Initial Grand Challenges
Frontiers in Marine Science launched the Marine Ecosystems Ecology (FMARS-MEE) section in 2014, with a paper that identified eight grand challenges for the discipline (Borja, 2014). Since then, this section has published a total of 370 papers, including 336 addressing aspects of those challenges. As editors of the journal, with a wide range of marine ecology expertise, we felt it was timely to evaluate research advances related to those challenges; and to update the scope of the section to reflect the grand challenges we envision for the next 10 years. This output will match with the United Nations (UN) Decade on Oceans Science for Sustainable Development (DOSSD; Claudet et al., 2020), UN Decade of Ecosystems Restoration (DER; Young and Schwartz, 2019), and the UN Sustainable Development Goals (SDGs; Visbeck et al., 2014).
First, we analyzed each published paper and assigned their topic to a maximum of two out of the eight challenges (all information available in Supplementary Table 1). We then extracted the 3–5 most cited papers within each challenge using two criteria: the total number of citations during this 6-year period, and the annual citation rate (i.e., the mean annual number of citations since publication). We then collated the topics covered by this reduced list of papers (Table 1) and summarized the outcomes for each topic.
Table 1
| Grand challenge | Papers published (nr) | (%) | Most cited references | Topic covered | Top papers citations (annual mean | total) | Comments |
|---|---|---|---|---|---|---|
| 1. Understanding the role of biodiversity in maintaining ecosystems functionality | 187 | 50.5 | Renaud et al., 2015 Kristensen et al., 2014 Heithaus et al., 2014 | Macroalgal detritus and food-web subsidies in the Arctic Effects of shifts in benthos and functional traits to biogeochemical cycling Relationships between seagrasses, turtles and sharks | 7.0 | 45 6.3 | 47 5.8 | 47 | From the papers received in 2014–2019, this is the main core topic of the journal. This includes the multiple relationships and interactions between different ecosystem components, between them and the physico-chemical component of the system, including processes, structure and functionality. Likely this will also be the main topic in the future |
| 2. Understanding relationships between human pressures and ecosystems | 72 | 19.5 | Katsanevakis et al., 2014 Patrício et al., 2016 Korpinen and Andersen, 2016 Chartrand et al., 2016 | Human activities and alien species mapping DPSIR framework review Review on marine cumulative impact assessments Dredging activity pressures on seagrasses | 10.7 | 76 7.3 | 38 5.8 | 24 3.5 | 27 | With increasing maritime activities, the need of understanding these relationships will be maintained, and, as such, occupying a part of the papers in the journal. Especially, the effects of multiple pressures on marine ecosystems will receive increasing attention. Some specific pressures (e.g., invasive species) will need a new grand challenge (Table 2) |
| 3. Understanding the impact of global change on marine ecosystems | 36 | 9.7 | Duarte and Krause-Jensen, 2017 Thomsen et al., 2019 Lindemann and St. John, 2014 | Seagrass meadows contribution to carbon sequestration Extinctions after heatwaves Phytoplankton dynamics in a changing world | 9.3 | 38 8.0 | 13 4.3 | 31 | This global problem will receive increasing attention in our journal in coming years, since it will be a transversal issue for multiple aspects of the marine systems, from natural communities, but also for resources, conservation and management |
| 4. Assessing marine ecosystems health in an integrative way | 31 | 8.4 | Borja et al., 2016 Aylagas et al., 2016 Danovaro et al., 2016 Goodwin et al., 2017 Borja et al., 2014 | Review on integrative methods to assess ocean's health Metabarcoding in assessing the status of benthos Innovative monitoring tools for ecological status DNA sequencing to monitor ecological status Methods to aggregate indicators in assessing the status | 14.5 | 95 11.5 | 57 6.0 | 44 6.0 | 22 5.5 | 57 | The importance of this challenge is highlighted with the number of citations and the increasing need of assessing the marine systems to take informed management decisions |
| 5. Delivering ecosystem services by conserving and protecting our seas | 14 | 3.8 | St. John et al., 2016 Galparsoro et al., 2014 Mačić et al., 2018 | Services provided by mesopelagic fishes Services provided by benthic habitats Conservation planning and biological invasions | 9.3 | 41 4.3 | 34 3.5 | 12 | The links between the oceans' health (through conservation and protection) and the ecosystem services delivered, as well as the benefits for human well-being, need increasing attention |
| 6. Recovering ecosystem structure and functioning through restoration | 16 | 4.3 | Duarte and Krause-Jensen, 2018 Pérez-Ruzafa et al., 2019 Rouse et al., 2019 Gillis et al., 2017 | Recovery from coastal eutrophication Recovery of a lagoon from eutrophicatio Conservation features for subsea infrastructures Restoring tropical coastal ecosystems | 2.0 | 5 2.0 | 5 2.0 | 2 0.3 | 2 | Although our journal has attracted little attention on this challenge, the recovery of marine systems after degradation should have an increasing attention |
| 7. Managing the seas using the ecosystem approach and spatial planning | 8 | 2.2 | Newton and Elliott, 2016 Smith et al., 2016 Tam et al., 2017 | Stakeholder engagement in marine management Conceptual models in marine management Thresholds and reference points for ecosystem-based management | 3.5 | 26 2.3 | 21 2.0 | 12 | Effects of management of the seas, an ecosystem-based approach and maritime spatial planning on marine ecosystems should receive increasing attention, because of different legislations worldwide |
| 8. Modeling ecosystems for better management | 43 | 11.6 | Faillettaz et al., 2018 Mayorga-Adame et al., 2017 Nanninga and Berumen, 2014 | Larvae dispersal and connectivity Modeling larval connectivity of coral Role of individual in larval dispersion | 4.0 | 8 3.3 | 11 2.5 | 17 | The use of models for habitats and species distribution, connectivity, climate change scenarios, monitoring and assessment, ecological processes, management, etc., will increase |
| Robinson et al., 2017 | Review of species distribution models | 3.3 | 12 | ||||
| Lynam et al., 2016 | Innovative modeling tools for management | 2.3 | 16 | ||||
| None of the above | 34 | 9.2 | Borja, 2014 Vázquez-Luis et al., 2017 Xavier et al., 2016 | Challenges in marine ecosystems ecology Mass mortality of an endangered bivalve Research challenges in the Southern Ocean | 8.3 | 57 4.3 | 22 2.8 | 21 | Social-ecological issues, socio-economic topics, ocean literacy, solutions for the problems of the oceans, human health and oceans, etc., will become more important |
Grand Challenges in Marine Ecosystems Ecology, as defined by Borja (2014), number of papers published (and percentage) on each challenge in Frontiers in Marine Science (section Marine Ecosystems Ecology), topics covered by the most cited references for each challenge, considering mean annual citations per paper (excluding self-citations from all authors for the period 2014–2019) and/or total number of citations received (as in SCOPUS on 15th January 2020).
Percentages add up to more than 100% because papers were assigned to up to two challenges.
Not surprisingly, 50.5% of the papers dealt broadly with the role of marine biodiversity in maintaining ecosystem function, since they are related to the core of the journal section. They are followed by papers addressing relationships between human pressures and marine ecosystems (19.5%), and ecosystem modeling (11.6%). Just fewer than 10% of the papers were unrelated to any of the challenges defined by Borja (2014) (Table 1). Papers related to the assessment of ocean health had the highest impact, with a relatively high number of citations, despite the low number of papers published on the topic (Figure 1). In fact, of the top papers assigned to each challenge, those assessing ocean health received the highest annual mean number of citations, followed by papers on understanding relationships between human pressures and ecosystems, and those dealing with understanding the role of biodiversity in maintaining ecosystems functionality (Table 1).
Figure 1
The topics of the publications spanned all ecosystem components, from microbes to mammals; habitats from pelagic to benthic; many individual and multiple human pressures and natural stressors affecting species, their populations, communities and habitats; methodologies for monitoring, modeling, and assessment; conservation, protection, restoration, and recovery of marine ecosystems; global change effects; and different management issues (Table 1). Some of the papers that did not focus on the grand challenges dealt with a special Research Topic, for example, ocean literacy (Borja et al., 2020a).
Grand Challenges for Coming Decade
Although publications in FMARS-MEE have focused on many of the challenges stated in 2014, critical gaps remain which will require considerable research effort to be bridged (Table 1). Furthermore, the analysis of the papers published from 2014 to 2019 in FMARS-MEE, and the discussion held by the editorial board when preparing this paper, points to some new or updated grand challenges, as core of our journal section. Other secondary challenges alongside governance, social, and methodological priorities, were identified as important and we also propose them for consideration into the next decade (Table 2). Addressing these challenges, which are deeply related to each-other (Table 2), would help increase our knowledge of the global ocean, raise awareness on ocean status and identify nature-based solutions to mitigate the impacts of current pressures.
Table 2
Summary of the new (N) and updated Grand Challenges faced by marine ecosystems in the next decade, as identified by the editorial board of Frontiers in Marine Science (section Marine Ecosystems Ecology), which need to be addressed from science in different ways.
Also, we highlight other secondary (S) challenges, governance (G), social, and methodological (M) priorities, and the interactions with the Grand Challenges. UN, United Nations; SDG, Sustainable Development Goals; MPA, Marine Protected Areas. Note: for complete names of the challenges, consult the text.
New and Updated Grand Challenges
Our revisited list of new (N) grand challenges (Table 2) includes:
(N1) Understanding of interaction among diversity and ecosystem processes, structure and function, which is still the core of FMARS-MEE. Expanding the scope and relevance of future studies will allow to better understand the complex biophysical relationships among biodiversity, food-web structure, ecological processes, and ecosystem functioning, and thus increase our predictive capacity of the ecological consequences of shifts in biodiversity;
(N2) Measuring ecosystem shifts, biodiversity and habitat loss, clearly related to international commitments on sustaining biodiversity (O'Hara et al., 2019). Although ecologists recognize that Earth is now experiencing the sixth mass extinction, quantifying ecosystem shifts, and biodiversity loss remains challenging and often leads to scientific debates (e.g., Vellend et al., 2017);
(N3) Restoring degraded systems, in line with the UN DER. Marine and coastal ecosystems have suffered substantial degradation in the last century, with important loss in their capacity to deliver ecosystem services (Rocha et al., 2015). Ecological restoration efforts often have low success rates, indicating the need for new strategies, that better account for marine connectivity and interactions with adjacent ecosystems, as well as the physical environment (Gillis et al., 2017). To date, restoration efforts have focused on coastal ecosystems, but with increasing exploration for hydrocarbons and other resources offshore and in areas beyond national jurisdiction, approaches for deep-sea and open sea restoration should be explored and tested;
(N4) Moving from descriptive studies to those providing functional assessments, improving the understanding of marine ecosystems, supporting management and sustainability strategies for human activities in the ocean, in line with the UN DOSSD;
(N5) Understanding the cause-effect pathways and the response of ecosystems to increasing cumulative human impacts and climate change (Ortiz et al., 2018), as drivers of shifts in most marine ecosystems, altering species distributions and threatening biodiversity (Halpern et al., 2019). Such cause-effect pathways are inherently non-linear and include direct and indirect feedbacks (Fu et al., 2018). Consequently, this challenge is complex and requires novel methods of assessment and models spanning across disciplines (Crain et al., 2008; Phillips et al., 2019). The assessment of success rates for management under these often synergistic pressures (Audzijonyte et al., 2016); and
(N6) Supporting marine conservation actions and their efficiency under global change and shifting policies. Climate change and a developing policy landscape (e.g., Blue Growth, UN SDGs) present great challenges for marine conservation, requiring changes in human attitudes, and adaptive and creative approaches, such as adaptive conservation planning (including Marine Protected Areas (MPAs) design) that account for climate hotspots and refugia (Queirós et al., 2016), assisted evolution, and shifting focus from protecting species to protecting ecological functions (Rilov et al., 2020).
Secondary Challenges
In addition to the grand challenges, we have also identified some secondary (S) challenges (Table 2), including:
(S1) Linking ocean health with human health, as in the recent agenda proposed by Borja et al. (2020b)
(S2) Understanding the impacts of alien and neonative (Essl et al., 2019) species on ecosystems. Species modify their natural range and invade new regions either aided by human activities (alien species) or by natural means, tracking human-induced environmental change (neonative species). In both cases, they may substantially modify recipient communities, ecosystem functioning and services. Important knowledge gaps restrict our understanding of traits that facilitate invasions and the magnitude of their impacts, our capacity to predict future shifts in ecosystem processes and functioning due to invasive species, and our ability to propose adequate mitigation measures;
(S3) Assessing urban development and subsequent loss of natural coastlines and ecosystem services (Barragán and de Andrés, 2015)
(S4) Understanding the impacts of human activities as well as climate change in the deep ocean (Levin and Le Bris, 2015; Danovaro et al., 2017)
(S5) Considering the land-ocean continuum, with major terrestrial and riverine inputs to the ocean (Xenopoulos et al., 2017). Better understanding these processes would help resolve massive uncertainties in global ocean function, including nutrient cycling, and especially carbon cycling, tightly linked to climate regulation (Friedlingstein et al., 2019)
(S6) Reassessing and evaluating ecosystem processes under the marine “holobiont” paradigm (Margulis, 1991), meaning that any marine organism is a multispecies entity of host and associated microbes. The role of these microbes in organismal function, performance, interaction and ecological context is grossly underappreciated and hence poorly understood;
(S7) Assessing cumulative effects to guide management, since such assessments are increasingly used to inform environmental policy and guide ecosystem-based management but are inherently complex and seldom linked to management processes (Stelzenmüller et al., 2018). There is a need for developing best practices for the operationalization of cumulative effects assessments in a management context (Greenwood et al., 2019; Stelzenmüller et al., 2020); and
(S8) Investigating emerging pollutants (e.g., plastics and additives, pharmaceuticals), artificial light at night, noise and toxin effects on coastal and marine species, habitats and ecosystems (Chae and An, 2017; Rako-Gospić and Picciulin, 2019), including monitoring and assessment.
Governance and Social Priorities
We identified some major challenges related to governance (G) and social priorities (Table 2), including:
(G1) Using ecological knowledge, as well as traditional knowledge, to meet UN SDGs, and contributing to the UN DOSSD and DER;
(G2) Incorporating new methods into decision support tools for policy frameworks, promoting effective ecosystem-based management (Pinarbaşi et al., 2019);
(G3) Implementing climate-ready Marine Spatial Planning, including the role of MPAs in conserving the oceans, and creating climatic refugia (Queirós et al., 2016; Frazão Santos et al., 2019);
(G4) Developing transnational observation strategies, in the long-term (Moltmann et al., 2019);
(G5) Engaging society more effectively in ocean science, from ocean literacy, to citizen science and participation in supporting management decision making (Pocock et al., 2018; Borja et al., 2020a); and
(G6) Investigating the role of fake news and how we can use science and science communication to offset this (Scheufele and Krause, 2019). Understanding the impact of social media in positive (e.g., citizen science) and negative ways (e.g., dissemination of fake news).
Methodological Priorities
In this section, we identified some methodological (M) priorities, including:
(M1) Further developing and refining molecular tools for marine applications as decision support tools, particularly those related to the implementation of DNA/RNA-based approaches, e.g. metabarcoding (Pochon et al., 2017; Keeley et al., 2018). These are highly promising approaches, but often still have limited direct applications for monitoring and assessment. International standardization of protocols, Quality Assured/Certified laboratory workflows, and minimal reporting standards, which are critical for improved policy-level uptake, are needed (Leese et al., 2018; Pawlowski et al., 2018). Integration of multi-omics tools for understanding ecosystems functioning is also important;
(M2) Addressing problems multidimensionally, taking into account the whole Earth (e.g., planetary boundaries; Nash et al., 2017);
(M3) Achieving “Consilience,” that is, a common path to knowledge by linking facts and fact-based theory across disciplines to create a common groundwork of explanation (Wilson, 1998); this will promote and embrace interdisciplinary and transdisciplinary studies, including e.g., marine ecologists, fisheries scientists, oceanographers, social scientists, economists;
(M4) Acknowledging cultural differences in conducting marine science. Much of the knowledge we produce today is an outcome of many ecologists who share their data and algorithms and release them open and free for access to other scientists and society. All this information can be used in big data and machine learning to tackle all the grand and secondary challenges outlined here (Ma et al., 2018)
(M5) Modeling the future states of marine ecosystems and their services in the face of scenario and process uncertainty (MacNeil et al., 2019). Real limitations still exist with our ability to project and simulate the ecology of a multiple stressors ocean, regime shifts, or extreme climate events (cold snaps, heatwaves); and
(M6) Developing thresholds/targets to assess current and future ecosystems health, especially under climate change (Borja et al., 2012; Queirós et al., 2018).
Final Remark
To adequately address these revised grand challenges over the next 10 years, the FMARS-MEE editors recommend promoting open access to scientific data and publications in order to provide wider distribution of marine ecosystem science, ecological processes, and the complex relationships between biotic and abiotic components, at all levels of biological organization and scales of observation. Free and easy access to data and publications creates a system of information that is transparent, promoting confidence among stakeholders, marine users, policy-makers and the society at large, thus facilitating informed decisions to find solutions for global and ocean-based challenges, such as the UN SDGs, DOSSD and DER. These are core values of FMARS-MEE, enhancing collaborations across the global ocean (Borja et al., 2017; Duarte et al., 2018; Behrenfeld et al., 2019; Duffy et al., 2019; Moltmann et al., 2019).
Statements
Author contributions
AB developed the idea of the paper and wrote the first draft. Each author contributed with ideas for new challenges and contributed equally to the discussion and in writing the final manuscript.
Acknowledgments
This paper was contribution number 973 from AZTI's Marine Research; Basque Research and Technology Alliance (BRTA). Heliana Teixeira thanks FCT/MCTES for the financial support to the host institution CESAM (UIDB/50017/2020+UIDP/50017/2020).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2020.00362/full#supplementary-material
References
1
AudzijonyteA.FultonE.HaddonM.HelidoniotisF.HobdayA. J.KuparinenA.et al. (2016). Trends and management implications of human-influenced life-history changes in marine ectotherms. Fish Fish.17, 1005–1028. 10.1111/faf.12156
2
AylagasE.BorjaA.IrigoienX.Rodriguez-EzpeletaN. (2016). Benchmarking DNA metabarcoding for biodiversity-based monitoring and assessment. Front. Mar. Sci.3:96. 10.3389/fmars.2016.00096
3
BarragánJ. M.de AndrésM. (2015). Analysis and trends of the world's coastal cities and agglomerations. Ocean Coast Manage.114, 11–20. 10.1016/j.ocecoaman.2015.06.004
4
BehrenfeldM. J.MooreR. H.HostetlerC. A.GraffJ.GaubeP.RussellL. M.et al. (2019). The North Atlantic Aerosol and Marine Ecosystem Study (NAAMES): science motive and mission overview. Front. Mar. Sci.6:122. 10.3389/fmars.2019.00122
5
BorjaA. (2014). Grand challenges in marine ecosystems ecology. Front. Mar. Sci.11:1. 10.3389/fmars.2014.00001
6
BorjaÁ.DauerD. M.GrémareA. (2012). The importance of setting targets and reference conditions in assessing marine ecosystem quality. Ecol. Indic.12, 1–7. 10.1016/j.ecolind.2011.06.018
7
BorjaA.ElliottM.AndersenJ. H.BergT.CarstensenJ.HalpernB. S.et al. (2016). Overview of integrative assessment of marine systems: the ecosystem approach in practice. Front. Mar. Sci.3:20. 10.3389/fmars.2016.00020
8
BorjaA.ElliottM.UyarraM. C.CarstensenJ.MeaM. (2017). Bridging the Gap Between Policy and Science in Assessing the Health Status of Marine Ecosystems, 2nd Edn. Lausanne: Frontiers Media. 10.3389/978-2-88945-126-5
9
BorjaA.PrinsT.SimbouraN.AndersenJ. H.BergT.MarquesJ. C.et al. (2014). Tales from a thousand and one ways to integrate marine ecosystem components when assessing the environmental status. Front. Mar. Sci.1:72. 10.3389/fmars.2014.00072
10
BorjaA.SantoroF.ScowcroftG.FletcherS.StrosserP. (2020a). Editorial: connecting people to their oceans: issues and options for effective ocean literacy. Front. Mar. Sci.6:837. 10.3389/fmars.2019.00837
11
BorjaA.WhiteM. P.BerdaletE.BockN.EatockC.KristensenP.et al. (2020b). Moving toward an Agenda on ocean health and human health in Europe. Front. Mar. Sci.7:37. 10.3389/fmars.2020.00037
12
ChaeY.AnY. J. (2017). Effects of micro- and nanoplastics on aquatic ecosystems: current research trends and perspectives. Mar. Pollut. Bull.124, 624–632. 10.1016/j.marpolbul.2017.01.070
13
ChartrandK. M.BryantC. V.CarterA. B.RalphP. J.RasheedM. A. (2016). Light thresholds to prevent dredging impacts on the Great Barrier reef seagrass, Zostera muelleri ssp. capricorni. Front. Mar. Sci.3:106. 10.3389/fmars.2016.00106
14
ClaudetJ.BoppL.CheungW. W. L.DevillersR.Escobar-BrionesE.HauganP.et al. (2020). A roadmap for using the un decade of ocean science for sustainable development in support of science, policy, and action. One Earth2, 34–42. 10.1016/j.oneear.2019.10.012
15
CrainC. M.KroekerK.HalpernB. S. (2008). Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315. 10.1111/j.1461-0248.2008.01253.x
16
DanovaroR.CarugatiL.BerzanoL.CahillA. E.CarvalhoS.ChenuilA.et al. (2016). Implementing and innovating marine monitoring approaches for assessing marine environmental status. Front. Mar. Sci.3:213. 10.3389/fmars.2016.00213
17
DanovaroR.CorinaldesiC.Dell'AnnoA.SnelgroveP. V. R. (2017). The deep-sea under global change. Curr. Biol.27, R461–R465. 10.1016/j.cub.2017.02.046
18
DuarteC. M.Krause-JensenD. (2017). Export from seagrass meadows contributes to marine carbon sequestration. Front. Mar. Sci.4:13. 10.3389/fmars.2017.00013
19
DuarteC. M.Krause-JensenD. (2018). Intervention options to accelerate ecosystem recovery from coastal eutrophication. Front. Mar. Sci.5:470. 10.3389/fmars.2018.00470
20
DuarteC. M.PoinerI.GunnJ. (2018). Perspectives on a global observing system to assess ocean health. Front. Mar. Sci.5:265. 10.3389/fmars.2018.00265
21
DuffyJ. E.Benedetti-CecchiL.TrinanesJ.Muller-KargerF. E.Ambo-RappeR.BoströmC.et al. (2019). Toward a coordinated global observing system for seagrasses and marine macroalgae. Front. Mar. Sci.6:317. 10.3389/fmars.2019.00317
22
EsslF.DullingerS.GenovesiP.HulmeP. E.JeschkeJ. M.KatsanevakisS.et al. (2019). A conceptual framework for range-expanding species that track human-induced environmental change. BioScience69, 908–919. 10.1093/biosci/biz101
23
FaillettazR.ParisC. B.IrissonJ. O. (2018). Larval fish swimming behavior alters dispersal patterns from marine protected areas in the North-Western Mediterranean Sea. Front. Mar. Sci.5:97. 10.3389/fmars.2018.00097
24
Frazão SantosC.EhlerC. N.AgardyT.AndradeF.OrbachM. K.CrowderL. B. (2019). Chapter 30 - marine spatial planning, in World Seas: an Environmental Evaluation, 2nd Edn, ed C. Sheppard (London: Academic Press), 571–592.
25
FriedlingsteinP.JonesM.O'SullivanM.AndrewR.HauckJ.PetersG.et al. (2019). Global carbon budget 2019. Earth Syst. Sci. Data11, 1783–1838. 10.5194/essd-11-1783-2019
26
FuC.Travers-TroletM.VelezL.GrüssA.BundyA.ShannonL. J.et al. (2018). Risky business: The combined effects of fishing and changes in primary productivity on fish communities. Ecol. Model.385, 265–276. 10.1016/j.ecolmodel.2017.12.003
27
GalparsoroI.BorjaA.UyarraM. C. (2014). Mapping ecosystem services provided by benthic habitats in the European North Atlantic Ocean. Front. Mar. Sci.1:23. 10.3389/fmars.2014.00023
28
GillisL. G.JonesC. G.ZieglerA. D.van der WalD.BreckwoldtA.BoumaT. J. (2017). Opportunities for protecting and restoring tropical coastal ecosystems by utilizing a physical connectivity approach. Front. Mar. Sci.4:374. 10.3389/fmars.2017.00374
29
GoodwinK.ThompsonL.DuarteB.KahlkeT.ThompsonA.MarquesJ.et al. (2017). DNA sequencing as tool to monitor marine ecological status. Front. Mar. Sci.4:107. 10.3389/fmars.2017.00107
30
GreenwoodN.DevlinM. J.BestM.FronkovaL.GravesC. A.MilliganA.et al. (2019). Utilizing eutrophication assessment directives from transitional to marine systems in the thames estuary and liverpool bay, UK. Front. Mar. Sci. 6: 10.3389/fmars.2019.00116
31
HalpernB. S.FrazierM.AfflerbachJ.StewartJ. S.MicheliF.O'HaraC.et al. (2019). Recent pace of change in human impact on the world's ocean. Sci. Rep.9:11609. 10.1038/s41598-019-47201-9
32
HeithausM. R.AlcoverroT.ArthurR.BurkholderD. A.CoatesK. A.ChristianenM. J. A.et al. (2014). Seagrasses in the age of sea turtle conservation and shark overfishing. Front. Mar. Sci.1:28. 10.3389/fmars.2014.00028
33
KatsanevakisS.CollM.PiroddiC.SteenbeekJ.Ben Rais LasramF.ZenetosA.et al. (2014). Invading the mediterranean sea: biodiversity patterns shaped by human activities. Front. Mar. Sci.1:32. 10.3389/fmars.2014.00032
34
KeeleyN.WoodS. A.PochonX. (2018). Development and preliminary validation of a multi-trophic metabarcoding biotic index for monitoring benthic organic enrichment. Ecol. Indic.85, 1044–1057. 10.1016/j.ecolind.2017.11.014
35
KorpinenS.AndersenJ. (2016). A global review of cumulative pressure and impact assessments in marine environment. Front. Mar. Sci.3:153. 10.3389/fmars.2016.00153
36
KristensenE.DelefosseM.QuintanaC. O.FlindtM. R.ValdemarsenT. (2014). Influence of benthic macrofauna community shifts on ecosystem functioning in shallow estuaries. Front. Mar. Sci.1:41. 10.3389/fmars.2014.00041
37
LeeseF.BouchezA.AbarenkovK.AltermattF.BorjaÁ.BruceK.et al. (2018). Chapter two - why we need sustainable networks bridging countries, disciplines, cultures and generations for aquatic biomonitoring 2.0: a perspective derived from the DNAqua-net COST action. Adv. Ecol. Res.58, 63–99. 10.1016/bs.aecr.2018.01.001
38
LevinL. A.Le BrisN. (2015). The deep ocean under climate change. Science350, 766–768. 10.1126/science.aad0126
39
LindemannC.St. JohnM. A. (2014). A seasonal diary of phytoplankton in the North Atlantic. Front. Mar. Sci.1:37. 10.3389/fmars.2014.00037
40
LynamC.UusitaloL.PatrícioJ.PiroddiC.QueirosA.TeixeiraH.et al. (2016). Uses of innovative modelling tools within the implementation of the marine strategy framework directive. Front. Mar. Sci.3:182. 10.3389/fmars.2016.00182
41
MaA.BohanD. A.CanardE.DeroclesS. A. P.GrayC.LuX.et al. (2018). Chapter seven - a replicated network approach to ‘Big Data', in Ecology in Advances in Ecological Research, eds. D. A. Bohan, A. J. Dumbrell, G. Woodward, and M. Jackson (London: Academic Press), 225–264.
42
MačićV.AlbanoP. G.AlmpanidouV.ClaudetJ.CorralesX.EsslF.et al. (2018). Biological invasions in conservation planning: a global systematic review. Front. Mar. Sci.5:178. 10.3389/fmars.2018.00178
43
MacNeilM. A.MellinC.MatthewsS.WolffN. H.McClanahanT. R.DevlinM.et al. (2019). Water quality mediates resilience on the Great Barrier Reef. Nat. Ecol. Evol.3, 620–627. 10.1038/s41559-019-0832-3
44
MargulisL. (1991). Symbiosis as a source of evolutionary innovation: speciation and morphogenesis, in Symbiogenesis and Symbionticism (Cambridge MA: MIT Press), 1–14.
45
Mayorga-AdameC. G.BatchelderH. P.SpitzY. H. (2017). Modeling larval connectivity of coral reef organisms in the Kenya-Tanzania region. Front. Mar. Sci.4:92. 10.3389/fmars.2017.00092
46
MoltmannT.TurtonJ.ZhangH.-M.NolanG.GouldmanC.GriesbauerL.et al. (2019). A Global Ocean Observing System (GOOS), delivered through enhanced collaboration across regions, communities, and new technologies. Front. Mar. Sci.6:291. 10.3389/fmars.2019.00291
47
NanningaG. B.BerumenM. L. (2014). The role of individual variation in marine larval dispersal. Front. Mar. Sci.1:71. 10.3389/fmars.2014.00071
48
NashK. L.CvitanovicC.FultonE. A.HalpernB. S.Milner-GullandE. J.WatsonR. A.et al. (2017). Planetary boundaries for a blue planet. Nat. Ecol. Evol.1:1625. 10.1038/s41559-017-0319-z
49
NewtonA.ElliottM. (2016). A typology of stakeholders and guidelines for engagement in transdisciplinary, participatory processes. Front. Mar. Sci.3:230. 10.3389/fmars.2016.00230
50
O'HaraC. C.Villaseñor-DerbezJ. C.RalphG. M.HalpernB. S. (2019). Mapping status and conservation of global at-risk marine biodiversity. Conserv. Lett.12:e12651. 10.1111/conl.12651
51
OrtizJ. C.WolffN. H.AnthonyK. R.DevlinM.LewisS.MumbyP. J. (2018). Impaired recovery of the Great Barrier Reef under cumulative stress. Sci. adv.4:eaar6127. 10.1126/sciadv.aar6127
52
PatrícioJ.ElliottM.MazikK.PapadopoulouN.SmithC. (2016). DPSIR - two decades of trying to develop a unifying framework for marine environmental management?Front. Mar. Sci.3:177. 10.3389/fmars.2016.00177
53
PawlowskiJ.Kelly-QuinnM.AltermattF.Apothéloz-Perret-GentilL.BejaP.BoggeroA.et al. (2018). The future of biotic indices in the ecogenomic era: Integrating (e)DNA metabarcoding in biological assessment of aquatic ecosystems. Sci. Total Environ. 637–638, 1295–1310. 10.1016/j.scitotenv.2018.05.002
54
Pérez-RuzafaA.CampilloS.Fernández-PalaciosJ. M.García-LacunzaA.García-OlivaM.IbañezH.et al. (2019). Long-term dynamic in nutrients, chlorophyll a, and water quality parameters in a coastal lagoon during a process of eutrophication for decades, a sudden break and a relatively rapid recovery. Front. Mar. Sci.6:26. 10.3389/fmars.2019.00026
55
PhillipsG.TeixeiraH.PoikaneS.HerreroF. S.KellyM. G. (2019). Establishing nutrient thresholds in the face of uncertainty and multiple stressors: a comparison of approaches using simulated datasets. Sci. Total Environ.684, 425–433. 10.1016/j.scitotenv.2019.05.343
56
PinarbaşiK.GalparsoroI.BorjaÁ. (2019). End users' perspective on decision support tools in marine spatial planning. Mar. Policy108:103658. 10.1016/j.marpol.2019.103658
57
PochonX.ZaikoA.FletcherL. M.LarocheO.WoodS. A. (2017). Wanted dead or alive? Using metabarcoding of environmental DNA and RNA to distinguish living assemblages for biosecurity applications. PLoS ONE12:e0187636. 10.1371/journal.pone.0187636
58
PocockM. J. O.ChandlerM.BonneyR.ThornhillI.AlbinA.AugustT.et al. (2018). Chapter six - a vision for global biodiversity monitoring with citizen science, in Advances in Ecological Research, eds D. A. Bohan, A. J. Dumbrell, G. Woodward, and M. Jackson (London: Academic Press), 169–223.
59
QueirósA. M.FernandesJ.GenevierL.LynamC. P. (2018). Climate change alters fish community size-structure, requiring adaptive policy targets. Fish Fish.19, 613–621. 10.1111/faf.12278
60
QueirósA. M.HuebertK. B.KeylF.FernandesJ. A.StolteW.MaarM.et al. (2016). Solutions for ecosystem-level protection of ocean systems under climate change. Glob. Change Biol.22, 3927–3936. 10.1111/gcb.13423
61
Rako-GospićN.PicciulinM. (2019). Chapter 20 - underwater noise: sources and effects on marine life, in World Seas: an Environmental Evaluation, 2nd Edn, ed C. Sheppard (London: Academic Press), 367–389. 10.1016/B978-0-12-805052-1.00023-1
62
RenaudP. E.LøkkenT. S.JørgensenL. L.BergeJ.JohnsonB. J. (2015). Macroalgal detritus and food-web subsidies along an Arctic fjord depth-gradient. Front. Mar. Sci.2:31. 10.3389/fmars.2015.00031
63
RilovG.FraschettiS.GissiE.PipitoneC.BadalamentiF.TamburelloL.et al. (2020). A fast-moving target: achieving marine conservation goals under shifting climate and policies. Ecol. Appl.30:e02009. 10.1002/eap.2009
64
RobinsonN. M.NelsonW. A.CostelloM. J.SutherlandJ. E.LundquistC. J. (2017). A systematic review of marine-based species distribution models (SDMs) with recommendations for best practice. Front. Mar. Sci.4:421. 10.3389/fmars.2017.00421
65
RochaJ.YletyinenJ.BiggsR.BlencknerT.PetersonG. (2015). Marine regime shifts: drivers and impacts on ecosystems services. Phil. Trans. R. Soc. B370:20130273. 10.1098/rstb.2013.0273
66
RouseS.LaceyN. C.HayesP.WildingT. A. (2019). Benthic conservation features and species associated with subsea pipelines: considerations for decommissioning. Front. Mar. Sci.6:00. 10.3389/fmars.2019.00200
67
ScheufeleD. A.KrauseN. M. (2019). Science audiences, misinformation, and fake news. Proc. Natl. Acad. Sci. U.S.A.116, 7662–7669. 10.1073/pnas.1805871115
68
SmithC.PapadopoulouK.-N.BarnardS.MazikK.ElliottM.PatrícioJ.et al. (2016). Managing the marine environment, conceptual models and assessment considerations for the European marine strategy framework directive. Front. Mar. Sci.3:144. 10.3389/fmars.2016.00144
69
StelzenmüllerV.CollM.CormierR.MazarisA. D.PascualM.LoiseauC.et al. (2020). Operationalizing risk-based cumulative effect assessments in the marine environment. Sci. Total Environ.724:138118. 10.1016/j.scitotenv.2020.138118
70
StelzenmüllerV.CollM.MazarisA. D.GiakoumiS.KatsanevakisS.PortmanM.et al. (2018). A risk-based approach to cumulative effect assessments for marine management. Sci. Total Environ.612, 1132–1140. 10.1016/j.scitotenv.2017.08.289
71
St. JohnM. A.BorjaA.ChustG.HeathM.GrigorovI.MarianiP.et al. (2016). A dark hole in our understanding of marine ecosystems and their services: perspectives from the mesopelagic community. Front. Mar. Sci.3:31. 10.3389/fmars.2016.00031
72
TamJ. C.LinkJ. S.LargeS. I.AndrewsK.FriedlandK. D.GoveJ.et al. (2017). Comparing apples to oranges: common trends and thresholds in anthropogenic and environmental pressures across multiple marine ecosystems. Front. Mar. Sci.4:282. 10.3389/fmars.2017.00282
73
ThomsenM. S.MondardiniL.AlestraT.GerrityS.TaitL.SouthP. M.et al. (2019). Local extinction of bull kelp (Durvillaea spp.) due to a marine heatwave. Front. Mar. Sci.6:84. 10.3389/fmars.2019.00084
74
Vázquez-LuisM.ÁlvarezE.BarrajónA.García-MarchJ. R.GrauA.HendriksI. E.et al. (2017). S.O.S. Pinna nobilis: a mass mortality event in the Western Mediterranean Sea. Front. Mar. Sci.4:220. 10.3389/fmars.2017.00220
75
VellendM.DornelasM.BaetenL.BeauséjourR.BrownC. D.De FrenneP.et al. (2017). Estimates of local biodiversity change over time stand up to scrutiny. Ecology98, 583–590. 10.1002/ecy.1660
76
VisbeckM.Kronfeld-GoharaniU.NeumannB.RickelsW.SchmidtJ.van DoornE.et al. (2014). A Sustainable development goal for the ocean and coasts: global ocean challenges benefit from regional initiatives supporting globally coordinated solutions. Mar. Policy49:87–89. 10.1016/j.marpol.2014.02.010
77
WilsonE. O. (1998). Consilience: The Unity of Knowledge. Vintage Books, A Division of Random House.New York, NY.
78
XavierJ. C.BrandtA.Ropert-CoudertY.BadheR.GuttJ.HavermansC.et al. (2016). Future challenges in Southern Ocean ecology research. Front. Mar. Sci.3:94. 10.3389/fmars.2016.00094
79
XenopoulosM. A.DowningJ. A.KumarM. D.Menden-DeuerS.VossM. (2017). Headwaters to oceans: ecological and biogeochemical contrasts across the aquatic continuum. Limnol. Oceanogr.62, S3–S14. 10.1002/lno.10721
80
YoungT. P.SchwartzM. W. (2019). The decade on ecosystem restoration is an impetus to get it right. Conserv. Sci. Pract. 1:e145. 10.1111/csp2.145
Summary
Keywords
biodiversity, ecosystem functioning, human pressures, global change, ecosystem health assessment, ecosystem services, conservation and protection, ecosystem-based management
Citation
Borja A, Andersen JH, Arvanitidis CD, Basset A, Buhl-Mortensen L, Carvalho S, Dafforn KA, Devlin MJ, Escobar-Briones EG, Grenz C, Harder T, Katsanevakis S, Liu D, Metaxas A, Morán XAG, Newton A, Piroddi C, Pochon X, Queirós AM, Snelgrove PVR, Solidoro C, St. John MA and Teixeira H (2020) Past and Future Grand Challenges in Marine Ecosystem Ecology. Front. Mar. Sci. 7:362. doi: 10.3389/fmars.2020.00362
Received
27 February 2020
Accepted
29 April 2020
Published
03 June 2020
Volume
7 - 2020
Edited and reviewed by
Martin Edwards, Marine Biological Association, United Kingdom
Updates
Copyright
© 2020 Borja, Andersen, Arvanitidis, Basset, Buhl-Mortensen, Carvalho, Dafforn, Devlin, Escobar-Briones, Grenz, Harder, Katsanevakis, Liu, Metaxas, Morán, Newton, Piroddi, Pochon, Queirós, Snelgrove, Solidoro, St. John and Teixeira.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Angel Borja aborja@azti.es
This article was submitted to Marine Ecosystem Ecology, a section of the journal Frontiers in Marine Science
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.