Coprolites reveal ecological interactions lost with the extinction of New Zealand birds.
ABSTRACT: Over the past 50,000 y, biotic extinctions and declines have left a legacy of vacant niches and broken ecological interactions across global terrestrial ecosystems. Reconstructing the natural, unmodified ecosystems that preceded these events relies on high-resolution analyses of paleoecological deposits. Coprolites are a source of uniquely detailed information about trophic interactions and the behaviors, gut parasite communities, and microbiotas of prehistoric animal species. Such insights are critical for understanding the legacy effects of extinctions on ecosystems, and can help guide contemporary conservation and ecosystem restoration efforts. Here we use high-throughput sequencing (HTS) of ancient eukaryotic DNA from coprolites to reconstruct aspects of the biology and ecology of four species of extinct moa and the critically endangered kakapo parrot from New Zealand (NZ). Importantly, we provide evidence that moa and prehistoric kakapo consumed ectomycorrhizal fungi, suggesting these birds played a role in dispersing fungi that are key to NZ's natural forest ecosystems. We also provide the first DNA-based evidence that moa frequently supplemented their broad diets with ferns and mosses. Finally, we also find parasite taxa that provide insight into moa behavior, and present data supporting the hypothesis of coextinction between moa and several parasite species. Our study demonstrates that HTS sequencing of coprolites provides a powerful tool for resolving key aspects of ancient ecosystems and may rapidly provide information not obtainable by conventional paleoecological techniques, such as fossil analyses.
Project description:Knowledge of extinct herbivore community structuring is essential for assessing the wider ecological impacts of Quaternary extinctions and determining appropriate taxon substitutes for rewilding. Here, we demonstrate the potential for coprolite studies to progress beyond single-species diet reconstructions to resolving community-level detail. The moa (Aves: Dinornithiformes) of New Zealand are an intensively studied group of nine extinct herbivore species, yet many details of their diets and community structuring remain unresolved. We provide unique insights into these aspects of moa biology through analyses of a multispecies coprolite assemblage from a rock overhang in a montane river valley in southern New Zealand. Using ancient DNA (aDNA), we identified 51 coprolites, which included specimens from four sympatric moa species. Pollen, plant macrofossils, and plant aDNA from the coprolites chronicle the diets and habitat preferences of these large avian herbivores during the 400 y before their extinction (?1450 AD). We use the coprolite data to develop a paleoecological niche model in which moa species were partitioned based on both habitat (forest and valley-floor herbfield) and dietary preferences, the latter reflecting allometric relationships between body size, digestive efficiency, and nutritional requirements. Broad ecological niches occupied by South Island giant moa (Dinornis robustus) and upland moa (Megalapteryx didinus) may reflect sexual segregation and seasonal variation in habitat use, respectively. Our results show that moa lack extant ecological analogs, and their extinction represents an irreplaceable loss of function from New Zealand's terrestrial ecosystems.
Project description: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.
Project description: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.
Project description:The extinction of New Zealand's moa (Aves: Dinornithiformes) followed the arrival of humans in the late 13th century and was the final event of the prehistoric Late Quaternary megafauna extinctions. Determining the state of the moa populations in the pre-extinction period is fundamental to understanding the causes of the event. We sampled 281 moa individuals and combined radiocarbon dating with ancient DNA analyses to help resolve the extinction debate and gain insights into moa biology. The samples, which were predominantly from the last 4,000 years preceding the extinction, represent four sympatric moa species excavated from five adjacent fossil deposits. We characterized the moa assemblage using mitochondrial DNA and nuclear microsatellite markers developed specifically for moa. Although genetic diversity differed significantly among the four species, we found that the millennia preceding the extinction were characterized by a remarkable degree of genetic stability in all species, with no loss of heterozygosity and no shifts in allele frequencies over time. The extinction event itself was too rapid to be manifested in the moa gene pools. Contradicting previous claims of a decline in moa before Polynesian settlement in New Zealand, our findings indicate that the populations were large and stable before suddenly disappearing. This interpretation is supported by approximate Bayesian computation analyses. Our analyses consolidate the disappearance of moa as the most rapid, human-facilitated megafauna extinction documented to date.
Project description:Climatic changes during the late Quaternary have resulted in substantial, often abrupt, rearrangements of terrestrial ecosystems, but the relationship between these environmental changes and prehistoric human culture and population size remains unclear. Using a database of archaeological radiocarbon dates alongside a network of paleoecological records (sedimentary pollen and charcoal) and paleoclimatic reconstructions, we show that periods of cultural and demographic change in the northeastern United States occurred at the same times as the major environmental-climatic transitions of that region. At 11.6, 8.2, 5.4, and 3.0 kyr BP (10(3) calendar years before present), changes in forest composition altered the distribution, availability, and predictability of food resources which triggered technological adjustments manifested in the archaeological record. Human population level has varied in response to these external changes in ecosystems, but the adoption of maize agriculture during the late Holocene also resulted in a substantial population increase. This study demonstrates the long-term interconnectedness of prehistoric human cultures and the ecosystems they inhabited, and provides a consolidated environmental-cultural framework from which more interdisciplinary research and discussion can develop. Moreover, it emphasizes the complex nature of human responses to environmental change in a temperate region.
Project description:Understanding extinction drivers in a human-dominated world is necessary to preserve biodiversity. We provide an overview of Quaternary extinctions and compare mammalian extinction events on continents and islands after human arrival in system-specific prehistoric and historic contexts. We highlight the role of body size and life-history traits in these extinctions. We find a significant size-bias except for extinctions on small islands in historic times. Using phylogenetic regression and classification trees, we find that while life-history traits are poor predictors of historic extinctions, those associated with difficulty in responding quickly to perturbations, such as small litter size, are good predictors of prehistoric extinctions. Our results are consistent with the idea that prehistoric and historic extinctions form a single continuing event with the same likely primary driver, humans, but the diversity of impacts and affected faunas is much greater in historic extinctions.
Project description:The pristine island ecosystems of East Polynesia were among the last places on Earth settled by prehistoric people, and their colonization triggered a devastating transformation. Overhunting contributed to widespread faunal extinctions and the decline of marine megafauna, fires destroyed lowland forests, and the introduction of the omnivorous Pacific rat (Rattus exulans) led to a new wave of predation on the biota. East Polynesian islands preserve exceptionally detailed records of the initial prehistoric impacts on highly vulnerable ecosystems, but nearly all such studies are clouded by persistent controversies over the timing of initial human colonization, which has resulted in proposed settlement chronologies varying from approximately 200 B.C. to 1000 A.D. or younger. Such differences underpin radically divergent interpretations of human dispersal from West Polynesia and of ecological and social transformation in East Polynesia and ultimately obfuscate the timing and patterns of this process. Using New Zealand as an example, we provide a reliable approach for accurately dating initial human colonization on Pacific islands by radiocarbon dating the arrival of the Pacific rat. Radiocarbon dates on distinctive rat-gnawed seeds and rat bones show that the Pacific rat was introduced to both main islands of New Zealand approximately 1280 A.D., a millennium later than previously assumed. This matches with the earliest-dated archaeological sites, human-induced faunal extinctions, and deforestation, implying there was no long period of invisibility in either the archaeological or palaeoecological records.
Project description:Often the mutualistic roles of extinct species are inferred based on plausible assumptions, but sometimes palaeoecological evidence can overturn such inferences. We present an example from New Zealand, where it has been widely assumed that some of the largest-seeded plants were dispersed by the giant extinct herbivorous moa (Dinornithiformes). The presence of large seeds in preserved moa gizzard contents supported this hypothesis, and five slow-germinating plant species (Elaeocarpus dentatus, E. hookerianus, Prumnopitys ferruginea, P. taxifolia, Vitex lucens) with thick seedcoats prompted speculation about whether these plants were adapted for moa dispersal. However, we demonstrate that all these assumptions are incorrect. While large seeds were present in 48% of moa gizzards analysed, analysis of 152 moa coprolites (subfossil faeces) revealed a very fine-grained consistency unparalleled in extant herbivores, with no intact seeds larger than 3.3 mm diameter. Secondly, prolonged experimental mechanical scarification of E. dentatus and P. ferruginea seeds did not reduce time to germination, providing no experimental support for the hypothesis that present-day slow germination results from the loss of scarification in moa guts. Paradoxically, although moa were New Zealand's largest native herbivores, the only seeds to survive moa gut passage intact were those of small-seeded herbs and shrubs.
Project description:There is a nearly 10,000-year history of human presence in the western Gulf of Alaska, but little understanding of how human foragers integrated into and impacted ecosystems through their roles as hunter-gatherers. We present two highly resolved intertidal and nearshore food webs for the Sanak Archipelago in the eastern Aleutian Islands and use them to compare trophic roles of prehistoric humans to other species. We find that the native Aleut people played distinctive roles as super-generalist and highly-omnivorous consumers closely connected to other species. Although the human population was positioned to have strong effects, arrival and presence of Aleut people in the Sanak Archipelago does not appear associated with long-term extinctions. We simulated food web dynamics to explore to what degree introducing a species with trophic roles like those of an Aleut forager, and allowing for variable strong feeding to reflect use of hunting technology, is likely to trigger extinctions. Potential extinctions decreased when an invading omnivorous super-generalist consumer focused strong feeding on decreasing fractions of its possible resources. This study presents the first assessment of the structural roles of humans as consumers within complex ecological networks, and potential impacts of those roles and feeding behavior on associated extinctions.
Project description:Parasite host switches may trigger disease emergence, but prehistoric host ranges are often unknowable. Lymphatic filariasis and loiasis are major human diseases caused by the insect-borne filarial nematodes Brugia, Wuchereria and Loa. Here we show that the genomes of these nematodes and seven tropical bird lineages exclusively share a novel retrotransposon, AviRTE, resulting from horizontal transfer (HT). AviRTE subfamilies exhibit 83-99% nucleotide identity between genomes, and their phylogenetic distribution, paleobiogeography and invasion times suggest that HTs involved filarial nematodes. The HTs between bird and nematode genomes took place in two pantropical waves, >25-22 million years ago (Myr ago) involving the Brugia/Wuchereria lineage and >20-17 Myr ago involving the Loa lineage. Contrary to the expectation from the mammal-dominated host range of filarial nematodes, we hypothesize that these major human pathogens may have independently evolved from bird endoparasites that formerly infected the global breadth of avian biodiversity.