Moa diet fits the bill: virtual reconstruction incorporating mummified remains and prediction of biomechanical performance in avian giants

The moa (Dinornithiformes) are large to gigantic extinct terrestrial birds of New Zealand. Knowledge about niche partitioning, feeding mode and preference among moa species is limited, hampering palaeoecological reconstruction and evaluation of the impacts of their extinction on remnant native biota, or the viability of exotic species as proposed ecological ‘surrogates''. Here we apply three-dimensional finite-element analysis to compare the biomechanical performance of skulls from five of the six moa genera, and two extant ratites, to predict the range of moa feeding behaviours relative to each other and to living relatives. Mechanical performance during biting was compared using simulations of the birds clipping twigs based on muscle reconstruction of mummified moa remains. Other simulated food acquisition strategies included lateral shaking, pullback and dorsoventral movement of the skull. We found evidence for limited overlap in biomechanical performance between the extant emu (Dromaius novaehollandiae) and extinct upland moa (Megalapteryx didinus) based on similarities in mandibular stress distribution in two loading cases, but overall our findings suggest that moa species exploited their habitats in different ways, relative to both each other and extant ratites. The broad range of feeding strategies used by moa, as inferred from interspecific differences in biomechanical performance of the skull, provides insight into mechanisms that facilitated high diversities of these avian herbivores in prehistoric New Zealand.     

A refined model of body mass and population density in flightless birds reconciles extreme bimodal population estimates for extinct moa

Flightless birds were once the largest and heaviest terrestrial fauna on many archipelagos around the world. Robust approaches for estimating their population parameters are essential for understanding prehistoric insular ecosystems and extinction processes. Body mass and population density are negatively related for extant flightless bird species, providing a method for quantifying densities and population sizes of extinct flightless species. Here we assemble an updated global data set of body mass and population densities for extant flightless birds and estimate the relationship between these variables. We use generalised least squares models that account for phylogenetic relatedness and incorporate the effects of limiting factors (e.g. habitat suitability) on population density. We demonstrate the applicability of this allometric relationship to extinct species by estimating densities for each of the nine species of moa (Dinornithiformes) and generating a combined spatially explicit map of total moa density across New Zealand. To compare our density estimates with those previously published, we summed individual species' abundances to generate a mean national density of 2.02–9.66 birds km⁻² for low- and high-density scenarios, respectively. Our results reconcile the extreme bimodality of previous estimates (< 2 birds km⁻² and > 10 birds km⁻²) and are comparable to contemporary densities of large herbivorous wild mammals introduced into New Zealand about 150 yr ago. The revised moa density has little effect on the harvest rates required to bring about extinction within 150–200 yr, indicating that rapid extinction was an inevitable response to human hunting, irrespective of the initial population of moa.     

High-resolution coproecology: using coprolites to reconstruct the habits and habitats of New Zealand's extinct upland moa (Megalapteryx didinus)

Knowledge about the diet and ecology of extinct herbivores has important implications for understanding the evolution of plant defence structures, establishing the influences of herbivory on past plant community structure and composition, and identifying pollination and seed dispersal syndromes. The flightless ratite moa (Aves: Dinornithiformes) were New Zealand's largest herbivores prior to their extinction soon after initial human settlement. Here we contribute to the knowledge of moa diet and ecology by reporting the results of a multidisciplinary study of 35 coprolites from a subalpine cave (Euphrates Cave) on the South Island of New Zealand. Ancient DNA analysis and radiocarbon dating revealed the coprolites were deposited by the extinct upland moa (Megalapteryx didinus), and span from at least 6,368±31 until 694±30 (14)C years BP; the approximate time of their extinction. Using pollen, plant macrofossil, and ancient DNA analyses, we identified at least 67 plant taxa from the coprolites, including the first evidence that moa fed on the nectar-rich flowers of New Zealand flax (Phormium) and tree fuchsia (Fuchsia excorticata). The plant assemblage from the coprolites reflects a highly-generalist feeding ecology for upland moa, including browsing and grazing across the full range of locally available habitats (spanning southern beech (Nothofagus) forest to tussock (Chionochloa) grassland). Intact seeds in the coprolites indicate that upland moa may have been important dispersal agents for several plant taxa. Plant taxa with putative anti-browse adaptations were also identified in the coprolites. Clusters of coprolites (based on pollen assemblages, moa haplotypes, and radiocarbon dates), probably reflect specimens deposited at the same time by individual birds, and reveal the necessity of suitably large sample sizes in coprolite studies to overcome potential biases in diet interpretation.     

Feathers to Fur: the status of New Zealand ecological research in 2009

We outline the scope of this special issue of New Zealand Journal of Ecology, which reviews progress in New Zealand ecology to 2009, based on a symposium in 2007. Both the issue and symposium update a 1986 conference and 1989 special issue of NZ J Ecol called ?Moas, Mammals and Climate? which has been influential and widely cited. This issue revisits several themes featured in 1989, including the extent of recent and prehistoric extinctions in the New Zealand fauna; effects of introduced mammalian herbivores replacing now-extinct browsing birds such as moa; the impacts of introduced mammalian predators on native birds (hence the Feathers to Fur title); the role of islands as refuges and opportunities for restoration; and the status of bird?plant mutualisms like pollination and fruit dispersal. Several topics not discussed in 1989 are raised, including the unusual size and functional composition of New Zealand?s tree flora, and several taxonomic groups (invertebrates, fungi) and habitats (fresh waters) that received little attention in 1989. We summarise four symposium talks which are not included elsewhere in this issue. New Zealand leads the world in ways both unenviable (e.g. levels of impact of introduced species) and enviable (e.g. predator eradication, translocations, rare species management. The recent advances reviewed in this issues have relevance well beyond New Zealand.     

Impacts of introduced deer and extinct moa on New Zealand ecosystems

There has been considerable ongoing debate about the extent to which the impacts of introduced deer on native vegetation have replaced those of moa, and since the 1980s there have been major changes in thinking about the impacts of deer and ratites on ecosystems. Although it has long been known that deer caused a predictable sequence of changes in forest understorey composition, recent work has shown that the foliage of species preferred by deer contains lower concentrations of fibre ? and decomposes faster ? than avoided species. Analyses of long-term permanent plot data suggest that some preferred species are failing to regenerate in forest types where deer are present. As well as likely altering the long-term biogeochemistry of forest ecosystems, deer have a strong negative effect on the abundance of litter-dwelling macrofauna (most likely through trampling). Estimating the impacts of extinct taxa on an ecosystem has much uncertainty, but recent experiments have shown that extant ratites and deer may have more similar feeding preferences than previously believed. It is likely that moa were important seed dispersers, but this has not been studied for deer in New Zealand. Although collectively the various taxa of deer in New Zealand use all of the habitats utilised by moa, and there is partial overlap in the diets of deer and moa, deer can attain densities and biomasses 100- fold greater than reasonably surmised for moa. We believe that the impacts of introduced deer on ecosystems are markedly different from those of moa. One way to compare the impacts of moa and deer is to use pollen to reconstruct the vegetation at a forested site in recent millennia and evaluate vegetation dynamics during the moa period, following the extinction of moa but prior to the arrival of deer (i.e. the moa gap), and following the arrival of deer. We illustrate the potential of this approach with a soil core from Chester Burn, Murchison Mountains in Fiordland. Five other areas that deserve further research are also identified.     

Do New Zealand invertebrates reflect the dominance of birds in their evolutionary history?

Pre-human New Zealand had some unusual feeding guilds of birds (e.g. the herbivorous moa fauna), thought to have developed as a result of the absence of a ?normal? mammal fauna. Insectivorous birds, on the other hand, are an integral part of all the world?s ecosystems, regardless of the presence or absence of mammals. While it is acknowledged the overall predation impact from birds in New Zealand is unlikely to have differed greatly from elsewhere, the low impact of mammalian insectivores (apart from microbats), coupled with the presence of a specialised avian feeding guild that concentrated on ground-active prey, might have exerted certain unique selection pressures. Do New Zealand invertebrates reflect this? It would be necessary to compare the New Zealand invertebrate fauna with that of mammal-dominated lands in greater detail than is available today before we could assert whether any unique anti-predator characteristics have evolved. Knowledge of the insects that succumbed to extinction when mammals invaded New Zealand should provide clues to avian-adapted features that might have rendered them particularly vulnerable to introduced rodents. Predation by kiwi (Apteryx spp.), an extraordinarily mammal-like nocturnal bird, may to some extent have prepared the invertebrate fauna for the arrival of small mammals.     

DNA content and distribution in ancient feathers and potential to reconstruct the plumage of extinct avian taxa

Feathers are known to contain amplifiable DNA at their base (calamus) and have provided an important genetic source from museum specimens. However, feathers in subfossil deposits generally only preserve the upper shaft and feather ‘vane’ which are thought to be unsuitable for DNA analysis. We analyse subfossil moa feathers from Holocene New Zealand rockshelter sites and demonstrate that both ancient DNA and plumage information can be recovered from their upper portion, allowing species identification and a means to reconstruct the appearance of extinct taxa. These ancient DNA sequences indicate that the distal portions of feathers are an untapped resource for studies of museum, palaeontological and modern specimens. We investigate the potential to reconstruct the plumage of pre-historically extinct avian taxa using subfossil remains, rather than assuming morphological uniformity with closely related extant taxa. To test the notion of colour persistence in subfossil feathers, we perform digital comparisons of feathers of the red-crowned parakeet (Cyanoramphus novaezelandiae novaezelandiae) excavated from the same horizons as the moa feathers, with modern samples. The results suggest that the coloration of the moa feathers is authentic, and computer software is used to perform plumage reconstructions of moa based on subfossil remains.     

Bone growth marks reveal protracted growth in New Zealand kiwi (Aves,Apterygidae)

The presence of bone growth marks reflecting annual rhythms in the cortical bone of non-avian tetrapods is now established as a general phenomenon. In contrast, ornithurines (the theropod group including modern birds and their closest relatives) usually grow rapidly in less than a year, such that no annual rhythms are expressed in bone cortices, except scarce growth marks restricted to the outer cortical layer. So far, cyclical growth in modern birds has been restricted to the Eocene Diatryma, the extant parrot Amazona amazonica and the extinct New Zealand (NZ) moa (Dinornithidae). Here we show the presence of lines of arrested growth in the long bones of the living NZ kiwi (Apteryx spp., Apterygidae). Kiwis take 5–6 years to reach full adult body size, which indicates a delayed maturity and a slow reproductive cycle. Protracted growth probably evolved convergently in moa and kiwi sometime since the Middle Miocene, owing to the severe climatic cooling in the southwest Pacific and the absence of mammalian predators.     

Legacy of avian-dominated plant?herbivore systems in New Zealand

Avian herbivores dominated New Zealand?s pre-settlement terrestrial ecosystems to an unparalleled extent, in the absence of a terrestrial mammal fauna. Approximately 50% (88 taxa) of terrestrial bird species consumed plant foliage, shoots, buds and flowers to some degree, but fewer than half these species were major herbivores. Moa (Dinornithiformes) represent the greatest autochthonous radiation of avian herbivores in New Zealand. They were the largest browsers and grazers within both forest and scrubland ecosystems. Diverse waterfowl (Anatidae) and rail (Rallidae) faunas occupied forests, wetlands and grasslands. Parrots (Psittacidae) and wattlebirds (Callaeidae) occupied a range of woody vegetation types, feeding on fruits/seeds and foliage/ fruits/nectar, respectively. Other important herbivores were the kereru (Columbidae), stitchbird (Notiomystidae) and two honeyeaters (Meliphagidae). Cryptic colouration, nocturnal foraging and fossil evidence suggest that avian populations were strongly constrained by predation. With the absence of migratory avian herbivores, plant structural, constitutive defences prevailed, with the unusual ?wire syndrome? representing an adaptation to limit plant offtake by major terrestrial avian browsers. Inducible plant defences are rare, perhaps reflecting longstanding nutrient-limitations in New Zealand ecosystems. Evidence from coprolites suggests moa were important dispersers of now rare, annual, disturbance-tolerant herb species, and their grazing may have maintained diverse prostrate herbs in different vegetation types. The impact of moa on forest structure and composition remains speculative, but many broadleaved woody species would likely have experienced markedly reduced niches in pre-settlement time. Several distinctive avian-mediated vegetation types are proposed: dryland woodlands, diverse turf swards, coastal herb-rich low-forest-scrubland, and conifer-rich forests. Since human settlement (c. 750 yrs ago), c. 50% of endemic avian herbivore species or c. 40% overall have become extinct, including all moa, 60% of waterfowl and 33% of rail species. Numerically, avian herbivore introductions (c. 24 taxa) since European settlement have compensated for extinctions (c. 27 taxa), but the naturalised birds are mostly small, seed-eating species restricted to human-modified landscapes. Several naturalised species (e.g. Canada goose, Branta canadensis; brown quail, Coturnix ypsilophorus) may provide modes and levels of herbivory comparable with extinct species. The original avian and current introduced mammal herbivore regimes were separated by several centuries when New Zealand lacked megaherbivores. This ?herbivory hiatus? complicates comparisons between pre-settlement and current herbivore systems in New Zealand. However, predation, animal mobility, feeding mode, nutrient transfer patterns and soil impacts were different under an avian regime compared with current mammalian herbivore systems. Levels of ecological surrogacy between avifauna and introduced mammals are less evident. Ungulates generally appear to have impacts qualitatively different from those of the extinct moa. Because of New Zealand?s peculiar evolutionary history, avian herbivores will generally favour the persistence of indigenous vegetation, while mammalian herbivores continue to induce population declines of select plant species, change vegetation regeneration patterns, and generally favour the spread and consolidation of introduced plant species with which they share an evolutionary history.     

More than One Way of Being a Moa: Differences in Leg Bone Robustness Map Divergent Evolutionary Trajectories in Dinornithidae and Emeidae (Dinornithiformes)

The extinct moa of New Zealand included three families (Megalapterygidae; Dinornithidae; Emeidae) of flightless palaeognath bird, ranging in mass from <15 kg to >200 kg. They are perceived to have evolved extremely robust leg bones, yet current estimates of body mass have very wide confidence intervals. Without reliable estimators of mass, the extent to which dinornithid and emeid hindlimbs were more robust than modern species remains unclear. Using the convex hull volumetric-based method on CT-scanned skeletons, we estimate the mass of a female Dinornis robustus (Dinornithidae) at 196 kg (range 155–245 kg) and of a female Pachyornis australis (Emeidae) as 50 kg (range 33–68 kg). Finite element analysis of CT-scanned femora and tibiotarsi of two moa and six species of modern palaeognath showed that P. australis experienced the lowest values for stress under all loading conditions, confirming it to be highly robust. In contrast, stress values in the femur of D. robustus were similar to those of modern flightless birds, whereas the tibiotarsus experienced the highest level of stress of any palaeognath. We consider that these two families of Dinornithiformes diverged in their biomechanical responses to selection for robustness and mobility, and exaggerated hindlimb strength was not the only successful evolutionary pathway.     

Partial amino acid sequence of osteocalcin from an extinct species of ratite bird

Osteocalcin the major gamma carboxyglutamic acid containing protein of vertebrate bone has been purified from the bones of a specimen of Pachyornis elephantopus, a species of the extinct class of New Zealand ratite birds, the moas. The sequence of the N-terminal region of moa osteocalcin was determined using gas phase N-terminal sequencing. The N-terminal sequences of the ostrich and rhea osteocalcins were also determined. Alignment of the N-terminal sequence of osteocalcin from the extinct moa against the osteocalcins of the extant ostrich, rhea and emu reveals the homology amongst the ratite species is greater than the homology with the chicken osteocalcin.     

Herbivory and the evolution of divaricate plants: Structural defences lost on an offshore island

Many island plants are characterized by unique morphology. For example, the high branching angles and small leaves of divaricate plants are a common feature of the New Zealand flora. The divaricate growth form may be an adaptation to deter browsing by extinct avian herbivores (moa); alternatively aspects of the insular climate may be responsible. However, our understanding of the selective pressures responsible for the high branching angles and small leaves of divaricate plants is incomplete. Here, I tested for differences in traits associated with the divaricate growth form between plants from Chatham Island and the New Zealand mainland. Moa never reached the Chatham Islands and its flora is derived from plants on mainland New Zealand. Therefore, I predicted Chatham Island plants to have lost morphological adaptations that may have deterred moa herbivory. Traits were quantified on 316 individuals in the field, allowing for 12 island‐mainland taxonomic comparisons. Chatham Island plants consistently produced smaller branching angles, larger leaves, shorter internodes and larger stems than related mainland plants. Results are therefore consistent with the hypothesis that selection for small leaves and high angled branching may be relaxed on the Chatham Islands due to an absence of moa. Smaller branching angles and larger leaves may offer a competitive advantage to Chatham Island plants.     

Is a large-scale DNA-based inventory of ancient life possible?

A complete DNA-based inventory of the Earth's present biota using large-scale high-throughput DNA sequencing of signature region(s) (DNA barcoding) is an ambitious proposal rivaling the Human Genome Project. We examine whether this approach will also enable us to assess the past diversity of the earth's biota. To test this, we sequenced the 5' terminus of the mitochondrial cytochrome c oxidase I (COI) gene of individuals belonging to a group of extinct ratite birds, the moa of New Zealand. Moa comprised a large number of taxa that radiated in isolation on this oceanic landmass. Using a phylogenetic approach based on a large data set including protein coding and 12S DNA sequences as well as morphology, we now have precise information about the number of moa species that once existed. We show that each of the moa species detected using this extensive data set has a unique COI barcode(s) and that they all show low levels of within-species COI variation. Consequently, we conclude that COI sequences accurately identify the species discovered using the larger data set. Hence, more generally, this study suggests that DNA barcoding might also help us detect other extinct animal species and that a large-scale inventory of ancient life is possible.     

Vicars,tramps and assembly of the New Zealand avifauna: a review of molecular phylogenetic evidence

The avifauna of New Zealand is taxonomically and ecologically distinctive, as is typical of island biotas. However, the potential for an old geological age of New Zealand has encouraged a popular notion of a ‘Moa’s ark’ based on the idea that much of the fauna was isolated when Zealandia broke from Gondwana c. 83 million years ago. Molecular phylogenetics has proved useful for exploring the relative importance of different biogeographical processes, revealing for example that ‘tramp’ species (widely dispersing taxa) have arrived in New Zealand even in the last few hundred years, and that some avian taxa have close phylogenetic relatives overseas (predominantly Australian), indicating their recent ancestors were tramps, too. Distinctive taxa with deep phylogenetic ancestry might be ‘vicars’ that owe their presence to vicariance, but lack of close morphological, taxonomic and phylogenetic affinity provides only tenuous evidence for this. Disproving the alternative possibility that apparent vicars are descended from tramps that dispersed in earlier times remains challenging, but molecular analyses have yielded startling insights. Among New Zealand’s iconic taxa, the world’s largest eagle shared a Pleistocene ancestor with a small Australian eagle, and giant, flightless moa are phylogenetic sisters of the much smaller, flying tinamous of South America. The New Zealand avifauna is neither isolated nor stable, but demonstrative of prolonged and ongoing colonization, speciation and extinction.     

Some Differences between Plants of the Chatham Islands and the New Zealand Mainland

A number of Chatham Island plants show morphological differences from related plants on mainland New Zealand. These differences could have arisen as a result of freedom from moa browsing on the Chatham Islands. A possible test for this hypothesis is suggested.     

Faunal influences on New Zealand seed dispersal characteristics

A range of distinctive dispersal features have been recognised within the New Zealand flora, and a wide range of fauna are involved in the dispersal of seed in New Zealand, either by consuming fruit or seed, or as transporters of adhesive seed. In this study the composition of New Zealand’s zoochorous fauna (except insects) was examined using both trait matching within environmental, morphological and behavioural variables, and compared to the trait pattern of the groups of plant species they disperse. The importance of the different dispersal groups to the plant species they disperse varies with habitat, landform, region of New Zealand, foraging behaviour, and morphology. Over half of New Zealand’s vertebrate fauna are involved in fruit dispersal, though only 6% are considered frugivorous—the remainder include varying quantities of insects and other plant material in their diets. Flighted species are over-represented in wooded environments and higher strata and flightless species predominate in low alpine and grassland habitats. The frugivore-fruiting plant interaction group shows some indications of ecological generalism as frugivorous species consume a range of fruit sizes across all vegetation strata and fruit-bearing plants have lower species diversity and occupy a wide range of habitats. Granivores are over-represented in wetland habitats and the eastern South Island. The importance of species which unintentionally disperse adhesive seed depends on whether they are volant (higher importance in coastal environments) or flightless (higher importance dry grasslands and in low alpine areas). A subgroup of birds, such as the ratite Apteryx spp. and the now extinct Dinornithiform moa, with loose feathers (“velcro” species) are over-represented in lower vegetation strata and this matches the zone where many attachment-dispersed plant species present their seed.     

A Megafauna’s Microfauna: Gastrointestinal Parasites of New Zealand’s Extinct Moa (Aves: Dinornithiformes)

We perform the first multidisciplinary study of parasites from an extinct megafaunal clade using coprolites from the New Zealand moa (Aves: Dinornithiformes). Ancient DNA and microscopic analyses of 84 coprolites deposited by four moa species (South Island giant moa, Dinornis robustus; little bush moa, Anomalopteryx didiformis; heavy-footed moa, Pachyornis elephantopus; and upland moa, Megalapteryx didinus) reveal an array of gastrointestinal parasites including coccidians (Cryptosporidium and members of the suborder Eimeriorina), nematodes (Heterakoidea, Trichostrongylidae, Trichinellidae) and a trematode (Echinostomida). Parasite eggs were most prevalent and diverse in coprolites from lowland sites, where multiple sympatric moa species occurred and host density was therefore probably higher. Morphological and phylogenetic evidence supports a possible vicariant Gondwanan origin for some of the moa parasites. The discovery of apparently host-specific parasite taxa suggests paleoparasitological studies of megafauna coprolites may provide useful case-studies of coextinction.     

The ancient DNA revolution: the latest era in unearthing New Zealand’s faunal history

In the 25 years since the first DNA sequences were obtained from the extinct moa, ancient DNA analyses have significantly advanced our understanding of New Zealand's unique fauna. Here, we review how DNA extracted from ancient faunal remains has provided new insights into the evolutionary histories and phylogenetic relationships of New Zealand animals, and the impacts of human activities upon their populations. Moreover, we review how ancient DNA has played a key role in improving our ability to taxonomically identify fragmentary animal remains, determine biological function within extinct species, reconstruct past faunas and communities based on DNA preserved in sediments, resolve aspects of the ecology of extinct animals and characterising prehistoric parasite faunas. As ancient DNA analyses continue to become increasingly applied, and sequencing technologies continue to improve, the next 25 years promises to provide many more exciting new insights and discoveries about New Zealand's unique fauna.     

Nest predators and the evolution of avian reproductive strategies: a comparison of Australian and New Zealand birds

Summary Nest predation has been considered an important factor in the evolution of avian life histories: smaller clutches and shorter incubation and nestling periods are expected where nest predation has significant effects on reproductive success. Unlike the Australian avifauna, terrestrial New Zealand birds have evolved in the absence of reptilian and mammalian predators. Here we compare the reproductive strategies of terrestrial native New Zealand birds with those of their Australian sister taxa. In 11 of 14 comparisons, New Zealand birds were larger than their Australian relatives, but we did not find any significant differences in reproductive tactics between the two regions, a result inconsistent with the nest predation hypothesis. We discuss several reasons why this may be so. One possibility is that selection imposed on avian life history tactics by mammalian predators following the arrival of humans in New Zealand has led to strategies similar to those adopted in Australia.