Changes in abundance and community structure of nematodes from the abyssal polymetallic nodule field, Tropical Northeast Pacific
Introduction
Polymetallic nodules cover millions of square kilometres of the deep-sea bottom and are considered a potential source of commercially important metals including Mn, Ni, Cu, and Co. Dense deposits of polymetallic nodules suitable for commercial mining have been found in the Pacific, Atlantic, and Indian Oceans (Seibold and Berger, 1993, Cronan, 2001, Baker et al., 2001, Wedding et al., 2015; https://www.isa.org.jm/mineral-resources/55). Currently, 14 national and international entities have concluded contracts with the International Seabed Authority for exploration in the Clarion-Clipperton Fracture Zone (CCFZ) in the NE sub-equatorial Pacific, and in the Central Indian Ocean Basin (CIOB). The nodules occur as more or less spherical concretions and are concentrated in the superficial 5–10 cm sediment layer only. It is expected that commercial mining will affect the upper sediment layers on many thousands of square kilometres of the sea bed (Glover and Smith, 2003). Consequently, it is inevitable that benthic organisms, which predominately inhabit the uppermost sediment layer and use nodules as a hard substratum, will be disturbed or even destroyed during mining activities (Glover and Smith, 2003, Ramirez-Llodra et al., 2011).
The free-living nematodes, the most abundant component of metazoan meiobenthos, are the most suitable candidates for assessing mining impacts on benthic communities because of their high density and diversity in the deep-sea. To date, studies have been published on free-living nematode communities inhabiting nodule fields in the Peru Basin in the SE Pacific (Bussau, 1993, Bussau et al., 1995, Thiel et al., 1993), the CCFZ (Snider et al., 1984, Spiess et al., 1987, Renaud-Mornant and Gourbault, 1990, Radziejewska et al., 2001a, Radziejewska et al., 2001b, Lambshead et al., 2003, Miljutina et al., 2010, Miljutin et al., 2011) and the CIOB (Singh et al., 2014). Also, there has been a review on the Pacific studies by Radziejewska (2014).
It has been shown that polymetallic nodules are themselves a habitat for specific nematode assemblages inhabiting the nodule surface and the interstitial space inside their crevices and internal cavities (Thiel et al., 1993). In addition, rates of recolonisation and recovery of nematode communities in deep-sea nodule fields following benthic disturbance experiments may vary widely (from several years to at least several decades) in different regions (Borowski, 2001, Vopel and Thiel, 2001, Radziejewska et al., 2001a, Radziejewska et al., 2001b, Radziejewska, 2002, Miljutin et al., 2011).
In terms of nematode communities, one of the most studied nodule sites is the French license area in the CCFZ. A pilot study at this site was undertaken during cruise NIXO-47 (RV “Jean Charcot”, IFREMER, France) in May 1986 to investigate undisturbed nodule-bearing and neighbouring nodule-free sites. It reported average total nematode densities of 65 and 69 ind/10 cm2 for nodule-bearing and nodule-free locations, respectively (Renaud-Mornant and Gourbault, 1990). Monhysteridae (among families), and Syringolaimus sp. and Molgolaimus sp. were the most abundant taxa (Renaud-Mornant and Gourbault, 1990).
Later, in May 2004 (i.e. the same season but 18 years later), samples were collected during the NODINAUT cruise (RV “L’Atalante”, IFREMER, France) in an undisturbed area ca. 90 km away from the original study site. Differences in the nematode community were recorded: average total nematode densities were 69 and 137 ind/10 cm2 for nodule-bearing and nodule-free locations, respectively, and the genera Thalassomonhystera, Acantholaimus, and Theristus were most abundant (Miljutina et al., 2010).
In 2012, another cruise (BIONOD, RV “L’Atalante”) was carried out in the French license area in the CCFZ. The samples were again taken from the same undisturbed locality as in the NODINAUT cruise, continuing the study of changes in nematode density and community structure.
The goal of the present study was to characterise the nematode community structure in the CCFZ abyssal plain in two different sampling periods, characterised by different levels of the primary production in the upper layers of the water column in 2004 and 2012, in order to provide a reference for future studies aimed at assessing the effects of deep-sea mining on abyssal communities.
Section snippets
Study area
The study area is located in the easternmost part of the French licence area in the CCFZ (Fig. 1A), at an average depth of about 5000 m and ca. 2200 km off the North American continental coast. This region is characterized by an asymmetrical succession of North–South oriented crests and valleys, between 100 and 300 m high and spaced 5 to 10 km apart. The seabed is covered by, on average, around 12 kg/m2 of polymetallic nodules varying from 2 cm to >15 cm in diameter (Du Castel, 1985, Hoffert, 2008).
Surface conditions
The time series of surface chlorophyll concentration within the 500 km-radius catchment area displayed clear seasonal and interannual variations (Fig. 2). Surface chlorophyll in the months prior to the 2004 cruise was lower than prior to the 2012 cruise, and were below (2004) and above (2012) typical seasonal values, respectively. Chlorophyll concentrations in low seasons (from June to October) were relatively constant across the whole time period, varying from 0.7 to 0.10 mg m−3 (on average),
Potential effects of methodology on nematode density and community structure
According to the test for possible effects of different sieve mesh sizes used in 2004 and 2012, the use of the 32 µm mesh sieve in 2012 may have increased the recorded total nematode abundance relative to the 40 µm mesh sieve. However, after removing the 20th percentile of small individuals from the 2012 dataset, the difference in the total density between the two sampling occasions was still significant for the nodule-free site.
The use of the 32 µm mesh sieve in 2012 potentially raised the
Acknowledgements
The authors thank the crew of RV “L’Atalante” and the chief-scientist of the BIONOD cruise Dr. Lenaick Menot (IFREMER, Brest, France) for their skilled help in sampling the material, the technical assistant Lena Albers (DZMB, Wilhelmshaven, Germany) for her help with the treatment of samples, and Dr. Carsten Ruehlemann (BGR, Hannover, Germany) for his valuable information on environmental conditions in the studied area. The authors also express their gratitude to Dr. Natalie Barnes for her
References (74)
Physically disturbed deep-sea macrofauna in the Peru Basin, southeast Pacific, revisited 7 years after the experimental impact
Deep-Sea Res. II
(2001)Manganese nodules
- et al.
Temporal change in deep-sea benthic ecosystems: a review of the evidence from recent time-series studies
Adv. Mar. Biol.
(2010) - et al.
Temporal changes (1989–1999) in deep-sea metazoan meiofaunal assemblages on the Porcupine Abyssal Plain, NE Atlantic
Deep-Sea Res. II
(2010) - et al.
A benthic storm in northeastern tropical Pacific over the fields of manganese nodules
Deep-Sea Res.
(1994) - et al.
Influence of mesh size and core penetration on estimates of deep-sea nematode abundance, biomass, and diversity
Deep-Sea Res. I
(2010) - et al.
Deep-sea nematode assemblage has not recovered 26 years after experimental mining of polymetallic nodules (Clarion-Clipperton Fracture Zone, Tropical Eastern Pacific)
Deep-Sea Res. I
(2011) - et al.
Fish-farm impact on metazoan meiofauna in the Mediterranean Sea: analysis of regional vs. habitat effects
Mar. Environ. Res.
(2010) - et al.
Primary production in the eastern tropical Pacific: a review
Prog. Oceanogr.
(2006) - et al.
Evaluation of abyssal meiobenthos in the eastern central Pacific (Clarion-Clipperton fracture zone)
Prog. Oceanogr.
(1990)
Comparison of the nematode fauna from the Weddel Sea Abyssal Plain with two North Atlantic abyssal sites
Deep-Sea Res. II
Local variations on distribution and composition of ferromanganese nodules in the Clarion-Clipperton Nodule Province
Mar. Geol.
The composition and distribution of meiofauna and nanobiota in central North Pacific deep-sea area
Deep-Sea Res.
Manganese nodule crevice fauna
Deep-Sea Res. I
The metazoan meiobenthos along the continental slope of the Goban Spur (NE Atlantic)
J. Sea Res.
Meiobenthos of the central Arctic Ocean with special emphasis on the nematode community structure
Deep-Sea Res. I
Abyssal nematode assemblages in physically disturbed and adjacent sites of the eastern equatorial Pacific
Deep-Sea Res. II
PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods
An environmental perspective
Accumulation and fate of phytodetritus on the sea floor
Oceanogr. Mar. Biol. Ann. Rev.
Sampler bias in the quantitative study of deep-sea meiobenthos
Mar. Ecol. Prog. Ser.
Taxonomische und ökologische Untersuchungen an Nematoden des Peru-Beckens
Evaluation of abyssal metazoan meiofauna from a manganese nodule area of the Eastern South Pacific
Vie Et. Milieu
Non-parametric multivariate analysis of changes in community structure
Aust. J. Ecol.
PRIMER v6*: User Manual/Tutorial
Deep-Seabed Polymetallic Nodule Exploration: Development of Environmental Guidelines
[On the bottom currents in areas of Fe-Mn nodules]
Doklady Ak. Nauk. SSSR
Etablissement d′une carte géologique au 1/20 000 d′’un domaine océanique profond dans une zone riche en nodules polymétalliques du Pacifique Nord (zone Clarion-Clipperton). Thèse de doctorat
Estuarine nematodes as indicators of organic pollution; an example from the Ems Estuary (the Netherlands)
Neth. J. Aquat. Ecol.
Deep-sea meiobenthic communities underneath the marginal ice zone off Eastern Greenland
Polar Biol.
Meiobenthology – The Microscopic Motile Fauna of Aquatic Sediments
The deep-sea floor ecosystem: current status and prospects of anthropogenic change by the year 2025
Environ. Conserv.
PAST: Paleontological Statistics Software Package for Education and Data Analysis
Palaeontol. Electron.
The northeastern Pacific abyssal plain
Along-slope oceanographic processes and sedimentary products around the Iberian margin
Geo-Mar. Lett.
Les nodules polymétalliques dans les grands fonds océaniques. Une extraordinaire aventure minière et scientifique sous-marine
Société Géologique De. Fr. Vuibert
Geologic effects of ocean bottom-currents: western north Atlantic
Cited by (15)
Community structure of deep-sea benthic metazoan meiofauna in the polymetallic nodule fields in the eastern Clarion-Clipperton Fracture Zone, Pacific Ocean
2022, Deep-Sea Research Part I: Oceanographic Research PapersCitation Excerpt :Sediment plumes arising from the mining process will further result in a large-scale smothering of habitats (Rolinski et al., 2001; reviewed in Allsopp et al., 2013). Previous disturbance studies, although conducted on a small spatial scale compared to the foreseeable extent of seabed mining, have demonstrated lasting changes in the abundance and composition of fauna, and exacerbated by long recovery times especially for sessile taxa reliant on hard-substrata (Bluhm et al., 1995; Bluhm, 2001; Miljutin et al., 2011, 2015; Stratmann et al., 2018). Disturbance tracks were also still visible after many years (e.g., after 26 years in Miljutin et al., 2011).
Assessment of scientific gaps related to the effective environmental management of deep-seabed mining
2022, Marine PolicyCitation Excerpt :The drivers and scales (e.g., intra-annual, inter-annual, decadal) of temporal variability in nodule regions are also poorly understood. Recent CCZ studies have reported changes to meroplankton (larvae of benthic fauna), nematode community structure, and vertical flux on timescales of weeks to months, likely associated with differences in primary production [77,78]. Meiofauna appear to have limited intra-annual variability in composition, standing stock, and diversity within single contract areas in the CCZ [79].
A local scale analysis of manganese nodules influence on the Clarion-Clipperton Fracture Zone macrobenthos
2021, Deep-Sea Research Part I: Oceanographic Research PapersCitation Excerpt :To have a proxy for surface water productivity we extracted VGPM (Vertically Generalized Production Model) based on MODIS satellite data for January 2015–June 2017 (1080 x 2160 files) and estimated net primary productivity (NPP, Fig. 3; Behrenfeld and Falkowski, 1997). In order to account for time-lagged responses in faunal and abiotic characteristics (Miljutin et al., 2015), we set the start of the estimation period to nine months prior to the GSRNOD15A sampling campaign. Monthly-averaged NPP values were downloaded as HDF files (http://www.science.oregonstate.edu/ocean.productivity/index.php), converted to geotiff (using SeaDAS) and finally perfected in QGIS v2.18 when a convex hull was drawn around the positions of all biological deployments and the Zonal statistics tool was used to compute monthly averaged NPP.
Abyssal macrofaunal community structure in the polymetallic nodule exploration area at the easternmost region of the Clarion-Clipperton Fracture Zone, Pacific Ocean
2020, Deep-Sea Research Part I: Oceanographic Research PapersCitation Excerpt :As the POC flux is especially essential for the food-deprived abyssal community, the organisms living on the abyssal seafloor are expected to be influenced greatly by ecological processes some 4–5 km away at the sea surface (Smith and Demopoulos, 2003). A number of previous exploration projects (e.g., NIXO 47, DOMES, Kaplan, ECHO-1, PRA), and survey cruises by GSR (Belgium), KIOST (South Korea), COMRA (China) and IFREMER (France), have described the community structure of benthic infauna (mostly meiofauna) at the CCFZ (Hecker and Paul, 1979; Wilson, 1987, 1992; Wilson and Hessler, 1987; Renaud-Mornant and Gourbault, 1990; Kim et al., 2000; Gao et al., 2002; Glover et al., 2002; Lambshead et al., 2003; Choi et al., 2004; Smith et al., 2008; Mahatma, 2009; Miljutina et al., 2010; Wang et al., 2013; Miljutin et al., 2015; De Smet et al., 2017; Pape et al., 2017; Min et al., 2018; Yu et al., 2018). Although the taxonomic resolution of the data presented by these studies was uneven, and faunal abundance varied between different sites across the CCFZ, they arrived at similar conclusions: 1) the biodiversity of the deep-sea benthos in the CCFZ is very high; and 2) only a small percentage of the fauna was previously described, indicating that many are new to science.
Bathymetric patterns in standing stock and diversity of deep-sea nematodes at the long-term ecological research observatory HAUSGARTEN (Fram Strait)
2017, Journal of Marine SystemsCitation Excerpt :Although deep-sea nematode ecology has been a subject of increasing interest during the last decade (Fonseca et al., 2010; Guilini et al., 2013; Lins et al., 2016), most of the previous studies that included bathymetric distribution patterns and environmental drivers have focused on continental slopes (e.g. Fonseca and Soltwedel, 2007; Leduc et al., 2012b; Danovaro et al., 2013; for a review see Soltwedel, 2000). Only a minority of investigations has extended such studies to deeper waters (Gambi et al., 2003; Vanhove et al., 2004; Guilini et al., 2013) or particularly focused on abyssal depths (Vanreusel et al., 1995; Vopel and Thiel, 2001; Miljutin et al., 2015; Vanreusel et al., 2010). Furthermore, owing to the logistic and technical difficulties involved in sampling deep-sea Arctic regions, our knowledge of the Arctic ecosystems is still limited.