Journal of Crustacean Biology Advance Access published 4 February 2021 Journal of Crustacean Biology The Crustacean Society Journal of Crustacean Biology (2021) 1–13. doi:10.1093/jcbiol/ruaa102 Downloaded from https://academic.oup.com/jcb/advance-article/doi/10.1093/jcbiol/ruaa102/6128500 by University of Newcastle user on 09 February 2021 Worldwide distribution and depth limits of decapod crustaceans (Penaeoidea, Oplophoroidea) across the abyssal-hadal transition zone of eleven subduction trenches and five additional deep-sea features Jackson A. Swan1, Alan J. Jamieson1, , Thomas D. Linley1, and Paul H. Yancey2 1School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, NE1 7RU, UK, and 2Biology Department, Whitman College, Walla Walla, WA 99362, U.S.A Correspondence: Alan J Jamieson; e-mail: [email protected] (Received 6 November 2020; accepted 4 January 2021) ABSTRACT Decapod crustaceans are conspicuous members of marine benthic communities to at least 7,700 m deep. To assess the bathymetric extent of this taxonomic group, baited landers were deployed to across the abyssal-hadal transition zone of 11 subduction trenches spanning the Pacific, Atlantic, Southern, and Indian oceans and additional sites. Decapods were dominated by penaeid shrimps (superfamily Penaeoidea), in particular Benthesicymus Spence Bate, 1881 and Cerataspis Gray, 1828, with the former being found deeper. Benthesicymus cf. crenatus Spence Bate, 1881 was observed in the Kermadec, Mariana, New Hebrides, Puerto Rico, Peru-Chile, Tonga, San Cristobal, and Santa Cruz trenches, plus the South Fiji Basin and the Wallaby- Zenith Fracture Zone. They were not recorded in the Abaco Canyon, Agulhas Fracture Zone, Java Trench, or any of the polar locations. Cerataspis cf. monstrosus Gray, 1828 was present in the Kermadec, Mariana, New Hebrides, Puerto Rico, and Java trenches, the Abaco Canyon, Agulhas Fracture Zone, Wallaby-Zenith Fracture Zone and the South Fiji Basin, but absent from the Tonga, San Cristobal and Santa Cruz trenches. Hymenopenaeus nereus (Faxon, 1893) was only recorded in the Peru-Chile Trench. Unidentified species belonging to superfamily Oplophoroidea were observed to a maximum depth of 6,931 m. Decapods are thus are pri- marily represented at hadal depths by penaeoid shrimps, consistently present at tropical and temperate latitudes to ~7,700 m, while absent from equivalent depths in polar regions. Their maximum depth may be limited due to hydrostatic pressure, while potentially affected by temperature and oxygen in some instances. Muscle samples of three specimens from 6,000 m (Mariana and Kermadec trenches) were found to have high levels of trimethylamine N-oxide (TMAO; 260 mmol kg–1), the major piezolyte, a protectant against hydrostatic pressure, in other deep-sea organisms. We speculate that physiological limits to TMAO concentration may prevent them from inhabiting the greatest hadal depths. Key Words: abyssal zone, deep-sea fauna, hadal zone, piezolytes, trimethylamine N-oxide (TMAO), subduction trenches INTRODUCTION that shrimps belonging to superfamilies Penaeoidea (suborder Dendrobranchiata) and Oplophoroidea (infraorder Caridea) Based on the first major trawling efforts at hadal depths were present in the trenches of the Western Pacific (mainly in the 1950s (Wolff, 1960, 1970), members of Decapoda the Japan and Kermadec trenches) to at least 7,703 m and were long thought to have no representatives greater than 6,890 m, respectively. This conclusion was, however, based 5,700 m (Herring, 2002; Blankenship & Levin, 2007), des- on just eight deployments of a baited camera spanning three pite some anecdotal evidence to the contrary (Pérès, 1965; localities in which decapods were observed in the shallowest Hessler et al., 1978). Jamieson et al. (2009a) demonstrated five deployments. © The Author(s) 2021. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved. For permissions, please e-mail: [email protected] J. A. SWAN ET AL. The study of Jamieson et al. (2009a) was followed by sev- depth in bony fishes, though as osmoregulators hypo-osmotic to eral other studies that showed that the dominant Penaeoidea seawater, there are no ‘shallow’ osmolytes to replace (Gillett et al., was Benthesicymus crenatus Spence Bate, 1881 and a species of 1997; Samerotte et al., 2007; Yancey et al., 2014). TMAO was pos- Oplophoroidea thought to belong to genus Acanthephyra A. Milne- tulated to play a major role in pressure adaptation in all these Edwards, 1881. The former was clearly attracted to the baited taxa, protecting macromolecules from pressure perturbations. camera by the elevated abundance of lysianassoid amphipods Moreover, bony fishes appear to be limited to depths below 8,400 which they were observed to prey upon, while the latter appeared m, with a limit to the impact of TMAO on osmoregulatory physi- Downloaded from https://academic.oup.com/jcb/advance-article/doi/10.1093/jcbiol/ruaa102/6128500 by University of Newcastle user on 09 February 2021 to be incidental observations as they showed no obvious interest ology possibly creating that limit (Yancey et al., 2014, Linley et al., in the bait or associated fauna (Jamieson et al., 2011, 2012, 2013; 2016; Downing et al., 2018). Linley et al., 2017). The last ten years have seen an increase in biological observa- tions at hadal depths (Jamieson, 2018), yet megafaunal studies tend MATERIALS AND METHODS to focus on either amphipods (e.g., Fujii et al., 2013; Ritchie et al., 2015; Lacey et al., 2016) or fishes (e.g., Linley et al., 2016, 2017). Sampling effort The technological limitations of working at such extreme depths has resulted in a lack of exploratory vehicles rated to 11,000 m Baited camera landers were deployed in every ocean at a number and the near-cessation of bottom trawling at hadal depths since of different geomorphological features (Table 1, Fig. 1). In the the 1950s. As a result, free-fall baited camera and trap landers North Pacific, the primary site was the Mariana Trench, where have become the dominant methodology at hadal depths. The 37 deployments were made between 4,040 and 10,925 m over bias towards fish and amphipod studies mirrors the ease in which three expeditions in 2014, 2017, and 2019. The primary site in these groups are imaged and captured using baited traps and cam- the southwestern Pacific was the Kermadec Trench, where 44 de- eras, respectively. In the pursuit of these more robust quantitative ployments were made between 3,946 and 9,281 m spanning five studies, however, there are several other taxonomic groups that expeditions between 2009 and 2014. Six deployments were made frequent the scientific vehicles that are often cryptic (e.g., Isopoda; between 6,848 and 10,823 m in the neighbouring Tonga Trench Jamieson et al., 2012), infrequent (e.g., Cephalopoda; Jamieson in 2019. Deployments were made in 2013 and 2015 between & Vecchione, 2020) or geographically limited (e.g., Gastropoda; 4,101 and 6,948 m in the New Hebrides Trench east of New Aguzzi et al., 2012). Drawing conclusions on the maximum depth Caledonia (1,600 km north of Kermadec and Tonga trenches), and geographical expanse at such extreme depths is difficult rela- as well as another four deployments between 4,078 and 4,100 tive to amphipods (Downing et al., 2018) and fishes (Yancey et al., m on the South Fiji Basin that connects the New Hebrides and 2014). Kermadec trenches. Five deployments were made further north Decapod crustaceans represents one such overlooked taxo- in the San Cristobal and Santa Cruz trenches off the Solomon nomic group that regularly appears in baited camera datasets. Islands in 2019, in and between the two trenches from 5,906 to The presence of decapods is often limited to a small number of 7,431 m (given the proximity and overlapping sampling, these images and their diversity appears low, but they are consistent in two trenches are hereafter referred to as the Solomon trenches). appearing in images from upper hadal depths. This has meant Two expeditions (2010 and 2018) made 21 deployments between that recent studies tend only to briefly mention the Decapoda 4,051 and 8,074 m in the Peru-Chile Trench, southeastern Pacific, in passing (e.g., Jamieson et al., 2011, 2013; Linley et al., 2017; with the majority in the southern sector, often called the Atacama Jamieson & Vecchione, 2020) and their significance is perhaps Trench. In the Indian Ocean, seven deployments were made in being under-appreciated. the Wallaby-Zenith Fracture Zone (west of Australia) between In the ten years since the first unequivocal finding of hadal 4,730 and 6,537 m in 2017, and a further seven deployments be- decapods, hundreds more lander deployments have been made tween 6,146 and 7,176 m in the Java (Sunda) Trench, south of to the great depths (Jamieson, 2018). In addition to the increase in Indonesia, in 2019. In the Atlantic Ocean, 12 deployments were the number of scientific observations being made at hadal depths, made between 4,040 and 8,370 m in the Puerto Rico Trench on the recent Five Deeps Expedition (Jamieson et al., 2019) provided two expeditions (2018 and 2019), another two deployments in the a platform in which to perform these investigations across multiple Abaco Canyon off the Bahamas in 2018 (4,900 m), and one in the sites spanning every ocean in less than a year (Stewart & Jamieson, Agulhas Fracture Zone southwest of South Africa in 2019 (5,493 2019). m). In the Southern Ocean, three deployments were made in the We collated all baited-camera records from the abyssal-hadal South Shetland Trench between 2,875 and 5,200 m in 2015, and transition zone from the Five Deeps Expedition (Jamieson et al., seven deployments in the South Sandwich Trench between 6,044 2019), the HADEEP projects (Jamieson et al., 2009b), HADES-M and 8,266 m in 2019.