Seamounts are submarine mountains that rise at least 1,000 m above the surrounding seafloor (Pitcher et al., 2007). Seamounts are common seafloor features, with tens to hundreds of thousands of seamounts estimated globally (Kim and Wessel, 2011; Yesson et al., 2011). Seamounts are still understudied habitats, but current data suggest that seamounts with summits shallower than 3000 m are often characterized by rich benthic and demersal megafaunal communities with high abundance, high biomass, and high diversity (Pitcher et al., 2007; Morato et al., 2010; Schlacher et al., 2010). The vast majority of these features are small, deep seamounts, but these are also the least studied and least understood class of seamounts (Wessel, 2001; Kim and Wessel, 2011).

The Clarion-Clipperton Zone (CCZ), a large region rich in polymetallic nodules in the eastern equatorial Pacific between Hawaii and Mexico, is currently being considered for deep seabed nodule mining. The International Seabed Authority (ISA) is responsible for environmental management in the CCZ and to that end has established nine, 400 km × 400 km no-mining zones called Areas of Particular Environmental Interest (APEIs; Wedding et al., 2013). The APEIs were designing as a representative system of protected areas to cover the biophysical gradients in productivity, nodule cover, and depth across the CCZ, as well as to protect the range of seafloor habitat types in the CCZ, including abyssal hills and seamounts (Wedding et al., 2013). The CCZ hosts approximately 221 seamounts, whose average summit depth is 2850 m below sea-level (data extracted from Yesson et al., 2011; Figure 1). It has recently been hypothesized that these seamounts, which will be spared from direct mining activities due to the rugosity and complexity of their terrain, may provide refugia for many species from the abyssal plain displaced or disturbed by mining and thus may provide source populations for recolonization of mined areas (Cuvelier et al., 2020). A prediction of this hypothesis is that seamounts and nearby abyssal plains share a substantial proportion of their fauna. Thus far, this hypothesis, referred to throughout this manuscript as the Seamount Refuge Hypothesis (SRH), has been evaluated and rejected for benthic megafauna (excluding highly mobile groups like fishes and crustaceans) in the eastern CCZ, where only 10% of fauna were observed on both seamounts and plains (Cuvelier et al., 2020). In addition, a recent study using a multi-gene environmental DNA metabarcoding approach, suggests substantial differences in metazoan communities with limited taxonomic overlap between seamounts and plains in the western CCZ (Laroche et al., 2020). However, an evaluation specific to fishes and other mobile top predators and scavengers is still lacking.

Knowledge of the distribution, ecology, and behavior of top predators is crucial to establish environmental baselines and conduct ecosystem-based management (Estes et al., 2011; Wedding et al., 2015, 2013). Even at low densities, predators can exert top-down control on prey populations, thereby controlling prey abundance, biomass, and diversity, and influencing habitat use/choice and behavior of prey (Myers et al., 2007; Polovina et al., 2009; Estes et al., 2011; Drazen and Sutton, 2017). In the CCZ, top seafloor predators are large fishes, crustaceans, and octopods, many of which are opportunistic scavengers readily attracted to baited cameras (Leitner et al., 2017; Drazen et al., 2019; Harbour et al., 2020). While these highly mobile predators are also detected in seafloor imaging transects, they are often observed in a very low (<1%) percentage of images (e.g., Milligan et al., 2016) due to their sparse distribution and avoidance of light, noise, and vibrations from survey vehicles, making baited imaging a key technique for studying the predator-scavenger component of abyssal seafloor ecosystems (Drazen et al., 2021, this vol.; Leitner et al., 2017).

Here we test the “shared-fauna” prediction of the SRH for bait-attending fauna in the western CCZ using data from two baited camera landers which were deployed a total of 17 times on three different seamounts and their proximate abyssal plains, one in each of the three western APEIs. Collectively, the DeepCCZ expedition has provided the first baited camera data from the western APEI regions. The data presented here also represent the first baited experiments on abyssal-depth seamounts. Thus, in addition to evaluating the SRH, we also report on the diversity and composition of the bait-attending megafauna and the potential importance of environmental characteristics such as seafloor habitat type and productivity in structuring this community.

The main goals of this study were to describe the bait-attending assemblage from abyssal seamounts for the first time and to test the “shared-fauna” prediction of the SRH in the western CCZ in the context of deep-sea mining for bait-attending abyssal-demersal fauna. These are mid-level and top predators, necrophagivores, and scavengers in abyssal seafloor ecosystems. From our observations, we cannot reject the SRH for the bait-attending community. All abyssal plain morphospecies were also seen on at least one seamount deployment. However, the reverse was not true. In fact, seven morphospecies were exclusive to seamount deployments. Therefore, these abyssal seamounts were found to host diverse and different bait-attending assemblages in comparison to their neighboring abyssal plains. In fact, abyssal plain assemblages hundreds of kilometers apart were more similar to each other, than to those assemblages on seamounts just 15 km away. The seamounts sampled also had different dominant fauna, with synaphobranchid eels dominating in the southern two seamounts, and large decapod shrimps dominating the community in the northern seamount. The significant differences in community structure make it unlikely that displaced animals will venture up into the seamount habitat in sufficient numbers to create and sustain viable populations on the timescales required for recovery (>26 years), even to avoid negative mining impacts such as extensive sediment plumes and reduction or elimination of infaunal and benthic prey (Gollner et al., 2017; Jones et al., 2017; Simon-Lledó et al., 2019). While highly mobile animals are often found in a variety of habitats, their core habitat, where they are naturally the most abundant, is often needed to sustain reproductive populations (Drazen et al., 2019). Moreover, seamounts make up only 0.3% of the habitat area of the CCZ (Washburn et al., 2021) and ecological research shows that a 99% habitat loss results in extinctions of essentially all species reliant on that habitat (Hanski et al., 2013; Rybicki and Hanski, 2013). Thus, protection of seamounts in the CCZ region alone does not appear to be sufficient to preserve abyssal biodiversity, even if all the mobile abyssal species can live on seamounts. Therefore, while we found no morphospecies exclusive to abyssal plains, we argue that distinct differences in densities indicate that only preserving seamounts is likely to be insufficient refuge for top predators and scavengers of the CCZ.

Often, seamounts are considered unusual habitats in the deep-sea because they provide hard substrate, which can be rare in much of the deep sea (but see Riehl et al., 2020; Smith et al., 2020). Previous works comparing seamounts to surrounding abyssal plains face two complications. Firstly, these studies mostly attempted to compare fauna at bathyal depths on seamounts to fauna at abyssal depths on plains (e.g., Christiansen et al., 2015; Vieira et al., 2018), so any difference between seamounts and abyssal plains may result from the strong vertical zonation of fauna across this depth gradient (Christiansen et al., 2015; Denda et al., 2017; Linley et al., 2017) instead of geomorphology. Secondly, most studies compared hard-substrate habitats, which predominate on seamounts, to soft-substrate plain habitats, making it difficult to distinguish a seamount effect from a substrate effect (e.g., Christiansen et al., 2015; Vieira et al., 2018). Here we specifically compared soft-sediment habitats on abyssal seamounts to surrounding soft-sediment abyssal plains, making the clear community differences between seamounts and abyssal plains reported particularly noteworthy, especially because bait-attending fauna are mobile and generally widespread. One study in the Atlantic abyssal plains for example, showed no difference in the fish communities between abyssal plains and abyssal highs with elevations less than 1,000 m (Milligan et al., 2016). However, for the same area, abyssal hills were found to have significantly higher biomass, higher diversity, and a different trophic composition for the invertebrate, benthic megafaunal community (Durden et al., 2015). Moreover, across a gradient of low relief bathymetric change within the CCZ, another study found significantly higher abundances, larger body sizes, higher diversity, and different community composition for bait-attending fauna at higher relative elevations (abyssal hills) vs. plains and depressions (Leitner et al., 2017). Finally, a recent study has found that even changes in depth as small as 10s of meters can significantly influence the benthic megafaunal community (Durden et al., 2020). Thus, a bathymetric change of 1,000 m, even without a substrate change, would be expected to affect the megafaunal community.

Cuvelier et al. (2020) and Laroche et al. (2020) conducted the only other tests of the SRH in the CCZ, and their results differ from ours in finding lower taxonomic overlap between seamounts and abyssal plains than reported here for bait-attending fauna. Cuvelier et al. (2020) used ROV video and compared the megafaunal communities, excluding fishes, of four seamounts and surrounding nodule fields and found, similar to the results here, that seamounts hosted distinct benthic megafaunal communities. However, they found only 10% taxonomic overlap between abyssal plains and seamounts. Laroche et al. (2020) also found that abyssal seamounts and neighboring abyssal-plain communities (the same locations studied here) were distinct based on eDNA sampling of sediment and bottom waters, finding only 16–19% seamount vs. plain overlap in amplicon sequence variants. Both studies concluded that the SRH was not valid for mining impacts in the CCZ due to low degrees of faunal overlap (Cuvelier et al., 2020). While we did find 7 of 22 morphospecies unique to the sampled seamounts, we found much higher (68%) taxonomic overlap between seamounts and plains. Moreover, all of the abyssal bait-attending morphospecies were also found on seamounts, though often in much lower numbers. Thus, seamounts may provide better refugia for the highly mobile scavengers/predators than for the much less mobile megafaunal deposit and suspension feeders. It should be noted that while Cuvelier et al. (2020) did have data from abyssal depths on three of the visited seamounts, all but one of their seamounts extended into bathyal depths, making these bathyal seamounts rather than the abyssal seamounts as discussed here. In addition, fishes were left out of their comparative statistical analysis due to their lack of representativity and possibly attraction to the ROV lights, although the authors did report greater fish diversity on seamounts than in abyssal nodule fields (Cuvelier et al., 2020). Laroche et al. (2020) found that fishes represented only a small fraction of the amplicon sequence variants identified, making seamount vs. abyssal-plain comparisons difficult.

Studies from bathyal seamounts in other regions, though shallower than the present work, show some similarities to our findings. Witte (1999) reported results from a large carcass experiment on a bathyal seamount summit (1,900 m depth) in the Arabian sea. High numbers of large aristeid shrimps were recorded at the bait, similar to our observations at the seamount in APEI 1. However, Witte also found a high number of macrourids at the bathyal seamount summit, which were absent at the nearby abyssal plain site, which was instead dominated by scavenging amphipods and large numbers of zoarcid fishes (Witte, 1999). Nevertheless, similar to our findings here, Witte found a distinct scavenging community at the seamount summit, though the dominant seamount taxa were different from those we found in the western CCZ. The only other baited camera data available from deep, oceanic seamounts come from Wilson et al. (1985), who studied the bait-attending community of one bathyal seamount (1,443 m) in the North Pacific. They observed halosaurs and shrimp from the genus Acanthephyra, which we find to be seamount-associated and absent from the proximate abyssal plains. Wilson et al. (1985) also observed high numbers of penaeid shrimp around the bait, as well as several morphospecies of synaphobranchid eels, though none in high numbers (MaxN = 4). Our results are also consistent with a study on the shallow Ampere Seamount in the NE Atlantic by Christiansen et al. (2015), who found large numbers of synaphobranchid eels on the bathyal slopes of the seamount. In this study only a single species (an alepocephalid) was shared between the deep slopes of Ampere seamount and the abyssal reference site.

Despite the fact that small abyssal seamounts (seamounts whose summit depths are ≥3,000 m) are the most common class of seamounts (Wessel et al., 2010), they are some of the most understudied, least explored habitats in the deep sea. The deployments discussed here, to our knowledge, yielded the first baited camera data published from abyssal seamounts. To date, seamount research has generally focused on shallower seamounts, which can be productivity hotspots, with abundant, high biomass, and diverse pelagic and benthic communities (Holland and Grubbs, 2007; Pitcher et al., 2007; Morato et al., 2010; Rowden et al., 2010; Leitner et al., 2020). This “seamount effect” is still not fully understood, but is likely due to the added habitat heterogeneity provided by the seamount structure and increased food availability due to modified hydrodynamics and topographic blocking of mesopelagic migrators (Genin et al., 1988; Genin, 2004; Genin and Dower, 2007; Morato et al., 2009; Lavelle and Mohn, 2010). Whether this “seamount effect” extends to the deepest, and most ubiquitous seamounts in the global ocean, remains uncertain, mostly due to the lack of data from deep features (Wilson et al., 1985; Wessel, 2001; Rowden et al., 2010). Evidence from abyssal hills suggest that such seamount effects may extend to the abyss, since abyssal hills can have higher detrital food availability (Morris et al., 2016; Durden et al., 2017).

Our observations provide initial evidence that this “seamount effect” can apply to abyssal seamounts in some cases. Seamounts in the western CCZ hosted higher community relative abundances than the proximate abyssal plains and had higher morphospecies richness. Moreover, our analysis showed that there are likely more as of yet unrecorded taxa on seamounts. Higher order diversity metrics showed that seamount diversity was lower than abyssal plain diversity, though this was due to low evenness, not to low richness. The extraordinarily high relative abundances of eels (in APEI 4 and 7) and shrimps (APEI 1) on these seamounts resulted in lower Shannon and Simpson diversity estimates. It must also be noted that the individual seamounts themselves had distinct communities, with each feature in each of the APEIs clustering separately. Therefore, while the communities on the three sampled seamounts were more similar to each other than to those on the surrounding plains, each seamount also had a unique community. Therefore, these abyssal seamounts enhance regional biodiversity, though the mechanisms are not yet fully clear. POC flux, a proxy for food availability in the deep-sea, was found to be a significant driver of differences in community composition (in addition to BBPI/habitat type). More sampling should be conducted on abyssal seamounts, especially on those within high productivity regimes, to examine further the relationship found here between high relative abundances on seamounts as well as high single taxon dominance and productivity.

Currently, community and diversity analyses are hampered by limited taxonomic resolution. While baited cameras are an efficient and unobtrusive method for observing abyssal fishes, scavengers, and predators, physical sampling through trawls and additional traps are important complementary sampling methods that would enable additional species level identifications (Drazen and Sutton, 2017; Priede, 2017; Drazen et al., 2021, this vol). This information is currently lacking for many megafaunal species in the CCZ, because there has been no trawling in this area. Nevertheless, ISA-mandated environmental baselines require detailed taxonomic resolution in order to be effective (Wedding et al., 2015; Smith et al., 2020). Thus, there is a need for additional complementary physical sampling at this stage.

Our results show that abyssal seamounts host distinct, morphospecies-rich, communities that contribute to the regional biodiversity of the CCZ. These seamounts may not face direct mining impacts due to their challenging terrain but, it must not be assumed that because CCZ seamounts will not face manganese nodule mining, that they will not be impacted by mining activities. Nodule extraction on abyssal plains will likely generate large sediment plumes, both at the seafloor and in the midwater, that potentially could spread over 100s of kilometers (Drazen et al., 2020; Smith et al., 2020). Nearby seamount habitats therefore could also sustain impacts from these sediment plumes. Therefore, these distinct habitats merit consideration for environmental protection and further scientific study.

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.

Ethical review and approval was not required for the animal study because this was a non-extractive video study.

AL, JD, and CS conceived of the project and conducted the field work, interpreted the results and drew final conclusions. AL annotated the video data, conducted statistical analyses, and wrote the body of the manuscript. JD and CS edited and made substantial contributions to the manuscript writing. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.