Australia: The Land Where Time Began

A biography of the Australian continent 

Deinonychus – Predatory Ecology and the Origin of Flapping Birds

Fearsome serrated teeth and sharp claws are features that characterise most non-avian dinosaurs. It has been hypothesised that the hypertrophied ‘killing claw’ on pedal digit (D) II of Deinonychus (Paraves: Dromaeosauridae), a maniraptoran theropod, was an adaptation for predatory slashing or climbing, which led to the suggestion that Deinonychus, as well as other dromaeosaurids were cursorial predators that had specialised for actively attacking and killing prey that were several times larger than themselves. This hypothesis is, however, problematic as extant animals with such hypertrophied claws do not use them to slash or climb up prey. In this paper Fowler et al. offer an alternative interpretation: that the hypertrophied D-II claw on dromaeosaurids was functionally analogous to an enlarged talon, which is also on D-II of Accipitridae (hawks and eagles; a family of birds that are commonly called “raptors”). According to this suggestion the talon is used to maintain the grip on the prey, which is smaller than the predator, while the prey is pinned down by the body weight of the raptor and is dismembered by the beak. The morphology of the foot of Deinonychus is consistent with a grasping function, which supports the prey immobilisation behaviour model. Opposite morphological trends within Deinonychosauria (Dromaeosauridae and Troodontidae) indicate ecological separation. In the context of avian evolution, the grasping foot of Deinonychus as well as other terrestrial predatory paravians is hypothesised to have been an exaptation (an existing trait that has been used in the evolution of a new behaviour) for the grasping foot of arboreal perching birds. In this paper Fowler et al. also describe “stability flapping”, a novel behaviour used for positioning and stability in the initial stages of immobilisation of the prey, which may have been pivotal to the evolution of the flapping stroke. The perception of predatory dinosaurs has been overhauled by these findings and highlights the role of exaptation in the evolution of novel structures and behaviours.

Deinonychus is usually depicted as a fast, intelligent  predator, that hunts in packs in order to take down prey that are larger than any individual in the pack (Manning et al., 2006; Maxwell & Ostrom, 1995; Carpenter, 1998). Cladistic analyses recovered Deinonychosauria (Senter, 2007) (Dromaeosauridae + Troodontidae) as the sister group of birds, which has prompted debate about how flight might have evolved from a Deinonychosaurian-like ancestor. Speculation has been the basis of what has been typically assumed about the ecology of Deinonychus, and Deinonychosauria in general. Few analyses have compared the claw morphology of dinosaurs to that of animals with known ecologies (Glen & Bennett; Feduccia, 1993), though much interest has been generated by the enlarged pedal D-II claw, mainly a result of a paucity of research carried out on claw morphology and function in general (Carpenter, 1998; Feduccia, 1993; Csermely & Rossi, 2006); although see (Van Valkenburgh, 1987; Zani, 2000). It was demonstrated by a novel experiment by Manning et al. (Manning et al., 2006) that the hypertrophied  D-II claws would not be effective in slashing, suggesting instead that it was used by dromaeosaurids as a climbing crampon for gripping the hides of prey that were several times larger than themselves (see supporting information Text S1for further review). Fowler et al. agree that the D-II claw is a most effective device, though modern analogues with similarly hypertrophied D-II claws don’t use them to climb up prey.

Variation in foot morphology in extant birds is associated with variation associated with factors such as speed, strength, agility, and even diet (Glen & Bennett, 2007; Csermely, 2006; Fisher, 1946; Goslow, 1972; Jollie, 1977; Raikow, 1985; Hopson, 2001; Rasmussen et al., 2001; Zhou & Farlow, 2001; Peters & Görgner, 1992; Ward, Weigl & Conroy, 2002; Fowler, Freedman & Scannella, 2009; Green, Barnes & Brooke, 2009). The way in which foot morphology is related to predatory behaviour in extant birds of prey has been investigated in a recently published study by Fowler et al (Fowler, Freedman & Scannella, 2009). In the study it was shown for the first time that the Accipitridae (hawks and eagles) also have a conspicuously hypertrophied talon on D-II and that this is used for the immobilisation of prey.

For extant predators it is important to subdue their prey quickly to avoid them escaping or fighting back. Prey immobilisation among extant raptors is variable and depends mostly on the relative size of the prey (Fowler, Freedman & Scannella, 2009), immobilisation of  prey is preferred to killing because accipitrids often begin feeding before the prey is dead (Harris, 1984; Newton, 1986). All birds of prey immobilise small prey that can be contained within the foot, assisted by constriction and beak attacks (Harris, 1984; Newton, 1986; Bond, 1936; Csermely, Mainardi & Agostini, 1991; Csermely & Gaibani, 1998). Among owls, which are small prey specialists (Ward, Weigl & Conroy, 2002), physical adaptations for increasing the strength of the feet are more developed. Immobilisation is aided by attempts to snap the spinal cord or crush the head with the beak among falcons and some owls. To accomplish this falcons have evolved a stronger bite force and a specialised “tomial tooth” on the beak. Large prey, are those that cannot be contained within the foot, and therefore cannot be constricted (Fowler, Freedman & Scannella, 2009) (Supporting information videos S1 and S2). Raptors pin large prey to the ground with their body weight to prevent escape, and then pluck feathers or fur to expose an area of flesh. Falcons attempt to quickly kill the prey by snapping the spinal cord, though accipitrids lack the physical specialisations to do this. Accipitrids have hypertrophied talons on D-I and D-II which are adaptations to manipulate grip on large struggling prey (Fowler, Freedman & Scannella, 200920). The talons of accipitrids lock into their prey and keep hold despite vigorous struggling of the prey, which allows the raptors to begin feeding. Death of the victim is hastened by massive blood loss in such cases while it is being eaten alive.

An understanding of how predatory ability is affected by foot morphology in extant birds can inform interpretations of similar variation that is observed in extinct non-avian theropods. Previous studies of comparison of the hindlimb morphology of dinosaurs have mainly focused on locomotion (Hutchinson & Allen, 2009) and references therein). The hindlimb is, however, just a component of the locomotor system, and the hindlimb in many taxa of theropod there are features that are consistent with hooking and grasping functions. The purpose of this paper is to elucidate the functional morphology of the pes of Deinonychosauria by comparison of the findings of the sibling study by Fowler et al. Raptor Prey Restraint (RPR or “ripper” model. Many of the peculiarities of the anatomy of Deinonychosauria are associated with specific predatory behaviour when this approach has been combined with considerations of phylogenetic trends that have already been recognised within the theropods. It is suggested by Fowler et al. that the enlarged D-II claws of deinonychosaurians were used to grapple prey in a fashion that is comparable to accipitrid birds of prey, and a part of a suite of features indicating ecological separation within Deinonychosauria and Paraves. Several new lines of research are opened by these findings into the predatory abilities of extinct theropods, and the evolution of novel structures and behaviours that lead to the birds. Included in this is description of a new flapping behaviour that may have implications for origin of flight.

Conclusions

Multiple new concepts that provide functional explanations for the morphological peculiarities of Deinonychus as well as other paravians are presented by the Raptor Prey Restraint (RPR) model. Many new lines of research into the predatory ability of extinct theropods are opened by these findings, as well as emphasising the importance of exaptation in the evolution of novel behaviours. The hypertrophied D-II talon on the feet of Accipitridae represents the closet analogue that has yet been presented for the similarly hypertrophied D-II talon of the Deinonychosauria. Within the Deinonychosauria gradual divergence of the proportions of the foot potentially indicates ecological separation between Dromosauridae and Troodontidae as large and small prey specialists respectively. Fowler et al. suggest that an analysis of foot functional morphology, which has the potential to test the hypotheses that have been presented recently by Zanno & Makovicky (Zanno & Makovicky, 2011) should be included in future research. A shift in emphasis for the restraint of prey from the manus to the pes, as the forelimbs became increasingly feathered and adapted for flapping functions through Coelosauria is demonstrated by the grasping foot of paravians.

According to Fowler et al. they hope to have opened a new direction of study in the evolution of flight in birds by their description of stability flapping and its importance to predatory success. It is demonstrated by the RPR model that there is no need for a scenario in which flight is gained (and lost) many times (Paul, 2002). Instead, Fowler et al. present the “flapping first” hypothesis which they claim is more parsimonious: that a range of flapping behaviours not related to flight were exhibited by the basal paravians (Burgers & Chiappe, 1999; Dial, 2003), though only the Avialae evolved true flapping flight as a method of aerial locomotion.

A definition of stability flapping is in preparation that is more precise so that studies in the future can focus better on potential osteological and biomechanical correlates. Other flapping behaviours not involving flight also require further investigation, which includes stability flapping that is executed outside of a predatory role. Therefore, there is much work that is required to characterise stability flapping, though as in the case of other models that have been proposed recently (Burgers & Chiappe, 1999; Dial, 2003) understanding (Padian & de Ricqles, 2009) of the physical capabilities of the ancestral taxa of modern birds is enriched by recognition of this novel behaviour.

Sources & Further reading

1. Fowler, D. W., E. A. Freedman, J. B. Scannella and R. E. Kambic (2011). "The Predatory Ecology of Deinonychus and the Origin of Flapping in Birds." PLoS ONE 6(12): e28964.