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Front. Mar. Sci., 05 September 2017 | https://doi.org/10.3389/fmars.2017.00268

The Structuring Role of Marine Life in Open Ocean Habitat: Importance to International Policy

Bethan C. O'Leary* and Callum M. Roberts
  • Environment Department, University of York, York, United Kingdom

Areas beyond national jurisdiction (ABNJ) lie outside the 200 nautical mile limits of national sovereignty and cover 58% of the ocean surface. Global conservation agreements recognize biodiversity loss in ABNJ and aim to protect ≥10% of oceans in marine protected areas (MPAs) by 2020. However, limited mechanisms to create MPAs in ABNJ currently exist, and existing management is widely regarded as inadequate to safeguard biodiversity. Negotiations are therefore underway for an “internationally legally binding instrument” (ILBI) to the United Nations Convention on the Law of the Sea to enable biodiversity conservation beyond national jurisdiction. While this agreement will, hopefully, establish a mechanism to create MPAs in ABNJ, discussions to date highlight a further problem: namely, defining what to protect. We have a good framework for terrestrial and coastal habitats, however habitats in ABNJ, particularly the open ocean, are less understood and poorly defined. Often, predictable broad oceanographic features are used to define open ocean habitats. But what exactly, constitutes the habitat—the water, or the species that live there? Complicating matters, species in the open sea are often highly mobile. Here, we argue that mobile marine organisms provide the structure-forming biomass and constitute “habitat” in the open ocean. For an ABNJ ILBI to offer effective protection to marine biodiversity it must consider habitats a function of their inhabitants and represent all marine life within its scope. Only by enabling strong protection for every element of biodiversity can we hope to be fully successful in conserving it.

Introduction

Areas beyond national jurisdiction (ABNJ) cover 58% of the ocean surface and lie outside the 200 nautical mile limits of national sovereignty (exclusive economic zones). International concern has steadily increased over the multiplication and intensification of threats to marine biodiversity in ABNJ, fragmented and uncoordinated management, and the lack of a comprehensive legal framework to properly address threats (Ban et al., 2014; Merrie et al., 2014; Gjerde et al., 2016; Wright et al., 2016). Global agreements on environmental protection recognize steep biodiversity losses in ABNJ and have set targets to protect >10% of coastal and marine areas in marine protected areas (MPAs) (Convention on Biological Diversity, 2010; United Nations, 2015). However, there is presently no agreed mechanism to protect biodiversity in ABNJ.

Following 10 years of informal negotiations, in March 2016 delegates from 193 countries, and representatives from numerous intergovernmental and non-governmental organizations, met at the United Nations (UN) in New York for the first of four meetings to negotiate the elements of an “international legally binding instrument” (ILBI) for the conservation and sustainable use of biodiversity beyond national jurisdiction under the UN Convention on the Law of the Sea (UNCLOS). These negotiations are framed by four issues which delegates have agreed must be considered “together and as a whole”: (1) marine genetic resources, including benefit sharing; (2) area-based management tools, including MPAs; (3) environmental impact assessments; and (4) capacity building and the transfer of marine technology (UNGA, 2015; Gjerde et al., 2016; Wright et al., 2016) This process should result in recommendations to the UN General Assembly by the end of 2017.

If successful, these negotiations will lead to an intergovernmental negotiating conference in 2018 to improve governance and management of biodiversity beyond national jurisdiction. However, while the ILBI will, hopefully, facilitate conservation and sustainable use of biodiversity in ABNJ, including a mechanism for establishing MPAs, these discussions highlight a further problem: namely, defining what to protect.

Existing global targets measure progress toward biodiversity conservation using the extent of ecosystems and habitats covered by protected areas (Convention on Biological Diversity, 2010). However, while we have a good working framework for terrestrial and coastal habitats, habitats in ABNJ, and particularly the open ocean, are less understood and poorly defined (e.g., IUCN, 2017). To inform these discussions we consider what constitutes “habitat” in the largely fluid environment of the open ocean.

Relating Habitat Concepts to Areas Beyond National Jurisdiction

Habitat or ecosystem concepts overlap substantially. The Convention on Biological Diversity (CBD) (Article 2) defines “ecosystem” as “a dynamic complex of plant, animal and micro-organism communities and their non-living environment interacting as a functional unit,” and “habitat” as “the place or type of site where an organism or population naturally occurs” (Convention on Biological Diversity, 2010). The definitions are therefore interrelated, and application of the terms is scale-dependent.

Even without clear definitions, the idea that the world is divided into a series of ecosystems and habitats is most easily grasped when fixed entities comprise a habitat with discrete boundaries (although visible boundaries often conceal complex networks of wider connections that may be overlooked–Box 1). For instance, on land it is easy to conceive where a lake or forest end and a different habitat or ecosystem begins. This principle clearly translates to coastal systems where, for example, mangrove trees, seagrass meadows, or coral and oyster reefs act as easily defined structuring elements. Similarly, some habitats in ABNJ, especially seabed features such as seamounts, hydrothermal vents, and ocean ridges, offer defined features around which boundaries can be drawn using traditional principles.

Box 1. Considering complex connections amongst ecosystems in the MPA context.

Whether on land or in the sea, ecosystems are an interconnected continuum in space and time across living and non-living realms. While ecosystems on land may be easier to perceive and define as distinct entities, it is increasingly understood that successful management and conservation must incorporate connectivity with the surrounding environment. For example, migratory salmon are an important mediator of marine-derived nutrients to freshwater and riparian habitats and the animals that rely on them; without considering the underlying ecology and importance of salmon in these systems, management is unlikely to achieve desired outcomes of maintaining habitat diversity, structure and function (Darimont et al., 2010; Artelle et al., 2016). Similarly, anthropogenic nutrient inputs from land may result in eutrophication of freshwater, estuarine, and coastal ecosystems leading to dead zones (Diaz and Rosenberg, 2008), harmful algal blooms (Heisler et al., 2008), contaminated water and seafood (Heisler et al., 2008), and increased mortality of wildlife (Fey et al., 2015). Broader considerations than simply the apparent spatial footprint of a habitat are therefore needed to attain management and conservation objectives.

The same broad approach applies to management in ABNJ. A seamount or hydrothermal vent ecosystem, for example, is not just a reflection of the bathymetric feature but rather a combination of influences which includes the water column and the creatures on and within it (Clark et al., 2010; Levin et al., 2016). Nutrient and food subsidies from seeps and vents influence surrounding fish and fisheries (Grupe et al., 2015) in a similar manner to coastal habitats such as seagrass meadows (Heck et al., 2008), although quantification is still limited. Other seabed features likely exert similar influences (Morato et al., 2010; Letessier et al., 2016). The vertical and horizontal footprint of such ecosystems is therefore much larger than simply where the physical habitat manifests, with the extent and scales of influence varying from place to place and among ecosystems (e.g., Levin et al., 2016). At the sea surface, distinctive habitats based on oceanographic features and areas of high productivity and biodiversity are identifiable using sea surface temperature, temperature at depth, chlorophyll, and nitrates among other variables (e.g., Hobday et al., 2011). Beneath these areas often lie diverse seabed ecosystems (Woolley et al., 2016) with nutrients, dissolved organic matter, and minerals moved through the water column, mediated by marine life as well as topographically induced currents, which influence both seabed and water column habitat characteristics (Turner, 2015; Soetaert et al., 2016).

For an international legally binding instrument for biodiversity protection beyond national jurisdiction under the UN Convention on the Law of the Sea to be effective, it needs to ensure these broader considerations are incorporated. To achieve this, species and habitat conservation need to be integrated, recognizing that habitats will not be protected if their component species are not.

Fluid realms, such as the open ocean (Norse, 2005) and airspace (Diehl, 2013), challenge our conception and application of habitat and ecosystem ideas. Predictable, broad oceanographic features, such as frontal zones, which aggregate nutrients and food and attract predators, offer opportunities to delineate boundaries (Scales et al., 2014). But what exactly defines the habitat? Is it the water, or the species that live there? With the exception of floating Sargassum weed (Hemphill, 2005), there is little structure-forming biomass in pelagic systems and even this is not fixed in space. The biomass present is held in the bodies of the creatures that live in the water and is highly mobile. It is those creatures, and the ecological roles they fulfill, we argue, that constitute “habitat” in the open sea.

Habitats as a Function of Their Inhabitants

Living and non-living realms interact to characterize ecosystems. The occupants of any habitat create and alter the system they live within. Species that create more complex habitat by modulating the availability of resources to other species are known as “ecosystem engineers” (Jones et al., 1994). Most research identifying marine organisms as ecosystem engineers has focused on species that either attach or interact with seabed communities, such as corals, bivalves, seagrasses, and species that modify sediments (e.g., Soetaert et al., 2016). Only recently have some begun to explore the potential for other marine organisms to act as ecosystem engineers. Examples in the open ocean include phytoplankton and zooplankton (Jones et al., 1994; Breitburg et al., 2010), and baleen and sperm whales (Roman et al., 2014).

The structuring role of plankton in pelagic food-webs has long been recognized. They are critical to ecosystem function, and their abundance and biomass determines the distribution and productivity of marine life (Chassot et al., 2010; Watson et al., 2015). However, plankton may also be considered ecosystem engineers—affecting the photic, chemical and thermal regimes of water and consequently the suitability of that habitat for other life (Haury et al., 1978; Duffy and Stachowicz, 2006; Breitburg et al., 2010). For example, Antarctic krill (Euphausia superba) are a fundamental food source for predators from squid to baleen whales (Constable et al., 2000), play a major role in ocean productivity by recycling iron in surface waters (Nicol et al., 2010), alter organic matter and trace element concentrations in surface waters during molting (Nicol and Stolp, 1989), and may be an important carbon sink (Swadling, 2006; Tarling and Johnson, 2006). However, most research examines krill-based food-webs or environmental factors affecting their populations rather than their influence on the non-living realm. Advances in technology and increased demand are anticipated to expand zooplankton fisheries in the future leading to calls for precautionary management to avert adverse ecosystem and habitat consequences of exploitation (Nicol et al., 2012; Brotz, 2016; Kawaguchi and Melle, 2016).

Emerging evidence suggests that mobile marine species can transform the environment as they move through it, transferring nutrients within the water column (deep to shallow and vice versa) and across oceans (Wilson et al., 2009; Pershing et al., 2010; Roman and McCarthy, 2010; Roman et al., 2014; St John et al., 2016). For example, depletion of whales due to commercial whaling resulted in substantial deep-sea habitat loss through a reduction in dead whale “falls” (Smith, 2007), declines in primary productivity due to reduced nutrient shuttling (Nicol et al., 2010; Roman and McCarthy, 2010), changes in food-web structure and biogeochemical cycles (Lavery et al., 2010; Roman and McCarthy, 2010), and reduced potential for organic carbon sequestration (Lavery et al., 2010; Pershing et al., 2010). The consequences of extraction therefore extended far beyond the decline of individual whale species.

Similar ecosystem-wide changes can be expected from exploitation of other large-bodied or highly abundant marine animals. For instance, mesopelagic fish (200–1,000 m) undertake daily migrations between near-surface and deep water (Robinson et al., 2010). Estimates suggest the global biomass of mesopelagic fish is on the order of 10 billion tones and, while there is uncertainty in this number, they likely represent the most abundant vertebrates on Earth (Irigoien et al., 2014) and the largest structuring biomass in the open sea. Their mass migration provides critical links in biogeochemical cycles across the water column, promoting carbon uptake and storage, thereby affecting climate regulation (Robinson et al., 2010; Giering et al., 2014; St John et al., 2016), modifies fluxes of nutrients and oxygen (Robinson et al., 2010; Bianchi et al., 2013a,b), and helps sustain the metabolic requirements of mesopelagic ecosystems (Burd et al., 2010; Bianchi et al., 2013b). They are also a key resource for higher trophic levels such as tunas and billfish (Potier et al., 2007; Duffy et al., 2017). There is increasing interest in exploiting mesopelagic fish, particularly for fishmeal and oil, but technical and economic constraints still prevent large-scale commercial activity (St John et al., 2016). Nonetheless, licenses to fish mesopelagics have been issued by Norway and Pakistan (The Economist, 2017), although the US has proactively prohibited directed commercial fisheries in its Pacific Ocean due to concerns over potential adverse ecosystem consequences (NOAA, 2016).

Many exploited marine species such as billfish, tuna, sharks, and rays that spend time in ABNJ regularly undertake extensive horizontal movements and deep-dives into the meso- and even bathypelagic (1,000–4,000 m) realms (Thorrold et al., 2014; Abascal et al., 2015; Fuller et al., 2015; Howey et al., 2016). Their roles in biogeochemical cycles are largely unquantified, but the movements link surface waters and the deep ocean and are likely to influence habitat characteristics in a similar manner to whales and mesopelagic fish.

Mobile, open ocean predators also structure habitats through their physical presence and behaviors. For example, hunting pelagic fish such as tuna provide visual cues to seabirds enabling prey detection over greater distances and enhancing bird foraging success by forcing prey close to the surface (Maxwell and Morgan, 2013). Other marine organisms may control the abundance of prey or act as food, either directly or through detritus, influences that change across life stages (Young et al., 2015). Although rarely considered this way, these roles are analogous in their significance to the structuring influence of kelp or seagrass in coastal habitats.

There are many examples of altered ocean food-web dynamics following depletion of apex predators. For example, the recent range expansion of the Humboldt squid into the eastern North Pacific has been linked to reduced predation and competition with large predatory fish targeted by fisheries, and expanded low oxygen waters (Zeidberg and Robison, 2007). Predator depletion has well-known effects on coastal habitats, e.g., sea otter loss led to kelp decline due to reduced predation on herbivores (Estes et al., 2011), and overfishing of apex predators has altered trophic structure leading to increased abundance of mid-size predators (Heithaus et al., 2008; Ritchie and Johnson, 2009; Ferretti et al., 2010; Ortuño Crespo and Dunn, 2017). In the open ocean, where ecosystems are defined by their inhabitants, community level impacts equate to ecosystem impacts. While the ecological impacts of apex predator depletion in ABNJ are poorly understood, by inference from known cases they can be expected to be significant.

Unifying Habitat and Species Protection in Areas Beyond National Jurisdiction

A habitat is malleable—preserving it in a particular state requires protection of the things that make it distinctive and recognizable. A woodland will not remain a woodland without protection for trees. It is easy to understand this because we can see the difference cutting down trees makes. However, protecting trees does not produce the same forest as protecting trees and all the species that live in and around them (Brodie, 2016), although the assumption is often made that it does. Similarly, protecting a seafloor habitat without protecting the species that regulate it, such as parrotfish in coral reefs (Mumby, 2009) or spiny lobster in kelp forests (Halpern et al., 2006), will alter the functioning and resilience of that habitat if those species are depleted. In the open ocean it is much harder to understand that removing big, predatory or highly abundant fish or marine mammals transforms an open sea habitat because it looks much the same as before. But the nature of open water habitats is also dictated by what occupies the space.

Nature conservation often operates on two levels, habitat and species protection, with protection added in layers through different laws and in varying mixes. Such an approach can create perverse outcomes, however, when the inanimate is emphasized at the expense of the animate. For example, it is unclear to many, including nature conservation bodies, what protecting shallow, sub-tidal sandbanks under the EU Habitats Directive should entail. Does it mean ensuring the sand remains where it is, or is there some obligation to protect the animals and plants that live on or around sandbanks? Most people would assume the latter, yet in many cases, there is no protection given to Special Areas of Conservation from highly disturbing and destructive practices like bottom trawling and dredging (Plumeridge and Roberts, 2017). It is the sand, not wildlife, that prevails under this stewardship. The physical characteristics of an area act only as a placeholder for the life that could or does occupy it. Areas little affected by human activity will possess the most intact communities (D'agata et al., 2016), others will need to rebuild their wildlife under protection. The habitat that results from protection therefore depends on the level of protection given and even the most diligent network design schemes will fail if the sites chosen get little protection. Strongly and fully protected MPAs (Lubchenco and Grorud-Colvert, 2015) therefore promote the highest levels of complexity and the most intact ecosystems (Edgar et al., 2014).

Conclusions and Suggestions

Given the horizontal and vertical spread of human activities through ABNJ (Merrie et al., 2014), the structure and function of open ocean habitats has certainly altered over time (Ortuño Crespo and Dunn, 2017). While some land-based habitats retain high conservation value as a function of human use, e.g., highly diverse flower meadows from seasonal cutting and grazing regimes, or understory flowers, insects and birds from coppiced woodlands, we are not aware of any comparable examples in the sea. Evidence that mobile species benefit from spatial protection in national waters is increasing (Jensen et al., 2010; Edgar et al., 2014; Dunphy-Daly, 2015). Likewise, protection could offer benefits to such species in ABNJ but the extensive movements of many of the animals inhabiting these regions reinforce the need for strong complementary protection measures to be applied outside MPA boundaries. Such measures could include dynamic management, effective fisheries regulation and, increasingly, precautionary regulation of emerging activities (Dunn et al., 2011, 2016; Maxwell et al., 2015; Jaeckel et al., 2017).

On purely biological grounds, the case is clear for fish and other exploited species to be an integral part of any agreement to protect biodiversity in ABNJ. Current negotiations consider what marine life and activities should be covered by any new protective legislation, and whether MPAs should be established through a new overarching mechanism or through existing regional and sectoral frameworks. The argument frequently made is that fisheries management bodies have a legal remit and competence to manage fisheries and are therefore best placed to look after fish (Vincent et al., 2014). But these bodies have so far failed to safeguard fisheries or fish (Gilman et al., 2014), are often limited to certain species, do not comprehensively cover the oceans, and introduce measures only applicable to members (Vincent et al., 2014). Furthermore, other activities in ABNJ affect marine life (e.g., Ramirez-Llodra et al., 2011) over which fisheries bodies have no remit. Objectives of MPAs go beyond tackling fishery problems, addressing threats from other activities such as maritime traffic or oil, mineral and genetic resource exploration and exploitation, as well as protecting biodiversity and ecosystem structure and function, and supporting cultural values and ecosystem services.

Given the indivisibility between species and habitats, and the potential for cumulative impacts from human activities currently managed separately, protection of biodiversity in ABNJ will require comprehensive and strategic management across sectors. Moving from a regional to global approach would also: promote universal participation; allow comprehensive environmental impact assessments to established standards that address cumulative impacts from different activities; provide a mandate to implement ecologically representative MPA networks; and help harmonize the implementation of UNCLOS with the CBD, Sustainable Development Goals, the Paris Agreement, and other instruments. Furthermore, the interrelatedness of the four issues framing the ABNJ ILBI negotiations cannot be addressed in isolation from each other. For example, environmental impact assessments will promote informed decisions regarding acceptable levels of harm from activities on marine life which represent genetic and provisioning resources, prior to activities being undertaken. While negotiations are constrained by the requirement that any new agreement “should not undermine existing relevant legal instruments and frameworks and relevant global, regional and sectoral bodies” (UNGA, 2015), the opportunity is there to unify existing regulatory and governance mechanisms and fill gaps where they exist.

Protection of animal life is crucial in the open ocean, because they structure the habitats there. Therefore, targets for habitat protection beyond national jurisdiction can only be fully met by protecting animal and plant communities in their entirety. Globally, efforts to align habitats and species conservation have increased in recent years. For example, 66 Ecologically and Biologically Significant Areas have been defined under the CBD that cover places in ABNJ (Bax et al., 2016) and the IUCN is developing a Red List for Ecosystems which includes marine habitats (Keith et al., 2015). Other efforts are pioneering approaches to identify important areas based on species distributions (e.g., Key Biodiversity Areas, Edgar et al., 2008; Important Marine Mammal Areas, Corrigan et al., 2014). These efforts are designed to inform global policy and future decisions regarding protection. Achieving habitat representation under global conservation targets will involve selecting sites for protection identified through these and similar efforts. Habitat conservation in whichever places are chosen for protection, however, will only be successful if MPAs and other measures safeguard more than just water, offering real refuges and protection for the creatures that define open sea habitats.

The ongoing UN negotiations for the conservation and sustainable use of biodiversity beyond national jurisdiction present a unique opportunity to move from a sectoral and fragmented ABNJ management system to one that is holistic and based on the ecosystem approach. To be effective the ILBI should consider habitats a function of their inhabitants and represent all marine life within its scope. To do otherwise will fail to improve governance and management of ABNJ and undermine our ability to recover depleted species and repair degraded habitats.

Author Contributions

All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.

Funding

BO' is supported by The Pew Charitable Trusts.

Conflict of Interest Statement

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.

Acknowledgments

We would like to thank our three reviewers for their constructive comments that greatly improved this manuscript.

References

Abascal, F. J., Mejuto, J., Quintans, M., Garcia-Cortes, B., and Ramos-Cartelle, A. (2015). Tracking of the broadbill swordfish, Xiphias gladius, in the central and eastern North Atlantic. Fish Res. 162, 20–28. doi: 10.1016/j.fishres.2014.09.011

CrossRef Full Text | Google Scholar

Artelle, K. A., Anderson, S. C., Reynolds, J. D., Cooper, A. B., Paquet, P. C., and Darimont, C. T. (2016). Ecology of conflict: marine food supply affects human-wildlife interactions on land. Sci. Rep. 6:25936. doi: 10.1038/srep25936

PubMed Abstract | CrossRef Full Text | Google Scholar

Ban, N. C., Bax, N. J., Gjerde, K. M., Devillers, R., Dunn, D. C., Dunstan, P. K., et al. (2014). Systematic conservation planning: a better recipe for managing the high seas for biodiversity conservation and sustainable use. Conserv. Lett. 7, 41–54. doi: 10.1111/conl.12010

CrossRef Full Text | Google Scholar

Bax, N. J., Cleary, J., Donnelly, B., Dunn, D. C., Dunstan, P. K., Fuller, M., et al. (2016). Results of efforts by the Convention on Biological Diversity to describe ecologically or biologically significant marine areas. Conserv. Biol. 30, 571–581. doi: 10.1111/cobi.12649

PubMed Abstract | CrossRef Full Text | Google Scholar

Bianchi, D., Galbraith, E. D., Carozza, D. A., Mislan, K. A. S., and Stock, C. A. (2013a). Intensification of open-ocean oxygen depletion by vertically migrating animals. Nat. Geosci. 6, 545–548. doi: 10.1038/ngeo1837

CrossRef Full Text | Google Scholar

Bianchi, D., Stock, C., Galbraith, E. D., and Sarmiento, J. L. (2013b). Diel vertical migration: ecological controls and impacts on the biological pump in a one-dimensional ocean model. Global Biogeochem. Cy. 27, 478–491. doi: 10.1002/gbc.20031

CrossRef Full Text | Google Scholar

Breitburg, D. L., Crump, B. C., Dabiri, J. O., and Gallegos, C. L. (2010). Ecosystem engineers in the Pelagic Realm: alteration of habitat by species ranging from microbes to jellfish. Integr. Comp. Biol. 50, 188–200. doi: 10.1093/icb/icq051

PubMed Abstract | CrossRef Full Text | Google Scholar

Brodie, J. F. (2016). How monkeys sequester carbon. Trends Ecol. Evol. 31, 414–416. doi: 10.1016/j.tree.2016.03.019

PubMed Abstract | CrossRef Full Text | Google Scholar

Brotz, L. (2016). “Jellyfish fisheries: a global assessment,” in Global Atlas of Marine Fisheries: A Critical Appraisal of Catches and Ecosystem Impacts, eds D. Pauly and D. Zeller (Washington, DC: Island Press), 110–124.

Google Scholar

Burd, A. B., Hansell, D. A., Steinberg, D. K., Anderson, T. R., Aristegui, J., Baltar, F., et al. (2010). Assessing the apparent imbalance between geochemical and biochemical indicators of meso- and bathypelagic biological activity: what the @#! is wrong with present calculations of carbon budgets? Deep Sea Res. II 57, 1557–1571. doi: 10.1016/j.dsr2.2010.02.022

CrossRef Full Text | Google Scholar

Chassot, E., Bonhommeau, S., Dulvy, N. K., Mélin, F., Watson, R., Gascuel, D., et al. (2010). Global marine primary production constrains fisheries catches. Ecol. Lett. 13, 495–505. doi: 10.1111/j.1461-0248.2010.01443.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Clark, M. R., Rowden, A. A., Schlacher, T., Williams, A., Consalvey, M., Stocks, K. I., et al. (2010). The ecology of seamounts: structure, function, and human impacts. Ann. Rev. Mar. Sci. 2, 253–278. doi: 10.1146/annurev-marine-120308-081109

PubMed Abstract | CrossRef Full Text | Google Scholar

Constable, A. J., de la Mare, W. K., Agnew, D. J., Everson, I., and Miller, D. (2000). Managing fisheries to conserve the Antarctic marine ecosystem: practical implementation of the Convention on the Conservation of Antarctic Marine Living Resources (CCAMLR). ICES J. Mar. Sci. 57, 778–791. doi: 10.1006/jmsc.2000.0725

CrossRef Full Text | Google Scholar

Convention on Biological Diversity (2010). TARGET 11 - Technical Rationale Extended (Provided in Document COP/10/INF/12/Rev.1). Available online at: https://www.cbd.int/sp/targets/rationale/target-11/ (Accessed Jan 12, 2017)

Corrigan, C. M., Ardron, J. A., Comeros-Raynal, M. T., Hoyt, E., Notarbartolo di Sciara, G., and Carpenter, K. E. (2014). Developing important marine mammal area criteria: learning from ecologically or biologically significant areas and key biodiversity areas. Aquat. Conserv. 24, 166–183. doi: 10.1002/aqc.2513

CrossRef Full Text | Google Scholar

D'agata, S., Mouillot, D., Wantiez, L., Friedlander, A. M., Kulbicki, M., and Vigliola, L. (2016). Marine reserves lag behind wilderness in the conservation of key functional roles. Nat. Commun. 7:12000. doi: 10.1038/ncomms12000

PubMed Abstract | CrossRef Full Text | Google Scholar

Darimont, C. T., Bryan, H. M., Carlson, S. M., Hocking, M. D., MacDuffee, M., Paquet, P. C., et al. (2010). Salmon for terrestrial protected areas. Conserv. Lett. 3, 379–389. doi: 10.1111/j.1755-263X.2010.00145.x

CrossRef Full Text | Google Scholar

Diaz, R. J., and Rosenberg, R. (2008). Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929. doi: 10.1126/science.1156401

PubMed Abstract | CrossRef Full Text | Google Scholar

Diehl, R. H. (2013). The airspace is habitat. Trends Ecol. Evolut. 28, 377–379. doi: 10.1016/j.tree.2013.02.015

PubMed Abstract | CrossRef Full Text | Google Scholar

Duffy, J. E., and Stachowicz, J. J. (2006). Why biodiversity is important to oceanography: potential roles of genetic, species, and trophic diversity in pelagic ecosystem processes. Mar. Ecol. Prog. Ser. 311, 179–189. doi: 10.3354/meps311179

CrossRef Full Text | Google Scholar

Duffy, L. M., Kuhnert, P. M., Pethybridge, H. R., Young, J. W., Olson, R. J., Logan, J. M., et al. (2017). Global trophic ecology of yellowfin, bigeye, and albacore tunas: understanding predation on micronekton communities at ocean-basin scales. Deep Sea Res. II 140, 55–73. doi: 10.1016/j.dsr2.2017.03.003

CrossRef Full Text | Google Scholar

Dunn, D. C., Boustany, A. M., and Halpin, P. N. (2011). Spatio-temporal management of fisheries to reduce by-catch and increase fishing selectivity. Fish Fish. 12, 110–119. doi: 10.1111/j.1467-2979.2010.00388.x

CrossRef Full Text | Google Scholar

Dunn, D. C., Maxwell, S. M., Boustany, A. M., and Halpin, P. N. (2016). Dynamic ocean management increases the efficiency and efficacy of fisheries management. Proc. Natl. Acad. Sci. U.S.A. 113, 668–673. doi: 10.1073/pnas.1513626113

PubMed Abstract | CrossRef Full Text | Google Scholar

Dunphy-Daly, M. M. (2015). A Meta-Analysis of the Value of Marine Protected Areas for Pelagic Apex Predators. Durham, NC: Duke University.

Google Scholar

Edgar, G. J., Langhammer, P. F., Allen, A., Brooks, T. M., Brodie, J., Crosse, W., et al. (2008). Key biodiversity areas as globally significant target sites for the conservation of marine biological diversity. Aquat. Conserv. 18, 969–983. doi: 10.1002/aqc.902

CrossRef Full Text | Google Scholar

Edgar, G. J., Stuart-Smith, R. D., Willis, T. J., Kininmonth, S., Baker, S. C., Banks, S., et al. (2014). Global conservation outcomes depend on marine protected areas with five key features. Nature 506, 216–220. doi: 10.1038/nature13022

PubMed Abstract | CrossRef Full Text | Google Scholar

Estes, J. A., Terborgh, J., Brashares, J. S., Power, M. E., Berger, J., Bond, W. J., et al. (2011). Trophic downgrading of planet Earth. Science 333, 301–306. doi: 10.1126/science.1205106

PubMed Abstract | CrossRef Full Text | Google Scholar

Ferretti, F., Worm, B., Britten, G. L., Heithaus, M. R., and Lotze, H. K. (2010). Patterns and ecosystem consequences of shark declines in the ocean. Ecol. Lett. 13, 1055–1071. doi: 10.1111/j.1461-0248.2010.01489.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Fey, S. B., Siepielski, A. M., Nusslé, S., Cervantes-Yoshida, K., Hwan, J. L., Huber, E. R., et al. (2015). Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events. Proc. Natl. Acad. Sci. U.S.A. 112, 1083–1088. doi: 10.1073/pnas.1414894112

PubMed Abstract | CrossRef Full Text | Google Scholar

Fuller, D. W., Schaefer, K. M., Hampton, J., Caillot, S., Leroy, B. M., and Itano, D. G. (2015). Vertical movements, behavior, and habitat of bigeye tuna (Thunnus obesus) in the equatorial central Pacific Ocean. Fish Res. 172, 57–70. doi: 10.1016/j.fishres.2015.06.024

CrossRef Full Text | Google Scholar

Giering, S. L. C., Sanders, R., Lampitt, R. S., Anderson, T. R., Tamburini, C., Boutrif, M., et al. (2014). Reconciliation of the carbon budget in the ocean's twilight zone. Nature 507, 480–483. doi: 10.1038/nature13123

PubMed Abstract | CrossRef Full Text | Google Scholar

Gilman, E., Passfield, K., and Nakamura, K. (2014). Performance of regional fisheries management organisations: ecosystem-based governance of bycatch and discards. Fish Fish. 15, 327–351. doi: 10.1111/faf.12021

CrossRef Full Text | Google Scholar

Gjerde, K., Nordtvedt Reeve, L. L., Harden-Davis, H., Ardron, J., Dolan, R., Durussel, C., et al. (2016). Protecting Earth's last conservation frontier: scientific, management and legal priorities for MPAs beyond national boundaries. Aquat. Conserv. 26, 45–60. doi: 10.1002/aqc.2646

CrossRef Full Text | Google Scholar

Grupe, B. M., Krach, M. L., Pasulka, A. L., Maloney, J. M., Levin, L. A., and Frieder, C. A. (2015). Methane seep ecosystem functions and services from a recently discovered southern California seep. Mar. Ecol. 36, 91–108. doi: 10.1111/maec.12243

CrossRef Full Text | Google Scholar

Halpern, B. S., Cottenie, K., and Broitman, B. R. (2006). Strong top-down control in Southern California Kelp Forest Ecosystems. Science 312, 1230–1232. doi: 10.1126/science.1128613

PubMed Abstract | CrossRef Full Text | Google Scholar

Haury, L. R., McGowan, J. A., and Wiebe, P. H. (1978). “Patterns and processes in the time-space scales of plankton distributions,” in Spatial Pattern in Plankton Communities, ed J. H. Steele (New York, NY: Plenum Press & NATO Scientific Affairs Division), 277–327.

Google Scholar

Heck, K. L. Jr., Carruthers, T. J. B., Duarte, C. M., Hughes, A. R., Kendrick, G., Orth, R. J., et al. (2008). Trophic transfers from seagrass meadows subsidize diverse marine and terrestrial consumers. Ecosystems 11, 1198–1210. doi: 10.1007/s10021-008-9155-y

CrossRef Full Text | Google Scholar

Heisler, J., Glibert, P. M., Burkholder, J. M., Anderson, D. M., Cochlan, W., Dennison, W. C., et al. (2008). Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8, 3–13. doi: 10.1016/j.hal.2008.08.006

PubMed Abstract | CrossRef Full Text | Google Scholar

Heithaus, M. R., Frid, A., Wirsing, A. J., and Worm, B. (2008). Predicting ecological consequences of marine top predator declines. Trends Ecol. Evolut. 23, 202–210. doi: 10.1016/j.tree.2008.01.003

PubMed Abstract | CrossRef Full Text | Google Scholar

Hemphill, A. H. (2005). Conservation on the High Seas – drift algae habitat as an open ocean cornerstone. Parks 15, 48–56.

Google Scholar

Hobday, A. J., Young, J. W., Moeseneder, C., and Dambacher, J. M. (2011). Defining dynamic pelagic habitats in oceanic waters off eastern Australia. Deep Sea Res. II 58, 734–745. doi: 10.1016/j.dsr2.2010.10.006

CrossRef Full Text | Google Scholar

Howey, L. A., Tolentino, E. R., Papastamatiou, Y. P., Brooks, E. J., Abercrombie, D. L., Watanabe, Y. Y., et al. (2016). Into the deep: the functionality of mesopelagic excursions by an oceanic apex predator. Ecol. Evol. 6, 5290–5304. doi: 10.1002/ece3.2260

PubMed Abstract | CrossRef Full Text | Google Scholar

Irigoien, X., Klevjer, T. A., Røstad, A., Martinez, U., Boyra, G., Acuña, J. L., et al. (2014). Large mesopelagic fishes biomass and trophic efficiency in the open ocean. Nat. Commun. 5:3271. doi: 10.1038/ncomms4271

PubMed Abstract | CrossRef Full Text | Google Scholar

IUCN (2017). Habitats Classification Scheme (Version 3.1). Available Online at: http://www.iucnredlist.org/technical-documents/classification-schemes/habitats-classification-scheme-ver3 (Accessed 02/07/2017)

Jaeckel, A., Gjerde, K. M., and Ardron, J. A. (2017). Conserving the common heritage of humankind – options for the deep-seabed mining regime. Mar. Pol. 78, 150–157. doi: 10.1016/j.marpol.2017.01.019

CrossRef Full Text | Google Scholar

Jensen, O. P., Ortega-Garcia, S., Martell, S. J. D., Ahrens, R. N. M., Domeier, M. L., Walters, C. J., et al. (2010). Local management of a “highly migratory species”: the effects of long-line closures and recreational catch-and-release for Baja California striped marlin fisheries. Prog. Oceanogr. 86, 176–186. doi: 10.1016/j.pocean.2010.04.020

CrossRef Full Text | Google Scholar

Jones, C. G., Lawton, J. H., and Shachak, M. (1994). Organisms as ecosystem engineers. Oikos 69, 373–386. doi: 10.2307/3545850

CrossRef Full Text

Kawaguchi, S., and Melle, W. (2016). PICES/ICES Workshop on “Zooplankton as a Potential Harvestable Resource”. PICES Press.

Google Scholar

Keith, D. A., Rodriguez, J. P., Brooks, T. M., Burgman, M. A., Barrow, E. G., Bland, L., et al. (2015). The IUCN red list of ecosystems: motivations, challenges, and applications. Conserv. Lett. 8, 214–226. doi: 10.1111/conl.12167

CrossRef Full Text | Google Scholar

Lavery, T. J., Roudnew, B., Gill, P., Seymour, J., Seuront, L., Johnson, G. C., et al. (2010). Iron defecation by sperm whales stimulates carbon export in the Southern Ocean. Proc. R. Soc. B 277, 3527–3531. doi: 10.1098/rspb.2010.0863

PubMed Abstract | CrossRef Full Text | Google Scholar

Letessier, T. B., Cox, M. J., Meeuwig, J. J., Boersch-Supan, P. H., and Brierley, A. S. (2016). Enhanced pelagic biomass around coral atolls. Mar. Ecol. Prog. Ser. 546, 271–276. doi: 10.3354/meps11675

CrossRef Full Text | Google Scholar

Levin, L. A., Baco, A. R., Bowden, D. A., Colaco, A., Cordes, E. E., Cunha, M. R., et al. (2016). Hydrothermal vents and methane seeps: rethinking the sphere of influence. Front. Mar. Sci. 3:72. doi: 10.3389/fmars.2016.00072

CrossRef Full Text | Google Scholar

Lubchenco, J., and Grorud-Colvert, K. (2015). Making waves: the science and politics of ocean protection. Science 350, 382–383. doi: 10.1126/science.aad5443

PubMed Abstract | CrossRef Full Text | Google Scholar

Maxwell, S. M., and Morgan, L. E. (2013). Foraging of seabirds on pelagic fishes: implications for management of pelagic marine protected areas. Mar. Ecol. Prog. Ser. 481, 289–303. doi: 10.3354/meps10255

CrossRef Full Text | Google Scholar

Maxwell, S. M., Hazen, E. L., Lewison, R. L., Dunn, D. C., Bailey, H., Bograd, S. J., et al. (2015). Dynamic ocean management: defining and conceptualizing real-time management of the ocean. Mar. Pol. 58, 42–50. doi: 10.1016/j.marpol.2015.03.014

CrossRef Full Text | Google Scholar

Merrie, A., Dunn, D. C., Metian, M., Boustany, A. M., Takei, Y., Elferink, A. O., et al. (2014). An ocean of surprises – Trends in human use, unexpected dynamics and governance challenges in areas beyond national jurisdiction. Glob. Environ. Change 27, 19–31. doi: 10.1016/j.gloenvcha.2014.04.012

CrossRef Full Text | Google Scholar

Morato, T., Hoyle, S. D., Allain, V., and Nicol, S. J. (2010). Seamounts are hotspots of pelagic biodiversity in the open ocean. Proc. Natl. Acad. Sci. U.S.A. 107, 9707–9711. doi: 10.1073/pnas.0910290107

PubMed Abstract | CrossRef Full Text | Google Scholar

Mumby, P. J. (2009). Herbivory versus corallivory: are parrotfish good or bad for Caribbean coral reefs? Coral Reefs 28, 683–690. doi: 10.1007/s00338-009-0501-0

CrossRef Full Text | Google Scholar

Nicol, S., and Stolp, M. (1989). Sinking rates of cast exoskeletons of Antarctic krill (Euphausia superba Dana) and their role in the vertical flux of particulate matter and fluoride in the Southern Ocean. Deep Sea Res. I 36, 1753–1762. doi: 10.1016/0198-0149(89)90070-8

CrossRef Full Text | Google Scholar

Nicol, S., Bowie, A., Jarman, S., Lannuzel, D., Meiners, K. M., and Van Der Merwe, P. (2010). Southern Ocean iron fertilization by baleen whales and Antarctic krill. Fish Fish. 11, 203–209. doi: 10.1111/j.1467-2979.2010.00356.x

CrossRef Full Text | Google Scholar

Nicol, S., Foster, J., and Kawaguchi, S. (2012). The fishery for Antarctic krill – recent developments. Fish Fish. 13, 30–40. doi: 10.1111/j.1467-2979.2011.00406.x

CrossRef Full Text | Google Scholar

NOAA (2016). Fisheries Off West Coast States; Comprehensive Ecosystem-Based Amendment 1; Amendments to the Fishery Management Plans for Coastal Pelagic Species, Pacific Coast Groundfish, U.S. West Coast Highly Migratory Species, and Pacific Coast Salmon [Online]. Available Online at: https://www.gpo.gov/fdsys/pkg/FR-2016-04-04/pdf/2016-07516.pdf (Accessed April 28, 2017).

Norse, E. (2005). Pelagic protected areas: the greatest parks challenge of the 21st century. Parks 15, 32–39.

Google Scholar

Ortuño Crespo, G., and Dunn, D. C. (2017). A review of the impacts of fisheries on open-ocean ecosystems. ICES J. Mar. Sci. doi: 10.1093/icesjms/fsx084. [Epub ahead of print].

CrossRef Full Text | Google Scholar

Pershing, A. J., Christensen, L. B., Record, N. R., Sherwood, G. D., and Stetson, P. B. (2010). The impact of whaling on the ocean carbon cycle: why bigger was better. PLoS ONE 5:e12444. doi: 10.1371/journal.pone.0012444

PubMed Abstract | CrossRef Full Text | Google Scholar

Plumeridge, A. A., and Roberts, C. M. (2017). Conservation targets in marine protected area management suffer from shifting baseline syndrome: a case study on the Dogger Bank. Marine Poll. Bull. 116, 395–404. doi: 10.1016/j.marpolbul.2017.01.012

PubMed Abstract | CrossRef Full Text | Google Scholar

Potier, M., Marsac, F., Cherel, Y., Lucas, V., Sarbatié, R., Maury, O., et al. (2007). Forage fauna in the diet of three large pelagic fishes (lancetfish, swordfish and yellowfin tuna) in the western equatorial Indian Ocean. Fish Res. 83, 60–72. doi: 10.1016/j.fishres.2006.08.020

CrossRef Full Text | Google Scholar

Ramirez-Llodra, E., Tyler, P. A., Baker, M. C., Bergstad, O. A., Clark, M. R., Escobar, E., et al. (2011). Man and the last great wilderness: human impact on the deep sea. PLoS ONE 6:e22588. doi: 10.1371/journal.pone.0022588

PubMed Abstract | CrossRef Full Text | Google Scholar

Ritchie, E. G., and Johnson, C. N. (2009). Predator interactions, mesopredator release and biodiversity conservation. Ecol. Lett. 12, 982–998. doi: 10.1111/j.1461-0248.2009.01347.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Robinson, C., Steinberg, D. K., Anderson, T. R., Arístegui, J., Carlson, C. A., Frost, J. R., et al. (2010). Mesopelagic zone ecology and biogeochemistry – a synthesis. Deep Sea Res. II 57, 1504–1518. doi: 10.1016/j.dsr2.2010.02.018

CrossRef Full Text | Google Scholar

Roman, J., and McCarthy, J. J. (2010). The whale pump: marine mammals enhance primary productivity in a coastal basin. PLoS ONE 5:e13255. doi: 10.1371/journal.pone.0013255

PubMed Abstract | CrossRef Full Text

Roman, J., Estes, J. A., Morissette, L., Smith, C., Costa, D. P., McCarthy, J., et al. (2014). Whales as marine ecosystem engineers. Front. Ecol. Environ. 12, 377–385. doi: 10.1890/130220

CrossRef Full Text | Google Scholar

Scales, K. L., Miller, P. I., Hawkes, L. A., Ingram, S. N., Sims, D. W., and Votier, S. C. (2014). On the Front Line: frontal zones as priority at-sea conservation areas for mobile marine vertebrates. J. Appl. Ecol. 51, 1575–1583. doi: 10.1111/1365-2664.12330

CrossRef Full Text | Google Scholar

Smith, C. R. (2007). “Bigger is better: the role of whales as detritus in marine ecosystems,” in Whales, Whaling, and Ocean Ecosystems eds J. A. Estes, D. P. DeMaster, D. F. Doak, T. M. Williams, and R. L. Brownell (Berkeley, CA: University of California Press), 286–300.

Google Scholar

Soetaert, K., Mohn, C., Rengstorf, A., Grehan, A., and van Oevelen, D. (2016). Ecosystem engineering creates a direct nutritional link between 600-m deep cold-water coral mounds and surface productivity. Sci. Rep. 6:35057. doi: 10.1038/srep35057

PubMed Abstract | CrossRef Full Text | Google Scholar

St John, M. A., Borja, A., Chust, G., Heath, M., Grigorov, I., Mariani, P., 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. doi: 10.3389/fmars.2016.00031

CrossRef Full Text | Google Scholar

Swadling, K. M. (2006). Krill migration: up and down all night. Curr. Biol. 16, R173–R175. doi: 10.1016/j.cub.2006.02.044

PubMed Abstract | CrossRef Full Text | Google Scholar

Tarling, G. A., and Johnson, M. L. (2006). Satiation gives krill that sinking feeling. Curr. Biol. 16, R83–R84. doi: 10.1016/j.cub.2006.01.044

PubMed Abstract | CrossRef Full Text | Google Scholar

The Economist (2017). The Mesopelagic: Cinderella of the Oceans [Online]. Available online at: https://www.economist.com/news/science-and-technology/21720618-one-least-understood-parts-sea-also-one-most-important

Thorrold, S. R., Afonso, P., Fontes, J., Braun, C. D., Santos, R. S., Skomal, G. B., et al. (2014). Extreme diving behaviour in devil rays links surface waters and the deep ocean. Nat. Commun. 5:4274. doi: 10.1038/ncomms5274

PubMed Abstract | CrossRef Full Text | Google Scholar

Turner, J. T. (2015). Zooplankton fecal pellets, marine snow, phytodetritus and the ocean's biological pump. Prog. Oceanogr. 130, 205–248. doi: 10.1016/j.pocean.2014.08.005

CrossRef Full Text | Google Scholar

UNGA (2015). Resolution 69/292. Development of an International Legally Binding Instrument Under the United Nations Convention on the Law of the Sea on the Conservation and Sustainable Use of Marine Biological Diversity of Areas Beyond National Jurisdiction. UNGA. Available online at: https://documents-dds-ny.un.org/doc/UNDOC/GEN/N15/187/55/PDF/N1518755.pdf?OpenElement

United Nations (2015). Sustainable Development Goal 14: Conserve and Sustainable Use the Oceans, Seas, and Marine Resources for Sustainable Development [Online]. Available Online at: https://sustainabledevelopment.un.org/sdg14 (Accessed March 02, 2017)

Vincent, A. C. J., Sadovy de Mitcheson, Y. J., Fowler, S. L., and Lieberman, S. (2014). The role of CITES in the conservation of marine fishes subject to international trade. Fish Fish. 15, 563–592. doi: 10.1111/faf.12035

CrossRef Full Text | Google Scholar

Watson, R. A., Nowara, G. B., Hartmann, K., Green, B. S., Tracey, S. R., and Carter, C. G. (2015). Marine foods sourced from farther as their use of global ocean primary production increases. Nat. Commun. 6:7365. doi: 10.1038/ncomms8365

PubMed Abstract | CrossRef Full Text | Google Scholar

Wilson, R. W., Millero, F. J., Taylor, J. R., Walsh, P. J., Christensen, V., Jennings, S., et al. (2009). Contribution of fish to the marine inorganic carbon cycle. Science 323, 359–362. doi: 10.1126/science.1157972

PubMed Abstract | CrossRef Full Text | Google Scholar

Woolley, S. N. C., Tittensor, D. P., Dunstan, P. K., Guillera-Arroita, G., Lahoz-Monfort, J. J., Wintle, B. A., et al. (2016). Deep-sea diversity patterns are shaped by energy availability. Nature 533, 393–396. doi: 10.1038/nature17937

PubMed Abstract | CrossRef Full Text | Google Scholar

Wright, G., Rochette, J., Druel, E., and Gjerde, K. (2016). The Long and Winding Road Continues: Towards a New Agreement on High Seas Governance. Paris: IDDRI.

Google Scholar

Young, J. W., Hunt, B. P. V., Cook, T. R., Llopiz, J. K., Hazen, E. L., Pethybridge, H. R., et al. (2015). The trophodynamics of marine top predators: current knowledge, recent advances and challenges. Deep Sea Res. II 113, 170–187. doi: 10.1016/j.dsr2.2014.05.015

CrossRef Full Text | Google Scholar

Zeidberg, L. D., and Robison, B. H. (2007). Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proc. Natl. Acad. Sci. U.S.A. 104, 12948–12950. doi: 10.1073/pnas.0702043104

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: areas beyond national jurisdiction, ABNJ, area-based management, biodiversity beyond national jurisdiction, BBNJ, high seas, marine protected areas, UNCLOS

Citation: O'Leary BC and Roberts CM (2017) The Structuring Role of Marine Life in Open Ocean Habitat: Importance to International Policy. Front. Mar. Sci. 4:268. doi: 10.3389/fmars.2017.00268

Received: 26 May 2017; Accepted: 03 August 2017;
Published: 05 September 2017.

Edited by:

Sara M. Maxwell, Old Dominion University, United States

Reviewed by:

Daniel Carl Dunn, Duke University, United States
Tammy Davies, BirdLife International, United Kingdom
Colleen Corrigan, The University of Queensland, Australia

Copyright © 2017 O'Leary and Roberts. 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) or licensor 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: Bethan C. O'Leary, bethan.oleary@york.ac.uk