Diversity of deep-sea scale-worms in the CCFZ: the most oligotrophic site is also the most diverse?
The Clarion-Clipperton Fracture Zone (CCFZ) harbours the largest field of polymetallic nodules in the world potentially holding 34 billion metric tons of manganese that could represent at least 25 trillion USD. A single mining operation has potential to directly impact approximately 200 km2 of the seabed per year (Volkmann and Lehnen, 2018). Yet, the biodiversity and functioning of the bentho-demersal ecosystem in the CCFZ remain poorly understood.
On a regional scale, recent studies indicate a high species diversity in a food-poor environment with the northward and westward gradients of decreasing primary productivity being strongly important driving variations in macrofaunal community structure (Bonifácio et al., 2020). Understanding the ecology of benthic communities in the CCFZ is however still impaired by the incomplete diversity assessment. For polychaetes, a species-rich group at abyssal depths representing often more than 50% of total macrofaunal abundances, for instance, the incomplete species inventories can be attributed to undersampling, species lumping and sampling inaccuracy (Bonifácio et al., 2020).
This study examines the Polynoidae, a diverse family of mobile polychaetes. Sampling with an box-corer, epibenthic sledge and an ROV was performed during the cruise SO239 within the eastern CCFZ. Five areas under the influence of a sea surface productivity gradient were visited. Specimens were identified using morphology and DNA to provide a more comprehensive account of polynoid diversity (taxonomic and phylogenetic) within the CCFZ. Additionally, we aim to further test hypotheses regarding the drivers of species turnover in the CCFZ. Based on quantitative box-core sampling, Bonifácio et al. (2020) showed a high species turnover among infaunal polychaete assemblages across the eastern CCFZ, attributing it to variations in trophic inputs and barriers to dispersal. In particular, the Clarion fracture was hypothesized to limit dispersal between the APEI no. 3 to the north and the core of the CCFZ to the south. Dispersal ability has also been advocated as a driver of differential distribution patterns between polychaete and isopods as well as among isopod families in the CCFZ (Janssen et al., 2019; Brix et al., 2020). By focusing on polynoids, we aspired to test whether mobile epifaunal polychaetes would show lower species turnover and greater species ranges than the more sedentary infaunal polychaete assemblages.
A total of 275 specimens accounted for 95 species belonging to the subfamilies Eulagiscinae, Polynoinae, and Macellicephalinae. Macellicephalinae was the most abundant and diverse group with 259 specimens belonging to 92 species. Within Macellicephalinae, a clade called Anantennata was also abundant and surprisingly very diverse with 65 specimens belonging to 42 species. The distribution of species indicated that 74 species were restricted to only one area with 58 species represented by a single specimen.
Variations in epibenthic polynoid assemblages across the CCFZ showed similarities with other faunal groups in that species turnover covaries with POC flux and thus food supply. A major difference from the infaunal pattern (Bonifácio et al., 2020) is that species richness was similar to or even higher at APEI no. 3, the most oligotrophic site located north of the Clarion fracture, in comparison to other exploration mining areas to the south. This unexpected pattern may result from sampling bias, but could also be due to: (i) higher shear strength of APEI no. 3 sediments making them less hospitable to infauna to the benefit of epifauna and (ii) evolutionary adaptations of macellicephalins towards a benthopelagic life strategy under oligotrophic conditions in the deep sea. The difference in species composition and community structure at APEI no. 3 brings into question the key principles of the APEI network, as this area appears not representative of the biogeography and habitat of the broader region (Wedding et al., 2013). However, such a conclusion is tentative, given the limited sampling within this APEI.
The polynoids in the CCFZ are highly diverse, with most diversity confined to the subfamily Macellicephalinae, which has particularly radiated in the deep sea. Our results (including 16 named species from Bonifácio and Menot, 2018) indicate the presence of at least 92 Macellicephalinae species with 42 being Anantennata in the eastern CCFZ, in the north-east Pacific. Macellicephalins are thus polychaetes thriving in cold and dark environments that have successfully colonised deep-sea habitats such as chemosynthetic ecosystems (hydrothermal vents and cold seeps; Pettibone, 1983; Chevaldonné et al., 1998; Hatch et al., 2020), trenches (Levenstein, 1971; Pettibone, 1976), manganese nodules (Bonifácio and Menot, 2018), and the deep Antarctic shelf (Neal et al., 2018a,b) but also analogous shallow water habitats such as submarine caves (Pettibone, 1985b).
Pettibone (1985a) described Natopolynoe kensmithi Pettibone, 1985a being abundant not only on the seafloor but also swimming up to 10 m above it.
The swimming behavior observed in Macellicephalinae was likely the key to exploitation of new trophic resources, unavailable to worms with a benthic lifestyle. This behavior may have enabled macellicephalins to explore benthic and pelagic niches in the deep sea, particularly within hadal depths where they are the most characteristic and diverse polychaetes (Paterson et al., 2009; Jamieson, 2015; see below the video produced by the Monterey Bay Aquarium Research Institute).
This research received funding from the JPI Oceans pilot action ‘Ecological Aspects of Deep-Sea Mining’, the European Union Seventh Framework Program (FP7/2007–2013) under the MIDAS project and REMIMA.
Read more in:
Bonifácio, P., Neal, L., & Menot, L. (2021). Diversity of Deep-Sea Scale-Worms (Annelida, Polynoidae) in the Clarion-Clipperton Fracture Zone. Frontiers in Marine Science, 8, 656899. https://doi.org/10.3389/fmars.2021.656899