Marine biodiversity has always been less well understood than that of terrestrial ecosystems. The obvious hazards and economic challenges of in situ surveys and sampling underwater have been and will remain barriers to scientific research at depth. While the marine biodiversity surveys in past centuries focused on the infralittoral and shallow depths, by the 1970s submersible technology allowed surveys of the deep-sea (Grassle et al., 1975; Heirtzler and Grassle, 1976; Barnes et al., 1977; Corliss et al., 1979; Tunnicliffe et al., 1986), with surprising discoveries of marine life that have resulted in a dramatic re-thinking of marine biodiversity patterns (e.g., Rex, 1981; Grassle, 1985). However, the marine realms between the deep-sea (>200 m depths) and shallow waters (0–∼30 m), the so-called “twilight” mesophotic zone, were scarcely examined, as the depths were too shallow for safe submersible operation yet too deep for conventional SCUBA diving (Pyle, 1996; Hinderstein et al., 2010; Kahng et al., 2010).

However, technological advances in both smaller, remotely operated submersibles (ROVs) (Fricke and Knauer, 1986; Stewart and Auster, 1989; Love et al., 1994; Lindsay et al., 2012), and in rebreather diving equipment (Stone, 1990; Pyle, 1999, 2000), have allowed exploration of these mesophotic ecosystems to expand greatly in scale and frequency. Research in these ecosystems have yielded important new discoveries about marine biodiversity (Erdmann et al., 1998; Pyle, 2000; Kane et al., 2014; Rowley, 2014; Kosaki et al., 2017). However, as seen from both shallow-water and deep-sea work, studies on understudied, or so-called “minor taxa”, have lagged.

One such understudied taxon is the order Zoantharia (=Zoanthidea, within Cnidaria: Anthozoa: Hexacorallia), commonly known as “colonial anemones.” Zoantharians have been reported from most marine regions of the world, from tidal zones of shallow tropical coral reefs (e.g., Karlson, 1988) to the deep seafloor greater than 5500 m (Reimer and Sinniger, 2010). The most commonly encountered zoantharian are the shallow coral reef zooxanthellate genera Palythoa and Zoanthus. Due to ease of observation, these groups are better documented than other shallow water Zoantharia (e.g., Karlson, 1988; Acosta et al., 2005; Irei et al., 2011). On the other hand, at mesophotic to deeper depths, many zoantharian are epizoic, living on other various organisms including sponges, hydroids, antipatharians, octocorals, eunicid worm tubes, and even echinoderms (e.g., Sinniger et al., 2010a; Swain, 2010; Kise and Reimer, 2016; Kise et al., 2018), utilizing these hosts to help obtain energy from the water column (Swain, 2010). Diversity-focused research in the deep sea has revealed previously unknown taxa that have reshaped our understanding of the order (Reimer et al., 2007; Reimer and Sinniger, 2010; Sinniger et al., 2013; Carreiro-Silva et al., 2017). We now know that the deep-sea harbors high levels of zoantharian diversity, mandating more research to catalog and understand this diversity (Reimer et al., 2007; Swain, 2010; Sinniger et al., 2013; Carreiro-Silva et al., 2017). However, studies on zoantharian at mesophotic and deeper depths are generally lacking, and collection of Zoantharia in mesophotic areas lags behind other benthic organisms such as sponges, stony corals, and octocorals. Thus, it is not known whether such depths harbor species affiliated with shallow (0–30 m) or deep (>200 m) communities, a mixture of both (=ecotone; region of transition between two biological communities), or unique depth-specific biodiversity as observed in brachyuran crabs (Hurley et al., 2016).

Here we report on mesophotic and deeper adjacent ecosystem (30–>200 m depths) surveys from four regions in Japan and Israel based on a variety of technologies including rebreathers, ROVs, traps, and phylogenetic tools. As an example of how our understanding of the biodiversity of understudied taxa can benefit from these platforms, we examine collated data (video images + specimens) from these surveys while focusing on the order Zoantharia. We use these findings to guide future research on neglected minor taxa at mesophotic and deeper depths.

While Zoantharia are “minor taxa”, they are nearly ubiquitous, reported from almost all marine regions of the world, and are considered important components of the marine fauna (e.g., Karlson, 1983; Irei et al., 2011). In this study, we observed Zoantharia in every survey with each type of technology employed, even though these surveys were not specifically focused on Zoantharia, demonstrating that these anthozoans may be widespread at mesophotic and deeper depths, at least in Okinawa and the Red Sea. These findings support previous research from other locations that has also indicated the potential for high diversity of zoantharians in deeper waters (Reimer et al., 2007; Swain, 2010; Sinniger et al., 2013; Carreiro-Silva et al., 2017).

Of particularly interest from our results are the presence of an Abyssoanthidae specimen at 300 to 400 m from Kochi, Japan. Previously, Abyssoanthidae has only been observed from depths of approximately 2000 to 5600 m in Japan (Reimer et al., 2007; Reimer and Sinniger, 2010) and the Mediterranean (Sinniger et al., 2010b), and the discovery of a specimen at these comparatively shallow depths is very surprising. Previously, E. planus has been the only zoantharian known to associate with Echinodermata, in association with sea urchins (Carlgren, 1923; Kise et al., 2018), and this newly reported Abyssoanthidae specimen represents the first record of a zoantharian in association with the class Crinoidea. This record also represents the first record of the family Abyssoanthidae as epizoic, as previously described specimens were found living directly on hard substrates (Reimer et al., 2007; Reimer and Sinniger, 2010).

Additionally, specimens MISE-MZ1 and MISE-MZ3 represent a potentially undescribed genus associated with glass sponges. Currently, the only formally described glass sponge-associated species belong to family Epizoanthidae (genera Epizoanthus, Thoracactis) or to genus Isozoanthus within Parazoanthidae (Carlgren, 1923; Low et al., 2016). The current specimens clearly belong within Parazoanthidae in the phylogenetic analyses, and thus may be an undescribed species from either Isozoanthus or an undescribed genus-level clade within Parazoanthidae.

Four specimens were nested within the genus Epizoanthus, and constitute two species-groups. Specimens MISE-MZ6, MISE-MZ8, and MISE-MZ9, which were sampled several years ago and have proliferated in Churaumi Aquarium holding tanks, covering various substrates including living slit snails, hermit crab shells, and empty shell rubble, indicating that this species, at least in aquaria, is a facultative symbiont. The other Epizoanthus (MISE-MZ7) was found on nylon rope, and was also apparently sampled some time ago, although no specific date was recorded. Both specimens do not match described species in the region, but without more in situ information such as depth or original substrate, no conclusions on their specific identities can be made.

Our work also discovered Parazoanthidae genera deeper than has been previously reported; Umimayanthus sp. in Okinawa (depth >200 m; MISE-MZ5) and Antipathozoanthus sp. in the northern Red Sea (153–169 m), as well as the first formal records of Savalia (MISE-MZ4) in Okinawa. Such results should be taken with caution. Although they represent range and depth extensions, the overall dearth of Zoantharia data from the deep may hinder our ability to make clear conclusions of depth ranges and distributions of species.

From the current results, as well as findings in previous recent research (Reimer et al., 2007; Swain, 2010; Sinniger et al., 2010b, 2013; Carreiro-Silva et al., 2017), we can make two preliminary conclusions. Firstly, it appears that most mesophotic and deep-sea Zoantharia genera are widely distributed in the world’s oceans, and across a much greater range of depths than is currently understood. Many genera have been reported from both the Atlantic and Indo-Pacific (Sinniger et al., 2010b; Carreiro-Silva et al., 2017), and our current work found genera both deeper (Umimayanthus; Antipathozoanthus) and much shallower (Abyssoanthidae) than has previously been recorded. Secondly, these results highlight the dearth of information and distributional records of Zoantharia, and thus, comparisons on mesophotic and deeper water diversity of zoantharians between different regions, such Japan and Israel in this study, remain premature. Moving forward, basic biological data such as records of occurrences of zoantharians from any mesophotic or deeper depths regardless of location should be a research priority, allowing future biogeographical analyses.

The affiliation of mesophotic Zoantharia with both shallow and deep (abyssal) realms invokes a novel biogeographic enigma. Previous studies of fishes and crabs have revealed that mesophotic biodiversity is affiliated almost exclusively with the genera and families of the shallow shelf fauna (Kahng et al., 2014; Hurley et al., 2016). Either Abyssoanthidae and other deep-sea zoantharians have a greater presence in shallow habitat than previously known, or the mesophotic Zoantharia have a “hybrid” origin that includes some deep-sea fauna. Further surveys will likely resolve this dilemma. Previously, it has been hypothesized that shallow-water zooxanthellate zoantharians evolved from deeper water, epibiotic species (Swain, 2010), and this could partially explain the presence of deep-sea specimens in shallower waters.

Examining the different technologies employed in this study, each has its own strengths and weaknesses. Rebreather surveys allow high resolution in situ images and sampling, while ROV surveys are costlier yet safer, longer, and able to reach greater depths than rebreathers. However, many ROVs such as PICASSO cannot collect specimens, relying instead on high-resolution in situ images. Both ROVs and rebreather divers can still provide initial photographic records of species (e.g., Nishikawa et al., 2011), an enormous step forward given the almost complete lack of data for many marine taxa in many regions of the world, including Zoantharia (e.g., Reimer et al., 2014). The combination of ROVs or submersibles covering wide areas of the benthic environment followed by rebreather divers targeting specific sites of interest may be the most productive use of both technologies (e.g., Pyle et al., 2016). Dredging and nets, employed by Churaumi Aquarium, are effective in recovering many specimens, but even when equipped with cameras do not often result in high-resolution images of small benthos such as zoantharians, and are indiscriminate in their sampling, potentially damaging other, non-target benthos.

The scant state of knowledge about mesophotic invertebrate fauna in general and Zoantharia in particular is underscored by the substantial gains presented here, based on a modest data set. The need for biodiversity data on understudied and unknown MCE taxa is critical to understanding burgeoning anthropogenic threats (Rocha et al., 2018) including ongoing climate change. With the majority of MCE and deep-sea biological research focusing instead on more recognizable taxa such as fishes and scleractinian corals, observations of “minor taxa” should be incorporated into these ongoing sampling and field protocols to maximize efficiency. For example, rebreather divers or ROVs could take a photographic benthic quadrat or high-resolution image every 10 min. Archiving and depositing such information would rapidly amplify the available distribution data. Specimen deposits are also greatly needed for many other “minor taxa”, not only Zoantharia. In addition to specimen vouchers, genetic voucher subsamples are critical to identify novel species and evolutionary processes (Hurley et al., 2016).

Further research at mesophotic and deep-sea depths will undoubtedly enhance our knowledge of zoantharian diversity, which potentially includes species that have a major ecological role in MCEs, such as the zoantharian “gold coral” S. savaglia (e.g., Cerrano et al., 2010). As Zoantharia is a cosmopolitan group, data on species distributions are key to a better understanding of marine biogeography (Briggs and Bowen, 2016). Such information will also help contribute to management decisions in the face of threats to mesophotic habitats (Rocha et al., 2018), such as tailing disposal (Edinger, 2012) and oil exploration (Francini-Filho et al., 2018). These minor taxa are a major component of marine ecosystems, and integral to understanding anthropogenic impacts and consequences.

Collection of Red Sea animals complied with a permit issued by the Israel Nature and National Parks Protection Authority. No permits are needed for the collection of Zoantharia in Japan, nor are there any ethical permits required.

All authors contributed to the conception and design of the research. All authors wrote sections of the manuscript. JR performed field work, collected specimens, conducted analyses, wrote the first draft of the manuscript, and provided funding. HK and MS conducted analyses and helped edit the manuscript. DL, BB, and YB performed field work, collected specimens, helped edit the manuscript, and provided funding. RP, JC, and TH performed field work, collected specimens, and helped edit the manuscript. MN helped edit the manuscript and provided funding. All authors read 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.