Abstract
Eurythenes S. I. Smith in Scudder, 1882 are one of the largest scavenging deep-sea amphipods (max. 154 mm) and are found in every ocean across an extensive bathymetric range from the shallow polar waters to hadal depths. Recent systematic studies of the genus have illuminated a cryptic species complex and highlighted the benefits of using a combination of morphological and molecular identification approaches. In this study, we present the ninth species, Eurythenes plasticus sp. nov., which was recovered using baited traps between the depths 6010 and 6949 m in the Mariana Trench (Northwest Pacific Ocean) in 2014. This new Eurythenes species was found to have distinct morphological characteristics and be a well-supported clade based on sequence variation at two mitochondrial regions (16S rDNA and COI). While this species is new to science and lives in the remote hadal zone, it is not exempt from the impacts of anthropogenic pollution. Indeed, one individual was found to have a microplastic fibre, 83.74% similar to polyethylene terephthalate (PET), in its hindgut. As this species has a bathymetric range spanning from abyssal to hadal depths in the Central Pacific Ocean basin, it offers further insights into the biogeography of Eurythenes.
References
Alomar, C. & Deudero, S. (2017) Evidence of microplastic ingestion in the shark Galeus melastomus Rafinesque, 1810 in the continental shelf off the western Mediterranean Sea. Environmental Pollution, 223, 223–229.
https://doi.org/10.1016/j.envpol.2017.01.015
Barnard, J.L. (1962) South Atlantic abyssal amphipods collected by R.V. Vema. In: Barnard, J.L., Menzies, R.J. & Băcescu, M.C. (Eds.), Abyssal Crustacea. Columbia University Press, New York and London, pp. 1–78.
Bellas, J., Martínez-Armental, J., Martínez-Cámara, A., Besada, V. & Martínez-Gómez, C. (2016) Ingestion of microplastics by demersal fish from the Spanish Atlantic and Mediterranean coasts. Marine Pollution Bulletin, 109 (1), 55–60.
https://doi.org/10.1016/j.marpolbul.2016.06.026
Besseling, E., Foekema, E.M., Van Franeker, J.A., Leopold, M.F., Kühn, S., Bravo Rebolledo, E.L., Heße, E., Mielke, L.J.I.J., Ijzer, J., Kamminga, P. & Koelmans, A.A. (2015) Microplastic in a macro filter feeder: humpback whale Megaptera novaeangliae. Marine Pollution Bulletin, 95 (1), 248–252.
https://doi.org/10.1016/j.marpolbul.2015.04.007
Birky, C., Wolf, C., Maughan, H., Herbertson, L. & Henry, E. (2005) Speciation and selection without sex. Hydrobiologia, 546 (1), 29–45.
https://doi.org/10.1007/s10750-005-4097-2
Blankenship, L.E. & Levin, L.A. (2007) Extreme food webs: Foraging strategies and diets of scavenging amphipods from the ocean’s deepest 5 kilometers. Limnology and Oceanography, 52 (4), 1685–1697.
Brandt, A., Błażewicz-Paszkowycz, M., Bamber, R.N., Mühlenhardt-Siegel, U., Malyutina, M.V., Kaiser, S., De Broyer, C. & Havermans, C. (2012) Are there widespread peracarid species in the deep sea (Crustacea: Malacostraca)? Polish Polar Research, 33 (2), 139–162.
https://doi.org/10.2478/v10183−012−0012−5
Charette, M.A. & Smith, W.H.F (2010) The volume of the Earth’s ocean. Oceanography, 23 (2), 112–114.
https://doi.org/10.5670/oceanog.2010.51
Chevreux, E. (1905) Description d’un amphipode (Katius obesus, nov. gen. et sp.), suivie d’une liste des amphipodes de la tribu des Gammarina ramenés par le filet à grand eouverture pendant la dernière campagne de la Princesse-Alice en 1904. Bulletin du Musée océanographique de Monaco, 35, 1–7.
Chiba, S., Saito, H., Fletcher, R., Yogi, T., Kayo, M., Miyagi, S., Ogido, M. & Fujikura, K. (2018) Human footprint in the abyss: 30 year records of deep-sea plastic debris. Marine Policy, 96, 204–212.
https://doi.org/10.1016/j.marpol.2018.03.022
Coleman, C.O. (2003) “Digital inking”: How to make perfect line drawings on computers. Organisms Diversity & Evolution, 3, 1–14.
Coleman, C.O. (2009) Drawing setae the digital way. Zoosystems Evolution, 85 (2), 305–310.
https://doi.org/10.1002/zoos.200900008
Cornils, A. & Held, C. (2014) Evidence of cryptic and pseudocryptic speciation in the Paracalanus parvus species complex (Crustacea, Copepoda, Calanoida). Frontiers in Zoology, 11 (1), 19.
https://doi.org/10.1186/1742-9994-11-19
Downing, A.B., Wallace, G.T. & Yancey, P.H. (2018) Organic osmolytes of amphipods from littoral to hadal zones: Increases with depth in trimethylamine N-oxide, scyllo-inositol and other potential pressure counteractants. DeepSea Research Part I: Oceanographic Research Papers, 138, 1–10.
https://doi.org/10.1016/j.dsr.2018.05.008
d’Udekem d’Acoz, C. & Havermans, C. (2015) Contribution to the systematics of the genus Eurythenes S. I. Smith in Scudder, 1882 (Crustacea: Amphipoda: Lysianassoidea: Eurytheneidae). Zootaxa, 3971 (1), 1–80.
https://doi.org/10.11646/zootaxa.3971.1.1
Drummond, A.J., Ho, S.Y.W., Phillips, M.J. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. Public Library of Science Biology, 4, e88.
https://doi.org/10.1371/journal.pbio.0040088
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29 (8), 1969–1973.
https://doi.org/10.1093/molbev/mss075
Escobar-Briones, E., Nájera-Hillman, E. & Álvarez, F. (2010) Unique 16S rRNA sequences of Eurythenes gryllus (Crustacea: Amphipoda: Lysianassidae) from the Gulf of Mexico abyssal plain. Revista Mexicana de Biodiversidad, 81, 177–185.
Eustace, R.M., Kilgallen, N.M., Ritchie, H., Piertney, S.B. & Jamieson, A.J. (2016) Morphological and ontogenetic stratification of abyssal and hadal Eurythenes gryllus sensu lato (Amphipoda: Lysianassidae) from the Peru-Chile Trench. Deep Sea Research I: Oceanographic Research Papers, 109, 91–98.
https://doi.org/10.1016/j.dsr.2015.11.005
Foekema, E.M., De Gruijter, C., Mergia, M.T., van Franeker, J.A, Murk, A.J. & Koelmans, A.A. (2013) Plastic in North Sea fish. Environmental Science & Technology, 47 (15), 8818–8824.
https://doi.org/10.1021/es400931b.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
Forrest, A., Giacovazzi, L., Dunlop, S., Reisser, J., Tickler, D., Jamieson, A.J. & Meeuwig, J.J. (2019) Eliminating plastic pollution: How a voluntary contribution from industry will drive the circular plastics economy. Frontiers in Marine Science, 6: 627.
https://doi.org/10.3389/fmars.2019.00627
France, S.C. & Kocher, T.D. (1996) Geographic and bathymetric patterns of mitochondrial 16S rRNA sequence divergence amount deep-sea amphipods, Eurythenes gryllus. Marine Biology, 126 (4), 633–643.
Fujii, T., Kilgallen, N.M., Rowden, A.A. & Jamieson, A.J. (2013) Deep-sea amphipod community structure across abyssal to hadal depths in the Peru-Chile and Kermadec trenches. Marine Ecology Progress Series, 492, 125–138.
https://doi.org/10.3354/meps10489
Garlitska, L., Neretina, T., Schepetov, D., Mugue N.M., De Troch, M., Baguley, J.G., & Azovsky, A. (2012) Cryptic diversity of the ‘cosmopolitan’ harpacticoid copepod Nannopus palustris: genetic and morphological evidence. Molecular Ecology, 21 (21), 5336–5347.
https://doi.org/10.1111/mec.12016
GEBCO (2015) GEBCO_2014Grid [WWWDocument]. Gen.Bathymetr.ChartOcean. (URL) Available from: http://www.gebco.net/data_and_products/gridded_bathymetry_data/ gebco_30_second_grid/ (accessed 05.11.19)
Geyer, R., Jambeck, J.R. & Lavender Law, K. (2017) Production, use, and fate of all plastic ever made. Science Advances, 3 (7), e1700782.
https://doi.org/10.1126/sciadv.1700782
Hargrave, B.T. (1985) Feeding rates of abyssal scavenging amphipods (Eurythenes gryllus) determined in situ by time-lapse photography. Deep Sea Research Part A. Oceanographic Research Papers, 32 (4), 443–450.
https://doi.org/10.1016/0198-0149(85)90090-1
Hasegawa, M., Kishino, H. & Yano, T. (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22 (2), 160–174.
Havermans, C., Sonet, G., d’Udekem d’Acoz, C., Nagy, Z.T., Martin, P., Brix, S., Riehl, T., Agrawal, S. & Held, C. (2013) Genetic and morphological divergences in the cosmopolitan deep-sea amphipod Eurythenes gryllus reveal a diverse abyss and bipolar species. Public Library of Science One, 8 (9), e74218.
https://doi.org/10.1371/journal.pone.0074218
Havermans, C. (2016) Have we so far only seen the tip of the iceberg? Exploring species diversity and distribution of the giant amphipod Eurythenes. Biodiversity, 17 (1–2), 12–25.
https://doi.org/10.1080/14888386.2016.1172257
Havermans, C. & Smetacek, V. (2018) Bottom-up and top-down triggers of diversification: A new look at the evolutionary ecology of scavenging amphipods in the deep sea. Progress in Oceanography, 164, 37–51.
https://doi.org/10.1016/j.pocean.2018.04.008
Hessler, R.R., Ingram, C.L., Yayanos, A.A. & Burnett, B.R. (1978) Scavenging amphipods from the floor of the Philippine Trench. Deep Sea Research, 25 (11), 1029–1047.
https://doi.org/10.1016/0146-6291(78)90585-4
Horn, D., Granek, E.F. & Steele, C.L. (2019) Effects of environmentally relevant concentrations of microplastic fibers on Pacific mole crab (Emerita analoga) mortality and reproduction. Limnology and Oceanography Letters.
https://doi.org/10.1002/lol2.10137
Horton, T. & Thurston, M.H. (2014) A revision of the bathyal and abyssal necrophage genus Cyclocaris Stebbing, 1888 (Crustacea: Amphipoda: Cyclocaridae) with the addition of two new species from the Atlantic Ocean. Zootaxa, 3796 (3), 507–527. http://dx.doi.org/10.11646/zootaxa.3796.3.6
Ingram, C.L. & Hessler, R.R. (1983) Distribution and behavior of scavenging amphipods from the central North Pacific. Deep Sea Research Part A. Oceanographic Research Papers, 30 (7), 683–706.
http://dx.doi.org/10.1016/0198-0149(83)90017-1
Ingram, C.L. & Hessler, R.R. (1987) Population biology of the deep-sea amphipod Eurythenes gryllus: inferences from instar analyses. Deep Sea Research Part A. Oceanographic Research Papers, 34 (12), 1889–1910.
Jamieson, A.J. (2015) The hadal zone: Life in the deepest oceans, 1st ed. Cambridge University Press, Cambridge, UK.
Jamieson, A.J., Lacey, N.C., Lörz, A.N., Rowden, A.A. & Piertney S.B. (2013) The supergiant amphipod Alicella gigantea (Crustacea: Alicellidae) from hadal depths in the Kermadec Trench, SW Pacific Ocean. Deep Sea Research II: Topical Studies in Oceanography, 92, 107–113.
https://doi.org/10.1016/j.dsr2.2012.12.002
Jamieson, A.J., Brooks, L.S.R., Reid, W.D.K., Piertney, S.B., Narayanaswamy, B.E., & Linley, T.D. (2019) Microplastics and synthetic particles ingested by deep-sea amphipods in six of the deepest marine ecosystems on Earth. Royal Society Open Science, 6 (2), 180667.
http://dx.doi.org/10.1098/rsos.180667
Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFTA online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20 (4), 1160–1166.
https://doi.org/10.1093/bib/bbx108
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Ecology, 16, 111–120.
King, N.J & Priede, I.G. (2008) Coryphaenoides armatus, the abyssal grenadier global distribution, abundance, and ecology as determined by baited landers. American Fisheries Society Symposium, 63, 139–161.
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7), 1870–1874.
https://doi.org/10.1093/molbev/msw054
Lichtenstein, H. (1822). §. 30 [Crustacea]. In: Mandt, M.G. (Ed.), Observationes in historiam naturalem et anatomiam comparatam in itinere Groenlandico factae. Dissertatioin auguralis quam consensu et auctoritate gratiosi medicorum ordinis in universitate literaria berolinens iutsummi in medicina et chirurgia honores rite sibiconcedantur die XXII. M. Iulii A. MDCCCXXIIH.L.Q.S., publice defendet auctor Martinus Gulielmus Mandt Beyenburgensis. Opponentibus: J.Th. v. Brandt Med. Cd., J. Ollenroth Med. Cd., E. Gabler Med. Cd.; FormisBrueschckianis, Berlin, pp.31–37.
Lusher, A.L., O’Donnell, C., Officer, R. & O’Connor, I. (2016) Microplastic interactions with North Atlantic mesopelagic fish. ICES Journal of Marine Science, 73, 1214–1225.
https://doi.org/10.1093/icesjms/fsv241
Madsen, F.J. (1961) On the zoogeography and origin of the abyssal fauna, in view of the knowledge of the Porcellanasteridae. Galathea Rep, 4, 177–218.
Markmann, M. & Tautz, D. (2005) Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal RNA signature sequences. Philosophical Transactions of the Royal Society B: Biological Sciences. 360 (1462), 1917–1924.
https://doi.org/10.1098/rstb.2005.1723
Milne Edwards, H. (1848) Sur un crustacé amphipode, remarquable par sa grand etaille. Annales des Sciences Naturelles, 3 (9), 398.
Murphy, F., Ewins, C., Carbonnier, F. & Quinn, B. (2016) Waste water treatment works (WwTW) as a source of microplastics in the aquatic environment. Environmental Science & Technology, 50 (11), 5800–5808.
https://doi.org/10.1021/acs.est.5b05416
Narahara-Nakano, Y., Nakano, T. &Tomikawa, K. (2018) Deep-sea amphipod genus Eurythenes from Japan, with a description of a new Eurythenes species from off Hokkaido (Crustacea: Amphipoda: Lysianassoidea). Marine Biodiversity, 48 (1), 603–620.
https://doi.org/10.1007/s12526-017-0758-4
Palumbi, S., Martin, A. & Romano, S. (2002) The simple fool’s guide to PCR, version 2.0. Department Zoology, University of Hawaii.
Palumbi, S.R. (1994) Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics, 25, 547–572.
https://doi.org/10.1146/annurev.es.25.110194.002555
Peng, G., Bellerby, R., Zhang, F., Sun, X. & Li, D. (2020) The ocean’s ultimate trashcan: Hadal trenches as major depositories for plastic pollution. Water Research, 168, 115121.
https://doi.org/10.1016/j.watres.2019.115121
Peng, X., Chen, M., Chen, S., Dasgupta, S., Xu, H., Ta, K., Du, M., Li, J., Guo, Z. & Bai, S. (2018) Microplastics contaminate the deepest part of the world’s ocean. Geochemical Perspective Letters, 9, 1-5.
https://doi.org/10.7185/geochemlet.1829
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, syy032.
https://doi.org/10.1093/sysbio/syy032
Ritchie, H., Jamieson, A.J. & Piertney, S.B. (2015) Phylogenetic relationships among hadal amphipods of the Superfamily Lysianassoidea: Implications for taxonomy and biogeography. DeepSea Research I: Oceanographic Research Papers, 105, 119–131.
https://doi.org/10.1016/j.dsr.2015.08.014
Ritchie, H., Jamieson, A.J. & Piertney, S.B. (2017) Genome size variation in deep-sea amphipods. Royal Society Open Science, 4, 170862.
http://dx.doi.org/10.1098/rsos.170862
Saunders, P. (1981) Practical conversion of pressure to depth. Journal of Physical Oceanography, 11, 573–574.
Schliep, K., Potts, A.J., Morrison, D.A. & Grimm, G.W. (2017) Intertwining phylogenetic trees and networks. Methods in Ecology and Evolution, 8, 1212–1220.
https://doi.org/10.1111/2041-210X.12760
Schlining, K., von Thun, S., Kuhnz, L., Schlining, B., Lundsten, L., Jacobsen Stout, N., Chaney, L. & Connor, J. (2013) Debris in the deep: Using a 22-year video annotation database to survey marine litter in Monterey Canyon, central California, USA. Deep Sea Research I: Oceanographic Research Papers, 79, 96–105.
http://dx.doi.org/10.1016/j.dsr.2013.05.006
Smith, S.I. (1882) Eurythenes Lillgeborg. In: Scudder, S.H. (Ed.), Zoologicus, N., 1882. An alphabetical list of all generic names that have been employed by naturalists for recent and fossil animals from the earliest times to the close of the year 1879. 1. Supplemental list of Genera in Zoology. Washington, 21 (1), 376.
Smith, C.R., De Leo, F.C., Bernardino, A.F., Sweetman, A.K. & Arbizu, P.M. (2008) Abyssal food limitation, ecosystem structure and climate change. Trends in Ecology & Evolution, 23 (9), 518–528.
https://doi.org/10.1016/j.tree.2008.05.002
Stoddart, H.E. & Lowry, J.K. (2004) The deep-sea lysianassoid genus Eurythenes (Crustacea, Amphipoda, Eurytheneidae n. fam.). Zoosystema, 26 (3), 425–468.
Taylor, M.L.,Gwinnett, C., Robinson, L.F. & Woodall, L.C. (2016) Plastic microfiber ingestion by deep-sea organisms. Scientific Reports, 6, 33997.
https://doi.org/10.1038/srep33997
Thurston, M.H., Petrillo, M. & Della Croce, N. (2002) Population structure of the necrophagous amphipod Eurythenes gryllus (Amphipoda: Gammaridae) from the Atacama Trench (south-east Pacific Ocean). Journal of the Marine Biological Association of the United Kingdom. 82, 205–211.
https://doi.org/10.1017/S0025315402005374
Wesch, C., Elert, A.M., Wörner, M., Braun, U., Klein, R. & Paulus, M. (2017) Assuring quality in microplastic monitoring: About the value of clean-air devices as essentials for verified data. Scientific Reports, 7, 5424.
https://doi.org/10.1038/s41598-017-05838-4
Yang, Z. (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution, 39, 306–314.
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876.
https://doi.org/10.1093/bioinformatics/btt499