Toward a Coordinated Global Observing System for Seagrasses and Marine Macroalgae
Abstract
In coastal waters around the world, the dominant primary producers are benthic macrophytes, including seagrasses and macroalgae, that provide habitat structure and food for diverse and abundant biological communities and drive ecosystem processes. Seagrass meadows and macroalgal forests play key roles for coastal societies, contributing to fishery yields, storm protection, biogeochemical cycling and storage, and important cultural values. These socio-economically valuable services are threatened worldwide by human activities, with substantial areas of seagrass and macroalgal forests lost over the last half-century. Tracking the status and trends in marine macrophyte cover and quality is an emerging priority for ocean and coastal management, but doing so has been challenged by limited coordination across the numerous efforts to monitor macrophytes, which vary widely in goals, methodologies, scales, capacity, governance approaches, and data availability. Here, we present a consensus assessment and recommendations on the current state of and opportunities for advancing global marine macrophyte observations, integrating contributions from a community of researchers with broad geographic and disciplinary expertise. With the increasing scale of human impacts, the time is ripe to harmonize marine macrophyte observations by building on existing networks and identifying a core set of common metrics and approaches in sampling design, field measurements, governance, capacity building, and data management. We recommend a tiered observation system, with improvement of remote sensing and remote underwater imaging to expand capacity to capture broad-scale extent at intervals of several years, coordinated with stratified in situ sampling annually to characterize the key variables of cover and taxonomic or functional group composition, and to provide ground-truth. A robust networked system of macrophyte observations will be facilitated by establishing best practices, including standard protocols, documentation, and sharing of resources at all stages of workflow, and secure archiving of open-access data. Because such a network is necessarily distributed, sustaining it depends on close engagement of local stakeholders and focusing on building and long-term maintenance of local capacity, particularly in the developing world. Realizing these recommendations will produce more effective, efficient, and responsive observing, a more accurate global picture of change in vegetated coastal systems, and stronger international capacity for sustaining observations
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SYSTEMATIC REVIEW published: 04 July 2019 doi: 10.3389/fmars.2019.00317 Frontiers in Marine Science | www.frontiersin.org 1July 2019 | Volume 6 | Article 317 Edited by: Christos Dimitrios Arvanitidis, Hellenic Centre for Marine Research (HCMR), Greece Reviewed by: Sotiris Orfanidis, Institute of Fisheries Research, Greece Luigi Piazzi, University of Sassari, Italy *Correspondence: J. Emmett Duffy [email protected] Specialty section: This article was submitted to Marine Ecosystem Ecology, a section of the journal Frontiers in Marine Science Received: 07 November 2018 Accepted: 27 May 2019 Published: 04 July 2019 Citation: Duffy JE, Benedetti-Cecchi L, Trinanes J, Muller-Karger FE, Ambo-Rappe R, Boström C, Buschmann AH, Byrnes J, Coles RG, Creed J, Cullen-Unsworth LC, Diaz-Pulido G, Duarte CM, Edgar GJ, Fortes M, Goni G, Hu C, Huang X, Hurd CL, Johnson C, Konar B, Krause-Jensen D, Krumhansl K, Macreadie P, Marsh H, McKenzie LJ, Mieszkowska N, Miloslavich P, Montes E, Nakaoka M, Norderhaug KM, Norlund LM, Orth RJ, Prathep A, Putman NF, Samper-Villarreal J, Serrao EA, Short F, Pinto IS, Steinberg P, Stuart-Smith R, Unsworth RKF, van Keulen M, van Tussenbroek BI, Wang M, Waycott M, Weatherdon LV, Wernberg T and Yaakub SM (2019) Toward a Coordinated Global Observing System for Seagrasses and Marine Macroalgae. Front. Mar. Sci. 6:317. doi: 10.3389/fmars.2019.00317 Toward a Coordinated Global Observing System for Seagrasses and Marine Macroalgae J. Emmett Duffy1*, Lisandro Benedetti-Cecchi2, Joaquin Trinanes3,4,5, Frank E. Muller-Karger6, Rohani Ambo-Rappe7, Christoffer Boström8, Alejandro H. Buschmann9, Jarrett Byrnes10, Robert G. Coles 11, Joel Creed12, Leanne C. Cullen-Unsworth13, Guillermo Diaz-Pulido 14, Carlos M. Duarte15, Graham J. Edgar16, Miguel Fortes 17, Gustavo Goni18, Chuanmin Hu 6, Xiaoping Huang 19, Catriona L. Hurd20, Craig Johnson 16, Brenda Konar21, Dorte Krause-Jensen 22,23, Kira Krumhansl24, Peter Macreadie 25, Helene Marsh26, Len J. McKenzie 27, Nova Mieszkowska28, Patricia Miloslavich 20,29, Enrique Montes6, Masahiro Nakaoka30, Kjell Magnus Norderhaug31, Lina M. Norlund32, Robert J. Orth 33, Anchana Prathep34, Nathan F. Putman35, Jimena Samper-Villarreal 36, Ester A. Serrao37, Frederick Short 38, Isabel Sousa Pinto39, Peter Steinberg40, Rick Stuart-Smith 16, Richard K. F. Unsworth41, Mike van Keulen42, Brigitta I. van Tussenbroek43, Mengqiu Wang6, Michelle Waycott44, Lauren V. Weatherdon45, Thomas Wernberg46 and Siti Maryam Yaakub47 1Smithsonian Institution, Edgewater, MD, United States, 2Department of Biology, University of Pisa and CoNISMa, Pisa, Italy, 3Instituto de Investigaciones Tecnoloxicas, Universidade de Santiago de Compostela, Santiago, Spain, 4Physical Oceanography Division, Atlantic Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration, Miami, FL, United States, 5Rosenstiel School of Marine and Atmospheric Sciences, Cooperative Institute for Marine and Atmospheric Studies, University of Miami, Miami, FL, United States, 6College of Marine Science, University of South Florida, St. Petersburg, FL, United States, 7Department of Marine Science, Hasanuddin University, Makassar, Indonesia, 8Faculty of Science and Engineering, Environmental and Marine Biology, Åbo Akademi University, Turku, Finland, 9Centro i-mar and Centro de Biotecnología y Bioingeniería (CeBiB), Universidad de Los Lagos, Puerto Montt, Chile, 10 Department of Biology, University of Massachusetts Boston, Boston, MA, United States, 11 Centre for Tropical Water and Aquatic Ecosystem Research, James Cook University, Douglas, QLD, Australia, 12 Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil, 13 Sustainable Places Research Institute, Cardiff University, Cardiff, United Kingdom, 14 School of Environment and Science, and Australian Rivers Institute, Coast and Estuaries, Griffith University, Brisbane, QLD, Australia, 15 Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia, 16 University of Tasmania, Hobart, TAS, Australia, 17 Marine Science Institute CS, University of the Philippines, Quezon, Philippines, 18 Atlantic Oceanographic and Meteorological Laboratory (AOML), National Oceanic and Atmospheric Administration, Miami, FL, United States, 19 South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China, 20 Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia, 21 College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, AK, United States, 22 Department of Bioscience, Aarhus University, Silkeborg, Denmark, 23 Arctic Research Centre, Aarhus University, Aarhus, Denmark, 24 Bedford Institute of Oceanography, Dartmouth, NS, Canada, 25 Centre for Integrative Ecology, Deakin University, Burwood, VIC, Australia, 26 Division of Tropical Environments and Societies, James Cook University, Townsville, QLD, Australia, 27 Centre for Tropical Water and Aquatic Ecosystem Research, James Cook University, Douglas, QLD, Australia, 28 Marine Biological Association of the UK, Plymouth, United Kingdom, 29 Departamento de Estudios Ambientales, Universidad Simón Bolívar, Caracas, Venezuela, 30 Akkeshi Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Hokkaido, Japan, 31 Institute of Marine Research IMR, Bergen, Norway, 32 Department of Earth Science, Uppsala University, Uppsala, Sweden, 33 Virginia Institute of Marine Science, The College of William and Mary, Gloucester Point, VA, United States, 34 Department of Biology, Faculty of Science, Prince of Songkla University, HatYai, Thailand, 35 LGL Ecological Research Associates, Bryan, TX, United States, 36 Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San José, Costa Rica, 37 Centre of Marine Sciences (CCMAR), Interdisciplinary Center for Marine and Environmental Research (CIMAR), University of Algarve, Faro, Portugal, 38 Natural Resources and the Environment, University of New Hampshire, Durham, NH, United States, 39 Interdisciplinary Center for Marine and Environmental Research (CIIMAR), Faculty of Sciences, University of Porto, Porto, Portugal, 40 Sydney Institute of Marine Science, Mosman, NSW, Australia, 41 Seagrass Ecosystem Research Group, Swansea University, Swansea, United Kingdom, 42 Centre for Sustainable Aquatic Ecosystems, Environmental & Conservation Sciences, Murdoch University, Murdoch, WA, Australia, 43 Instituto de Ciencias del Mar y Limnología (ICML), Universidad Nacional Autónoma de México, Puerto Morelos, Mexico, 44 Department for Environment and Water, The University of Adelaide and the State Herbarium of South Australia, Adelaide, SA, Australia, 45 UN Environment World Conservation Monitoring Centre, Cambridge, United Kingdom, 46 Oceans Institute and School of Biological Sciences, University of Western Australia, Perth, WA, Australia, 47 Ecological Habitats and Processes Department, DHI Water & Environment, Singapore, Singapore
Duffy et al. Global Marine Macrophyte Observing System In coastal waters around the world, the dominant primary producers are benthic macrophytes, including seagrasses and macroalgae, that provide habitat structure and food for diverse and abundant biological communities and drive ecosystem processes. Seagrass meadows and macroalgal forests play key roles for coastal societies, contributing to fishery yields, storm protection, biogeochemical cycling and storage, and important cultural values. These socio-economically valuable services are threatened worldwide by human activities, with substantial areas of seagrass and macroalgal forests lost over the last half-century. Tracking the status and trends in marine macrophyte cover and quality is an emerging priority for ocean and coastal management, but doing so has been challenged by limited coordination across the numerous efforts to monitor macrophytes, which vary widely in goals, methodologies, scales, capacity, governance approaches, and data availability. Here, we present a consensus assessment and recommendations on the current state of and opportunities for advancing global marine macrophyte observations, integrating contributions from a community of researchers with broad geographic and disciplinary expertise. With the increasing scale of human impacts, the time is ripe to harmonize marine macrophyte observations by building on existing networks and identifying a core set of common metrics and approaches in sampling design, field measurements, governance, capacity building, and data management. We recommend a tiered observation system, with improvement of remote sensing and remote underwater imaging to expand capacity to capture broad-scale extent at intervals of several years, coordinated with stratified in situ sampling annually to characterize the key variables of cover and taxonomic or functional group composition, and to provide ground-truth. A robust networked system of macrophyte observations will be facilitated by establishing best practices, including standard protocols, documentation, and sharing of resources at all stages of workflow, and secure archiving of open-access data. Because such a network is necessarily distributed, sustaining it depends on close engagement of local stakeholders and focusing on building and long-term maintenance of local capacity, particularly in the developing world. Realizing these recommendations will produce more effective, efficient, and responsive observing, a more accurate global picture of change in vegetated coastal systems, and stronger international capacity for sustaining observations. Keywords: biodiversity, seagrass, network, macroalgae, biodiversity observation network (BON), essential ocean variables (EOV) INTRODUCTION Seagrasses and macroalgae (macrophytes) are the foundation of submerged vegetated ecosystems in shallow coastal waters throughout the world. They are among the most productive habitats on land or sea, provide critical habitat for a diverse range of animals, including commercial, and subsistence fisheries and species of concern (Heck et al., 2003; Hamilton and Konar, 2007; Hughes et al., 2009; Unsworth R. et al., 2018; Lefcheck et al., 2019), and provide coastal protection, uptake of terrestrial nutrient runoff, and carbon storage. These habitats and the services they provide are threatened by a range of interacting human activities, notably coastal development, declining water quality, invasive species, climate warming, sea level rise, and storms (Carpenter et al., 2008; Waycott et al., 2009; Polidoro et al., 2010; Filbee-Dexter and Wernberg, 2018). Large, perennial organisms such as seagrasses and canopy-forming macroalgae (Laminariales, Tilopteridales, Desmarestiales, and Fucales, commonly known as kelp and fucoids or rockweeds) are especially vulnerable to human disturbance and, under repeated and interacting impacts, they often yield dominance to faster-growing opportunistic algae (Duarte, 1995; Bonsdorff et al., 1997; Filbee-Dexter and Wernberg, 2018). Growing understanding of the valuable services provided by seagrass and macroalgal stands has strengthened interest in conserving them. Originally, these concerns were based primarily on contributions of coastal vegetated ecosystems to commercial fisheries but have expanded to include their importance to biodiversity and threatened species, Frontiers in Marine Science | www.frontiersin.org 2July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System artisanal fisheries (Nordlund et al., 2018), good water quality, resilience against climate change, and cultural significance (Macreadie et al., 2017; Wernberg et al., 2019). As a result of their ecological value and vulnerability, protection of coastal macrophyte habitats is mandated by many national and international conventions and policies, including the international Ramsar Convention on Wetlands of International Importance and Convention on Biological Diversity (Miloslavich et al., 2018) as well as the USEPA 2003 Clean Water Act, the European Union 1992 Habitat Directive, the 2000 Water Framework Directive, and the 2008 Marine Strategy Framework Directive. Effective resource management requires understanding the extent, conditions, and trends in the marine ecosystems that support them. Moreover, because drivers of change interact, ecosystem-level responses to environmental forcing can be complex, emphasizing the need for tracking both environmental conditions and key biological components of these systems (Duffy et al., 2013a). For example, long-term field monitoring and experiments in the Baltic Sea suggest that seagrass decline resulted from combined nutrient loading and the cascading effects of fishing (Baden et al., 2010; Eriksson et al., 2011; Östman et al., 2016). The interdependency of coastal habitat quality and offshore fisheries in this region would not have been recognized without long-term monitoring. Such interactions also highlight the importance of connecting monitoring to ecological theory, experiments, and modeling to evaluate mechanisms and the generality of system dynamics (Duffy et al., 2013b). For example, both shallow rooted macrophytes (Short and Burdick, 1996; Greening et al., 2018) and macroalgal forests (Benedetti-Cecchi et al., 2015; Filbee- Dexter and Wernberg, 2018) can shift rapidly to unvegetated or alternate vegetation states, with important management implications. Experiments and theory help predict the warning signs and mechanisms of such transitions. Knowledge derived from both monitoring macrophytes and mechanistic research is critical to informing policy and helping to design and implement effective management actions. Similarly, macrophyte species differ widely in morphology, but these traits often covary predictably with physiology (Duarte, 1991). Forecasting the responses of macrophyte communities to perturbations can be strengthened by incorporating mechanistic trait-based approaches, as has proven successful in terrestrial plants (Wright et al., 2004) and corals (Darling et al., 2012; Madin et al., 2014). More than 45 programs worldwide conduct repeated observations of submerged vegetation at regional to global scales (Table S1), providing key indicators of marine ecosystem change (Marbà et al., 2013; Krumhansl et al., 2016; Miloslavich et al., 2018). Most programs operate in isolation and are restricted in space and duration (Krumhansl et al., 2016). This constrains our perception of status, trends, and dynamics of macrophyte ecosystems on the scales necessary for informing effective management and policy, particularly on national and international scales. The Global Ocean Observing System (GOOS), launched in 2009, oversaw a community process to identify a set of core physical, biogeochemical, and more recently biological “Essential Ocean Variables” (EOVs), aimed at providing data to inform requirements for international reporting and assessments (Lindstrom et al., 2012). Seagrass and macroalgal canopy cover and composition were identified as two of the seven biological EOVs based on their scientific and societal relevance and feasibility for global implementation (Miloslavich et al., 2018). However, coordinated observations of these coastal macrophytes have lagged behind those of pelagic phytoplankton and coral reefs. GOOS is collaborating with the Partnership for the Observation of the Global Ocean (POGO), the Marine Biodiversity Observation Network (MBON) (Muller-Karger et al., 2018), and other parties to draft plans for long-term, large-scale implementation of the EOVs. The immediate goal is recommendations for consolidating existing data and metadata toward a globally coherent system under the FAIR (findable, accessible, interoperable, and reusable) data principle (Wilkinson et al., 2016). This white paper presents a consensus assessment and recommendations for advancing observation of marine macrophytes, integrating contributions from researchers with broad geographic and disciplinary expertise. We carried out an in-depth analysis of the current knowledge of seagrass and macroalgae monitoring efforts worldwide. Based on this review, we summarize the status of marine macrophyte habitats, focusing on seagrasses, macroalgal forests, and pelagic Sargassum; the services they provide to humanity; and the threats facing them. We then outline the rationale for considering macrophyte abundance and composition as Essential Ocean Variables as well as steps toward more effectively incorporating them into global observing systems that inform policy and management needs. We close with recommendations for establishing a coordinated global observing system for marine macrophytes. VEGETATION TYPES Seagrasses Seagrasses are a group of 72 species of flowering plants that spend all or most of their lives submerged in seawater (Short et al., 2011). Most seagrasses root in shallow sediment bottoms (exceptions include the rocky shore surfgrasses, Phyllospadix spp., as well genera like Amphibolis, Thalassodendron, Cymodocea, and Posidonia, which occur on rocky bottoms under some conditions). Seagrass depth limits are set by sufficient light to support net positive growth—generally <20 m depth, but deeper in oceanic waters (e.g., >30 m in the Canary Islands) and much shallower in turbid estuaries. Seagrasses form dense populations in estuarine and protected coastal waters from the equator to high latitudes on all continents except Antarctica, and are most diverse in southeast Asia and Western Australia (Lamit et al., 2017). Six seagrass bioregions have been recognized (Figure 1), encompassing all the oceans of the world, across both tropical and temperate waters (Short et al., 2007). The seagrass Atlas (Green and Short, 2003) was able to identify and confirm only around 150,000 km2of seagrass meadows globally. But the global area of habitat suitable for seagrasses has recently been estimated at around 1.6 million km² based on environmental models (Jayathilake and Costello, 2018), and the total coastal area with sufficient light for seagrass growth is estimated at 4.32 million km2(Gattuso et al., 2006; Duarte, 2017), not taking into Frontiers in Marine Science | www.frontiersin.org 3July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System FIGURE 1 | Locations of current long-term seagrass observing networks and seagrass geographic bioregions. (1) Temperate North Atlantic, (2) Tropical Atlantic, (3) Mediterranean, (4) Temperate North Pacific, (5) Tropical Indo-Pacific, (6) Temperate Southern Oceans. Observing systems are shown as 2 degree grids. account other habitat requirements such as suitable substrate conditions. Modeled estimates of seagrass potential extent can cover much larger areas than in situ measurements but have high uncertainty, particularly on local scales, as they are based on environmental conditions considered suitable rather than on direct evidence of seagrass presence. Seagrasses support biotic communities that are often considerably more diverse and productive than in surrounding unvegetated sediments as a result of the physical structure of seagrass meadows and the high productivity of associated algae (Orth and Van Montfrans, 1984; Duffy et al., 2013b). Seagrass meadows are especially important as nursery habitats for juvenile life stages of fishes and larger invertebrates (Beck et al., 2001; Heck et al., 2003; Lefcheck et al., 2019) and provide feeding and breeding habitats for several threatened species, including sea turtles and sirenians (dugongs and manatees). However, much seagrass production is ungrazed and flows into detritus food webs or is buried in sediments, making seagrass meadows important sites of blue carbon burial (Fourqurean et al., 2012; Duarte et al., 2013). Exported seagrass material may also contribute to carbon sequestration in deeper oceanic sinks distant from seagrass habitats (Duarte and Krause-Jensen, 2017). A host of global and local stressors affect seagrasses, including sediment and nutrient runoff, physical disturbance, algal blooms, invasive species, climate warming, and disease (Orth et al., 2006; Waycott et al., 2009). The sheltered coastal and island waters in which seagrasses grow best are prime real estate for coastal and harbor development, imposing pressures from land reclamation, deforestation, aquaculture, fishing, and marine debris (Unsworth R. et al., 2018). A principal local stressor throughout the world is poor water quality resulting from nutrient pollution (eutrophication) and/or sediment loading from land runoff (Cloern, 2001; Burkholder et al., 2007). Requirements for clear water and low nutrient concentrations make seagrasses vulnerable to eutrophication, as nutrient and sediment loading reduce light availability and favor fastergrowing algae (Burkholder et al., 2007). Recently, massive influxes of pelagic Sargassum spp. have caused loss of near-coastal seagrass meadows in the Caribbean (van Tussenbroek et al., 2017), and invasive macroalgae can threaten both seagrasses and canopy macroalgae elsewhere as well (e.g., Lophocladia lallemandii in the Mediterranean Sea, Ballesteros et al., 2007a). Disruption of coastal food webs can also threaten seagrass ecosystems, both by altering grazing by megaherbivores and through cascading effects of overfishing (Eriksson et al., 2011) and hunting (Hughes et al., 2013). Climate change is a growing concern for seagrass ecosystems (Waycott et al., 2011; Short et al., 2016; Fortes et al., 2018). Many temperate seagrasses are sensitive to high temperatures, and warming-induced mortality has been observed over recent decades in several regions (Short and Neckles, 1999; Reusch et al., 2005; Moore and Jarvis, 2008; Hammer et al., 2018). While warming can be particularly detrimental near the equatorial end of the distribution range (e.g., major declines of Zostera marina at its southern range in SW Iberia; Cunha et al., 2013), seagrasses and macroalgae may instead benefit from warming at the polar end of the distribution range (Mieszkowska et al., 2006, 2014; Kortsch et al., 2012; Krause-Jensen et al., 2012). Shallow seagrasses are also vulnerable to die-off under hypersaline conditions (>45 psu) resulting from combined low precipitation and elevated water temperatures (Walker and McComb, 1990; Koch et al., 2007; Johnson et al., 2018). Large-scale (>50 km2) seagrass die-off associated with Frontiers in Marine Science | www.frontiersin.org 4July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System hypersaline conditions is a recurring problem in Florida Bay in the USA, in the French Mediterranean Sea, and southern Australia (Robblee et al., 1991; Seddon et al., 2000; Greve et al., 2003), and is expected to become more frequent and widespread under future warming. Another serious concern is the frequency of disease epidemics, which are associated with warming in many systems (Harvell et al., 2002; Altizer et al., 2013; Kaldy, 2014; Sullivan et al., 2017). In part as a result of these multifarious stressors, ten of the 72 currently known seagrass species are at elevated risk of extinction and three species are classified as Endangered (Short et al., 2011). In the Caribbean Sea, the CARICOMP regional monitoring study detected long-term declines in the relative abundance of the robust, slow-growing seagrass Thalassia testudinum in 43% of 35 long-term monitoring stations consistent with environmental deterioration (van Tussenbroek et al., 2014). In the Mediterranean, dramatic losses in cover of the seagrasses Posidonia and Cymodocea have been predicted (Chefaoui et al., 2018) and observed, and many local extinctions were reported in SW Iberia (Cunha et al., 2013). Many tropical Pacific seagrasses are also declining, mainly in populated areas, due to increased nutrient loading and sedimentation, the two most common stressors of seagrasses worldwide (Short et al., 2014). It is likely that ongoing environmental change will similarly lead to seagrass declines in other locations including the diverse tropical regions where robust environmental protection is often poorly implemented. The wide uncertainty in estimates of global seagrass area, and particularly the geographic bias in our knowledge, makes estimates of threats and projected losses speculative, but there is widespread concern about losing seagrass meadows that have not yet been identified or assessed. This makes establishing a globally harmonized approach for monitoring these coastal ecosystems all the more important and urgent. Benthic Macroalgal Forests A variety of large macroalgae live in dense populations that can be described as marine forests (Wernberg and Filbee-Dexter, 2019). Among the most prominent and widely distributed are large brown algae (Ochrophyta) known as kelps and rockweeds (orders Laminariales, Tilopteridales, Desmarestiales, and Fucales), the largest being the giant kelp Macrocystis pyrifera, which can reach >45 m in length. Large green (Chlorophyta) and red (Rhodophyta) macroalgae can also form marine forests. Macroalgal forests vary greatly in height, structure, and function and, like seagrasses, provide three-dimensional landscape structure that generally supports dense communities of other algae, invertebrates, fishes, and some marine mammals— most of which could not persist in the absence of the canopy (Tegner and Dayton, 2000; Krumhansl and Scheibling, 2012; Teagle et al., 2017). Macroalgal forests are confined to hard substrata, typically rocky reefs, and are generally found from the intertidal zone to 15–25 meters in depth, although the lower limit can exceed 50–100 m in clear water (Graham et al., 2007; Marzinelli et al., 2015b; Assis et al., 2016, 2018). Tidal height, water clarity, wave exposure, and herbivory, particularly by sea urchins, often limit their spatial distribution. Macroalgal forests are particularly prominent along temperate and polar latitudes (Steneck and Johnson, 2013; Wernberg et al., 2019), but laminarian kelp forests occur near the equator in clear, nutrient-rich water below the thermocline (>30 meters) (Graham et al., 2007), and extensive Sargassum forests are common in many shallow tropical and subtropical environments (Fulton et al., 2014). Macroalgal forests dominate at least 25% of the world’s coastlines (Steneck and Johnson, 2013; Wernberg et al., 2019). Macroalgal forests are impacted by a variety of stressors, including sediment and nutrient loading (Foster and Schiel, 2010); direct harvesting (Vásquez et al., 2014); fishing (Ling et al., 2009); climate change in the form of rising water temperatures, ocean acidification, extreme weather events, melting glaciers (Mieszkowska et al., 2006; Wernberg et al., 2012; Araujo et al., 2016); pollution by heavy metals and organic chemicals (Thibaut et al., 2005; Coleman et al., 2008; Fowles et al., 2018); harvesting for food and the phycocolloid industry (Rebours et al., 2014; Buschmann et al., 2017); aquaculture (Yang et al., 2015); and disease (Altizer et al., 2013; Marzinelli et al., 2015a). Climate warming has directly affected the abundance, distribution, and geographic range of many macroalgal species (Johnson et al., 2011; Nicastro et al., 2013; Assis et al., 2014; Brodie et al., 2014; Neiva et al., 2015; Filbee-Dexter et al., 2016; Lourenco et al., 2016; Wernberg et al., 2016; Martinez et al., 2018). Near the poles, climate warming is likely to stimulate the expansion of macroalgal forests (Krause-Jensen and Duarte, 2014). Disturbances to food webs have also threatened macroalgal forests. Overfishing has led indirectly to loss of canopy-forming macroalgae by releasing sea urchins from predatory control and allowing them to overgraze kelps (Wilmers et al., 2012; Filbee-Dexter and Scheibling, 2014; Konar et al., 2014; Ling et al., 2015; Estes et al., 2016). Such trophic cascades are expected to increase in the future. Other herbivores can similarly overgraze macroalgal forests (Chenelot and Konar, 2007; Gianni et al., 2017). Over the last decade or so, tropical herbivores have expanded into temperate regions, increasing the abundance, diversity, and feeding pressure of herbivores and in some cases eradicating macroalgal forests (Johnson et al., 2013; Vergés et al., 2014; Araujo et al., 2016). As a result of these multiple stressors, macroalgal communities are declining worldwide, particularly laminarian kelp forests. Among macroalgal time series extending >20 years, 61% are in decline and only 5% are increasing (Krumhansl et al., 2016; Wernberg et al., 2019). Losses of canopy-forming macroalgae are predicted to increase with rising global temperatures and more frequent and severe weather events (Oliver et al., 2018). Unfortunately, 66% of the bioregions with laminarian kelp forests have no time series data (Mieszkowska et al., 2006; Krumhansl et al., 2016). In many regions, kelps and other canopy-forming macroalgae have been in transition to dominance by turf and coralline algae over the past two decades (Benedetti-Cecchi et al., 2001; Filbee-Dexter and Scheibling, 2014; Strain et al., 2014; Filbee-Dexter and Wernberg, 2018). Community states dominated by turf or coralline algae are often maintained by multiple, complex feedbacks, suppressing their return to dominance by canopy-forming macroalgae (Benedetti-Cecchi et al., 2015; O’Brien et al., 2015; Rindi et al., 2017; Filbee-Dexter and Wernberg, 2018). This Frontiers in Marine Science | www.frontiersin.org 5July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System emphasizes the need to understand ecological processes as well as abundance trends. Pelagic Macroalgae Large macroalgae also occur in the open pelagic regions of the Atlantic Ocean, Gulf of Mexico, and Caribbean Sea, where extensive accumulations of two pelagic brown seaweeds, Sargassum fluitans and S. natans, occur with a diversity of morphological forms (Schell et al., 2015). Both species are holopelagic, reproduce by vegetative fragmentation (Huffard et al., 2014) and form “Lagrangian ecosystems” that drift with winds and currents. In addition to these naturally pelagic macroalgae, floating rafts of normally benthic algae have increased over recent years in several regions. In the East China Sea, floating seaweed rafts are formed by S. horneri, which grows on the bottom but can be detached by strong waves (Qi et al., 2017). Aggregations of detached S. horneri have recurred since 2008, along with blooms of the green macroalga Ulva prolifera in the Yellow Sea. Strategies have been developed to monitor these algal blooms that can also be applied to Sargassum blooms (Hu et al., 2017). Kelps can also separate from the substrate and drift long distances, transporting biomass and associated animals on their way through the ocean (Fraser et al., 2018). Pelagic Sargassum occurs over vast areas of open ocean but is patchy and ephemeral. Its distribution is largely controlled by physical processes, notably ocean circulation and wind (Brooks et al., 2018). Sargassum accumulates in areas of convergence, similar to debris and other pollutants (Powers et al., 2013). Monitoring of pelagic Sargassum is constrained by lack of basic information on its life history, demography, and responses to environmental conditions. The broad distribution and drifting of Sargassum also presents challenges for monitoring. Since 2011, large rafts of Sargassum have entered the Caribbean Sea, washing ashore in massive amounts and affecting navigation and the economies of the island nations in the region, which are largely driven by tourism and, to a lesser extent, fishing. Sargassum accumulation and pollution often co-occur, threatening the endemic and other species that rely on Sargassum (Witherington et al., 2012; Powers et al., 2013). The ecological implications of these accumulations are poorly studied (van Tussenbroek et al., 2017; Gavio and Santos- Martinez, 2018). In the short term, Sargassum can suffocate coastal fauna by depleting dissolved oxygen as the algal biomass decomposes, stress coral reefs by shading their photosynthetic symbionts, and render sea turtle nesting beaches unusable. But moderate influx of biomass and marine-derived nutrients may enhance the growth of dune vegetation and stabilize coastlines. Understanding such ecological processes is necessary for informed management decisions. MARINE VEGETATION, ECOSYSTEM SERVICES, AND HUMAN WELL-BEING Ecosystem services are benefits that humans receive from the Earth’s natural systems and include provisioning, regulating, cultural, and supporting processes (Costanza et al., 1997; Rapport et al., 1998; MEA, 2005). In coastal ecosystems, marine macrophytes provide services including fisheries support, nutrient cycling, coastal protection, water purification, provision of raw materials, and carbon storage that can counteract climate change (Geider et al., 2001; Boström et al., 2003; UNEP, 2006; Bos et al., 2007; Cullen-Unsworth and Unsworth, 2013; Vassallo et al., 2013; Campagne et al., 2015; Dewsbury et al., 2016; Nordlund et al., 2016; Lamb et al., 2017; Filbee-Dexter and Wernberg, 2018). Because seagrasses are sensitive to nutrient loading and water transparency, they also serve as valuable indicators of the state of coastal ecosystems (Dennison, 1987). Seagrasses contribute to water quality by reducing pathogens that cause disease in corals and humans (Lamb et al., 2017) and by taking up nutrient runoff from land. They protect coastal lives and property by stabilizing coastal sediments via both their belowground rhizome structure and leaf canopies (Cruz-Palacios and Van Tussenbroek, 2005; Bos et al., 2007). Seagrass ecosystems are also increasingly recognized as protecting underwater cultural heritage (Krause-Jensen et al., 2018). Similarly, macroalgal forests provide a range of ecosystem services (Vásquez et al., 2014; Bennett et al., 2016; Macreadie et al., 2017; Blamey and Bolton, 2018), including direct support of commercial, recreational, and subsistence fisheries and aquaculture. Indirect ecosystem services include erosion control, climate change mitigation and adaptation, and biogeochemical cycling of nitrogen, carbon, and phosphorus. Intrinsic ecosystem services include cultural and religious significance, biodiversity, and scientific value. Cultural services provided by macrophytes remain understudied (Ruiz-Frau et al., 2017) but include tourism, aesthetic values, and some traditional ways of life that are intricately associated with these ecosystems for food, recreation, and spiritual fulfillment (Wyllie-Echeverria et al., 2002; de la Torre-Castro and Rönnbäck, 2004; Cullen-Unsworth and Unsworth, 2013; Filbee-Dexter and Wernberg, 2018). Few studies have valued macroalgal ecosystem services economically (Bennett et al., 2016), but laminarian kelp forests have been estimated to contribute around 1 million USD per kilometer of coastline (Filbee-Dexter and Wernberg, 2018). The true value is likely to be orders of magnitude higher if indirect and non-use values are fully considered (Bennett et al., 2016). Marine Macrophytes and Fisheries Marine macrophytes provide critical habitat that supports fisheries’ productivity and food security across the world, especially in developing regions (Beck et al., 2001; Green and Short, 2003; Orth et al., 2006; Brun et al., 2009; Unsworth et al., 2014; Nordlund et al., 2016, 2018; Unsworth R. et al., 2018). In the Mediterranean, for example, seagrass covers <2% of the seafloor but seagrass-associated fishes and invertebrates comprise 30– 40% of the total value of commercial fisheries landings (Jackson et al., 2015). Shallow seagrass meadows are easily exploitable and support subsistence, commercial, or recreational fishing in many regions, ranging from hand-gleaning to commercial trawling and targeting multiple fish and invertebrate species (Nordlund et al., 2018). Kelp forests similarly serve as nurseries for fished species in some regions (Hamilton and Konar, 2007). Some kelp ecosystems have been overfished (Tegner and Dayton, Frontiers in Marine Science | www.frontiersin.org 6July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System 2000; Bertocci et al., 2015), but knowledge of these fisheries is geographically limited. Other marine macrophytes are also important for fisheries (Kritzer et al., 2016), including tropical seaweed beds (Tano et al., 2016, 2017). The increasing human populations and standards of living in developing nations put a premium on maximizing the productivity and sustainability of fisheries generally and on conserving the marine macrophyte habitats that support them (Unsworth R. et al., 2018). There is a strong need to include the value of seagrass and macroalgal habitats in spatial planning and management (Nordlund et al., 2018; Unsworth R. et al., 2018). Finally, pelagic Sargassum also has been designated an “essential fish habitat” (NOAA, 1996), as it provides shelter and food for early life-stages of pelagic fishes (Wells and Rooker, 2004) and may play an important role in the recruitment dynamics of economically important species (Kingsford and Choat, 1985). Carbon and Nutrient Storage by Marine Macrophytes Marine ecosystems play key roles in mitigating rising atmospheric CO2by sequestering and storing carbon in coastal plant biomass and sediments—known as “blue carbon.” Seagrass meadows, tidal marshes, and mangrove forests are key blue carbon habitats, occupying just 1% of the seafloor but storing over half the ocean’s carbon (Duarte et al., 2013), sequestering much more carbon on a per-area basis than terrestrial vegetated ecosystems (Mcleod et al., 2011; Röhr et al., 2018). But the magnitude of this carbon storage is highly variable (Nelleman, 2009; Kennedy et al., 2010; Mcleod et al., 2011; Kindeberg et al., 2018; Röhr et al., 2018). Macroalgae form the most extensive of marine vegetated habitats, but until recently were overlooked as contributors to carbon sequestration because they are mostly confined to rocky substrata that do not support carbon burial in sediments (Howard et al., 2017). However, macroalgal forests can export material to carbon sinks in shelf sediments and in the deep sea where it can be sequestered (Krumhansl and Scheibling, 2012; Hill et al., 2015; Krause-Jensen and Duarte, 2016; Wernberg and Filbee-Dexter, 2018). A first-order estimate indicates that this macroalgal contribution is of the same order of magnitude as carbon sequestration by seagrasses, saltmarshes, and mangroves combined (Krause-Jensen and Duarte, 2016). The contribution of macroalgae to carbon sequestration varies among species (Trevathan-Tackett et al., 2015), but more direct estimates are needed to quantify sequestration, and this requires a paradigm shift in accounting procedures as well as development of methods to trace carbon from donor to sink habitats in the ocean (Krause-Jensen et al., 2018). As vegetated ecosystems have declined substantially in area (Waycott et al., 2009), many coastal areas have been converted from carbon sinks to sources, a shift that can, in principle, be reversed (Pendleton et al., 2012; Macreadie et al., 2015, 2017; Marbà et al., 2015; Kerrylee et al., 2018). One approach to quantifying the processes that mediate carbon storage and release from seagrass sediments is the TeaComposition H2O project, which uses widely available tea bags to measure organic carbon preservation in seagrass and other wetland sediments, currently under way across 350 nearshore marine sites. Similarly, the SUKER Network has recently completed globally distributed litterbag experiments across 40 sites between Alaska and Portugal to measure the fate of sugar kelp detritus. Anthropogenic nitrogen inputs are a major stressor facing coastal ecosystems worldwide (Duarte et al., 2009). Historically, nitrogen has been a limiting factor for primary production in many coastal regions, but nutrient loading from agricultural runoff and coastal development has greatly increased usable nitrogen availability in coastal systems worldwide. These inputs shift the character of the vegetation and produce far-reaching impacts that ripple through coastal ecosystems (Breitburg et al., 2009). Macrophytes can help mitigate such eutrophication. Seagrass meadows suffer less decline where they are separated from terrestrial runoff by fringing marshes, probably because of denitrification and burial of terrestrial nitrogen within the marshes before it reaches the seagrasses offshore (Valiela and Cole, 2002). Seaweed aquaculture also has been proposed as a way to mitigate eutrophication impacts (Chopin et al., 2001; Neori et al., 2004), and in certain locations on the coast of China, algal cultivation has reduced nutrients and resulting algal blooms, including toxic microalgae (Yang et al., 2014). But algal aquaculture has more often been detrimental, resulting in widespread seagrass loss (Eklöf et al., 2006; Unsworth R. K. et al., 2018). Marine Macrophytes and Animal Species of Conservation Concern Macrophyte ecosystems provide food and habitat to a wide range of invertebrates, fishes, and some marine mammals and reptiles, including several listed under CITES [e.g., the dugong, Dugong dugon; the West Indian manatee, Trichechus manatus; and the African manatee, Trichechus senegalensis, all listed in CITES Appendix 1, and the green turtle, Chelonia mydas, classified as Endangered on the IUCN Red List and also on CITES Appendix 1 (Moore et al., 2017; Sievers et al., 2019)]. Most large animals that depend on seagrasses have declined substantially during historical times, and about 30% of named seahorse species, all of which use seagrass habitats, are included on the IUCN Red List (Hughes et al., 2009). Prior to European colonization, large seagrass-feeding vertebrates were extremely abundant in some regions. The Cayman Islands fishery in the Caribbean landed ∼13,000 sea turtles each year for decades beginning in the late Seventeenth century (Jackson, 1997), and the number of dugongs along the coast of the Great Barrier Reef Region south of Cairns was much greater than it is today (Marsh et al., 2005). The formerly larger densities of megaherbivores undoubtedly had major impacts on seagrasses (Marsh et al., 2011, 2018; Vonk et al., 2015), but megaherbivore grazing can also increase seagrass productivity (Aragones and Marsh, 2000; Christianen et al., 2011; Marsh et al., 2011, 2018). Live seagrass seeds have been found in megaherbivore feces, indicating the potential for green turtles and dugongs to disperse seeds up to hundreds of kilometers (Tol et al., 2017) and excavating dugongs can also increase microbial nutrient cycling in seagrass sediments (Perry and Dennison, 1999). Megaherbivores associated with seagrasses also support Frontiers in Marine Science | www.frontiersin.org 7July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System provisioning and cultural ecosystem services, including hunting, fishing, tourism, and cultural values (Butler et al., 2012; Cullen- Unsworth et al., 2014). Large-scale loss of seagrass results in mortality and reduced fecundity of seagrass-dependent megaherbivores (Marsh et al., 2011; Fuentes et al., 2016). Kelp forests of the northeastern Pacific formerly supported the largest known herbivorous marine mammal, Steller’s sea cow (Hydrodamalis gigas). This giant 8– 9 m relative of the dugong was hunted to extinction within a few decades of its first encounter with Europeans in 1741 (Marsh et al., 2011), and the sea otter (Enhydra lutris) nearly met a similar fate, having been eliminated from the North Pacific apart from a few remote islands of the Aleutian chain prior to protection in the 1970s. There is some evidence of a symbiotic relationship between sea otters and seagrasses (Hughes et al., 2013). As is true of marine invertebrates generally, we have very limited knowledge of the conservation status of most macrophyte-associated invertebrates. Several gastropods and echinoderms are popular as curios and traditional medicines, and harvesting may contribute to their population decline or extinction (Hughes et al., 2009). Pelagic Sargassum serves as nursery habitat for oceanic-stage juvenile sea turtles (Carr, 1987; Witherington et al., 2012). Young turtles likely grow faster in association with pelagic Sargassum owing to foraging on invertebrates in the algae and higher temperatures achieved by basking in surface rafts, and the thick mats may also reduce predation risk (Mansfield and Putman, 2013; Mansfield et al., 2014). In 2014, the US National Marine Fisheries Service designated waters in the U.S. Exclusive Economic Zone with abundant pelagic Sargassum as a “critical habitat” for the loggerhead sea turtle (Caretta caretta) in the Northwest Atlantic Ocean. There is also growing evidence that small sea turtles of several species actively orient toward pelagic Sargassum (Mansfield and Putman, 2013; Putman and Mansfield, 2015). New satellite-based mapping (Figures 2A,C) now makes it possible to integrate Sargassum distribution with models of sea turtle behavior and movement (Putman et al., 2012) to explore its role in turtle population dynamics. Marine Macrophytes and Coastal Protection In addition to their role in climate change mitigation through carbon storage, marine macrophytes also contribute to climate change adaptation e.g., by dampening the wave energy and stimulating sedimentation, thereby protecting coastlines against rising water levels and storms (Duarte et al., 2013). Coastal wetlands, including seagrass meadows and some macroalgal forests, form protective barriers that shelter coastal land from erosion and storm surge by attenuating waves and reducing property damage and human deaths. Both living plants and their dead biomass accreted as peat strengthen shorelines and provide a robust barrier that protects coastal land against sea level rise (Gedan et al., 2011), severe storms, and wave action. Analysis of 34 major US hurricanes found that economic damage declined with greater area of wetland in the storm zone, and that wind speed and wetland area together explained 60% of the FIGURE 2 | Tracking of pelagic Sargassum density and movement in the Caribbean region. (A) Sargassum area density map (0.5◦×0.5◦) in July 2018. The red color indicate pixels where the area density (% cover) exceeds 0.1 units. (B) Trajectories of spatial drifters deployed by NOAA/AOML in the Atlantic. Each color represents a type of drifter. The trajectories of drifters with transmitters attached to real and artificial Sargassum are shown in green. (C) Cumulative weekly AFAI field from VIIRS&MODIS (20 June 2018). The structures in green/red may correspond to Sargassum patches, which extended over large areas in the Caribbean Sea during that period. Clouds are masked to black. variation in damage; coastal wetlands were estimated to provide more than 23 billion USD per year in storm protection in the USA (Costanza et al., 2008). And studies in the UK concluded that maintenance of natural marsh is much less expensive than building and maintaining sea walls as protection against erosion (King and Lester, 1995; Rupprecht et al., 2017). Frontiers in Marine Science | www.frontiersin.org 8July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System Mapping the risk of storm and wave hazards along the coastline of the USA shows that, under several projected climate scenarios, the number of people and the total value of residential property exposed to hazards could be reduced by half by preserving existing coastal habitats (Arkema et al., 2013). Models predict that climate change will increase wave heights, especially at higher latitudes (Izaguirre et al., 2011). In Northern Europe, the intensity of destructive storms has already increased more than 3-fold since 1990 (Gregow et al., 2017), and monthly mean wave heights have risen up to 0.6 m in the North Atlantic during the latter twentieth century (Woolf et al., 2002). Natural infrastructure provided by coastal habitats holds strong but understudied potential to mitigate such hazards and increase coastal resilience under climate change (Sutton-Grier et al., 2015). OBSERVATION SYSTEMS FOR MACROPHYTES Current Status of Observing: Seagrasses To examine the current status of marine macrophyte observing, we collated information on monitoring programs with more than three repeated observation events over a period >3 years, with a least one observation event in the last decade (2008– 2018). This eliminated the large number of localized, shortterm monitoring projects. Of the 20 active long-term seagrass observing programs meeting these criteria (Table S1), the largest were the global programs SeagrassNet and Seagrass-Watch. Together these programs include long-term monitoring across five of the six seagrass bioregions (Figure 1), with 21 countries currently participating in SeagrassNet and 11 in Seagrass-Watch. One of the largest regional networks is in the temperate North Atlantic region, where 23 countries monitor seagrass via 11 programs (e.g., COMBINE; PMN) (Marbà et al., 2013) in compliance with the pan-European Water Framework Directive (WFD, 2000/60/EC) (Foden and Brazier, 2007). The WFD stimulated widespread monitoring of macroalgae and seagrasses in Europe by prescribing assessment of ecological status based on biological elements, including aquatic plants. However, while the WFD requires that ecological status is defined relative to a reference, and that status classifications are intercalibrated within ecoregions, member states are free to develop their own indicators, which has resulted in a proliferation of seagrass indicators that are often not comparable (Krause-Jensen et al., 2005; Marbà et al., 2013). The motivations for existing seagrass observing networks range from broad—increasing general scientific knowledge and tracking the status of seagrass—to more narrow efforts to support conservation and regulatory agreements. The book Global Seagrass Research Methods (Short and Coles, 2001) provides detailed methodology for assessing all aspects of seagrass ecosystems. Two broad approaches are currently used to monitor seagrass ecosystems. The first involves air-borne or satellite remote sensing to map seagrass and estimate broad-scale changes in extent over time. The second approach quantifies indicators of seagrass condition in situ at smaller spatial scales, often to assess the effects of stressors. These approaches have been powerfully combined in a hierarchical framework for monitoring based on spatial extent, frequency of monitoring, and scope (Neckles et al., 2012). The first tier within the hierarchical framework characterizes overall distribution of seagrasses across a region of interest. This approach is widely used to assess status and trends at broad scales, over long time periods, with low observing frequency. Aerial and hyperspectral satellite imagery are wellestablished techniques at such scales, but such remote technology restricts observations to shallow depths and is often unworkable in the complex multi-habitat seascapes and turbid waters where seagrasses are most abundant (Knudby and Nordlund, 2011). Measures derived from remote sensing are often limited to presence/absence and extent. Rapidly evolving technological advances may offer partial solutions, with improvements in resolution and availability of both satellite sensors and highquality drone and autonomous or remotely operated sensors (both above and within water) increasing the environmental window of opportunity for observing and quantifying seagrass. Currently, there is no consistent approach or recommended sensor for seagrass globally. Some observing networks supplement remote sensing with in situ manual sampling of species identity and abundance, which constitute the second and subsequent tiers within a hierarchical monitoring framework. In situ sampling characterizes seagrass condition by selecting statistically rigorous sampling units and monitoring frequency, e.g., SeagrassNet. These measurements are predominantly in situ and done by hand, providing more detailed indicators of spatiotemporal variation in species composition, size, and abundance (e.g., cover, density, biomass). These second-tier measures involve a greater number of sampling units, a higher temporal frequency, and higher resolution than the first tier of remote sensing. Finer-scale tiers generally focus more specifically on evaluating drivers of change at higher frequency, with more metrics, and a smaller number of sites. These in situ methods are far more accurate and detailed than remote sensing but accordingly more labor intensive and thus restricted in scope. The GOOS has proposed harmonization of monitoring protocols toward development of seagrass cover and composition as an Essential Ocean Variable (Miloslavich et al., 2018). Several collective decisions need to be made to achieve this goal. First, there is currently no widely accepted standard for site selection, and observing networks vary widely in the types, sizes, and replication of sampling and reporting units. Most networks use some version of stratified random sampling, with or without constraints. For example, areas of investigation are often divided using expert knowledge into subpopulations—e.g., by water depth—that maximize variation between and minimize the variation within units. Sampling units are then randomly drawn and may be allocated proportionately to provide robust estimates of variance (Neckles et al., 2012; see also FKMMP, Texas Seagrass Monitoring program). This approach aims to balance reporting area size, level of detail necessary, accessibility, legacy, safety, and budget. Once the reporting unit or site is established, the second decision to be considered involves the frequency of assessment Frontiers in Marine Science | www.frontiersin.org 9July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System and person-power (Table S1). Approaches that are robust and usable across a variety of seascapes, taxa, and habitats are most accessible to diverse contributors and regions. A simple, standardized core field sampling architecture can then provide a scaffolding for integration—and ground-truthing— of new technology, including remote sensing, machine learning techniques for species recognition from imagery, and eDNA, when and where resources are available. Given the number of methods available, aims need to be clearly defined to assess trade-offs between data resolution and monitoring feasibility. Keep It Relevant Achieving widespread community buy-in for coordinated monitoring of marine macrophytes will be advanced by clearly linking observing activities to the needs of local participants, policy makers, and decision makers. The data collected need to be scientifically rigorous enough for acceptance by policy makers but simple enough to be conducted widely and communicated clearly to the general public. Coordination among efforts will also increase efficiency and add value. Better coordination and mapping of macrophyte extent and quality would advance initiatives to develop integrated seagrass accounts that map ecosystem services and value them as natural capital. Building a clearly articulated natural capital base for marine macrophytes could open doors to new funding streams by linking ecosystem services to end users (e.g., fishers, carbon traders, tourist industry). For example, Essential Ocean Variables for marine macrophytes could link to blue carbon initiatives, which have the potential to develop a commercial user base and supplementary funding. Focus on Contributors Any long-term project will experience lapses in funding, leadership, and/or other interruptions, and most rely on substantial leveraging of in-kind support from participants. To sustain an observing system under such circumstances, it is imperative that the work addresses local needs, builds capacity and community, and provides opportunities across career levels, including future generations. Local participants must also feel ownership and a degree of control if efforts are to be sustained. These results can be met with an approach based on a standardized but flexible sampling design and protocols that provide a scaffolding on which additional activities of local interest can be built and that catalyzes and adds value to those activities. For example, implementing a standard seagrass monitoring protocol often provides opportunities for participants to quantify commercially important species during the same surveys, provides educational opportunities to local students, and so on. An important component of all observing networks is feedback and outreach. Not only is this critical for networks that rely on voluntary data contributions, but it ensures project outputs remain useful for evidencebased policy and management decisions. Sustaining a network of monitoring sites ultimately requires strong collaborations in addition to knowledge and technology transfer among participating observatories. This is especially urgent in Small Island Developing States and Least Developed Countries, where the knowledge gaps are largest and coastal ecosystems are particularly vulnerable. This is a core goal of the Group on Earth Observations Biodiversity Observation Networks (Pereira et al., 2013). Similarly, GOOS aims to tackle this challenge by promoting standardized protocols and data management best practices (Bax et al., 2018). In many regions, Local Ecological Knowledge (LEK) can provide unique data to establish baselines and to understand historical change (Johannes et al., 2000; Beaudreau and Levin, 2014; Frans and Auge, 2016; Aswani et al., 2018), as it often incorporates observations over longer time periods and preserves memories of rare and extreme events (Moller et al., 2004). LEK can also be used to direct exploratory scientific sampling efforts. Engaging fishers and other users specifically can take advantage of their regular access to the sea (Hashim et al., 2017; Cullen- Unsworth et al., 2018). A combination of science and LEK can provide data across larger temporal and spatial scales. LEK and associated citizen science have been increasingly applied to help map and monitor marine habitats, including seagrasses, at global scales in cost-effective ways (Titilola, 1990; Moller et al., 2004; Jones et al., 2017) and to help design marine protected areas (Ban et al., 2009). Such approaches also provide opportunities for engagement, empowerment, and an improved sense of wellbeing. The capacity for LEK to contribute to large-scale ocean observation systems remains largely untapped. Finally, citizenbased monitoring can provide valuable data under the right circumstances (McKenzie et al., 2000; Short et al., 2006), although it is difficult to implement in regions where macrophytes are submerged and inaccessible. Provide Support and Training Reliable replication over space and time and rigorous standardization are essential in any monitoring program aimed at detecting changes. Providing support, training, coordination, and data management for monitoring is a challenge for all long-term observing networks as they face periods of reduced funding, which can compromise data quality. A key part of support is consistent and sustainable training tools and protocols for new technicians and other members to ensure consistent application of methods over time and space. Some networks have institutionalized training or require passing courses (e.g., KEEN, PISCO, Reef Life Survey, and MBON Pole to Pole), a model that should be widely adopted. Ensure Continuity Sustaining observing efforts over the long term requires plans for continuity of leadership, funding, training, and data management. In most networks, a small number of champions act as a driving force, and there is little planning for succession and turnover. Such plans are needed to sustain any program through the long-term. The Kelp Forest Monitoring program provides a valuable model in that it has successfully turned over leadership twice in its multi-year lifespan, in part due to such planning. Expand the Reach Nearly all monitoring programs are conducted by marine scientists or environmental practitioners. However, over the last couple of decades, citizen science has also begun to Frontiers in Marine Science | www.frontiersin.org 16 July 2019 | Volume 6 | Article 317
Duffy et al. Global Marine Macrophyte Observing System contribute significantly to science, education, and policy (Jones et al., 2017). Citizen monitoring is most successful when it requires minimal specialized equipment and resources. Nearly a third of the current long-term seagrass observing networks include some level of citizen science, including SeagrassWatch and SeagrassSpotter.org as well as TeaComposition H2O. The incorporation of approaches based on Information and Communication Technology (ICT) into citizen science expands its reach. By using a web and phone app approach, SeagrassSpotter.org has to date collected data in 75 countries and included observations of 36 species, and www.marineforests. com includes thousands of photographic records around the world. Citizen science is also included in the Kelp Ecosystem Ecology Network. In Southeast Asia, citizen initiatives are key to the effective linkage between science, policy, and practice, which is the core of coastal natural resources management (Fortes et al., 2018). Data Management, Ownership, and Access Observing systems are only as good as the data produced. Collection, storage, and use of data must be designed with a longterm vision, engaging global institutions to ensure data security and accessibility. To assure users of data quality, observing networks should implement clear, formal, and transparent practices for quality assurance and quality control (QA/QC) and data management. Data management is opaque for many current long-term monitoring programs, with only a few having centralized systems and even fewer with clear QA/QC protocols. Clear and transparent policies on data ownership and procedures for data access are also critical for any observing network (Wilkinson et al., 2016), particularly when it includes multiple contributors from many organizations. Implementing standard data agreements facilitates confidence among data collectors, stewards, and users. Promote Rigorous Taxonomic Standards Comparisons across space and time can be challenging where taxonomic expertise is inadequate. Some observation systems target only major structure-forming taxa, while others sample a much broader taxonomic range. Increasing taxonomic depth is time consuming and expensive, and the inherent tradeoff between sampling scale and taxonomic depth is a key hurdle to harmonizing biological observation efforts. The level of taxonomic resolution also depends strongly on the knowledge of system participants. One possible solution involves strong, independent cross-verification of identifications based on archived voucher collections. Methods based on imagery have the advantage of being independently verified by other observers in future analyses. Photographs and voucher collections have been particularly important in cases where species names change as cryptic species are discovered (Zardi et al., 2015; Neiva et al., 2017). Thus, archiving images and voucher collections makes surveys more valuable. Formal systems for classifying functional groups (Althaus et al., 2015) would advance cross-system comparisons, including across temperate and tropical systems. Achieving harmonized strategies for aligning taxonomic or functional levels, good management of leadership, methodologies, training, and data management, should not only produce more effective and efficient observing in practice but will facilitate a more accurate global picture of change in macrophyte systems. Such efforts should incorporate rigorous documentation and open-access archiving of protocols and all stages of workflow, from field surveys to data management (e.g., through Ocean Best Practices), and provide open access data. Adopt an Ecosystem Approach Over the last decade or so, fisheries have increasingly explored, and sometimes adopted, an ecosystems approach (Travis et al., 2014; Patrick and Link, 2015), recognizing that harvested species are connected via a web of complex interactions with abiotic forcing and other species that may confound management based on simpler models. The same situation holds for coastal vegetation (Duffy et al., 2013b). Long-term observations have confirmed that decline in coastal macrophyte ecosystems resulted from both excess nutrient loading and altered food webs resulting from harvesting in the Baltic Sea (Eriksson et al., 2011) and California (Hughes et al., 2013). These examples emphasize the need for an ecosystem-based approach to coastal resource management and that this requires management—and monitoring—of multiple biological and environmental variables. The substantial prior efforts devoted to monitoring and research on seagrasses, macroalgal forests, and pelagic Sargassum offer several valuable lessons for envisioning a more ambitious, coordinated effort in support of a global observing system. Successful observing programs are driven by tractable questions with rigorous, common statistical designs that meet specific scientific and policy needs. Long-term observation projects for coastal seagrasses and macroalgae have been substantially underresourced relative to observations of oceanic phytoplankton despite the outsized importance of coastal vegetation in fisheries support, coastal protection, global carbon dynamics, and other ecosystem services. A key, achievable goal is to reach consensus on when, where, and how methods can be harmonized to provide a minimal set of common metrics, agreed sampling designs, and data reporting mechanisms and standards that build toward global coverage. Implementing a robust large-scale observation network should consider the past, with the wealth of legacy data and LEK available, the shifting baselines of the present, and focus attention proactively on the range of possible future outcomes for the health and ecosystem services provided by seagrass meadows, macroalgal forests, and pelagic Sargassum. AUTHOR CONTRIBUTIONS JD, LB-C, JT, and FM-K developed the project idea and coordinated writing and editing. LM and JB led assembly of network data for Table S1. All authors contributed to manuscript writing and/or editing. FUNDING This review was supported by US National Science Foundation award OCE-1829922 to JD, as well as a large number of sources to the 47 co-authors. 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Duffy et al. Global Marine Macrophyte Observing System ACKNOWLEDGMENTS This is contribution 34 from the Smithsonian’s MarineGEO Network. JT was funded by NOAA/OceanWatch & GG was funded by NOAA/AOML. This manuscript is also a contribution to the Marine Biodiversity Observation Network (MBON) of the Group on Earth Observations Biodiversity Observation Network, and to the Integrated Marine Biosphere Research (IMBeR) project, which is supported by the Scientific Committee on Oceanic Research (SCOR) and Future Earth. The work leading up to the manuscript was funded in part under the US National Ocean Partnership Program (NOPP RFP NOAA-NOS- IOOS-2014-2003803 in partnership between NOAA, BOEM, NASA, the US Integrated Ocean Observing System (IOOS) Program Office, and NSF. Specifically, the MBON work was funded through NASA grant NNX14AP62A to FM-K [National Marine Sanctuaries as Sentinel Sites for a Demonstration Marine Biodiversity Observation Network (MBON)]. 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Shepherd (Amsterdam: Elsevier), 57–78. doi: 10.1016/B978-0-12-805052-1.00003-6 Frontiers in Marine Science | www.frontiersin.org 25 July 2019 | Volume 6 | Article 317