Biodiversity, Connectivity and Ecosystem Function Across the Clarion-Clipperton Zone: A Regional Synthesis for an Area Targeted for Nodule Mining

Macrofauna are an abundant and diverse component of abyssal benthic communities and are likely to be heavily impacted by polymetallic nodule mining in the Clarion-Clipperton Zone (CCZ). In 2012, the International Seabed Authority (ISA) used available benthic biodiversity data and environmental proxies to establish nine no-mining areas, called Areas of Particular Environmental Interest (APEIs) in the CCZ. The APEIs were intended as a representative system of protected areas to safeguard biodiversity and ecosystem function across the region from mining impacts. Since 2012, a number of research programs have collected additional ecological baseline data from the CCZ. We assemble and analyze macrofaunal biodiversity data sets from eight studies, focusing on three dominant taxa (Polychaeta, Tanaidacea, and Isopoda), and encompassing 477 box-core samples to address the following questions: (1) How do macrofaunal abundance, biodiversity, and community structure vary across the CCZ, and what are the potential ecological drivers? (2) How representative are APEIs of the nearest contractor areas? (3) How broadly do macrofaunal species range across the CCZ region? and (4) What scientific gaps hinder our understanding of macrofaunal biodiversity and biogeography in the CCZ? Our analyses led us to hypothesize that sampling efficiencies vary across macrofaunal data sets from the CCZ, making quantitative comparisons between studies challenging. Nonetheless, we found that macrofaunal abundance and diversity varied substantially across the CCZ, likely due in part to variations in particulate organic carbon (POC) flux and nodule abundance. Most macrofaunal species were collected only as singletons or doubletons, with additional species still accumulating rapidly at all sites, and with most collected species appearing to be new to science. Thus, macrofaunal diversity remains poorly sampled and described across the CCZ, especially within APEIs, where a total of nine box cores have been taken across three APEIs. Some common macrofaunal species ranged over 600–3000 km, while other locally abundant species were collected across ≤ 200 km. The vast majority of macrofaunal species are rare, have been collected only at single sites, and may have restricted ranges. Major impediments to understanding baseline conditions of macrofaunal biodiversity across the CCZ include: (1) limited taxonomic description and/or barcoding of the diverse macrofauna, (2) inadequate sampling in most of the CCZ, especially within APEIs, and (3) lack of consistent sampling protocols and efficiencies.

Environmental variables such as food supply, nodule abundance, sediment characteristics, and water chemistry may influence abyssal seafloor communities and ecosystem functions at scales from meters to thousands of kilometers. Thus, knowledge of environmental variables is necessary to understand drivers of organismal distributions and community structure, and for selection of proxies for regional variations in community structure, biodiversity, and ecosystem functions. In October 2019, the Deep CCZ Biodiversity Synthesis Workshop was conducted to (i) compile recent seafloor ecosystem data from the Clarion-Clipperton Zone (CCZ), (ii) synthesize patterns of seafloor biodiversity, ecosystem functions, and potential environmental drivers across the CCZ, and (iii) assess the representativity of no-mining areas (Areas of Particular Environmental Interest, APEIs) for subregions and areas in the CCZ targeted for polymetallic nodule mining. Here we provide a compilation and summary of water column and seafloor environmental data throughout the CCZ used in the Synthesis Workshop and in many of the papers in this special volume. Bottom-water variables were relatively homogenous throughout the region while nodule abundance, sediment characteristics, seafloor topography, and particulate organic carbon flux varied across CCZ subregions and between some individual subregions and their corresponding APEIs. This suggests that additional APEIs may be needed to protect the full range of habitats and biodiversity within the CCZ.

Extractive activities in the ocean are expanding into the vast, poorly studied deep sea, with the consequence that environmental management decisions must be made for data-poor seafloor regions. Habitat classification can support marine spatial planning and inform decision-making processes in such areas. We present a regional, top–down, broad-scale, seafloor-habitat classification for the Clarion-Clipperton Fracture Zone (CCZ), an area targeted for future polymetallic nodule mining in abyssal waters in the equatorial Pacific Ocean. Our classification uses non-hierarchical, k-medoids clustering to combine environmental correlates of faunal distributions in the region. The classification uses topographic variables, particulate organic carbon flux to the seafloor, and is the first to use nodule abundance as a habitat variable. Twenty-four habitat classes are identified, with large expanses of abyssal plain and smaller classes with varying topography, food supply, and substrata. We then assess habitat representativity of the current network of protected areas (called Areas of Particular Environmental Interest) in the CCZ. Several habitat classes with high nodule abundance are common in mining exploration claims, but currently receive little to no protection in APEIs. There are several large unmanaged areas containing high nodule abundance on the periphery of the CCZ, as well as smaller unmanaged areas within the central CCZ, that could be considered for protection from mining to improve habitat representativity and safeguard regional biodiversity.

Environmental DNA (eDNA) metabarcoding could facilitate rapid and comprehensive biotic surveys in the deep ocean, yet many aspects of the sources and distribution of eDNA in the deep sea are still poorly understood. In order to examine the influence of the water column on benthic eDNA surveys in regions targeted for deep-sea polymetallic nodule mining, we investigated the occurrence of pelagic eDNA across: (1) two different deep-sea habitat types, abyssal plains and seamounts, (2) benthic sample types, including nodules, sediment, and seawater within the benthic boundary layer (BBL), and (3) sediment depth horizons (0–2 and 3–5 cm). Little difference was observed between seamounts and the adjacent abyssal plains in the proportion of legacy pelagic eDNA sampled in the benthos, despite >1,000 m depth difference for these habitats. In terms of both reads and amplicon sequence variants (ASVs), pelagic eDNA was minimal within sediment and nodule samples (<2%), and is unlikely to affect benthic surveys that monitor resident organisms at the deep seafloor. However, pelagic eDNA was substantial within the BBL (up to 13% ASVs, 86% reads), derived both from the high-biomass upper ocean as well as deep pelagic residents. While most pelagic metazoan eDNA found in sediments and on nodules could be sourced from the epipelagic, protist legacy eDNA sampled on these substrates appeared to originate across a range of depths in the water column. Some evidence of eDNA degradation across a vertical sediment profile was observed for protists, with higher diversity in the 0–2 cm layer and a significantly lower proportion of legacy pelagic eDNA in deeper sediments (3–5 cm). Study-wide, our estimated metazoan sampling coverage ranged from 40 to 74%, despite relatively large sample size. Future deep-sea eDNA surveys should examine oceanographic influences on eDNA transport and residence times, consider habitat heterogeneity at a range of spatial scales in the abyss, and aim to process large amounts of material per sample (with replication) in order to increase the sampling coverage in these diverse deep ocean communities.