Many animals build complex structures to aid in their survival, but very few are built exclusively from materials that animals create 1,2. In the midwaters of the ocean, mucoid structures are readily secreted by numerous animals, and serve many vital functions3,4. However, little is known about these mucoid structures owing to the challenges of observing them in the deep sea. Among these mucoid forms, the ‘houses’ of larvaceans are marvels of nature5, and in the ocean twilight zone giant larvaceans secrete and build mucus filtering structures that can reach diameters of more than 1 m6. Here we describe in situ laser-imaging technology7 that reconstructs three-dimensional models of mucus forms. The models provide high-resolution views of giant larvacean houses and elucidate the role that house structure has in food capture and predator avoidance. Now that tools exist to study mucus structures found throughout the ocean, we can shed light on some of nature’s most complex forms.
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The custom MATLAB code developed as part of this study can be downloaded from our public repository at https://bitbucket.org/mbari/batho3dr.
The data reported in this paper are archived and can be openly accessed using MBARI’s Video Annotation and Reference System (VARS) query tool (https://www.mbari.org/products/research-software/video-annotation-and-reference-system-vars/query-interface/) with the search term ‘Nature20190609559’. In addition, the data that support the findings of this study are available from the corresponding author upon reasonable request.
Hansell, M. Built by Animals: The Natural History of Animal Architecture (Oxford Univ. Press, 2007).
Gosline, J. M., DeMont, M. E. & Denny, M. W. The structure and properties of spider silk. Endeavour 10, 37–43 (1986).
Grutter, A. S., Rumney, J. G., Sinclair-Taylor, T., Waldie, P. & Franklin, C. E. Fish mucous cocoons: the ‘mosquito nets’ of the sea. Biol. Lett. 7, 292–294 (2011).
Gilmer, R. W. Free-floating mucus webs: a novel feeding adaptation for the open ocean. Science 176, 1239–1240 (1972).
Alldredge, A. L. Appendicularians. Sci. Am. 235, 94–105 (1976).
Hamner, W. M. & Robison, B. H. In situ observations of giant appendicularians in Monterey Bay. Deep Sea Res. A 39, 1299–1313 (1992).
Katija, K., Sherlock, R. E., Sherman, A. D. & Robison, B. H. New technology reveals the role of giant larvaceans in oceanic carbon cycling. Sci. Adv. 3, e1602374 (2017).
Ellis, A. E. Innate host defense mechanisms of fish against viruses and bacteria. Dev. Comp. Immunol. 25, 827–839 (2001).
Fol, H. Etudes sur les Appendiculaires du détroit de Messine. Mem. Soc. Phys. Hist. Nat. Geneve 21, 445–499 (1872).
Flood, P. R. Architecture of, and water circulation and flow rate in, the house of the planktonic tunicate Oikopleura labradoriensis. Mar. Biol. 111, 95–111 (1991).
Acuña, J. L., Deibel, D. & Morris, C. C. Particle capture mechanism of the pelagic tunicate Oikopleura vanhoefeni. Limnol. Oceanogr. 41, 1800–1814 (1996).
Flood, P. R. & Deibel, D. in The Biology of Pelagic Tunicates 105–125 (Oxford Univ. Press, 1998).
Landry, M. R., Peterson, W. K. & Fagerness, V. L. Mesozooplankton grazing in the Southern California Bight. I. Population abundances and gut pigment contents. Mar. Ecol. Prog. Ser. 115, 55–71 (1994).
Hopcroft, R. R. & Roff, J. C. Production of tropical larvaceans in Kingston Harbour, Jamaica: are we ignoring an important secondary producer? J. Plankton Res. 20, 557–569 (1998).
Gorsky, G. & Fenaux, R. in The Biology of Pelagic Tunicates 161–169 (Oxford Univ. Press, 1998).
Jaspers, C., Nielsen, T. G., Carstensen, J., Hopcroft, R. R. & Moller, E. F. Metazooplankton distribution across the Southern Indian Ocean with emphasis on the role of larvaceans. J. Plankton Res. 31, 525–540 (2009).
Fernández, D., Lopez-Urrutia, A., Fernández, A., Acuña, J. L. & Harris, R. P. Retention efficiency of 0.2 to 6 μm particles by the appendicularians Oikopleura dioica and Fritillaria borealis. Mar. Ecol. Prog. Ser. 266, 89–101 (2004).
Conley, K. R., Lombard, F. & Sutherland, K. R. Mammoth grazers on the ocean’s minuteness: a review of selective feeding using mucous meshes. Proc. R. Soc. B 285, 20180056 (2018).
Sherlock, R. E., Walz, K. R., Schlining, K. L. & Robison, B. H. Morphology, ecology, and molecular biology of a new species of giant larvacean in the eastern North Pacific: Bathochordaeus mcnutti sp. nov. Mar. Biol. 164, 20 (2017).
Flood, P. R. in Response of Marine Ecosystems to Global Change: Impact of Appendicularians (eds Gorsky, G. et al.) 59–85 (Contemporary Publishing International, 2005).
Sherlock, R. E., Walz, K. R. & Robison, B. H. 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. Mar. Biodivers. Rec. 9, 79 (2016).
Katija, K., Choy, C. A., Sherlock, R. E., Sherman, A. D. & Robison, B. H. From the surface to the seafloor: how giant larvaceans transport microplastics into the deep sea. Sci. Adv. 3, e1700715 (2017).
Silver, M. W., Coale, S. L., Pilskaln, C. H. & Steinberg, D. R. Giant aggregates: importance as microbial centers and agents of material flux in the mesopelagic zone. Limnol. Oceanogr. 43, 498–507 (1998).
Robison, B. H., Reisenbichler, K. R. & Sherlock, R. E. Giant larvacean houses: rapid carbon transport to the deep sea floor. Science 308, 1609–1611 (2005).
Barham, E. G. Giant larvacean houses: observations from deep submersibles. Science 205, 1129–1131 (1979).
Deibel, D. Feeding mechanism and house of the appendicularian Oikopleura vanhoeffeni. Mar. Biol. 93, 429–436 (1986).
Sagane, Y., Hosp, J., Zech, K. & Thompson, E. M. Cytoskeleton-mediated templating of complex cellulose-scaffolded extracellular structure and its association with oikosins in the urochordate Oikopleura. Cell. Mol. Life Sci. 68, 1611–1622 (2011).
Hosp, J., Sagane, Y., Danks, G. & Thompson, E. M. The evolving proteome of a complex extracellular matrix, the Oikopleura house. PLoS ONE 7, e40172 (2012).
Vaugeois, M., Diaz, F. & Carlotti, F. A mechanistic individual-based model of the feeding processes for Oikopleura dioica. PLoS ONE 8, e78255 (2013).
Martí-Solans, J. et al. Oikopleura dioica culturing made easy: a low-cost facility for an emerging animal model in EvoDevo. Genesis 53, 183–193 (2015).
Hopcroft, R. R. & Robison, B. H. A new mesopelagic larvacean, Mesochordaeus erythrocephalus, sp. nov., from Monterey Bay, with a description of its filtering house. J. Plankton Res. 21, 1923–1937 (1999).
Alldredge, A. L. House morphology and mechanisms of feeding in the Oikopleuridae (Tunicata, Appendicularia). J. Zool. 181, 175–188 (1977).
Körner, W. F. Untersuchungen über die gehäusebildung bei appendicularien (Oikopleura dioica Fol). Z. Morphol. Oekol. Tiere 41, 1–53 (1952).
Kishi, K., Hayashi, M., Onuma, T. A. & Nishida, H. Patterning and morphogenesis of the intricate but stereotyped oikoplastic epidermis of the appendicularian, Oikopleura dioica. Dev. Biol. 428, 245–257 (2017).
Conley, K. R., Gemmell, B. J., Bouquet, J.-M., Thompson, E. M. & Sutherland, K. R. A self-cleaning biological filter: how appendicularians mechanically control particle adhesion and removal. Limnol. Oceanogr. 63, 927–938 (2018).
Flood, P. R., Deibel, D. & Morris, C. C. Visualization of the transparent, gelatinous house of the pelagic tunicate Oikopleura vanhoeffeni using sepia ink. Biol. Bull. 178, 118–125 (1990).
Conley, K. R. & Sutherland, K. R. Particle shape impacts export and fate in the ocean through interactions with the globally abundant appendicularian Oikopleura dioica. PLoS ONE 12, e0183105 (2017).
Alldredge, A. L. Field behavior and adaptive strategies of appendicularians (Chordata: Tunicata). Mar. Biol. 38, 29–39 (1976).
Flood, P. R. House formation and feeding behaviour of Fritillaria borealis (Appendicularia: Tunicata). Mar. Biol. 143, 467–475 (2003).
Fenaux, R. Rhythm of secretion of Oikopleurid’s houses. Bull. Mar. Sci. 37, 498–503 (1985).
Purcell, J. E., Sturdevant, M. V. & Galt, C. P. in Response of Marine Ecosystems to Global Change: Impact of Appendicularians (eds Gorsky, G. et al.) 359–435 (Contemporary Publishing International, 2005).
Engelmann, J., Hanke, W., Mogdans, J. & Bleckmann, H. Hydrodynamic stimuli and the fish lateral line. Nature 408, 51–52 (2000).
Janssen, J. & Strickler, J. R. in Communication in Fishes, vol. 1 (eds Ladich, F. et al.) 207–222 (Science Publishers, 2006).
Montgomery, J. C. in The Mechanosensory Lateral Line 561–574 (Springer, 1989).
Batchelor, G. K. An Introduction to Fluid Dynamics (Cambridge Univ. Press, 1967).
We thank D. Graves, C. Kecy, D. Klimov, J. Erickson and MBARI technical staff for their engineering contributions to the development of DeepPIV, the crews of RVs Rachel Carson and Western Flyer, and the pilots of ROVs Doc Ricketts, Ventana and MiniROV for their contributions to this project. This work is a contribution of the Deep Ocean Inspiration Group and was supported by the David and Lucile Packard Foundation.
The authors declare no competing interests.
Peer review information Nature thanks Cornelia Jaspers, Kelly Sutherland and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
a, DeepPIV is used to visualize gelatinous or mucus structures and conduct in situ three-dimensional scanning laser reconstructions using ROV MiniROV. b, Enlarged view of DeepPIV components affixed to the laser housing to generate a laser-sheet and fluorescent-dye field, as well as components to aid in pilot control of the vehicle during ROV deployments. c, MiniROV being launched in Monterey Bay from RV Rachel Carson.
During a single laser sheet scan using DeepPIV, multiple planes (1–5 from dorsal to ventral) are illuminated to reveal different features in the mucus house structure of B. stygius. Scale bars, 4 cm.
Extended Data Fig. 3 The inner and outer house as well as the connective mucus structures of B. stygius.
a, Line drawing of the typical structure of the outer house and inlet channels with embedded inlet filters near the animal trunk. b, c, Overviews of the outer house structure with the animal–house complex oriented downwards (b) and upwards (c). d–f, Magnified views of the two inlet channels connecting laterally to the inner house from outside the outer house looking laterally (d), inside the inlet channel looking laterally (e) and inside the outer house looking dorsally (f).
Extended Data Fig. 4 Three-dimensional reconstructions of mucus and gelatinous structures using DeepPIV.
a–f, White-light illumination (a, c, e) provides two-dimensional snapshots of structures in midwater, where the scanning laser illumination of DeepPIV (b, d, f) can yield three-dimensional reconstructions of floating egg masses (a, b), larvacean bodies (c, d) and other gelatinous or mucus structures such as siphonophore swimming bells (e, f; Desmophyes annectens). Scale bars, 1 cm.
This file contains Supplementary Materials and Methods and Supplementary Table 1.
Video compilation showing a giant larvacean, Bathochordaeus stygius, illuminated by white light and followed by a DeepPIV laser scan with the ROV approaching the inner house dorsally (Table S1, 3DR4). The red lights shown in the white illumination clip correspond to the DeepPIV laser sheet.
Video compilation showing a giant larvacean, B. stygius, illuminated by white light and followed by a DeepPIV laser scan with the ROV approaching the inner house anteriorly (Table S1, 3DR5).
Fly around video showing a 3D reconstructed model (Table S1, 3DR4) of a giant larvacean (black) occupying its inner house. The lateral inlet channels are shown along with the inner house, which includes the inlet filters, suspensory threads, ramp, supply chambers, and food concentrating filters.
Dye visualizations reveal flow through the inner house being driven by the beating giant larvacean tail (Table S1, Batho3).
Compilation of DeepPIV particle videos revealing fluid motion within various features of the giant larvacean inner house.
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Katija, K., Troni, G., Daniels, J. et al. Revealing enigmatic mucus structures in the deep sea using DeepPIV. Nature 583, 78–82 (2020). https://doi.org/10.1038/s41586-020-2345-2
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