Conservation Issues: Oceanic Ecosystems

Conservation Issues: Oceanic EcosystemsN Neeman, Drexel University, Philadelphia, PA, USAJA Servis and E Naro-Maciel, City University of New York, Staten Island, NY, USA

ã 2015 Elsevier Inc. All rights reserved.

Introduction: Marine Biodiversity and Its Importance 1Anthropogenic Threats to Marine Ecosystems 1Pollution 2Climate Change 3Habitat Alteration 3Overexploitation 4Invasive Species 5Conservation Strategies 6Protecting Ecosystems 6Protecting Key Species 7Conclusions 8References 8

Introduction: Marine Biodiversity and Its Importance

Marine biodiversity has many definitions, including the species richness and abundance present in marine ecosystems (Tittensoret al., 2010). This measure can refer to any level of taxonomic organization, such as bacteria, phytoplankton, zooplankton, algae,invertebrates, fishes, seabirds, and mammals (Borja, 2014). In addition to taxon-specific levels, a complete description ofbiodiversity also involves the genetic structure of populations and habitats, as well as the ecosystem’s integrity including its foodwebs and biophysical relationships (Borja, 2014; Figure 1).

Though suffering from species loss, marine ecosystems remain biologically and physically diverse (Borja, 2014; Selig et al.,2014). Ranging from the open ocean and deep waters to coastal estuaries and coral reefs, marine ecosystems have many utilitarianvalues because humans and other living organisms use them directly and indirectly. Direct utilitarian benefits include theproduction of food, medicine, and industrial materials, as well as tourism and recreation. Indirect benefits include nutrient cycling,coastal protection, and cultural, spiritual, and esthetic values (Borja, 2014). Marine ecosystems also have intrinsic value, meaningthey have inherent worth independent from their use by humans and other living organisms. Conserving the biodiversity of marineecosystems is important because it maintains ecosystem functioning and prevents systems from transitioning into undesirablestates that lead to the loss of both direct and indirect benefits that they provide (Borja, 2014; Selig et al., 2014). For these reasons,most conservation strategies for marine ecosystems target biodiversity (Salafsky et al., 2002).

Marine ecosystems are currently threatened by human activity as well as by natural processes unrelated to anthropogenic action(Arai, 2014; Halpern et al., 2008; Jackson et al., 2001). The latter threats, which are beyond the scope of this article, include disease,stochasticity, physical destruction by storms and natural disasters, and temperature and salinity changes due to natural cycles suchas El Nino (Arai, 2014). Anthropogenic effects include pollution, climate change, habitat alteration, overexploitation, and invasivespecies (Halpern et al., 2008). These combined risks have placed oceans at risk of being overexploited beyond recovery (Halpernet al., 2008; Jackson et al., 2001), which has prompted the scientific community to prioritize the study and the protection of marineecosystems (Borja, 2014; Broderick, 2015; Selig et al., 2014). Human population growth and overconsumption are drivers of thesethreats, which would not be as serious if not for these underlying factors.

The need for an ecosystem-based strategy for monitoring and conserving marine life and resources, as opposed to current onesfocusing on single species, has become increasingly accepted (Borja, 2014; Coll et al., 2012; Crowder et al., 2008; Micheli et al.,2013). This comprehensive approach considers entire ecosystems, including humans, and, because of its holistic nature, must unifyscientific, political, social, and economic interests at an international level (Crowder and Norse, 2008). While this broad approachto marine conservation necessarily requires moving beyond single-issue and single-species management practices, a number of keythreats impact marine ecosystems globally and are broadly discussed in the following sections along with current conservationpractices and recommendations.

Anthropogenic Threats to Marine Ecosystems

Human activities, driven by population growth and overconsumption, can alter marine ecosystems through both direct andindirect means (Halpern et al., 2008). Land-based activities affect marine ecosystems through nutrient and pollutant runoff, whileocean-based activities extract resources and can therefore affect biodiversity and species composition (Broderick, 2015; Halpern

Reference Module in Earth Systems and Environmental Sciences http://dx.doi.org/10.1016/B978-0-12-409548-9.09198-3 1

http://dx.doi.org/10.1016/B978-0-12-409548-9.09198-3

et al., 2008; Tallis et al., 2008). Some of these threats, like urban and agricultural runoff, are localized and spatially restricted, whileothers, like overfishing or anthropogenic climate change, have widespread impacts (Halpern et al., 2008).

In general, the health of marine ecosystems improves with distance frommajor land masses and therefore from the influence ofanthropogenic activities (Broderick, 2015). Coral reefs, estuaries, and coastal seas are then under the greatest threat. However, asmore advanced technologies are developed, the reach of human activities may increase, threatening the health of open ocean anddeep-sea ecosystems as well (Broderick, 2015). Attempts to quantify and map cumulative anthropogenic impacts on marineecosystems have proved challenging as empirical data are lacking and can vary dramatically along geographic and politicalboundaries (Halpern et al., 2008; Micheli et al., 2013). Further, estimates are often static and cannot predict future trajectoriesof ecosystem health given nonlinear impact responses and the possible implementation of various management strategies (Micheliet al., 2013).

An understanding of the current threats facing marine ecosystems is vital for future conservation planning. Here, we havefocused on anthropogenic, as opposed to natural, threats. The main threats covered in this section include pollution, climatechange, habitat alteration, overexploitation, and invasive species.

Pollution

Pollution can occur in various forms and is a major threat to marine ecosystems (Lascelles et al., 2014). Oil spills can have large,population-level impacts on migratory marine species (MMS) when they take place in sensitive areas (Lascelles et al., 2014).Organic pollutants impair the immune and reproductive systems in marine species like corals, killer whales, and seals (Lascelleset al., 2014; Tallis et al., 2008). Nitrogen loading from terrestrial ecosystems can alter macrophyte communities and cause sea staroutbreaks that damage corals, as well as toxic phytoplankton blooms and anoxia (Tallis et al., 2008). Organic carbon release hasbeen shown to increase microbial production and switch carbon sinks to carbon sources, altering their trophic structure (Talliset al., 2008). Light and noise pollution can also become important because they cause behavioral changes in several species(Lascelles et al., 2014). For instance, seabirds collide due to light pollution in offshore platforms and sea turtle hatchlings andadults become disoriented due to lights on nesting beaches (Lascelles et al., 2014).

Plastic pollution has become ubiquitous in marine systems and is recognized as one of the most important stressors for manymarine species and habitats (Lascelles et al., 2014; Vegter et al., 2014). Plastics are now distributed throughout the world’s oceans,deposited on many coastlines, and even found in remote areas of the deep sea (Vegter et al., 2014). The distribution of floatingplastic debris can be affected by oceanic and atmospheric circulation patterns, leading to very high accumulations of debris inconvergence zones such as the North Pacific Subtropical Gyre, colloquially termed the ‘Great Pacific garbage patch’ (Goldsteinet al., 2013).

Marine wildlife is affected by plastic pollution through entanglement, ingestion, bioaccumulation, and habitat degradation(Lascelles et al., 2014; Vegter et al., 2014). These negative impacts are well documented for several taxa including mammals,seabirds, sea turtles, fish, and many invertebrates (Vegter et al., 2014). Accidental ingestion of or entanglement in plastics can leadto gut impaction and perforation, impaired feeding, reduced reproduction, impaired movement, transfer of toxic compounds, anddeath in many marine species (Lascelles et al., 2014; Vegter et al., 2014).

Plastic pollutants can affect different marine habitats in several ways (Vegter et al., 2014). For example, plastic debrisaccumulates in intertidal habitats and can alter light and oxygen availability and water movements leading to changes in benthiccommunities and foraging habits (Vegter et al., 2014). On sandy beaches, microplastics change the permeability and temperatureof sediments, which can affect animals with temperature-dependent sex determination such as reptiles (Vegter et al., 2014).In subtidal habitats, large plastics change the availability of refugia and provide new surfaces for species to settle on (Vegter et al.,

Figure 1 Coral reefs are one of the most diverse marine ecosystems.

2 Conservation Issues: Oceanic Ecosystems

2014). Additionally, the decline of coral reef habitats has been attributed to fouling by entangled fishing lines, direct suffocation,abrasion, and the shading of colonies by fishing nets (Vegter et al., 2014).

Climate Change

Global climate change is associated with changes in sea level, atmospheric and sea surface temperatures, ocean pH, and rainfallpatterns (Borja, 2014; Vegter et al., 2014). Sea level can rise as glaciers melt, temperatures can increase as the planet warms, andoceans become more acidic due to carbon dioxide. These changes can have important conservation implications from organismalto ecosystem levels. For example, the spread of invasive species is expected to increase with suitable habitat availability (Hawkins,2012; Ojaveer et al., 2014; Vegter et al., 2014). In addition, artificial fortification and modification of coastal habitats may becomeubiquitous along shorelines to stave off the impacts of rising sea levels (Airoldi et al., 2005), and plastics and other pollutants mayspread to previously uncontaminated areas through increasingly extreme weather and precipitation patterns (Vegter et al., 2014).It remains unclear how these myriad impacts will interact with one another. However, future climate change will undoubtedlyresult in even more dramatic shifts than those observed until now and will affect many marine ecosystems, potentially counteringcurrent conservation efforts (Magris et al., 2014).

The effects of climate change on species and communities can be broadly divided into four pathways: phenological shifts,changes in distribution, alterations in physiological processes, and local adaptation (Hughes, 2000). Meta-analyses have shownthat around 80% of all observations of distribution, phenology, community composition, abundance, demography, and calcifi-cation across taxa and ocean basins are consistent with the predicted effects of climate change on marine organisms (Borja, 2014).Further, climate change can affect different systems in different ways (Vegter et al., 2014), and species sensitivity or adaptation willdepend on both the degree to which its environment is altered and its inherent biological traits (Lascelles et al., 2014).

Habitat Alteration

Coastal erosion is a natural process that continually reshapes shorelines through ocean currents, tidal movements, and wind andwave action (Airoldi et al., 2005). However, the urbanization of coastlines involving activities such as offshore dredging, decreasingsediment supply from rivers, and the destruction of seagrass meadows, marshes, and coastal sand dunes can intervene in coastalprocesses and exacerbate erosion (Airoldi et al., 2005). Preventing the recession and destruction of these economically, socially,and politically important coastal areas has become increasingly important and challenging. Even without any further urbanizationand other forms of human engineering along coastlines, protecting these areas will likely become increasingly challengingconsidering predicted rises in sea level and storm frequency due to global climate change (Airoldi et al., 2005).

Measures to prevent coastal degradation may also lead to threats. These primarily include the construction of hard-substratedefense structures, which prevent erosion and flooding, stabilize and retain beaches and reclaimed land, and increase therecreational value of the area. The various types of defense structures include breakwaters, groynes, seawalls, dykes, or otherarmored structures. In addition to the intentional changes these structures produce in the physicality of the coast, they can also havedramatic impacts on the surrounding biotic features and ecological communities (Airoldi et al., 2005; Dugan et al., 2008).Shoreline hardening or bulkheading are some of the greatest threats to sandy coasts, which represent the most common coastalhabitat (Tallis et al., 2008). These structures can prevent sediment accretion and, therefore, the development of salt marshes as wellas deplete important habitat for eelgrass, surf smelt, and other species (Tallis et al., 2008). Sandy beaches also host a diversity ofmacroinvertebrates and provide critical foraging and nesting habitat for vertebrates such as shorebirds and sea turtles (Duganet al., 2008).

In the Italian waters of the Adriatic Sea, Airoldi and Bulleri (2011) found that breakwaters provide important structures fordynamic communities of opportunistic and dominant invertebrate and macroalgal species. Biotic and abiotic components of thecoastal habitat such as the amount of wave action on the breakwater and the timing in larval recruitment of key species variedspatially and temporally and drove changes in local community composition. Moreover, the study highlighted the impact ofcontinual maintenance of the breakwater, which was a primary source of disturbance that drove the abundance, distribution,establishment, and success of invasive and other recruited macroalgal and invertebrate organisms. Therefore, in addition toutilizing low-impact structural designs, such as the use of suitable materials with optimal surface textures and habitat complexity,these findings underscore the need for continual assessment and effort to reduce the impacts of hard coastal infrastructure. Forexample, routine maintenance could be timed so as to avoid seasons of larval recruitment and establishment of key species.

Another important form of habitat alteration is the impact of bottom trawling on benthic communities (Dannheim et al.,2014). These effects are twofold, including both the physical effects of sediment disturbance and resuspension and the biologicaleffect of the damage and mortality of benthic organisms (Dannheim et al., 2014; Kaiser et al., 2000). Both of these changes havefar-reaching effects. Trawling alters the biophysical and chemical composition of the sediment as well as the sources of food inputto the system through discards of bycatch (which benefit scavenger species) as well as direct mortality caused by the gear used(Dannheim et al., 2014; Kaiser et al., 2000). This can have huge effects on the trophic interactions and the general functioning ofthe benthic ecosystem (Dannheim et al., 2014).

Long-term trawling can shift the species composition of entire benthic communities towards short-lived, fast-growing, smallerorganisms, which are better suited for this artificial disturbance regime (Dannheim et al., 2014; Kaiser et al., 2000). Long-livedorganisms that live close to the sediment surface and reproduce infrequently, such as large bivalves, may be the most affected by

Conservation Issues: Oceanic Ecosystems 3

trawling, while smaller species that can withstand resuspension may be less affected (Kaiser et al., 2000). For the system as a whole,these changes in composition can mean a shift from high diversity, high biomass, and low turnover to high turnover, low diversity,and low biomass (Dannheim et al., 2014). The recovery times, even after full cessation of trawling, can be several years (Dannheimet al., 2014).

Overexploitation

Overfishing can be seen as an example of the ‘tragedy of the commons,’ in which several entities tend to exploit a shared resourceleaving it depleted (Day, 2008; Hardin, 1968). It can also be difficult to quantify due to the intergenerational loss of informationabout the natural abundance of exploited species, which results in shifting baseline values (McClenachan et al., 2012; Pauly, 1995).Species overexploitation can have an enormous effect on marine ecosystems as its impacts range from species-specific populationdepletion (in extreme cases to extinction) to dramatic alterations at the ecosystem level (Crowder et al., 2008; Hobday et al., 2011;Jackson et al., 2001).

Commercial and recreational fishing can directly affect marine species by depleting the stock to levels difficult or impossible torecover (Allison et al., 1998; Lascelles et al., 2014). When populations are exploited until they reach sufficiently small sizes, anextinction risk vortex can occur due to genetic processes, such as inbreeding depression and genetic drift, or ecological effects suchas stochasticity and environmental fluctuations (Wootton and Pfister, 2013).

As opposed to terrestrial ecosystems in which autotrophs and herbivores are commonly exploited, exploitation in marineecosystems is usually directed at top predators, including some of the oceans’ most charismatic and highly migratory species(Allison et al., 1998; Lascelles et al., 2014). Once these predators are depleted, fishing activities may switch to their prey species,effectively fishing down the ecosystem’s food web (Foley, 2013). This practice is unsustainable, and indications of decreasingtrophic level in harvested species can be used as a measure of overfishing (Foley, 2013).

Intentional capture has led to overfishing of tuna, marlins, and other large, open-water fish species, while dolphin, sea turtle,whale, and chondrichthyan (sharks, rays, and chimaeras) populations have suffered greatly from unintentional catch, or bycatch(Crowder et al., 2008; Lascelles et al., 2014). Shark fin soup is a well-known case study affecting these oceanic predators.Overfishing can also threaten macroalgal communities, due to the removal of large species that consume macroalgal grazers(Durrant et al., 2014).

The effects of overfishing a single species or population at one trophic level can be seen throughout the associated marine foodweb and greater ecosystem through indirect impacts (Crowder et al., 2008; Hobday et al., 2011). Indirect impacts on targetedspecies include changes in behaviors, such as habitat selection and mating, or population-level genetics due to size-selective fishing(Crowder et al., 2008). Nontarget species also face indirect risks from species-specific overexploitation through habitat destructionand changes in food web dynamics and structure (Crowder et al., 2008; Hobday et al., 2011).

Many of the fundamental alterations seen in ecosystems suffering from overfishing are caused by the removal of key top-downregulators, as was observed in the ecological extinction of oysters in the Chesapeake Bay of the Eastern United States ( Jackson et al.,2001). Studies of the collapse of these estuarine ecosystems indicate that a loss of benthic suspension feeders, primary top-downcontrollers of community structure, predates the extreme degradation of abiotic and biotic components of oyster reefs. It was onlysubsequent to the introduction of mechanical harvesting with dredges in the 1870s that other biotic and abiotic components of thehabitat, including bottom-up increases in nutrients such as nitrogen and phosphorous causing phytoplankton blooms, hypoxicand anoxic conditions characteristic of eutrophication, and the spread of parasitic oyster disease, became prevalent. Poor waterquality, disease, and dredging activities continue to prevent the recovery of oyster populations and their associated estuarinecommunities in the Chesapeake Bay ( Jackson et al., 2001; Figure 2).

Figure 2 Oysters inhabiting the sensitive estuarine ecosystems of the Eastern United States have historically suffered from overfishing. Pictured hereis an oyster bed at Cape Romain National Wildlife Refuge in North Carolina.


In response to growing understanding of these broader impacts, fisheries management in recent decades has moved beyondsingle-species to ecosystem-based fisheries management (EBFM) (Crowder et al., 2008; Hobday et al., 2011). EBFM is part of thebroader ecosystem-based management approach that addresses all environmental, ecological, and anthropogenic (includingfisheries) impacts on an ecosystem and takes into account the interconnectedness and interdependence of various componentsof an ecosystem (Curtin and Prellezo, 2010). It differs from traditional fisheries management approaches by encompassingimportant indirect fisheries impacts such as those described earlier (Curtin and Prellezo, 2010; Hobday et al., 2011).

Invasive Species

The introduction of invasive species can greatly impact the structure and function of an ecosystem by altering native speciescomposition and disrupting food webs and nutrient cycling, among other key processes. Nonnative species can also wreak havoceconomically by depleting fisheries resources, interfering with the shipping industry by clogging intake pipes, adversely affectinghuman health, and decreasing biodiversity (Lo et al., 2012; Molnar et al., 2008). Humans can transport marine species tononnative environments intentionally and unintentionally through a number of pathways and vectors (Ojaveer et al., 2014).The main ways marine invasive species are introduced globally are through the ballast water and fouled hulls of ships (Lo et al.,2012; Molnar et al., 2008; Ojaveer et al., 2014). Other major causes of invasive species introductions include aquaculture practices,canal construction, and aquarium and seafood trade (Molnar et al., 2008; Vegter et al., 2014).

Some well-known examples of destructive invasive species include the lionfish (Pterois spp.) and zebra mussels (Dreissenapolymorpha) (Havel et al., 2015; Jud et al., 2015). Lionfish have quickly invaded the Western Atlantic and the Caribbean. As habitatand diet generalists, they are able to colonize a large range and effectively prey on many native species ( Jud et al., 2015; Figure 3).Zebra mussels were spread through European shipping channels to North America by ballast water. Their impact as invasive specieshas been greatly intensified by their ability to act as ecosystem engineers by filtering out most of the algae from the water column,leaving little food for zooplankton and increasing the amount of light for vascular plants, which transitions the system from apelagic to a littoral-based food web (Havel et al., 2015).

Research concerning invasive species has been performed primarily on the local or regional level; however, studies haveincreasingly been turning to a global perspective that considers entire marine realms or ecoregions to identify and implementconservation efforts (Molnar et al., 2008; Ojaveer et al., 2014). A primary roadblock for synthesizing information about invasivespecies and designing large-scale mitigation efforts is a lack of empirical data concerning the impacts, routes of introduction, anddistribution of species at the local and regional levels (Edelist et al., 2013; Molnar et al., 2008). However, this ecosystem-basedapproach is crucial as the mechanisms and pathways of invasive species transport have reached global scales and the effectiveassessment and management of these invasions requires international cooperation among biologists, policymakers, and industrystakeholders. Including cooperation with stakeholders, the International Council for the Exploration of the Sea (ICES) recom-mends ten key requirements for assessing and managing global marine invasive species. These suggestions include taking amultivector management approach, investigating and assessing propagule pressures, standardizing data and information systems,

Figure 3 The lionfish, an Indo-Pacific native, has invaded a variety of ecosystems in the Western Atlantic and Caribbean, including coral reefs, seagrassbeds, mangroves, and human-created habitats.


and increasing the development and use of molecular tools and taxonomic expertise to detect invasive species and reconstruct thepathways of their introduction (Ojaveer et al., 2014).

Conservation Strategies

Mitigating these previously described threats to marine ecosystems requires a multitude of strategies and approaches that can begrouped into four broad categories: protection and management, law and policy, education and awareness, and changingincentives (Salafsky et al., 2002). Examples of tools used to protect and manage marine ecosystems should be adaptable to changesin the ecosystem and can include the creation of protected areas, fishing bans and regulations, and captive breeding andreintroduction programs. Law and policy approaches include developing international treaties, establishing standards for the useof natural resources and monitoring their compliance, and implementing sanctions. Preventing the spread of invasive species, forexample, is a goal that has relied on implementing and monitoring standards for expelling ballast water from ships before cominginto port and regulating the commercial trade of potentially invasive organisms across international borders. Education andawareness can be improved through the development of formal and informal curricula and through the use of media and otheroutlets for scientists to share their research. Incentives encourage stakeholders to act to conserve marine biodiversity and naturalresources and can involve sustainable development and ecotourism (Leslie, 2005; Mawdsley et al., 2009; Salafsky et al., 2002).

One of the greatest challenges facing marine conservation is how to include the many aspects of biodiversity and ecosystemfunctioning when choosing a conservation strategy (Tornroos et al., 2013). Because there are always costs and limitationsassociated with gathering data, it is common to use surrogate estimates and proxies to estimate the less easily quantifiable variableof interest (Tornroos et al., 2013). For example, a type of predefined habitat can be used as a proxy for overall biodiversity, or theabundance of certain species can be used as a proxy for the presence or abundance of less observable species (Tornroos et al., 2013).This leads to two main conservation strategies: targeting either certain areas or certain species for conservation (Tornrooset al., 2013).

Protecting Ecosystems

Area-focused conservation can lead to the creation of marine reserves, in which all extractive or destructive activities are banned, ormarine protected areas, which are more general and include all area-based conservation and management efforts (Leslie, 2005).The IUCN has created a framework to categorize marine protected areas, ranging from I to VI, from strictly protected no-go zones(Ia) to areas that prohibit almost all extractive activities (Ib, II), to those that allow some limited extraction (IV), to those that focuson sustainable use (VI) (Ban et al., 2014).

The designation of these areas has expanded dramatically over the last few decades because they can serve many functions suchas conserving biodiversity, providing sites for tourism, protecting sensitive habitats, providing refuge for overfished species inunprotected habitats, enhancing the production of certain target species by acting as nurseries, providing management framework,enhancing ecosystem resilience, and providing a point of comparison with unprotected areas for scientific studies (Allison et al.,1998; Borja, 2014). The Convention on Biological Diversity has even proposed that countries should aim to have 10% of all coastaland marine areas as protected areas by 2020 (Broderick, 2015; Selig et al., 2014).

Priority areas designated for conservation can be defined based on several explicit ecological or socioeconomic criteria,including biodiversity, species endemism, and degree of anthropogenic threats (Leslie, 2005; Selig et al., 2014). Because reservesand protected areas allow for strong local control, they are most appropriate in areas where local human impact is strong, such asareas with high fishing pressure, pollution potential, and habitat perturbation (Allison et al., 1998). Studies have shown thatmarine protected areas have greater diversity, higher abundance, larger organisms, and even different community structures thanunprotected areas (Allison et al., 1998) and that protecting specific marine habitats can act as a surrogate for the taxonomic andfunctional zoobenthic community structure (Tornroos et al., 2013). Macroalgal forests, which can support high faunal diversity,have also been shown to benefit from marine protected areas, through the increase of predatory fish and lobsters that suppressgrazing invertebrates (Durrant et al., 2014).

However, despite their protected status, marine reserves are not fully isolated from anthropogenic impacts (Allison et al., 1998).Conservation in marine reserves can be limited by many processes that are unique to marine systems and that make themtemporally dynamic and highly interconnected (Allison et al., 1998; Mazor et al., 2013). Hydrographic circulation patterns andepisodic events like El Nino Southern Oscillation (ENSO) can have effects on biological patterns that span hundreds of kilometers(Allison et al., 1998). For instance, ocean currents have a large influence on the dispersal of organisms (which can vary by speciesand life stage), diseases, and pollutants (Allison et al., 1998; Magris et al., 2014). This means that species residing in protected areasare still exposed to the conditions of adjacent water masses, including chemical pollution and any conditions altered due to climatechange (Allison et al., 1998).

In order to reduce these region-wide effects and to provide connectivity between populations of protected species, networks ofmarine protected areas have been proposed (Allison et al., 1998). These would provide an effective solution to large-scale coveragewhile restricting human activities on a relatively small fraction of the total area (Allison et al., 1998; Magris et al., 2014). The size,spacing, and configuration of protected areas within these networks can also be tailored to specific habitats as well as their needsand connectivity (Magris et al., 2014). Managing these networks of marine protected areas will rely on international collaboration,


since global priority areas and hot spots often span several countries (Mazor et al., 2013). Studies have shown that internationalcollaboration for the conservation of shared marine resources can actually increase conservation efficiency and decrease overallcosts for individual countries (Mazor et al., 2013; Table 1).

Protecting Key Species

MMS include some of the most charismatic known organisms, like marine mammals, sea turtles, seabirds, sharks, rays, and tuna(Heupel et al., 2015; Lascelles et al., 2014). The species migrate between distinct geographic areas throughout their different lifestages, for feeding (like the central place foraging of seabirds), reproduction (nesting, calving, or spawning sites), and otherbehaviors (Lascelles et al., 2014; Olds et al., 2014). These species are among the most threatened due to the range of risks to whichthey are exposed during their migratory movements, with as many as 36% of MMS listed as globally threatened (Lascelles et al.,2014). Their international migration routes present a unique challenge for their conservation, requiring coordinated efforts amongseveral countries and organizations (Heupel et al., 2015; Lascelles et al., 2014; Figure 4).

MMS can play an important role in the stability and health of the ecosystems they move between, are vulnerable to exploitation,and have high socioeconomic significance (Heupel et al., 2015; Olds et al., 2014). Many of these species are therefore seen asmarine focal (or link) species and act as flagship, keystone, surrogate, or umbrella species for conservation, with their presence andabundance used to estimate both the occurrence of other species and the health of their habitats (Heupel et al., 2015; Lascelles

Table 1 Zoning in marine protected areas

Zone Synonyms Activities allowedActivitiesprohibited Purposes

Marinereserve

No-take,no-access

Limited Take,access

Counter harmful processes; address conservation andfishery management objectives; provide insurance againstmanagement failure (Agardy, 2000; NAS, 2001)

Restrictedaccess

Sanctuaries,no-take areas

Limited public activity, such asswimming, diving, and ecotourism

Extraction,take

Meet sustainable use goals, attract public attention, andsupport; household or park income from ecotourism; pridein community involvement; fishery and conservationbenefits

Generalreserve

Regulated access and take;ecotourism, restricted fishing,research, education; recreation

Destructivepractices

Address stakeholder interests

Buffer area Traditional useareas; partialreserves

Entry, take Destructivepractices

Buffer between the park and surroundings; potentiallycapable of protecting core areas from pollutants and otherthreats; integrated conservation and development projects(ICDPs), as well as educational and administrativefacilities, are often housed in the buffer zone

Adapted from Naro-Maciel, E., Sterling, E. J. and Rao, M. Protected areas and biodiversity conservation I: reserve planning and design. http://ncep.amnh.org/linc.

Figure 4 Bull sharks undertake long range movements and exploit a wide range of habitats, and thus are subjected to various management regimesand degrees of protection.


et al., 2014; Olds et al., 2014). Many of these species are apex predators and their removal from an ecosystem has important effectson community species composition (Heupel et al., 2015; Lascelles et al., 2014). For instance, the removal of a marine top predatorcan lead to population booms in their prey species as well as changes in their predator-avoidance behavior (Lascelles et al., 2014).This importance has led to the creation of the Convention onMigratory Species, the prime international legal instrument to addressthe conservation of these species, which has provided the basis for several global or regional conservation and managementagreements (Lascelles et al., 2014).

Due to the variety of threats faced by MMS, conservation measures need to be taken at both the ocean basin and local scale(Lascelles et al., 2014). Better data on the migratory routes of these species are necessary in order to better to guide futureconservation efforts, which will need to consider these species as single units, disregarding jurisdictional boundaries (Heupelet al., 2015; Lascelles et al., 2014; Mazor et al., 2013). Here, we have focused on MMS to highlight some of the challenges in theirconservation measures, but many of these lessons are equally true for other focal species and local conservation measures.

Conclusions

Marine conservation planning is moving beyond representing features of existing biodiversity and towards ensuring the long-termpersistence and viability of full species assemblages (Magris et al., 2014). This requires a much better understanding of the naturalprocesses of marine ecosystems as well as their spatial and temporal dynamics (Magris et al., 2014). In addition to protecting keyspecies and ecosystems, monitoring, evaluating, and adapting management plans will be essential for effective and efficientmanagement and conservation of marine ecosystems (Day, 2008; Katsanevakisa et al., 2011; Leslie, 2005).

Marine habitats provide unique management challenges because the interconnectedness of habitats, logistic difficulties atsampling sites, and ownership issues often leave marine ecosystems subject to the ‘tragedy of the commons.’ However, a lack ofbaseline data at the local and global scales remains a primary roadblock to designing effective and efficient conservation strategies,and steps need to be taken to encourage long-term, standardized, replicable, and cost-effective measures for monitoring marinehabitats (Day, 2008).

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