OceTHE OFFICIALa MAGAZINEn ogOF THE OCEANOGRAPHYra SOCIETYphy CITATION Haddock, S.H.D., L.M. Christianson, W.R. Francis, S. Martini, C.W. Dunn, P.R. Pugh, C.E. Mills, K.J. Osborn, B.A. Seibel, C.A. Choy, C.E. Schnitzler, G.I. Matsumoto, M. Messié, D.T. Schultz, J.R. Winnikoff, M.L. Powers, R. Gasca, W.E. Browne, S. Johnsen, K.L. Schlining, S. von Thun, B.E. Erwin, J.F. Ryan, and E.V. Thuesen. 2017. Insights into the biodiversity, behavior, and bioluminescence of deep-sea organisms using molecular and maritime technology. Oceanography 30(4):38–47, https://doi.org/ 10.5670/oceanog.2017.422. DOI https://doi.org/10.5670/oceanog.2017.422 COPYRIGHT This article has been published in Oceanography, Volume 30, Number 4, a quarterly journal of The Oceanography Society. Copyright 2017 by The Oceanography Society. All rights reserved. USAGE Permission is granted to copy this article for use in teaching and research. Republication, systematic reproduction, or collective redistribution of any portion of this article by photocopy machine, reposting, or other means is permitted only with the approval of The Oceanography Society. Send all correspondence to: [email protected] or The Oceanography Society, PO Box 1931, Rockville, MD 20849-1931, USA. DOWNLOADED FROM HTTP://TOS.ORG/OCEANOGRAPHY CELEBRATING 30 YEARS OF OCEAN SCIENCE AND TECHNOLOGY AT THE MONTEREY BAY AQUARIUM RESEARCH INSTITUTE Insights into the BIODIVERSITY, BEHAVIOR, AND BIOLUMINESCENCE OF DEEP-SEA ORGANISMS Using Molecular and Maritime Technology By Steven H.D. Haddock, Lynne M. Christianson, Warren R. Francis, Séverine Martini, Casey W. Dunn, Philip R. Pugh, Claudia E. Mills, Karen J. Osborn, Brad A. Seibel, C. Anela Choy, Christine E. Schnitzler, George I. Matsumoto, Monique Messié, Darrin T. Schultz, Jacob R. Winnikoff, Meghan L. Powers, Rebeca Gasca, William E. Browne, Sönke Johnsen, Kyra L. Schlining, Susan von Thun, Benjamin E. Erwin, Joseph F. Ryan, and Erik V. Thuesen 38 Oceanography | Vol.30, No.4 ABSTRACT. Since its founding, the Monterey Bay Aquarium Research Institute were devoted to water column research, (MBARI) has pioneered unique capabilities for accessing the deep ocean and its though, were numbered in the dozens inhabitants through focused peer relationships between scientists and engineers. to low hundreds—sufficient for making This focus has enabled breakthroughs in our understanding of life in the sea, leading opportunistic discoveries, but not ideal for to fundamental advances in describing the biology and the ecology of open-ocean experiments or long-term studies. Even and deep-sea animals. David Packard’s founding principle was the application of today with MBARI’s marine operations technological advances to studying the deep ocean, in part because he recognized the and the remotely operated vehicle (ROV) critical importance of this habitat in a global context. Among other fields, MBARI’s dives conducted by other nongovernmen- science has benefited from applying novel methodologies in molecular biology and tal organizations and governmental ocean genetics, imaging systems, and in situ observations. These technologies have allowed exploration programs around the world MBARI’s bioluminescence and biodiversity laboratory and worldwide collaborators to (e.g., NOAA Ship Okeanos Explorer, address centuries-old questions related to the biodiversity, behavior, and bio-optical Ocean Exploration Trust’s E/V Nautilus, properties of organisms living in the water column, from the surface into the deep sea. and Schmidt Ocean Institute’s R/V Falkor; Many of the most interesting of these phenomena are in the midwater domain—the see Oceanography ocean exploration vast region of ocean between the sunlit surface waters and the deep seafloor. supplements at https://tos.org/ ocean- exploration), the combined effort covers a INTRODUCTION hydrozoans), doliolids (sea squirt rela- minute fraction of the massive volume of When the Monterey Bay Aquarium tives), and other key players in water- deep-sea habitat (Figure 1). Research Institute (MBARI) was founded column ecosystems that had otherwise At the time of MBARI’s found- in 1987, the biodiversity of gelatinous not been known, despite centuries of ing, molecular methods were in their deep-sea organisms was mainly known sampling using more destructive meth- relative infancy, with DNA ampli- from trawl-based studies and a few pio- ods. Specialists focused on these poorly fication via polymerase chain reac- neering dives with Woods Hole Ocean- known invertebrates, studying everything tion (PCR) not widely used, and ographic Institution’s Alvin submersible from basic taxonomy (e.g., Pugh, 1992; DNA sequencing achieved only and Harbor Branch Oceanographic Insti- Pugh and Harbison, 1986; Madin and through time-consuming and labor- tution’s Johnson-Sea-Link submersibles. Harbison, 1978) to metabolic rates intensive methods. As an example, the International teams of taxonomists and (Bailey et al., 1995) and bioluminescence gene for the photoprotein aequorin, used ecologists were beginning to appreciate (Herring et al., 1992; Widder et al., 1992; in the bioluminescence systems of some the undocumented species of comb jellies Haddock and Case, 1999). The number jellies, had just been cloned (Prasher et al., (ctenophores), siphonophores (a clade of of dives and sampling opportunities that 1986), and the gene for green-fluorescent VOLUME BY PERCENTAGE 1% 5% 1% Terrestrial (100 m high) FIGURE 1. Perspective of the habitable space Shallow Ocean (<200 m) on the planet differs substantially whether Benthic Ocean (50 m up) area or volume is considered. By area, the Deep Pelagic Ocean ocean indeed covers about 70% of Earth’s sur- 93% face. Factoring in that the average depth of the HABITAT BY AREA ocean is 4,000 m, and considering that the liv- ing space over land is perhaps 100 m high, we find that 98% of the volume of the biosphere is seawater. Of that, the vast majority is the deep, dark ocean below 200 m. The field of deep-sea research has historically focused on organisms living in and on the seafloor—ignoring the kilo- meters of water that lie above. While unfamil- iar to most, this deep water column is a source of nutrients and food for shallow-living species, and home to spectacular biodiversity, massive HABITAT BY VOLUME daily migrations, and processes controlling the cycling and sequestration of carbon. The study of midwater animals can provide unique insights into the evolutionary history of many animals, because most animals there have rel- atives in shallow water or the benthos. Despite its size and global importance, few institutions support research on the midwater environment. Oceanography | December 2017 39 BOX 1. EDUCATION AND OUTREACH IMPACTS The public is often intrigued by observations and research related international venues. The Monterey Bay Aquarium also has been to the remote midwater and open-ocean environments. Anything involved in research collaborations that have resulted in unique we can do to make these habitats and organisms more approach- studies of the origin of luciferin in jellies (Haddock et al., 2001) able and part of the public’s everyday life will have broad socie- and the use of natural fluorescence as a lure for prey (Haddock tal impacts. By shifting public perception of the deep sea from a and Dunn, 2015). Other research collaborations are with the staff frightening and desolate environment to one rich with fascinating of the Monterey Bay National Marine Sanctuary. diversity, we can instill an appreciation of how our fates are inter- Another mechanism for dissemination of our ever-expanding linked and inspire conservation of the ocean and life within. knowledge of deep-ocean biodiversity is MBARI’s Deep-Sea One of the most direct and powerful ways to educate the pub- Guide (http://dsg.mbari.org; https://youtu.be/6-vpezVgD9o). This lic is by producing videos that combine our ROV footage with ani- guide provides public access to the species, data, and concepts mations and scientific information. These videos reach hundreds that have been identified, observed, and collected since MBARI of thousands or millions of viewers, and are widely used as con- was founded. More formally, the software to operate the Video tent in classrooms spanning elementary schools to universities. Annotation and Reference System (VARS; http://mbari.org/vars) is Because many of the organisms and interactions are new to sci- also open source, so that others can use it. entists, they are also novel to the general public, and appeal to our universal fascination with all things strange and wonderful. MBARI also offers in-depth engagement with students, research- ers, and teachers through many participatory programs and fellow- ships. Educational efforts include the summer internship program, the EARTH teacher professional development program, and the Monterey Bay Aquarium WATCH program at local high schools. MBARI’s sister institution, the Monterey Bay Aquarium, Monterey Bay hosts nearly two million visitors per year, and MBARI research, Aquarium Exhibits knowledge, and images have been instrumental in the cre- ation of several popular exhibits, including “Jellies: Living Art,” “Mysteries of the Deep,” “The Jellies Experience,” and their LiveLink auditorium program. MBARI staff have also participated in the creation of exhibits at the Smithsonian Institution National Museum of Natural History, the American Museum of Natural History, the Exploratorium, and other MBARI VIDEO. There’s No Such Thing as a Jellyfish » More than 300,000 views on YouTube SpectorDance – Bioluminescence. Photo credit: W. Roden/New Dawn Studios MBARI VIDEO. The Secret Life of Velella: Adrift with the By-the-Wind Sailor » More than 80,000 views on YouTube 40 Oceanography | Vol.30, No.4 protein (GFP), which would ultimately procedure and database have become the development of the databases does not revolutionize biotechnology and lead to Video Annotation and Reference System mean that annotations have not changed the Nobel Prize in chemistry for its devel- (VARS; Schlining and Jacobsen Stout, over the years. For many species, as we opers, had not yet been isolated (Prasher 2006).