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. 2011;6(12):e28964.
doi: 10.1371/journal.pone.0028964. Epub 2011 Dec 14.

The predatory ecology of Deinonychus and the origin of flapping in birds

Denver W Fowler  1 , Elizabeth A Freedman, John B Scannella, Robert E Kambic
Affiliations

The predatory ecology of Deinonychus and the origin of flapping in birds

Denver W Fowler et al. PLoS One. 2011.

Abstract

Most non-avian theropod dinosaurs are characterized by fearsome serrated teeth and sharp recurved claws. Interpretation of theropod predatory ecology is typically based on functional morphological analysis of these and other physical features. The notorious hypertrophied 'killing claw' on pedal digit (D) II of the maniraptoran theropod Deinonychus (Paraves: Dromaeosauridae) is hypothesized to have been a predatory adaptation for slashing or climbing, leading to the suggestion that Deinonychus and other dromaeosaurids were cursorial predators specialized for actively attacking and killing prey several times larger than themselves. However, this hypothesis is problematic as extant animals that possess similarly hypertrophied claws do not use them to slash or climb up prey. Here we offer an alternative interpretation: that the hypertrophied D-II claw of dromaeosaurids was functionally analogous to the enlarged talon also found on D-II of extant Accipitridae (hawks and eagles; one family of the birds commonly known as "raptors"). Here, the talon is used to maintain grip on prey of subequal body size to the predator, while the victim is pinned down by the body weight of the raptor and dismembered by the beak. The foot of Deinonychus exhibits morphology consistent with a grasping function, supportive of the prey immobilisation behavior model. Opposite morphological trends within Deinonychosauria (Dromaeosauridae + Troodontidae) are indicative of ecological separation. Placed in context of avian evolution, the grasping foot of Deinonychus and other terrestrial predatory paravians is hypothesized to have been an exaptation for the grasping foot of arboreal perching birds. Here we also describe "stability flapping", a novel behaviour executed for positioning and stability during the initial stages of prey immobilisation, which may have been pivotal to the evolution of the flapping stroke. These findings overhaul our perception of predatory dinosaurs and highlight the role of exaptation in the evolution of novel structures and behaviours.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. RPR “ripper” behavioural model, illustrated by a small dromaeosaurid.
(A) grasping foot holds on to prey. (B) hypertrophied D-II claw used as anchor to maintain grip on large prey. (C) predator's bodyweight pins down victim. (D) beam-like tail aids balance. (E) low-carried metatarsus helps restrain victim. (F) “stability flapping” used to maintain position on top of prey (see Supporting Information Videos S1 and S2). (G) arms encircle prey (“mantling”), restricting escape route. (H) head reaches down between feet, tearing off strips of flesh (may explain unusual deinonychosaurian dental morphology). Victim is eaten alive or dies of organ failure.
Figure 2
Figure 2. Phylogenetic distribution of characters pertinent to the RPR model.
1. D-II ungual larger than D-III; 2. elongate metatarsus; 3. arctometatarsalian metatarsus; 4. short robust metatarsus; 5. dorso-ventrally flattened pedal unguals; 6. D-II ungual smaller than D-III; 7. elongate D-IV; 8. hyperextensible D-II; 9. enlarged D-II ungual; 10. subarctometatarsalian metatarsus; 11. hypertrophied D-II ungual; 12. reduced forelimbs; 13. stiffened tail; 14. ginglymoid distal articulations of metatarsals. Phylogeny from Senter .
Figure 3
Figure 3. Correspondence Analysis comparing relative ungual and digit sizes of Deinonychus and extant avians.
Deinonychus plots nearest to Accipitridae, emphasizing similarity in pedal morphology. Axis 1  = 50.68% of variation, Axis 2 = 24.15% of variation. Extant avian data (mostly birds of prey) from Fowler et al. . n = 42.
Figure 4
Figure 4. Correspondence Analysis comparing relative proportions of pedal non-ungual phalanges among non-avian theropod dinosaurs.
Separation along Axis 1 (64.99% of variation) discriminates cursorial Ornithomimidae from less-cursorial Dromaeosauridae. Troodontidae plot closer to Ornithomimidae than their sister-taxon Dromaeosauridae, indicating a more cursorial habit. Archaeopteryx plots close to Dromaeosauridae, but in a more intermediate position, as do Tyrannosauroidea, Allosauroidea, and Ceratosauridae. The separation of Archaeopteryx from Tyrannosauroidea and Allosauroidea along Axis 2 (13.89% of variation) suggests an additional discriminatory aspect of phalanx proportions. n = 30.
Figure 5
Figure 5. Variation in foot proportions consistent with cursoriality or grasping.
Cursorial-proportioned feet of Gallimimus (A) and Allosaurus (B) exhibit D-II and D-IV of subequal lengths, with D-IV significantly shorter than D-III. This is contrasted with Deinonychus (C) where D-IV is significantly elongated, being subequal in length to D-III, with distal-most non-ungual phalanges of D-III and IV subequal in length to the preceding penultimate non-ungual phalanx; features consistent with a grasping habit . Scale  = 5 cm. Modified from original sources , , .
Figure 6
Figure 6. Comparison of ginglymoid vs non-ginglymoid articulation facets in first pedal phalanges of Troodon sp. (all dorsal view).
The distal articulation facet is ginglymoid in D-II-1 (A; MOR 553S-6.29.9.89), but not in D-III-1 (B; MOR 553S-8.11.9.209) or D-IV-1 (C; MOR 553S-8.11.92.213). Specimens are derived from a multi-individual bonebed and may not be from the same individual, hence differences in size are not relevant. Scale bar  = 2 cm.
Figure 7
Figure 7. Comparison of ginglymoid vs non-ginglymoid articulation facets in first pedal phalanges of Deinonychus (MOR 747; all dorsal view).
The distal articulation facet is ginglymoid in D-II-1 (A), D-III-1 (B) and more weakly so in D-IV-1 (C). Specimens found as part of an articulated pes. Scale bar  = 2 cm.
Figure 8
Figure 8. Ventral view of Deinonychus foot (MOR 747) in flexion.
D-I is not reversed, but is rotated slightly so that the claw faces laterally into the ‘fist’, as observed in articulated specimens of Velociraptor . Ginglymoid articulation facets of MT-II and III restrict the motion of D-II and III to a parallel dorso-ventral plane, but the distal ball joint of MT-IV allows D-IV to take a variable position, spreading more laterally, or allowing it to reach over the metatarsus, opposing D-I. Not shown at maximum flexion. Scale  = 5 cm.
Figure 9
Figure 9. MOR 553S-8.6.92.168, Troodon sp. left MT-I in posterior (A), anterior (B), medial (C), and dorsal (D) views.
MT-I has a ball-shaped articulation facet, allowing greater movement and positioning of D-I compared to MT-I of Deinonychus (Figure 10). Scale bar  = 2 cm.
Figure 10
Figure 10. MOR 747, Deinonychus left MT-I in posterior (A), anterior (B), medial (C), and dorsal (D) views.
MT-I has a ginglymoid articulation facet, limiting movement, but increasing strength, contrasting with the more mobile MT-I of Troodon sp. (Figure 9). Scale bar  = 2 cm.
Figure 11
Figure 11. Wing proportions of birds.
(A) Archaeopteryx. (B) Variation of wing aspect ratio in extant birds, from left (low) to right (high): goshawk (Accipiter gentilis), golden eagle (Aquila chrysaetos), northern royal albatross (Diomedea sanfordi). The short broad wings of Archaeopteryx are similar to the goshawk, where they afford great maneuverability. Image in (A) altered from Longrich .
See this image and copyright information in PMC

References

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