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Holman, L. E.

Publications and source records attributed to Holman, L. E..

10 recordsLinked to original sources

Ancient environmental DNA reveals the distinct fingerprints of whaling and climate change on Antarctic marine biodiversity

The Southern Ocean is a disproportionately large contributor to Earth system processes, playing a crucial role in the global transport of carbon, oxygen and heat. It also hosts enormous seasonal biological productivity that supports diverse endemic marine biodiversity. Industrial whaling in the first half of the 20th century and recent human-driven climate change have both profoundly altered Antarctic ecosystems, but ecological surveys of these impacts are limited to well-known taxa in the short period since monitoring began. Here, we analysed five sediment records to reconstruct more than two centuries of ecosystem change across the Western Antarctic Peninsula, spanning periods before and during major human impacts. Environmental DNA metabarcoding of these records revealed substantial biodiversity shifts, with change accelerating in recent decades. We find a significant role for both climate change and whaling in restructuring communities, identifying unique variance in whole-community change explained by each driver. Moreover, we find a negative association between whaling and metazoan families which feed from the water column, suggesting that pre-whaling ecosystems had greater pelagic productivity. Overall, our results reveal baseline Antarctic biodiversity from long before observational records and identify a distinct fingerprint of human drivers in this fragile, rapidly changing ecosystem.

ecology↗

Getting to the core of the matter: Assessing the role of replication in sedimentary DNA metabarcoding

Replication is central to most experimental and sampling designs, increasing inferential power and capturing fine-scale data heterogeneity. However, its importance remains poorly evaluated in some ecological and evolutionary settings. This is the case of metabarcoding studies using DNA recovered from sedimentary archives, in which biological signals may integrate ecological information through depositional and burial processes, and are often inferred from a single sediment core per site. Here, we evaluated the effect of different types of replication using sedimentary DNA (sedaDNA) metabarcoding data from two genetic markers (mitochondrial COI and nuclear 18S), under a nested sampling design. The design included three intertidal sites, three spatially separated sediment cores per site (biological replicates), two sediment depth horizons per core, and eight PCR (technical) replicates per sediment sample. Variance partitioning showed that site identity and sediment age group together explained >70% of the variation in beta diversity, indicating that among-site spatial variation and stratigraphic variation were the dominant drivers of community composition. In contrast, variation among different cores within sites was small and non-significant (<5%). Among PCR replicates from the same sediment sample, richness varied substantially, whereas Shannon diversity was more consistent. Despite this variability, differences in community composition among technical replicates remained smaller than among biological replicates and site identity, indicating limited influence on broader ecological patterns. Community composition was highly similar among replicate cores within sites, consistent with stratigraphic coherence. These results indicate limited within-site heterogeneity and suggest that, under stratigraphically coherent conditions, increasing biological replication may yield limited additional information, whereas enhancing technical replication and stratigraphic resolution can improve ecological inference from sedaDNA metabarcoding datasets.

ecology↗

Metabarcoding replicate detection frequency tracks ddPCR copy number for cod and herring eDNA in ancient marine sediments

O_LIDetecting environmental DNA (eDNA) from rare or low-abundance aquatic species remains a major challenge, particularly when it is highly degraded, present at low concentrations, and dominated by DNA from non-target taxa. These challenges are further amplified in sedimentary ancient DNA (sedaDNA) studies, where thousands of years can degrade eDNA further, making the detection and quantitative interpretation of weak biological signals difficult. C_LIO_LIMetabarcoding is commonly used to produce high-throughput community-level data from eDNA but is inherently compositional and influenced by amplification biases. Nonetheless, metabarcoding read abundance or PCR replicate detection frequency are increasingly used as proxies for relative DNA concentration, but their quantitative interpretation has rarely been evaluated against independent measures of absolute DNA abundance. C_LIO_LIWe used droplet digital PCR (ddPCR) to quantify mitochondrial DNA from Atlantic cod (Gadus morhua) and Atlantic herring (Clupea harengus) in 136 ancient eDNA extracts from Icelandic marine sediment cores spanning the last three millennia. We compared ddPCR copy number estimates with metabarcoding (18S) derived relative abundance and detection frequency, and evaluated whether temporal DNA trends corresponded with proxy reconstructed sea surface temperature (SST) variability. C_LIO_LIWe found that ddPCR-measured fish sedaDNA abundance was positively correlated with the proportion of metabarcoding PCR replicates for both Atlantic cod and Atlantic herring. Moreover, temporal trends in Atlantic herring DNA abundance were consistent with proxy reconstructed SST variability, supporting the ecological relevance of the molecular signal. C_LIO_LIOverall, our results show that ddPCR-derived DNA concentrations and metabarcoding PCR replicate detection frequency capture consistent patterns in low-abundance fish sedaDNA from marine sediments. The observed agreement between approaches supports the use of PCR replicate detection frequency as a semi-quantitative proxy for low-abundance sedaDNA. C_LI

genetics↗

Metabarcoding of sedimentary ancient DNA reveals centuries of species turnover and introductions of non-indigenous species in a highly urbanised estuary

Understanding how anthropogenic pressures shape ecosystems over time is crucial for managing both biodiversity and bioinvasion risk. Despite recent research efforts focussing on temporal community changes as a result of human impacts, little is known about such changes over periods exceeding a century. Here, we reconstructed long-term community changes and non-indigenous species (NIS) dynamics by using sedimentary ancient DNA (sedaDNA) metabarcoding and geochemical analysis of sediment cores samples collected from a temperate estuary (Southampton Water, southern British Isles) subject to significant human impacts for centuries. We detected 73 species of Metazoa and Plantae and classified them by their status (native, cryptogenic and NIS). Our results revealed sporadic detection of NIS (both failed and continuously successful NIS introductions) throughout the entire sedimentary record. Notably, some NIS were detected as early as the 18th century, indicating the presence of NIS introductions in pre-industrial times. We found a continuous overall decline in native species richness since the 19th century. In addition, we found distinct peaks in copper and zinc concentrations reflecting recent periods of intensified industrial and port activity, highlighting the role of human activities in shaping biodiversity patterns and NIS dynamics. Our findings demonstrate how metabarcoding of sedaDNA archives can reveal trends in the distribution of NIS and wider biodiversity over centuries. The integrated approach used here provides new insights into biodiversity changes through time, unravels key information for biodiversity conservation management and biosecurity policy, and shows the potential that sedaDNA metabarcoding has for investigating intrinsic attributes of NIS introductions.

ecology↗

Ancient environmental DNA indicates limited human impact on marine biodiversity in pre-industrial Iceland

Human activities are affecting marine biodiversity globally by accelerating extinction rates, altering ecosystem conditions, and changing community structures. These changes can only be understood through establishing the ecosystem state prior to significant anthropogenic impact, and by disentangling the anthropogenic effect from natural climatic changes. Here, we reconstruct marine biodiversity in Iceland across three millennia (1315 BCE-1785 CE), encompassing periods of climatic fluctuation and human settlement, to explore the comparative effect of natural and anthropogenic forces on marine biodiversity. We performed 18S metabarcoding of ancient environmental DNA from two sediment cores collected from northern Icelandic shelf seas, integrating local climatic records, population estimates and zooarchaeological remains from published sources to estimate the influence of climatic and anthropogenic impacts. Against the backdrop of increasing human populations and marine exploitation, we observe no large-scale taxonomic shifts or anthropogenic biodiversity changes across the period. In contrast, we found a positive correlation between herring (Clupea harengus) detection rates and proxy-reconstructed sea surface temperature, suggesting a role for climate in shaping marine biodiversity. Overall, our data suggest that despite impacts on terrestrial ecosystems and the development of a substantial export fishery across the study period, Icelandic society may have had a limited effect on marine biodiversity.

ecology↗

Fine-scale oceanographic processes shape marine biodiversity patterns in the Galapagos Islands

Uncovering the drivers that shape biodiversity patterns is critical to understand ecological and evolutionary dynamics. Despite evidence that biodiversity composition is influenced by processes at different spatial scales, little is known about the role of fine-scale oceanographic processes on the structure of marine communities. This is particularly important in biodiversity hotspot regions, where small changes in environmental conditions may lead to substantial changes in species composition. We combined ocean modelling and 12S environmental DNA (eDNA) metabarcoding, targeting teleost and elasmobranch species, to explore if oceanographic processes influenced biogeographic patterns around the biodiverse Galapagos Islands. We first detected significant differences in eDNA-measured community structure across the archipelagos diverse seascape. We found no significant relationship between Lagrangian particle tracking metrics and nektonic biodiversity, and thus developed a novel metric to measure the cumulative seawater flow resistance between pairs of geographic sites. This metric explained a significant proportion of variation in eDNA-measured beta dissimilarity between sites, comparable in influence to important abiotic drivers, such as temperature and geographic distance between sites. Cumulatively, our results indicate that marine communities are particularly sensitive to changes in local current systems, and suggest that fine-scale oceanographic processes may have an underappreciated role in structuring marine communities globally.

ecology↗

Early Pastoralism in Central European Forests: Insights from Ancient Environmental Genomics

Central European forests have been shaped by complex human interactions throughout the Holocene, with significant changes following the introduction of domesticated animals in the Neolithic ([~]7.5 - 6.0 kyr BP). However, understanding early pastoral practices and their impact on forests is limited by methods for detecting animal movement across past landscapes. Here we examine ancient sedimentary DNA (sedaDNA) preserved at the Velky Mamu[t]ak rock shelter, in northern Bohemia (Czech Republic), which has been a forested enclave since the early Holocene. We find that domesticated animals, their associated microbiomes, and plants potentially gathered for fodder, have clear representation by the Late Neolithic, around 6.0 kyr BP, and persist throughout the Bronze Age into recent times. We identify a change in dominant grazing species from sheep to pigs in the Bronze Age ([~]4.1 - 3.0 kyr BP) and interpret the impact this had in the mid-Holocene retrogressions that still define the structure of Central European forests today. This study highlights the ability of ancient metagenomics to bridge archaeological and paleoecological methods and provide an enhanced perspective on the roots of the Anthropocene.

genomics↗

Managing human mediated range shifts: understanding spatial, temporal and genetic variation in marine non- native species

The use of molecular methods to manage natural resources is increasingly common. However, DNA-based methods are seldom used to understand the spatial and temporal dynamics of species range shifts. This is important when managing range-shifting species such as non-native species (NNS), which can have negative impacts on biotic communities. Here we investigated the range-shifting NNS Ciona robusta, Clavelina lepadiformis, Microcosmus squamiger and Styela plicata using a combined methodological approach. We first conducted non-molecular biodiversity surveys for these NSS along the South African coastline, and compared the results with historical surveys. We detected no consistent change in range size across species, with some displaying range stability and others showing range shifts. We then sequenced a section of cytochrome c oxidase subunit I (COI) from tissue samples and found genetic differences along the coastline but no change over recent times. Finally, we found that environmental DNA metabarcoding data showed broad congruence with both the non-molecular biodiversity and the COI datasets, but failed to capture complete incidence of all NSS. Overall, we demonstrated how a combined methodological approach can effectively detect spatial and temporal variation in genetic composition and range size, which is key for managing biodiversity changes of both threatened and NSS.

ecology↗

Consistent marine biogeographic boundaries across the tree of life despite centuries of human impacts

Over millennia, ecological and evolutionary mechanisms have shaped macroecological distributions across the tree of life. Research describing patterns of regional and global biogeography has traditionally focussed on the study of conspicuous species. Consequently, there is limited understanding of cross-phyla biogeographic structuring, and an escalating need to understand the macroecology of both microscopic and macroscopic organisms. Here we used environmental DNA (eDNA) metabarcoding to explore the biodiversity of marine metazoans, micro-eukaryotes and prokaryotes along an extensive and highly heterogeneous coastline. Our results showed remarkably consistent biogeographic structure across the kingdoms of life, which were underpinned by environmental and anthropogenic influence. Additionally, metazoan communities displayed biographic patterns that suggest regional biotic homogenisation of conspicuous species. Against the backdrop of global pervasive anthropogenic environmental change, our work highlights the importance of considering multiple domains of life to understand the maintenance and drivers of marine biodiversity across broad taxonomic, ecological and geographical scales.

ecology↗

The detection of novel and resident marine non-indigenous species using environmental DNA metabarcoding of seawater and sediment

Environmental DNA (eDNA) surveys are increasingly being used for biodiversity monitoring, principally because they are sensitive and can provide high resolution community composition data. Despite considerable progress in recent years, eDNA studies examining how different environmental sample types can affect species detectability remain rare. Comparisons of environmental samples are especially important for providing best practice guidance on early detection and subsequent mitigation of non-indigenous species. Here we used eDNA metabarcoding of COI (cytochrome c oxidase subunit I) and 18S (nuclear small subunit ribosomal DNA) genes to compare community composition between sediment and water samples in artificial coastal sites across the United Kingdom. We first detected markedly different communities and a consistently greater number of distinct operational taxonomic units in sediment compared to water. We then compared our eDNA datasets with previously published rapid assessment biodiversity surveys and found excellent concordance among the different survey techniques. Finally, our eDNA surveys detected many non-indigenous species, including several newly introduced species, highlighting the utility of eDNA metabarcoding for both early detection and temporal / spatial monitoring of non-indigenous species. We conclude that careful consideration on environmental sample type is needed when conducting eDNA surveys, especially for studies assessing community change.

molecular biology↗