Marine Snow: A Brief Historical Sketch

"Marine Snow" is a nearly ubiquitous phenomenon in oceanic waters. The individual particles of marine snow are often fragile, difficult to sample intact, and provide distinctive microenvironments that support unique biological, chemical, and physical processes. Here, I discuss the history of marine snow research, focusing on major discoveries made prior to the end of the 20th century. Researchers from many disciplines have contributed to knowledge of this phenomenon, some of whose work is described here. I also mention aspects of my own studies on marine snow, undertaken with students and colleagues over the years. In the early 1800s, scientific studies of the ocean became possible due to availability of ships that could access the ocean's deep waters. These included voyages of scientific exploration (e.g., collecting animals far below the surface), as well as ocean surveys that served emerging technological needs, such as measuring seafloor depths for laying cable. A key issue, from the perspective of science-oriented researchers, was the question whether life was present in the dark, high-pressure environment below the sunlit zone and, if so, the nature of the food and habitats supporting such life. The first question was convincingly answered by the beginning of the 20th century, whereas the second is still an active area of research, including studies on the role of marine snow in supporting activities of deep ocean communities. Results from voyages early in the 19th century presented evidence of life at great depths. The British Arctic Expedition (1818, led by John Ross) in the northwest Atlantic and sampling by George Aime in waters off Algeria obtained living animals from the seabed at depths of several thousand meters, but their discoveries were not effectively communicated. Indeed, mid-century "findings" argued against life in the deep sea. In the early 1840s, Edward Forbes dredged the ocean floor, recovering live benthic animals to 300 fathoms (approximately 550 m), but found only minimal evidence of life below that depth. He interpreted his results as evidence of a nonsupportive environment: darkness (disallowing food production), high pressure, and low temperatures. This notion of a deep "azoic zone" was generally accepted in the mid 19th century, in spite of the earlier findings. [See Deacon (1997) for an excellent review on this subject.] "It has already been stated that plant-life is limited to the shallow waters, but fishes and members of all the invertebrate groups are distributed over the floor of the ocean at all depths. The majority of these deep-sea animals live by eating the mud, clay, or ooze, or by catching the minute particles of organic matter which fall from the surface." Such a food source, although reasonable to hypothesize, was not documented until well into the next century. "When I think of the floor of the deep sea…I see always the steady, unremitting, downward drift of materials from above, flake upon flake, layer upon layer- the most stupendous "snowfall" the earth has ever seen…" William Beebe and the Bathysphere. Left panel: Beebe looking out of the entrance port of the Bathysphere (image courtesy of the Wildlife Conservation Society). Right panel: The Bathysphere and cables on deck showing the two small windows, one for projecting light out, the other for viewing (© Ned Philibrick Crouch). Several decades after the bathysphere dives of Beebe, in the late 1940s and early 1950s, marine researchers in Japan began the first studies of suspended, mucous-rich particles, ones containing abundant populations of microorganisms. In the more southerly, warmer waters off Japan, the local fishing communities had long been aware of the seasonal presence of mucous-rich particles near or on the ocean's surface. These particles, called "nuta," coated surfaces such as fishing nets and their presence served as a predictor of local fishing conditions (Tsujita 1953). Starting in the late 1940s, Tokimi Tsujita of the Seikai Fisheries Research Laboratory carefully collected the particles from surface waters. He described and drew their contents, aided by both light and electron microscopy, illustrating the matrix and microorganisms embedded in the "suspended organic matter," (Fig. 2). Drawing of near-surface marine snow ("nuta") and its contents, from waters adjacent to the most southerly of the islands of Japan. Image shows phytoplankton and other small organisms (possibly nauplii and Noctiluca) in the marine snow, collected and illustrated in Tsujita's publication from 1953. He described the material as being "formed after explosive multiplication of plankton…" with the contents consisting of a matrix and within it, constituents of the plankton community. His excellent drawings of the material sampled in 1948 resemble materials similar to ones my students collected in central California waters decades later. Summarizing his findings in 1955, ones slightly different from those of his earlier studies, Tsujita (in English, translated from Japanese) stated that "the large forms of the suspended organic matter in the sea are [a product] of microplankton after its death," that is, non-living, decomposing "protoplasm," and possibly related to "leptopel," a phenomenon described below. "Many particles of suspended matter, usually yellowish-white in the reflection of the search-light outside the Chamber, were always observable by naked eye through the window glass of the Chamber, though they were not apparent in the upper layer, shallower than about 10 m depth, probably due to the light background." (Nishizawa et al. 1954) Images from marine snow studies conducted from the Hokkaido fisheries vessel, the Oshio Maru II, and its associated submersible Kuroshio, Hokkaido University, Japan, circa 1953–55, courtesy of Prof. Kajiwara. (a) Prof. Inoue (with hat), returning from a bathysphere dive; (b) the submersible Kuroshio; (c) caged birds serving as air quality monitors; (d) image of marine snow particles taken from the submersible's viewing port. These images were graciously made available to the author from Professor Kajiwara of Hokkaido University, and were compiled from a book "Midget Submarine Kuroshio-go," published by Hokkaido University, 1972. Later, Nishizawa came to work with Gordon Riley in the United States to study the phenomenon Riley called "organic aggregates," which included organic, non-living material of mostly very small dimensions, a major focus of investigations in the west during the next several decades. In the 1950s, interest in non-living, suspended particles was growing in the oceanography community in the west, with researchers using standard oceanographic collection techniques, that is, an open, cylindrical water sampling bottle clamped to a weighted cable, lowered by a winch, closed at the depth of interest, then returned to the ship's deck. Water samples were then withdrawn and subjected to various analyses, including optical measurements of light scattering to study the suspended particles (Jerlov 1955). The methodology—from today's vantage—likely broke the more fragile particles (e.g., marine snow), given vessel motions or when the sample was transferred to a land-based laboratory. Large particles were occasionally noted in the water, and, when viewed with a microscope, sometimes contained recognizable material of biological origin. The name "leptopel" was given to this larger material by Scripps Institution of Oceanography researchers (Fox et al. 1952), who likened leptopel's visual characteristics to those of suspended organic detritus, sometimes even to the "marine snow" described by Japanese divers. Research on particulate matter in the ocean's water column became an important focus for western scientists in the 1960s and 1970s, especially for biology-oriented oceanographers. Their studies included ones on the chemistry, origins, abundance, and size of the particles, and their association with microorganisms. The particles were generally considered biologically "refractive," that is, inert detritus, and their abundance found to be considerably greater than that of living organisms in the water (Parsons and Strickland 1962). The origin of the particles, typically obtained from water sampling bottles, for example, Nansen or later- Niskin - bottles, was of considerable interest. Baylor et al. (1962) experimentally produced such organic particles by bubbling air through Millipore filtered seawater, and Riley (1963) generalized these findings, arguing that the aggregates (from micrometers to several millimeters in dimension) form "mainly by adsorption of dissolved matter on bubbles and other naturally occurring surfaces in the sea," a mechanism later brought into question (Nishizawa 1969). The oceanographic community generally called these particles, "organic aggregates" and suggested they could provide "substrate for bacterial growth and probably food for animals in the water column" (Riley 1963). The importance of such particles as microbial centers of activity was variously regarded, especially for waters at depth. Menzel and Goering (1966) considered particles below the euphotic zone to be refractory, stating that detrital matter below 200 m was remarkably constant in time, space, and depth and "uniformly resistant to decomposition." Contrarily, Pomeroy and Johannes (1968) argued "organic aggregates appear to be the locus of much of the metabolic activity in the ocean, including in the mesopelagic zone (at least to depths of 500 m)." In a comprehensive review, Riley (1970) acknowledged the presence of large amounts of "non-living" particulate material in the sea, noting its occasional role in housing associated microorganisms and even small zooplankton throughout the water column. In the 1960s, a newly popular, largely recreational technology opened avenues to directly observing animal behavior underwater, including that of plankton, though this technology was not much used by marine scientists for that purpose until the 1970s. This development, that is, self contained underwater breathing apparatus (SCUBA), together with wet suits and the popular culture generated by Jacques Cousteau's underwater photography and documentaries, attracted great media attention. I recall, though, that some members of the oceanographic community were dismissive of the style and content of early, popular underwater films made using this technology. The use of SCUBA to observe fragile pelagic animals; however, later led to discoveries of previously unknown feeding behaviors of zooplankton. Specifically, William Hamner and his students collectively discovered fragile, feeding-related mucous structures, mostly previously unknown to science, ones that contained rich populations of food items, for example, Gilmer (1972), Hamner et al. (1975), Alldredge (1976). These structures remained in the water after abandonment by their zooplankton producers, providing habitat for planktonic organisms and representing a special class of "organic aggregates," that is, larger (mm to cm) snow particles, with concentrated populations of microplankton, for example, abandoned larvacean feeding structures (Davoll and Silver 1986). My own field studies on marine snow began when two undergraduate students in my biological oceanography class at the University of California approached me after my lecture describing the Hamner's group discoveries about feeding behaviors of some zooplankton. Alan Shanks and Jon Trent asked whether I would sponsor such SCUBA studies in local (Monterey Bay, California) waters, to which I agreed. After acquiring the diving tools needed for viewing plankton, the students discovered that the presence of abundant marine snow resulted in poor visibility, obscuring the zooplankton they had hoped to study (Fig. 4). We discussed an alternative: to focus instead on the microorganisms on snow particles, researching their contribution to the total number of the same taxa of microorganisms at that depth. Such a task meant we needed to quantify the numbers of snow particles, characterize their associated microbiota, and then make comparisons with the total populations of these organisms collected in bulk-water samples at the site. This led Shanks and Trent to devise quantitative protocols for visually counting the snow particles in transects of known volumes of water (Trent et al. 1978). Additionally, they used plastic medical syringes (removing the tip), to serve as a plunger for hand collecting individual snow particles, as well as collecting large-volume water samples containing the in situ mix of marine snow and "surrounding water" at the site. Their ability to hand collect individual, typically fragile, "snow-sized" particles provided a unique methodology to identify the associated materials and organisms associated with that substrate, as compared with materials and organisms suspended independently in the water. On recovering these samples, I identified and quantified the larger microalgal, protozoan, and other recognizable particles (e.g., fecal pellets) on individual snow particles and those same items in subsamples of bulk water in which the marine snow occurred. This study was the first to quantify, in situ, both the abundance of marine snow particles and snow's contribution to the total community of microorganisms in the water (Silver et al. 1978). Our results showed that marine snow particles were "hotspots" of microorganisms, with concentrations of associated populations up to 3 or 4 orders of magnitude greater than those in water around the particles. Marine snow in Monterey Bay, CA, with diver in background. Photo credit: Alan Shanks. During the late 1900s, many major discoveries were made about marine snow phenomena. Particularly important, to my mind, was evidence provided by Alldredge and Cohen (1987) that marine snow constitutes a unique chemical and physical microhabitat in the water. They found that fecal pellets and flocculent marine snow, carefully collected by hand and returned to the laboratory, had substantial oxygen and pH gradients from their interior to surface (distances of mm). Oxygen sometimes was undetectable in the center of fecal pellets (typically dense particles that are common sources of snow) containing steep chemical gradients to their exterior. In contrast, less compact snow had shallower gradients and measurable oxygen levels throughout. The authors argued that metabolic activities of microorganisms could produce a fundamentally different microenvironment from that outside the particle, thus supporting different types of organisms, and even permitting "processes requiring low oxygen, including denitrification." Another discovery, aided by the use of sediment traps to collect particles sinking through the water, was that particular taxa of microorganisms often were highly concentrated in marine snow, indicating snow's importance as both specialized habitat and potential food source for life at meso- and bathypelagic depths (Silver and Gowing 1991). The presence of marine snow at depth is easily visible if lights are projected into the water, as discovered by Beebe in the Bathysphere in the 1930s. However, the spatial distribution of marine snow in the water was not seriously investigated until late in the 1900s, as doing so required new technologies. Such a study, in which colleagues and I participated (Silver et al., 1998), was enabled by the use of a remotely operated vehicle (ROV), the Ventana (Fig. 5), constructed by the Monterey Bay Aquarium Research Institute (MBARI), and outfitted with a "structured light system." This device projected a horizontal column of light from two angled mirrors, set approximately 2 m forward of the vehicle, allowing the individual particles in the light beam to be videotaped as the ROV advanced slowly forward (Davis and Pilskaln 1998). Calibration using variously sized beads allowed the dimensions of particles in the light beam to be determined. Using this device, we quantified marine snow abundance and size at depths between 40 and 1000 m in a continental margin environment (Monterey Submarine Canyon) off California. Our results showed significant variations in size and abundance of materials over seasons and annual cycles and that the sources of material at depth often differed (Silver et al. 1998). The ROV of the MBARI allows underwater viewing, serving as a real-time device for studying the water column and the seafloor, with a variety of lighting systems and sensors on board. The "structured lighting system" (not shown in this image) made possible three-dimensional measurements of marine snow in the water column. A quick view of studies conducted in the last several decades shows that additional research (not described here) on marine snow is still vibrant, with new technologies providing exciting data and insights about pelagic phenomena previously unknown to science. Clearly, there are many discoveries yet to be made. Some will focus on the microbiota that populates the particles and their unique metabolic activities in situ, as compared with activities of freely suspended microorganisms at the same depth in the sea. Others will elucidate snow's role as a source of food for pelagic animals through the water column, as hypothesized by the early students of this phenomenon. Yet others will consider how snow conveys organisms and materials to the seafloor, where they provide both food and—likely—population inocula for benthic organisms. Hopefully, research on this phenomenon will continue to thrive and be financially supported, as these pelagic "islands" in the water provide a major habitat for aqueous life on the planet. This paper is an outgrowth of a "tutorial" presentation by Professor Silver at the ASLO 2013 Ocean Sciences Meeting. She delivered her talk as part of a special session, "Let It Snow!" organized by Karen Shapiro (University of California, Davis) and Fred Dobbs (Old Dominion University), with contributions from Maille Lyons (Old Dominion University). The author expresses her deep gratitude for the help of John Bower of the University of Hokkaido, Professor in the Faculty of Fisheries, who assisted in locating sources of materials and information from the university. Professor Kajiwara of Hokkaido University graciously gave permission to reprint the image in Figure 3. The author also is extremely grateful for the assistance of Professor Fred Dobbs, who made many useful suggestions for this review.