Phorusrhacidae

Phorusrhacids, colloquially known as terror birds, are an extinct clade of large carnivorous flightless birds that were the largest species of apex predators in South America during the Cenozoic era; their temporal range covers from 62 to 1.8 million years (Ma) ago.

They ranged in height from 1 – tall. Their closest modern-day relatives are believed to be the 80 cm-tall seriemas. Titanis walleri, one of the larger species, is known from Texas and Florida in North America. This makes the phorusrhacids the only known large South American predator to migrate north in the Great American Interchange that followed the formation of the Isthmus of Panama land bridge (the main pulse of the interchange began about 2.6 Ma ago; Titanis at 5 Ma was an early northward migrant).

It was once believed that T. walleri became extinct in North America around the time of the arrival of humans, but subsequent datings of Titanis fossils provided no evidence for their survival after 1.8 Ma. Still, reports from Uruguay of new findings of relatively small forms dating to 450,000 and 17,000 years ago, would imply that some phorusrhacids survived there until very recently (i.e., until the late Pleistocene); but this claim is debated.

Phorusrhacids may have even made their way into Africa; the genus Lavocatavis was recently discovered in Algeria, but its status as a true phorusrhacid is questioned. A possible European form, Eleutherornis, has also been identified, suggesting that this group had a wider geographical range in the Paleogene.

The closely related bathornithids occupied a similar ecological niche in North America across the Eocene to Early Miocene; some, like Paracrax, reached sizes similar to the largest phorusrhacids. At least one analysis recovers Bathornis as sister taxa to phorusrhacids, on the basis of shared features in the jaws and coracoid, though this has been seriously contested, as these might have evolved independently for the same carnivorous, flightless lifestyle.

Description
Based on Claudia P. Tambussi, Ricardo de Mendoza, Federico J. Degrange, and Mariana B. Picasso’s work, the phorusrhacid’s neck can be divided into three main regions (region 1, region 2, and region 3). In the higher regions of the neck, the phorusrhacid has bifurcate neural spines (BNS), while it has high neural spines in its lower regions. This suggests that the phorusrhacid had a highly flexible and developed neck allowing it to carry its heavy head and strike with terrifying speed and power. Although the phorusrhacid externally looks like it has a short neck, its flexible skeletal neck structure proves that it can expand farther beyond the expected reach and intimidate its prey using its height, allowing it to strike more easily. Once stretched out into its full length in preparation for a downward strike, its developed neck muscles and heavy head can produce enough momentum and power to cause fatal damage to the terror bird’s prey.

Kelenken guillermoi, from the Langhian stage of the Miocene epoch, some 15 million years ago, discovered in Patagonia in 2006, represents the largest bird skull yet found. The fossil has been described as being a 71 cm, nearly intact skull. The beak is roughly 46 cm long and curves in a hook shape that resembles an eagle's beak. Most species described as phorusrhacid birds were smaller, 60 - 90 cm tall, but the new fossil belongs to a bird that probably stood about 3 m tall. Scientists theorize that the large terror birds were extremely nimble and quick runners, able to reach speeds of 48 km/h. Examination of phorusrhacid habitats also indicates that phorusrhacids may have presented intense competition to predatory marsupial sparassodonts such as borhyaenids and thylacosmilids, causing the mammalian predators to choose forested habitats to avoid the more successful and aggressive avian predators on the open plains.

Palaeobiology
Most phorusrhacids were very fast runners. All members possessed a large, sharp beak, a powerful neck and sharp talons. However, even with these attributes, the phorusrhacids are often assumed to have preyed on relatively small animals (about the size of a rabbit) that could be dispatched with a minimum of struggle. This is due to the fact that with the phorusrhacids' beak proportions, the jaw could not generate a great deal of bite force with which to kill the prey. This is disputable as many big-game hunting predators such as Smilodon, great white sharks and Allosaurus have weaker bite forces and often laterally weak skulls as adaptations towards, not away from, killing large prey, relying instead on the presence of a cutting edge, a wide gape made possible by the reduction of jaw musculature, and the driving force of the body or neck. Since phorusrhacids share many of the same adaptations, such as a large, laterally flattened skull with a sharp-edged beak and powerful neck musculature, it is possible that they were specialized predators of relatively large prey.

The bones of the beak were tightly fused together, making the beak more resilient to force from the front to back direction, thus suggesting that it could cause a great amount of harm through pecking as opposed to side-to-side head movements like shaking prey. Generally speaking, it is thought that a terror bird would use its feet to injure prey by kicking it, and to hold the prey down and dispatch by pecking at it with its large beak. Larger prey may also have been attacked by pecking and kicking, or by using the beak as a blade to strike at or slash vital organs.

It has been recently shown that at least some phorusrhacids like Andalgalornis, while very fast runners in a straight line, were poor at tight turns at speed, which contradicts the idea of phorusrhacids being agile predators of small prey.

Diet
All phorusrhacids are thought to have been carnivorous. The strong downwards curve from the tip of this beak suggests that it ripped the flesh from the body of other animals. Many extant bird species with this feature are carnivorous. CT scans performed on the skull of a phorusrhacid reveal that the species would not have been able to shake its prey side to side, but rather exert significant downward force.

Extinction
During the Miocene and early Pliocene epochs, there was an increase in the phorusrhacid population size in South America, suggesting that, in that time frame, the various species flourished as predators in the savannah environment.

When the Isthmus of Panama emerged, 2.7 million years ago, carnivorous dogs, bears, and cats from North America were able to cross into South America, increasing competition. (They had been preceded by procyonids as early as 7.3 million years ago. ) The population of phorusrhacids declined thereafter, suggesting that competition with newly arrived predators was a major contributor to their extinction. Similar ideas have been considered for sparassodonts and for South America's terrestrial sebecid crocodilians.

However, the role of competitive displacement in South American predator lineages is now being questioned by some researchers. The timing of turnover events does not correlate well with the arrival of large carnivores like canids or sabretooths (although it does correlate well with the earlier-arriving procyonids), with native South American predator lineages (including most phorusrhacids and all sparassodonts and sebecids) dying out well before the arrival of most larger placental carnivores. Bathornithids, which were similar in ecology and are likely close relatives of phorusrhacids, existed entirely within North America during part of the Cenozoic and competed successfully for a time with large carnivorans such as nimravids, before becoming extinct in the Early Miocene, about 20 million years ago. The phorusrhacid Titanis expanded northward into a small area of North America during the Interchange and coexisted for several million years with large canids and big cats like Xenosmilus, before its extinction about 1.8 million years ago.

There were some suggestions that phorusracids, like the majority of Pleistocene megafauna, were killed off by human activity such as hunting or habitat change. This idea is no longer considered valid, as improved dating on Titanis specimens show that the last phorusracids went extinct over one million years before humans arrived. However, fossil finds in South America dating to the late Pleistocene indicate that Psilopterus, a relatively small form, may have been present until 96,040 ± 6300 years ago. If true, this extends the existence of this group of avian predators considerably.

Recent skull discoveries
In the past, these birds were thought to have high beaks, round orbits, and vaulted braincases though there was never enough empirical evidence to support this. However, new fossils have been discovered in Cormollo, Argentina. These skulls reveal that the terror bird has a triangular dorsal view, a rostrum that is hooked and more than half the length of the actual skull, and a more compact caudal portion. The external nares and antorbital fenestras (areas found in the nose) were found to be more square than triangular. These all contribute to a skull that is more rectangular in view rather than triangular. The structure of the fossils also suggest that these birds may have been swifter than originally thought.

A skull from a smaller subspecies of this bird was also found recently. With this fossil, it was found that the internal structure of the beak is hollow and reinforced with thin-walled trabeculae. There is also an absence of both zona flexoria palatina and zona flexoria arcus jugalis, which are key features that relate to the evolution of cranial akinesis. The discovery of this skull allows for the establishment of primary osteological homologies, which are useful in comparative anatomy, functional morphology, and phylogenetic studies.

Classification
The etymology of the name Phorusrhacidae is based on the type genus Phorusrhacos. When first described by Florentino Ameghino in 1887, the etymology of Phorusrhacos was not given. Current thinking is that the name is derived from a combination of the Greek words "phoros", which means bearer or bearing, and "rhacos", which translates to wrinkles, scars or rents. Researchers have compared Phorusrhacidae with the living families of Cariamidae and Sagittaridae, but their differences in body mass are too drastic, and thus, one cannot overly depend on these living families for answers.

Following the revision by Alvarenga and Höfling (2003), there are now 5 subfamilies, containing 14 genera and 18 species: These species were the product of adaptive radiation.

Family Phorusrhacidae
 * Genus Patagorhacos - Early Miocene of Rio Negro Province, Argentina.
 * Subfamily Brontornithinae — gigantic species, standing over 2.3 m high. Placement in Phorusrhacidae and/or monophyly disputed.
 * Genus Brontornis (Early - Middle Miocene)
 * Genus Paraphysornis (Late Oligocene/Early Miocene of São Paulo State, Brazil)
 * Genus Physornis (Middle - Late Oligocene of Santa Cruz Province, Argentina)
 * Subfamily Phorusrhacinae — giant species 3.2 m high, but somewhat slender and decidedly more nimble than the Brontornithinae
 * Genus Devincenzia (Late Miocene - Early Pliocene of NE Argentina and Arroyo Roman, Uruguay)
 * Genus Kelenken (Middle Miocene of Río Negro province, Argentina; largest known phorusrhacid)
 * Genus Phorusrhacos (Early - Middle Miocene)
 * Genus Titanis (Early Pliocene - Early Pleistocene)
 * Subfamily Patagornithinae — intermediate sized and very nimble species, standing around 1.7 m high
 * Genus Patagornis (Santa Cruz Early - Middle Miocene of Santa Cruz Province, Argentina) - includes Morenomerceraria, Palaeociconia, Tolmodus
 * Genus Andrewsornis (Middle - Late Oligocene of S Argentina)
 * Genus Andalgalornis (Late Miocene - Early Pliocene)
 * Subfamily Psilopterinae — small species, standing 70 - 100 cm high
 * Genus Eleutherornis (Middle Eocene of Rhône, France)
 * Genus ?Paleopsilopterus (Middle Paleocene of Itaboraí, Brazil) (identity as a phorusrhacid dubious)
 * Genus Procariama (Late Miocene - Early Pliocene of Catamarca Province, Argentina)
 * Genus Psilopterus (Deseado Middle Oligocene - Arroyo Chasicó Late Miocene of S and E Argentina)
 * Subfamily Mesembriornithinae — medium-sized species, standing between 1.2 - 1.5 m high
 * Genus Mesembriornis (Late Miocene - Late Pliocene)
 * Genus Llallawavis (Late Pliocene)

Alvarenga and Höfling did not include the Ameghinornithidae from Europe in the phorusrhacoids; these have meanwhile turned out to be more basal members of Cariamae. Though traditionally considered as members of the Gruiformes, based on both morphological and genetic studies (the latter being based on the seriema ) they may belong to a separate group of birds (the Cariamae) and their closest living relatives, according to the last nuclear studies, are a clade conformed by Falconidae, Psittaciformes and Passeriformes