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Linking Movement Ecology with Wildlife Management and Conservation

Linking Movement Ecology with Wildlife Management and Conservation REVIEW published: 12 January 2016 doi: 10.3389/fevo.2015.00155 Linking Movement Ecology with Wildlife Management and Conservation Andrew M. Allen* and Navinder J. Singh Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, Sweden A common challenge in species conservation and management is how to incorporate species movements into management objectives. There often is a lack of knowledge of where, when, and why species move. The field of movement ecology has grown rapidly in the last decade and is now providing the knowledge needed to incorporate movements of species into management planning. This knowledge can also be used to develop management strategies that are flexible in time and space and may improve the effectiveness of management actions. Therefore, wildlife management and conservation may benefit by strengthening the link with movement ecology. We present a framework that illustrates how animal movement can be used to enhance conservation planning and identify management actions that are complementary to existing strategies. The framework contains five steps that identify (1) the movement attributes of a species, (2) their impacts on ecosystems, (3) how this knowledge can be used to guide the scale and type of management, (4) the implementation, and (5) the evaluation of management Edited by: actions. We discuss these five steps in detail, highlighting why the step is important Matt W. Hayward, Bangor University, UK and how the information can be obtained. We illustrate the framework through a Reviewed by: case study of managing a highly mobile species, the Atlantic salmon (Salmo salar), a Robert A. Montgomery, harvested species of conservation concern. We believe that the movement-management Michigan State University, USA Johannes Signer, framework provides an important, and timely, link between movement ecology and University of Göttingen, Germany wildlife management and conservation, and highlights the potential for complementary, *Correspondence: dynamic solutions for managing wildlife. Andrew M. Allen andrew.allen@slu.se Keywords: adaptive management, animal movement, conservation, movement ecology, wildlife management Specialty section: This article was submitted to INTRODUCTION Conservation, a section of the journal The field of movement ecology has grown rapidly in the last decade due to a number of recent Frontiers in Ecology and Evolution technological and analytical advances in tracking animal movement (Tomkiewicz et al., 2010). Received: 08 October 2015 Alongside the growth in technological advances have been advances in conceptual frameworks Accepted: 22 December 2015 that aim to unify research in animal movement (Nathan et al., 2008) and incorporate movement Published: 12 January 2016 into biodiversity research (Jeltsch et al., 2013). This growth has provided a number of benefits for Citation: conservation and management, such as improving our understanding of habitats important for Allen AM and Singh NJ (2016) Linking wildlife and the area traversed by wide-ranging species (Hebblewhite and Haydon, 2010). However, Movement Ecology with Wildlife it has also highlighted a number of challenges for conservation, such as maintaining connectivity, Management and Conservation. both within the landscape and for species with wide-ranging movements like nomadic or migratory Front. Ecol. Evol. 3:155. doi: 10.3389/fevo.2015.00155 species (Sanderson et al., 2002; Martin et al., 2007; Runge et al., 2014). At the same time, studies have Frontiers in Ecology and Evolution | www.frontiersin.org 1 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management revealed that traditional approaches to conservation, such as (Figure 1). A fourth step considers the implementation of protected areas, may be inadequate due to reasons like the spatial management actions whilst the final step incorporates an scale of a species movements (e.g., Thirgood et al., 2004), conflicts adaptive management component of evaluation (Figure 1). with stakeholders (e.g., Symes et al., 2015), or available finances The primary requirement for the framework is the availability (e.g., Carwardine et al., 2008; Chadés et al., 2015). Traditional of animal movement data that is appropriate for the management approaches will continue to have a vital role in conservation objective(s). The movement data required will depend upon the planning, however their effectiveness may be improved if they ecological or conservation questions underlying the management are combined with strategies that are flexible in time and/or space objectives, and may involve considerations like whether the (Runge et al., 2014; Chadés et al., 2015; Tulloch et al., 2015). time period of observation is long enough to make general Research in movement ecology is generating knowledge of conclusions on movement patterns, or whether the sample size species movements that enables managers to implement actions is large enough to make population level inferences (Figure 1). that are flexible in space and time. As a result, managers In addition, quantitative methods for analysing movements have have begun to link the movement ecology of a species with progressed rapidly with time (Patterson et al., 2008; Kranstauber management planning, resulting in targeted management actions et al., 2012; Fleming et al., 2015). These methods have specific that incorporate species movements or specific areas where requirements regarding the quality of data needed, as few as 10 threats are located (Table 1). An example is how the results of locations per month may be sufficient to estimate a home range a tracking study for leatherback turtles (Dermochelys coriacea) but this would not be sufficient for understanding resource use were used to identify new potential conservation strategies to (Marzluff et al., 2004; Börger et al., 2006). However, it should reduce leatherback-fisheries interactions that included targeted be noted that detailed movement data is not always available. spatial actions and dynamic time-area closures along the Instead, informed decisions can be made based on predictive migration corridor (Table 1; Shillinger et al., 2008). Knowledge of modeling that are performed in conjunction with alternative species movements is also being used to prioritize management sources of data, such as expert opinion or presence data (Low actions and achieve maximum benefit from the limited funds Choy et al., 2009; Iwamura et al., 2014). These data sources may available (Martin et al., 2007; Carwardine et al., 2008, 2012). guide initial decision making processes whilst more detailed data An example is focusing management actions on bottleneck sites, are acquired (Grantham et al., 2009), and may also benefit study which are particular areas that species rely upon like stopover design by identifying existing knowledge gaps. Collecting new sites (Iwamura et al., 2014), or where landscape connectivity is movement data may be limited by the study species, available being constrained by physical barriers (Table 1; Sawyer et al., time, or money. Nevertheless, the improved knowledge that 2013; Seidler et al., 2015). These studies highlight the potential for movement data provides may lead to more effective management linking management planning with movement ecology. However, actions as opposed to costly mistakes (Carwardine et al., 2008; the examples are few and greater emphasis is needed to link the Grantham et al., 2009). fields of movement ecology and conservation if we are to improve upon the existing model. Movement Attributes We formulated a conceptual Movement-management The target for managers is to develop an understanding of how framework (hereon described as framework) to illustrate how individual movements affect a species survival and reproduction knowledge of animal movement may enhance management and therefore population dynamics. An individual’s decision planning. The workflow described in the framework is applicable to move is influenced by several factors that include food across taxa, as many species exhibit movements that vary resource availability and/or quality, predator avoidance and from being sedentary year round, to migration, nomadism, environmental conditions, which will enhance its capacity to and dispersal (Table 1). Furthermore, these movements share survive and reproduce (Morales et al., 2010; van Moorter et al., common attributes across taxa, such as the use of pathways, 2013). Movement attributes, like the timing of spring migration, stopover sites, seasonal ranges, or breeding sites. We outline the may have direct effects on the fitness of individuals (Winkler steps used in the framework, their rationale and highlight some et al., 2014). A number of bird species have not advanced the aspects that require important considerations. We discuss its timing of their spring migrations in response to climate change, implementation, how it links to existing practices and identify and appear to be declining because the timing of breeding has potential challenges for its implementation. Through a case study become mismatched with peak food availability (Møller et al., of the Atlantic salmon (Salmo salar), we show how knowledge 2008). Furthermore, the performance of a population may also be of movement has been used and can be used further to guide influenced by the ability of individuals to adapt their movements management planning. to environmental change, such as adapting foraging movements to habitat loss (McNamara et al., 2011; Winkler et al., 2014). Applying the first step of the framework allows managers MOVEMENT-MANAGEMENT FRAMEWORK to identify how animal movements influence demography and The framework is organized into five interlinked steps, whereby subsequent population dynamics (Figure 1). Animal movement baseline information on species movements are used to guide can be described according to three major population-level management decisions (Figure 1). The first three steps include distribution strategies that include being sedentary in annual understanding species’ movements, their ecosystem impacts and ranges, migration and nomadism (Mueller and Fagan, 2008). how these are linked to the scale of management required Being sedentary on an annual scale involves having stable home Frontiers in Ecology and Evolution | www.frontiersin.org 2 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management TABLE 1 | Links between movement ecology and wildlife management. Taxa Movement attributes Ecosystem impacts Scale of management Source BIRDS New World land birds Migratory Scale and Timing Services (pest predation) Ecological Networks Martin et al., 2007; Kellermann et al., (stopover, summer/winter) 2008; Faaborg et al., 2010 Waterfowl Migratory Timing Seed Dispersal; Temporary wetlands Kerbes et al., 1990; Figuerola and Aggregative impacts, Ecological networks, Green, 2002; O’Neal et al., 2008; Disease transmission Altizer et al., 2011 Greater sage-grouse Sedentary/Migratory Scale, Trophic level (umbrella Localized Actions Rowland et al., 2006; Dzialak et al., (Centrocercus Timing, and Drivers species), Nutrient 2011; Fedy et al., 2012 urophasianus) transfer MAMMALS Woodland/Mountain Migratory Scale, Timing, Nutrient Transfer; Direct Ecological Network Ferguson and Elkie, 2004; Johnson Caribou (Rangifer tarandus and Drivers use; Ecosystem Temporary et al., 2004; Saher and Schmieglow, caribou) Indicator 2004; Pinard et al., 2012 Saiga (Saiga tatarica) Migratory Scale and Timing Nutrient Transfer; Temporary (Proposed) Milner-Gulland, 1997; Singh and Potential for Direct use Threat management Milner-Gulland, 2011; Bull et al., 2013 Wildebeest (Connochaetes Sedentary/Migratory Scale Nutrient Transfer; Direct Localized Actions (PA) Thirgood et al., 2004; Holdo et al., 2010 taurinus) and Drivers use Mule deer (Odocoileus Migratory Scale, Timing, Nutrient cycling; Direct Ecological Networks Myers et al., 2004; Monteith et al., hemionus) and Drivers Use; Seed Dispersal (Connectivity) 2011; Sawyer and Kauffman, 2011 Mongolian gazelle (Procapra Nomadic Scale and Drivers Nutrient Transfer Temporary Mueller et al., 2008; Sawyer et al., 2013 gutturosa) FISH Near-shore species Sedentary Scale Regulatory services, Ecological Network, Size Holmlund and Hammer, 1999; Moffitt nutrient transfer, trophic of reserve et al., 2009; Gaines et al., 2010 level Bluefin tuna (Thunnus spp.) Migratory Scale, Timing, Trophic level, nutrient Temporary Armsworth et al., 2010 and Drivers transfer INSECTS Monarch butterfly (Danaus Migratory Scale and Drivers Services (Cultural, Ecological network Barkin, 2003; Howard and Davis, 2009; plexippus) pollination). Ecotourism (connectivity of wintering López-Hoffman et al., 2010; Brower and breeding sites, et al., 2012 pathway) Dragonfly spp. Migratory Drivers Trophic Level Ecological Network, Wikelski et al., 2006; Hobson et al., Temporary 2012 REPTILES Leatherback Sea Turtle Migratory Scale, Timing, Trophic Level Temporary Threat Sherrill-Mix et al., 2008; Shillinger et al., (Dermochelys coriacea) and Drivers management 2008; Fossette et al., 2010 Examples from the literature where aspects of the movement-management framework have been applied. The species in focus are from varying taxonomic groups that include mediums of travel on the ground, in air and water. The movement attributes were summarized into the type of movement (sedentary, migratory, nomadic) and what is known about the species’ movements, namely “Scale”—distance of movements and knowledge of space use, “Timing”—when movements occur or “Drivers”—factors influencing movement like habitat, cues or predators. Ecosystem Impacts describe both the services a species may provide and the potential impacts of their movements. The scale of management indicates the current or recommended management actions—the term “Temporary” refers to any temporary form of management such as time-area closures. The studies listed in source are referenced in Appendix A. ranges or territories, where an individual occupies a relatively actions needed, such as preserving connectivity for dispersing small area compared to the population distribution (Mueller and nomadic movements, setting aside reserves for species which and Fagan, 2008). Migration consists of seasonal, round-trip are sedentary in their annual home ranges or adopting a flyway movements between spatially disjunct areas (Mueller and Fagan, approach for conserving migratory species (Klaassen et al., 2008; 2008; Harris et al., 2009). Nomadism differs from being sedentary Howard and Davis, 2009; Minor and Lookingbill, 2010; Hodgson or migratory as individuals move across the landscape using et al., 2011). Previous research has shown that management routes that do not repeat across years (Mueller and Fagan, 2008). interventions have been less effective when management actions A fourth movement type that managers need to consider is have not matched the spatial, or temporal, scale of species dispersal. Dispersal is the movement to a site of reproduction movements (Thirgood et al., 2004; Moffitt et al., 2009). and includes movements away from the site of birth (natal In addition to the types of movement present in the dispersal) and movements between successive reproductive sites population, it is important to understand the characteristics of (breeding dispersal; Matthysen, 2012). The types of movements movements. These comprise of movement pathways, distance present in the population will influence the type of management and timing of movements, shapes and sizes of home ranges, Frontiers in Ecology and Evolution | www.frontiersin.org 3 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management FIGURE 1 | Movement-management framework. Movement-Management framework that provides a workflow for incorporating movement ecology into decision-making processes. Before applying the framework, one must consider the quality of the movement data and whether it is appropriate for achieving the management goal. This includes questions like resolution, sample size, and the type of methods that will be used. Data may also be available from alternative sources, such as expert opinion or presence data, which can be combined with predictive modeling. Once appropriate movement data is available, the first step of the framework concerns understanding the movement attributes occurring in a study population or system. This includes the movement types that exist in a population that include “migration,” “dispersal,” “sedentary,” and “nomadism.” It is important to understand the characteristics of these movements, for example, movement pathways, home ranging patterns, or the timing of movements. The second step is to determine the ecosystem impacts and services resulting from movements. The knowledge gained from the first two steps guides the decision making process and identifies potential management actions that complement existing management plans. These may include actions that are flexible in space and time, such as time-area closures, which require detailed knowledge of species movements. The fourth step considers the implementation of the proposed actions, including considerations like available knowledge, cost, stakeholder interests and how these influence the effectiveness and feasibility of proposed actions. The final step evaluates the effectiveness of management actions, thereby creating an adaptive management cyclical process whereby the outcomes of the evaluation guide management objectives and future actions. habitat selection along movement paths and the use of subsequent habitat suitability (Chetkiewicz and Boyce, 2009; stopover sites by migratory species (Figure 1). Understanding Lu et al., 2012). Knowledge of movement characteristics may the type of movement in the population determines the also identify potential threats, such as the increased risk of types of management actions needed, but understanding exploitation due to the predictable and aggregating nature of the characteristics of movements is necessary for planning, some migratory species (Bolger et al., 2007; Harris et al., 2009). designing, and implementing management actions. For example, We expand upon how knowledge of the types and characteristics understanding movement pathways is particularly important of species movements can be used to guide the scale of when managers aim to maintain connectivity, particularly as management in Section Scale of Management. the loss of some sites can lead to sudden population decline (Webster et al., 2002; Iwamura et al., 2013). Movement pathways Ecosystem Impacts also indicate whether species use matrix habitats (Fischer et al., Animal movement is a core component of an ecosystem and 2005), are restricted to specific habitat types (Hagen et al., maintaining movement patterns may be vital for sustaining 2012), or barriers prevent movements (Sawyer et al., 2013). ecosystem processes like trophic and species interactions Other movement characteristics, such as the size and shape of (Lundberg and Moberg, 2003; Massol et al., 2011). Movement home ranges, are often used to guide the scale of management provides links between ecosystems and these links may be (Schwartz, 1999) and to determine habitat preference and classified as either resource, genetic or process links (reviewed Frontiers in Ecology and Evolution | www.frontiersin.org 4 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management in Jeltsch et al., 2013). The frequency and type of link will be influencing species movements (e.g., Hornseth and Rempel, be affected by the spatiotemporal scale of movement, such 2015). However, an ongoing challenge in conservation is how as foraging movements within the home range or the less to achieve the scale of management required. Knowing species frequent but larger scale movements of migration (Jeltsch et al., movements answers important management questions like 2013). Movement is also important for maintaining interaction where, when, how and why animals move, which can be used networks in both antagonist (e.g., predator-prey) and mutualist to develop management actions that increase the dynamism (e.g., plant-pollinator) networks (Tylianakis et al., 2010; Hagen and scale of wildlife management, and are complementary to et al., 2012). The loss of species interaction networks may existing plans. Alternative management actions may include have cascading effects on for example food web dynamics ecological networks, time-area closures or threat management, resulting in secondary extinctions (Hagen et al., 2012). Managers and we expand upon these alternative management actions also need to consider how movement may disturb ecosystems. below. The aggregating nature, and long-range movements, of many The first approach is concerned with incorporating localized migratory species may impact ecosystems through exploitation of management actions, such as protected areas or reserves, into a habitats, disease transmission and nutrient loading (Kerbes et al., network of areas and thus increasing the scale of management. 1990; Post et al., 2008). Ecological networks should maintain ecosystem processes, which Animal movement may provide important ecosystem services includes the movement of organisms and subsequent species and these services have been termed mobile-agent based interactions networks (Opdam et al., 2006; Hagen et al., 2012). ecosystem services (MABES; Kremen et al., 2007). These services Ecological networks also incorporate multiple objectives into the are provided at a local scale by species moving within or among spatial planning process, such as conservation goals and different habitats (Kremen et al., 2007). For example, the movements land uses by stakeholders (Opdam et al., 2006). A principal of bees pollinate both wild and agricultural plants (Kremen concept of ecological networks is connectivity, whereby a set of et al., 2007), seeds may be dispersed long distances by birds areas or ecosystems are linked to maintain or enhance population and mammals (Nathan and Muller-landau, 2000) and nutrients viability by facilitating movement (Beier, 1998; Opdam et al., are transferred between marine and terrestrial environments by 2006). Management tools used to improve connectivity of two or the foraging movements of seabirds (Ellis et al., 2006). The more areas are matrix management and corridors (Beier, 1998; ongoing modification of the landscape by humans is altering Fischer et al., 2005). Identifying which habitats are important for landscape connectivity and threatens the future provision of species helps managers create a “soft,” more permeable matrix. MABES (Mitchell et al., 2013). Linking animal movement with For example, a matrix containing scattered trees facilitated management planning allows managers to identify the ecosystem the movement of birds in Australia (Fischer et al., 2005). functions and services that movement provides and thus improve Habitat patches may also act as important stepping stones landscape management (Jeltsch et al., 2013; Mitchell et al., 2013). for long-distance dispersal and range expansions, following climate-driven shifts in habitat suitability (Saura et al., 2014). Scale of Management Strengthening the link between corridor design and species A challenge for management is identifying the scale of movements improves connectivity in the landscape, for instance, management required for effective species conservation. The corridors that were identified through tracking studies were more scale of management may be guided by, amongst others, effective than those identified through modeling approaches the distance of movements like migrations (Klaassen et al., (LaPoint et al., 2013). Corridors may be beneficial for species 2008), by the size of home ranges (Schwartz, 1999), or by moving at larger scales like the Mule deer Odocoileus hemionus the habitat requirements of a species (Angelstam et al., 2004). R., for maintaining connectivity within a species home range, and Habitat selection studies have commonly been used to identify to preserve dispersal events and maintain functional connectivity the habitat requirements of a species, in particular using the (Table 1; Baguette and Van Dyck, 2007; LaPoint et al., 2013; four orders of habitat selection described by Johnson (1980). Sawyer et al., 2013). The first-order of selection identifies the geographical range The second approach is the use of time-area closures. Time- of the species and has commonly been used to map species area closures may be dynamic in time only, i.e., excluding distributions and develop habitat suitability models, which are unwanted practices during a specific time of year, such as a used to guide the scale of conservation planning (Johnson, stopover site for migratory waterfowl (O’Neal et al., 2008). Time- 1980; Angelstam et al., 2004; Guisan et al., 2013). The second, area closures may also be dynamic in space and time, i.e., third and fourth orders of selection concern the selection of the closure tracks the species’ movements like the movements the home range, habitat patches within the home range and of pelagic species (Hobday and Hartmann, 2006). Time-area microhabitats within used patches respectively (Johnson, 1980; closures provide a viable alternative for managing species’ with Meyer and Thuiller, 2006). Meyer and Thuiller (2006) introduce predictable movements. They can be implemented when species a fifth order of selection, which are areas used by populations are most vulnerable, such as aggregation or spawning areas and within the geographical range. These orders of selection inform during critical movement phases (Table 1; Hunter et al., 2006; managers about local reserve site selection (Aldridge and Boyce, Shillinger et al., 2008; Bull et al., 2013). Time-area closures 2007; Guisan et al., 2013), provide indications of habitat may also achieve conservation targets whilst incorporating quality and improvements needed (e.g., Dickson and Beier, stakeholder interests, for example by maintaining alternative 2002; Zeale et al., 2012) and how human disturbance may land-use or harvesting practices, and are being increasingly Frontiers in Ecology and Evolution | www.frontiersin.org 5 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management utilized in marine and freshwater ecosystems (Hobday and A number of approaches have been developed to identify Hartmann, 2006; O’Neal et al., 2008; Shillinger et al., 2008). which management actions will maximize benefits, such as When it is not possible to spatially delineate large areas, it decision theoretic approaches and systematic conservation may be more appropriate to manage the primary threats to a planning (e.g., Margules and Pressey, 2000; Wilson et al., 2009). species instead (Carwardine et al., 2012). Understanding a species Decision theoretic approaches consist of an objective or desired threats enables managers to prioritize management actions that outcome, a description of our knowledge of the system, state achieve the greatest impact (Auerbach et al., 2014; Tulloch variables in the area of interest, such as species populations or et al., 2015). Identifying threats to a species may also indicate habitats, control variables which represent possible management which movement attributes increase species vulnerability. Traits strategies, model constraints and an equation that describes the of some species, such as the predictability of routes, timing of relationship between the benefit of actions and the potential movements, or reliance upon particular sites may increase the management strategies in the area of interest (Wilson et al., 2009). risk of exploitation (Bolger et al., 2007). This knowledge can Understanding species movements enables managers to improve be used to guide management decisions, for instance threat their understanding of the threats, use their knowledge of where management actions may involve time-specific interventions like and when a species will be to identify alternative management anti-poaching activities at important locations and times of the actions, and also recognize the challenges of achieving the year (Berger et al., 2008; Murgui, 2014). Recent advances in management objectives which may not be apparent if a species’ tracking technologies also provide the opportunity to incorporate movements are unknown. Decision theoretic approaches enable real-time monitoring data into threat management schemes, thus managers to prioritize management actions that will better justifying the cost of tracking animal movements (Wall et al., achieve the management objectives (Tulloch et al., 2015). 2014). Real-time tracking data from African elephants Loxodonta Previously, actions were prioritized on areas with the highest africana in Kenya was used to notify wildlife managers when threats or species richness, but now the management actions elephants were about to move into community areas (Wall et al., themselves are being prioritized depending upon whether they 2014). Wildlife managers were able to intervene and prevent are cost-effective, have the greatest impact and are achievable the elephants causing crop damage and reduce human-wildlife (Auerbach et al., 2014; Tulloch et al., 2015). Multiple-action conflicts, a major threat to elephants in Africa (Wall et al., 2014). prioritization schemes are also being considered, whereby a combined set of strategies may be more cost effective and have greater impact than any one strategy alone (Wilson et al., 2009; Implementation Chadés et al., 2015). Therefore, it is vital for managers to evaluate The feasibility of management actions described above may all possible management scenarios to improve the effectiveness of be limited at the implementation phase by considerations like the decision-making process. costs, stakeholder interests, and enforcement. Incorporating animal movement into management planning may entail a Evaluation number of costs, such as the costs of acquiring land and the The importance of evaluating management actions has costs associated with establishing and maintaining a network been highlighted in recent decades to avoid implementing of managed areas (Naidoo et al., 2006). Emphasis is now management actions that do not achieve management goals being placed on identifying the most cost effective action that and thus waste limited funds (e.g., Ferraro and Pattanayak, maximizes benefits (Naidoo et al., 2006; Carwardine et al., 2006; Walsh et al., 2012). Therefore, management strategy 2012; Auerbach et al., 2014). The interests of local stakeholders evaluation (MSE) is vital for determining whether actions may also influence the implementation of management actions have either succeeded or failed in achieving the management due to conflicts between involved parties, for example conflicts objective, and using this knowledge to inform future decisions arising over land-use, resettlement, policies or legislation, and and actions (Pullin et al., 2013). Evaluation is an integral part human-wildlife conflicts (Davies et al., 2013; Symes et al., 2015). of adaptive management and is thus applicable to any form of In addition, limitations may arise due to available manpower, wildlife management. With regards to our framework, evaluation either in relation to monitoring the outcomes of management may be important for determining the effectiveness of actions actions or enforcing them (Keane et al., 2008). These challenges implemented with incomplete knowledge of species movements, are especially pertinent when a species movements takes them and may help prioritize the type of knowledge needed to improve across several country borders (Iwamura et al., 2014; Kark future management. Evaluation is also important for tracking et al., 2015). Cross-boundary collaborations may provide a future uncertainties, such as how variation in the timing of number of benefits, such as improving the cost effectiveness movement may affect management strategies like time-area of management actions and increasing the scale of threat closures, which rely upon knowledge of where and when a management, however it also presents a number of challenges species will be. like political instability, increased costs related to establishing The effectiveness of management actions can be simulated the collaboration, conflicting national goals, and potential delays prior to their implementation, through frameworks like the MSE in implementing actions (Kark et al., 2009, 2015). However, framework (Smith et al., 1999), which has thus far been used incorporating the above challenges into the decision making mostly in commercial fisheries but also has relevance for the process allows managers to identify management strategies that management and conservation of terrestrial species (Bunnefeld are implementable and attainable. et al., 2011; Milner-Gulland, 2011). MSE compares multiple Frontiers in Ecology and Evolution | www.frontiersin.org 6 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management management strategies prior to their implementation, allowing to nearby tributaries (McCormick et al., 1998). After 1 to managers to identify their effectiveness and understand the 5 years the salmon migrates downstream to enter the sea varying forms of uncertainty, such as incomplete knowledge of (Lundqvist, 1983; Otero et al., 2014). Salmon movements in the species movements (Bunnefeld et al., 2011). The outcomes of sea remain difficult to study but this phase can be described as MSE are used to inform the management objectives, study design, nomadic where the distribution of salmon is largely influenced and implementation of management actions (Bunnefeld et al., by environmental factors like sea temperature, surface currents, 2011; Milner-Gulland, 2011). For example, comparative analyses and food availability (Klemetsen et al., 2003; Trudel et al., 2011). could be performed to determine whether management actions Salmon from multiple river systems mix in the Main Basin of should be implemented with limited knowledge of movement the Baltic Sea, leading to mixed-stock fisheries (Karlsson and or whether priority should instead be placed on acquiring data Karlstrårn, 1994). Salmon normally migrate back to their natal that can be used to develop management actions that are more river systems to spawn (Lundqvist, 1983). The movements of tailored to species movements and consequently have greater hatchery-reared salmon may differ from wild salmon in their impact, such as those developed for the leatherback turtle extent, timing, and fidelity (McKinnell et al., 1994; Jutila et al., discussed earlier (Shillinger et al., 2008). 2003). Step 2—Ecosystem Impacts APPLYING THE The stage-structured life cycle of salmon means that juveniles MOVEMENT-MANAGEMENT FRAMEWORK and adults occupy and connect different ecosystems (Schreiber and Rudolf, 2008; Miller and Rudolf, 2011). Species with complex We illustrate the potential for linking movement ecology with life cycles may cause abrupt changes in different ecosystems, management through a case study of the Atlantic salmon. By such as how changes in juvenile abundance may lead to trophic following the steps of the framework, we show how existing cascades across ecosystems to the adult habitat (Knight et al., knowledge of salmon movement ecology has been used to 2005; Schreiber and Rudolf, 2008). The salmon’s life cycle develop management actions and how further knowledge could influences food web dynamics by preying on aquatic species be used to identify alternative management actions. and being preyed upon by aquatic, terrestrial, and avian species (Holmlund and Hammer, 1999, 2004). The Atlantic salmon Case Study—Managing Atlantic Salmon is iteroparous, meaning it can spawn repeatedly as opposed to dying after spawning like the semelparous Pacific salmon (Salmo salar) in the Baltic Sea (Oncorhynchus spp.; Klemetsen et al., 2003). Salmon deaths, and Background repeated migrations, link ecosystems and transfer nutrients and Atlantic salmon have had large population declines in the Baltic carbon between marine and freshwater ecosystems (Holmlund Sea (Karlsson and Karlstrårn, 1994; Klemetsen et al., 2003) so it and Hammer, 1999, 2004). Salmon provide several ecosystem is an important issue for management and conservation alike. services. Spawning salmon regulate sediment processes whilst Overfishing and the loss of connectivity in river systems, due to their movements between marine and freshwater ecosystems hydroelectric dams, has been a driving cause of salmon declines support aquatic/terrestrial food webs and nutrient cycling and in the 1990s only 12 of the 44 naturally reproducing salmon (Bottom et al., 2009; Kulmala et al., 2012). Salmon populations stocks in the Gulf of Bothnia remained (Karlsson and Karlstrårn, provide a highly valued food source for both commercial, 1994). A number of actions have been taken to restore these personal-use, and recreational fisheries (Kulmala et al., 2012). populations but several rivers are not self-sustaining and many salmon rivers are below 50% of potential smolt production (ICES, Step 3—Scale of Management 2012). In this case study, we focus on the management goals The life cycle of the salmon illustrates the importance of of the Swedish government, through the Swedish Agency for understanding their movements due to the direct influence that Marine and Water Management (SwAM). Their aim is to reverse salmon movement has on their survival and reproduction. As a the decline of salmon stocks whilst maintaining activities like consequence, the scale of management may vary in accordance recreational and commercial fishing. Multiple techniques have to the specific life cycle stage and process that is being targeted been used to monitor the movements of salmon that include by management. For instance, management may consider the observational and trapping data (Lundqvist et al., 2010), tagging implementation of more localized management actions during methods (Payne et al., 2010), acoustic or radio telemetry (Serrano the sedentary phases of the salmon’s life cycle. These include the et al., 2009), stable isotopes, and genetics (Barnett-Johnson et al., development phase after hatching salmon and spawning phase 2008). Therefore, several sources of movement data are available of adults. Management actions have therefore focused on either to continue with the movement-management framework. preserving existing habitats used by salmon, or alternatively, Step 1—Movement Attributes restoration actions have been taken to improve habitat suitability Salmon can exhibit all four types of movement (sedentary, for spawning and recently hatched salmon (Nilsson et al., 2005). dispersal, nomadism, and migration) during its life cycle. A key aspect of salmon movements is the migration from Salmon hatch in freshwater rivers, where they are solitary and the natal/spawning areas to the sea and their return to rivers. defend territories for food, thus exhibiting sedentary movements Lundqvist et al. (2008) indicate that a salmon population (Lundqvist, 1983). During this phase they may also disperse could increase by 500% if connectivity was improved along Frontiers in Ecology and Evolution | www.frontiersin.org 7 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management the migration path. The severe implications resulting from loss life cycle, the nomadic movements of adults need transboundary of connectivity has resulted in several management actions collaborations for effective management. The Main Basin of that target connectivity between river systems and the sea the Baltic Sea is an offshore fishery that is exploited by (McKinnell et al., 1994; Lundqvist et al., 2008; Serrano et al., many countries in the region. Therefore, international measures 2009). Knowledge of migration timing has enabled managers are needed to effectively manage the mixed-stock fishery and to adopt actions that are flexible in time, which may increase knowledge of movements and genetics is vital to achieve this their acceptance by impacted stakeholders like the hydroelectric goal. Harvest quotas are provided by the Common Fisheries power industry. These have included diverting water from Policy but the Atlantic salmon would benefit further from the re- hydroelectric dams to a bypass during the migratory period only, establishment of an International Baltic Treaty. Transboundary or transporting salmon 88 km upstream in trucks from the first collaborations provide a number of challenges that influence barrier to the spawning grounds (Lundqvist et al., 2008; Serrano the implementation potential of management actions (Kark et al., 2009; Hagelin et al., 2015). et al., 2015). These may include increased financial costs, Meanwhile, a key aim should be to reduce the amount of delayed conservation planning or countries “free-riding” on the fishing effort in the Main Basin, due to stock mixing, which assumption that management actions will be implemented by includes threatened stocks. Instead, fishing efforts could be other countries (Kark et al., 2009, 2015). However, transboundary focused in coastal areas or river estuaries where the stock status collaborations may also improve the cost effectiveness of is known. Understanding the movements of hatchery-reared management and increase the scale of management to more salmon may also identify alternative management actions for effectively manage a highly mobile species (Kark et al., 2015). implementation. Research indicates that hatchery-reared salmon are more likely to be caught in the Bothnian Sea compared Step 5—Evaluation to wild stocks because hatchery-reared salmon are less likely Mathematical and statistical models have been developed that to migrate to the Main Basin of the Baltic Sea (Jutila et al., link biological and economic data to identify management 2003). Hatchery-reared salmon may also arrive in the northern actions for salmon in the Baltic (Kulmala et al., 2008). Kulmala Baltic later than wild salmon stocks (McKinnell et al., 1994). et al. (2008) explicitly incorporate the migratory movements of This knowledge may be used to implement a time-area based salmon to determine optimal harvest solutions, and identify that approach, providing a potentially viable management option driftnet fisheries should be excluded as a harvest method. Several that maintains recreational and commercial harvesting whilst studies have also evaluated the effectiveness of management simultaneously increasing the harvest of hatchery-reared salmon. plans prior to their implementation, which include both national plans and international plans (Haapasaari and Karjalainen, 2010; Step 4—Implementation Levontin et al., 2011). Bayesian network analyses have been used The management of salmon influences a number of stakeholders to incorporate several sources of data that include the biology of like commercial fisheries, the power industry, general public, the species, expert knowledge, and sociological data to evaluate and conservation community. Understanding the movement alternative management options (Haapasaari and Karjalainen, ecology of salmon has enabled managers to identify actions 2010; Levontin et al., 2011). These studies have determined the that have a higher likelihood of acceptance by stakeholders and commitment of stakeholders to management options and how thus improved effectiveness. An example includes the time- this may influence the effectiveness of proposed management area based approach for fisheries, whereby the coastal fishery actions (Haapasaari and Karjalainen, 2010; Levontin et al., is opened later in the season meaning that most wild salmon 2011). have already entered the river system and the fisheries harvest With regards to movement, management interventions like is dominated by hatchery-reared salmon (ICES, 2012). Such fish ladders may not guarantee connectivity, as illustrated by an approach maintains the livelihoods of fisherman whilst Lundqvist et al. (2008). The project evaluation found that reducing harvest pressure on wild salmon and thus achieving salmon migrating upstream were not drawn to the bypass conservation targets. Another example is how the knowledge containing the fish ladder, due to differing discharge rates of timing of salmon migrations enables hydroelectric dams to from the hydroelectric dam and the bypass. Salmon survival regulate discharge rates, which target conservation goals during was also reduced the following spring as salmon were not the salmon migration and electricity production at other times drawn to the fish ladder during the seawards migration, but of the year (Lundqvist et al., 2008; Håkansson, 2009). Achieving traveled through the turbines instead. Improved knowledge of management targets increasingly relies upon identifying trade- the movement ecology of salmon, such as how they move offs that are acceptable to all stakeholders (Redpath et al., 2013). in the river and what cues they are drawn to are needed to By linking movement ecology with management, alternative improve the designs of existing and future connectivity measures management actions can be identified that allow managers to (Lundqvist et al., 2008). In addition, management actions are explore trade-off scenarios with stakeholders, which increase the not being implemented for the full movement cycle. In the implementation potential of proposed management actions. example of transporting salmon upstream by truck, no actions Several management actions for salmon are executed within are being taken for the downstream migration of salmon, national boundaries, such as maintaining connectivity in resulting in very low survival rates (Bergman et al., 2014; Hagelin freshwater systems, improving breeding habitats, and managing et al., 2015). The recovery of this river’s stock is therefore coastal fisheries. However, during the marine phase of the salmon limited by not considering the migratory connectivity of both Frontiers in Ecology and Evolution | www.frontiersin.org 8 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management upstream and downstream migrations. In this instance it would species will be is a pre-requisite for the successful implementation be important to evaluate both the effectiveness of translocating of time-area approaches, which allow managers to develop trade- individuals to spawning areas (Fischer and Lindenmayer, 2000), off scenarios that balance conservation needs with alternative land-use practices (O’Neal et al., 2008; Shillinger et al., 2008; and subsequently whether the action is meeting management Game et al., 2009; Redpath et al., 2013). objectives of population recovery. We have highlighted how knowledge gained from movement ecology can be used to identify alternative, complementary MANAGEMENT IMPLICATIONS strategies in wildlife management. Our conceptual framework provides a step by step workflow that aims to understand the Studies continue to highlight that management actions focused movement patterns of a species and use this knowledge to guide in one area, such as protected areas, are not sufficient for management actions. As the field of movement ecology continues effectively conserving a species (Thirgood et al., 2004; Martin to grow, it is important to strengthen the link with wildlife et al., 2007; Runge et al., 2014). Shortfalls include the scale management to further improve the decision-making capabilities of management, conflicts with stakeholders, alternative land- of practitioners and managers. uses and limited space available (Sanderson et al., 2002; Runge et al., 2014; Symes et al., 2015). Management actions focused in one area also fail to account for species movements (Thirgood AUTHOR CONTRIBUTIONS et al., 2004; Runge et al., 2014). Linking movement ecology to conservation has several implications for the future management AA and NS conceived the idea. AA wrote the majority of the of wildlife. Understanding a species movements enable managers manuscript with input from NS to implement actions along the entire movement path, such as a flyway approach for birds and butterflies (Klaassen et al., FUNDING 2008; Howard and Davis, 2009) or dynamic protected areas in the ocean (Shillinger et al., 2008; Game et al., 2009) and The study was funded by the thematic programme in Wildlife and on land (Singh and Milner-Gulland, 2011; Bull et al., 2013). Forestry at the Swedish University of Agricultural Sciences, the Understanding movement also enables managers to identify Swedish Environmental Protection Agency (Naturvårdsverket, threats, such as the loss of important sites (Iwamura et al., 2013) 802-0102-11) and their committee for Wildlife Research, the or barriers to movement (Seidler et al., 2015), and therefore Swedish Association for Hunting Wildlife Management. prioritize the most effective management actions that have the highest chance of success (Game et al., 2013; Auerbach et al., 2014; Tulloch et al., 2015). Knowledge of species movements ACKNOWLEDGMENTS allows managers to identify alternative management actions We thank Ascelin Gordon, Anouschka Hof, Göran Spong, and that are flexible in space and time, such as time-area based Nils Bunnefeld, and the two reviewers, Robert A. 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No use, distribution or 10.1111/j.1469-1795.2012.00537.x reproduction is permitted which does not comply with these terms. Frontiers in Ecology and Evolution | www.frontiersin.org 13 January 2016 | Volume 3 | Article 155 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Frontiers in Ecology and Evolution Unpaywall

Linking Movement Ecology with Wildlife Management and Conservation

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REVIEW published: 12 January 2016 doi: 10.3389/fevo.2015.00155 Linking Movement Ecology with Wildlife Management and Conservation Andrew M. Allen* and Navinder J. Singh Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, Sweden A common challenge in species conservation and management is how to incorporate species movements into management objectives. There often is a lack of knowledge of where, when, and why species move. The field of movement ecology has grown rapidly in the last decade and is now providing the knowledge needed to incorporate movements of species into management planning. This knowledge can also be used to develop management strategies that are flexible in time and space and may improve the effectiveness of management actions. Therefore, wildlife management and conservation may benefit by strengthening the link with movement ecology. We present a framework that illustrates how animal movement can be used to enhance conservation planning and identify management actions that are complementary to existing strategies. The framework contains five steps that identify (1) the movement attributes of a species, (2) their impacts on ecosystems, (3) how this knowledge can be used to guide the scale and type of management, (4) the implementation, and (5) the evaluation of management Edited by: actions. We discuss these five steps in detail, highlighting why the step is important Matt W. Hayward, Bangor University, UK and how the information can be obtained. We illustrate the framework through a Reviewed by: case study of managing a highly mobile species, the Atlantic salmon (Salmo salar), a Robert A. Montgomery, harvested species of conservation concern. We believe that the movement-management Michigan State University, USA Johannes Signer, framework provides an important, and timely, link between movement ecology and University of Göttingen, Germany wildlife management and conservation, and highlights the potential for complementary, *Correspondence: dynamic solutions for managing wildlife. Andrew M. Allen andrew.allen@slu.se Keywords: adaptive management, animal movement, conservation, movement ecology, wildlife management Specialty section: This article was submitted to INTRODUCTION Conservation, a section of the journal The field of movement ecology has grown rapidly in the last decade due to a number of recent Frontiers in Ecology and Evolution technological and analytical advances in tracking animal movement (Tomkiewicz et al., 2010). Received: 08 October 2015 Alongside the growth in technological advances have been advances in conceptual frameworks Accepted: 22 December 2015 that aim to unify research in animal movement (Nathan et al., 2008) and incorporate movement Published: 12 January 2016 into biodiversity research (Jeltsch et al., 2013). This growth has provided a number of benefits for Citation: conservation and management, such as improving our understanding of habitats important for Allen AM and Singh NJ (2016) Linking wildlife and the area traversed by wide-ranging species (Hebblewhite and Haydon, 2010). However, Movement Ecology with Wildlife it has also highlighted a number of challenges for conservation, such as maintaining connectivity, Management and Conservation. both within the landscape and for species with wide-ranging movements like nomadic or migratory Front. Ecol. Evol. 3:155. doi: 10.3389/fevo.2015.00155 species (Sanderson et al., 2002; Martin et al., 2007; Runge et al., 2014). At the same time, studies have Frontiers in Ecology and Evolution | www.frontiersin.org 1 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management revealed that traditional approaches to conservation, such as (Figure 1). A fourth step considers the implementation of protected areas, may be inadequate due to reasons like the spatial management actions whilst the final step incorporates an scale of a species movements (e.g., Thirgood et al., 2004), conflicts adaptive management component of evaluation (Figure 1). with stakeholders (e.g., Symes et al., 2015), or available finances The primary requirement for the framework is the availability (e.g., Carwardine et al., 2008; Chadés et al., 2015). Traditional of animal movement data that is appropriate for the management approaches will continue to have a vital role in conservation objective(s). The movement data required will depend upon the planning, however their effectiveness may be improved if they ecological or conservation questions underlying the management are combined with strategies that are flexible in time and/or space objectives, and may involve considerations like whether the (Runge et al., 2014; Chadés et al., 2015; Tulloch et al., 2015). time period of observation is long enough to make general Research in movement ecology is generating knowledge of conclusions on movement patterns, or whether the sample size species movements that enables managers to implement actions is large enough to make population level inferences (Figure 1). that are flexible in space and time. As a result, managers In addition, quantitative methods for analysing movements have have begun to link the movement ecology of a species with progressed rapidly with time (Patterson et al., 2008; Kranstauber management planning, resulting in targeted management actions et al., 2012; Fleming et al., 2015). These methods have specific that incorporate species movements or specific areas where requirements regarding the quality of data needed, as few as 10 threats are located (Table 1). An example is how the results of locations per month may be sufficient to estimate a home range a tracking study for leatherback turtles (Dermochelys coriacea) but this would not be sufficient for understanding resource use were used to identify new potential conservation strategies to (Marzluff et al., 2004; Börger et al., 2006). However, it should reduce leatherback-fisheries interactions that included targeted be noted that detailed movement data is not always available. spatial actions and dynamic time-area closures along the Instead, informed decisions can be made based on predictive migration corridor (Table 1; Shillinger et al., 2008). Knowledge of modeling that are performed in conjunction with alternative species movements is also being used to prioritize management sources of data, such as expert opinion or presence data (Low actions and achieve maximum benefit from the limited funds Choy et al., 2009; Iwamura et al., 2014). These data sources may available (Martin et al., 2007; Carwardine et al., 2008, 2012). guide initial decision making processes whilst more detailed data An example is focusing management actions on bottleneck sites, are acquired (Grantham et al., 2009), and may also benefit study which are particular areas that species rely upon like stopover design by identifying existing knowledge gaps. Collecting new sites (Iwamura et al., 2014), or where landscape connectivity is movement data may be limited by the study species, available being constrained by physical barriers (Table 1; Sawyer et al., time, or money. Nevertheless, the improved knowledge that 2013; Seidler et al., 2015). These studies highlight the potential for movement data provides may lead to more effective management linking management planning with movement ecology. However, actions as opposed to costly mistakes (Carwardine et al., 2008; the examples are few and greater emphasis is needed to link the Grantham et al., 2009). fields of movement ecology and conservation if we are to improve upon the existing model. Movement Attributes We formulated a conceptual Movement-management The target for managers is to develop an understanding of how framework (hereon described as framework) to illustrate how individual movements affect a species survival and reproduction knowledge of animal movement may enhance management and therefore population dynamics. An individual’s decision planning. The workflow described in the framework is applicable to move is influenced by several factors that include food across taxa, as many species exhibit movements that vary resource availability and/or quality, predator avoidance and from being sedentary year round, to migration, nomadism, environmental conditions, which will enhance its capacity to and dispersal (Table 1). Furthermore, these movements share survive and reproduce (Morales et al., 2010; van Moorter et al., common attributes across taxa, such as the use of pathways, 2013). Movement attributes, like the timing of spring migration, stopover sites, seasonal ranges, or breeding sites. We outline the may have direct effects on the fitness of individuals (Winkler steps used in the framework, their rationale and highlight some et al., 2014). A number of bird species have not advanced the aspects that require important considerations. We discuss its timing of their spring migrations in response to climate change, implementation, how it links to existing practices and identify and appear to be declining because the timing of breeding has potential challenges for its implementation. Through a case study become mismatched with peak food availability (Møller et al., of the Atlantic salmon (Salmo salar), we show how knowledge 2008). Furthermore, the performance of a population may also be of movement has been used and can be used further to guide influenced by the ability of individuals to adapt their movements management planning. to environmental change, such as adapting foraging movements to habitat loss (McNamara et al., 2011; Winkler et al., 2014). Applying the first step of the framework allows managers MOVEMENT-MANAGEMENT FRAMEWORK to identify how animal movements influence demography and The framework is organized into five interlinked steps, whereby subsequent population dynamics (Figure 1). Animal movement baseline information on species movements are used to guide can be described according to three major population-level management decisions (Figure 1). The first three steps include distribution strategies that include being sedentary in annual understanding species’ movements, their ecosystem impacts and ranges, migration and nomadism (Mueller and Fagan, 2008). how these are linked to the scale of management required Being sedentary on an annual scale involves having stable home Frontiers in Ecology and Evolution | www.frontiersin.org 2 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management TABLE 1 | Links between movement ecology and wildlife management. Taxa Movement attributes Ecosystem impacts Scale of management Source BIRDS New World land birds Migratory Scale and Timing Services (pest predation) Ecological Networks Martin et al., 2007; Kellermann et al., (stopover, summer/winter) 2008; Faaborg et al., 2010 Waterfowl Migratory Timing Seed Dispersal; Temporary wetlands Kerbes et al., 1990; Figuerola and Aggregative impacts, Ecological networks, Green, 2002; O’Neal et al., 2008; Disease transmission Altizer et al., 2011 Greater sage-grouse Sedentary/Migratory Scale, Trophic level (umbrella Localized Actions Rowland et al., 2006; Dzialak et al., (Centrocercus Timing, and Drivers species), Nutrient 2011; Fedy et al., 2012 urophasianus) transfer MAMMALS Woodland/Mountain Migratory Scale, Timing, Nutrient Transfer; Direct Ecological Network Ferguson and Elkie, 2004; Johnson Caribou (Rangifer tarandus and Drivers use; Ecosystem Temporary et al., 2004; Saher and Schmieglow, caribou) Indicator 2004; Pinard et al., 2012 Saiga (Saiga tatarica) Migratory Scale and Timing Nutrient Transfer; Temporary (Proposed) Milner-Gulland, 1997; Singh and Potential for Direct use Threat management Milner-Gulland, 2011; Bull et al., 2013 Wildebeest (Connochaetes Sedentary/Migratory Scale Nutrient Transfer; Direct Localized Actions (PA) Thirgood et al., 2004; Holdo et al., 2010 taurinus) and Drivers use Mule deer (Odocoileus Migratory Scale, Timing, Nutrient cycling; Direct Ecological Networks Myers et al., 2004; Monteith et al., hemionus) and Drivers Use; Seed Dispersal (Connectivity) 2011; Sawyer and Kauffman, 2011 Mongolian gazelle (Procapra Nomadic Scale and Drivers Nutrient Transfer Temporary Mueller et al., 2008; Sawyer et al., 2013 gutturosa) FISH Near-shore species Sedentary Scale Regulatory services, Ecological Network, Size Holmlund and Hammer, 1999; Moffitt nutrient transfer, trophic of reserve et al., 2009; Gaines et al., 2010 level Bluefin tuna (Thunnus spp.) Migratory Scale, Timing, Trophic level, nutrient Temporary Armsworth et al., 2010 and Drivers transfer INSECTS Monarch butterfly (Danaus Migratory Scale and Drivers Services (Cultural, Ecological network Barkin, 2003; Howard and Davis, 2009; plexippus) pollination). Ecotourism (connectivity of wintering López-Hoffman et al., 2010; Brower and breeding sites, et al., 2012 pathway) Dragonfly spp. Migratory Drivers Trophic Level Ecological Network, Wikelski et al., 2006; Hobson et al., Temporary 2012 REPTILES Leatherback Sea Turtle Migratory Scale, Timing, Trophic Level Temporary Threat Sherrill-Mix et al., 2008; Shillinger et al., (Dermochelys coriacea) and Drivers management 2008; Fossette et al., 2010 Examples from the literature where aspects of the movement-management framework have been applied. The species in focus are from varying taxonomic groups that include mediums of travel on the ground, in air and water. The movement attributes were summarized into the type of movement (sedentary, migratory, nomadic) and what is known about the species’ movements, namely “Scale”—distance of movements and knowledge of space use, “Timing”—when movements occur or “Drivers”—factors influencing movement like habitat, cues or predators. Ecosystem Impacts describe both the services a species may provide and the potential impacts of their movements. The scale of management indicates the current or recommended management actions—the term “Temporary” refers to any temporary form of management such as time-area closures. The studies listed in source are referenced in Appendix A. ranges or territories, where an individual occupies a relatively actions needed, such as preserving connectivity for dispersing small area compared to the population distribution (Mueller and nomadic movements, setting aside reserves for species which and Fagan, 2008). Migration consists of seasonal, round-trip are sedentary in their annual home ranges or adopting a flyway movements between spatially disjunct areas (Mueller and Fagan, approach for conserving migratory species (Klaassen et al., 2008; 2008; Harris et al., 2009). Nomadism differs from being sedentary Howard and Davis, 2009; Minor and Lookingbill, 2010; Hodgson or migratory as individuals move across the landscape using et al., 2011). Previous research has shown that management routes that do not repeat across years (Mueller and Fagan, 2008). interventions have been less effective when management actions A fourth movement type that managers need to consider is have not matched the spatial, or temporal, scale of species dispersal. Dispersal is the movement to a site of reproduction movements (Thirgood et al., 2004; Moffitt et al., 2009). and includes movements away from the site of birth (natal In addition to the types of movement present in the dispersal) and movements between successive reproductive sites population, it is important to understand the characteristics of (breeding dispersal; Matthysen, 2012). The types of movements movements. These comprise of movement pathways, distance present in the population will influence the type of management and timing of movements, shapes and sizes of home ranges, Frontiers in Ecology and Evolution | www.frontiersin.org 3 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management FIGURE 1 | Movement-management framework. Movement-Management framework that provides a workflow for incorporating movement ecology into decision-making processes. Before applying the framework, one must consider the quality of the movement data and whether it is appropriate for achieving the management goal. This includes questions like resolution, sample size, and the type of methods that will be used. Data may also be available from alternative sources, such as expert opinion or presence data, which can be combined with predictive modeling. Once appropriate movement data is available, the first step of the framework concerns understanding the movement attributes occurring in a study population or system. This includes the movement types that exist in a population that include “migration,” “dispersal,” “sedentary,” and “nomadism.” It is important to understand the characteristics of these movements, for example, movement pathways, home ranging patterns, or the timing of movements. The second step is to determine the ecosystem impacts and services resulting from movements. The knowledge gained from the first two steps guides the decision making process and identifies potential management actions that complement existing management plans. These may include actions that are flexible in space and time, such as time-area closures, which require detailed knowledge of species movements. The fourth step considers the implementation of the proposed actions, including considerations like available knowledge, cost, stakeholder interests and how these influence the effectiveness and feasibility of proposed actions. The final step evaluates the effectiveness of management actions, thereby creating an adaptive management cyclical process whereby the outcomes of the evaluation guide management objectives and future actions. habitat selection along movement paths and the use of subsequent habitat suitability (Chetkiewicz and Boyce, 2009; stopover sites by migratory species (Figure 1). Understanding Lu et al., 2012). Knowledge of movement characteristics may the type of movement in the population determines the also identify potential threats, such as the increased risk of types of management actions needed, but understanding exploitation due to the predictable and aggregating nature of the characteristics of movements is necessary for planning, some migratory species (Bolger et al., 2007; Harris et al., 2009). designing, and implementing management actions. For example, We expand upon how knowledge of the types and characteristics understanding movement pathways is particularly important of species movements can be used to guide the scale of when managers aim to maintain connectivity, particularly as management in Section Scale of Management. the loss of some sites can lead to sudden population decline (Webster et al., 2002; Iwamura et al., 2013). Movement pathways Ecosystem Impacts also indicate whether species use matrix habitats (Fischer et al., Animal movement is a core component of an ecosystem and 2005), are restricted to specific habitat types (Hagen et al., maintaining movement patterns may be vital for sustaining 2012), or barriers prevent movements (Sawyer et al., 2013). ecosystem processes like trophic and species interactions Other movement characteristics, such as the size and shape of (Lundberg and Moberg, 2003; Massol et al., 2011). Movement home ranges, are often used to guide the scale of management provides links between ecosystems and these links may be (Schwartz, 1999) and to determine habitat preference and classified as either resource, genetic or process links (reviewed Frontiers in Ecology and Evolution | www.frontiersin.org 4 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management in Jeltsch et al., 2013). The frequency and type of link will be influencing species movements (e.g., Hornseth and Rempel, be affected by the spatiotemporal scale of movement, such 2015). However, an ongoing challenge in conservation is how as foraging movements within the home range or the less to achieve the scale of management required. Knowing species frequent but larger scale movements of migration (Jeltsch et al., movements answers important management questions like 2013). Movement is also important for maintaining interaction where, when, how and why animals move, which can be used networks in both antagonist (e.g., predator-prey) and mutualist to develop management actions that increase the dynamism (e.g., plant-pollinator) networks (Tylianakis et al., 2010; Hagen and scale of wildlife management, and are complementary to et al., 2012). The loss of species interaction networks may existing plans. Alternative management actions may include have cascading effects on for example food web dynamics ecological networks, time-area closures or threat management, resulting in secondary extinctions (Hagen et al., 2012). Managers and we expand upon these alternative management actions also need to consider how movement may disturb ecosystems. below. The aggregating nature, and long-range movements, of many The first approach is concerned with incorporating localized migratory species may impact ecosystems through exploitation of management actions, such as protected areas or reserves, into a habitats, disease transmission and nutrient loading (Kerbes et al., network of areas and thus increasing the scale of management. 1990; Post et al., 2008). Ecological networks should maintain ecosystem processes, which Animal movement may provide important ecosystem services includes the movement of organisms and subsequent species and these services have been termed mobile-agent based interactions networks (Opdam et al., 2006; Hagen et al., 2012). ecosystem services (MABES; Kremen et al., 2007). These services Ecological networks also incorporate multiple objectives into the are provided at a local scale by species moving within or among spatial planning process, such as conservation goals and different habitats (Kremen et al., 2007). For example, the movements land uses by stakeholders (Opdam et al., 2006). A principal of bees pollinate both wild and agricultural plants (Kremen concept of ecological networks is connectivity, whereby a set of et al., 2007), seeds may be dispersed long distances by birds areas or ecosystems are linked to maintain or enhance population and mammals (Nathan and Muller-landau, 2000) and nutrients viability by facilitating movement (Beier, 1998; Opdam et al., are transferred between marine and terrestrial environments by 2006). Management tools used to improve connectivity of two or the foraging movements of seabirds (Ellis et al., 2006). The more areas are matrix management and corridors (Beier, 1998; ongoing modification of the landscape by humans is altering Fischer et al., 2005). Identifying which habitats are important for landscape connectivity and threatens the future provision of species helps managers create a “soft,” more permeable matrix. MABES (Mitchell et al., 2013). Linking animal movement with For example, a matrix containing scattered trees facilitated management planning allows managers to identify the ecosystem the movement of birds in Australia (Fischer et al., 2005). functions and services that movement provides and thus improve Habitat patches may also act as important stepping stones landscape management (Jeltsch et al., 2013; Mitchell et al., 2013). for long-distance dispersal and range expansions, following climate-driven shifts in habitat suitability (Saura et al., 2014). Scale of Management Strengthening the link between corridor design and species A challenge for management is identifying the scale of movements improves connectivity in the landscape, for instance, management required for effective species conservation. The corridors that were identified through tracking studies were more scale of management may be guided by, amongst others, effective than those identified through modeling approaches the distance of movements like migrations (Klaassen et al., (LaPoint et al., 2013). Corridors may be beneficial for species 2008), by the size of home ranges (Schwartz, 1999), or by moving at larger scales like the Mule deer Odocoileus hemionus the habitat requirements of a species (Angelstam et al., 2004). R., for maintaining connectivity within a species home range, and Habitat selection studies have commonly been used to identify to preserve dispersal events and maintain functional connectivity the habitat requirements of a species, in particular using the (Table 1; Baguette and Van Dyck, 2007; LaPoint et al., 2013; four orders of habitat selection described by Johnson (1980). Sawyer et al., 2013). The first-order of selection identifies the geographical range The second approach is the use of time-area closures. Time- of the species and has commonly been used to map species area closures may be dynamic in time only, i.e., excluding distributions and develop habitat suitability models, which are unwanted practices during a specific time of year, such as a used to guide the scale of conservation planning (Johnson, stopover site for migratory waterfowl (O’Neal et al., 2008). Time- 1980; Angelstam et al., 2004; Guisan et al., 2013). The second, area closures may also be dynamic in space and time, i.e., third and fourth orders of selection concern the selection of the closure tracks the species’ movements like the movements the home range, habitat patches within the home range and of pelagic species (Hobday and Hartmann, 2006). Time-area microhabitats within used patches respectively (Johnson, 1980; closures provide a viable alternative for managing species’ with Meyer and Thuiller, 2006). Meyer and Thuiller (2006) introduce predictable movements. They can be implemented when species a fifth order of selection, which are areas used by populations are most vulnerable, such as aggregation or spawning areas and within the geographical range. These orders of selection inform during critical movement phases (Table 1; Hunter et al., 2006; managers about local reserve site selection (Aldridge and Boyce, Shillinger et al., 2008; Bull et al., 2013). Time-area closures 2007; Guisan et al., 2013), provide indications of habitat may also achieve conservation targets whilst incorporating quality and improvements needed (e.g., Dickson and Beier, stakeholder interests, for example by maintaining alternative 2002; Zeale et al., 2012) and how human disturbance may land-use or harvesting practices, and are being increasingly Frontiers in Ecology and Evolution | www.frontiersin.org 5 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management utilized in marine and freshwater ecosystems (Hobday and A number of approaches have been developed to identify Hartmann, 2006; O’Neal et al., 2008; Shillinger et al., 2008). which management actions will maximize benefits, such as When it is not possible to spatially delineate large areas, it decision theoretic approaches and systematic conservation may be more appropriate to manage the primary threats to a planning (e.g., Margules and Pressey, 2000; Wilson et al., 2009). species instead (Carwardine et al., 2012). Understanding a species Decision theoretic approaches consist of an objective or desired threats enables managers to prioritize management actions that outcome, a description of our knowledge of the system, state achieve the greatest impact (Auerbach et al., 2014; Tulloch variables in the area of interest, such as species populations or et al., 2015). Identifying threats to a species may also indicate habitats, control variables which represent possible management which movement attributes increase species vulnerability. Traits strategies, model constraints and an equation that describes the of some species, such as the predictability of routes, timing of relationship between the benefit of actions and the potential movements, or reliance upon particular sites may increase the management strategies in the area of interest (Wilson et al., 2009). risk of exploitation (Bolger et al., 2007). This knowledge can Understanding species movements enables managers to improve be used to guide management decisions, for instance threat their understanding of the threats, use their knowledge of where management actions may involve time-specific interventions like and when a species will be to identify alternative management anti-poaching activities at important locations and times of the actions, and also recognize the challenges of achieving the year (Berger et al., 2008; Murgui, 2014). Recent advances in management objectives which may not be apparent if a species’ tracking technologies also provide the opportunity to incorporate movements are unknown. Decision theoretic approaches enable real-time monitoring data into threat management schemes, thus managers to prioritize management actions that will better justifying the cost of tracking animal movements (Wall et al., achieve the management objectives (Tulloch et al., 2015). 2014). Real-time tracking data from African elephants Loxodonta Previously, actions were prioritized on areas with the highest africana in Kenya was used to notify wildlife managers when threats or species richness, but now the management actions elephants were about to move into community areas (Wall et al., themselves are being prioritized depending upon whether they 2014). Wildlife managers were able to intervene and prevent are cost-effective, have the greatest impact and are achievable the elephants causing crop damage and reduce human-wildlife (Auerbach et al., 2014; Tulloch et al., 2015). Multiple-action conflicts, a major threat to elephants in Africa (Wall et al., 2014). prioritization schemes are also being considered, whereby a combined set of strategies may be more cost effective and have greater impact than any one strategy alone (Wilson et al., 2009; Implementation Chadés et al., 2015). Therefore, it is vital for managers to evaluate The feasibility of management actions described above may all possible management scenarios to improve the effectiveness of be limited at the implementation phase by considerations like the decision-making process. costs, stakeholder interests, and enforcement. Incorporating animal movement into management planning may entail a Evaluation number of costs, such as the costs of acquiring land and the The importance of evaluating management actions has costs associated with establishing and maintaining a network been highlighted in recent decades to avoid implementing of managed areas (Naidoo et al., 2006). Emphasis is now management actions that do not achieve management goals being placed on identifying the most cost effective action that and thus waste limited funds (e.g., Ferraro and Pattanayak, maximizes benefits (Naidoo et al., 2006; Carwardine et al., 2006; Walsh et al., 2012). Therefore, management strategy 2012; Auerbach et al., 2014). The interests of local stakeholders evaluation (MSE) is vital for determining whether actions may also influence the implementation of management actions have either succeeded or failed in achieving the management due to conflicts between involved parties, for example conflicts objective, and using this knowledge to inform future decisions arising over land-use, resettlement, policies or legislation, and and actions (Pullin et al., 2013). Evaluation is an integral part human-wildlife conflicts (Davies et al., 2013; Symes et al., 2015). of adaptive management and is thus applicable to any form of In addition, limitations may arise due to available manpower, wildlife management. With regards to our framework, evaluation either in relation to monitoring the outcomes of management may be important for determining the effectiveness of actions actions or enforcing them (Keane et al., 2008). These challenges implemented with incomplete knowledge of species movements, are especially pertinent when a species movements takes them and may help prioritize the type of knowledge needed to improve across several country borders (Iwamura et al., 2014; Kark future management. Evaluation is also important for tracking et al., 2015). Cross-boundary collaborations may provide a future uncertainties, such as how variation in the timing of number of benefits, such as improving the cost effectiveness movement may affect management strategies like time-area of management actions and increasing the scale of threat closures, which rely upon knowledge of where and when a management, however it also presents a number of challenges species will be. like political instability, increased costs related to establishing The effectiveness of management actions can be simulated the collaboration, conflicting national goals, and potential delays prior to their implementation, through frameworks like the MSE in implementing actions (Kark et al., 2009, 2015). However, framework (Smith et al., 1999), which has thus far been used incorporating the above challenges into the decision making mostly in commercial fisheries but also has relevance for the process allows managers to identify management strategies that management and conservation of terrestrial species (Bunnefeld are implementable and attainable. et al., 2011; Milner-Gulland, 2011). MSE compares multiple Frontiers in Ecology and Evolution | www.frontiersin.org 6 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management management strategies prior to their implementation, allowing to nearby tributaries (McCormick et al., 1998). After 1 to managers to identify their effectiveness and understand the 5 years the salmon migrates downstream to enter the sea varying forms of uncertainty, such as incomplete knowledge of (Lundqvist, 1983; Otero et al., 2014). Salmon movements in the species movements (Bunnefeld et al., 2011). The outcomes of sea remain difficult to study but this phase can be described as MSE are used to inform the management objectives, study design, nomadic where the distribution of salmon is largely influenced and implementation of management actions (Bunnefeld et al., by environmental factors like sea temperature, surface currents, 2011; Milner-Gulland, 2011). For example, comparative analyses and food availability (Klemetsen et al., 2003; Trudel et al., 2011). could be performed to determine whether management actions Salmon from multiple river systems mix in the Main Basin of should be implemented with limited knowledge of movement the Baltic Sea, leading to mixed-stock fisheries (Karlsson and or whether priority should instead be placed on acquiring data Karlstrårn, 1994). Salmon normally migrate back to their natal that can be used to develop management actions that are more river systems to spawn (Lundqvist, 1983). The movements of tailored to species movements and consequently have greater hatchery-reared salmon may differ from wild salmon in their impact, such as those developed for the leatherback turtle extent, timing, and fidelity (McKinnell et al., 1994; Jutila et al., discussed earlier (Shillinger et al., 2008). 2003). Step 2—Ecosystem Impacts APPLYING THE The stage-structured life cycle of salmon means that juveniles MOVEMENT-MANAGEMENT FRAMEWORK and adults occupy and connect different ecosystems (Schreiber and Rudolf, 2008; Miller and Rudolf, 2011). Species with complex We illustrate the potential for linking movement ecology with life cycles may cause abrupt changes in different ecosystems, management through a case study of the Atlantic salmon. By such as how changes in juvenile abundance may lead to trophic following the steps of the framework, we show how existing cascades across ecosystems to the adult habitat (Knight et al., knowledge of salmon movement ecology has been used to 2005; Schreiber and Rudolf, 2008). The salmon’s life cycle develop management actions and how further knowledge could influences food web dynamics by preying on aquatic species be used to identify alternative management actions. and being preyed upon by aquatic, terrestrial, and avian species (Holmlund and Hammer, 1999, 2004). The Atlantic salmon Case Study—Managing Atlantic Salmon is iteroparous, meaning it can spawn repeatedly as opposed to dying after spawning like the semelparous Pacific salmon (Salmo salar) in the Baltic Sea (Oncorhynchus spp.; Klemetsen et al., 2003). Salmon deaths, and Background repeated migrations, link ecosystems and transfer nutrients and Atlantic salmon have had large population declines in the Baltic carbon between marine and freshwater ecosystems (Holmlund Sea (Karlsson and Karlstrårn, 1994; Klemetsen et al., 2003) so it and Hammer, 1999, 2004). Salmon provide several ecosystem is an important issue for management and conservation alike. services. Spawning salmon regulate sediment processes whilst Overfishing and the loss of connectivity in river systems, due to their movements between marine and freshwater ecosystems hydroelectric dams, has been a driving cause of salmon declines support aquatic/terrestrial food webs and nutrient cycling and in the 1990s only 12 of the 44 naturally reproducing salmon (Bottom et al., 2009; Kulmala et al., 2012). Salmon populations stocks in the Gulf of Bothnia remained (Karlsson and Karlstrårn, provide a highly valued food source for both commercial, 1994). A number of actions have been taken to restore these personal-use, and recreational fisheries (Kulmala et al., 2012). populations but several rivers are not self-sustaining and many salmon rivers are below 50% of potential smolt production (ICES, Step 3—Scale of Management 2012). In this case study, we focus on the management goals The life cycle of the salmon illustrates the importance of of the Swedish government, through the Swedish Agency for understanding their movements due to the direct influence that Marine and Water Management (SwAM). Their aim is to reverse salmon movement has on their survival and reproduction. As a the decline of salmon stocks whilst maintaining activities like consequence, the scale of management may vary in accordance recreational and commercial fishing. Multiple techniques have to the specific life cycle stage and process that is being targeted been used to monitor the movements of salmon that include by management. For instance, management may consider the observational and trapping data (Lundqvist et al., 2010), tagging implementation of more localized management actions during methods (Payne et al., 2010), acoustic or radio telemetry (Serrano the sedentary phases of the salmon’s life cycle. These include the et al., 2009), stable isotopes, and genetics (Barnett-Johnson et al., development phase after hatching salmon and spawning phase 2008). Therefore, several sources of movement data are available of adults. Management actions have therefore focused on either to continue with the movement-management framework. preserving existing habitats used by salmon, or alternatively, Step 1—Movement Attributes restoration actions have been taken to improve habitat suitability Salmon can exhibit all four types of movement (sedentary, for spawning and recently hatched salmon (Nilsson et al., 2005). dispersal, nomadism, and migration) during its life cycle. A key aspect of salmon movements is the migration from Salmon hatch in freshwater rivers, where they are solitary and the natal/spawning areas to the sea and their return to rivers. defend territories for food, thus exhibiting sedentary movements Lundqvist et al. (2008) indicate that a salmon population (Lundqvist, 1983). During this phase they may also disperse could increase by 500% if connectivity was improved along Frontiers in Ecology and Evolution | www.frontiersin.org 7 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management the migration path. The severe implications resulting from loss life cycle, the nomadic movements of adults need transboundary of connectivity has resulted in several management actions collaborations for effective management. The Main Basin of that target connectivity between river systems and the sea the Baltic Sea is an offshore fishery that is exploited by (McKinnell et al., 1994; Lundqvist et al., 2008; Serrano et al., many countries in the region. Therefore, international measures 2009). Knowledge of migration timing has enabled managers are needed to effectively manage the mixed-stock fishery and to adopt actions that are flexible in time, which may increase knowledge of movements and genetics is vital to achieve this their acceptance by impacted stakeholders like the hydroelectric goal. Harvest quotas are provided by the Common Fisheries power industry. These have included diverting water from Policy but the Atlantic salmon would benefit further from the re- hydroelectric dams to a bypass during the migratory period only, establishment of an International Baltic Treaty. Transboundary or transporting salmon 88 km upstream in trucks from the first collaborations provide a number of challenges that influence barrier to the spawning grounds (Lundqvist et al., 2008; Serrano the implementation potential of management actions (Kark et al., 2009; Hagelin et al., 2015). et al., 2015). These may include increased financial costs, Meanwhile, a key aim should be to reduce the amount of delayed conservation planning or countries “free-riding” on the fishing effort in the Main Basin, due to stock mixing, which assumption that management actions will be implemented by includes threatened stocks. Instead, fishing efforts could be other countries (Kark et al., 2009, 2015). However, transboundary focused in coastal areas or river estuaries where the stock status collaborations may also improve the cost effectiveness of is known. Understanding the movements of hatchery-reared management and increase the scale of management to more salmon may also identify alternative management actions for effectively manage a highly mobile species (Kark et al., 2015). implementation. Research indicates that hatchery-reared salmon are more likely to be caught in the Bothnian Sea compared Step 5—Evaluation to wild stocks because hatchery-reared salmon are less likely Mathematical and statistical models have been developed that to migrate to the Main Basin of the Baltic Sea (Jutila et al., link biological and economic data to identify management 2003). Hatchery-reared salmon may also arrive in the northern actions for salmon in the Baltic (Kulmala et al., 2008). Kulmala Baltic later than wild salmon stocks (McKinnell et al., 1994). et al. (2008) explicitly incorporate the migratory movements of This knowledge may be used to implement a time-area based salmon to determine optimal harvest solutions, and identify that approach, providing a potentially viable management option driftnet fisheries should be excluded as a harvest method. Several that maintains recreational and commercial harvesting whilst studies have also evaluated the effectiveness of management simultaneously increasing the harvest of hatchery-reared salmon. plans prior to their implementation, which include both national plans and international plans (Haapasaari and Karjalainen, 2010; Step 4—Implementation Levontin et al., 2011). Bayesian network analyses have been used The management of salmon influences a number of stakeholders to incorporate several sources of data that include the biology of like commercial fisheries, the power industry, general public, the species, expert knowledge, and sociological data to evaluate and conservation community. Understanding the movement alternative management options (Haapasaari and Karjalainen, ecology of salmon has enabled managers to identify actions 2010; Levontin et al., 2011). These studies have determined the that have a higher likelihood of acceptance by stakeholders and commitment of stakeholders to management options and how thus improved effectiveness. An example includes the time- this may influence the effectiveness of proposed management area based approach for fisheries, whereby the coastal fishery actions (Haapasaari and Karjalainen, 2010; Levontin et al., is opened later in the season meaning that most wild salmon 2011). have already entered the river system and the fisheries harvest With regards to movement, management interventions like is dominated by hatchery-reared salmon (ICES, 2012). Such fish ladders may not guarantee connectivity, as illustrated by an approach maintains the livelihoods of fisherman whilst Lundqvist et al. (2008). The project evaluation found that reducing harvest pressure on wild salmon and thus achieving salmon migrating upstream were not drawn to the bypass conservation targets. Another example is how the knowledge containing the fish ladder, due to differing discharge rates of timing of salmon migrations enables hydroelectric dams to from the hydroelectric dam and the bypass. Salmon survival regulate discharge rates, which target conservation goals during was also reduced the following spring as salmon were not the salmon migration and electricity production at other times drawn to the fish ladder during the seawards migration, but of the year (Lundqvist et al., 2008; Håkansson, 2009). Achieving traveled through the turbines instead. Improved knowledge of management targets increasingly relies upon identifying trade- the movement ecology of salmon, such as how they move offs that are acceptable to all stakeholders (Redpath et al., 2013). in the river and what cues they are drawn to are needed to By linking movement ecology with management, alternative improve the designs of existing and future connectivity measures management actions can be identified that allow managers to (Lundqvist et al., 2008). In addition, management actions are explore trade-off scenarios with stakeholders, which increase the not being implemented for the full movement cycle. In the implementation potential of proposed management actions. example of transporting salmon upstream by truck, no actions Several management actions for salmon are executed within are being taken for the downstream migration of salmon, national boundaries, such as maintaining connectivity in resulting in very low survival rates (Bergman et al., 2014; Hagelin freshwater systems, improving breeding habitats, and managing et al., 2015). The recovery of this river’s stock is therefore coastal fisheries. However, during the marine phase of the salmon limited by not considering the migratory connectivity of both Frontiers in Ecology and Evolution | www.frontiersin.org 8 January 2016 | Volume 3 | Article 155 Allen and Singh Linking Movement with Management upstream and downstream migrations. In this instance it would species will be is a pre-requisite for the successful implementation be important to evaluate both the effectiveness of translocating of time-area approaches, which allow managers to develop trade- individuals to spawning areas (Fischer and Lindenmayer, 2000), off scenarios that balance conservation needs with alternative land-use practices (O’Neal et al., 2008; Shillinger et al., 2008; and subsequently whether the action is meeting management Game et al., 2009; Redpath et al., 2013). objectives of population recovery. We have highlighted how knowledge gained from movement ecology can be used to identify alternative, complementary MANAGEMENT IMPLICATIONS strategies in wildlife management. Our conceptual framework provides a step by step workflow that aims to understand the Studies continue to highlight that management actions focused movement patterns of a species and use this knowledge to guide in one area, such as protected areas, are not sufficient for management actions. As the field of movement ecology continues effectively conserving a species (Thirgood et al., 2004; Martin to grow, it is important to strengthen the link with wildlife et al., 2007; Runge et al., 2014). Shortfalls include the scale management to further improve the decision-making capabilities of management, conflicts with stakeholders, alternative land- of practitioners and managers. uses and limited space available (Sanderson et al., 2002; Runge et al., 2014; Symes et al., 2015). Management actions focused in one area also fail to account for species movements (Thirgood AUTHOR CONTRIBUTIONS et al., 2004; Runge et al., 2014). Linking movement ecology to conservation has several implications for the future management AA and NS conceived the idea. AA wrote the majority of the of wildlife. Understanding a species movements enable managers manuscript with input from NS to implement actions along the entire movement path, such as a flyway approach for birds and butterflies (Klaassen et al., FUNDING 2008; Howard and Davis, 2009) or dynamic protected areas in the ocean (Shillinger et al., 2008; Game et al., 2009) and The study was funded by the thematic programme in Wildlife and on land (Singh and Milner-Gulland, 2011; Bull et al., 2013). Forestry at the Swedish University of Agricultural Sciences, the Understanding movement also enables managers to identify Swedish Environmental Protection Agency (Naturvårdsverket, threats, such as the loss of important sites (Iwamura et al., 2013) 802-0102-11) and their committee for Wildlife Research, the or barriers to movement (Seidler et al., 2015), and therefore Swedish Association for Hunting Wildlife Management. prioritize the most effective management actions that have the highest chance of success (Game et al., 2013; Auerbach et al., 2014; Tulloch et al., 2015). Knowledge of species movements ACKNOWLEDGMENTS allows managers to identify alternative management actions We thank Ascelin Gordon, Anouschka Hof, Göran Spong, and that are flexible in space and time, such as time-area based Nils Bunnefeld, and the two reviewers, Robert A. 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Ecol. 82, 770–780. doi: conducted in the absence of any commercial or financial relationships that could 10.1111/1365-2656.12045 be construed as a potential conflict of interest. Wall, J., Wittemyer, G., Klinkenberg, B., and Douglas-Hamilton, I. (2014). Novel opportunities for wildlife conservation and research with real-time monitoring. Copyright © 2016 Allen and Singh. This is an open-access article distributed Ecol. Appl. 24, 593–601. doi: 10.1890/13-1971.1 under the terms of the Creative Commons Attribution License (CC BY). The use, Walsh, J. C., Wilson, K. A., Benshemesh, J., and Possingham, H. P. (2012). distribution or reproduction in other forums is permitted, provided the original Unexpected outcomes of invasive predator control: the importance of author(s) or licensor are credited and that the original publication in this journal evaluating conservation management actions. Anim. Conserv. 15, 319–328. doi: is cited, in accordance with accepted academic practice. 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