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High concentrations of floating neustonic life in the plastic-rich North Pacific Garbage Patch [1]

['Fiona Chong', 'Energy', 'Environment Institute', 'University Of Hull', 'Hull', 'United Kingdom', 'School Of Environmental Sciences', 'Matthew Spencer', 'University Of Liverpool', 'Liverpool']

Date: 2023-05

Abstract Floating life (obligate neuston) is a core component of the ocean surface food web. However, only 1 region of high neustonic abundance is known so far, the Sargasso Sea in the Subtropical North Atlantic gyre, where floating life provides critical habitat structure and ecosystem services. Here, we hypothesize that floating life is also concentrated in other gyres with converging surface currents. To test this hypothesis, we collected samples through the eastern North Pacific Subtropical Gyre in the area of the North Pacific “Garbage Patch” (NPGP) known to accumulate floating anthropogenic debris. We found that densities of floating life were higher inside the central NPGP than on its periphery and that there was a positive relationship between neuston abundance and plastic abundance for 3 out of 5 neuston taxa, Velella, Porpita, and Janthina. This work has implications for the ecology of subtropical oceanic gyre ecosystems.

Citation: Chong F, Spencer M, Maximenko N, Hafner J, McWhirter AC, Helm RR (2023) High concentrations of floating neustonic life in the plastic-rich North Pacific Garbage Patch. PLoS Biol 21(5): e3001646. https://doi.org/10.1371/journal.pbio.3001646 Academic Editor: Andrew J. Tanentzap, University of Cambridge, UNITED KINGDOM Received: April 8, 2022; Accepted: February 23, 2023; Published: May 4, 2023 Copyright: © 2023 Chong et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the paper and its Supporting Information files. All raw images and processed images are deposited in Zenodo (doi:10.5281/zenodo.7510473; https://zenodo.org/record/7510473). Funding: This work was supported by the United States National Aeronautics and Space Administration grants (80NSSC21K0857 to NM, JH, and RH; 80NSSC17K0559 to NM and JH; and NNX17AH43G to NM and JH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction Marine surface-dwelling organisms (obligate neuston) are a critical ecological link between diverse ecosystems [1], but we know very little about where these organisms are found. Obligate neuston includes multiple cnidarians and mollusks, as well as barnacles, copepods, and algae (Fig 1). All of these taxa are at the nexus of a surface food web that includes diverse sea birds, fish, and turtles. Hundreds of species that live in the water column, seafloor, or even in freshwater spend part of their lifecycle at the ocean’s surface (see review in [1]). As floating organisms, obligate neuston are transported and concentrated by ocean surface currents. PPT PowerPoint slide

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TIFF original image Download: Fig 1. The neustonic organisms represented in this study, based on [ The neustonic organisms represented in this study, based on [ 1 ]. (a) Top-down view of by-the-wind sailor Velella sp. (b) Top-down view of blue button Porpita sp. (c) Side view of Portuguese man-o-war Physalia sp. (d) Side view of violet snail Janthina sp. (e) Top-down view of the blue sea dragons Glaucus sp. Images by Denis Riek. https://doi.org/10.1371/journal.pbio.3001646.g001 Many genera of neuston are globally distributed, but currently only 1 ocean region is known to concentrate neuston into high densities. The Sargasso Sea is named for the neustonic Sargassum algae and is a marine biodiversity hotspot supported by neuston. The Sargasso Sea is critical to the ecology of the North Atlantic and provides millions to billions of US dollars in ecosystem services annually [2,3]. But is the Sargasso Sea the only region of the world’s oceans where floating life concentrates? Plastic pollution, transported by the same surface currents that transport neuston, provides a clue: Large amounts of floating debris are transported to and concentrated in “garbage patches” identified in all 5 main subtropical gyres, including the North Atlantic (the Sargasso Sea), South Atlantic, Indian Ocean, North Pacific, and South Pacific [4,5]. Obligate neuston, subjected to the same oceanographic forces that move buoyant man-made waste and pollutants, may also be concentrated in “garbage patches.” We hypothesize that these regions could be neuston seas, like the Sargasso Sea, and could provide similarly critical ecological and economic roles. Convergence of obligate neustonic life into high densities may be critical for many neustonic species and the organisms that depend on them. Many obligate neuston, including foundational members of the neuston food web, Physalia, Velella, and Porpita, are incapable of swimming or directional movement. Predatory obligate neuston such as the blue sea dragon Glaucus and the violet snails Janthina also lack the ability to direct their movement and must physically bump into prey in order to feed [6,7]. Even more strikingly, Glaucus and possibly some species of Janthina must also be in physical contact to mate [8–10]. These adaptations point to the need for extremely high-density regions in order for these species to survive and reproduce. Some members of the neustonic community may also have adaptations to survive in relatively low nutrient waters (characteristic of many subtropical gyres [11]), including the presence of endosymbiotic zooxanthellae [12], similar to those found in corals (e.g., Velella and Porpita; Fig 1). Neuston are in turn consumed by diverse species [1] that may seek out dense concentrations as feeding grounds [13–15]. Identifying neuston hotspots can provide insights into the ecological dynamics of the wider region. The North Pacific Garbage Patch (NPGP) is the largest and most infamous of the garbage patches [16]. It exists within the North Pacific Subtropical Gyre (NPSG), a massive region characterized in part by comparatively low nutrient densities [17,18]. Diverse neustonic species are documented from the NPSG [19–21], including several species of blue sea dragons (Glaucus spp.) for which this is the type locality [20]. While the NPGP has a dynamic spatial structure and exhibits significant variations temporarily, because it is thousands of miles from shore few surveys of neuston have been performed in this region. To test our hypothesis that subtropical gyres and associated garbage patches may be neuston seas, including the NPGP, we conducted a community science survey through the NPGP with the sailing crew accompanying long-distance swimmer Benoît Lecomte (https://benlecomte.com/) as he swam through the NPGP (The Vortex Swim). The sampling scheme was coordinated through the use of a model that predicted the densities of floating objects. We found increased concentrations of floating life in the NPGP and a positive relationship between the abundance of floating life and floating plastic for 3 out of 5 neuston taxa. Ocean “garbage patches” and other convergence zones may be overlooked areas of high neuston abundance and could serve similar ecological roles to the North Atlantic Sargasso Sea, providing food and habitat for diverse species and valuable economic services. There is an urgent need to better understand these ecosystems and the role of plastic debris.

Discussion Our data suggest higher concentrations of floating life and plastic inside than outside the NPGP, and positive correlations between the logs of neuston concentrations and the log of plastic concentration for 3 out of 5 neuston taxa, Velella, Porpita, and Janthina. The obligate neustonic taxa Velella, Porpita, and Janthina may be concentrated by the same physical forces that concentrate plastic within the region and these concentrations may be important for the ecology of these species. A limited number of studies have examined obligate neuston in this region, so it is difficult to infer processes and patterns by comparing them, especially because neuston concentrations in this region may vary seasonally or annually. Nevertheless, the possible overlap between garbage patches and neuston seas has important implications for established and emerging high seas impacts and activities. Physical forces may be partly responsible for our observed distribution and abundance of obligate neuston, and these concentrations may be important for neuston life history. Physical forces are responsible for the high concentration of plastics in the NPGP [32], and in the North Atlantic subtropical gyre are responsible for concentrating neustonic Sargassum algae in the Sargasso Sea [33]. Within our study, a patchy distribution of neuston and plastic at the surface may be due to small-scale (sub-mesoscale) physical surface dynamics such as slicks. We found the highest concentration of both neuston and plastic in a slick (observation SJR_019), and this is true for other studies as well. For example, off the coast of the island of Hawai'i, nearly 40% of surface-associated larval fish, 26% of surface invertebrates, and 95.7% of plastic were found in surface slicks, which represented only 8% of the sea surface area of the West Hawai'i study region [13–14]. In the North Atlantic, neustonic Sargassum is often concentrated in slicks under appropriate conditions [34,35]. Sea surface slicks create a relatively small area where diverse species come into physical contact through drifting. Because neustonic predators such as Janthina and Glaucus, both found in our study, rely on physically contacting prey [1,6,36,37], and similarly Glaucus spp. and likely some members of the genus Janthina depend on direct physical contact to mate [8–10], regional concentrations and small-scale surface slicks may be an important habitat feature for neustonic organisms. In our study, we found evidence that obligate neuston may also be reproducing in the NPGP: in at least 1 sample, we found many small Velella roughly 0.5 cm in length and Janthina sp. and Porpita sp. less than 1 mm in length. Based on a growth estimate for Velella, the small Velella in our sample may be approximately 5 to 16 days old [38]. More and better data will be needed before strong conclusions can be drawn about neuston distributions in the NPGP, and methodological differences may account for some of the apparent differences in results between this study and Egger and colleagues [21]. The ad hoc study design for our data, common to many community science projects, is a weakness. Randomized sampling is logistically difficult in this environment, but lattice designs may be feasible and are often considered suitable for the study of spatial patterns [39]. It will also be important to ensure that enough objects of interest are collected. In both studies, there was little information on relationships between neuston and plastic for taxa with low counts (and in the Egger and colleagues [21] data, the median count was zero for every taxon). Future work should also account for spatial structure in the sampling design. Our analyses assumed independent and identically distributed observation-level random effects. Where observations are clustered in space (as in some of the data used by Egger and colleagues [21], where most of the observations consisted of sets of 3 trawls very close together), a hierarchical error structure could account for this clustering. More generally, a spatially structured covariance model such as a Matérn function [39], possibly based on distances from a transport model rather than Euclidean distance, might be appropriate. We did not pursue these ideas here because the low sample sizes and (in the case of the Egger and colleagues [21]) low counts would make estimation difficult. Additionally, different counting approaches should be evaluated. We modeled the photographic sampling process used in our study, but because there was little information in the data on detectability, we cannot say much about absolute densities. On the other hand, the process of freezing, shipping, and then counting samples used by Egger and colleagues [21] might reduce the counts of soft-bodied species relative to hard-bodied organisms (R. Helm, personal observation). Immediate counting of fresh samples may be the most reliable method, where possible. Direct comparison of these approaches before designing future studies would be useful. We expect neuston abundance to vary over time, due to differences in morphology, anatomy, sizes, and life history of individuals and species. For example, we observed higher densities of Velella within the patch, while for the Egger and colleagues [21] data, higher densities of Velella were found outside the patch. However, Velella come in 2 different forms, with sails that either tilt to the left (NW-type) or right (SW-type). Savilov [19] observed a higher abundance of NW type Velella outside the patch and SW type Velella inside the patch, meaning that the observations of Egger and colleagues [21] may have sampled 2 morphologically different Velella populations. Neither our study nor Egger and colleagues [21] examined orientation type, though this may be an important biological difference for Velella. For Janthina, both studies found higher densities in and around the patch than outside it. Janthina, like small plastics, is likely not moved by the wind to the same degree as the wind-harnessing Velella, and this may be why both studies observed Janthina inside the NPGP. Future studies also need to account for seasonal variation. For example, we already know that there are seasonal aggregations of Velella off the coast of California [40], but know much less about within-patch seasonality. Differences in observed neuston abundance between studies could also be due to interannual variability. In our study, a regional chlorophyll bloom occurred in the NPSG near our sampling, and although our sampling did not overlap with this observed bloom, this increased primary productivity in the subtropical gyre may be related to our comparatively high observed neuston densities [41]. Neuston may also interact with plastic in the patch or with communities growing on plastic. For example, the sea skater insect Halobates may increase in abundance due to the presence of plastic, on which it lays its eggs [42]. Rafting organisms [43], which grow on large plastic debris, may also interact with obligate neuston, though it is not clear yet what the nature of these interactions may be. Neuston may also consume microplastics, similar to rafting barnacles [44], though this has not been documented for neuston, and the effects, if any, may be challenging to detect. Regardless, the impact of plastic on the surface environment in this region is worth future study. Our findings suggest that subtropical gyres and other areas of high plastic concentration may be more than just garbage patches, and that these regions may serve important ecosystem functions as “neuston seas.” Obligate neuston are present in the diet of a variety of species, including those that are known to ingest plastic, such as sea turtles [45,46] and the Laysan albatross [47]. In the North Atlantic Sargasso Sea, the neustonic ecosystem is a feeding ground, a nursery ground, and a habitat [15]. Similar to the Sargasso Sea, our results suggest the central NPGP has high surface life densities relative to surrounding waters, yet much is still unknown about the ecology of these organisms. Studies on the food webs and life history of neustonic species will allow us to better understand their temporal cycles and connectivity. It is also important for high seas industries and emerging high sea activities to consider their impacts on the ocean’s surface ecosystem [48]. Lastly, our study highlights the value of community science and its importance in studying life at the air–sea interface.

Acknowledgments We thank Ben Lecomte and the crew of the Vortex Swim for generously providing us with an opportunity to collect samples, and Dr. Sara-Jeanne Royer and Dr. Kara Lavender Law for providing the trawls. We would like to thank the organizers and attendees of the “The Ocean Cleanup Symposium 2019” at the University of Liverpool Institute for Risk and Uncertainty.

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001646

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