertivoreS soft invertivore, Tetra Hunt tetrapod hunter

Fig. 4

Fig. 4

Violin plots of bird body mass, by diet. Masses of carnivores (A, B) and herbivores (C, D) are grouped by trends apparent in Fig. 3C, D, excluding (A, C) and including (B, D) semi-specialists. Carnivores are split into invertivores and vertivores, herbivores are split into folivores + frugivores (FolFrug) and granivores + nectarivores (GranNect). Cut-off points, calculated using the Youden index (see “Methods”), are labelled with a line. Diets with the same letters above them do not have significantly different average masses in phylogenetic HSD at the p = 0.05 level (Table 2)

Fig. 5

Fig. 5

Phylomorphospace of avian and longipterygid unguals, based on traditional morphometrics, grouped by pedal ecology. Grey lines indicate phylogenetic relationships. Line drawings of claws for selected taxa are provided for reference. Data is visualised with PCA (A) and LDA (B). In PCA (A), PC1 describes talon curvature and PC2 describes interdigital size variation. In LDA (B), LD1 describes the size ratio of digits II and IV to digit III and LD2 describes the size ratio of digits I and IV to digit III. See Additional file 1: Fig. S1 for precise character loadings. Taxon abbreviations: Lx1 Longipteryx chaoyangensis, Lx2 Longipteryx sp., Rp Rapaxavis pani, Sw Shanweiniao cooperorum, Sj Shenjingornis yangi

Fig. 6

Fig. 6

Functional phylomorphospace of avian and longipterygid upper jaws, based on mechanical advantage and functional indices, grouped by diet. Grey lines indicate phylogenetic relationships. Data is visualised with PCA (A, B) and LDA (C, D), excluding (A, C) and including (B, D) semi-specialists. In PCA (A, B), PC1 primarily describes AMA, MCH, ACH, and AO and PC2 primarily describes OMA and PMA. In LDA (C, D), LD1 primarily describes AMA, OMA, and ACH and LD2 primarily describes AMA, PMA, and AO. Diagrams of functional indices from Fig. 2 are included roughly in the orientation they are loaded on the plot. See Additional file 1: Fig. S4 for precise character loadings. Diet abbreviations: FrugivoreH hard frugivore, FrugivoreS soft frugivore, GranivoreS swallowing granivore, GranivoreH husking granivore, InvertivoreH hard invertivore, InvertivoreM medium invertivore, InvertivoreS soft invertivore, Tetra Hunt tetrapod hunter. Taxon abbreviations: Lr Longirostravis, LxL large-toothed Longipteryx, LxS small-toothed Longipteryx, Rp Rapaxavis, Sw Shanweiniao

Fig. 7

Fig. 7

Violin plots of mesh-weighted arithmetic mean (MWAM) strain of bird lower jaw finite element models in this study, organised by more inclusive diets and the whole range of diets considered. Plots are provided excluding (A) and including (B) semi-specialists. Diets with the same letter above them are not significantly different from one another under phylogenetic HSD of their strain intervals at the p = 0.05 level (Additional file 1: Table S5). Diet abbreviations: FrugivoreH hard frugivore, FrugivoreS soft frugivore, GranivoreS swallowing granivore, GranivoreH husking granivore, InvertivoreH hard invertivore, InvertivoreM medium invertivore, InvertivoreS soft invertivore, Tetra Hunt tetrapod hunter. Taxon abbreviations: Lr Longirostravis, LxL large-toothed Longipteryx, LxS small-toothed Longipteryx, Rp Rapaxavis, Sw Shanweiniao

Fig. 8

Fig. 8

Phylogenetic strain-space of total maximum in-plane principal strain of bird lower jaw finite element models in this study. Grey lines indicate phylogenetic relationships. Contour plots for selected taxa are provided for reference. Results are visualised with PCA (A, B) and LDA (C, D), excluding (A, C) and including (B, D) semi-specialists. Results are obtained using the intervals method [34] where the percentage of model area under intervals of strain are treated as variables for multivariate analysis. Seventy five intervals were used for PCA and LDA. In PCA (A, B), overall strain increases along PC1 and unevenness of strain distribution increases along PC2. In LDA (C, D), LD1 and LD2 have loadings made of various low-strain intervals, with high-strain intervals clustering near the origin. See Additional file 1: Fig. S5 for precise character loadings. Diet abbreviations: FrugivoreH hard frugivore, FrugivoreS soft frugivore, GranivoreS swallowing granivore, GranivoreH husking granivore, InvertivoreH hard invertivore, InvertivoreM medium invertivore, InvertivoreS soft invertivore, Tetra Hunt tetrapod hunter. Taxon abbreviations: Lr Longirostravis, LxL large-toothed Longipteryx, LxS small-toothed Longipteryx, Rp Rapaxavis, Sw Shanweiniao

Fig. 9

Fig. 9

Reconstruction of the pes of large-toothed morphotype of Longipteryx gripping the mayfly Epicharmeropsis hexavenulosus from the same geological formation. Note that the mayfly is just large enough to be completely encircled by _Longipteryx_’s toes, as is typical for prey of extant owls [24]. The hindwing of E. hexavenulosus is excluded to better show the position of digit I. Longipteryx pes redrawn from specimen DNHM-D2889 [16], E. hexavenulosus redrawn from specimen CNU-E-YX-2007004 [99]

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