Vertical Zoning in Marine Protected Areas: Ecological Considerations for Balancing Pelagic Fishing with Conservation of Benthic

Feature: Conservation

Vertical Zoning in Marine Protected Areas: Ecological Considerations for Balancing Pelagic Fishing with Conservation of Benthic Communities Grober-Dunsmore was a marine ecologist with NOAA Fisheries, Southwest Fisheries Science Center Rikki Grober-Dunsmore, (SWFSC) in Santa Cruz, California, and is presently an associate professor at the University of the South Pacific, Fiji. She can be contacted at [email protected]. Lisa Wooninck, Wooninck is a resource protection specialist with Monterey Bay National Marine Sanctuary in Monterey, California. John Field, Field is a fisheries biologist with NOAA Fisheries, SWFSC.

Cameron Ainsworth, Ainsworth is now a post-doctoral fellow at the National Marine Fisheries Service in Seattle, Washington. Jim Beets, Beets is a professor at University of Hawaii—Hilo.

Steve Berkeley, Berkeley’s contribution as a research biologist at the University of California Santa Cruz Long Marine Laboratory was invaluable. Jim Bohnsack, Bohnsack is a fisheries biologist with NOAA Fisheries, Southeast Fisheries Science Center in Miami, Florida. Rafe Boulon, Boulon is the chief of resource management at Virgin Islands National Park/Coral Reef National Monument. Richard Brodeur, Brodeur and Brodziak are fisheries biologists with NOAA Fisheries, Northwest Fisheries Science Center in Newport, Oregon. John Brodziak,

Larry Crowder, Crowder is a professor at the Duke Center for Marine Conservation in Beaufort, North Carolina.

Danny Gleason, Gleason is a professor in the Biology Department at Georgia Southern University in Statesboro.

Mark Hixon, Hixon is a professor in the Zoology Department at Oregon State University in Corvallis.

Les Kaufman, Kaufman is a professor in the Biology Department of Boston University.

Bill Lindberg, Lindberg is a professor in the Fisheries and Aquatic Sciences Department at University of Florida in Gainesville. Marc Miller, Miller is a professor in the School of Marine Affairs at University of Washington in Seattle, Washington. Lance Morgan, Morgan is chief scientist for the Marine Conservation Biology Institute in Glenn Allen, California.

and Charles Wahle Wahle is a scientist with the National Marine Protected Areas Center in Monterey, California.

Abstract: Marine protected areas (MPAs), ideally, manage human uses that threaten ecosystems, or components of ecosystems. During several recent MPA designation processes, concerns have arisen over the scientific justification for no-take MPAs, particularly those that restrict recreational fishing for pelagic species. An important question is: under what conditions might recreational pelagic fishing be compatible with the conservation goals of an MPA that is primarily focused on benthic communities? In 2005, an expert workshop of fisheries biologists, marine ecologists, MPA managers, and recreational fishermen was convened by NOAA’s National MPA Center to evaluate the limited empirical data on benthic-pelagic coupling and to help provide practical advice on this topic. The participants (i) proposed a preliminary conceptual framework for addressing vertical zoning, (ii) developed preliminary guidelines to consider when evaluating whether to allow or restrict pelagic fishing in an MPA, and (iii) identified future research priorities for understanding benthic-pelagic coupling. A suite of ecological conditions where recreational pelagic fishing may not be compatible with benthic conservation were identified: (1) high relief habitats, (2) depths shallower than 50–100 m (depending upon the specific location), (3) major topographic and oceanographic features, and (4) spawning areas. Similarly, pelagic fishing is not likely to affect benthic communities adversely in many circumstances. Until further scientific study can shed more light on the issue of how benthic- pelagic linkages affect specific conservation targets, the proposed framework in this manuscript provides practical, easily-applied guidance for using vertical zoning to manage fishing in multiple use MPAs that focus on benthic conservation.

598 Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g Zonación vertical en Áreas Marinas Protegidas: consideraciones ecológicas en el balance entre la pesca pelágica y la conservación de comunidades bentónicas Resumen: Las Áreas Marinas Protegidas (AMP) idealmente, administran el uso humano que amenaza los ecosistemas o sus componentes. Durante el actual proceso de declaración de AMP, han surgido algunas preocupaciones acerca de la justificación científica para establecer áreas de no pesca, particularmente aquellas que restringen la pesca recreativa de especies pelágicas. Una pregunta importante es ¿bajo qué condiciones la pesca pelágica recreativa es compatible con los objetivos de conservación de un AMP que se enfoca principalmente en comunidades bentónicas? En 2005, un taller de expertos en biología pesquera, ecología marina, manejo de AMP y pescadores recreativos fue convocado por el Centro Nacional de AMP de la NOAA para evaluar los pocos datos empíricos del acoplamiento entre los sistemas pelágico y bentónico, y ofrecer asesoría práctica sobre el tema. Los participantes (i) propusieron un marco conceptual preliminar para abordar el tema de la zonación vertical, (ii) desarrollar directrices preliminares para que cuando se haga una evaluación si se permite o restringe la pesca pelágica dentro de la AMP, y (iii) identificar futuras líneas de investigación para comprender mejor el acoplamiento entre el bentos y el sistema pelágico. Se identificó una serie de condiciones ecológicas en las que la pesca recreativa pelágica puede no ser compatible con la conservación del bentos: (1) hábitat de alto relieve, (2) profundidades menores a 50 m–100 m (dependiendo de la zona), (3) características oceanográficas y topográficas sobresalientes, y (4) áreas de desove. De igual forma, bajo varias circunstancias, la pesca pelágica puede no afectar las comunidades bentónicas. Hasta que los estudios científicos brinden más información acerca de cómo las relaciones entre el bentos y el ambiente pelágico afectan los objetivos específicos de la conservación, el contexto propuesto en este trabajo provee una guía práctica y de fácil aplicación para utilizar la zonación vertical en el manejo pesquero en varios aspectos de las AMP que se enfocan en la conservación del bentos.

INTRODUCTION Halpern and Warner 2003; Agardy 2005)? • Synthesize expert insights into practical Translated into practical terms in the policy preliminary guidelines informed by sci- Marine protected areas (MPAs) can be arena, this question often becomes: when ence, yet with practical application, to effective conservation and management tools might managed fishing be ecologically sus- assist MPA planners, stakeholders, sci- when properly designed, effectively managed, tainable within an MPA without compro- entists, and managers in determining the and supported by user communities (Allison mising the protected area’s effectiveness? At ecological conditions under which verti- et al. 1998; Murray et al. 1999). Historically, present, less than 0.01% of the area contained cal zoning can be used to manage pelagic most of the science and policy emphasis of within U.S. MPAs is managed as no-take, fishing inside an MPA, without compro- MPA design has focused on siting consider- with some form of fishing allowed, including mising the long-term conservation and ations, examining issues such as optimum size, pelagic fishing, in the majority of the MPA management goals of the benthic-focused shape, and connectivity, resilience, and eco- area in the country (Grober-Dunsmore et al. MPA. system responses to protection. Increasingly, 2008). Evaluating the potential compatibility Here, we present the results of that work- however, MPA designation processes are of pelagic recreational fishing in MPAs is a shop to inform future policy discussions about grappling with an equally important scien- daunting challenge, especially in the midst of MPA design, and specifically to help evaluate tific issue with significant policy implications: an ongoing MPA designation or management the appropriateness of managing sport fishing what are the appropriate levels and types of plan review process. for pelagic fishes through a vertical zoning protection needed in each MPA to effectively To fill this growing information gap in approach to MPA design. While our discus- achieve its unique conservation and manage- MPA design, NOAA’s National MPA Center sions focused exclusively on recreational ment goals? convened an expert workshop of fisheries fishing pressure, the principles and concepts This issue is particularly relevant to pro- biologists, marine ecologists, MPA manag- derived may apply to both commercial and posed or existing MPAs that are focused ers, and recreational fishermen in November recreational fishing, though affects on linkage primarily or exclusively on conserving ben- 2005 in Monterey, California. This diverse strength will certainly vary with fishing inten- thic habitats and resources. Examples of the team, with very different backgrounds, exper- sity. These findings address how pelagic fish- importance of the appropriate level of protec- tise, and perspectives on MPAs, worked col- ing may or may not affect benthic organisms tion in proposed MPAs include designations laboratively to: in the Gulf of Mexico by the regional fisheries within the MPA, and assume that harvest of management council, in California’s Channel • Describe the current knowledge about pelagic fishes is not regulated by the MPA. Islands Marine Reserves process, and in the the nature, direction, strength, and pre- Rather, pelagic fishes are assumed to be man- ongoing Marine Life Protection Act initiative dictability of ecological linkages between aged over broader spatial scales. in California state waters. In each case, stake- pelagic fish assemblages and benthic com- holder concerns were raised over the need munities, including fish, invertebrates, and ECOLOGICAL LINKAGES BETWEEN and scientific justification for implementing plants; PELAGIC FISHES AND BENTHIC completely no-take MPAs that would pre- • Develop a conceptual framework for pre- COMMUNITIES clude fishing for pelagic species. dicting whether and how the removal of Underlying this policy debate is a com- pelagic fishes through recreational fishing Benthic communities are often viewed plex and increasingly critical scientific issue: inside the boundary of an MPA may sig- as functionally distinct from the dynamics of under what conditions must MPAs restrict nificantly disrupt or otherwise influence surface waters and associated pelagic popu- all extractive uses (i.e., no-take reserves; ecological linkages to the benthos; and, lations. However, these two realms may be

Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g 599 linked ecologically in ways that profoundly during the course of the study. Consequently, energy is shaded in gray. The varying amounts influence local ecosystem dynamics (Ebersole it is difficult to assess the community level of black and gray represent the proportion of et al. 2005). These linkages, and their impli- effects of removing some portion of a tar- energy that originated from these two major cations for resource management, must be geted pelagic predator population. While diet pathways (Field et al. 2006). For example, considered when designing fishing restrictions content, acoustic tagging, and stable isotope rockfish, hakeMerluccius ( spp.), sablefish in MPAs (Pinnegar et al. 2000). However, studies can provide some insight into the for- (Anoplopoma fimbria), and groundfish (typi- at present there is little direct empirical evi- aging behaviors of certain species (Estrada et cally associated with benthic habitat) derive dence of the nature, strength, and direction al. 2005; Jumars 2007; Collins et al. 2008), the majority of their energy from small pelagic of benthic-pelagic coupling for most species, such studies offer only a point of departure for prey (primarily euphausiids and forage fishes; locations, and environmental conditions assessing the spatial and temporal complexity Field et al. 2006). Clearly, energy flows from (Ebersole et al. 2005). An annotated bibli- of benthic-pelagic linkages. benthic communities up the food web, and ography summarizing empirical evidence for Linkages between benthic and pelagic from pelagic communities down the food web the existence or absence of linkages between assemblages are most evident in marine food through multiple, complex linkages in the benthic and pelagic communities for coastal web models (Walters et al. 1999; Aydin et al. food web. pelagics (Buckel et al. 1999a; Buckel and 2002; Coll et al. 2006; Field et al. 2006, Coll Food web dynamics can reverberate across McKown 2002), oceanic pelagics (Davis and et al. 2007). Marine food webs can be highly the community with major implications for Stanley 2002; Junior et al. 2004; Estrada et al. complex, with an extraordinary number of ecosystem function and fisheries production 2005) and mid-water conduits (Buckley and interactions among a large diversity of spe- (Bascompte et al. 2005; Frank et al. 2005; Livingston 1997; Buckel et al. 1999b; Hunt cies, with energy—often in the form of prey— Mumby et al. 2006) through the effects of et al. 1999) was used for discussions among moving across many gradients (Cohen et al. trophic cascades. Tropic cascades are inter- workshop participants. 2003). Figure 1 illustrates this complexity for actions between trophic levels (e.g., decom- Our understanding of benthic-pelagic the Northern California Current shelf ecosys- poser, producer, herbivore, predator) that linkages is largely derived through diet con- tem, highlighting the importance of under- result in inverse patterns in abundance or tent studies conducted over a short period standing the nature, direction, and strength biomass across more than one trophic link in of time on individual taxa. Often associ- of interactions among different trophic levels a food web (Steele et al. 2007). Simple food ated environmental data (such as depth and (adapted from Field et al. 2006). The colors chain cascades might have unforeseen con- habitat type) are not collected, and the stock represent alternative energy pathways. Pelagic sequences on benthic communities, such as condition and population dynamics of the (primary production) energy pathways are occurred with the removal of sea otters on the predator and prey species are rarely known shown in black and benthic (detrital loop) U.S. Pacific coast (Estes et al. 2004).

Figure 1. Complex marine food web of linkages between pelagic and benthic communities. Gray lines indicate linkages from benthic communities up the food web, and black lines indicate linkages from pelagic communities down the food web. In marine systems, the primary trophic levels can be categorized into groups including top large carnivores (e.g., sharks, marlin), smaller carnivores (e.g., tunas, salmon), planktivores (e.g., baitfishes, herring), herbivores (e.g., parrotfishes), and detritivores (e.g., benthic invertebrates).

600 Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g General Categories of Benthic-Pelagic resource management, though resource man- removal of the pelagic predator through fish- Linkages agers must recognize that spatial and temporal ing could disrupt the flow of energy between variation in linkage strength is most likely the the benthic and pelagic communities (Harvey To distill this complexity for decision- norm. Therefore, these guidelines should be et al. 2003; Savenkoff et al. 2007). Depletion making and provide a general rule of thumb used only as a rule of thumb. Further research of pelagic predators may in turn directly for decision-making, general categories of will likely provide insights into the complexity impact benthic community dynamics of the benthic-pelagic linkages were defined as a inherent among benthic pelagic interactions, MPA (e.g., changes in the relative abundance starting point for assessing the conditions and will reveal how variation in benthic- of certain functional groups, shifts in species where vertical zoning may or may not be pelagic interactions is influenced by local dominance) by increasing prey species abun- appropriate. Benthic-pelagic (BP) linkages conditions (i.e., density of predators and prey, dance and subsequently affecting their inter- show a variety of types, strengths, directions, MPA size, and oceanographic conditions). actions with other benthic species, such as and impacts on a local scale, yet three broad occurs in trophic cascades (Beukers and Jones categories: (i) direct and strong; (ii) indirect Direct and Strong BP Linkages. 1997; Estes et al. 2004; Steneck et al. 2004). and strong, and (iii) weak (Figure 2) that Disturbance of strong bottom-up (Steele et al. define the extremes of benthic-pelagic inter- Direct linkages between benthic and 2007) and top-down biotic forcing pathways actions were considered as a starting point for pelagic assemblages can occur primarily via may ultimately lead to trophic cascades with reference. Obviously, benthic-pelagic inter- predation by free-swimming pelagic species the removal of key species in the food web actions in the real world occur somewhere directly upon fish and/or invertebrates on (Sala 2004; Coll et al. 2007) among these extremes, exhibiting variation or near the bottom (Paine 1992; Wootton Where linkages are direct and strong, in response to a variety of environmental and 1997) or by benthic predators feeding directly pelagic fishing may not be an appropri- oceanographic factors. These three catego- on pelagic prey (Field et al. 2006). Such ate allowed activity in an MPA established ries were identified to be easily applicable to direct linkages tend to be strong and thus the to maintain natural benthic communities.

Figure 2. Generalized conceptual model illustrating strength of benthic-pelagic linkages in typical marine habitats. This provides guidance on ecological conditions that may influence when and where pelagic fishing might be compatible with the goals of a benthic-focused MPA. For example, where benthic- pelagic linkages are direct and strong or where the habitat type is coral reef and the primary fish group of concern is coastal pelagics, then recreational pelagic fishing is most likely not compatible with the objectives of a benthic-focused MPA.

Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g 601 Workshop participants defined shallow water Weak BP Linkages and management planning processes, in the as < 50 m, and deep waters were defined absence of sufficient empirical data, to iden- as those greater than 100 m based on their In certain, perhaps many areas of the tify the ecological conditions where vertical knowledge of recreational fishing techniques ocean, benthic and pelagic communities may zoning may or may not be appropriate. This and interactions between pelagic and benthic be weakly linked or not linked at all (Micheli framework was intended to offer practical species. Figure 2 provides some of the eco- 1999; Estrada et al. 2005; Figure 2). Linkages advice to policymakers, with the input of the logical circumstances where direct and strong tend be weak in deeper water where there is scientific and fishing communities. The con- benthic-pelagic linkages might be expected, little direct interaction between the pelagic ceptual framework consists of one primary and thus where pelagic fishing might not be and benthic communities, since pelagic (water depth) and three secondary ecological appropriate. Vertical zoning may not be ideal predators may forage only on organisms in considerations (habitat type, predator type, in: (1) shallow water habitats (< 50 m depth), the upper water column (Abitia-Cardenas et and taxonomic, mobility and life history al. 1999; Olson and Galvan-Magana 2002) (2) habitats with high topographic relief (e.g., characteristics of pelagic species). and benthic communities may only interact reefs, canyons and sea mounts), (3) areas with directly with surface waters when detritus Water Depth strong-biophysical coupling (e.g., upwelling and carcasses of organisms sink to the ben- zones), (4) areas with permanent or seasonal thos. Even in deep water areas, there could In the proposed conceptual framework, spawning or feeding aggregations, and (5) be important coupling of the pelagic and ben- the primary ecological consideration for dominated by coastal pelagic and mid-water thic zone, since the benthos may have little assessing the feasibility of vertical zoning is conduit species (depending upon location or no primary production and be dependent depth. The depth of the water column within may include shad, mackerel, or anchovy). on subsidies from the pelagic zone. Weak and surrounding an MPA will likely influence The rationale for these recommendations will linkages may occur when there is redundancy the strength or weakness of its benthic-pelagic be discussed in the conceptual framework. in functional groups such that removal of linkages, primarily by affecting the proximity some individuals from either community will of pelagic predators with bottom-dwelling Indirect and Strong BP Linkages not perceptibly alter the flow of energy, or in prey. Consequently, shallow water habitats the case of mid-water prey when only a small will generally have stronger benthic-pelagic Pelagic and benthic communities may part of the diet of the intermediary is from the linkages than deeper water areas (Figure 2). In also be linked indirectly through mid-water benthic zone. Where linkages are weak, verti- areas shallower than 50 m, linkages are likely species such as forage fishes (e.g., shad, ancho- cal zoning may be appropriate since pelagic strong and often direct, as pelagic predators vies). Such forage fishes often serve as verti- fishing is likely to have limited influence on often interact with benthic and mid-water cal conduits of energy and material between the benthic community (Figure 2). prey (Arendt et al. 2001; Rosas-Alayola et upper and deeper waters (Figure 2; Harvey et In summary, where benthic-pelagic link- al. 2002). Important ecological linkages may al. 2003; Wilson et al. 2006). For example, ages are weak, and the impacts of pelagic fish- also exist in habitats occurring at depths large schools of forage fishes often feed directly ing are minimal, recreational pelagic fishing exceeding 100 m (Aydin et al. 2002; Cartes on organisms living in benthic communities managed through vertical zoning may be and Carrasson 2004) depending on the area’s (Cabral and Murta 2002; Wilson et al. 2006); appropriate. Where benthic-pelagic link- ecosystem type, local oceanography, and spe- consequently the removal of these fishes may ages are strong, and the potential impacts of cies composition. disrupt these linkages, resulting in changes in pelagic fishing on benthic communities are benthic community structure (e.g., increases expected to be high, pelagic fishing of any Habitat Type or decreases in the abundance of benthic kind is probably not an appropriate manage- organisms that are prey items of forage fishes; ment strategy. Under this scenario, a no-take Several habitat attributes can create con- Coll et al. 2006; Jumars 2007). Benthic MPA may be the most effective approach to ditions conducive for strong benthic-pelagic organisms may also depend upon midwater achieving the protected area’s benthic con- linkages (Pinnegar et al. 2000; Aydin et al. prey (Bosley et al. 2004), exerting bottom- servation goals. However, the majority of sit- 2002). For example, coral reefs, rocky reef, uations are likely considerably more complex kelp forest, and other topographically com- up (emanating from the sea floor up into the and fall somewhere between these two ends plex habitats are likely to have strong benthic- water column) influences on trophic energy of the spectrum. pelagic linkages reflecting diverse food web flow. Though less direct, these linkages can dynamics between surface waters and bottom- be strong, and potentially exert considerable A CONCEPTUAL FRAMEWORK dwelling species (Figure 2). Generally, these control over benthic and pelagic community heterogeneous habitats often attract transient structure (Sala and Graham 2002; Bascompte Because placing benthic-pelagic link- pelagic predators from deeper water habitats. et al. 2005; Field et al. 2006). Consequently, ages into the simplified categories indicated Prominent topographic features such as sea- recreational pelagic fishing may not be above will be challenging, and will not cap- mounts and canyons are often oceanographic appropriate in benthic-focused MPAs, where ture the full complexity of real world condi- hotspots that attract pelagic fishes (Dower indirect, yet strong benthic-pelagic coupling tions, a preliminary conceptual framework and Brodeur 2004; Wilson and Boehlert persists. Depending upon the level of fishing which addresses known ecological conditions 2004; Sydeman et al. 2006), increasing the pressure, disruption or elimination of indi- such as water depth, predator type, habi- strength of linkages. Similarly, areas charac- rect ecological linkages between benthic and tat type and predator taxonomic, mobility, terized by robust and predictable biophysical pelagic communities could result in cascading and life history characteristics is proposed. coupling (e.g., upwelling) create conditions changes in community structure. Examples of This conceptual framework was developed favorable for strong benthic-pelagic linkages such circumstances are shown in Figure 2. to help inform real-world MPA designation (Navarrete et al. 2005), as do areas with sig-

602 Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g nificant gradients in temperature, currents, of this group, assuming that benthic-pelagic the population status of the pelagic species of and complexity. Often this coincides with linkages will be greater in areas of strong interest. the location of the continental shelf break, upwelling, high topographic complexity, and though not always. around physiographic features may be the Taxonomic, Mobility and Life History most prudent guideline available. Characteristics of Pelagic Species Pelagic Predator Type Oceanic pelagics are migratory and spend the majority of their lives in deep waters The patterns described above among The strength and nature of benthic- offshore (typically beyond the continental different pelagic predator types can be illus- pelagic linkages in any specific MPA is likely shelf). For many oceanic pelagics including trated for particular species of interest to influenced heavily by the taxonomic com- sharks and marlins, benthic-pelagic linkages MPA managers and fishermen (Table 2). position and densities of predator and prey can be relatively weak (Moteki et al. 2001; Each recreationally-fished pelagic species species and the community structure of the Olson and Galvan-Magana 2002; Sinopoli localized food web. As a starting point for et al. 2004; Lucifora et al. 2005), though not (and some reef fishes) was classified using decision-making, predicted linkage strengths always (Sinopoli et al. 2004). These species the best available scientific information and were developed based on the behavior of key may range into coastal waters or over the con- the experience and knowledge of workshop predator species and their location relative to tinental shelf for brief periods, depending on participants to provide estimates of the water depth and distance from shore. A broad seasonal fluctuations, oceanographic condi- effects of removing these species from an spectrum of taxa was grouped into four mobil- tions, or climatic anomalies. Generally, how- MPA. Each species was categorized based ity categories relative to their interactions ever, these species occur far offshore, in waters on its bio-geographic and offshore/onshore with benthic communities: coastal pelagics, deeper than 100 m. Based on the limited data range of occurrence and placed in a mobil- oceanic pelagics, mid-water conduits, and for- available for this group, benthic-pelagic link- ity guild (resident, visitor, and transient). age fish (Table 1). ages are predictably weak. Understanding the relative mobility of tar- Coastal pelagics occur in near shore Forage fishes are linked to multiple geted pelagics is important since removal of waters typically on the continental shelf. The trophic groups in the food web, consuming a more resident species (e.g., cero mackerel distance of the continental shelf from shore prey from multiple trophic levels (Robinson Scomberomorus regalis) that primarily reside varies considerably with physiographic condi- 2000; Miller and Brodeur 2007) and being within a localized area (i.e., MPA) is likely tions; therefore, the distance from shore will consumed by a variety of predators. Because not always be sufficient for classifying species. linkages are more indirect, it is difficult to pro- to have greater consequences on disrupt- Coastal pelagics may range off of the conti- pose guidelines for this group (Table 1). ing benthic-coupling compared to remov- nental shelf break, but spend the majority of For these last three groups, site- and ing a more transient species (e.g., sailfish time over the continental shelf. Generally situation-specific information will be needed Istiophorus platypterus; Table 2). The mobil- taxa within this mobility guild occur in shal- to develop practical guidelines for consider- ity of the pelagic species must be considered low waters and are relatively accessible to the ing fishing impacts on benthic communities. to evaluate the possible effects of removing recreational fishery. Often, benthic-pelagic For example, for mid-water conduits, oceanic individuals of certain species, but mobility linkages for this broad group are moderate- pelagics, and forage fishes, benthic-pelagic must also be assessed relative to the bound- strong (Meyer et al. 2001; Bertrand et al. linkages will likely vary in areas of (1) upwell- aries of the MPA. If the pelagic species is 2002; Bertrand et al. 2004; Wetherbee et ing, (2) increased physiographic complexity, moving regularly in and out of the MPA, the al. 2004), though not always (Buckel et al. (3) increased population sizes of target species, location of harvest is irrelevant. The question 1999b; Bertrand et al. 2004). and (4) increased fishing pressure. Temporal is whether a large proportion of the targeted Mid-water conduits occur between the variance in benthic-pelagic coupling may also fish population is moving inside and out of upper water column and the benthic com- occur, since in some years (such as during El the MPA, such that fishing on the edge may munity, including some demersal fishes, and Nin~o), a species may be more coastal than in can serve as conduits of energy and materials La Nin~a years, where the same species may be little different than fishing inside. If this is between benthic and pelagic communities. be more oceanic in distribution. Differences the case, the act of removal within the MPA Mid-water conduits can range widely in the in the behavior of species may occur among may be indistinguishable from removal out- strength of benthic-pelagic linkages, from regions, in response to variation in oceano- side the MPA (Walters et al. 1999). weak (Bromley et al. 1997; Hunt et al. 1999; graphic conditions, physiographic features, In addition, the spatial and temporal pre- Kaeriyama et al. 2004) to strong (Buckley and the location of the continental shelf, and dictability of occurrence within an MPA Livingston 1997), and act as either predators or prey. For example, most semi-pelagic (mid- Table 1. Pelagic fish groups, general benthic pelagic linkage strength and general guidelines water schooling) rockfish are primarily plank- useful for vertical zoning. tivorous, though prey consumption varies from zooplankton, forage fish, and cephalo- Pelagic fish group Example species Linkage strength Direct pods to mesopelagic fishes, with diet varying Coastal pelagics (< 100 m depth or onshore) Jacks, mackerels, bluefish Strong with fish species (Brodeur and Pearcy 1984). Indirect Mid-water conduits (neritic zone-conduits) Rockfishes, snappers, cod The degree to which mid-water species inter- Weak—Strong act with benthic and pelagic communities can Indirect Forage fishes Herring, sardine, shad, anchovy also vary greatly with ontogeny (e.g., Able et Weak—Unknown Indirect al. 2003). Until further scientific information Oceanic pelagics (> 100 m depth) Marlin, tuna, sharks Weak can shed more light on the foraging ecology

Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g 603 Table 2. Potential strength of benthic-pelagic linkages for selected recreationally-targeted pelagic Notes: species (does not include benthic reef fishes except for groupers and snappers) representing different a = catch and release, regions, species types, and mobilities. For each taxon, the table illustrates general information on: b = varies with oceanographic features, (i) predicted mobility; c = temperature dependent, (ii) spatial and temporal predictability of occurrence within an MPA d = seasonal, (H = high potential, M = moderate, L = low potential); e = chumming can alter behavior, (iii) the likely role of each species in maintaining benthic-pelagic coupling; f = scale of movement unknown, g = patchy distribution. (iv) the potential for each species to be overfished within an MPA; (v) the likelihood of benthic-pelagic linkages being disrupted by fishing, While snappers and groupers are generally benthic which synthesizes information from the previous five categories; and reef-associated fishes, they are included in the table (vi) the potential for bycatch of other non-targeted species, which could since at particular stages in their life history, they can indirectly affect benthic-pelagic linkage strength and direction inadvertantly. occur in the water column or pelagic environment.

Likelihood Spatial Temporal Potential of BP Potential predict. predict. of Strength of to be Species type Species name Mobility category linkages for bycatch occurrence occurrence BP linkage overfished disrupted impacts in MPA in MPA in MPA by fishing

ATLANTIC spanish and cero mackerel coastal pelagic Scomberomorus maculatus; resident H H H M M H Scomberomorus regalis migratory king mackerel H visitor/transient M M M L L coastal pelagic Scomberomorus cavalla amber jack (reef-associated) H coastal pelagic visitor/transient M M M L L Seriola lalandi non-migratory blue runner (jack) H resident H H H H H coastal pelagic Caranx crysos

non-migratory bar jack visitor/transient H H H H H H coastal pelagic Carangoides ruber

non-migratory crevalle, horse eye other jacks visitor/transient M M M? L L H coastal pelagic Caranx hippos; Caranx latus tarpon coastal pelagic Resident H H H L a L a H Megalops atlanticus oceanic and dolphin/mahi coastal pelagic (visits visitor/transient M b H L L L H Coryphaena hippurus coast) migratory sailfish visitor Le M-H L L L L oceanic pelagic Istiophorus albicans

PACIFIC migratory salmon depends on L d L (surface) visitor/transient M-H L L coastal pelagic Oncorhynchus spp. time of year H d H (deep)

migratory tunas transient L M L-M L L L coastal pelagic Thunnus spp.

non-migratory jacks visitor/transient M H M-H L-M L-M M coastal pelagic Caranx spp.

migratory sardines visitor/ transient L H c H L L L coastal pelagic Sardinella spp.

migratory anchovies visitor/transient L H H L L L coastal pelagic Engraulis spp.

migratory Pacific mackerel visitor/transient L H M L L L coastal pelagic Sconber japonicus

non-migratory midwater rockfish resident/visitor H H H H H H coastal pelagic Sebastes spp.

migratory oceanic sharks transient L H d L L L L oceanic pelagic Carcharhinus spp.

604 Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g Likelihood Spatial Temporal Potential of BP Potential predict. predict. of Strength of to be Species type Species name Mobility category linkages for bycatch occurrence occurrence BP linkage overfished disrupted impacts in MPA in MPA in MPA by fishing

CARIBBEAN SEA or GULF OF MEXICO tarpon coastal pelagic resident H H H La L a H Megalops spp.

oceanic pelagic dolphin (mahi) visitor/transient Mb Ha L L ? H (visits coast) Megalops atlanticus

oceanic pelagic wahoo visitor/transient M M M L L ? (visits coast) Acanthocybium solandri

oceanic pelagic barracuda resident/visitor ? ? M L L ? (visits coast) Sphyraeana spp.

oceanic and amber jack visitor/transient M M M? L L H coastal pelagic Seriola lalandi

oceanic and blue runner (jack) resident H H H H H H coastal pelagic Caranx crysos

bar jack coastal pelagic visitor H H H H H H Carangiodes spp. oceanic and coastal crevalle, horse eye, other jacks visitor/transient M M M? L L H pelagic Caranx spp. oceanic and coastal dolphin/mahi visitor/transient M H L L L H pelagic (visits coast) Coryphaena hippurus migratory sailfish oceanic pelagic visitor Le M-H L L L L Istiophorus albicans (visits coast) migratory marlin (blue) oceanic pelagic visitor L L L L L L Makaira nigricans (visits coast) blue and mako sharks oceanic pelagic Prionace glauca transient L L L L L L

reef sharks coastal pelagic resident/visitor H H H H H H Carcharhinus spp. tuna (dogtooth) coastal pelagic resident H H H H H H Thunnus spp. oceanic and coastal tuna (small) visitor M M M L L L pelagic (visits coast) Thunnus spp. migratory tuna (large) oceanic and coastal transient L L L L L L Thunnus spp. pelagic snapper (reef-associated) non-migratory (yellowtail) resident/visitor H H H H H H coastal species Lutjanus spp. non-migratory snapper (reef fish) resident M-H H H H H H coastal reef fish Lutjanus spp. non-migratory fusiliers resident H H H H H M coastal pelagic Caesio spp. coastal barracuda (reef) resident/visitors/ H H H H H L-M (mostly non- Sphyreana spp. transients L? M L? L? L? H migratory) (offshore) groupers (gag and scamp) resident/visitors/ coastal reef fish (reef fish) H H H H H L transients Mycteroperca spp. non-migratory ballyhoo oceanic and coastal ? f M g M d L-H ? L? L? Hemiramphus spp. pelagic cobia coastal pelagic visitors and transients L M d M/H? L L-M ? Rachycentron canadum

Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g 605 (Table 2) may provide additional guidance was proposed by synthesizing information in it is still effectively removed from the system on how removal of particular species may the preceding five categories for each species (Alpine and Hobday 2007). The predictabil- disrupt benthic-pelagic linkages. If the spa- (Table 2). This final classification should not ity of the pelagic predator and the harvest tial and temporal predictability of a pelagic be interpreted as a rule; rather it should be rates by pelagic fishing are likely to influence species within an MPA is high, then their used as a rough guide, and where possible the level of uncertainty in decision-making. removal may have greater consequences on environmental and behavioral factors and benthic-pelagic linkages than removing spe- site-specific information should be coupled RESEARCH PRIORITIES cies that have low spatial and temporal pre- to provide the best decision for each MPA. dictability. For example, tarpon (Megalops The workshop distilled broad areas of atlanticus) have a higher predicted spatial Reducing Uncertainty agreement around basic principles of ben- and temporal occurrence within a particu- thic-pelagic linkages and generated guide- lar area; therefore their influence on local Due to a lack of scientific information lines for where a vertical zoning approach for benthic-pelagic coupling may be greater on benthic-pelagic linkages, considerable MPA design may be appropriate. In addi- than that expected for a species such as a uncertainty on several topics exists for MPA tion, a number of avenues of further scien- tuna, which has lower spatial and temporal planners and stakeholders when deciding tific inquiry were identified. Among these predictability. whether vertical zoning of fishing is -war were four key areas of research. The role of each species in maintaining ranted in a given area. These include: First, new methods (e.g., stable isotope coupling between benthic and pelagic com- MPA Size—The size of an MPA rela- ratios, DNA analysis) can help supplement munities was also proposed, by considering tive to the population or stock size is an traditional food habit studies to expand on the feeding ecology and relative position important consideration (Planes et al. 2000; studies of spatial (i.e., depth, habitat qual- of each species in the water column (Table Murawski et al. 2005; Meyer et al. 2007) ity, oceanographic conditions) and temporal 2). This is important since exploitation of and may influence whether or not fishing (i.e., ontogenetic shifts, seasonal) variability species with different life history strategies levels will actually impact benthic-pelagic in the food habits of many species. Such can have different population and food web linkages. For example, many MPAs are so information would greatly increase the ability consequences (Schindler et al. 2002). Food small that the potential of recreational fish- to use food web models to understand energy web responses are expected to be strongest ing to disrupt benthic-pelagic linkages may transfers across space, time, and trophic lev- where unexploited biomass of long-lived be minor, especially under relatively low els. Spatially explicit multi-species modeling species is high and predation (in this case extraction levels and among highly migra- approaches are being developed that can aid fishing) is relatively specialized compared tory species. However, this is not always the in exploring species interactions that may be with other apex predators (Schindler et al. case (Westera et al. 2003). important to consider in marine reserve design 2002). In many cases, species exhibit a shift Home Range Size—The mobility of the (Walters et al. 1999; Pauly et al. 2000). Such in their diet to more pelagic or benthic prey pelagic component relative to the size of the studies highlight the importance of species with increasing size (Brodeur et al. in press), MPA and the home range sizes of organisms interactions and harvest dynamics for deter- therefore life history stage and potentially within the MPA should also be considered mining the appropriate reserve size, spacing, other species-specific characteristics may during MPA design (Kerwath et al. 2007; and performance of an MPA (Baskett et al. influence food web dynamics and benthic- Meyer et al. 2007). As MPAs control the spa- 2007). These modeling approaches represent pelagic linkage strength. tial location where pelagic fishing occurs, it one way of quantitatively evaluating optimal This species-specific life history infor- most likely does not matter whether a school fishing policies, for predicting ecosystem mation was evaluated to provide a rough of bait fish, for example, is caught within or level changes following changes in fishing guide for assessing the compatibility of verti- immediately outside of an MPA, since the pressure, and potentially for determining the cal zoning for pelagic species by estimating effect of their removal from the ecosystem effectiveness of an MPA based upon its size, overfishing potential and the likelihood that will be the same. If the range of movement oceanographic conditions, and trophic and removal of a particular species would disrupt of a school of baitfish is larger than the size of population structure (Walters et al. 1999; benthic-pelagic coupling (Table 2). The the MPA, then the MPA is only providing a Pelletier and Mahevas 2005). Advances in potential for a particular species to be over- temporary spatial relief from fishing (Shipp multi-species modeling approaches and data fished within an MPA was estimated using 2003). As soon as the school moves outside availability should provide the means to bet- information on home range size, school- the boundaries of the MPA, it becomes vul- ter cope with the challenges of incorporating ing behavior, and population status. For nerable to capture, thereby negating local- such complexity in the face of spatially-com- example, salmon which are highly migra- ized management measures within the MPA plex management regimes. tory, moving inside and outside the bound- (Parnell et al. 2006). Second, satellite tagging technologies aries of most small MPAs, are less likely to Predator Predictability—If the pelagic are now widely used to document the geo- be over-fished than more resident species of species is present within the MPA at pre- graphic and vertical movements (Wilson rockfish, which have affinities for specific dictable times, such as at spawning aggre- et al. 2007) and identify feeding, spawning, habitat types or benthic communities. If the gations (Kerwath et al. 2007), then a high and resting areas (e.g., Block et al. 2001) of boundaries of an MPA overlap with these catch rate may lead to local depletion of the pelagic fishes. Increasingly, such tags are used specific habitat types, then the potential for stock and disrupt local benthic-pelagic link- to record measurements of depth and tem- rockfishes to be overfished inside the MPA ages. However, if pelagic predators are more perature to assess the frequency, persistence may be considerable. ephemeral in space and/or time, it may not and patterns of vertical movements for vari- The likelihood of benthic-pelagic link- matter if a pelagic is caught within or imme- ous pelagic species including whale sharks ages being disrupted by recreational fishing diately outside the boundaries of the MPA; (Rhincodon typus; Wilson et al. 2007), sea

606 Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g turtles (Gaspar et al. 2006), tunas (Block et al. 2001), and marlin (Horodysky et al. 2007). Notably, such research could also provide more evidence to support or modify the depth criteria (50-100 m and TrackTrack youryour fishfish withwith thethe > 100 m). Advances in tracking technology and data availability will mostmost advancedadvanced acousticacoustic be invaluable for evaluating the oceanographic and physiographic conditions where vertical zoning may be appropriate for individual trackingtracking receiverreceiver species. Third, the impacts of disrupting benthic-pelagic linkages within availableavailable today.today. specific benthic communities and habitat types are often poorly understood, particularly in heterogeneous ecosystems such as coral reefs and kelp beds. Community-level studies replicated in various habitats, geographic locations, and ecological conditions that exam- ine the consequences of disrupting energy transfer between pelagic and benthic communities are needed to provide critical informa- tion for assessing how marine ecosystems are mediated by bottom- up and top-down processes. Benthic ecosystems that are controlled by bottom-up processes may be less affected by pelagic fishing than those that are mediated primarily through top-down controls. As studies account for variation in fishing pressure and other ecological characteristics intrinsic to benthic-pelagic coupling, future work may provide insights on how benthic pelagic coupling varies spatially and temporally. Finally, understanding the effects of pelagic fishing on benthic- pelagic relationships is best accomplished through cooperative research with recreational fishermen to determine when bycatch occurs, at what depth and with what gear. This type of scientific part- nership has great potential for assessing the effects of pelagic fishing on benthic communities. Furthermore, recreational fishermen are VEMCO’s VR100 Acoustic key partners for developing fishing methods that minimize bycatch and damage to benthic communities. The creative “know-how” of Tracking Receiver is the the fishing community can be engaged by soliciting their advice and ultimate fish tracking solution. practical knowledge of gear efficiency, fish behavior, and best fishing practices and by working side by side with them on the water and in hether you are actively tracking large pelagic fish laboratories. Collaborative research will not only yield innovative Wor conducting presence/absence studies, the sustainable fishing practices, but also productive and positive rela- VR100 will get the job done. The VR100 has a flexible tionships among scientists and fishermen (arguably the most knowl- systems architecture with 8MB of non-volatile internal edgeable marine user group). memory, GPS positioning and precise timing, USB link to PC or laptop, and field installable software upgrades. TOWARD VERTICAL ZONING IN MULTIPLE USE MPAS Other features include:

 Depending on the responses to and tests of its utility as a practi- Simultaneous, multi-frequency reception and cal management tool, the Benthic-Pelagic Linkages Workshop rep- detection tracking algorithms  resents a significant advance in resolving a key issue in MPA design: Wide dynamic range allowing multi-tag reception determining the appropriate level and type of protection for the area without gain adjustment  in question. The participants overcame vast differences in experi- Splash proof case with marine grade connectors  ence and interests to find common ground on the question of when Operates with coded and continuous tags it might be appropriate to consider allowing recreational pelagic fish- (sold separately)  Operation frequency 10-100kHz ing in MPAs focused primarily on benthic conservation. This kind of collaborative problem solving integrates knowledge and experi- VEMCO (a division of AMIRIX Systems Inc.) ences of scientists, managers, and resource users to form effective and Tel: 902-450-1700 Fax: 902-450-1704 equitable conservation solutions to conserve important ocean areas. Important practical next steps include advancing new research to fill www.vemco.com the key information gaps listed above, expanding this assessment to commercial pelagic fisheries, and developing best practices for low impact recreational fishing in MPAs and elsewhere. In addition, the Making Waves in challenges of effective enforcement in a vertically zoned MPA and Vemco (A Division of Amirix) the development of novel and practical approaches to the growing Acoustic Telemetry need to monitor and enforce compliance within established MPAs cannot be understated.

Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g 607 Acknowledgments Arendt, M. D., J. E. Olney, and J. A. the development of food webs in pelagic Lucy. 2001. Stomach content analysis of 0-group cod (Gadus morhua L.), had- The resource managers, recreational fish- cobia, Rachycentron canadum, from lower dock (Melanogrammus aeglefinus), whiting ermen, and scientists who participated in the Chesapeake Bay. Fishery Bulletin 99:665- (Merlangius merlangus L.), saithe (Pollachius MPA Science Institute’s benthic-pelagic link- 670. virens L.), and Norway pout (Trisopterus ages workshop held in Monterey, California, in Aydin, K. Y., V. V. Lapko, V. I. Radchenko, esmarkii Nilsson) in the northern North Sea. November 2005 each contributed to the ideas and P. A. Livingston. 2002. A comparison of ICES Journal of Marine Science 54. and recommendations presented. Participants the Eastern Bering and Western Bering Sea Buckel, J. A., D. O. Conover, N. D. Steinberg, included: Cameron Ainsworth, Jim Beets, Shelf and Slope ecosystems through the use and K. A. McKown. 1999a. Impact of age-0 Bill Bennett, Jeff Benoit, Steve Berkeley, of mass-balance food web models, National bluefish Pomatomus ( saltatrix) predation on Barbara Block, Jim Bohnsack, Rafe Boulon, Marine Fisheries Service Deep Sea Research age-0 fishes in the Hudson River estuary: Rick Brodeur, Jon Brodziak, Carrie Byron, Part II: Topical Studies in Oceanography. Evidence for density-dependent loss of juve- Greg Calliet, Mark Carr, Larry Crowder, John Volume 52, Issues 5-6. nile striped bass (Morone saxatilis). Canadian Bascompte, J., C. J. Melian, and E. Sala. 2005. Ebersole, Bob Fletcher, Danny Gleason, Rikki Journal of Fisheries and Aquatic Sciences Interaction strength combinations and the Grober-Dunsmore, Dennis Heinemann, 56:275-287. overfishing of a marine food web. Proceedings Dan Hellin, Mark Hixon, Les Kaufman, Bill Buckel, J. A., M. J. Fogarty, and D. O. of the National Academy of Sciences of the Lindberg, Rebecca Martone, Karen McLeod, Conover. 1999b. Foraging habits of bluefish, United States of America 102:5443-5447. Pomatomus saltatrix, on the U.S. east coast Marc Miller, Lance Morgan, Gil Radonski, Baskett, M. L., F. Micheli, and S. A. Levin. Tom Raftican, Rick Starr, Charlie Wahle, continental shelf. Fishery Bulletin 97:758- 2007. Designing marine reserves for interact- 775. Jack Wiggin, and Lisa Wooninck. Bob Zales ing species: insights from theory. Biological II, a member of the MPA Federal Advisory Buckel, J. A., and K. A. McKown. 2002. Conservation 137:163-179. Competition between juvenile striped bass Committee, also contributed thoughtful Bertrand, A., M. A. Barbieri, J. Cordova, C. comments to the paper. It is with great respect and bluefish: resource partitioning and Hernandez, F. Gomez, and F. Leiva. 2004. growth rate. Marine Ecology Progress Series and sadness that we dedicate this article to Diel vertical behaviour, predator-prey rela- 234:191-204. the memory of Steve Berkeley, whose spirit tionships, and occupation of space by jack Buckley, T. W., and P. A. Livingston. 1997. embodies the very collaborative nature of mackerel (Trachurus murphyi) off Chile. Geographic variation in the diet of Pacific this work in bringing scientists and fishermen ICES Journal of Marine Science 61:1105- hake, with a note on cannibalism. California together to resolve complex fishery manage- 1112. Cooperative Oceanic Fisheries Investigations ment issues. His input on this controversial Bertrand, A., F. X. Bard, and E. Josse. 2002. Reports 38:53-62. topic added tremendous inspiration, perspec- Tuna food habits related to the micronekton Cabral, H. N., and A. G. Murta. 2002. The tive, and significant dollops of provocation; distribution in French Polynesia. Marine diet of blue whiting, hake, horse mackerel your wisdom, humor and friendship are deeply Biology 140:1023-1037. and mackerel off Portugal. Journal of Applied Beukers, J. S., and G. P. Jones. 1997. Habitat missed. Ichthyology 18:14-23. complexity modifies the impact of piscivores Cartes, J. E., and M. Carrasson. 2004. on a coral reef fish population. Oecologia References Influence of trophic variables on the depth- 114: 50-59. range distributions and zonation rates of Block, B. A., H. Dewar, S. B. Blackwell, T. Abitia-Cardenas, L. A., F. Galvan-Magana, F. J. deep-sea megafauna: the case of the west- D. Williams, E. D. Prince, C. J. Farwell, A. Gutierrez-Sanchez, J. Rodriguez-Romero, ern Mediterranean assemblages. Deep-Sea B. Aguilar-Palomino, and A. Moehl-Hitz. Boustany, S. L. H. Teo, A. Seitz, A. Walli, Research Part I-Oceanographic Research 1999. Diet of blue marlin Makaira mazara off and D. Fudge. 2001. 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608 Fisheries • v o l 33 n o 12 • d e c e m b e r 2008 • w w w .f i s h e r i e s .o r g on the Shag Rocks shelf (Southern Ocean). Journal of Fish Biology 72:271-286. Davis, T. L. O., and C. A. Stanley. 2002. Vertical and horizontal move- ments of southern bluefin tunaThunnus ( maccoyii) in the Great VEMCO’sVEMCO’s VR2WVR2W deliversdelivers Australian Bight observed with ultrasonic telemetry. Fishery Bulletin 100:448-465. thethe bestbest resultsresults inin freshwaterfreshwater Dower, J. F., and R. D. Brodeur. 2004. The role of biophysical coupling in concentrating marine organisms around shallow topographies. andand marinemarine environmentsenvironments Journal of Marine Systems 50:1-2. Ebersole, J., C. J. Byron, J. Benoit, and D. Hellin. 2005. Synthesis of existing information on linkages between pelagic fishes and the ben- thic communities within marine protected areas. National Oceanic Over 10,000 units deployed worldwide and Atmospheric Administration, Monterey, California. provides opportunities for researchers Estes, J. A., E. M. Danner, D. F. Doak, B. Konar, A. M. Springer, P. to collaborate and share data! D. Steinberg, M. T. Tinker, and T. M. Williams. 2004. Complex trophic interactions in kelp forest ecosystems. Bulletin of Marine The VR2W Single Channel Receiver was designed us- Science 74:621-638. ing the same proven technology as the VR2. Affordable, Estrada, J. A., M. Lutcavage, and S. R. Thorrold. 2005. Diet and trophic compact, easy to use, long-lasting and flexible, the VR2W position of Atlantic bluefin tuna Thunnus( thynnus) inferred from sta- is ideal for any freshwater and marine research project. With ble carbon and nitrogen isotope analysis. Marine Biology 147:37-45. the VR2W, VEMCO has made the VR2 even better! Field, J. C., R. C. Francis, and K. Aydin. 2006. Top-down modeling and bottom-up dynamics: Linking a fisheries-based ecosystem model with  Significantly faster upload climate. Progress in Oceanography 68:238-270. speed - retrieve data 20 Frank, K. T., B. Petrie, J. S. Choi, and W. C. Leggett. 2005. Trophic times faster than the VR2 cascades in a formerly cod-dominated ecosystem. Science 308:1621- and from up to 7 receivers 1623. simultaneously Gaspar, P., J. Y. Georges, S. Fossette, A. Lenoble, S. Ferraroli, and  Increased data storage Y. Le Maho. 2006. Marine animal behaviour: neglecting ocean cur- capability enables users to rents can lead us up the wrong track. Proceedings of the Royal Society collect substantial amounts B-Biological Sciences 273:2697-2702. of field data - 8 MBytes Grober-Dunsmore, R., L. Wooninck, C. Wahle, and L. Wenzel. 2008. (1-million detections), 4 State of the nation’s de facto marine protected areas. National Oceanic times that of the VR2 and Atmospheric Administration, Santa Cruz, California. Halpern, B. S., and R. R. Warner. 2003. Matching marine reserve design  Field upgradable design to reserve objectives. Proceedings of the Royal Society of London allows the VR2W to be Series B-Biological Sciences 270:1871-1878. upgraded in the field Harvey, C. J., S.P. Cox, T. E. Essington, S. Hansson, and J. F. Kitchell.  All detections are retained in non-volatile memory so 2003. An ecosystem model of food web and fisheries interactions in data is saved even if the unit unexpectedly fails the Baltic Sea. International Council for the Exploration of the Sea 60:939–950.  Fully compatible with various size coded transmitters Horodysky, A. Z., D. W. Kerstetter, R. J. Latour, and J. E. Graves. and sensor tags 2007. Habitat utilization and vertical movements of white marlin The VR2W also uses enhanced PC Software. The new (Tetrapturus albidus) released from commercial and recreational fish- VEMCO User Environment (VUE) PC Software for ing gears in the western North Atlantic Ocean: inferences from initialization, configuration and data short duration pop-up archival satellite tags. Fisheries Oceanography upload from VEMCO receivers allows 16:240-256. users to combine data from multiple Hunt, S. L., T. J. Mulligan, and K. Komori. 1999. Oceanic feeding receivers of varying types into a single habits of Chinook salmon, Oncorhynchus tshawytscha, off northern integrated database. California. Fishery Bulletin 97:717-721. Jumars, P. A. 2007. Habitat coupling by mid-latitude, subtidal, marine Contact us about affordable options for upgrading mysids: import-subsidised omnivores. Oceanography and Marine your VR1s and VR2s to VR2W receivers. Biology (45): 89-138. Junior, T. V., C. M. Vooren, and R. P. Lessa. 2004. Feeding habits of VEMCO (a division of AMIRIX Systems Inc.) four species of Istiophoridae (Pisces : Perciformes) from northeastern Tel: 902-450-1700 Fax: 902-450-1704 Brazil. Environmental Biology of Fishes 70:293-304. Kaeriyama, M., M. Nakamura, R. Edpalina, J. R. Bower, H. Yamaguchi, www.vemco.com R. V. Walker, and K. W. Myers. 2004. Change in feeding ecology and trophic dynamics of Pacific salmon Oncorhynchus( spp.) in the central Gulf of Alaska in relation to climate events. Fisheries Oceanography Making Waves in 13:197-207. Vemco (A Division of Amirix) Kerwath, S. E., A. Gotz, C. G. Attwood, W. H. H. Sauer, and C. Acoustic Telemetry G. Wilke. 2007. Area utilisation and activity patterns of roman Chrysoblephus laticeps (Sparidae) in a small marine protected area.

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