Comparative cognition for conservationists
Authors: Alison L. Greggor, Nicola S. Clayton, Ben Phalan, Alex Thornton
Journal: Trends in Ecology & Evolution (2014)

•Animal behaviour affects conservation and is driven by underlying cognition.•Using cognitive principles can modify behaviour across taxonomic groups.•We discuss concepts previously unexplored in conservation contexts.•We create a novel guide for applying cognition to diverse conservation issues. Every animal occupies a unique cognitive world based on its sensory capacities, and attentional and learning biases. Behaviour results from the interaction of this cognitive world with the environment. As humans alter environments, cognitive processes ranging from perceptual processes to learned behaviour govern animals' reactions. By harnessing animals' perceptual biases and applying insights from cognitive theory, we can purposefully alter cues to reduce maladaptive responses and shape behaviour. Despite the fundamental connection between cognition and behaviour, the breadth of cognitive theory is underutilised in conservation practice. Bridging these disciplines could augment existing conservation efforts targeting animal behaviour. We outline relevant principles of perception and learning, and develop a step-by-step process for applying aspects of cognition towards specific conservation issues. Every animal occupies a unique cognitive world based on its sensory capacities, and attentional and learning biases. Behaviour results from the interaction of this cognitive world with the environment. As humans alter environments, cognitive processes ranging from perceptual processes to learned behaviour govern animals' reactions. By harnessing animals' perceptual biases and applying insights from cognitive theory, we can purposefully alter cues to reduce maladaptive responses and shape behaviour. Despite the fundamental connection between cognition and behaviour, the breadth of cognitive theory is underutilised in conservation practice. Bridging these disciplines could augment existing conservation efforts targeting animal behaviour. We outline relevant principles of perception and learning, and develop a step-by-step process for applying aspects of cognition towards specific conservation issues. Why cognition?Ethology is an important component of conservation [1Candolin U. Wong B.B.M. Behavioural Responses to a Changing World; mechanisms and consequences. Oxford University Press, 2012Crossref Scopus (83) Google Scholar]. Behaviour drives ecological patterns, such as dispersal and predator–prey interactions, thereby affecting the distribution of species and influencing ecosystem functioning. Many urgent animal conservation issues (e.g., eradicating invasive species [2Sutherland W.J. et al.A horizon scan of global conservation issues for 2014.Trends Ecol. Evol. 2014; 29: 15-22Abstract Full Text Full Text PDF PubMed Scopus (81) Google Scholar]) depend upon successfully manipulating behaviour. But what ultimately shapes behavioural patterns? Behaviour is an interaction with the environment stemming from what animals perceive, learn, remember, and decide to do; all of which make up cognition in its widest sense [3Shettleworth S. Cognition, Evolution, and Behaviour. Oxford University Press, 2010Google Scholar] (see Glossary). Cognitive mechanisms therefore underlie behavioural responses, and are central to understanding behaviour in conservation contexts (Figure 1).Animal conservation incorporates diverse policies and wildlife management methods, and some, including reintroductions [4Urbanek R.P. et al.Reintroduction techniques: post-release performance of 54 sandhill cranes (1) released into wild flocks and (2) led on migration by ultralight aircraft.Proc. North Am. Crane Work. 2005; 9: 203-211Google Scholar], trapping [5Phillips R.B. Winchell C.S. Reducing nontarget recaptures of an endangered predator using conditioned aversion and reward removal.J. Appl. Ecol. 2011; 48: 1501-1507Crossref Scopus (12) Google Scholar], invasive species mitigation [6O'Donnell S. et al.Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader.J. Appl. Ecol. 2010; 47: 558-565Crossref Scopus (114) Google Scholar], and deterrents [7Schakner Z.A. Blumstein D.T. Behavioral biology of marine mammal deterrents: A review and prospectus.Biol. Conserv. 2013; 167: 380-389Crossref Scopus (40) Google Scholar] rely on manipulating animals' behavioural responses. These interventions could be improved with insights from comparative cognition. For example, avian collisions with human-made structures kill millions of birds every year – including threatened and endangered species [8Drewitt A.L. Langston R.H.W. Collision effects of wind-power generators and other obstacles on birds.Ann. N. Y. Acad. Sci. 2008; 1134: 233-266Crossref PubMed Scopus (160) Google Scholar] – and are linked to population decline [9Phipps W.L. et al.Do power lines and protected areas present a catch-22 situation for cape vultures (Gyps coprotheres)?.PLoS ONE. 2013; 8: e76794Crossref PubMed Scopus (27) Google Scholar]. Existing solutions, like strategically placing [8Drewitt A.L. Langston R.H.W. Collision effects of wind-power generators and other obstacles on birds.Ann. N. Y. Acad. Sci. 2008; 1134: 233-266Crossref PubMed Scopus (160) Google Scholar], or altering structures [10Alonso J.C. et al.Mitigation of bird collisions with transmission lines through groundwire marking.Biol. Conserv. 1994; 67: 129-134Crossref Scopus (58) Google Scholar], have had only limited success [11Martin G.R. Understanding bird collisions with man-made objects: a sensory ecology approach.Ibis (Lond. 1859). 2011; 153: 239-254Crossref Scopus (140) Google Scholar]. Crucially, wind farm deterrents will only be effective if they are reliably perceived, and rapidly learned; both of which are facets of cognition. Cognitive theory can thus help predict how best to manipulate and exploit attentional biases, innate responses, and learning tendencies to enhance conservation efforts. Because basic cognitive principles can be applied throughout the animal kingdom, these tactics can be used to address diverse problems.Although elements of cognition have been explored in conservation contexts [12Sih A. et al.Evolution and behavioural responses to human-induced rapid environmental change.Evol. Appl. 2011; 4: 367-387Crossref Scopus (699) Google Scholar, 13Brown C. Experience and learning in chaning environments.in: Candolin U. Wong B. Behavioural Responses to a Changing World; Mechanisms and Consequences. Oxford University Press, 2012: 46-62Google Scholar, 14Sih A. Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview.Anim. Behav. 2013; 85: 1077-1088Crossref Scopus (327) Google Scholar], discussions that integrate the breadth of cognitive theory in applied conservation contexts are lacking. Below, we outline the range of cognitive principles that can be used by conservationists, at each stage of problematic behaviour (Figure 1). Specifically, we discuss perceptual principles that influence behaviour towards novel cues, and emphasise the role of learning in determining repeated responses. Different mitigation tactics may be required for maladaptive behaviours that originate from attraction or aversion to novel cues. We conclude with a guide to applying these concepts (Figure 2) and with several case studies illustrating potential solutions.Figure 2Applying cognition. Guides the reader through the three steps of cue manipulation to change a problematic behaviour: (1) cue assessment; (2) identifying relevant cognitive mechanisms; and (3) applying cognitive theory to the specific problem. See case studies and supplementary material for examples. When groups of stimuli occur, use the same cognitive strategy at every location and occurrence to promote generalisation.View Large Image Figure ViewerDownload (PPT)Cognition as adaptationAnimals possess perceptual biases and specialisations in learning and memory that have evolved in response to the specific challenges of their ancestral environments [3Shettleworth S. Cognition, Evolution, and Behaviour. Oxford University Press, 2010Google Scholar]. Human-induced rapid environmental change (HIREC [12Sih A. et al.Evolution and behavioural responses to human-induced rapid environmental change.Evol. Appl. 2011; 4: 367-387Crossref Scopus (699) Google Scholar]) generates evolutionarily novel cues and potentially imposes strong selection pressures on these biases and specialisations. Cognitive adaptations can therefore be as powerful as morphological adaptations in helping or hindering animals when environments change. For example, a cognitive mechanism that causes avoidance of novel food is as encumbering as a specialised feeding apparatus that prevents an animal from eating that food. Identifying the cognitive biases of target species requires stepping outside our own sensory experience and evaluating the saliency of novelty from the perspective of animals [15Van Dyck H. Changing organisms in rapidly changing anthropogenic landscapes: the significance of the "Umwelt"-concept and functional habitat for animal conservation.Evol. Appl. 2012; 5: 144-153Crossref Scopus (60) Google Scholar]. Even though the cognitive biases of all species are not perfectly catalogued, fundamental perceptual and learning theories are highly relevant across species.Perception of noveltyHow animals perceive novel cues critically influences their response. Novel cues that resemble evolutionarily relevant cues are more likely to evoke common responses (i.e., the cue similarity hypothesis [12Sih A. et al.Evolution and behavioural responses to human-induced rapid environmental change.Evol. Appl. 2011; 4: 367-387Crossref Scopus (699) Google Scholar]) that can be adaptive (e.g., fleeing novel predators that resemble existing ones [16Blumstein D.T. The multipredator hypothesis and the evolutionary persistence of antipredator behavior.Ethology. 2006; 112: 209-217Crossref Scopus (210) Google Scholar]). This helps explain why introduced species are more successful in novel environments that are similar to their ancestral ones [17Blackburn T.M. Duncan R.P. Determinants of establishment success in introduced birds.Nature. 2001; 414: 195-197Crossref PubMed Scopus (262) Google Scholar]. However, when novel cues match relevant cues, but fail to produce beneficial outcomes, animals are at risk of perceptual errors and evolutionary traps (see [18Robertson B.a. et al.Ecological novelty and the emergence of evolutionary traps.Trends Ecol. Evol. 2013; 28: 552-560Abstract Full Text Full Text PDF PubMed Scopus (275) Google Scholar] for a recent review). For example, the colour, shape, and motion of plastic waste often resembles that of natural prey, provoking fishes, turtles, seabirds, and marine mammals to ingest them, with fatal consequences [19Derraik J.G.B. The pollution of the marine environment by plastic debris: a review.Mar. Pollut. Bull. 2002; 44: 842-852Crossref PubMed Scopus (2284) Google Scholar].CategorisationBoth adaptive and maladaptive responses to cue similarity can be explained through categorisation. Categorisation involves classifying or differentiating cues based upon perceptual or conceptual similarity [3Shettleworth S. Cognition, Evolution, and Behaviour. Oxford University Press, 2010Google Scholar], and allows novel cues to be processed and learned more quickly and efficiently [20Wasserman E.A. The conceptual abilities of pigeons.Am. Sci. 1995; 83: 246-255Google Scholar]. Although some animals can categorise disparate cues, generally novel cues that perceptually overlap with known cues are more easily classified. For example, prey more easily categorise novel predators that resemble native ones [21Ferrari M.C.O. et al.Generalization of learned predator recognition: an experimental test and framework for future studies.Proc. Biol. Sci. 2007; 274: 1853-1859Crossref PubMed Scopus (178) Google Scholar]. However this same process can lead to damaging miscategorisation. For example, buprestid beetles (Julodimorpha bakewelli) are attracted to beer bottles whose colour and contours mimic those of their mates [22Gwynne D.T. Rentz D.C.F. Beetles on the bottle: male buprestids mistake stubbies for females (Coleoptera).J. Aust. Entomol. Soc. 1983; 22: 79-80Crossref Scopus (86) Google Scholar]. Miscategorisation could be prevented by designing bottles of different colours and textures (i.e., 'cue disarming' [18Robertson B.a. et al.Ecological novelty and the emergence of evolutionary traps.Trends Ecol. Evol. 2013; 28: 552-560Abstract Full Text Full Text PDF PubMed Scopus (275) Google Scholar]).Humans have long exploited perceptual and categorisation errors to shape behaviour. We take advantage of them in household pest control with bug zappers and poisonous baits, but we can also use them for conservation purposes. Insight into the aspects of cues that evoke inappropriate behaviour allows us to reduce perceptual errors [18Robertson B.a. et al.Ecological novelty and the emergence of evolutionary traps.Trends Ecol. Evol. 2013; 28: 552-560Abstract Full Text Full Text PDF PubMed Scopus (275) Google Scholar]. For example, using lamps with larger wavelengths could help reduce the impact of human-made lights on moths [23Van Langevelde F. et al.Effect of spectral composition of artificial light on the attraction of moths.Biol. Conserv. 2011; 144: 2274-2281Crossref Scopus (194) Google Scholar], and simple alterations to lighthouses and oil rigs can prevent birds from succumbing to artificial light cues [24Poot H. et al.Green light for nocturnally migrating birds.Ecol. Soc. 2008; 13: 1-14Google Scholar, 25Jones J. Francis C.M. The effects of light characteristics on avian mortality at lighthouses.J. Avian Biol. 2003; 34: 328-333Crossref Scopus (72) Google Scholar]. Nevertheless, conservationists need to explore solutions beyond reducing perceptual errors because they represent but a small fraction of possible cognitive manipulations. Fundamentally, much behaviour is not driven by automatic responses to cue similarity, but by experiences with cue novelty.NeophobiaFearing or failing to fear human-made cues can generate problematic behaviour. Negative emotional responses to novel cues, termed neophobia, are adaptive in helping animals avoid unknown dangers [26Greenberg R. Mettke-Hofmann C. Ecological aspects of neophobia and neophilia in birds.in: Current Ornithology. vol. 16. Springer, 2001: 119-178Google Scholar]. However, when humans produce novelty, high levels of neophobia can prevent adaptive responses, such as inhibiting animals from incorporating new foods into their diet [27Marples N.M. et al.Responses of wild birds to novel prey: evidence of dietary conservatism.Oikos. 1998; 83: 161-165Crossref Scopus (132) Google Scholar], whereas low neophobia levels can aid in invading novel habitats [28Sol D. et al.Exploring or avoiding novel food resources? The novelty conflict in an invasive bird.PLoS ONE. 2011; 6: e19535Crossref PubMed Scopus (155) Google Scholar]. The extent to which neophobia produces avoidance behaviour depends upon the species [26Greenberg R. Mettke-Hofmann C. Ecological aspects of neophobia and neophilia in birds.in: Current Ornithology. vol. 16. Springer, 2001: 119-178Google Scholar], the individual's temperament [29Réale D. et al.Integrating animal temperament within ecology and evolution.Biol. Rev. Camb. Philos. Soc. 2007; 82: 291-318Crossref PubMed Scopus (2161) Google Scholar], developmental stage, and experience [26Greenberg R. Mettke-Hofmann C. Ecological aspects of neophobia and neophilia in birds.in: Current Ornithology. vol. 16. Springer, 2001: 119-178Google Scholar, 30Marples N.M. et al.Deactivation of dietary wariness through experience of novel food.Behav. Ecol. 2007; 18: 803-810Crossref Scopus (45) Google Scholar]. Neophobia can be quantified in laboratory and field avoidance tests (e.g., [31Seferta A. et al.Learning differences between feral pigeons and zenaida doves: the role of neophobia and human proximity.Ecology. 2001; 107: 281-293Google Scholar]), therefore, measuring variation in neophobic behaviour within a population could predict how animals will respond to novel cues. With this information, the principles of neophobia can be applied to modify novel cues and increase or decrease fear responses.Increasing fear responses can reduce human–animal conflict in farming and fishing contexts. Animals raid farms and steal catches, creating conflict with humans that results in needless culling and negative attitudes towards wildlife, often reducing support for local conservation programmes [32Hill C.M. Human-Wildlife Conflict: Identifying the Problem and Possible Solutions. (Albertine Rift Technical Report Series, Vol. 1). Wildlife Conservation Society, 2002Google Scholar]. Capitalising on animals' adaptive fear responses by amplifying biologically relevant surprise and danger signals can reliably deter animals from feeding [7Schakner Z.A. Blumstein D.T. Behavioral biology of marine mammal deterrents: A review and prospectus.Biol. Conserv. 2013; 167: 380-389Crossref Scopus (40) Google Scholar], and tapping into neophobia could further enhance avoidance behaviour. For example, fear responses of animals to naturally aversive startle displays [33Olofsson M. et al.Deimatic display in the European swallowtail butterfly as a secondary defence against attacks from great tits.PLoS ONE. 2012; 7: e47092Crossref PubMed Scopus (34) Google Scholar] and alarm calls [3Shettleworth S. Cognition, Evolution, and Behaviour. Oxford University Press, 2010Google Scholar] would be amplified if combined with cues that elicit neophobia, such as moving and changing objects [34Corey D.T. The determinants of exploration and neophobia.Neurosci. Biobehav. Rev. 1978; 2: 235-253Crossref Scopus (144) Google Scholar]. Additionally, incorporating other naturally aversive stimuli into deterrents, such as noxious chemicals like chili powder [35Sitati N.W. Walpole M.J. Assessing farm-based measures for mitigating human-elephant conflict in Transmara District, Kenya.Oryx. 2006; 40: 279Crossref Scopus (113) Google Scholar] or quinine (e.g., [36Caller G. Brown C. Evolutionary responses to invasion: cane toad sympatric fish show enhanced avoidance learning.PLoS ONE. 2013; 8: e54909Crossref PubMed Scopus (19) Google Scholar]), might be effective (see [7Schakner Z.A. Blumstein D.T. Behavioral biology of marine mammal deterrents: A review and prospectus.Biol. Conserv. 2013; 167: 380-389Crossref Scopus (40) Google Scholar]).Although lessons from perception can manipulate initial reactions towards stimuli, shaping subsequent interactions requires an understanding of learning.LearningLearning is a change in cognitive state that results from experience [3Shettleworth S. Cognition, Evolution, and Behaviour. Oxford University Press, 2010Google Scholar]. Learning is crucial to conservation because it can allow animals to acquire appropriate behavioural responses to novel cues [37Garcia T.S. et al.Antipredator behavior of american bullfrogs (Lithobates catesbeianus) in a novel environment.Ethology. 2012; 118: 867-875Crossref Scopus (17) Google Scholar] (Box 1). Basic learning abilities are ubiquitous, but what, when, and how animals learn depends upon several factors. Evolved learning biases can direct attention towards adaptive cues, but only if evolutionarily relevant cues are preserved [13Brown C. Experience and learning in chaning environments.in: Candolin U. Wong B. Behavioural Responses to a Changing World; Mechanisms and Consequences. Oxford University Press, 2012: 46-62Google Scholar]. Learning biases can favour certain sensory modalities. For example, animals more easily associate nausea with a taste than a shock or a light (Garcia effect [38Garcia J. et al.Behavioral regulation of the milieu interne in man and rat.Science. 1974; 185: 824-831Crossref PubMed Scopus (751) Google Scholar]). Natural selection has directed attention towards taste cues around food because taste more reliably predicts the presence and quantity of toxins. Generally, experiences that are more biologically relevant and perceptually salient are learned faster than less relevant ones [3Shettleworth S. Cognition, Evolution, and Behaviour. Oxford University Press, 2010Google Scholar].Box 1How learning can reduce impacts of invasive speciesMajor goals of conservation biology are to preserve species and to maintain genetic diversity within species. Greater genetic diversity allows species to respond adaptively to future environmental changes, even if such adaptation is learning dependent [14Sih A. Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview.Anim. Behav. 2013; 85: 1077-1088Crossref Scopus (327) Google Scholar]. However, novel selection pressures, such as those posed by HIREC, can reduce the genetic diversity of affected species.Populations of many predatory species are at risk in Australia where the toxic cane toad (Rhinella marina) has invaded large portions of the country and is often mistaken as prey. Some predator populations, such as the red-bellied black snake (Pseudechis porphyriacus), have persisted through the selective survival of individuals that are morphologically preadapted with smaller jaws; restricting their ability to consume large enough toads to be poisoned [64Phillips B. Shine R. An invasive species induces rapid adaptive change in a native predator: cain toads and black snakes in Australia.Proc. R. Soc. B: Biol. Sci. 2006; 273: 1545-1550Crossref PubMed Scopus (182) Google Scholar]. Other species, such as the common planigale (Planigale maculata) (Figure I) and crimson spotted rainbow fish (Melanotaenia duboulayi) [36Caller G. Brown C. Evolutionary responses to invasion: cane toad sympatric fish show enhanced avoidance learning.PLoS ONE. 2013; 8: e54909Crossref PubMed Scopus (19) Google Scholar] use food aversion learning to avoid poisoning after ingesting nonfatal amounts of toad toxin [65Webb J. et al.A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid a toxic invader.Aust. Ecol. 2008; 33: 821-829Crossref Scopus (85) Google Scholar]. Although the planigale and rainbow fish have still suffered losses – and comparisons between populations of rainbow fish in areas with and without invasive cane toads show evidence of selection for aversion learning [36Caller G. Brown C. Evolutionary responses to invasion: cane toad sympatric fish show enhanced avoidance learning.PLoS ONE. 2013; 8: e54909Crossref PubMed Scopus (19) Google Scholar] – their losses are less drastic than for toad-eating snakes [66Covacevich J. Archer M. The distribution of the cane toad, Bufo marinus, in Australia and its effect on indigenous vertebrates.Mem. Queensl. Museum. 1975; 17: 305-310Google Scholar], and less phenotypically discriminating than species that undergo rapid morphological evolution. Aversion learning requires initially ingesting a nonfatal amount of toxin, therefore, survival is determined more by the size of the toad or tadpole encountered than by a specific phenotype [67Brown R.L. Learning, evolvability and exploratory behaviour: extending the evolutionary reach of learning.Biol. Philos. 2013; 28: 933-955Crossref Scopus (11) Google Scholar]. Therefore, learned behavioural responses could help maintain genetic diversity [67Brown R.L. Learning, evolvability and exploratory behaviour: extending the evolutionary reach of learning.Biol. Philos. 2013; 28: 933-955Crossref Scopus (11) Google Scholar] (see Figure S3 in the supplementary material online).Figure IA planigale encountering a cane toad. Reproduced with permission from Jonathan Webb.View Large Image Figure ViewerDownload (PPT)Although learning without human intervention might buffer certain species against diversity losses [67Brown R.L. Learning, evolvability and exploratory behaviour: extending the evolutionary reach of learning.Biol. Philos. 2013; 28: 933-955Crossref Scopus (11) Google Scholar], actively encouraging learning could help species and/or individuals that might otherwise fail to make life-saving associations. This has become clear for another declining Australian predator, the northern quoll (Dasyurus hallucatus), that failed to learn about the toad not because they lack learning abilities, but because they hunt boldly, attacking large toads and suffering fatal first encounters. Reintroduction efforts have successfully trained quolls through aversive conditioning. Researchers coated small dead toads with nausea-inducing thiabendazole to foster an association of sickness with toads, thereby training released individuals to avoid natural encounters with the toads and survive [6O'Donnell S. et al.Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader.J. Appl. Ecol. 2010; 47: 558-565Crossref Scopus (114) Google Scholar]. It has been proposed that training baits could be aerially dropped in the wild to train populations about the toad before it arrives [6O'Donnell S. et al.Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader.J. Appl. Ecol. 2010; 47: 558-565Crossref Scopus (114) Google Scholar]. Through this method, targeting cognitive mechanisms to expedite learning could help protect a globally endangered species.HabituationHabituation, measured as a decrease in response to a repeated cue, is considered the simplest form of learning, and allows animals to filter irrelevant information [39Rankin C.H. et al.Habituation revisited: an updated and revised description of the behavioral characteristics of habituation.Neurobiol. Learn. Mem. 2009; 92: 135-138Crossref PubMed Scopus (889) Google Scholar]. Habituation is often used to describe the process of behaviourally adapting to anthropomorphic disturbance across contexts ranging from chronic noise [40Anderson P.A. et al.Sound, stress, and seahorses: the consequences of a noisy environment to animal health.Aquaculture. 2011; 311: 129-138Crossref Scopus (92) Google Scholar] to human visitors [41Ellenberg U. et al.Habituation potential of yellow-eyed penguins depends on sex, character and previous experience with humans.Anim. Behav. 2009; 77: 289-296Crossref Scopus (77) Google Scholar]. Different underlying processes can contribute to habituation between contexts, so animals might not tolerate shipping noise as readily as disruptions from tourists. The degree to which animals habituate has serious consequences for conservation programmes depending on the context. For example, crop deterrents will be less effective on animals that easily habituate, and animals that habituate poorly might be less tolerant to disturbances caused by habitat fragmentation.Habituation relies on experiencing predictable cues [3Shettleworth S. Cognition, Evolution, and Behaviour. Oxford University Press, 2010Google Scholar] and can be prevented by amplifying differences in cues between presentations and timing presentations unpredictably. For example, randomly rotating crop deterrents between objects of different colours, sizes, and shapes, and by pairing them with different sounds will help prevent habituation (however, deterrents must also produce aversive experiences or cue variation will still fail to deter, e.g., [42Muirhead S. et al.Roo-Guard® sound emitters are not effective at deterring tammar wallabies (Macropus eugenii) from a source of food.Wildl. Res. 2006; 33: 131-136Crossref Scopus (7) Google Scholar]). In promoting habituation to minimise the effects of human disturbance, predictability should be maximised. For example, ecotourists in areas with disturbance-sensitive animals could be encouraged to wear similar clothes, follow similar paths, and only visit at specific times of day.ImprintingImprinting is a specialised form of learning that occurs during a short sensitive period in development to create strong preferences for one's own species [43Immelmann K. Ecological significance of imprinting and early learning.Annu. Rev. Ecol. Syst. 1975; 6: 15-37Crossref Google Scholar], specific foods, habitats [44Davis J.M. Patterns of variation in the influence of natal experience on habitat choice.Q. Rev. Biol. 2008; 83: 363-380Crossref PubMed Scopus (63) Google Scholar], or sites [43Immelmann K. Ecological significance of imprinting and early learning.Annu. Rev. Ecol. Syst. 1975; 6: 15-37Crossref Google Scholar]. Imprinting can propagate parental behavioural patterns in future generations. For example, habitat imprinting can spread preferences for urban habitats, thereby facilitating animals' urbanisation [45Evans K.L. et al.A conceptual framework for the colonisation of urban areas: the blackbird Turdus merula as a case study.Biol. Rev. Camb. Philos. Soc. 2010; 85: 643-667PubMed Google Scholar]. Imprinting on evolutionarily novel cues can cause maladaptive behaviours. For instance, zebra finches (Taeniopygia guttata) solicit an incorrect mate after imprinting upon a different species [46Bischof H-J. Clayton N. Stabilization of sexual preferences by sexual experience in male zebra finches taeniopygia guttata castanotis.Behaviour. 1991; 118: 144-154Crossref Scopus (48) Google Scholar].Imprinting manipulations can aid conservation efforts – such as translocation programmes that depend upon animals preferring suitable environments [47Binder D. et al.Emergence, growth, ageing and provisioning of Providence petrel (Pterodroma solandri) chicks: implications for translocation.Emu. 2013; 113: 33Crossref Scopus (6) Google Scholar] – and are often used in salmonid (Salmonidae) release programmes [48Brown C. Day R.L. Th