Oceanography The Official Magazine of
The Oceanography Society
Volume 30 Issue 04

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Volume 30, No. 4
Pages 26 - 37

The Coevolution of Midwater Research and ROV Technology at MBARI

Bruce H. Robison Kim R. ReisenbichlerRob E. Sherlock
Article Abstract

Coevolution is a process through which two interactive systems mutually influence each other’s development. Midwater research and remotely operated vehicle technology are two such interactive systems, and at the Monterey Bay Aquarium Research Institute they have been coevolving for 30 years. As the technology has matured, the scope, scale, and complexity of the research has also advanced, particularly in such areas as observing animal behavior and in situ experimentation, which were virtually impossible before we gained direct access to the environment. Here we examine midwater research domains and the technologies that enable them: how new instrumentation enables in situ respiration and fluid dynamics measurements; how imaging and data handling systems build data sets that allow long-term analyses of seasonal, episodic, and anthropogenic environmental changes; and how variable ballast and thruster controls have allowed us to make close-up observations and conduct delicate experimental manipulations without disturbing the animals we are studying. The coevolution continues and future developments will focus on integrating diverse sensor systems to provide new perspectives for midwater ecology, and on automating research processes to expand the scale of operations, improve efficiency, and promote technology transfer.

Citation

Robison, B.H., K.R. Reisenbichler, and R.E. Sherlock. 2017. The coevolution of midwater research and ROV technology at MBARI. Oceanography 30(4):26–37, https://doi.org/10.5670/oceanog.2017.421.

References

Alldredge, A.L., B.H. Robison, A. Fleminger, J.J. Torres, J.M. King, and W.M. Hamner. 1984. Direct sampling and in situ observation of a persistent copepod aggregation in the mesopelagic zone of the Santa Barbara Basin. Marine Biology 80:75–81, https://doi.org/10.1007/BF00393130.

Barham, E.G. 1957. The Ecology of Sonic Scattering Layers in the Monterey Bay Area. PhD thesis, Stanford University, Palo Alto, CA.

Bigelow, H.B., and M. Leslie. 1930. Reconnaissance of the waters and plankton of Monterey Bay, July 1928. Bulletin of the Museum of Comparative Zoology at Harvard College 52:430–581.

Bolin, R.L. 1964. Hydrographic data from the area of the Monterey Submarine Canyon, 1951–1955. Final Report, Stanford University, Hopkins Marine Station, Pacific Grove, CA, 12 pp

Burford, B.P., B.H. Robison, and R.E. Sherlock. 2015. Behaviour and mimicry in the juvenile and subadult life stages of the mesopelagic squid Chiroteuthis calyx. Journal of the Marine Biological Association of the United Kingdom 95:1,221–1,235, https://doi.org/​10.1017/S0025315414001763.

Bush, S.L. 2012. Economy of arm autotomy in the mesopelagic squid Octopoteuthis deletron. Marine Ecology Progress Series 458:133–140, https://doi.org/​10.3354/meps09714.

Bush, S.L., H.J.T. Hoving, C.L. Huffard, B.H. Robison, L.D. Zeidberg 2012. Brooding and sperm storage by the deep-sea squid Bathyteuthis berryi (Cephalopoda: Decapodiformes). Journal of the Marine Biological Association of the United Kingdom 92:1,629–1,636, https://doi.org/10.1017/S0025315411002165.

Bush, S.L., and B.H. Robison. 2007. Ink utilization by mesopelagic squid. Marine Biology 152:485–494, https://doi.org/10.1007/s00227-007-0684-2.

Bush, S.L., B.H. Robison, and R.L. Caldwell. 2009. Behaving in the dark: Locomotor, chromatic, postural, and bioluminescent behaviors of the deep-sea squid Octopoteuthis deletron Young 1972. Biological Bulletin 216:7–22, https://doi.org/10.1086/BBLv216n1p7.

Choy, C.A., S.H.D. Haddock, and B.H. Robison. 2017. Deep pelagic food web structure as revealed by in situ feeding observations. Proceedings of the Royal Society B 284:20172116, https://doi.org/10.1098/rspb.2017.2116.

Drazen, J.C., and B.H. Robison. 2004. Direct observations of the association between a deep-sea fish and a giant scyphomedusa. Marine and Freshwater Behaviour and Physiology 37(3):209–214, https://doi.org/10.1080/10236240400006190.

Ehrlich, P.R., and P.H. Raven. 1964. Butterflies and plants: A study in coevolution. Evolution 18:586–608, https://doi.org/​10.1111/​j.1558-5646.1964.tb01674.x.

Gilly, W.F., J.M. Beman, S.Y. Litvin, and B.H. Robison. 2013. Oceanographic and biological effects of shoaling of the oxygen minimum zone. Annual Review of Marine Science 5:393–420, https://doi.org/​10.1146/annurev-marine-120710-100849.

Haddock, S.H.D. 2004. A golden age of gelata: Past and future research on planktonic ctenophores and cnidarians. Hydrobiologia 530/531:549–556, https://doi.org/10.1007/s10750-004-2653-9.

Haddock, S.H.D., T.J. Rivers, and B.H. Robison. 2001. Can coelenterates make coelenterazine? Dietary requirement for luciferin in cnidarian bioluminescence. Proceedings of the National Academy of Sciences of the United States of America 98(20):11,148–11,151, https://doi.org/10.1073/pnas.201329798.

Hamner, W.M., and B.H. Robison. 1992. In situ observations of giant appendicularians in Monterey Bay. Deep Sea Research 39:1,299–1,313, https://doi.org/​10.1016/0198-0149(92)90070-A.

Harbison, G.R., G.I. Matsumoto, and B.H. Robison. 2001. Lampocteis cruentiventer gen. nov., sp. nov.: A new mesopelagic lobate ctenophore, representing the type of a new family (Phylum Ctenophora (Class Tenticulata, Order Lobata, Family Lampoctenidae, fam. nov.). Bulletin of Marine Science 68:299–311.

Hopcroft, R.R., and B.H. Robison. 1999. A new mesopelagic larvacean, Mesochordaeus erythrocephalus, sp. nov., from Monterey Bay, with a description of its filtering house. Journal of Plankton Research 21:1,923–1,937, https://doi.org/10.1093/plankt/21.10.1923.

Hoving, H.J.T., S.L. Bush, and B.H. Robison. 2012. A shot in the dark: Same-sex sexual behavior in a deep-sea squid. Biology Letters 8(2):287–290, https://doi.org/10.1098/rsbl.2011.0680.

Hoving, H.J.T., V.V. Laptikhovsky, and B.H. Robison. 2015. Vampire squid reproductive strategy is unique among coleoid cephalopods. Current Biology 25(8):R322–R323, https://doi.org/10.1016/​j.cub.2015.02.018.

Hoving, H.J.T., and B.H. Robison. 2012. Vampire squid: Detritivores in the oxygen minimum zone. Proceedings of the Royal Society B 279(1747):4,559–4,567, https://doi.org/​10.1098/rspb.2012.1357.

Hoving, H.J.T., and B.H. Robison. 2016. Deep-sea in situ observations of gonatid squid and their prey reveal high occurrence of cannibalism. Deep Sea Research Part I 116:94–98, https://doi.org/10.1016/​j.dsr.2016.08.001.

Hoving, H.J.T., and B.H. Robison. 2017. The pace of life in deep dwelling squids. Deep Sea Research Part I 126:40–49, https://doi.org/10.1016/j.dsr.​2017.05.005.

Hoving, H.J.T., L.D. Zeidberg, M.C. Benfield, S.L. Bush, M. Vecchione, and B.H. Robison. 2013. First in situ observations of the rare deep-sea squid Grimalditeuthis bonplandi reveal unique use of tentacles. Proceedings of the Royal Society B 280:20131436, https://doi.org/10.1098/rspb.2013.1463.

Hull, P.M., K.J. Osborn, R.D. Norris, and B.H. Robison. 2011. Seasonality and depth distribution of a mesopelagic foraminifer, Hastigerinella digitata, in Monterey Bay, California. Limnology and Oceanography 56(2):562–576, https://doi.org/​10.4319/lo.2011.56.2.0562.

Hunt, J.C., L. Zeidberg, W.M. Hamner, and B.H. Robison. 2000. The behavior of Loligo opalescens (Mollusca: Cephalopoda) as observed by a remotely operated vehicle. Journal of the Marine Biological Association of the United Kingdom 80:873–883.

Irigoien, X., T.A. Klevjer, A. Rostad, U. Martinez, G. Boyra, J.L. Acuña, A. Bode, F. Echevarria, J.I. Gonzales-Gordillo, S. Hernandez-Leon, and others. 2014. Large mesopelagic fishes biomass and trophic efficiency in the open ocean. Nature Communications 5, 3721, https://doi.org/10.1038/ncomms4271.

Katija, K., C.A. Choy, R.E. Sherlock, A.D. Sherman, and B.H. Robison 2017a. From the surface to the seafloor: How giant larvaceans transport microplastics into the deep sea. Science Advances 3(8):e1700715, https://doi.org/10.1126/sciadv.1700715.

Katija, K., R.E. Sherlock, A.D. Sherman, and B.H. Robison. 2017b. New technology reveals the role of giant larvaceans in oceanic carbon cycling. Science Advances 3(5):e1602374, https://doi.org/​10.1126/sciadv.1602374.

Kirkwood, W.J., M. Chaffey, E. Mellinger, D. Au, S. Etchemendy, and B.H. Robison. 2009. An ocean research platform: ROV Tiburon. The Journal of Ocean Technology 4(1):16–30.

Matsumoto, G.I., and B.H. Robison. 1992. Kiyohimea usagi, a new species of lobate ctenophore from the Monterey Submarine Canyon. Bulletin of Marine Science 51:19–29.

Moynihan, M. 1985. Why are cephalopods deaf? The American Naturalist 125(3):465–469, https://doi.org/​10.1086/284353.

Newman, J.B., and B.H. Robison. 1993. Development of a dedicated ROV for ocean science. Marine Technology Society Journal 26:46–53.

Osborn, K.J. 2008. Phylogenetics and Ecology of Pelagic Munnopsid Isopods (Crustacea Asellota). PhD dissertation, UC Berkeley, Berkeley, CA, UMI Microform 3306283.

Osborn, K.J., S.H.D. Haddock, F. Pleijel, L.P. Madin and G.W. Rouse. 2009. Deep-sea swimming worms with luminescent “bombs. Science 325:964, https://doi.org/10.1126/science.1172488.

Osborn, K.J., G.W. Rouse, S.K. Goffredi, and B.H. Robison. 2007. Description and relationships of Chaetopterus pugaporcinus, an unusual pelagic polychaete (Annelida, Chaetopteridae). The Biological Bulletin 212(1):40–54, https://doi.org/​10.2307/25066579.

Packard, D. 1989. Welcoming remarks to The Oceanography Society at its inaugural meeting. Oceanography 2(2):46–47, http://doi.org/10.5670/oceanog.1989.15.

Pugh, P.R. 1989. Gelatinous zooplankton—the forgotten fauna. Progress in Underwater Science 14:67–78.

Raskoff, K.A. 2001. The impact of El Niño events on populations of mesopelagic hydromedusae. Hydrobiologia 451:121–129, https://doi.org/​10.1007/978-94-010-0722-1_11.

Reisenbichler K.R., M.R. Chaffey, F. Cazaneve, R. McEwen, R. Henthorn, R.E. Sherlock, and B.H. Robison. 2016. Automating MBARI’s midwater time-series video surveys: The transition from ROV to AUV. Pp. 3,027–3,035 in Proceedings, MTS IEEE Oceans 2016 Conference, September 19–23, 2016, Monterey, CA, https://doi.org/10.1109/oceans.2016.7761499.

Reisenbichler, K.R., and B.H. Robison 1991. Deep sea diving from an armchair: Using an ROV for mesopelagic research. Pp. 75–78 in Proceedings, AAUS, 11th Annual Symposium, Honolulu, HI.

Robison, B.H. 1972. Distribution and Ecology of the Midwater Fishes of the Eastern North Pacific Ocean. PhD dissertation. Stanford University, Palo Alto, CA.

Robison, B.H. 1983. Midwater biological research with the WASP ADS. Marine Technology Society Journal 17:21–27.

Robison, B.H. 1993. Midwater research methods with MBARI’s ROV. Marine Technology Society Journal 26:32–39.

Robison, B.H. 1999. Shape change behavior by mesopelagic animals. Marine and Freshwater Behaviour and Physiology 32:17–25, https://doi.org/​10.1080/​10236249909379034.

Robison, B.H. 2000. The coevolution of undersea vehicles and deep-sea research. Marine Technology Society Journal 33:65–73.

Robison, B.H. 2004. Deep pelagic biology. Journal of Experimental Marine Biology and Ecology 300(1–2):253–272, https://doi.org/10.1016/​j.jembe.2004.01.012.

Robison, B.H. 2009. Conservation of deep pelagic biodiversity. Conservation Biology 23:847–858.

Robison, B.H., K.R. Reisenbichler, J.C. Hunt, and S.H.D. Haddock. 2003. Light production by the arm tips of the deep-sea cephalopod Vampyroteuthis infernalis. Biological Bulletin 205(2):102–109, https://doi.org/10.2307/1543231.

Robison, B.H., K.A. Raskoff, and R.E. Sherlock. 2005a. Adaptations for living deep: A new bathypelagic doliolid, from the eastern North Pacific. Journal of the Marine Biological Association of the United Kingdom 85(3):595–602, https://doi.org/10.1017/S0025315405011525.

Robison, B.H., K.R. Reisenbichler, and R.E. Sherlock. 2005b. Giant larvacean houses: Rapid carbon transport to the deep sea floor. Science 308:1,609-1,611, https://doi.org/10.1126/science.1109104.

Robison, B.H., K.R. Reisenbichler, R.E. Sherlock, J.M.B. Silguero, and F.P. Chavez. 1998. Seasonal abundance of the siphonophore, Nanomia bijuga, in Monterey Bay. Deep Sea Research Part II 45(8–9):1,741–1,751, https://doi.org/10.1016/S0967-0645(98)80015-5.

Robison, B.H., R.E. Sherlock, and K.R. Reisenbichler. 2010. The bathypelagic community of Monterey Canyon. Deep Sea Research Part II 57(16):1,551–1,556, https://doi.org/10.1016/​j.dsr2.2010.02.021.

Schlining, B.M., and N.J. Stout. 2006. MBARI’s Video annotation and reference system. Pp. 1–5 in Proceedings of the Marine Technology Society/Institute of Electrical and Electronics Engineers Oceans Conference, September 18–21, 2006, Boston, MA, https://doi.org/10.1109/oceans.2006.306879.

Seibel, B.A., B.H. Robison, and S.H.D. Haddock. 2005. Post-spawning egg care by a squid. Nature 438:929, https://doi.org/10.1038/438929a.

Sherlock, R.E., and B.H. Robison. 2000. Effects of temperature on the development and survival of Nanomia bijuga (Hydrozoa, Siphonophora). Invertebrate Biology 119(4):379–385, https://doi.org/​10.1111/j.1744-7410.2000.tb00106.x.

Sherlock, R.E., K.R. Walz, and B.H. Robison. 2016. The first definitive record of the giant larvacean, Bathochordaeus charon, since its original description in 1900 and a range extension to the northeast Pacific Ocean. Marine Biodiversity Records 9(79):1–10, https://doi.org/10.1186/s41200-016-0075-9.

Sherlock, R.E., K.R. Walz, K.L. Schlining, and B.H. Robison. 2017. Morphology, ecology, and molecular biology of a new species of giant larvacean in the eastern North Pacific: Bathochordaeus mcnutti sp. nov. Marine Biology 164:20, https://doi.org/10.1007/s00227-016-3046-0.

Silguero, J.M.B., and B.H. Robison. 2000. Seasonal abundance and vertical distribution of mesopelagic calycophoran siphonophores in Monterey Bay, CA. Journal of Plankton Research 22:1,139–1,153, https://doi.org/10.1093/plankt/22.6.1139.

Skikne, S.A., R.E. Sherlock, and B.H. Robison. 2009. Uptake of dissolved organic matter by ephyrae of two species of scyphomedusae. Journal of Plankton Research 31(12):1,563–1,570, https://doi.org/10.1093/plankt/fbp088.

Skogsberg, T. 1936. Hydrography of Monterey Bay, California. Thermal conditions. Transactions of the American Philosophical Society N.S. 29:1–152.

Skogsberg, T., and A. Phelps. 1946. Hydrography of Monterey Bay, California. Thermal conditions, Part II (1934–1937). Proceedings of the American Philosophical Society 90(5):350–386, https://doi.org/​10.2307/1005510.

Stewart, J.S., E.L. Hazen, S.J. Bograd, J.E.K. Byrnes, D.G. Foley, W.F. Gilly, B.H. Robison, and J.C. Field. 2014. Combined climate- and prey-mediated range expansion of Humboldt squid (Dosidicus gigas), a large marine predator in the California Current System. Global Change Biology 20(6):1,832–1,843, https://doi.org/10.1111/gcb.12502.

Swift, H.F., W.M. Hamner, B.H. Robison and L.P. Madin. 2009. Feeding behavior of the ctenophore Thalassocalyce inconstans: Revision of anatomy of the order Thalassocalycida. Marine Biology 156:1,049–1,056, https://doi.org/10.1007/s00227-009-1149-6.

Tamburri, M.N., M.N. Halt, and B.H. Robison. 2000. Chemically regulated feeding by a midwater medusa. Limnology and Oceanography 45(7):1,661–1,666, https://doi.org/10.4319/lo.2000.45.7.1661.

Trueblood, L.A., S. Zylinski, B.H. Robison, and B.A. Seibel. 2015. An ethogram of the Humboldt squid Dosidicus gigas Orbigny (1835) as observed from remotely operated vehicles. Behaviour 152(14):1,911–1,932, https://doi.org/​10.1163/1568539X-00003324.

Vecchione, M., B.H. Robison, and C.F.E. Roper. 1992. A tale of two species: Tail morphology in paralarval Chiroteuthis. Proceedings of the Biological Society of Washington 105:683–692.

Widder, E.A., S.A. Bernstein, D.F. Bracher, J.F. Case, K.R. Reisenbichler, J.J. Torres, and B.H. Robison. 1989. Bioluminescence in the Monterey Submarine Canyon: Image analysis of video recordings from a midwater submersible. Marine Biology 100(4):541–551, https://doi.org/10.1007/BF00394831.

Widder, E.A., B.H. Robison, K.R. Reisenbichler and S.H.D. Haddock. 2005. Using red light for in situ observations of deep-sea fishes. Deep Sea Research Part I 52:2,077–2,085, https://doi.org/​10.1016/j.dsr.2005.06.007.

Youngbluth, M.J. 1984. Manned submersibles and sophisticated instrumentation: tools for oceanographic research. Pp.335–344 in Proceedings of SUBTECH, 1983, The Society for Underwater Technology, November 15–17, London, England.

Zeidberg, L.D., and B.H. Robison. 2007. Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proceedings of the National Academy of Sciences of the United States of America 104(31):12,948–12,950, https://doi.org/10.1073/pnas.0702043104.