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For tens of millions of years the ratite moa (Aves: Dinornithiformes) were the largest herbivores in New Zealand’s terrestrial ecosystems. In occupying this ecological niche for such a long time, moa undoubtedly had a strong influence on the evolution of New Zealand’s flora and played important functional roles within ecosystems. The extinction of moa in the 15th century ce therefore marked a significant event in New Zealand’s biological history, not only in terms of biodiversity loss, but in the loss of an evolutionarily and ecologically distinct order of birds. Understanding the full extent and magnitude of this loss, and its implications for New Zealand ecosystems, depends upon a detailed knowledge of moa diets. Over the past 100 years, periodic discoveries of preserved moa gizzard content and coprolites (ancient preserved dung) have gradually begun to shed light on the diets of moa and their roles within New Zealand ecosystems. Here, we review how the study of such samples has shaped our understanding of moa diets through time. We then provide a synthesis of current knowledge about moa diets, including summarising 2755 records of plant remains from 23 moa gizzard contents and 158 moa coprolites. A clear picture is now emerging of distinct differences between the feeding ecologies of moa species, which together with differences in habitat preferences facilitated niche partitioning. Such insights provide empirical data to inform the debate surrounding the role of moa herbivory in the evolution of distinctive plant traits within the New Zealand flora. These data also help identify specific ecological functions and roles that have been lost due to the extinction of moa, and resolve to what extent these could be replaced via surrogate taxa.
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... 47 Many endemic species became extinct rapidly following the arrival of humans in New 48 Zealand [10][11][12], including the moa-an order of giant, flightless, palaeognathous birds 49 comprising nine Late Quaternary species [13,14]. Moa species appear to have been 50 adapted to different habitats and diets, inhabiting a wide range of environments, including 51 subalpine areas, forest, and open shrubland-grasslands [15,16] periods (Late Pleistocene: specimens older than 11.65 kya; Holocene: specimens 111 younger than 11.65 kya) for specimens of known age. To examine whether eastern moa 112 found within their potential LGM range (southern South Island) contained higher levels of 113 genetic diversity (i.e. more rare/private haplotypes) than populations outside of this range, 114 we repeated these analyses after binning samples within/outside this putative range, and 115 constructed a median-joining haplotype network in PopART [35] to visualise these results. ...
... Although we are unable to determine 177 the exact timing of this increase, we suggest that it corresponds to the expansion of 178 eastern moa from their southern refugium following the LGM. Although little is known 179 about the diet of eastern moa (recently reviewed by [15]), it has been suggested that they 180 perhaps had a similar diet to stout-legged moa (Euryapteryx curtus gravis), comprising 181 fruits and leaves from trees and shrubs [15,40]. Thus, a possible driver of both the proportional to haplotype frequency, while mutations are represented by hatch marks. ...
... Although we are unable to determine 177 the exact timing of this increase, we suggest that it corresponds to the expansion of 178 eastern moa from their southern refugium following the LGM. Although little is known 179 about the diet of eastern moa (recently reviewed by [15]), it has been suggested that they 180 perhaps had a similar diet to stout-legged moa (Euryapteryx curtus gravis), comprising 181 fruits and leaves from trees and shrubs [15,40]. Thus, a possible driver of both the proportional to haplotype frequency, while mutations are represented by hatch marks. ...
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Cycles of glacial expansion and contraction throughout the Pleistocene drove increases and decreases, respectively, in the geographical range and population size of many animal species. Genetic data have revealed that during glacial maxima the distribution of many Eurasian animals was restricted to small refugial areas, from which species expanded to reoccupy parts of their former range as the climate warmed. It has been suggested that the extinct eastern moa ( Emeus crassus )—a large, flightless bird from New Zealand—behaved analogously during glacial maxima, possibly surviving only in a restricted area of lowland habitat in the southern South Island of New Zealand during the Last Glacial Maximum (LGM). However, previous studies have lacked the power and geographical sampling to explicitly test this hypothesis using genetic data. Here we analyse 46 ancient mitochondrial genomes from Late Pleistocene and Holocene bones of the eastern moa from across their post-LGM distribution. Our results are consistent with a post-LGM increase in the population size and genetic diversity of eastern moa. We also demonstrate that genetic diversity was higher in eastern moa from the southern extent of their range, supporting the hypothesis that they expanded from a single glacial refugium following the LGM.
... These were large (some over 3 m tall), flightless, now extinct, herbivorous birds (Worthy and Holdaway, 2002). The coprolites indicate what the birds were eating (Wood et al., 2020) and provide a further window to the nature of the local vegetation. ...
... These include conifers. In particular, Prumnopitys taxifolia, is known to have been ingested (in other areas) by all the moa species present in the study area (Wood et al., 2020). It is inconceivable that if it formed a prominent part of the vegetation near the shelters, some trace of it would not have been found in the course of this study. ...
... That is, they contain a subset of the plants found in the dry vegetation zone, and it's likely that continued study would find the rest. The cuticle results support Wood et al.'s (2012) cuticle record of Myrsine consumption and of mistletoes (Wood et al., 2020(Wood et al., , 2021. It also confirms the suggestion of that based on the presence of its pollen in coprolites, Carmichaelia was probably directly consumed by the moa. ...
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Looks at Holocene leaf cuticle in rock overhangs and moa coprolites.
... These adaptations allowed moa to have a wide variety of tensile conditions in their diet, including divaricate species (e.g. Wood et al. 2020). Furthermore, Bond also compared Madagascar wire plants-with similar divaricate characteristics-for stem tensile strengths to related nondivaricate species from Southern Africa (Bond & Silander 2007). ...
... Different moa species occupied different niches and thus diet changed depending on adaptation and location. Gizzard and coprolite moa samples do however indicate browsing on a range of tree and shrub species, with at least some moa species consuming divaricates (Burrows 1989;Wood et al. 2020). ...
Article
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Divaricate plant species account for more than 10% of New Zealand/Aotearoa's woody flora, a higher proportion for that life form than anywhere else on earth. Two main hypotheses have been proposed to account for the prevalence of this phenotype. The first suggests herbivorous birds, particularly large flightless moa, exerted selective pressure on many plants to adopt the form. The second proposes climate as the main driver since insular New Zealand has many exposed habitats and, historically, experienced stressing conditions during the Pleistocene. Our study investigated two questions to shed further light on the evolution of divaricates, in particular related to the potential influence of browsing by large avian herbivores. First, divaricate plants have been posited to have a higher tensile strength than non‐divaricates as a defence mechanism against moa browsing. We tested the great majority of New Zealand plant genera within which divaricates occur, contrasting the stem tensile strength of these plants against their closest non‐divaricate counterparts using accurate testing technology. The results indicate divaricate species have tensile strength that approaches twice that of non‐divaricates across a broad and disparate phylogenetic range that includes gymnosperms and many clades of angiosperms. Second, we tested the species level distributions of widely dispersed woody plant genera across the New Zealand archipelago on islands where moa had been present or always absent. We found that no endemic divaricate species occurred on any islands from which moa had been permanently absent. In contrast, their non‐divaricate counterparts were commonly endemic to those same islands.
... Ecological conditions specific to New Zealand, such as the absence of grazing mammals and fire regimes through evolutionary time (Antonelli et al., 2011), could also have promoted diversification. Veronica may have been consumed by now-extinct mega-herbivores (Wood et al., 2020), which could have driven differences in extinction or defence mechanisms. ...
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How mountains accumulate species diversity remains poorly understood, particularly the relative role of in situ cladogenesis compared with colonization from lower elevations. Here, we estimated the contributions of in situ cladogenesis and colonization in generating biodiversity of a large mountain plant radiation and determined the importance of niche adaptation and divergence in these processes. We expected cladogenesis would accompany novel habitats formed by mountain uplift, but colonization would become more important with time as dispersal opportunities accrue. New Zealand, Southern Alps. Veronica sect. Hebe (Plantaginaceae). We estimated the most complete time‐calibrated phylogeny to date for Veronica sect. Hebe to quantify rates of in situ cladogenesis and colonization of mountain habitat based on historical biogeographical models. We used environmental niche modelling to quantify species' climate niches and estimate niche disparity and divergence over time. In situ cladogenesis generated more species in the mountains than colonization from lowlands. Whereas cladogenesis slowed over time, colonization increased, especially in the alpine zone. Both adaptive ecological speciation along climate niche axes and non‐adaptive, vicariant speciation contributed to cladogenesis. However, climate niche disparity through time became saturated, suggesting competition for niche space was important. Colonization brought more divergent species into mountain niches. We suggest mountain diversity accumulates through three main stages: high cladogenesis after initial colonization, decreasing cladogenesis with increasing competition and increasing colonization after niches saturate, likely promoted by niche divergence. Combining lineage and mountain uplift trajectories, these stages provide a conceptual model to understand how diversity accumulates elsewhere. Assuming these deep‐time findings apply to anthropogenic conditions, alpine specialists could struggle to outcompete colonizers facilitated by climate change, especially from generalist clades. Considering novel competitive interactions alongside niche traits and biogeographical processes will be crucial for predicting the fate of alpine biodiversity in a changing world.
... Ecological conditions specific to New Zealand, such as the absence of grazing mammals and fire regimes through evolutionary time (Antonelli et al., 2011), could also have promoted diversification. Veronica may have been consumed by now-extinct mega-herbivores (Wood et al., 2020), which could have driven differences in extinction or defense mechanisms. Pollination and seed dispersal interactions, by contrast, are unlikely to have been important, as Veronica pollinators tend to be generalists and seeds are wind or gravity dispersed (Bayly & Kellow, 2006). ...
Thesis
Global change is putting unprecedented pressure on plants to adapt or migrate to avoid extinction. Studying the past responses of plants to environmental change can shed light on the potential evolutionary outcomes and sensitivity of species to future environmental change. These processes are especially relevant to highly diverse, evolutionarily rich, and ecologically vulnerable alpine ecosystems. My PhD aims to narrow the uncertainty about how plant lineages with a range of lowland and alpine species will be impacted by global change by studying the historical biogeography, trait and species diversification, and ecological strategies of alpine species in a phylogenetic framework. Chapter 1 reviews current knowledge about the relative roles of migration and adaptation in plant responses to climate change and how historical biogeographical and evolutionary modeling provide novel insights to these questions. Chapter 2 applies recent developments in sequencing methods to construct a new, near-complete phylogeny of a diverse species radiation, New Zealand Veronica, also addressing questions about how to resolve difficulties in reconstructing phylogenetic relationships in recent, rapid radiations such as Veronica. This group serves as an important case study for further evolutionary questions about the relationships between habitat, species diversity, and environmental change. Chapter 3 estimates the contributions of in situ cladogenesis (i.e., the formation of new species) and colonization from lowland habitat in generating mountain diversity in Veronica. Further, the chapter explores the importance of niche adaptation and divergence in contributing to cladogenesis, and presents a general, conceptual model to understand how mountain diversity accumulates. Chapter 4 compares the potential range and niche change required for plant species to respond to future climate change relative to the change undergone since the mid-Holocene. It also determines which niche traits can predict “winners” and “losers” under climate change. Chapter 5 discusses the main findings of the thesis and ends with proposed avenues for future research.
... One can speculate that, in New Zealand, grazing by these birds may have been a major driving force behind the toxicity of U. ferox stings. Indeed, recent investigations of subfossil moa gizzard contents and coprolites have shown that Urtica was part of the diet of several moa species (31). ...
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The stinging hairs of plants from the family Urticaceae inject compounds that inflict pain to deter herbivores. The sting of the New Zealand tree nettle (Urtica ferox) is among the most painful of these and can cause systemic symptoms that can even be life-threatening; however, the molecular species effecting this response have not been elucidated. Here we reveal that two classes of peptide toxin are responsible for the symptoms of U. ferox stings: Δ-Uf1a is a cytotoxic thionin that causes pain via disruption of cell membranes, while β/δ-Uf2a defines a new class of neurotoxin that causes pain and systemic symptoms via modulation of voltage-gated sodium (NaV) channels. We demonstrate using whole-cell patch-clamp electrophysiology experiments that β/δ-Uf2a is a potent modulator of human NaV1.5 (EC50: 55 nM), NaV1.6 (EC50: 0.86 nM) and NaV1.7 (EC50: 208 nM), where it shifts the activation threshold to more negative potentials and slows fast inactivation. We further found that both toxin classes are widespread among members of the Urticeae tribe within Urticaceae, suggesting that they are likely to be pain-causing agents underlying the stings of other Urtica species. Comparative analysis of nettles of Urtica, and the recently described pain-causing peptides from nettles of another genus, Dendrocnide, indicates that members of tribe Urticeae have developed a diverse arsenal of pain-causing peptides.
... Before human arrival in New Zealand, the ratite moa were the largest of the terrestrial herbivores. pollen, macrofossil, and ancient DNA studies of their distinctive coprolites (Fig. 1b) show that these birds browsed widely on trees, shrubs, climbers, herbs, forbs, and ferns (Wood et al. 2020). The extinction of all nine moa species by ca. ...
Preprint
(Follow the doi above for the article pdf) Pollen and ancient DNA from coprolites and peat reveal new and surprising insights about past pollination, herbivory, and native/alien status in New Zealand. These paleoecological findings help in understanding ecosystem structure and function before human arrival, informing current conservation, restoration, and management issues.
... Evidence of their existence remains in New Zealand's flora, some of which retains anachronistic defenses against browsing by moa [368,369]. Moa coprolites and preserved gizzard contents indicate that they were generalist herbivores, though some degree of species-specific dietary niche partitioning existed [370]. ...
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The extant diversity of the avian clade Palaeognathae is composed of the iconic flightless ratites (ostriches, rheas, kiwi, emus, and cassowaries), and the volant tinamous of Central and South America. Palaeognaths were once considered a classic illustration of diversification driven by Gondwanan vicariance, but this paradigm has been rejected in light of molecular phylogenetic and divergence time results from the last two decades that indicate that palaeognaths underwent multiple relatively recent transitions to flightlessness and large body size, reinvigorating research into their evolutionary origins and historical biogeography. This revised perspective on palaeognath macroevolution has highlighted lingering gaps in our understanding of how, when, and where extant palaeognath diversity arose. Towards resolving those questions, we aim to comprehensively review the known fossil record of palaeognath skeletal remains, and to summarize the current state of knowledge of their evolutionary history. Total clade palaeognaths appear to be one of a small handful of crown bird lineages that crossed the Cretaceous-Paleogene (K-Pg) boundary, but gaps in their Paleogene fossil record and a lack of Cretaceous fossils preclude a detailed understanding of their multiple transitions to flightlessness and large body size, and recognizable members of extant subclades generally do not appear until the Neogene. Despite these knowledge gaps, we combine what is known from the fossil record of palaeognaths with plausible divergence time estimates, suggesting a relatively rapid pace of diversification and phenotypic evolution in the early Cenozoic. In line with some recent authors, we surmise that the most recent common ancestor of palaeognaths was likely a relatively small-bodied, ground-feeding bird, features that may have facilitated total-clade palaeognath survivorship through the K-Pg mass extinction, and which may bear on the ecological habits of the ancestral crown bird.
Chapter
As an introduced ‘invasive’ species, sika in New Zealand are regarded by some as conservation pests and by others as a hunting resource. We trace the history of herd development over the 116 years since sika were first introduced and summarise the changes in the management of the herd. Introduced as a hunting resource, they (and other deer species) quickly became regarded as pests and were subject to population control and then, in a minor way, to commercial hunting. Since the 1980s, however, recreational sika hunting has been predominant. Despite sika being highly valued as a recreational hunting resource, and despite there being no limits on when and how many sika can be harvested, current hunting pressure is insufficient to prevent high sika densities other than in the most readily accessible areas. That results in small body sizes with poor meat yield and/or trophy quality. Those high densities also cause substantial changes in the structure and composition of the native vegetation, so sika (and deer generally) continue to be seen as conservation pests. However, there is too little conservation funding to prioritise action against the unwanted impacts of sika on the local vegetation ahead of more urgent and important threats to indigenous biodiversity elsewhere. The result is poor outcomes both for hunting and for conservation. More active management of at least part of the herd (mainly through increased female harvest) is currently being mooted and could provide better joint outcomes.
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Large herbivores facilitate a range of important ecological processes yet globally have experienced high rates of decline and extinction over the past 50,000 years. To some extent this lost function may be replaced through the introduction of ecological surrogate taxa, either by active management or via historic introductions. However, comparing the ecological effects of herbivores that existed in the same location, but at different times, can be a challenging proposition. Here we provide an example from New Zealand that demonstrates an approach for making such comparisons. In New Zealand it has been suggested that post-19th Century mammal introductions (e.g. deer and hare) may have filled ecological niches left vacant after the 15th Century AD extinction of large avian herbivores (moa). We quantified pollen assemblages from fecal samples deposited by these two asynchronous herbivore communities to see whether they were comparable. The fecal samples were collected at the same location, and in a native-dominated vegetation community that has experience little anthropogenic disturbance and their contents reflect both the local habitat and diet preferences of the depositing herbivore. The results reveal that the current forest understory is relatively sparse and species depauperate compared to the prehistoric state, indicating that deer and moa had quite different impacts on the local vegetation community. The study provides an example of how combining coprolite and fecal analyses of prehistoric and modern herbivores may clarify the degree of ecological overlap between asynchronous herbivore communities and provide insights into the extent of ecological surrogacy provided by introduced taxa.
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A key rationale for pursuing de-extinction is the potential to restore lost processes and function to modern ecosystems. However, understanding and providing for the ecological requirements of the candidate species will also play a key role in determining the ultimate success of a de-extinction. This assessment is challenging for prehistoric extinct species, where empirical studies or observations on their ecology are not available or are incomplete. 2.A healthy, stable and self-sustaining population of a resurrected species needs to be embedded in an ecological interaction network that consists not only of interactions between a resurrected species and its external environment (e.g. habitat, diet), but also those where the resurrected species is the environment (e.g. microbiota and parasites). Palaeoecology can provide information on all of these interactions for extinct species, and this information can help guide and inform the selection of suitable de-extinction candidates or traits for resurrection. 3.Ecological interaction network analyses offer a complementary tool to existing frameworks for determining the suitability of de-extinction candidates, allowing palaeoecological information to be used to identify and quantify the potential implications of removing or adding resurrected species/functions to an ecosystem. 4.Although palaeoecological data and understanding clearly have an important role in informing and modelling the potential ecological functions provided by extinct species, they can only ever provide an incomplete picture, and therefore would only complement, rather than replace, observational or experimental data on the resurrected organisms themselves. This article is protected by copyright. All rights reserved.