A tiny stem group representative of Pici (Aves, Piciformes) from the early Oligocene of the Czech Republic
We describe a new stem group representative of Pici (woodpeckers, honeyguides, barbets, and allies) from the early Oligocene (Rupelian) of the Czech Republic. The holotype of Picavus litencicensis, gen. et sp. nov. is a postcranial skeleton with well-preserved feather remains. The new species is distinguished from crown group Pici in several plesiomorphic features and is assigned to the new taxon Picavidae, fam. nov. The absence of an elongated accessory trochlea for the reversed fourth toe shows P. litencicensis to be the most basal representative of Pici, and concerning the morphology of the distal tarsometatarsus the species represents a morphological link between Pici and their sister taxon, the Galbulae. Like all other early Oligocene piciform birds, P. litencicensis is a tiny bird, the size of the smallest extant Pici. Because all Palaeogene Pici were found in Europe and some of these are outside the crown group, an Old World origin of Pici is likely. With definitive crown group representatives of Pici being unknown before the late Oligocene/early Miocene, the fossil record does not support earlier molecular calibrations, which resulted in a late Cretaceous divergence of crown group Pici.
KeywordsFossil birdsRupelianMenilite FormationPicavidae, fam. nov.Picavus litencicensis, gen. et sp. nov
Wir beschreiben einen neuen Stammgruppen-Vertreter der Pici (Spechte, Honiganzeiger, Bartvögel und Verwandte) aus dem unteren Oligozän (Rupelium) der Tschechischen Republik. Der Holotypus von Picavus litencicensis, gen. et sp. nov. ist ein postcraniales Skelett mit sehr gut erhaltener Befiederung. Die neue Art unterscheidet sich in mehreren plesiomorphen Merkmale von Kronengruppen-Pici und wird dem neuen Taxon Picavidae, fam. nov. zugeordnet. Das Fehlen einer verlängerten zusätzlichen Trochlea für die zurückgedrehte vierte Zehe weist P. litencicensis als basalen Vertreter der Pici aus, und bezüglich der Morphologie des distalen Tarsometatarsus stellt die neue Art eine morphologische Übergangsform zwischen Pici und ihrem Schwestertaxon, den Galbulae, dar. Wie alle anderen unteroligozänen piciformen Vögel ist P. litencicensis ein winziger Vogel, von der Größe der kleinsten heutigen Pici. Weil alle paläogenen Pici in Europa gefunden wurden und weil einige von diesen außerhalb der Kronengruppe sind, ist ein altweltlicher Ursprung der Pici wahrscheinlich. Da es keine definitiven Kronengruppen-Vertreter der Pici aus Ablagerungen vor dem späten Oligozän/frühen Miozän gibt, stützt der Fossilbericht keine Aufspaltung der Kronengruppen-Pici in der späten Kreidezeit, welche aus früheren molekularen Kalibrierungen resultierte.
SchlüsselwörterFossile VögelRupelMenilit-FormationPicavidae, fam. nov.Picavus litencicensis, gen. et sp. nov
Pici, the clade including woodpeckers (Picidae), honeyguides (Indicatoridae), and toucans and barbets (Ramphastidae), has a comparatively scarce fossil record, which is especially true for its Paleogene representatives (Mayr 2009; De Pietri et al. 2011). The earliest specimen is a fragmentary tarsometatarsus of uncertain affinities from the early Oligocene (stratigraphic level MP 21) of Belgium (Mayr and Smith 2001). Another early Oligocene species is Rupelramphastoides knopfi from the Rupelian (MP 23) of Germany (Mayr 2005, 2006a). This tiny species is one of the smallest representatives of Pici and is known from two partial skeletons. Concerning the long and slender legs, R. knopfi corresponds with Ramphastidae, but some presumably plesiomorphic features may indicate a position outside the crown group (Mayr 2005).
An incomplete tarsometatarsus of a member of Pici was described from the late Oligocene (MP 29) of Germany (Mayr 2001). The exact phylogenetic affinities of this specimen were considered uncertain in the original description, but De Pietri et al. (2011) noted that the distal end of the bone resembles the distal tarsometatarsus of Piculoides saulcetensis from the early Miocene (MN 1-2) of France, which is the oldest definitive record of Picidae (De Pietri et al. 2011). Indicatoridae are known from the early Pliocene of South Africa (Olson 1985), but these fossils have not yet been described. The earliest Ramphastidae belong to the taxon Capitonides and were found in the early Miocene (MN 3) of Germany (Ballmann 1969). Notably, there still appear to have been stem group representatives of Pici in the early Miocene. These belong to the Miopiconidae, a taxon that was erected by Mayr (1998) for the Moroccan Miopico benimellalensis Mayr, 1998. This latter species is only known from the distal end of a tarsometatarsus, whose morphology departs from that of extant Pici in that the accessory trochlea for the reversed fourth toe reaches much less far distally.
Here, we describe a postcranial skeleton of a new tiny piciform bird from the early Oligocene (Rupelian) locality of Litenčice (Czech Republic). The fossil was found by R.G. during an excavation campaign in 2010, which was supported by the field excavation program of the National Geographic Society.
The only other avian skeletal remains from the Litenčice locality belong to the procellariiform Diomedeoididae (Gregorová 2006), but earlier authors noted the occurrence of isolated feathers in the Menilite Formation of Moravia (Boué 1829; Kalabis 1950). Bird remains were also found in Polish sites of the Menilite Formation and belong to Trochilidae (hummingbirds), Passeriformes, and indeterminate birds (passerines; Bocheński and Bocheński 2008; Bocheński et al. 2010, 2011). Fulín and Holec (2008) further reported a bird leg from the early Oligocene (Rupelian) of the Central Carpathian basin.
Materials and methods
Osteological terminology follows Baumel and Witmer (1993). If not indicated otherwise, bone measurements refer to the maximum length along the longitudinal axis. Concerning the claws, the distance between the tuberculum extensorium and the apex phalangis was measured. The term Pici is used for the total group (Pan-Monophylum), i.e., the clade including stem and crown group.
Institutional abbreviations: MM—Moravian Museum, Brno, Czech Republic; SMF—Forschungsinstitut Senckenberg, Frankfurt am Main, Germany.
Piciformes (Meyer and Wolf, 1810)
Pici sensu Simpson and Cracraft (1981)
Picavidae, fam. nov.
Picavus, gen. nov.
Tiny piciform birds, the size of the smallest extant Picumninae, which are characterized by the following features: (1) proximal tarsometatarsus with marked, laterally directing tubercle on lateral surface, presumably for attachment of the ligamentum collaterale laterale; trochlea metatarsi IV (2) without distally elongated trochlea accessoria, (3) distal portion sharply plantarly deflected, and (4) lateroplantar surface of base excavated by a marked fossa; (5) distal end of tarsometatarsus, proximal of trochlea metatarsi III, with flat dorsal surface; (6) incisura intertrochlearis lateralis sloping laterally; (7) lateral surface of distal end at base of trochlea metatarsi IV without notch for branch of tendon of musculus extensor digitorum longus leading to fourth toe; (8) trochlea metatarsi III as long as wide; (9) proximal phalange of second toe mediolaterally curved. Characters (1) and (6) are considered autapomorphic for the new taxon. Characters (3)–(5), and (9) are apomorphies of Pici, whereas (2), (7), and (8) are plesiomorphic features that distinguish the new taxon from crown group Pici and other fossil stem group representatives of Pici (Rupelramphastoides, Miopiconidae).
Picavus, gen. nov.
Picavuslitencicensis, sp. nov.
As for family; in addition to the short trochlea accessoria, the new genus differs from the coeval Rupelramphastoides in the much stouter tarsometatarsus, which has also proportionally wider proximal and distal ends.
Picavuslitencicensis, sp. nov.
Type locality and horizon
Litenčice near Brno, Czech Republic; early Oligocene (Rupelian), Menilite Formation (standard calcareous nannonplankton zonation NP 23).
As for genus. The new species is among the smallest known representatives of Pici.
Measurements (in mm, left/right)
Carpometacarpus, ~7.9 (right); femur, ~11–12 (left); tibiotarsus, ~18–19 (right); tarsometatarsus (from cotylae to trochlea metatarsi III), ~10.5 (left), ~10.8 (right). Pedal phalanges: I1, 4.1/–; I2, 2.8/2.8; II1, 3.4/3.3; II2, ~2.8/3.0; II3, –/~3.2; III1, 3.3/3.7; III2, ~3.7/3.9; III3, ~3.6/3.8; III4, ~2.8/3.3; IV1, 2.4/–; IV2, 3.0/2.9; IV3, 3.1/2.9; IV4, 3.0/–; IV5, 3.5/3.6. Wing (measured from wrist joint), –/~56; longest primary (from tip of distal wing phalange to tip of feather), –/42.5; distalmost primary (from tip of distal wing phalange to tip of feather), –/9.5.
The species epithet refers to the type locality.
Description and comparisons
The distal end of the tarsometatarsus exhibits a distinctive morphology. The trochlea metatarsi IV is laterally splayed and plantarly reversed, which is a characteristic trait of birds with zygodactyl feet, i.e., with a permanently reversed fourth toe. In lateral view, the morphology of this trochlea corresponds with Psittaciformes (parrots), Pici, and the extinct Zygodactylidae in that its narrow distal portion is sharply plantarly deflected, resulting in a somewhat comma-shaped outline of the trochlea (the lateral surface of the trochlea metatarsi IV is damaged on the left foot). As in Picidae and Zygodactylidae but contrary to Psittaciformes and other zygodactyl birds, the lateroplantar surface of the base of the trochlea metatarsi IV is excavated by a marked fossa (Fig. 6f). The trochlea metatarsi IV of Picavuslitencicensis is shorter than that of crown group Pici and its distal end only reaches the base of the trochlea metatarsi III (Fig. 6f). The distal tarsometatarsus further differs from that of crown group Pici in that it lacks a distally elongated trochlea accessoria, which is one of the distinctive apomorphies of Pici (e.g., Ballmann 1969; Mayr 1998). Although most of this accessory trochlea cannot be observed directly in the fossil, it is clearly visible on both feet that it was short as in Galbulae (jacamars and puffbirds), the sister taxon of Pici (Fig. 6). Absence of a distally elongated trochlea accessoria is also indicated by the morphology of the first phalange of the fourth toe (see below). Contrary to crown group Pici, the incisura intertrochlearis lateralis is not concave but laterally sloping. On the lateral surface of the distal end, at the base of the trochlea metatarsi IV, there is no notch for the branch of the tendon of musculus extensor digitorum longus that leads to the fourth toe, which is typically present in crown group Pici albeit weakly marked in some species (Fig. 6h; De Pietri et al. 2011). Also unlike extant Pici but as in the zygodactyl Cuculidae (cuckoos), the dorsal portion of the trochlea accessoria forms a raised ridge, which served as a guiding structure for the tendon of musculus extensor brevis digiti IV (Steinbacher 1935: figs. 16, 17).
The dorsally bulging trochlea metatarsi III is proportionally larger than in crown group Pici and has a symmetrical shape, with a moderately deep trochlear furrow. Most of the trochlea metatarsi II of both feet is still embedded in sediment, but the narrow second toe suggests that this trochlea was also very narrow. The foramen vasculare distale is small and on both tarsometatarsi it is situated in a wide fossa, which may, however, be an artifact of the preservation of the bone. The dorsal surface of the distal end of the bone, proximal of the trochlea metatarsi III, is flat as in crown group Pici.
The toes are very long and slender. The fourth toe is the longest and preserved in a reversed position in both feet; its proximal phalanges are not as strongly abbreviated as in most Psittaciformes and Picidae. The proximal end of the first phalange of the fourth toe does not bear a plantarly directed wing-like flange, which in crown group Pici articulates with the trochlea accessoria (Fig. 6e, l). The second toe is very narrow, thus indicating a narrow trochlea metatarsi II; its proximal phalange is markedly curved mediolaterally as in Rupelramphastoides and most crown group Pici (e.g., Psilopogon pyrolophus, Ramphastidae; Fig. 6e, k). The hallux is well developed. The pedal phalanges exhibit prominent tubercula extensoria, and their distal ends are mediolaterally expanded just proximal of the capitulum phalangis. The claws are long and moderately curved, with well-developed tubercula flexoria and marked sulci neurovasculares. The claw of the hallux is the shortest, the equally sized ones of the third and fourth toes are the longest.
The wing feathers are very well preserved (Figs. 2, 4a), but those of the tail seem to have been lost together with the caudal vertebrae and the pygostyle. In both wings, the secondaries and primaries are separated into two clusters. With a length of about 56 mm, the wing is somewhat longer than that of the smallest extant Picumninae (exemplar wing lengths are 49 mm in Sasia africana, 46.5 in Picumnus cirrhatus, and 53 in P. temminckii). As in extant Pici, the distalmost primary, which is preserved on the right wing, is much shorter than the proximally adjacent one. Provided that the feathers of P.litencicensis are made up mainly of melanosome remains as seems to be the case in most fossils preserved in sediment (Vinther et al. 2008, 2010), the feathers of the new species lacked a distinct barring, which is well visible in some fossil birds (e.g., Mayr 2006b).
Although much of the holotype skeleton of Picavuslitencicensis, gen. et sp. nov. is badly crushed and does not allow the recognition of osteological details, the preservation of the feet is exquisite and the tarsometatarsus exhibits a characteristic derived morphology, which allows a phylogenetic placement of the new species.
The laterally splayed trochlea metatarsi IV and the retroverted fourth toe clearly indicate that P.litencicensis was a zygodactyl bird. Among extant birds, this derived foot arrangement is found only in Cuculiformes, Psittaciformes and Piciformes (Galbulae and Pici). Extinct early Oligocene taxa with zygodactyl feet are Eocuculus, which may be a stem lineage representative of Cuculiformes (Chandler 1999; Mayr 2006c), and the Zygodactylidae, which most likely are the sister taxon of Passeriformes (Mayr 2008).
Comparisons between Picavus and Eocuculus are limited due to the preservation of the known specimens of these taxa as skeletons on slabs, and the morphology of the trochlea metatarsi IV, for example, is not well known for Eocuculus. However, Picavus differs from Eocuculus in the less marked tuberositas musculi tibialis cranialis, the proportionally longer trochlea metatarsi III, the distinctly curved first phalange of the second toe, and the proportionally longer proximal phalanges of the fourth toe (Fig. 6a, b). Moreover, the carpometacarpus of Picavus is much shorter than the tarsometatarsus, whereas it is only slightly so in Eocuculus (ratio carpometacarpus: tarsometatarsus 0.65 in P.litencicensis versus 0.89 in E. cherpinae, after measurements in Chandler 1999).
Among other features (e.g., the deep caudal incisions of the sternum and the narrow processus terminalis ischii), Picavuslitencicensis is distinguished from extant Cuculiformes in the shape of the trochlea metatarsi IV, which exhibits a very small lateral portion with a sharply plantarly deflected distal section. The undoubtedly derived condition seen in Picavus occurs only in Psittaciformes, Zygodactylidae, and Pici. The Czech fossil differs from Psittaciformes and agrees with Pici and Zygodactylidae in that the carpometacarpus is proportionally shorter, the caudal margin of the sternums bears two pairs of deep incisions, and in that the base of the trochlea metatarsi IV is lateroplantarly excavated by a marked fossa (in Galbulae, this feature is weakly developed in Galbulidae but absent in Bucconidae). At least the latter of these characters is derived for neornithine birds and is here interpreted as a synapomorphy of Picavus and Pici, which evolved convergently in Zygodactylidae. Contrary to P.litencicensis, early Oligocene Zygodactylidae have a distally elongated trochlea accessoria and the new species further differs from Zygodactylidae in the proportionally much shorter tarsometatarsus.
Apart from the just-mentioned derived shape of the trochlea metatarsi IV (which is shared with zygodactylids), assignment of P.litencicensis to Pici is supported by two other derived characters, i.e., the flat dorsal surface of the distal tarsometatarsus (convex in zygodactylids and most other birds) and the very narrow trochlea metatarsi II (as indicated by the narrow second toe). P. litencicensis differs from crown group Pici in the short trochlea accessoria, which, by outgroup comparisons with Galbulae, the sister taxon of Pici (e.g., Mayr et al. 2003; Ericson et al. 2006; Hackett et al. 2008), is plesiomorphic for Piciformes. This latter feature identifies the fossil species as a stem group representative of Pici.
Mayr (2005) noted that Rupelramphastoides may possibly be outside crown group Pici, but the affinities of this taxon are not yet unambiguously resolved. Unlike Picavus, Rupelramphastoides does exhibit the characteristic, distally elongated trochlea accessoria of crown group Pici, and Picavus is certainly outside a clade including Rupelramphastoides and crown group Pici. The trochlea accessoria of the early Miocene Miopiconidae is shorter than that of Rupelramphastoides and crown group Pici, but nevertheless much better developed than in Picavus. The absence of a distally elongated trochlea accessoria shows P.litencicensis to be the most basal representative of Pici and, concerning the morphology of the distal tarsometatarsus, the species represents a morphological link between Galbulae (which primitively lack a distally elongated trochlea accessoria) and Pici (which have a dorsally flat distal tarsometatarsus and exhibit the derived shape of the trochlea metatarsi IV visible in P. litencicensis).
All Palaeogene Pici known so far have been found in Europe, and because some of these are clearly (Picavus) or possibly (Rupelramphastoides) outside the crown group, an Old World origin of Pici is likely. This is also supported by the interrelationships of the extant taxa, as molecular phylogenies of both Picidae (Fuchs et al. 2007) and Ramphastidae (Moyle 2004) indicate an Old World origin of these taxa. Ramphastidae probably colonized the New World only once (Moyle 2004), whereas the biogeographic history of Picidae is more complex, involving multiple dispersal events (Fuchs et al. 2007). Definitive crown group Pici are unknown before the late Oligocene/early Miocene, and the fossil record does thus not support a late Cretaceous divergence as derived from earlier molecular clock estimations (Nahum et al. 2003).
Notably, all early Oligocene Pici belong to tiny species, which reached only the size of the smallest extant representatives of the group, i.e., the species of Picumninae. Very small piciform birds still occur in the Old and New World tropics today, and the reasons that led to their disappearance in Europe are unknown. Mayr (2005) hypothesized that food competition with passerines during the cold Northern Hemispheric winters may have played a role. However, we now consider it more likely that disappearance of tiny Pici from Europe was related directly to the emergence of a marked Northern Hemispheric seasonality during the Cenozoic (see, e.g., Mosbrugger et al. 2005). With few exceptions, such as the Eurasian Wryneck (Jynx torquilla), most Pici have poor migration capabilities (del Hoyo et al. 2002), and today only Jynginae and true Picinae (woodpeckers) occur in Northern latitudes. During the cold winter months, woodpeckers usually change their diet from insects and their larvae to seeds and nuts (del Hoyo et al. 2002). All other Pici, however, feed mainly on insects and fruits and are thus more prone to food shortage under unfavorable climatic conditions, which is especially true for very small species that have a lower fasting endurance and are affected by heat loss to a greater extent (e.g., Ashton 2002). Cenozoic climatic cooling thus seems to be a likely explanation for the disappearance of tiny Pici from Europe, but more data on the exact extinction date need to be gathered before well-founded hypotheses can be put forth.
We thank Olaf Vogel for the expert preparation of the legs of the fossil and Sven Tränkner for taking the photographs. This study was supported by research project MK 00009486201 of the Moravian Museum, Brno, and a research and exploration grant for “Field Excavation of Oligocene Deep-sea Fauna at the Litenčice pit (West Carpathians, Czech Republic)” from the National Geographic Society (grant number 8786-10). Comments by D. Ksepka and an anonymous referee improved the manuscript.