Unexpected high abyssal ophiuroid diversity in polymetallic nodule fields of the northeast Pacific Ocean and implications for conservation

Abstract

Abstract. The largest and commercially appealing mineral deposits can be found in the abyssal sea floor of the Clarion-Clipperton Zone (CCZ), a polymetallic nodule province, in the NE Pacific Ocean, where experimental mining is due to take place. In anticipation of deep-sea mining impacts, it has become essential to rapidly and accurately assess biodiversity. For this reason, ophiuroid material collected during eight scientific cruises from five exploration licence areas within CCZ, one area being protected from mining (APEI3, Area of Particular Environmental Interest) in the periphery of CCZ and the DISturbance and re-COLonisation (DISCOL) Experimental Area (DEA), in the SE Pacific Ocean, was examined. Specimens were genetically analysed using a fragment of the mitochondrial cytochrome c oxidase subunit I (COI). Maximum-likelihood and neighbour-joining trees were constructed, while four tree-based and distance-based methods of species delineation (automatic barcode gap discovery, ABGD; barcode index numbers, BINs; general mixed Yule–coalescent, GMYC; multi-rate Poisson tree process, mPTP) were employed to propose secondary species hypotheses (SSHs) within the ophiuroids collected. The species delimitation analyses' concordant results revealed the presence of 43 deep-sea brittle star SSHs, revealing an unexpectedly high diversity and showing that the most conspicuous invertebrates in abyssal plains have been so far considerably underestimated. The number of SSHs found in each area varied from five (IFREMER area) to 24 (BGR (Federal Institute for Geosciences and Natural Resources, Germany) area) while 13 SSHs were represented by singletons. None of the SSHs were found to be present in all seven areas while the majority of species (44.2 %) had a single-area presence (19 SSHs). The most common species were Ophioleucidae sp. (Species 29), Amphioplus daleus (Species 2) and Ophiosphalma glabrum (Species 3), present in all areas except APEI3. The biodiversity patterns could be mainly attributed to particulate organic carbon (POC) fluxes that could explain the highest species numbers found in BGR (German contractor area) and UKSRL (UK Seabed Resources Ltd, UK contractor area) areas. The five exploration contract areas belong to a mesotrophic province, while conversely the APEI3 is located in an oligotrophic province, which could explain the lowest diversity as well as very low similarity with the other six study areas. Based on these results the representativeness and the appropriateness of APEI3 to meet its purpose of preserving the biodiversity of the CCZ fauna are questioned. Finally, this study provides the foundation for biogeographic and functional analyses that will provide insight into the drivers of species diversity and its role in ecosystem function.

Adult life strategy affects distribution patterns in abyssal isopods – implications for conservation in Pacific nodule areas

“…3 and 6 (Amon et al, 2017;Martinez and Haeckel, 2015). Published data on a number of fauna groups based on these samples indicate little resemblance between APEI3 communities and the contractor areas studied (Vanreusel et al, 2016;Jakiel et al, 2019;Bonifacio et al, 2020;Christodoulou et al, 2020). Bonifacio et al (2020), for instance, investigated polychaete communities from the same sampling campaign as ours and found considerably lower densities, diversity, and similarity in species composition of APEI3 relative to contractor areas.…”

“…The expected number of species per area was inferred using extrapolation methods. Chao1 (Chao, 1994;Colwell and Coddington, 1994) uses the proportions of singletons and doubletons in the sample to estimate expected species richness, while ACE (Chazdon et al, 1998) is an abundance-based coverage estimator. For the analysis of beta (regional) diversity, the total multiple-site beta diversity β SOR was calculated using the modified Sørensen index (Sørensen, 1948; Balseaga and Orme, 2012), and β SOR was decomposed into its additive components "multiple-site species turnover" β SIM (Simpson Index, Simpson, 1943) and "multiple-site nestedness" β SNE using the R package betapart (Balseaga, 2010; Balseaga and Orme, 2012).…”

“…However, molecular studies have shown that morphologically similar, but genetically distinct (cryptic), species are common among deep-sea lineages, fundamentally changing our understandings of deep-sea species distributions (e.g., Vrijenhoek et al, 1994;Pfenninger and Schwenk, 2007;Raupach et al, 2007;Havermans et al, 2013;Brix et al, 2014Brix et al, , 2015Jennings et al, 2018Jennings et al, , 2019. Conversely, for some species there is morphological and genetic support for wide geographic distributions even across major topographic barriers (Brix et al, 2011;Menzel et al, 2011;Riehl and Kaiser, 2012;Janssen et al, 2015;Easton and Thistle, 2016;Bober et al, 2018;Brix et al, 2018, Christodoulou et al, 2020. However, biological data on dispersal distances of deep-sea species are still fragmentary due to the low sampling effort compared to the sheer area of deep-sea floor and the scant knowledge of species' taxonomy.…”

“…Environmental conditions have been shown to differ significantly in the APEI3 compared to areas in the CCZ, notably lower POC fluxes to the seafloor, lower total organic carbon (TOC) content, and lower clay content (Volz et al, 2018). These differences likely explain the observed community differences (Błażewicz et al, 2019;Bonifacio et al, 2020;Christodoulou et al, 2020). In a study of Icelandic isopods (Brix et al, 2018), TOC and mud content were shown to be the main explanatory variables for variation in the distribution of families with different lifestyles (e.g., in-vs. epi-vs. suprafauna) and thus likely differential use of food resources and substrate associations.…”

“…The prerequisite for these areas is that they are representative in terms of biodiversity and species composition and cover the entire spectrum of the habitat and community types available in the CCZ. However, data from APEIs, which have been very limited to date, bring into question their representativeness and suitability as a biodiversity reservoir (Vanreusel et al, 2016;Bonifacio et al, 2020;Christodoulou et al, 2020).…”