Biomonitoring tool for New Zealand peatlands: Testate amoebae and vascular plants as promising bioindicators.

In the last two centuries, a high proportion of peatlands have been lost or severely degraded across the world. The value of peatlands is now well-recognised for biodiversity conservation, flood management, and carbon mitigation, with peatland restoration now central to many government policies for climate action. A challenge, however, is to determine 'natural' and 'disturbed' conditions of peatlands to establish realistic baselines for assessing degradation and setting restoration targets. This requires a tool or set of tools that can rapidly and reliably capture peatland condition across space and time. Our aim was to develop such a tool based on combined analysis of plant and testate amoebae; a group of shelled protists commonly used as indicators of ecological change in peatlands. The value of testate amoebae is well established in Northern Hemisphere Sphagnum-dominated peatlands; however, relatively little work has been undertaken for Southern Hemisphere peat forming systems. Here we provide the first assessment and comparison of the bioindicator value of testate amoebae and vascular plants in the context of Southern Hemisphere peatlands. Our results further demonstrate the unique ecohydrological dynamics at play in New Zealand peat forming systems that set them apart from Northern Hemisphere peatlands. Our results show that plant and testate amoeba communities provided valuable information on peatland condition at different scales, we found that testate amoebae tracked changes in the abiotic variables (depth to water table, pH, and conductivity) more closely than vascular plants. Our results further demonstrate that functional traits of testate amoebae showed promising relationships with disturbance. Amoeba test compression, aperture position and test size were linked to changes in hydrology driven by fluctuations in ground water tables; however, trait responses manifested differently in ombrotrophic and minerotrophic peatlands. Overall, testate amoebae provide a promising bioindicator for tracking degradation in New Zealand peatlands and a potential additional tool to assess peatland condition.

Long-term trajectories of non-native vegetation on islands globally.

Human-mediated changes in island vegetation are, among others, largely caused by the introduction and establishment of non-native species. However, data on past changes in non-native plant species abundance that predate historical documentation and censuses are scarce. Islands are among the few places where we can track human arrival in natural systems allowing us to reveal changes in vegetation dynamics with the arrival of non-native species. We matched fossil pollen data with botanical status information (native, non-native), and quantified the timing, trajectories and magnitude of non-native plant vegetational change on 29 islands over the past 5000 years. We recorded a proportional increase in pollen of non-native plant taxa within the last 1000 years. Individual island trajectories are context-dependent and linked to island settlement histories. Our data show that non-native plant introductions have a longer and more dynamic history than is generally recognized, with critical implications for biodiversity baselines and invasion biology.

Superficially described and ignored for 92 years, rediscovered and emended: Apodera angatakere (Amoebozoa: Arcellinida: Hyalospheniformes) is a new flagship testate amoeba taxon from Aotearoa (New Zealand).

Eukaryotic microbial diversity is known to be extensive but remains largely undescribed and uncharted. While much of this unknown diversity is composed of inconspicuous flagellates and parasites, larger and morphologically distinct protists are regularly discovered, most notably from poorly studied regions. Here we report a new flagship species of hyalospheniid (Amoebozoa; Arcellinida; Hyalospheniformes) testate amoeba from New Zealand and an unusual story of overlooked description under a preoccupied name and subsequent oversight for nearly one century. Through a process involving The Maori Language Commission, we named the species Apodera angatakere, meaning "a shell with a keel." This species resembles Apodera vas but differs by the presence of a distinctive hollow keel. Cytochrome Oxidase Subunit 1 (COI) sequence data show that this species forms a distinct clade nested within genus Apodera. This conspicuous species is so far known only from New Zealand and is restricted to peatlands. It is one of the few examples of endemic microorganisms from this biodiversity hotspot and biogeographer's paradise. As over 90% of New Zealand's peatlands have been lost since European colonization and much of the remaining surfaces are threatened, Apodera angatakere could be a flagship species not only for microbial biogeography but also for island biodiversity conservation.

Mitogenomes Uncover Extinct Penguin Taxa and Reveal Island Formation as a Key Driver of Speciation.

The emergence of islands has been linked to spectacular radiations of diverse organisms. Although penguins spend much of their lives at sea, they rely on land for nesting, and a high proportion of extant species are endemic to geologically young islands. Islands may thus have been crucial to the evolutionary diversification of penguins. We test this hypothesis using a fossil-calibrated phylogeny of mitochondrial genomes (mitogenomes) from all extant and recently extinct penguin taxa. Our temporal analysis demonstrates that numerous recent island-endemic penguin taxa diverged following the formation of their islands during the Plio-Pleistocene, including the Galápagos (Galápagos Islands), northern rockhopper (Gough Island), erect-crested (Antipodes Islands), Snares crested (Snares) and royal (Macquarie Island) penguins. Our analysis also reveals two new recently extinct island-endemic penguin taxa from New Zealand's Chatham Islands: Eudyptes warhami sp. nov. and a dwarf subspecies of the yellow-eyed penguin, Megadyptes antipodes richdalei ssp. nov. Eudyptes warhami diverged from the Antipodes Islands erect-crested penguin between 1.1 and 2.5 Ma, shortly after the emergence of the Chatham Islands (∼3 Ma). This new finding of recently evolved taxa on this young archipelago provides further evidence that the radiation of penguins over the last 5 Ma has been linked to island emergence. Mitogenomic analyses of all penguin species, and the discovery of two new extinct penguin taxa, highlight the importance of island formation in the diversification of penguins, as well as the extent to which anthropogenic extinctions have affected island-endemic taxa across the Southern Hemisphere's isolated archipelagos.

Multiscale climate change impacts on plant diversity in the Atacama Desert.

Comprehending ecological dynamics requires not only knowledge of modern communities but also detailed reconstructions of ecosystem history. Ancient DNA (aDNA) metabarcoding allows biodiversity responses to major climatic change to be explored at different spatial and temporal scales. We extracted aDNA preserved in fossil rodent middens to reconstruct late Quaternary vegetation dynamics in the hyperarid Atacama Desert. By comparing our paleo-informed millennial record with contemporary observations of interannual variations in diversity, we show local plant communities behave differentially at different timescales. In the interannual (years to decades) time frame, only annual herbaceous expand and contract their distributional ranges (emerging from persistent seed banks) in response to precipitation, whereas perennials distribution appears to be extraordinarily resilient. In contrast, at longer timescales (thousands of years) many perennial species were displaced up to 1,000 m downslope during pluvial events. Given ongoing and future natural and anthropogenically induced climate change, our results not only provide baselines for vegetation in the Atacama Desert, but also help to inform how these and other high mountain plant communities may respond to fluctuations of climate in the future.

An avian seed dispersal paradox: New Zealand's extinct megafaunal birds did not disperse large seeds.

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.

Resolving lost herbivore community structure using coprolites of four sympatric moa species (Aves: Dinornithiformes).

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.

Functional and environmental determinants of bark thickness in fire-free temperate rain forest communities.

PREMISE OF THE STUDY: In fire-prone ecosystems, variation in bark thickness among species and communities has been explained by fire frequency; thick bark is necessary to protect cambium from lethal temperatures. Elsewhere this investment is deemed unnecessary, and thin bark is thought to prevail. However, in rain forest ecosystems where fire is rare, bark thickness varies widely among species and communities, and the causes of this variation remain enigmatic. We tested for functional explanations of bark thickness variation in temperate rain forest species and communities. METHODS: We measured bark thickness in 82 tree species throughout New Zealand temperate rain forests that historically have experienced little fire and applied two complementary analyses. First, we examined correlations between bark traits and leaf habit, and leaf and stem traits. Second, we calculated community-weighted mean (CWM) bark thickness for 272 plots distributed throughout New Zealand to identify the environments in which thicker-barked communities occur. KEY RESULTS: Conifers had higher size-independent bark thickness than evergreen angiosperms. Species with thicker bark or higher bark allocation coefficients were not associated with "slow economic" plant traits. Across 272 forest plots, communities with thicker bark occurred on infertile soils, and communities with thicker bark and higher bark allocation coefficients occurred in cooler, drier climates. CONCLUSIONS: In non-fire-prone temperate rain forest ecosystems, investment in bark is driven by soil resources, cool minimum temperatures, and seasonal moisture stress. The role of these factors in fire-prone ecosystems warrants testing.

Use of pollen and ancient DNA as conservation baselines for offshore islands in New Zealand.

Islands play a key role globally in the conservation of endemic species. Many island reserves have been highly modified since human colonization, and their restoration and management usually occur without knowledge of their prehuman state. However, conservation paleoecology is increasingly being recognized as a tool that can help to inform both restoration and conservation of island reserves by providing prehuman vegetation baselines. Many of New Zealand's mammal-free offshore islands are foci for biological diversity conservation and, like many islands in the Polynesian region, were deforested following initial human settlement. Therefore, their current restoration, replanting, and management are guided either by historic vegetation descriptions or the occurrence of species on forested islands. We analyzed pollen and ancient DNA in soil cores from an offshore island in northern New Zealand. The result was a 2000-year record of vegetation change that began >1200 years before human settlement and spanned 550 years of human occupation and 180 years of forest succession since human occupation ceased. Between prehuman and contemporary forests there was nearly a complete species turnover including the extirpation of a dominant conifer and a palm tree. The podocarp-dominated forests were replaced by a native but novel angiosperm-dominated forest. There is no modern analog of the prehuman forests on any northern New Zealand island, and those islands that are forested are dominated by angiosperms which are assumed to be climax forests. The pollen and DNA evidence for conifer- and palm-rich forests in the prehuman era challenge this climax forest assumption. Prehuman vegetation records can thus help to inform future restoration of degraded offshore islands by informing the likely rate and direction of successional change; helping to determine whether natural rates of succession are preferable to more costly replanting programs; and providing past species lists if restoration replanting is desired.

High-precision radiocarbon dating shows recent and rapid initial human colonization of East Polynesia.

The 15 archipelagos of East Polynesia, including New Zealand, Hawaii, and Rapa Nui, were the last habitable places on earth colonized by prehistoric humans. The timing and pattern of this colonization event has been poorly resolved, with chronologies varying by >1000 y, precluding understanding of cultural change and ecological impacts on these pristine ecosystems. In a meta-analysis of 1,434 radiocarbon dates from the region, reliable short-lived samples reveal that the colonization of East Polynesia occurred in two distinct phases: earliest in the Society Islands A.D. ∼1025-1120, four centuries later than previously assumed; then after 70-265 y, dispersal continued in one major pulse to all remaining islands A.D. ∼1190-1290. We show that previously supported longer chronologies have relied upon radiocarbon-dated materials with large sources of error, making them unsuitable for precise dating of recent events. Our empirically based and dramatically shortened chronology for the colonization of East Polynesia resolves longstanding paradoxes and offers a robust explanation for the remarkable uniformity of East Polynesian culture, human biology, and language. Models of human colonization, ecological change and historical linguistics for the region now require substantial revision.

Floristic homogenization of South Pacific islands commenced with human arrival.

The increasing similarity of plant species composition among distinct areas is leading to the homogenization of ecosystems globally. Human actions such as ecosystem modification, the introduction of non-native plant species and the extinction or extirpation of endemic and native plant species are considered the main drivers of this trend. However, little is known about when floristic homogenization began or about pre-human patterns of floristic similarity. Here we investigate vegetation trends during the past 5,000 years across the tropical, sub-tropical and warm temperate South Pacific using fossil pollen records from 15 sites on 13 islands within the biogeographical realm of Oceania. The site comparisons show that floristic homogenization has increased over the past 5,000 years. Pairwise Bray-Curtis similarity results also show that when two islands were settled by people in a given time interval, their floristic similarity is greater than when one or neither of the islands were settled. Importantly, higher elevation sites, which are less likely to have experienced human impacts, tended to show less floristic homogenization. While biotic homogenization is often referred to as a contemporary issue, we have identified a much earlier trend, likely driven by human colonization of the islands and subsequent impacts.

Reconstructing colonization dynamics to establish how human activities transformed island biodiversity.

Drivers and dynamics of initial human migrations across individual islands and archipelagos are poorly understood, hampering assessments of subsequent modification of island biodiversity. We developed and tested a new statistical-simulation approach for reconstructing the pattern and pace of human migration across islands at high spatiotemporal resolutions. Using Polynesian colonisation of New Zealand as an example, we show that process-explicit models, informed by archaeological records and spatiotemporal reconstructions of past climates and environments, can provide new and important insights into the patterns and mechanisms of arrival and establishment of people on islands. We find that colonisation of New Zealand required there to have been a single founding population of approximately 500 people, arriving between 1233 and 1257 AD, settling multiple areas, and expanding rapidly over both North and South Islands. These verified spatiotemporal reconstructions of colonisation dynamics provide new opportunities to explore more extensively the potential ecological impacts of human colonisation on New Zealand's native biota and ecosystems.

Ecological dynamics of moa extinctions reveal convergent refugia that today harbour flightless birds.

Human settlement of islands across the Pacific Ocean was followed by waves of faunal extinctions that occurred so rapidly that their dynamics are difficult to reconstruct in space and time. These extinctions included large, wingless birds called moa that were endemic to New Zealand. Here we reconstructed the range and extinction dynamics of six genetically distinct species of moa across New Zealand at a fine spatiotemporal resolution, using hundreds of thousands of process-explicit simulations of climate-human-moa interactions, which were validated against inferences of occurrence and range contraction from an extensive fossil record. These process-based simulations revealed important interspecific differences in the ecological and demographic attributes of moa and established how these differences influenced likely trajectories of geographic and demographic declines of moa following Polynesian colonization of New Zealand. We show that despite these interspecific differences in extinction dynamics, the spatial patterns of geographic range collapse of moa species were probably similar. It is most likely that the final populations of all moa species persisted in suboptimal habitats in cold, mountainous areas that were generally last and least impacted by people. We find that these refugia for the last populations of moa continue to serve as isolated sanctuaries for New Zealand's remaining flightless birds, providing fresh insights for conserving endemic species in the face of current and future threats.

Rapid landscape transformation in South Island, New Zealand, following initial Polynesian settlement.

Humans have altered natural patterns of fire for millennia, but the impact of human-set fires is thought to have been slight in wet closed-canopy forests. In the South Island of New Zealand, Polynesians (Maori), who arrived 700-800 calibrated years (cal y) ago, and then Europeans, who settled ∼150 cal y ago, used fire as a tool for forest clearance, but the structure and environmental consequences of these fires are poorly understood. High-resolution charcoal and pollen records from 16 lakes were analyzed to reconstruct the fire and vegetation history of the last 1,000 y. Diatom, chironomid, and element concentration data were examined to identify disturbance-related limnobiotic and biogeochemical changes within burned watersheds. At most sites, several high-severity fire events occurred within the first two centuries of Maori arrival and were often accompanied by a transformation in vegetation, slope stability, and lake chemistry. Proxies of past climate suggest that human activity alone, rather than unusually dry or warm conditions, was responsible for this increased fire activity. The transformation of scrub to grassland by Europeans in the mid-19th century triggered further, sometimes severe, watershed change, through additional fires, erosion, and the introduction of nonnative plant species. Alteration of natural disturbance regimes had lasting impacts, primarily because native forests had little or no previous history of fire and little resilience to the severity of burning. Anthropogenic burning in New Zealand highlights the vulnerability of closed-canopy forests to novel disturbance regimes and suggests that similar settings may be less resilient to climate-induced changes in the future.

A lost link between a flightless parrot and a parasitic plant and the potential role of coprolites in conservation paleobiology.

Late Quaternary extinctions and population fragmentations have severely disrupted animal-plant interactions globally. Detection of disrupted interactions often relies on anachronistic plant characteristics, such as spines in the absence of large herbivores or large fruit without dispersers. However, obvious anachronisms are relatively uncommon, and it can be difficult to prove a direct link between the anachronism and a particular faunal taxon. Analysis of coprolites (fossil feces) provides a novel way of exposing lost interactions between animals (depositors) and consumed organisms. We analyzed ancient DNA to show that a coprolite from the South Island of New Zealand was deposited by the rare and threatened kakapo (Strigops habroptilus), a large, nocturnal, flightless parrot. When we analyzed the pollen and spore content of the coprolite, we found pollen from the cryptic root-parasite Dactylanthus taylorii. The relatively high abundance (8.9% of total pollen and spores) of this zoophilous pollen type in the coprolite supports the hypothesis of a former direct feeding interaction between kakapo and D. taylorii. The ranges of both species have contracted substantially since human settlement, and their present distributions no longer overlap. Currently, the lesser short-tailed bat (Mystacina tuberculata) is the only known native pollinator of D. taylorii, but our finding raises the possibility that birds, and other small fauna, could have once fed on and pollinated the plant. If confirmed, through experimental work and observations, this finding may inform conservation of the plant. For example, it may be possible to translocate D. taylorii to predator-free offshore islands that lack bats but have thriving populations of endemic nectar-feeding birds. The study of coprolites of rare or extinct taxonomic groups provides a unique way forward to expand existing knowledge of lost plant and animal interactions and to identify pollination and dispersal syndromes. This approach of linking paleobiology with neoecology offers significant untapped potential to help inform conservation and restoration plans.

Dating the late prehistoric dispersal of Polynesians to New Zealand using the commensal Pacific rat.

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.

The testate amoebae of New Zealand: A checklist, identification key and assessment of biogeographic patterns.

New Zealand (NZ) is a well-known hotspot of biodiversity and endemism for macroscopic organisms, but its microbial diversity is comparatively poorly documented. We assembled all records on NZ testate amoebae published since the early 20th century and present a comprehensive taxonomic checklist for NZ. Testate amoebae are reported from six major habitat types across both the North and South Islands of NZ, but the sampling effort is ecologically and geographically biased in favour of wetlands and the South Island. As a result, 93% of all 128 morphotypes recorded in NZ occur in wetlands, 28% are restricted to the South Island, and diversity is greater at higher latitudes. Around 50% of morphotypes have a broad latitudinal distribution across the NZ mainland, whereas 15% have narrow latitudinal ranges. Future research should aim to broaden the geographical and ecological ranges. We predict that our list of NZ testate amoebae will expand substantially with future work, and that the latitudinal diversity gradient will be inverted. We also introduce an interactive, fully illustrated, online Lucid key for the rapid identification of NZ testate amoebae. As many morphospecies are cosmopolitan, this key provides a useful tool for testate amoebae identification in other parts of the world.

Vertical distribution of prokaryotes communities and predicted metabolic pathways in New Zealand wetlands, and potential for environmental DNA indicators of wetland condition.

Globally, wetlands are in decline due to anthropogenic modification and climate change. Knowledge about the spatial distribution of biodiversity and biological processes within wetlands provides essential baseline data for predicting and mitigating the effects of present and future environmental change on these critical ecosystems. To explore the potential for environmental DNA (eDNA) to provide such insights, we used 16S rRNA metabarcoding to characterise prokaryote communities and predict the distribution of prokaryote metabolic pathways in peats and sediments up to 4m below the surface across seven New Zealand wetlands. Our results reveal distinct vertical structuring of prokaryote communities and metabolic pathways in these wetlands. We also find evidence for differences in the relative abundance of certain metabolic pathways that may correspond to the degree of anthropogenic modification the wetlands have experienced. These patterns, specifically those for pathways related to aerobic respiration and the carbon cycle, can be explained predominantly by the expected effects of wetland drainage. Our study demonstrates that eDNA has the potential to be an important new tool for the assessment and monitoring of wetland health.

Response to Comment on "A global environmental crisis 42,000 years ago".

Our study on the exact timing and the potential climatic, environmental, and evolutionary consequences of the Laschamps Geomagnetic Excursion has generated the hypothesis that geomagnetism represents an unrecognized driver in environmental and evolutionary change. It is important for this hypothesis to be tested with new data, and encouragingly, none of the studies presented by Picin et al. undermine our model.

Response to Comment on "A global environmental crisis 42,000 years ago".

Our paper about the impacts of the Laschamps Geomagnetic Excursion 42,000 years ago has provoked considerable scientific and public interest, particularly in the so-called Adams Event associated with the initial transition of the magnetic poles. Although we welcome the opportunity to discuss our new ideas, Hawks' assertions of misrepresentation are especially disappointing given his limited examination of the material.