Elephant Birds Research Articles

Extinction in the Anthropocene.

Samuel Turvey and Jennifer Crees introduce the effects of humans on biodiversity.

A giant early Pleistocene bird from eastern Europe: unexpected component of terrestrial faunas at the time of early Homo arrival

ABSTRACTGiant birds, comparable in size to elephant birds and moa, have never been reported from Europe. Here, we describe a femur from the lower Pleistocene of the north Black Sea area (Crimea) that is referred to Pachystruthio dmanisensis, comb. nov., a giant bird with an estimated body mass of about 450 kg. This value makes this extinct bird one of the largest known avians (comparable to Aepyornis maximus) and the only bird of such giant size in Europe and the Northern Hemisphere in general. In contrast to very large insular birds, Pachystruthio dmanisensis was a good runner, which may be explained by its coexistence with large carnivoran mammals. Pachystruthio dmanisensis and associated assemblage of fossil mammals are shared with the Dmanisi locality in Georgia (∼1.8–1.7 Ma); thus, this giant bird was likely a typical component of eastern European faunas at the time of early hominin arrival. We suggest that Pachystruthio dmanisensis, together with early Homo and a variety of mammals, reached the northern Black Sea region via the southern Caucasus and Anatolia, because the older (Pliocene) finds of this fauna are known from Georgia and Turkey.

Unexpected diversity within the extinct elephant birds (Aves: Aepyornithidae) and a new identity for the world's largest bird.

Madagascar's now-extinct radiation of large-bodied ratites, the elephant birds (Aepyornithidae), has been subject to little modern research compared to the island's mammalian megafauna and other Late Quaternary giant birds. The family's convoluted and conflicting taxonomic history has hindered accurate interpretation of morphological diversity and has restricted modern research into their evolutionary history, biogeography and ecology. We present a new quantitative analysis of patterns of morphological diversity of aepyornithid skeletal elements, including material from all major global collections of aepyornithid skeletal remains, and constituting the first taxonomic reassessment of the family for over 50 years. Linear morphometric data collected from appendicular limb elements, and including nearly all type specimens, were examined using multivariate cluster analysis and the Bayesian information criterion, and with estimation of missing data using multiple imputation and expectation maximization algorithms. These analyses recover three distinct skeletal morphotypes within the Aepyornithidae. Two of these morphotypes are associated with the type specimens of the existing genera Mullerornis and Aepyornis, and represent small-bodied and medium-bodied aepyornithids, respectively. Aepyornis contains two distinct morphometric subgroups, which are identified as the largely allopatric species A. hildebrandti and A. maximus. The third morphotype, which has not previously been recognized as a distinct genus, is described as the novel taxon Vorombe titan. Vorombe represents the largest-bodied aepyornithid and is the world's largest bird, with a mean body mass of almost 650 kg. This new taxonomic framework for the Aepyornithidae provides an important new baseline for future studies of avian evolution and the Quaternary ecology of Madagascar.

Preserving and Optimising a World-Class African Ornithological Collection

The Durban Natural Science Museum houses a world-class collection of African bird study skins and other ornithological specimens including eggs, nests, skeletons, open wings and ethanol specimens. This presentation briefly outlines the value of these holdings. The bird study skins comprise the core of the collection and number nearly 40 000. This ranks the collection as one of the top three or four on the continent. These study skins are globally renowned for the quality of their preparation, far exceeding that of other African museums. The study skin collection houses an unparalleled assemblage of holotypes and paratypes of (mainly) southern African subspecies. A recent landmark book on geographical variation in southern African birds was largely based on examination of this collection. The collection also boasts the largest collection of study skins in existence from Mozambique. The collection includes one of the most significant Dodo Raphus cucullatus skeletons in the world, which has been subject to intense investigation in recent years, as well as a complete egg of a Madagascar Elephant bird (Aepyornithidae). Also discussed are ongoing best-practice measures to both preserve this collection and render it of optimal value to users, including a brief summary of the key outside stakeholders exploiting the collection for research and other purposes. An issue of particular note is the increasing demand for tissue samples (typically 'toe-pads') from the study skins for molecular investigations - raising problematic challenges relevant to destructive sampling. Particular attention is paid to describing a recent migration of the digital database to a global standard in the form of the ‘Specify’ collection database and management tool.

The avian egg exhibits general allometric invariances in mechanical design

The avian egg exhibits extraordinary diversity in size, shape and color, and has a key role in avian adaptive radiations. Despite extensive work, our understanding of the underlying principles that guide the “design” of the egg as a load-bearing structure remains incomplete, especially over broad taxonomic scales. Here we define a dimensionless number C, a function of egg weight, stiffness and dimensions, to quantify how stiff an egg is with respect to its weight after removing geometry-induced rigidity. We analyze eggs of 463 bird species in 36 orders across five orders of magnitude in body mass, and find that C number is nearly invariant for most species, including tiny hummingbirds and giant elephant birds. This invariance or “design guideline” dictates that evolutionary changes in shell thickness and Young’s modulus, both contributing to shell stiffness, are constrained by changes in egg weight. Our analysis illuminates unique reproductive strategies of brood parasites, kiwis, and megapodes, and quantifies the loss of safety margin for contact incubation due to artificial selection and environmental toxins. Our approach provides a mechanistic framework for a better understanding of the mechanical design of the avian egg, and may provide clues to the evolutionary origin of contact incubation of amniote eggs.

Eggshell palaeogenomics: Palaeognath evolutionary history revealed through ancient nuclear and mitochondrial DNA from Madagascan elephant bird (Aepyornis sp.) eggshell

Palaeognaths, the sister group of all other living birds (neognaths), were once considered to be vicariant relics from the breakup of the Gondwanan supercontinent. However, recent molecular studies instead argue for dispersal of volant ancestors across marine barriers. Resolving this debate hinges upon accurately reconstructing their evolutionary relationships and dating their divergences, which often relies on phylogenetic information from extinct relatives and nuclear genomes. Mitogenomes from the extinct elephant birds of Madagascar have helped inform the palaeognath phylogeny; however, nuclear information has remained unavailable. Here, we use ancient DNA (aDNA) extracted from fossil eggshell, together with target enrichment and next-generation sequencing techniques, to reconstruct an additional new mitogenome from Aepyornis sp. with 33.5X coverage. We also recover the first elephant bird nuclear aDNA, represented by 12,500bp of exonic information. While we confirm that elephant birds are sister taxa to the kiwi, our data suggests that, like neognaths, palaeognaths underwent an explosive radiation between 69 and 52Ma—well after the break-up of Gondwana, and more rapidly than previously estimated from mitochondrial data alone. These results further support the idea that ratites primarily diversified immediately following the Cretaceous-Palaeogene mass extinction and convergently evolved flightlessness. Our study reinforces the importance of including information from the nuclear genome of extinct taxa for recovering deep evolutionary relationships. Furthermore, with approximately 3% endogenous aDNA retrieved, avian eggshell can be a valuable substrate for recovering high quality aDNA. We suggest that elephant bird whole genome recovery is ultimately achievable, and will provide future insights into the evolution these birds.

Phylogenomics and Morphology of Extinct Paleognaths Reveal the Origin and Evolution of the Ratites

The Palaeognathae comprise the flightless ratites and the volant tinamous, and together with the Neognathae constitute the extant members of class Aves. It is commonly believed that Palaeognathae originated in Gondwana since most of the living species are found in the Southern Hemisphere [1-3]. However, this hypothesis has been questioned because the fossil paleognaths are mostly from the Northern Hemisphere in their earliest time (Paleocene) and possessed many putative ancestral characters [4]. Uncertainties regarding the origin and evolution of Palaeognathae stem from the difficulty in estimating their divergence times [1, 2] and their remarkable morphological convergence. Here, we recovered nuclear genome fragments from extinct elephant birds, which enabled us to reconstruct a reliable phylogenomic time tree for the Palaeognathae. Based on the tree, we identified homoplasies in morphological traits of paleognaths and reconstructed their morphology-based phylogeny including fossil species without molecular data. In contrast to the prevailing theories, the fossil paleognaths from the Northern Hemisphere were placed as the basal lineages. Combined with our stable divergence time estimates that enabled a valid argument regarding the correlation with geological events, we propose a new evolutionary scenario thatcontradicts the traditional view. The ancestral Palaeognathae were volant, as estimated from their molecular evolutionary rates, and originated during the Late Cretaceous in the Northern Hemisphere. They migrated to the Southern Hemisphere and speciated explosively around the Cretaceous-Paleogene boundary. They then extended their distribution to the Gondwana-derived landmasses, such as New Zealand and Madagascar, by overseas dispersal. Gigantism subsequently occurred independently on each landmass.

A juvenile subfossil crocodylian from Anjohibe Cave, Northwestern Madagascar

Madagascar’s subfossil record preserves a diverse community of animals including elephant birds, pygmy hippopotamus, giant lemurs, turtles, crocodiles, bats, rodents, and carnivorans. These fossil accumulations give us a window into the island’s past from 80,000 years ago to a mere few hundred years ago, recording the extinction of some groups and the persistence of others. The crocodylian subfossil record is limited to two taxa, Voay robustus and Crocodylus niloticus, found at sites distributed throughout the island. V. robustus is extinct while C. niloticus is still found on the island today, but whether these two species overlapped temporally, or if Voay was driven to extinction by competing with Crocodylus remains unknown. While their size and presumed behavior was similar to each other, nearly nothing is known about the growth and development of Voay, as the overwhelming majority of fossil specimens represent mature adult individuals. Here we describe a nearly complete juvenile crocodylian specimen from Anjohibe Cave, northwestern Madagascar. The specimen is referred to Crocodylus based on the presence of caviconchal recesses on the medial wall of the maxillae, and to C. niloticus based on the presence of an oval shaped internal choana, lack of rostral ornamentation and a long narrow snout. However, as there are currently no described juvenile specimens of Voay robustus, it is important to recognize that some of the defining characteristics of that genus may have changed through ontogeny. Elements include a nearly complete skull and many postcranial elements (cervical, thoracic, sacral, and caudal vertebrae, pectoral elements, pelvic elements, forelimb and hindlimb elements, osteoderms). Crocodylus niloticus currently inhabits Madagascar but is locally extinct from this particular region; radiometric dating indicates an age of ∼460–310 years before present (BP). This specimen clearly represents a juvenile based on the extremely small size and open sutures/detached neural arches; total body length is estimated to be ∼1.1 m (modern adults of this species range from ∼4–6 m). This fossil represents the only juvenile subfossil crocodylian specimen reported from Madagascar.

Sexual dimorphism in the late Miocene mihirung Dromornis stirtoni (Aves: Dromornithidae) from the Alcoota Local Fauna of central Australia

ABSTRACTThe dromornithids were giant flightless birds endemic to Australia from the late Paleogene to the late Pleistocene. Dromornithids are generally considered to be divergent members of the Anseriformes, but they display many convergent features with extant ratites. In this study, we investigate Dromornis stirtoni from the Alcoota Local Fauna, a species for which little is known of its biology. We used traditional methods of comparative morphology, mass estimation, landmark-based morphometrics, and histological investigations to determine the presence of medullary bone, to assess the possible presence, form, and extent of sexual dimorphism in D. stirtoni. Two morphological groups were identified for each main leg element, differing primarily in relative robustness. Core samples from femora and tibiotarsi shafts revealed medullary bone in the less robust morph, indicating that these were females. Mass, as estimated by algorithms applied to our preferred measurement of least-shaft circumference of tibiotarsi, was significantly different between males (mean = 528 kg) and females (mean = 451 kg). Therefore, male D. stirtoni were more robust but not much taller than the females and challenge the elephant bird, Aepyornis maximus, for the title of the most massive bird to have existed. Sexual dimorphism in this largest of all dromornithids, therefore, was like that of extant Anseriformes. We infer long-term monogamy, mutual display, shared parental care, female incubation, and aggressive defense of nests in these birds. The techniques of geometric morphometrics applied in this study maximize the use of fragmentary material, helping to overcome the common paleontological challenge of limited sample sizes.SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVPCitation for this article: Handley, W. D., A. Chinsamy, A. M. Yates, and T. H. Worthy. 2016. Sexual dimorphism in the late Miocene mihirung Dromornis stirtoni (Aves: Dromornithidae) from the Alcoota Local Fauna of central Australia. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2016.1180298.

The Rukh and the influence of Chinese mythology

The Rukh bird that was mentioned in the Arabian Nights became popular in the West due to the Venetian traveller Marco Polo (1254–1324) who referred to it in his travel account. Though Marco Polo did not claim to see the Rukh himself, he narrated what Arab navigators described as a giant bird that appeared near the island of Madagascar (Polo in The travels of Marco Polo the Venetian, 1914) (McElroy observes that in southern part of Madagascar, ‘near Isalo, exploerers still found the giant eggs of the roc, the great elephant bird….’ (McElroy in Over the lip of the World: among the storytellers of Madagascar, 2001) or Aepyornis, which is believed to be the source of the Rukh’s myth). Other travellers like Ibn Baţūţah (c.1304–c.1377) stated that the bird had the reputation of attacking ships whenever it saw them. Previous studies emphasized the link between the Persian Simurgh and the Rukh, but this article argues that the Rukh has been influenced by Chinese mythology especially by the P‘eng bird, while the Arabs’ oral tradition is indirectly associated with the Rukh through a number of traditional practices and rituals popular in the early twentieth century. Further, the article provides textual evidence that assist in further understanding some Arabian Nights tales.

Faunal diversity in a semi-evergreen forest of Bornadi-Khalingduar Complex of Assam, India

The Bornadi-Khalingduar Complex under the Manas Tiger Reserve, Assam is known to be an important area for wildlife movement to and from India and Bhutan. The contiguous landscape encompassing the two neighbouring countries provides a good habitat for diversity of wildlife and also as an important corridor area. We carried out an opportunistic camera-trapping exercise to document the faunal diversity in the area. A month-long exercise photo-captured a total of 19 species belonging to 12 families, including the Leopard, Wild Dog, Leopard Cat, Binturong, Elephant, Sambar, Barking Deer and various birds. These findings of the study reveal the importance, threats and potential of the area and recommendations have been made to secure this corridor for continuous animal movement. Anthropogenic disturbance is a major deterrent to undisturbed animal movement in this area with resultant forest fragmentation and degradation. This indicates the need for effective conservation strategies in order to maintain the remnants of this corridor complex.

Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution.

The evolution of the ratite birds has been widely attributed to vicariant speciation, driven by the Cretaceous breakup of the supercontinent Gondwana. The early isolation of Africa and Madagascar implies that the ostrich and extinct Madagascan elephant birds (Aepyornithidae) should be the oldest ratite lineages. We sequenced the mitochondrial genomes of two elephant birds and performed phylogenetic analyses, which revealed that these birds are the closest relatives of the New Zealand kiwi and are distant from the basal ratite lineage of ostriches. This unexpected result strongly contradicts continental vicariance and instead supports flighted dispersal in all major ratite lineages. We suggest that convergence toward gigantism and flightlessness was facilitated by early Tertiary expansion into the diurnal herbivory niche after the extinction of the dinosaurs.

Ruffling ancient ratite feathers

Evolution![Figure][1] An adult kiwi and an elephant bird egg. PHOTO: KYLE DAVIS AND PAUL SCOFIELD/CANTERBURY MUSEUM Biologists have often pointed to the breakup of the supercontinent Gondwana to explain how related species ended up on far-flung continents, but as new research shows, that explanation doesn't fly with ratite birds. Ratite birds are a lineage of large, mostly flightless birds including the African ostrich, the Australian emu, the South American rhea, the diminutive New Zealand kiwi, and the extinct Madagascar elephant bird. Mitchell et al. examined the phylogeny of these birds, adding ancient mitochondrial DNA sequences from the extinct elephant bird. It seems that ratites originated from flighted ancestors who evolved large sizes and loss of flight only after flying to their new homes. Science , this issue p. [898][2]. [1]: pending:yes [2]: /lookup/doi/10.1126/science.1251981

Bird fossils from Ankilitelo Cave: inference about Holocene environmental changes in southwestern Madagascar.

The identifications of non-permineralized fossil bird bones recovered from Ankilitelo Cave in southwestern Madagascar are presented. Among the more than 560 elements recovered, 29 different taxa were identified, the vast majority being species that still occur in this region of the island. Eggshell remains from the extinct elephant bird (Family Aepyornithidae) and assigned to Aepyornis sp. were found at the site. Two identified extant taxa, Scopus umbretta and Monias benschi, no longer occur in the area immediately surrounding the cave. The available radiocarbon measurements of collagen from fossil bird bones and avian eggshell carbonate of recovered from the cave range from 13,270 Cal yr BP to modern times. Hence, the presumed ecological shifts that took place resulting in the disappearance or range contractions of these three taxa is within the Holocene and are presumed to be associated with natural climatic change and in more recent centuries associated human pressures. Information is also presented on the origin of guinea fowl (Numida) and inference on the period of colonization of Corvus albus on Madagascar.

A Molecular Phylogeny of Plesiorycteropus Reassigns the Extinct Mammalian Order ‘Bibymalagasia’

Madagascar is well known for its diverse fauna and flora, being home to many species not found anywhere else in the world. However, its biodiversity in the recent past included a range of extinct enigmatic fauna, such as elephant birds, giant lemurs and dwarfed hippopotami. The ‘Malagasy aardvark’ (Plesiorycteropus) has remained one of Madagascar’s least well-understood extinct species since its discovery in the 19th century. Initially considered a close relative of the aardvark (Orycteropus) within the order Tubulidentata, more recent morphological analyses challenged this placement on the grounds that the identifiably derived traits supporting this allocation were adaptations to digging rather than shared ancestry. Because the skeletal evidence showed many morphological traits diagnostic of different eutherian mammal orders, they could not be used to resolve its closest relatives. As a result, the genus was tentatively assigned its own taxonomic order ‘Bibymalagasia’, yet how this order relates to other eutherian mammal orders remains unclear despite numerous morphological investigations. This research presents the first known molecular sequence data for Plesiorycteropus, obtained from the bone protein collagen (I), which places the ‘Malagasy aardvark’ as more closely related to tenrecs than aardvarks. More specifically, Plesiorycteropus was recovered within the order Tenrecoidea (golden moles and tenrecs) within Afrotheria, suggesting that the taxonomic order ‘Bibymalagasia’ is obsolete. This research highlights the potential for collagen sequencing in investigating the phylogeny of extinct species as a viable alternative to ancient DNA (aDNA) sequencing, particularly in cases where aDNA cannot be recovered.

Why all those spines? Anachronistic defences in the Didiereoideae against now extinct lemurs

Plants evolve physical defences, such as spines, against browsing herbivores. However, in some cases, these defences may be anachronistic because the principal consumers of protected parts of the plant are extinct. In such cases, there may be few extant species consuming heavily defended resources. Here we examine the spiny defences of Madagascar’s endemic Didiereoideae, and ask whether they may be anachronistic. To accomplish this aim, we reviewed the literature to determine which species consume these plants today, and then used stable isotope biogeochemistry to determine who may have exploited Didiereoideae in the recent past. There are four major groups of browsers that are now extinct in Madagascar: giant lemurs, elephant birds (Aepyornis and Mullerornis: Aepyornithidae), pygmy hippopotamuses (Hippopotamus) and giant tortoises (Aldabrachelys: Testudinidae). Each group was evaluated for isotopic evidence of didiereoid plant consumption. Given the structure of members of this plant clade (especially Alluaudia), we predicted that lemurs would be their most important consumers. Three extant lemur species consume Didiereoideae. Several of the extinct lemurs, particularly Hadropithecus stenognathus, may have relied heavily on these spiny plants. None of the non-lemur megafaunal browsers (elephant birds, hippopotamuses and giant tortoises) were important consumers of Didiereoideae.

Early Holocene fauna from a new subfossil site: A first assessment from Christmas River, south central Madagascar

We report on faunal remains recovered during recent explorations at ‘Christmas River’, the only subfossil locality known from Madagascar’s south central plateau. Recovered remains of several extinct taxa date to approximately 10,000 14 C years before present (BP), including crocodiles, tortoises, the elephant bird Aepyornis, the carnivoran Cryptoprocta spelea, the lemurs Archaeolemur majori, Pachylemur insignis, and Megaladapis edwardsi, and abundant remains of the dwarf hippopotamus, Hippopotamus lemerlei. The presence of southern - limited, forest - dependent species at Christmas River supports the hypothesis that forest once extended, perhaps discontinuously, across the central highlands towards the west. One theory is that sites in the north central highlands, which are higher in elevation, maintained more mesic conditions during Plio - Quaternary climate shifts than those of the lower elevation sites of the south central highlands. Thus, elevation above sea level may have acted as a filter that limited species dispersal across the island in the past. Such a scenario would explain the distinction between more humid, higher elevation, northern highland subfossil communities versus more arid, lower elevation, southern subfossil communities. Continued exploration at Christmas River thus provides a remarkable opportunity for deciphering ecological changes that have taken place in south central Madagascar during the Holocene.

A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in Southern Madagascar

The Spiny Thicket Ecoregion (STE) of Southern and southwestern Madagascar was recently home to numerous giant lemurs and other "megafauna," including pygmy hippopotamuses, giant tortoises, elephant birds, and large euplerid carnivores. Following the arrival of humans more than 2,000 years ago, dramatic extinctions occurred. Only one-third of the lemur species which earlier occupied the STE survive today; other taxa suffered even greater losses. We use stable isotope biogeochemistry to reconstruct past diets and habitat preferences of the recently extinct lemurs of the STE. We show that the extinct lemurs occupied a wide range of niches, often distinct from those filled by coeval non-primates. Many of the now-extinct lemurs regularly exploited habitats that were drier than the gallery forests in which the remaining lemurs of this ecoregion are most often protected and studied. Most fed predominantly on C3 plants and some were likely the main dispersers of the large seeds of native C3 trees; others included CAM and/or C4 plants in their diets. These new data suggest that the recent extinctions have likely had significant ecological ramifications for the communities and ecosystems of Southern and southwestern Madagascar.

Fossil avian eggshell preserves ancient DNA

Owing to exceptional biomolecule preservation, fossil avian eggshell has been used extensively in geochronology and palaeodietary studies. Here, we show, to our knowledge, for the first time that fossil eggshell is a previously unrecognized source of ancient DNA (aDNA). We describe the successful isolation and amplification of DNA from fossil eggshell up to 19 ka old. aDNA was successfully characterized from eggshell obtained from New Zealand (extinct moa and ducks), Madagascar (extinct elephant birds) and Australia (emu and owl). Our data demonstrate excellent preservation of the nucleic acids, evidenced by retrieval of both mitochondrial and nuclear DNA from many of the samples. Using confocal microscopy and quantitative PCR, this study critically evaluates approaches to maximize DNA recovery from powdered eggshell. Our quantitative PCR experiments also demonstrate that moa eggshell has approximately 125 times lower bacterial load than bone, making it a highly suitable substrate for high-throughput sequencing approaches. Importantly, the preservation of DNA in Pleistocene eggshell from Australia and Holocene deposits from Madagascar indicates that eggshell is an excellent substrate for the long-term preservation of DNA in warmer climates. The successful recovery of DNA from this substrate has implications in a number of scientific disciplines; most notably archaeology and palaeontology, where genotypes and/or DNA-based species identifications can add significantly to our understanding of diets, environments, past biodiversity and evolutionary processes.

Were Malagasy Uncarina fruits dispersed by the extinct elephant bird?

We hypothesise that the spiny fruits of the endemic Madagascar genus Uncarina (Pedaliaceae) are trample burrs that evolved to be dispersed on the feet of the extinct elephant bird (Aepyornis). Our evidence is: i) the morphology of the fruit with its large grapple hooks is more likely to attach to a foot than to adhere to fur and ii) the presentation of mature fruits on the ground rather than in the canopy. These differences to adhesive burrs make lemurs unlikely dispersers. We argue, given the absence of other large terrestrial mammals in Madagascar, that the most likely dispersers of Uncarina fruits were the extinct large birds. If correct, our hypothe- sis has implications for conservation of Uncarina, the bio- geography of the elephant birds and dispersal biology. For example, we predict that the demography of Uncarina will be skewed towards adult plants, and that the dispersal mutualism