Two-phase extinction of “Southern Hemispheric” birds in the Cenozoic of Europe and the origin of the Neotropic avifauna
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- Mayr, G. Palaeobio Palaeoenv (2011) 91: 325. doi:10.1007/s12549-011-0062-4
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A considerable number of fossil birds from the Cenozoic of Europe belong to taxa whose extant representatives are only found in the Southern Hemisphere. This study presents the first detailed analysis of the stratigraphic occurrences of these groups. Two well-separated extinction phases can be distinguished: one in the Paleogene, which concerned birds with crown group representatives in South America, Madagascar and Australia, and the second in the Miocene, which involved taxa that are today found in Africa or have a pantropic distribution. It is hypothesised that this unusual pattern is the result of a successive action of biotic and abiotic factors. South America was least affected by both extinction phases and served as a refugium for bird groups, which had a more widespread distribution in the Paleogene.
KeywordsBiogeographyFossil birdsClimatic coolingGrande coupure
As early as the 19th century it was noted that the Cenozoic avifauna of Central Europe includes representatives of avian groups that today inhabit the tropic and subtropic regions, such as parrots and trogons (e.g. Milne-Edwards 1867–1871). As our knowledge of the Cenozoic avifaunas of the Northern Hemisphere increased, it has become evident that many other avian taxa have a complex biogeographic history.
Europe in particular has an extensive and well-studied fossil record, which for some geological intervals provides a detailed picture of the prevalent avifaunas and indicates that the extant distribution of many Southern Hemispheric avian “families” is relictual (Mayr 2009a; Mourer-Chauviré 1982; Olson 1989; contra Cracraft 2001). Olson (1989: p. 2024) even concluded that “almost all the major taxa that are ‘characteristic’ of the southern continents are actually relicts of once more widespread groups that occurred in the Northern Hemisphere in the Paleogene or even later”.
In particular, a large number of birds existed in the Cenozoic of Europe whose closest extant relatives only occur in South or Central America (Mourer-Chauviré 1999). It has been briefly noted that the extinction of the “South American” taxa precedes that of other “Southern Hemispheric” avian groups in the Miocene (Blondel and Mourer-Chauviré 1998), but the extent, timing and cause of these extinctions remain elusive. Whereas some authors assume that ecological competition played a major role (Mayr 2009a; Olson 1989), others consider global cooling during the Cenozoic to be the main cause (Hawkins et al. 2006; Lindow and Dyke 2006; Martin 2010).
Here I give the first detailed stratigraphic account on the occurrence of “Southern Hemispheric” birds in Europe and show that the extinction dates of these taxa correlate closely with the distribution area of their extant representatives. Successive and independent actions of biotic and abiotic factors best explain the observed two-phase extinction pattern.
The stratigraphic occurrences of 71 bird species from Cenozoic Northern Hemispheric localities are analysed whose crown group representatives either have a pantropical distribution or are only found on the Southern Hemispheric continents, i.e., South America, Africa (including Madagascar) and Australia. The Podargidae (frogmouths), whose crown group representatives live in Australia and southeast Asia, are also considered. Taxonomic sampling is restricted to well-constrained exemplar species per stratigraphic unit. With the exception of few records of Anhingidae (darters) there are no aquatic birds from Cenozoic Northern Hemispheric fossil sites whose crown group representatives have a pantropic distribution or are restricted to the Southern Hemisphere, and all taxa considered in this analysis represent terrestrial or arboreal birds. The temporal focus is on Eocene and Miocene fossils because the poorly known Paleocene avifaunas include no taxa of relevance for the present study, whereas Pliocene avifaunas have an essentially modern higher level composition. The data are based on both own examination of fossils (mainly Paleogene European taxa) and a literature review.
Results and comments
All taxa which disappeared in the Miocene occur today in the Ethiopian zoogeographic realm or have a pantropic extant distribution. Some of these groups, i.e., Coliiformes (mousebirds), Trogoniformes (trogons) and Psittaciformes (parrots), have a long evolutionary history in Europe. For others, there exists an earlier fossil record in Africa, and these birds may have dispersed into Europe during the Miocene thermal maximum. Such was probably the case for Struthionidae (ostriches), which first occur in the early Miocene of Namibia (Mourer-Chauviré et al. 1996), Bucorvinae (ground hornbills), which were reported from the middle Miocene of Morocco (Brunet 1971), and Musophagiformes (turacos), which have a fossil record in the early Oligocene of Egypt (Rasmussen et al. 1987).
In contrast, all taxa that became extinct in the Paleogene have crown group representatives in South or Central America, Madagascar or southeast Asia and Australia. Pervasive as the “South American” pattern appears, the list of involved groups may not even be complete, as only published species with a substantial fossil record were considered. Not included, for example, are putative early Eocene Anhimidae (screamers) from Europe and North America, which have not yet been formally described (Mayr 2009a), as well as putative Galbulae from the early Eocene North American Green River Formation (Weidig 2010), whose tentative identification needs further verification.
Taking into account that North American avifaunas are less well known than the European ones, the general pattern in North America is similar to that seen in Europe. This is especially evident for forest-dwelling taxa, with early Eocene North American avifaunas showing a high taxonomic congruence with those from the middle Eocene of Europe. However, due to the earlier disappearance of paratropical forests in North America, many of the arboreal taxa disappeared earlier there than in Europe (Mayr 2009a). None of the Miocene forest dwelling taxa with African affinities have been recorded in North America, and Balearicinae (crowned cranes), which inhabit open habitats, represent the only “Ethiopian” faunal element in the Miocene of North America.
Paleogene and early Cenozoic avifaunas of Asia and the Southern Hemisphere are poorly known. Anseranatidae (magpie geese) occur in the late Oligo-Miocene of Australia (Worthy and Scanlon 2009), and stem group representatives of the Cariamae (seriemas and allies) and Cathartidae (New World vultures) have been reported from the Paleogene of South America (Alvarenga 1985; Mayr 2009a). Some species from the Paleogene of South America are closely related to birds from contemporaneous European deposits, and it is likely, albeit not yet proven, that stem group representatives of the European taxa with South American affinities also lived in the early Cenozoic of South America (Mourer-Chauviré 1999).
After the mid-Eocene, global cooling proceeded during the Cenozoic, and by the end of the Miocene climatic optimum maximum, there had been a drop of about 11°C in the minimum cold months temperature (Fig. 1; Böhme 2003). Emergence of a marked climatic seasonality towards the late Miocene (Mosbrugger et al. 2005) limited food availability in the cold northern hemispheric winters. Accordingly, the extinctions after the onset of the late Miocene cooling involve taxa whose extant representatives have poor dispersal capabilities and a predominantly insectivorous or frugivorous diet, such as Coliiformes, Musophagiformes, Bucorvinae, Psittaciformes, and Ramphastidae (barbets sensu Dickinson 2003). These groups still occur today in the warm regions of the Old World, and at least the latter three are species rich and widely distributed. Their disappearance between the stratigraphic units MN 6 and MN 11 (Fig. 1) corresponds well with Central European extinctions of thermophilic reptiles during the same period (Böhme 2003).
The Paleogene extinctions, however, do not correlate with major climatic events. Although the mean annual temperatures declined significantly by about 15°C during the Eocene, they were still equable during the Oligocene (e.g. Mosbrugger et al. 2005). As noted above, thermophilic reptiles, such as crocodilians and chameleons, were found in Central Europe until the middle Miocene (MN 6), with Varanidae persisting even until the late Miocene (MN 11; Böhme 2003). It is unlikely that birds were more affected by global cooling than these ectothermic groups. Climate-driven extinctions are further not expected to have had such a strong correlation with the distribution area of the closest extant relatives, which mainly survived in the Neotropical region but not in the geographically closer Old World zones with similar climates.
Because most of the taxa that disappeared in the Paleogene have affinities to South America, which was isolated from the northern continents until the Pliocene closure of the Panamanian Isthmus (Smith et al. 1994), biotic factors are more likely to have caused their extinction. The extant representatives of these groups have very different life histories, and previous attempts to explain their disappearance have failed to find an explanation (Mayr 2009a). However, it went unnoticed that their last occurrences correspond with the disappearance of flightless birds in the early Cenozoic of continental Europe.
In modern insular environments, predation by mammals and snakes is the main cause of avian extinctions, and apart from true carnivores, rats and mice pose a particular threat for eggs and nestlings (e.g. Wanless et al. 2007). The new mammalian taxa, which arrived in Europe just after the Grande Coupure, indeed included muroid rodents as well as carnivorans, such as viverrids and felids (Rose 2006). If a lower predation pressure in the Eocene allowed more exposed nesting sites, arboreal birds are expected to have been seriously affected by the new immigrants (e.g. Sieving 1992; Galetti et al. 2009). Although this hypothesis can not be verified through the fossil record, it is notable that extant “caprimulgiform” and apodiform birds, which are among the groups with the most distinctive Southern Hemispheric pattern (Fig. 2), exhibit strikingly different nesting behaviours, ranging from ground breeding (Caprimulgidae, nightjars), cave nesting (Steatornithidae, oilbirds), hole breeding (Aegothelidae, owlet-nightjars) and saliva use (Apodidae, swifts), to elaborate nest constructions (Trochilidae). The independent evolution of such divergent strategies is in line with the hypothesis of strong selective forces acting on the breeding biology of the Paleogene representatives of the respective lineages. Psittaciformes and Trogoniformes, by contrast, which were not affected by the Paleogene extinctions, excavate nesting cavities in tree trunks (Aegothelidae are dependent on existing ones). Coliiformes build open-bowl nests like passeriform birds, whose sophisticated nest building behaviour is considered a key factor to explain their adaptive radiation (Olson 2001).
Carnivorous marsupials also occurred in the Cenozoic of South America (e.g. Rose 2006), but contrary to the Northern continents there were no pre-Pliocene large-scale immigrations of new taxa, and birds thus coevolved with their predators. It is the sudden immigration of new predators in the Cenozoic of Europe, which is considered to have had a dramatic impact on avian communities.
In conclusion, the extinctions of “Southern Hemispheric” taxa in Europe are best explained by a two-phase extinction model that combines late Miocene extinctions due to the emergence of Northern Hemispheric winters and earlier Paleogene extinctions after faunal turnovers. Contrary to previous hypotheses (Lindow and Dyke 2006), climatic cooling does not explain Paleogene extinctions of “Southern Hemispheric” taxa. Likewise, not all Southern Hemispheric taxa are relics of groups that were once more widespread on the Northern Hemisphere (contra Olson 1989) and, as noted above, some of the African taxa seem to have dispersed into Europe during the Miocene.
It is especially the Neotropic realm and, to a lesser degree, Madagascar and Australia, which served as refugia for avian groups that had a more widespread distribution on the Northern Hemisphere during the early Cenozoic. There are also some non-avian faunal elements in the Paleogene of Europe, whose closest extant relatives are found in South America, Madagascar, or Australia, such as Marsupialia and Boidae (e.g. Morlo et al. 2004). The high number of “Neotropic” elements in Paleogene European avifaunas is, however, unparalleled by other vertebrates and can be explained by the much greater dispersal capabilities of birds. If these groups did not already have a wide distribution in the Paleogene, they could certainly better respond to environmental changes by dispersal than non-volant vertebrates.
I thank Ursula Göhlich, Naturhistorisches Museum Wien, for photos of coliiform birds from Kohfidisch in Austria. Comments by B. Lindow and the reviewers Z. Bochenski and C. Mourer-Chauviré improved the manuscript.