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.

Keywords: New Zealand; ancient DNA; coprolites; metabarcoding; moa.

Fig. 1.

Map of New Zealand’s South Island with localities of the coprolites used in this study. Relevant paleoenvironments are shown.

Fig. 2.

Proportions of reads per sample to taxonomic and ecological groups as determined using QIIME. All OTUs present in extraction blanks are filtered. Note the unequal total read counts among samples.

Fig. 3.

Distribution of select taxa among samples, identified to the lowest possible taxonomic rank. *Designates a taxon inclusive of the taxon immediately following. The number of OTUs is in brackets. (Top Right) An approximation and overlap of the different moa species distributions relative to precipitation/aridity and altitude. Taxon groups: Al, Alveolata; As, Ascomycota; Ba, Basidiomycota; Br, Bryophyta; Di, dicots; Mo, monocots; Ne, Nematoda; Pt, Pteridiophyta (ferns); Tr, Trematoda. Sites: C, Honeycomb Cave; D, Dart River; E, Euphrates Cave; H, Hodge Creek; K, Kawarau Gorge; N, Mt. Nicholas; R, Roxburgh Gorge; S, Shepherd’s Creek; Z, zoo.