When good animals love bad restored habitats ... - Wiley Online Library

Journal of Applied Ecology 2017, 54, 1478–1486

doi: 10.1111/1365-2664.12829

REVIEW

When good animals love bad restored habitats: how maladaptive habitat selection can constrain restoration Robin Hale* and Stephen E. Swearer School of BioSciences, University of Melbourne, Parkville, Vic., Australia

Summary 1. Restoration is increasingly undertaken to ameliorate the risks of habitat loss and transformation to biodiversity. Despite significant expenditure of time and resources world-wide, restored habitats commonly fail to achieve these objectives. 2. Restoration could fail because animals either avoid restored habitats (perceptual traps) or prefer restored habitats where their fitness is reduced (ecological traps). Consequently, restoration may have a neutral impact or more worryingly provide an additional risk to population persistence. Whether traps arise as an unintended consequence of restoration has largely been unexplored. 3. Our aim is to highlight how traps can compromise restoration efforts and propose ways to reduce this possibility. We first highlight five criteria for successful habitat restoration to identify how and where ecological and perceptual traps could arise and use case studies to demonstrate some of the diverse ways restoration could cause traps. Managing traps that form via restoration depends on reinstating the links between habitat quality and preference. We suggest resource-based habitat approaches, which consider what represents functional habitats from the perspective of animals, are a potentially useful tool in this regard. Furthermore, cognitive theory may help to improve our understanding of how animals select habitats and to address problematic behaviours as they arise. 4. Synthesis and applications. Restoration will fail if habitat quality and preference are not strongly linked, but this possibility has received limited attention. Our review will help ensure that restored habitats provide the resources required by animals, and that animals assess and respond to these habitats adaptively. We hope to stimulate further discussion between evolutionary, behavioural and restoration ecologists to improve the success of habitat restoration.

Key-words: constraint, ecological trap, failure, fitness, habitat management, habitat selection, maladaptive behaviour, perceptual trap, restoration, undervalued resource

Introduction Humans have and continue to change natural ecosystems at faster rates and greater extents than any other comparable period in history (Millenium Ecosystem Assessment 2005). Consequently, biodiversity is threatened by the individual and interactive effects of a range of stressors including habitat loss, pollution, overexploitation, invasive species and climate change (Butchart et al. 2010). These stressors are ubiquitous, affecting terrestrial (e.g. Lambin *Correspondence author. E-mail: [email protected]

& Meyfroidt 2011), freshwater (e.g. Vorosmarty et al. 2010) and marine (e.g. Halpern et al. 2015) ecosystems. For animals, one of the main consequences of anthropogenic changes to ecosystems is the loss or transformation of habitats. More than 20% of global land area has been converted for human uses, with even greater losses of particular habitat types (e.g., 69% of dry forests in southeast Asia; Hoekstra et al. 2005). In recognition of this loss and the risks it poses to biodiversity, efforts are increasingly underway to restore habitats for animals. The purpose of ecological restoration is to assist in the recovery of degraded, damaged or destroyed ecosystems

© 2016 The Authors. Journal of Applied Ecology © 2016 British Ecological Society

Maladaptive behaviours can constrain restoration (Society for Ecological Restoration 2004). While restoration ecology is a relatively young discipline, the underlying science is well structured. Conceptual frameworks exist that outline the types of restoration and the various steps involved, from identifying the processes leading to degradation through to the eventual monitoring of restoration efforts and assessments of their success (e.g. Hobbs & Norton 1996; Society for Ecological Restoration 2004). Work has also focussed on providing guidance for particular steps in this process, such as defining goals and measuring success (e.g. Society for Ecological Restoration 2004; Palmer et al. 2005), and more generally exploring the links between restoration and ecological theory (e.g. Lake 2001; Lake, Bond & Reich 2007; Perring et al. 2015).

What does restoration for animals involve and how successful is it? Ecological restoration has traditionally been focussed on restoring abiotic conditions and vegetation. However, it is often assumed that these changes, which return structural habitat resources, will lead to responses by animals, such as increases in biodiversity or abundances of target species (i.e. the ‘Field of Dreams hypothesis’ – Palmer, Ambrose & Poff 1997). Restoration for animals generally focuses on individual species and their habitat needs (McAlpine et al. 2016), often in terms of considering these within the wider landscape, such as to enhance functional connectivity (Thomson et al. 2009). Assessing whether restoration is successful is challenging, as adequate monitoring is frequently not undertaken. For example, in the National River Restoration Science Synthesis project, less than half of all projects reviewed set measurable objectives that were quantitatively assessed to evaluate success (Bernhardt et al. 2005). Even when monitoring occurs, setting appropriate standards for measuring success is difficult and poses a challenge to evaluation (Suding 2011), particularly when targets may differ between stakeholders in the same projects. For instance, a lack of biotic responses may not indicate restoration has failed, as other notions of success (e.g. improved aesthetics, provision of ecosystem services) may still be achieved (Zedler 2007). Despite these challenges, some studies have demonstrated improved biodiversity (although potentially not to levels comparable with reference locations; Benayas et al. 2009) and the recovery of ecosystems following the cessation of human disturbances (when given sufficient time; Jones & Schmitz 2009). Generally though, most assessments illustrate that successful restoration is likely to be the exception (e.g. Moreno-Mateos et al. 2012; Palmer, Hondula & Koch 2014).

Ecological and perceptual traps can cause restoration failure Given that restoration ecology has a strong underlying conceptual basis, and involves the expenditure of

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significant time and resources, why does restoration commonly fail to produce desired outcomes for animals? What should practitioners consider to improve restoration success? Responses to restoration can be constrained in a number of ways, by a range of abiotic (e.g. climate, hydrology), biotic (e.g. availability of colonists) and anthropogenic factors (e.g. intensity of land use) (e.g. Hobbs & Norton 1996; Bond & Lake 2003; Sudduth et al. 2011). One likely, but largely unexplored, reason for restoration failure is that human perceptions of the environment, which guide restoration activities, do not match how animals perceive and use habitats. Humans typically view and treat ‘habitat’ synonymously with structural units such as vegetation type or land cover (van Dyck 2012). However, animals perceive habitats quite differently. The ‘Umwelt’ concept (originally developed by von Uexk€ ull 1909) describes how animals perceive and utilize different subsets of the environment due to their developmental and evolutionary history, ultimately determining what structural characteristics of habitats provide functionality to animals (van Dyck 2012). This mismatch in human and animal perceptions of habitat could mean that restoration does not provide the key elements of habitats that ultimately determine their suitability for animals. Many animals use indirect cues as proxies to assess the likely current and future state of the environment and to guide habitat selection decisions. Successful restoration will provide suitable habitats that animals assess and respond to adaptively in comparison with other available habitats. Understanding if restoration is successful, therefore, requires knowledge about how animals select and use habitats; however, behaviour is rarely considered when evaluating restoration success (Lindell 2008). If animals respond in unpredictable and inappropriate ways, restoration can fail. One possibility is that restoration improves habitat quality, but animals fail to perceive these changes, leading to avoidance of restored habitats, i.e. a ‘perceptual trap’ (Patten & Kelly 2010) or ‘undervalued resource’, analogous to scarecrows that are used to prevent birds settling in arable fields, but provide an erroneous indicator of risk, thus discouraging settlement into suitable habitat (Gilroy & Sutherland 2007). This could occur if restoration improves habitat quality, but restored sites lack suitable cues for animals to detect these improvements. Perceptual traps will lead to restored sites being avoided by animals, but more serious consequences for local and regional persistence can arise if restoration creates poor-quality habitats that animals prefer. Such ‘ecological traps’ (habitats that animals prefer or equally prefer but where their fitness is lower relative to other available habitats – Robertson & Hutto 2006) can compromise population persistence (e.g. Hale, Treml & Swearer 2015) and increase extinction risks (Battin 2004). Perhaps the most compelling example of ecological traps

© 2016 The Authors. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 54, 1478–1486

1480 R. Hale & S. E. Swearer is insects that are attracted to lay their eggs on artificial surfaces (e.g. roads, bridges, cars and tombstones) via polarized light, resulting in their death (Horvath & Zeil 1996; Horvath, Bernath & Molnar 1998). Underlying the ecological trap concept is the notion that rapid environmental change leads to maladaptive behaviour by decoupling the links between habitat quality and preference. While restoration is known to cause traps (Robertson, Rehage & Sih 2013), efforts to prevent and mitigate traps are still in their infancy (but see Battin 2004; Robertson 2012; Hale et al. 2015a). Previously, we have highlighted how urban management activities could cause traps, and how these could be identified and managed (Hale et al. 2015a). We build on that work here, by first considering the steps involved in successful habitat restoration for animals, and how ecological and perceptual traps fit within that process. We then use case studies to demonstrate some of the potential ways that restoration can cause traps. We conclude by highlighting methods that offer great promise in managing maladaptive habitat selection behaviours in the context of restoration.

Criteria for successful habitat restoration We use efforts to describe constraints on habitat restoration (Bond & Lake 2003) and key considerations in goal setting (Miller & Hobbs 2007) as the basis for outlining five criteria to ensure restoration provides suitable habitat for animals. Our purpose is not to review this literature in detail but rather to highlight when and how ecological and perceptual traps might compromise restoration success. Restoration is commonly undertaken on the assumption that animals will respond to improvements in structural habitat (Palmer, Ambrose & Poff 1997). It is, therefore, critical that restoration improves structural habitat (Fig. 1),

as the basis for expecting responses by animals no longer exists if habitats do not change. Violin et al. (2011) provide a useful example of when restoration has been unsuccessful in changing structural habitats. They compared a range of physical and biological variables describing habitat structure in degraded urban, restored urban and forested streams in North Carolina, showing that restored urban streams were similar to their degraded urban counterparts and both had less habitat complexity than forested streams, which had invertebrate communities characterized by less-tolerant species. Large-scale and long-term phenomena have the potential to constrain both the timing and magnitude of responses to restoration, such as when the influence of large dams on river hydrology can overwhelm local-scale efforts to restore habitats by adding large woody debris (Bond & Lake 2003). The spatial and temporal scales of restoration efforts must, therefore, match the scales of the process causing degradation (Hobbs & Norton 1996). Animals must be available to colonize restored habitats (Fig. 1). A mixture of landscape-level characteristics (e.g. size, shape, location of restored habitats, distance to sources, connectivity, matrix characteristics, barriers to colonization – Bond & Lake 2003; Miller & Hobbs 2007) and life-history traits (e.g. dispersal ability) of animals are likely to determine encounter rates with habitats in general (Hale, Treml & Swearer 2015), as well as those subject to restoration efforts. For example, the proximity of source populations to restored sites can be a key determinant of restoration success (Sundermann, Stoll & Haase 2011). Large-scale and long-term processes may also affect the colonization of sites even if local-scale habitat conditions improve. In southern Australia, restoration of degraded riparian zones improved structural habitat (e.g. increased density of plants,

Fig. 1. Outline of five critical criteria for ensuring habitat restoration for animals is successful. The right hand column illustrates key considerations for each of these steps (summarized from Palmer, Ambrose & Poff 1997; Bond & Lake 2003; Miller & Hobbs 2007; Hale, Treml & Swearer 2015). Perceptual traps form when animals avoid restored sites where their fitness would be higher than in other available sites. Ecological traps form when animals prefer restored sites where their fitness is lower than in other available sites. © 2016 The Authors. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 54, 1478–1486

Maladaptive behaviours can constrain restoration groundcover and leaf litter), but birds did not respond, most likely due to the effects of ongoing population declines in the region associated with land-use changes and drought (Hale et al. 2015b). Matching the scale of restoration efforts to the scale of degrading processes is important, but the scale at which animals perceive and respond to the environment must also be considered. The ‘functional grain’ of the landscape describes the spatial scale of the interaction between landscape structure (in terms of resource distribution) and the perception of an organism (Baguette & van Dyck 2007). Mismatches between the perceptual range of animals (the distance at which animals can perceive elements of the landscape – Zollner & Lima 1997) and the scale of restoration efforts may mean sites are undetectable (e.g. replanted sites are ‘oases’ in an agricultural barren landscape – Hale et al. 2015b). Whether restored sites are detectable will depend both on the characteristics of restoration efforts (e.g. size, location within the landscape) and the behaviour of animals, as those with larger perceptual ranges may perceive sites from further away. Understanding the process underlying habitat selection and colonization is critical, given that the use of restored habitats by target species is a vital component to restoration (Andrews, Brawn & Ward 2015). Experiments with Grasshopper sparrows (Ammodramus savannarum) demonstrate the need to understand habitat selection behaviour to assess restoration success (Andrews, Brawn & Ward 2015). Many birds use social cues (e.g. vocalizations) to select habitats, and seemingly appropriate but unoccupied habitats can be colonized when social cues are added. Sparrows located and settled into newly created grasslands lacking these cues; however, densities were nearly double later in the season when conspecific vocalizations were broadcast. These social cues may indicate the reproductive success of individuals at a site, and hence future reproduction. Initial settlers are likely to be using other cues (perhaps from vegetation), before social cues become important later in the season. Understanding habitat selection behaviour and how it changes through time is an important element of assessing how birds use restored grasslands, and how animals respond to restored habitats more generally. It is critical that restored sites provide resources that match the requirements of target species (van Dyck 2012), for example, requirements for shelter, food and breeding (Miller & Hobbs 2007). The suitability of habitats for particular species may also change through time following restoration, as different resources are returned. For example, revegetation is likely to provide resources for grounddwelling birds in the short-term (e.g. leaf litter), but there may be considerable time lags in the provision of resources used by arboreal species (e.g. tree hollows for nesting) (Vesk et al. 2008). It will be important to consider that meeting this criteria might result in unintended interactions that affect other species, for example, the attraction of competitors or predators or exclusion of

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mutualists. This is important as successful restoration should not lead to any lasting harm to the ecosystem (Palmer et al. 2005). Restoration should lead to self-sustaining ecosystems that require little ongoing maintenance or repair (Palmer et al. 2005), requiring that restored sites have a net reproductive rate greater than one (Lindell 2008). A key consideration, therefore, is the degree to which restoration increases productivity (in terms of the population growth of a target animal species), or simply attracts individuals from elsewhere. This ‘attraction vs. production’ hypothesis has been discussed extensively in marine systems, for example, in terms of whether higher catches of fish at artificial reefs represent increased production or simply reefs attracting fish from elsewhere (Bohnsack 1989). If the latter, restoration will not be successful in developing selfsustainable and resilient ecosystems.

Perceptual and ecological traps: when habitat suitability and selection become decoupled Ecological and perceptual traps occur when the attractiveness of habitats poorly reflects their suitability for animals (Robertson & Hutto 2006; Patten & Kelly 2010). For perceptual traps, this can occur when rapid environmental change either: (i) modifies settlement cues so habitats become less attractive but habitat quality remains unchanged, (ii) improves habitat quality but not settlement cues so higher quality habitats do not become more attractive, or (iii) simultaneously increases the quality of habitats and decreases their attractiveness to animals (Patten & Kelly 2010). Perceptual traps will, therefore, arise when a pool of potential colonists exists, but these animals avoid restored sites (Fig. 1). The mechanisms underlying ecological traps are similar, but they lead to animals selecting restored habitats where their fitness is lower than in other available non-restored habitats (i.e. between the third and fourth criteria in Fig. 1). Specifically, ecological traps can arise in three ways: (i) settlement cues change making habitats more attractive while their quality remains unchanged, (ii) habitat quality decreases but settlement cues remain unchanged so habitats are as attractive as they were previously, or (iii) both settlement cues and habitats themselves change, so habitats become more attractive but of poorer quality (Robertson & Hutto 2006). Changes in structural habitat that occur following restoration, which are often presumed to be indicative of the successful provision of habitats for animals, might actually translate into worse conditions for animals based on their perception of the environment (van Dyck 2012). Restoration can cause a range of maladaptive behaviours (Robertson, Rehage & Sih 2013), but only a handful of studies have demonstrated that it can cause ecological traps (Hale & Swearer 2016). We use some of these and other case studies from the wider literature to demonstrate the diverse ways that this can occur.


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Restoration could cause ecological traps in a variety of ways Ecological traps arising from restoration efforts can directly affect animals. For example, butterflies oviposited more frequently in restored wetlands in southern Oregon that were seasonally flooded, resulting in survival seven times lower than in nearby unrestored wetlands (Severns 2011), creating an ecological trap caused by the direct effects of increased exposure to disturbance. Disturbances can alter habitat structure and availability and compromise restoration efforts (e.g. the effects of droughts and floods on stream restoration – Reich & Lake 2015) and will cause ecological traps if these changes reduce the fitness of animals at preferred restored sites. The underlying cause of ecological traps can also be more complicated. Hawlena et al. (2010) demonstrated that experimental treatments simulating vegetation replanting caused an ecological trap for desert lizards by increasing the effects of avian predators. In this instance, the ecological trap did not arise via direct exposure to disturbance, but through the effects of predation on the trapped lizards. Restored sites might attract undesirable species, for example, revegetation programmes in Australia may benefit introduced red foxes (Vulpes vulpes) (Arthur, Henry & Reid 2010). While a major concern has been an exacerbation of the effects of foxes on livestock, native fauna could also be affected if they preferentially select revegetated sites but suffer increased predation. Restoration can cause ecological traps by creating spatial mismatches between the requirements of animals and the quality of habitats. In large Neotropical rivers, ecological traps can be unintended consequences of removing barriers to restore fish passage (Pelicice & Agostinho 2008). Fish may subsequently move into upstream areas that lack spawning and nursery habitats that are present below the passage barrier. The effects of such traps could be further compounded if different dispersal phenotypes exist and some are selectively removed (Hale, Morrongiello & Swearer 2016). While ecological traps have been studied in terms of spatial mismatches between habitat suitability and their use by animals, temporal mismatches could also occur. Many animals use cues to indicate the optimal timing for life-history events (e.g. breeding, migration), and there can be severe consequences when these cues become misleading and such events are mistimed so they occur during unsuitable environmental conditions (McNamara et al. 2011; van Dyck et al. 2015). The flow regimes of many rivers have been greatly altered (Bunn & Arthington 2002), with environmental flow releases used as an important management tool in many areas of the world. These can stimulate fish spawning and recruitment (King, Tonkin & Mahoney 2009), but releases at inappropriate times could lead to fish using spawning habitats when environmental conditions are unsuitable (e.g. food resources are low, predators are present) causing an ecological trap.

When are traps likely to be most important? The examples above represent just a subset of the possible ways restoration could cause traps. It is worth considering briefly when restoration is most likely to cause traps, and when traps are likely to be most important, relative to other potential constraints on restoration success. Maladaptive behaviours are most likely when animals encounter cues that closely resemble those that have previously been accurate indicators of environmental conditions, and likely to have most severe effects when animals experience new conditions that are very different to those under which their traits have been shaped (Ghalambor et al. 2007; Sih 2013). Consequently, animals would (i) be more likely to prefer restored ecological traps that contain similar cues to those used adaptively previously, and (ii) have their fitness most compromised when restored habitats expose them to novel conditions very different to those they have previously experienced. Ultimately, the likelihood that animals select traps and the costs if they do will be determined by these two factors, along with their behavioural characteristics (e.g. simplicity/complexity of habitat selection behaviour) and life-history traits (e.g. reproductive rate, generation time, capacity for learning), as well as the landscape context of traps (e.g. size, position within habitat networks) (Battin 2004; Hale, Treml & Swearer 2015). Undoubtedly, the importance of ecological and perceptual traps will change relative to the other biotic and abiotic constraints on restoration success outlined above. For example, traps are likely to be of less concern when largescale and long-term processes overwhelm local-scale responses to restoration. Likewise traps cannot form when there is no pool of available colonists, given that they describe effects on these colonists when they are selecting habitats. Formally comparing the relative importance of different causes of restoration failure will be challenging as unsuccessful projects are less likely to be published than those in which positive responses are detected. To help learn and adapt future efforts, it is important that the results of unsuccessful projects are published, and some journals have taken steps to make this possible (e.g. Restoration Ecology now publishes a ‘Setbacks and Surprises’ section). It would be ideal to be able to consider the underlying mechanism of each of these constraints (e.g. do they mean that habitat structure has not changed, that no pool of colonists exist, that restoration does not provide required resources for animals, that animals maladaptively respond to restored habitats and that restoration does not increase productivity), and whether this only leads to a lack of response to restoration, or to the fitness and population persistence of animals being compromised.

Reinstating the links between habitat quality and habitat selection Successful restoration will result in the creation of highquality habitats that animals assess and respond to


Maladaptive behaviours can constrain restoration adaptively in comparison with other available habitats. Managing the effects of ecological and perceptual traps, therefore, depends on reinstating the links between habitat quality and habitat selection, which, depending on how the trap has formed, requires reducing the attractiveness of ecological traps, increasing their quality, or both (Robertson, Rehage & Sih 2013). Broadly, the first alternative requires identifying and subsequently improving the aspects of habitats that are reducing the fitness of animals, for example, by improving habitat quality by remediating polluted sediments in wetlands (Hale et al. 2015a). The second requires identifying the cues that trapped animals use to select habitats and manipulating these (e.g. removal of attractive cues, targeted addition of repulsive cues) to reduce habitat attractiveness (Robertson 2012). In comparison, mitigating a perceptual trap will require making restored habitats for animals more attractive, by fixing the cues animals use to select habitats or using methods to attract individuals (e.g. song playback or decoys) (Patten & Kelly 2010). We outline below how recent work describing ways to view the functionality of habitats for animals offers great promise in targeting efforts to improve habitat quality, as does applying the principles of animal cognition to understand how individuals use cues to select habitats, as the basis for manipulating the attractiveness of habitats. DEFINING HABITAT IN TERMS OF RESOURCES

Restoration will fail if resources are not provided that match the requirements of animals. The crux is how ‘habitat’ is defined, and if this definition matches the requirements of animals. While researchers and managers implicitly or explicitly define habitats, this match or potential mismatch is rarely considered (Mitchell & Powell 2003). Understanding what defines suitable habitat in terms of growth, reproduction and survival, however, is central to both successful habitat restoration and the management of traps. This requires moving away from classifying habitats typologically to more explicitly considering how animals might view and respond to them in terms of the resources they provide (Mitchell & Powell 2003; van Dyck 2012). Ecological traps are also studied most frequently at the local-scale (i.e. by testing if some of several patches are traps), but understanding their effects requires considering how they fit within the gradients of habitat quality that are likely present across the landscape (Hale & Swearer 2016). Taking a more animal-centric view of the environment is critical, especially in terms of how they perceive and use structural elements of habitats (i.e. their Umwelt). One useful method to do so is the ‘resource-based’ habitat approach (Dennis, Shreeve & Van Dyck 2003; Dennis, Shreeve & van Dyck 2006). This involves considering the resources that animals require at different life-cycle stages, in terms of consumables (e.g. food) and utilities (e.g. conditions for existence, development, persistence, suitable microclimate, enemy-free space), and how this affects their movements across life-cycle stages. Habitats are

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defined by the intersection and union of these resources. Vanreusel & van Dyck (2007) used this method to generate spatially explicit maps describing functional habitat resources for the green hairstreak butterfly (Callophrys rubi). They identified the resources likely to provide a range of key ecological functions in a national park in North East Belgium, coupled with mark–recapture–release studies to estimate movements, and surveys to examine habitat use. Only a small subset (22%) of their study area was identified as functional habitat using this approach, but this contained >80% of all observed butterfly records. As this example demonstrates, restoration based solely on structural habitats might, therefore, result in the provision of large amounts of habitat that are unlikely to be used by animals. This approach can also be used to better target areas with the highest potential for habitat restoration (i.e. those that contain some but not all key resources or habitat selection cues that can be provided via restoration). Although this method will be more suitable for some species more than others (e.g. those that can be easily tracked and resources identified), it provides a useful illustration of how restoration based on animal perceptions of the environment might be more successful. Stream restoration presents another informative example of how realigning human and animal perceptions of the environment can improve success. Typically, stream restoration involves actions to change the hydrology and geomorphology of the channel, and while physical aspects of habitats (e.g. channel form, substrate and velocity) are often substantially improved, improvements in biodiversity are rare (Palmer, Hondula & Koch 2014). While other stressors can constrain restoration efforts (Palmer, Menninger & Bernhardt 2010), it is possible that the habitat elements most important to animals are not being restored. Local abundances of some semi-aquatic insects may be governed more strongly by factors affecting reproductive success, in particular the availability of suitable spawning sites (e.g., rocks protruding from streams on which to lay their eggs) (Peckarsky, Taylor & Caudill 2000), than by juvenile or adult habitat availability. Some species have very specific requirements in assessing such sites, e.g. the size of the ‘landing pad’ emerging from the stream, and microhabitat conditions such as local current velocity (Reich & Downes 2003a,b). Restoration that leads to changes in geomorphology and hydrology may be unsuccessful if oviposition sites with these particular characteristics are not provided. USING COGNITION TO MANIPULATE HABITAT SELECTION

Adopting a mechanistic view of animal behaviour can aid in identifying levers for modifying behaviour and influencing population-level processes (Blumstein & Berger-Tal 2015). The general pathways via which traps can form have been identified (Robertson, Rehage & Sih 2013), but the proximate sensory-cognitive causes have not (Robertson & Chalfoun 2016). For example, do maladaptive


1484 R. Hale & S. E. Swearer behaviours arise because animals have sensory organs that are poorly designed to process novel information thus resulting in errors in assessing cues, or do these organs successfully pass this information to the brain but processes for evaluating it have become corrupted (Robertson & Chalfoun 2016)? In the context of traps and habitat restoration, gaining a better understanding of habitat selection behaviour will be critical. We suggest that principles from cognition (the mechanisms by which animals acquire, process, store and act on information from the environment – Shettleworth 2010) could prove useful in guiding efforts to manipulate the habitat selection behaviour of animals to ensure they respond adaptively to high-quality restored habitats. Greggor et al. (2014) outline the pathway via which animals can develop problematic behaviours, and the three steps involved in applying cognition to help mitigate these behaviours: (i) identifying the cue triggering the behaviour from the perspective of the animal, (ii) identifying the cognitive mechanism (e.g. neophobia, imprinting, social and associative learning) and (iii) targeting those processes within the constraints of both the animal and the context of cue. Cognition is likely to be most useful as a tool to help reduce the potential for perceptual traps. Avian habitat management, which is often based on the presumption that providing adequate structural habitat (i.e. vegetation) will lead to positive responses by birds, provides a useful example to demonstrate this possibility. Birds often do not use all available sites with seemingly optimal habitat for breeding, potentially due to social behaviours, in particular a lack of calling from conspecifics (Ahlering & Faaborg 2006). A cognitive approach could be used to increase the attractiveness, and hence use, of restored habitats (Fig. 2a). For example, Black-capped Vireo (Vireo atricapilla) settled into previously unoccupied sites in Texas after vocalizations were broadcast (Ward & Schlossberg

2004). The main threat to V. atricapilla (the brood parasitic brown-headed cowbird, Molothrus ater) was controlled and nesting success was high after 1 year of playbacks, and birds recolonized sites in the following year without playbacks, indicating a positive feedback loop had developed between nesting behaviour and breeding success. An enhanced response could be possible by providing food to settling birds as a form of positive reinforcement. Restored sites might lack suitable cues for habitat selection, or alternatively cues may be present indicating erroneously that they should be avoided, analogous to the example of scarecrows scaring birds from settling in arable fields. Encounters with humans can cause animals to change their distribution patterns, for example, loons (Gavia spp.) avoid areas with high shipping traffic in the German sea (Schwemmer et al. 2011). Restored habitats that are located in areas close to humans (e.g. around cities) could mean that animals experience a range of disturbances (e.g. light, noise). If these cues cause animals to avoid restored habitats that do not compromise their fitness, then reducing interactions with cues will be important (Fig. 2b). If this cue can be changed (e.g. by limiting traffic noise), then the focus will be on changing the avoidance response to one of indifference (Fig. 2b). The underlying cognitive method to do this is habituation, where exposure to consistent, ‘weak’ innocuous stimuli leads to a decrease in responsiveness to stimuli; this is often an adaptive response as it reduces the likelihood animals respond to harmless stimuli (Blumstein 2016). For example, traffic noise might provide birds with an erroneous indicator that restored habitats are of poorer quality than other alternatives, leading to them being avoided. If so, regular but low-level exposure to traffic noise could lead to habituation and eventually promote birds to no longer avoid noisy restored habitats if there are no fitness costs to these decisions (Fig. 2b). In a similar vein, managers could

Fig. 2. Applying cognitive theory to manipulate cues to reduce avoidance of restored habitats. Simplified pathways modified from fig. 2 in Greggor et al. (2014) showing how maladaptive behaviours could be managed when: (a) birds avoid restored sites because of the absence of calls from conspecifics and (b) birds avoid restored sites because of traffic noise. © 2016 The Authors. Journal of Applied Ecology © 2016 British Ecological Society, Journal of Applied Ecology, 54, 1478–1486

Maladaptive behaviours can constrain restoration reduce the impacts of human disturbance on waterbirds by deliberately promoting habituation (Nisbet 2000). Using cognition to mitigate maladaptive habitat selection behaviour may not be possible in all cases due to the behavioural characteristics of animals, or a lack of knowledge about the likely applicability of different cognitive mechanisms for particular situations. At the least though, Greggor et al. (2014) provide a useful way of thinking clearly and systematically about the underlying mechanisms of maladaptive habitat selection (e.g. what cues are and how they are perceived), and some of the ways problematic behaviours could be changed.

Management implications Habitat restoration has an important role to play in ameliorating the effects of anthropogenic disturbance on animals, but many factors can constrain or overwhelm how animals respond to these efforts. Animal behaviour is rarely considered when assessing the success of habitat restoration (Lindell 2008), but failing to understand how animals perceive, respond to and utilize habitats could be a key cause of failure. Eliminating the potential that ecological and perceptual traps constrain restoration requires strong links between habitat quality and habitat selection so animals can adaptively select habitats. Knowledge about what represents functional habitat for animals, the behaviours that animals use to assess habitat quality, and how restoration might change both habitat quality and habitat selection cues is, therefore, required. The Umwelt concept and resource-based habitat approaches can help researchers and managers take a more animal-centric view of habitats in the context of restoration, particularly in terms of the key characteristics that restored habitats must have to be suitable for animals. Similarly, cognitive theory may be a useful way to better understand the process via which animals select habitats and to ameliorate problematic behaviours, such as avoidance of good restored habitats, as they arise. Our review provides conceptual guidance for ensuring that strong links exist between habitat quality and habitat selection, an important component of successful habitat restoration that has thus far received limited attention. We hope this will stimulate further discussion and strengthen links between the fields of evolutionary, behavioural and restoration ecology.

Authors’ contributions Both authors developed, wrote and revised the manuscript.

Acknowledgements We thank Rhys Coleman, Paul Reich, Dan Blumstein and an anonymous reviewer for insightful comments that helped improve the manuscript. We acknowledge funding from Melbourne Water, the Centre for Aquatic Pollution, Identification and Management, and the Australian Research Council (LP140100343).

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