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Schematic of subsurface-predator facilitated foraging. Image credit: Drew Briscoe 

Schematic of subsurface-predator facilitated foraging. Image credit: Drew Briscoe 

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Scientists and managers have become increasingly interested in how pelagic marine protected areas (PMPAs), or protected areas away from the coast, can be used to protect pelagic species. Subsurface-predator facilitated foraging (‘facilitated foraging’) between seabirds and subsurface predators, such as tunas, is a key ecological interaction in the...

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... has been an increasing trend in the creation of mostly pelagic marine protected areas (PMPAs) to protect ocean ecosystems ( Table 1). Marine ecosystems encompass 99% of the earth’s biosphere volume (Angel 1993), and the vast majority of this volume occurs in the pelagic realm, or areas away from the coastal zone (e.g. non-neritic). Protection of pelagic ecosystems, in addition to coastal regions, is necessary to meet global marine conservation targets, such as the Convention on Biological Diversity’s call to establish 10% of the worlds’ oceans as MPAs by 2020 (Convention on Biological Diversity 2010). Additionally, pelagic ecosystems provide > 80% of global fish production (Pauly et al. 2002), are critical in the regulation of the Earth’s climate (Field 1998), and support the majority of marine life during all or some part of their life history (Hays et al. 2005). Still, pelagic ecosystems face a number of threats, including overfishing, pollution, climate change, and species introductions (Halpern et al. 2008), and PMPAs have been proposed as one means of ameliorating these effects (Game et al. 2009). Protecting pelagic or wide-ranging species from effects is often cited as one of the primary reasons for designating PMPAs, but the areas must be large enough to incorporate significant portions of the habitat of far-ranging or migratory animal species or protect crucial life history phases (Hyrenbach et al. 2000, Norse 2005, Alpine & Hobday 2007, Ardron et al. 2008, Game et al. 2009). Additionally, protective measures must re flect effects managers are attempting to ameliorate (e.g. fishing must be reduced or prohibited to prevent overfishing), and areas must be effectively enforced (Walmsley & White 2003). Several PMPAs, particularly in the Central Pacific and Indian Oceans (e.g. Chagos Marine Reserve, Phoenix Islands Protected Area, Papah naumoku kea Marine National Monument [MNM], and the Pacific Remote Islands MNM), are now in place (Table 1), and managers are beginning to grapple with the dif- ficulties of developing and monitoring indicators of effectiveness for these protected areas within an eco- system-based management context. This is particularly difficult in PMPAs because of the dynamic processes that occur in pelagic ecosystems (e.g. eddies and fronts) and the highly mobile species that are the focus of protection (Game et al. 2009). Tropical seabirds are 1 example of a highly mobile species group that managers are aiming to protect. Many tropical seabirds are far-ranging foragers, breeding on small islands and atolls and carving out an existence in largely oligotrophic parts of the oceans (Owen 1981, Ballance et al. 1997). Many rely on dynamic and ephemeral oceanographic processes to forage. PMPAs may be of particular ecological sig- nificance to tropical seabirds because they are central place foragers during the breeding season, when they must return to colonies to incubate eggs and feed chicks (Ashmole & Ashmole 1967, Ballance et al. 2006). Seabirds may travel thousands of kilometers in a single foraging trip, but their long-distance movements are centered on the colony during the breeding season (King 1974, Flint 1991, Laniawe 2008, Catry et al. 2009a). This increases the chances that protection from PMPAs may influence seabirds throughout some or all of their foraging range be cause foraging opportunities may be increased through the additional protection of the resources they depend on. PMPAs that reduce or eliminate commercial fishing may influence seabirds via direct and indirect mechanisms. (We refer to PMPAs that reduce or eliminate fishing effort when referring to PMPAs for the remainder of the text.) Reduced fishing within PMPAs may lower seabird bycatch or diminish the opportunities for seabirds to forage on fishery discards (Tasker et al. 2000, Lewison & Crowder 2003, Votier et al. 2004). Additionally, reduced pressure of some fisheries may increase foraging opportunities for seabirds by increasing the abundance of prey species. However, unlike the majority of temperate seabirds, most tropical seabirds lack deep diving capabilities and instead must forage in the top-most surface layer (Ashmole & Ashmole 1968, Harrison et al. 1983). This has led to the evolution of subsurface- predator facilitated foraging (hereafter referred to as ‘facilitated foraging’) (Fig. 1). In this interaction, large pelagic fishes, such as tunas, drive forage fish into surface waters, making them available to surface predators (Murphy & Ikehara 1955, Ashmole & Ashmole 1967). Though this interaction occurs in many parts of the world (Burger 1988), it is of particular importance in the tropical waters of the world’s oceans because it is one of the primary means by which tropical seabirds forage (Au & Pitman 1986, Spear et al. 2007). Because it is a critical interaction for seabirds, a reduction or cessation of fishing efforts targeting prey species or subsurface predators within tropical PMPAs may increase subsurface predator or prey density, resulting in more foraging opportunities for seabirds. Facilitated foraging has been relatively well studied in the Eastern Tropical Pacific (ETP) (see Au & Pitman 1986, Spear & Ainley 2005, Spear et al. 2007), but it has been largely unstudied in the Central Tropical Pacific (CTP) (but see Ashmole & Ashmole 1967), although distinct differences in facilitated foraging occur between the 2 systems. For example, tunas, primarily skipjack Katsuwonus pelamis and yellow fin Thunnus albacares , are the main subsurface pred ators in the CTP, in contrast to dolphins and tunas in the ETP (Spear et al. 2007). These species have different vertical and horizontal movement patterns, which may influence facilitated foraging be havior. Additionally, seabird assemblages in the CTP differ from those in the ETP (Ashmole & Ashmole 1967). Still, it is unknown how variability in the interaction influences seabird populations. Given the corre lations previously identified between fishery development and seabird crashes in many areas of the world (Harrison et al. 1983, Cury et al. 2011), there is a need to understand how seabirds interact with subsurface predators, particularly commercially important species, such as skipjack and yellowfin tunas, across the range where these interactions occur. These interactions are of particular interest to managers of large PMPAs in tropical oceans as seabirds are often a guild that managers aim to protect. One such MPA is the US Pacific Remote Islands Marine National Monument (PRIMNM), created in 2009 by Presidential Proclamation (Federal Register 2009), resulting in 225 038 km 2 of protected area in the CTP. It includes the far-flung and mostly unpop- ulated US territories of Wake Island, Johnston Atoll, Palmyra Atoll and Kingman Reef, Jarvis Island, and Howland and Baker Islands. These islands and atolls are home to as many as 4.4 million breeding seabirds representing at least 16 species (Table 2). Co-managed by the US National Oceanic and Atmospheric Administration (NOAA) and the US Fish and Wildlife Service (USFWS), monument managers want to know if the PMPA is likely to have a positive effect on seabirds and, subsequently, how to adequately monitor and manage seabird and pelagic fish populations. To assess our current state of knowledge of facilitated foraging in the CTP and to determine the key research questions and methodologies for managing human activities that may influence facilitated foraging, we conducted a literature review and held an expert workshop. We focused specifically on the seabirds breeding on the PRIMNM islands and atolls (Table 2), though this information is applicable to other tropical areas. We further focused on a set of topics we identified in conjunction with managers at the NOAA Pacific Islands Regional Office, which is responsible for PRIMNM management. These topics were intended to focus future research on key ele- ments of seabird and subsurface predator ecology and included the determination of the importance of subsurface predators to tropical seabird foraging, the distributions of seabirds and tunas, and the foraging behaviors and diets of seabirds in the PRIMNM re gion. At the heart of this review is this question: how do subsurface predator populations influence seabird population behavior and reproductive performance, and how can this knowledge be integrated into management of seabird and subsurface predator species in PMPAs? Below, we review current re search aimed at answering this ...

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... MPAs (Breen et al., 2016;Maxwell & Morgan, 2013;Paiva et al., 2015). programme of editorial assistance, and we thank Daniel Brooks for managing it. ...
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The pelagic ecosystem is the ocean's largest by volume and of major importance for food provision and carbon cycling. The high fish species diversity common in the tropics presents a major challenge for biomass estimation using fisheries acoustics, the traditional approach for evaluating mid-water bio-mass. Converting echo intensities to biomass density requires information on species identity and size, which are typically obtained by lethal means, and thus unsuitable in the portion of the ocean that is 'no take'. To improve conservation and ecosystem based management, we present a procedure for determining fish biomass density, using data on species identity, relative abundance, and lengths obtained from stereo baited remote underwater video systems (stereo-BRUVS) to inform the scaling of echosounder survey data (at 38 kHz). We apply the procedure in the British Indian Ocean Territory marine protected area, using acoustic data from 3025 km of survey transects and 546 BRUVS deployments recording relative abundance and size of 12,335 individual fish. Using a Generalised Additive Model of biomass density (GAM, adjR 2 = 0.61) we predict, on the basis of oceanographic conditions and bathymetry, that the top 200 m pelagic ecosystem in the Chagos Archipelago, some 118,324 km 2 , held 3.84 (2.66, 5.62, 95% CI), 33.09 (23.41, 47.35) and 4.08 (3.1, 5.44) million tonnes of fish in November 2012, January 2015, and February 2016, respectively. Our non-extractive procedure yields ecologically credible patterns in biomass across multiple temporal (hours and years) and spatial (metres and kilometres) scales, and marks an improvement on the use of echo intensity alone as a biomass proxy. High seasonal and interannual variability has implication for pelagic fish monitoring.