ArticlePDF AvailableLiterature Review

Determinants of uncertainty in wildlife responses to human disturbance

October 2015
Biological reviews of the Cambridge Philosophical Society

October 2015

DOI:10.1111/brv.12224

Authors:

Zulima Tablado

Estación Biológica de Doñana CSIC

Lukas Jenni

Swiss Ornithological Institute

Outdoor recreation is increasing in intensity and space. Areas previously inaccessible are now being visited by ever-growing numbers of people, which increases human-wildlife encounters across habitats. This has raised concern among researchers and conservationists as, even in non-aggressive encounters, animals often perceive humans as predators and mount physiological and behavioural responses that can have negative consequences. However, despite all the research in recent decades, not many general patterns have emerged, especially at the level of populations, and many studies have yielded seemingly contradictory or inconclusive results. We argue that this is partly due to incomplete knowledge of the number and complexity of factors that may modulate the responses of animals. Thus, we aim to provide a conceptual approach intended to highlight the reasons that make it difficult to detect general patterns. We present a comprehensive compilation of factors modulating animal responses to humans at increasing levels (from sensory detection and immediate behavioural and physiological reactions, to changes in fitness and population trends), which may help understanding the uncertainty in the patterns. We observed that there are many modulating factors, which can be categorized as reflecting characteristics of the recreational activity itself (e.g. intensity of human presence), of the animals concerned (e.g. age or antipredatory strategy), and of the spatio-temporal context (e.g. habitat or timing of the encounter). Some factors appear to have non-linear and complex effects, which, if not considered, may lead to erroneous conclusions. Finally, we conclude that the difficulty in finding general patterns will be amplified at higher levels (i.e. at the level of populations), since as we proceed from one level to the next, the number of potential modulating factors accumulates, adding noise and obscuring direct associations between recreation and wildlife. More comprehensive knowledge about which (and how) factors affect animal responses across levels will certainly improve future research design and interpretation, and thus, our understanding of human recreational impacts on wildlife.

Conceptual model showing the different levels in the

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Biol. Rev. (2017), 92, pp. 216–233. 216

doi: 10.1111/brv.12224

Determinants of uncertainty in wildlife

responses to human disturbance

Zulima Tablado∗and Lukas Jenni

Swiss Ornithological Institute, Seerose 1, CH-6204, Sempach, Switzerland

ABSTRACT

Outdoor recreation is increasing in intensity and space. Areas previously inaccessible are now being visited by

ever-growing numbers of people, which increases human–wildlife encounters across habitats. This has raised concern

among researchers and conservationists as, even in non-aggressive encounters, animals often perceive humans as

predators and mount physiological and behavioural responses that can have negative consequences. However, despite

all the research in recent decades, not many general patterns have emerged, especially at the level of populations,

and many studies have yielded seemingly contradictory or inconclusive results. We argue that this is partly due to

incomplete knowledge of the number and complexity of factors that may modulate the responses of animals. Thus, we

aim to provide a conceptual approach intended to highlight the reasons that make it difﬁcult to detect general patterns.

We present a comprehensive compilation of factors modulating animal responses to humans at increasing levels (from

sensory detection and immediate behavioural and physiological reactions, to changes in ﬁtness and population trends),

which may help understanding the uncertainty in the patterns. We observed that there are many modulating factors,

which can be categorized as reﬂecting characteristics of the recreational activity itself (e.g. intensity of human presence),

of the animals concerned (e.g. age or antipredatory strategy), and of the spatio-temporal context (e.g. habitat or

timing of the encounter). Some factors appear to have non-linear and complex effects, which, if not considered, may

lead to erroneous conclusions. Finally, we conclude that the difﬁculty in ﬁnding general patterns will be ampliﬁed at

higher levels (i.e. at the level of populations), since as we proceed from one level to the next, the number of potential

modulating factors accumulates, adding noise and obscuring direct associations between recreation and wildlife. More

comprehensive knowledge about which (and how) factors affect animal responses across levels will certainly improve

future research design and interpretation, and thus, our understanding of human recreational impacts on wildlife.

Key words: human disturbance, recreational activities, vertebrates, adrenocortical response, ﬂight initiation distance,

stress response, survival, reproduction, spatial use, population growth.

CONTENTS

I. Introduction .............................................................................................. 217

II. Level 1: Sensory detection of human approach .......................................................... 222

(1) Mechanisms .......................................................................................... 222

(2) Modulators ........................................................................................... 222

III. Level 2: Physiological and behavioural responses to human presence .................................... 223

(1) Mechanisms .......................................................................................... 223

(2) Modulators ........................................................................................... 223

IV. Level 3: Impacts of recreational activities on ﬁtness and space use ....................................... 225

(1) Mechanisms .......................................................................................... 225

(2) Modulators ........................................................................................... 226

V. Level 4: Consequences of human disturbance for animal populations and species ....................... 227

(1) Mechanisms .......................................................................................... 227

(2) Modulators ........................................................................................... 227

VI. Conclusions .............................................................................................. 228

VII. Acknowlegdements ....................................................................................... 228

VIII. References ................................................................................................ 229

* Address for correspondence (Tel: +41 414629927; E-mail: Zulima.Tablado@vogelwarte.ch).

Modulators of wildlife response to recreation 217

I. INTRODUCTION

Outdoor recreational activities have increased dramatically

over the past decades (Boyle & Samson, 1985; Balmford

et al., 2009). Natural habitats and species that remained

relatively undisturbed in the past are now being visited by

an ever-increasing number of tourists (Balmford et al., 2009;

Buckley, 2009; Carney & Sydeman, 1999). The development

of technologies and transportation has allowed humans to

reach areas that were previously inaccessible to most people,

such as Antarctica, underwater habitats, or rainforests

(Sinclair & Jayawardena, 2010; Tisdell, 2010; Ríos-Jara

et al., 2013). This trend, together with the ever-decreasing

amount of ‘natural’ areas, calls for a deeper understanding

of the effects that human–nature interactions may impose

on wildlife species around the world (Buckley, 2004b;Bejder,

2005; Arlettaz et al., 2007; Price, 2008). Many authors

have investigated various responses of animals to human

disturbance; however, most have focused on single species or

on single locations (van der Zande & Vos, 1984; Harper

& Eastman, 2000; Bolduc & Guillemette, 2003; Thiel

et al., 2008). Most studies measured changes in behaviour

or hormones as a direct response to human disturbance

without further investigating possible consequences for

demographic rates, population size or species resilience

(Gill, Norris & Sutherland, 2001; Stankowich & Blumstein,

2005; Breuner, Patterson & Hahn, 2008; Bonier

et al., 2009).

Despite the interest and concern directed towards this

subject in the last few decades, not many general patterns

have emerged. The ﬁndings to date are often inconclusive

or in disagreement, especially concerning consequences of

human disturbance for animal ﬁtness parameters or popu-

lation trends (Burger, Gochfeld & Niles, 1995; Price, 2008;

Bonier et al., 2009). We suggest that this difﬁculty in ﬁnding

patterns is in part due to an incomplete understanding of the

mechanisms linking animal responses to human disturbance

and, perhaps more importantly, to insufﬁcient knowledge

of the factors modulating the response mechanisms. We also

suggest that these factors sometimes modify animal responses

to disturbance in complex non-linear ways that have been

largely overlooked. Moreover, the combined effect of several

modulating factors could largely obscure the effects of human

activities. Therefore, to obtain a better insight into the effect

of human recreational activities on wildlife, a comprehensive

understanding of the modulating factors is necessary. Our

objective in this review is to present an overview of the

modulating factors and mechanisms that underlie responses

of wildlife to encounters with humans at multiple levels of

complexity.

To do so, we present a conceptual scheme (Fig. 1) that

integrates the different levels in human–wildlife interactions,

beginning with detection of recreationists by animals,

and followed by immediate physiological or behavioural

responses, consequences at the level of individual ﬁtness

and habitat use, and subsequent impacts on populations or

species. It is not our intention to describe exhaustively the

Fig. 1. Conceptual model showing the different levels in the

process of interaction between recreationists and wildlife. The

resultant responses of animals to human disturbance can be

modulated by factors depending on the source of the disturbance

(i.e. characteristics of human activity), on properties of the

animal, and on the spatio-temporal context (e.g. habitat, climate,

timing). Decreases in the width of the green/black arrows,

as we go down the diagram, represent the dilution of the

association between human disturbance and animal response,

due to confounding effects of the accumulation of modulating

factors across levels.

mechanisms of response of disturbed animals (for that see,

for example, Sapolsky, Romero & Munck, 2000; Romero,

2004; Bejder, 2005; Breuner et al., 2008; Bejder et al., 2009;

Bonier, 2012), but rather to focus on factors that may alter

the expected patterns of response. At each level we ﬁrst

present a synthesis of the mechanisms of response; we then

identify factors that may modulate those mechanisms, and

the type of effects they may cause (i.e. ampliﬁcation or

attenuation, in a linear or non-linear manner), according

to what has been described, so far, in the literature (Table 1

and Fig. 2).

We classify the modulating factors into three different

categories: (i) factors dependent on the humans themselves

(e.g. number and frequency of people visiting an area

or the nature of the recreational activity), (ii) intrinsic

characteristics of the animals being disturbed, such as their

antipredatory strategy or sex, and (iii) modulators depending

on the spatio-temporal context in which the disturbance

takes place (e.g. season, climate or habitat). Although the

modulating factors and mechanisms act at speciﬁc levels,

these levels are not independent of each other (Fig. 1).

218 Zulima Tablado and Lukas Jenni

Table 1. Summary of factors modulating animal responses to human recreation activities at different levels

Levels Mechanisms Modulators

LEVEL 1a

Human Intrinsic Spatio-temporal context

Visual, hearing, olfactory

activation

Size (e.g. human

group size)

+[1] Sensory abilities (e.g.

larger versus smaller

species)

+[2– 4] Time of day (changes

in sensorial abilities

and vigilance

during the day)

A[5–7]

Colouration

(conspicuity)b

+[8– 10] Vigilance +[11– 13] Habitat characteristics

(vegetation density

and topography)

−[14– 16]

Noise (volume) +[17,18] Previous experience

(i.e. learn to better

recognize and be

more vigilant)

+[19– 21] Climate (cloud, rain,

etc. reducing

disturbance

detection)

−[22– 24]

Odour +[25– 28] Social aggregation +[13,29] Relative position of

disturbance to

animal (e.g.

perching height)

+[30,31]

Rate of movement +[32,33]

Proximity +[14,34]

LEVEL 2a

Human Intrinsic Spatio-temporal context

Behavioural changes (Behav),

physiological responses, i.e.

corticosteroid reactivity

(Cort), heart rate (HR)

Size (e.g. human

group size)

+[1,35] Antipredator strategy:

passive (hiding,

crypticity) versus

active (ﬂushing,

ﬁghting)

B [36– 38] Time of day

(circadian,

ultradian)

K[39–42]

Colouration

(difference from

animal)b

+[10] Previous experience

(with humans and

natural predators)

C [37,43– 49] Time of year (e.g.

breeding season,

moulting)

L [40,50– 52]

Noise (volume, type) +[18,53,54] Cognitive aptitudes −[55] Habitat characteristics

(vegetation density)

−[14,16,56– 58]

Speed of movement +[59,60] Flushing performancecD [37,48,61–66] Climate (i.e. direct

effect of

temperature)

−[14,65]

Proximity +[37,67] Offspring value and

parental care (as

determined by, for

example, mating

system, breeding

season length and

survival rates)

E [68– 73] Relative position of

disturbance to

animal (e.g.

perching height)

−[58,74– 76]

Directness of human

approach and gaze

+[59,60,77,78] Social aggregation F [14,37,79 – 81] Predation pressure +[82– 84]

Unpredictability +[34,85– 87] Mass-speciﬁc

metabolic rates

+[88] Concomitant stressful

events (e.g. extreme

weather agonistic

or predator

encounters)

+[89– 92]

Modulators of wildlife response to recreation 219

Table 1. Continued

Levels Mechanisms Modulators

Type (i.e.

aggressiveness or

similarity to

predators, hearing

versus seeing

humans)

+[25,93– 95] Sex and reproductive status (e.g.

effects through sexual

hormones)

G [64,75,96– 107]

Body condition (e.g. due to high

density of conspeciﬁcs, poor

habitat)

H [72,108– 110]

Coping style (due to selection,

neonatal development,

perinatal stress exposure, social

rank, etc.)

I [111– 114]

Age (developmental)dJ [72,75,84,115– 121]

LEVEL 3

Human Intrinsic Spatio-temporal context

Decrease in reproduction,

decrease in survival,

space-use changes,

chronic stress

Intensity (amount of

visitors)

+[122,123] Social aggregation M [124– 128] Timing of the disturbance (e.g.

periods of higher vulnerability

of nest abandonment, HPA

axis maturation)

+[129– 131]

Frequency or

continuity

+[126,132– 134] Cognitive aptitudes (smarter

animals will learn to recognize

faster non-consumptive

recreation activities, avoiding

chronic stress)

−[55,135] Habitat quality (e.g. food

availability, offspring

concealment) and its value

relative to alternative areas.

−[43,136– 138]

Energetic constraints (limited

compensation for

disturbance-induced energy

loss; e.g. migratory birds)

+[118– 120] Predation pressure +[130,139]

Body condition (body reserves to

buffer negative effects of

disturbance)

N [43,138,140,141] Climate (i.e. harsh weather and

climatic conditions)

+[129,142– 144]

Coping style (due to selection,

neonatal development,

perinatal stress exposure, social

rank, etc.)

O [43,90,145]

Previous investment in an area P [43,138]

LEVEL 4

Human Intrinsic Spatio-temporal context

Decreases in

demographic rates

leading to population

decreases, increased

extinction risk and

changes in distribution

Spatial and temporal

scale

+[146– 148] Life-history traits (e.g. a higher

number of reproductive

attempts, higher survival may

compensate for negative

medium-term responses)

−[149– 151] Concomitant deterioration of

habitate

+[152– 154]

Ecological generality

of the disturbance

Q [155– 158] Site ﬁdelity and philopatry (low

plasticity or learning ability to

avoid disturbed areas)

R [159– 162] Concomitant changes in

disturbance-independent

factors (e.g. climate change,

migration patterns, invasions

overriding the effects of human

disturbance)

T [163– 167]

220 Zulima Tablado and Lukas Jenni

Table 1. Continued

Levels Mechanisms Modulators

Social aggregation +[125,168]

Density (through release from density-dependent negative effects) −[169– 171]

Meta-population dynamics (disturbed population is a source or a

sink)

S [172– 174]

Capacity to adapt (genetic/phenotypic variation, and phenotypic

plasticity)f

−[175– 177]

Sign columns indicate the direction of the effect of a given factor. For the more complex effects a capital letter is assigned which corresponds to a graph in Fig. 2, depicting the shape of the relationship. We

only included mechanism, effects and trends which have been already described in, suggested in, or emerge through combining, previous studies.

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aIn many cases previous research does not allow us to distinguish between the effects of human recreation on detection (level 1) from the effects on short-term behavioural/physiological response (level 2; see

for example the human factor ‘size’ for which we cited the same reference). Nevertheless, when possible, we emphasized this difference. A good example is the intrinsic factor ‘social aggregation’. A larger

group size facilitates the detection of humans and other predators; however, the effect of group size on the decisions of the animals to ﬂush away after detecting the disturbance is likely to be the opposite.

Some authors have found that animals in larger groups show a lower physiological response to stressors and tolerate for longer the approaching human before ﬂushing, when comparing alert distances, which

we use as a proxy of detection, with ﬂight initiation distance (FID). This could be due either to the dilution of risk in larger groups, or to group-dependent antipredator strategies, such as in some ﬁsh species.

In any case at too large aggregation densities the pattern can start to reverse and increases in arousal and general stress could increase again in some species.

bAnimals tend to see humans wearing bright/conspicuous colours earlier; however once detected the reaction of the animals towards those humans depends on their own coloration pattern. Some authors

have shown that animals tolerate humans better when dressed in colours similar to their own.

cAs the economics of ﬂeeing predicts, animals should escape only when the cost of staying is greater than the cost of ﬂushing away. In this line, animals with a lower ability to ﬂush, such as gravid females

or newborn individuals with reduced mobility, rely on crypsis/hiding and allow closer approach. As performance increases, FID also increases; however, FID decreases again in individuals whose escaping

ability is much higher than the risk of staying (e.g. In some species, the better locomotor performance of adults, allows them to rely more on last-minute escaping strategies than in the case of juveniles of the

same species).

dWe chose to consider age using a developmental perspective and not directly as days after birth in order to take into account the differences in physiological maturation between altricial and precocial

species (e.g. varying timing of the hypothalamic— pituitary— adrenal axis hyporesponsive period).

eIt is important to understand the difference between direct effects of human presence (e.g. tourists visiting penguin colonies) and the additional anthropogenic effects through habitat deterioration (e.g.

construction of roads or ski resorts).

fAdaptation to humans will be positive for a species, provided that it does not entail a concomitant relaxation of the anti-predator response to other non-human/real predators. Otherwise, excessive boldness

may be counterproductive for the species.

Modulators of wildlife response to recreation 221

Day Night

Time of day

Nocturnal

animals

Level 1:

Detection

Diurnal

animals

(A)

Passive ----------------> Active

Anti-predator strategy

Behav

(B)

Day Night

Time of day

Nocturnal

animals

Diurnal

animals

(K)

Body condition

Spatial change

(N)

Previous investment in the area

Demogr. process c hange

Chronic stress

Spatial change

(P)

Ecological extent of disturbance

Concomitant impact on

prey (or beneficial species)

Concomitant impact on

predators (or competitors )

(Q)

Source -------->Sink population

Meta-population dynamics

(S)

Concomitant changes in disturbance-

independent factors

Factors with positiv e impact on

the population/s

Factors with additional negative impact

(T)

Previous experience

Aggressive

(Natural predators, hunters)

Neutral or positive

(C)

Flushing per formanc e

(D)

Behav

Parental care per capita

Offspring value

(E)

Sex hormones (Masculine --> Feminine)

Parental care hormones

(G)

age (development)

Behav

Cort

(J)

Reactive/Shy --------> Proactive/Bold

Copying style

(I)

Body condition

Behav

Cort

(H)

Prebreed. Breeding Postbreed.

Time of year

(L)

(moult

in birds)

(R)

Site fidelity/philopatry

Change of

distribution

Population decrease and

extinction risk

Reactive/Shy --------> Proactive/Bold

Copying style

(O)

Social aggregation

Demogr. process c hange

Chronic stress

Spatial change

(M)

Social aggregation

(F)

Level 2: Physiologicala

behaviouralresponses

Level 2: Physiological and

behavioural response

Level 2: Physiological and

behavioural responses

Level 2: Physiologicaland

behavioural responses

Level 2:Physiologicaland

behaviouralresp

onses

Level 2: Physiological and

behaviouralre

sponses

Level2:Physiologicala

behavioural responses

Level 2: Physiological and

behavioural responses

Level2

:Physiologicaland

behavioural responses

Level 2:Physiologicala

behavioural responses

Level 2: Physiological and

behavioural responses

Level 3: C hanges i n fitnes s

andspaceu

Demogr. process c hange

Chronic stress

Level 3:Changes in fitness

and space use

Level 3:Changes infitn

ess

andspace use

Level 3:Changes in fitness

andspaceu

Level4:Population and

species trends

Level 4: Populationand

speciest

rends

Level 4: Populationand

species trends

Level 4: Populationand

species trends

Fig. 2. Schematic representation of complex associations between detection or responses of animals to direct human presence

and some modulating factors. Letters correspond to the relationship marked with the same letter in Table 1, where supporting

references can be found. As in Table 1, we only included relationships that have been documented in, suggested in, or can be

inferred from combining, the existing literature. Black and grey lines summarize the trends when all mechanisms within a given

level respond similarly to a factor; coloured lines indicate mechanism-speciﬁc associations to a factor (e.g. speciﬁc physiological

responses or behavioural responses within level 2). Cort =adrenocortical response; HR =heart rate; Behav =ﬂushing/escaping

distance; Demogr. =demographic.

222 Zulima Tablado and Lukas Jenni

That is, responses at a certain level will only happen if

the responses at previous levels have already taken place

(e.g. human disturbance can only have negative effects

on demographic rates if animals detect people and react

to them). This dependence on previous levels entails the

accumulation of modulating factors across levels, which

will generally lead to a weakening of the association

between disturbance and animal responses at higher levels

(see Fig. 1).

To support this conceptual model, we focus mainly on

studies of the effects of human recreation on vertebrate

species, especially birds, given the large representation of this

taxon in the disturbance literature (e.g. Keller, 1996; Carney

& Sydeman, 1999; Buckley, 2004a; Price, 2008; Steven,

Pickering & Castley, 2011). We also used complementary

literature from other ﬁelds, such as predation ecology,

urban wildlife, or laboratory-induced stress (e.g. Lima, 1993;

Møller, 2012; Elbaz et al., 2013). Our approach focuses

on disturbance caused by recreational activities with the

least alteration of the habitat (such as people walking or

cross-country skiing). In this way, we hope to extract the

direct responses of animals to the presence of humans.

Anthropogenic activities associated with substantial habitat

modiﬁcations, such as the construction of tourist resorts or

roads, will be assumed to amplify (i.e. modulate) the impact

of recreationists, and are included, therefore, as modulating

factors. We hope that the comprehensive overview given

here about the scope and inﬂuence of modulating factors

will serve to help future researchers identify variables

that need to be taken into account in the design and

interpretation of studies and, thereby, to provide a better

understanding of the effect of recreational activities on

wildlife.

II. LEVEL 1: SENSORY DETECTION OF HUMAN

APPROACH

(1) Mechanisms

As suggested by previous research, wild species may perceive

humans as predators (Frid & Dill, 2002; Beale & Monaghan,

2004b); however, for this to happen, animals must ﬁrst detect

them. What are the cues and mechanisms used by vertebrate

animals to detect the presence of humans? Wildlife perceive

humans (as well as predators) visually, auditorially, and

olfactorially (Utne-Palm, 2001; Smith, Kane & Popper, 2004;

Whittingham et al., 2004; Bates et al., 2007; Hagelin & Jones,

2007; Fernandez-Juricic et al., 2012), although, as we will see

later, the type and threshold of the sensory response will

vary according to factors such as the intensity of the human

signal, the taxon, and the environment. Detection of human

presence is typically characterized by an immediate orienting

reﬂex (also called ‘alert’ position) in which the animals cease

their current activity (feeding, singing, etc.) and focus their

senses on the anthropogenic stimulus, increasing vigilance

to gather further information about the potential threat and

assess the danger (Sokolov et al., 1963; Gabrielsen, Blix &

Ursin, 1985; Knight & Gutzwiller, 1995).

(2) Modulators

Many factors may modify the ability of animals to detect

recreationists (Table 1 and Fig. 2). First, detection likelihood

depends on the obviousness of the anthropogenic presence

in itself, such as the number of people approaching, clothing

colour (Cuthill et al., 2005; Gomez & Thery, 2007), noise

level (Karp & Root, 2009; Margalida et al., 2011), odour

(e.g. presence or absence of pet species) (Miller, Knight &

Clinton, 2001; Bates et al., 2007; Roth, Cox & Lima, 2008),

distance (Miller et al., 2001; Fernandez-Juricic, Jimenez

& Lucas, 2002), and speed of movement (Siegel, 1972;

Ewert et al., 2001). That is, animals will more easily sense

humans if they are in larger groups, conspicuously dressed,

louder, smell stronger, and are moving fast or in close

proximity.

Second, the intrinsic properties of the species and

individuals being approached will also affect the likelihood of

detection. Among these intrinsic characteristics are variation

in sensory abilities (e.g. raptors have better vision than other

bird species, larger animals have a larger range of detection

than smaller ones) (Kiltie, 2000; Jones, Pierce & Ward,

2007), vigilance effort (which may vary with an individual’s

body condition or reproductive status) (Fernandez-Juricic

& Schroeder, 2003; Beauchamp, 2010), previous experience

(i.e. individuals may learn better to recognize human

presence) (Utne-Palm, 2001; Kelley & Magurran, 2003),

and degree of gregariousness (animals in larger social groups

usually have a structured sentinel system leading to a higher

overall vigilance level and probability of detection) (Schaik

et al., 1983; Beauchamp, 2010). The last category of factors

inﬂuencing detection is related to the spatio-temporal con-

text of human–wildlife interaction. For example, time of the

day, habitat characteristics, weather conditions and relative

position of the animal to the recreational activity will deter-

mine whether animals detect people or not. Time of day will

inﬂuence not only light levels and other environmental char-

acteristics that may inﬂuence the ability to detect humans,

but also the level of awareness and sensory ability of animals

(e.g. nocturnal animals have senses and activity patterns

better adapted for night life while it is the opposite for diurnal

species) (Gordon, Dickman & Thompson, 2010; Amo, Caro

& Visser, 2011; Elbaz et al., 2013). Characteristics of the

habitat (i.e. vegetation density and pronounced topography),

together with weather conditions, such as precipitation or

fog, will also limit the detection ability of animals, as they may

decrease visibility, odour and sound transmission (Lazarus

& Symonds, 1992; Hilton, Ruxton & Cresswell, 1999;

Fernandez-Juricic et al., 2002; Whittingham et al., 2004;

Carere et al., 2009; Martin, 2011). Finally, the position of

people relative to the animal may also affect detection, that is,

for instance animals resting/nesting high in trees may have a

larger range of visibility than ground dwellers (Moreno, 1984;

Carlson, 1985).

Modulators of wildlife response to recreation 223

III. LEVEL 2: PHYSIOLOGICAL AND

BEHAVIOURAL RESPONSES TO HUMAN

PRESENCE

(1) Mechanisms

When human presence is detected, the sensory response

(and the corresponding alert reﬂex) may be followed by

a behavioural and physiological anti-predatory response

(Gabrielsen & Smith, 1995; Berger et al., 2007; Blumstein,

2010), depending on the degree to which human presence

is perceived as a threat. Behaviourally, this reaction may be

passive or active. That is, upon perception of a threat, an

individual will evaluate the situation and respond accordingly

by relying on staying still and not being seen (i.e. hide or

freeze and remain cryptic) or by actively escaping from or

ﬁghting the threat (Lima & Dill, 1990; Lima, 1993; Bracha,

2004).

At the physiological level, there are almost instantaneous

increases in the secretion of acetylcholine and catecholamines

from the autonomic nervous system (Fisher, 1990; Knight

& Gutzwiller, 1995; Sapolsky et al., 2000; Romero & Butler,

2007), and corticotropin-releasing hormone (CRH) from the

hypothalamus in the brain (Sapolsky et al., 2000; Reeder

& Kramer, 2005). These secreted substances contribute

importantly to passive or active behavioural reactions

by decreasing or increasing locomotion, cardiovascular

activity, oxygen consumption, glucose mobilization, and

body temperature (Fisher, 1990; Knight & Gutzwiller,

1995; Wingﬁeld et al., 1997; Sapolsky et al., 2000). They also

produce temporary interruptions of reproductive behaviour

and appetite during stressful events (Sapolsky et al., 2000;

Wingﬁeld & Sapolsky, 2003). Simultaneously, there is an

activation of the immune system through the release of

cytokines in preparation for potential injuries and infections

(Wingﬁeld et al., 1997; Sapolsky et al., 2000; Wingﬁeld &

Sapolsky, 2003; Romero, Dickens & Cyr, 2009).

In addition to its role in the immediate arousal reaction,

the release of CRH triggers the slower adrenocortical stress

response (Sapolsky et al., 2000; Romero, 2004) through the

activation of the hypothalamic–pituitary–adrenal (HPA)

axis (or the homologous hypothalamic–pituitary–interrenal

axis, depending on the vertebrate taxon) (Sapolsky et al., 2000;

Rollins-Smith, 2001; Øverli et al., 2007; Gasser, Lowry &

Orchinik, 2009; Wingﬁeld, 2013). Thus, hypothalamic CRH

promotes the secretion of adrenocorticotropic hormone

(ACTH) from the pituitary gland (also called hypophysis)

which in turn stimulates the adrenal cortex to increase

production of corticosteroids (CORT; mainly cortisol in ﬁsh

and most mammals and corticosterone in birds, reptiles,

amphibians, and many rodents) (Sapolsky et al., 2000;

Romero, 2004; Reeder & Kramer, 2005). The stress-induced

levels of CORT start to be detected in plasma a few minutes

after disturbance and exert numerous effects throughout

the body. These effects will depend on the abundance

and distribution of CORT receptors in different organs

(Bellingham, Sar & Cidlowski, 1992; Kapoor et al., 2006;

Crespi et al., 2013; Lattin et al., 2015) and the action of CORT

binding globulins (a plasma protein that binds CORT with

high afﬁnity and can regulate CORT delivery and availability

at speciﬁc sites) (Breuner & Orchinik, 2002; Malisch &

Breuner, 2010; but see Schoech et al., 2013).

CORT produces its effect through both rapid and

delayed mechanisms (Sapolsky et al., 2000; Gasser et al.,

2009). In the former case, CORT acts through non-genomic

pathways and, in the course of minutes, induces changes

in concentrations of monoamines (e.g. catecholamines) in

some brain areas. It also alters brain cell excitability and

activation that result in autonomic output and rapid changes

in behaviour (Gasser et al., 2009; Groeneweg et al., 2011;

Sarabdjitsingh, Jo¨

els & De Kloet, 2012). The delayed effects,

on the other hand, entail genomic processes, such as gene

transcription and protein formation, and produce effects

hours and days after the disturbance (Sapolsky et al., 2000;

Romero, 2004; Wingﬁeld, 2013). All these effects of CORT

serve to improve survival under threatening situations by

redirecting energy and attention away from non-essential

processes, to help the body to return to homeostasis after

the perturbation is over, and to prepare the animal for

subsequent stressors and energy expenditures (Wingﬁeld

& Sapolsky, 2003; Tarlow & Blumstein, 2007; Wingﬁeld,

2013). In this sense, stress-induced CORT contributes to

the inhibition of reproductive behaviour and physiology,

the facilitation of locomotor responses, the enhancement

of stress-related memory and learning, and the increase of

energy availability (e.g. by promoting gluconeogenesis, fat

and protein catabolism, and decreasing peripheral glucose

uptake by non-essential tissues). CORT also acts to suppress

stress-induced immune responses to prevent them from

overshooting and to down-regulate the HPA axis itself

through negative feedback (Sapolsky et al., 2000; Gasser et al.,

2009; Breuner, 2010).

(2) Modulators

The physiological and behavioural responses to human

presence will also be modulated by anthropogenic, intrinsic

and context-dependent factors (Table 1 and Fig. 2). In

regard to human-dependent factors, the perception of risk

increases when animals are approached by people: (i)in

large groups (Burger & Gochfeld, 1991; Geist et al., 2007);

(ii) wearing coloured clothing that differs markedly from

the animal’s colouration (Gutzwiller & Marcum, 1997);

(iii) involved in activities that generate considerable noise

(Burger & Gochfeld, 1998; Waynert et al., 1999; Karp &

Root, 2009); and (iv) engaged in activities characterized

by rapid movements (Cooper, 1997; Bateman & Fleming,

2011). Perceived risk also increases when humans get closer

to animals (Stankowich & Blumstein, 2005; Weston et al.,

2012), and move and look directly towards them (Cooper,

1997; Stankowich & Coss, 2006; Carter et al., 2008; Bateman

& Fleming, 2011, 2014). Predictability of the disturbance

is another key factor to take into account. Animals are

more distressed by recreationists appearing suddenly in an

unpredictable way (Boissy, 1995; Miller et al., 2001; Desire,

Boissy & Veissier, 2002; Taylor & Knight, 2003). Activities

224 Zulima Tablado and Lukas Jenni

that are more aggressive or similar to predation, such as

consumptive recreation (e.g. hunting, capture, and handling),

or presence of predator-like animals (e.g. dogs), will also

inﬂuence animal risk assessment (Gabrielsen & Smith, 1995;

Martinetto & Cugnasse, 2001; Gonz´

alez et al., 2006; Bates

et al., 2007; Bateman et al., 2014). Some research has also

shown that animals may be more reactive to the visual

presence of humans than to anthropogenic noise (Gabrielsen

& Smith, 1995).

Other modulating factors are the characteristics of the

animals being approached (Table 1 and Fig. 2). For example,

certain species have more passive antipredatory strategies,

such as hiding and crypticity, while others opt for active

strategies like ﬂushing or ﬁghting (Espmark & Langvatn,

1985; Steen, Gabrielsen & Kanwisher, 1988; Stankowich &

Blumstein, 2005). Factors such as previous experience (Ikuta

& Blumstein, 2003; M¨ullner, Eduard Linsenmair & Wikelski,

2004; R¨

odl et al., 2007) and cognitive ability (Lendvai et al.,

2013) will also inﬂuence the way in which animals distinguish

non-dangerous humans from real threats, affecting the

response exhibited. Prior interactions with human activities

or natural predation might increase stress responses in

further encounters (i.e. sensitization of individuals exposed

to hunting, noxious anthropogenic stimuli or high natural

predation pressure) (Bejder et al., 2009; Bateman et al., 2014).

However, human-induced stress response can be low when

animals are naïve to predation risk due to the lack of natural

predators or when individuals have been habituated to harm-

less anthropogenic stimuli (Ydenberg & Dill, 1986; Helfman,

1989; Bejder et al., 2009). The ability to escape (ﬂushing

performance in Table 1 and Fig. 2D) may affect animal

reactivity (Ydenberg & Dill, 1986; Losos, 1990; Iriarte-Diaz,

2002; Bishop, 2005; Møller, V´

ag´

asi & Pap, 2013). That is,

even if they perceive a high risk, animals with extremely poor

ﬂushing abilities (e.g. gravid females or newborn offspring)

will rely on hiding, thereby showing reduced behavioural

responses compared to animals better able to escape (Bra˜

na,

1993; Stankowich & Blumstein, 2005). However, animals

with better ﬂushing performance and/or ﬁtter may be

‘conﬁdent’ of their ability to escape and, therefore may

tolerate a closer approach, exhibiting a minimal behavioural

response (Ydenberg & Dill, 1986; Cooper, Hawlena &

P´

erez-Mellado, 2009; Blumstein, 2010; Møller et al., 2013).

The behavioural and physiological response of parents

with dependent offspring have been shown to be less strong

if the value of the offspring is high. Offspring value is

high if there is little chance for the individual to reproduce

again, and vice versa, which may depend, for example, on

sex, mating system, survival likelihood (i.e. individual age

and the chance of future reproduction), and environmental

conditions (Silverin & Wingﬁeld, 1998; Warner, 1998;

Lendvai & Chastel, 2008; B´

okony et al., 2009; Breuner,

2010; Schmid et al., 2013). Antipredator responses will also

vary with social aggregation, which is expected to decrease

the perceived danger by single individuals (i.e. risk dilution

and coordinated defence strategies) at least up to a certain

group size. However, at even larger group sizes this trend

may switch, since the higher overall stress and lower arousal

thresholds (e.g. more likely alarm calls) of highly dense

groups may increase responsiveness (Fernandez-Juricic et al.,

2002; Pride, 2005; Ramp, Russell & Croft, 2005; Stankowich

& Blumstein, 2005; Kikusui, Winslow & Mori, 2006). Other

properties that may affect the physiological and psychological

state of individuals, and therefore their stress response, are

mass-speciﬁc metabolic rates (i.e. faster metabolism favours

stress reactivity) (Jessop, Woodford & Symonds, 2013), sex

and hormone proﬁles, body condition, coping style, and

developmental age (i.e. from foetus to adults). Sex hormones

and hormones involved in parental care play an important

role in modulating the physiological and behavioural stress

response. For example, oestrogens are related to higher

adrenocortical reactivity, while prolactin reduces parental

stress responses, thereby favouring offspring care and survival

(Peczely, 1979; Steidl & Anthony, 1996; Tilbrook et al., 2006;

Wynne-Edwards & Timonin, 2007; Solomon, 2009; Malo,

Acebes & Traba, 2011). Poor body condition (i.e. typical of

high anxiety levels, high densities, or poor habitats) favours

self-maintenance mechanisms, energy-saving behaviours

and a higher adrenocortical response (Moore & Jessop, 2003;

Beale & Monaghan, 2004a;Breuneret al., 2008). Individuals

may exhibit considerable variability in stress reactivity (i.e.

the intensity and duration of their response to a given

stressor). These variations in ‘coping style’ have both genetic

and environmental inﬂuences, such as perinatal exposure to

stressors and corticosteroids (Carere, Caramaschi & Fawcett,

2010; Schoech, Rensel & Heiss, 2011). The coping style will

be reﬂected both in the behavioural and the physiological

response to disturbance. That is, shyer individuals are

generally more fearful and, thus, are likely to mount a

higher adrenocortical response and ﬂush (or hide) earlier

than bolder individuals (Thaker, Lima & Hews, 2009b;

Carere et al., 2010; Atwell et al., 2012). Physiological and

behavioural responses to disturbance will vary non-linearly

with developmental age. During early development, which

occurs mostly prenatally (or in ovo) in precocial species and

extends further into postnatal (or posthatch) life in altricial

species, there is a hypo-responsive period of the HPA axis

when CORT responses are low (Berger et al., 2007; Breuner

et al., 2008; Wada & Breuner, 2010). This has been suggested

to protect developing animals from the detrimental effects of

high CORT levels, which could cause permanent alterations

of the HPA axis, may cause damage to memory and cognitive

functions, and reduce growth rates (Kitaysky et al., 2003;

Hayward & Wingﬁeld, 2004; Breuner et al., 2008; Rensel,

Boughton & Schoech, 2010; Wada & Breuner, 2010).

Later the HPA axis responsiveness increases and reaches

relatively high levels during juvenile and early-adulthood

periods. Some studies have shown that HPA reactivity

may, to a certain degree, decrease again during adulthood

(Table 1, Fig. 2J). That is, juvenile individuals and younger

adults would show a higher adrenocortical response than

experienced adults (Berger et al., 2007; Breuner et al., 2008;

Wilcoxen et al., 2011). With senescence; however, the

trendappearstoswitchoncemoreandtheresponsiveness

Modulators of wildlife response to recreation 225

of the HPA axis tends to increase (Goutte et al., 2010;

Wilcoxen et al., 2011). Behavioural responses also often

show a complex non-linear relationship with age (Table 1,

Fig. 2J). Behavioural responses may be lower (more passive)

in newborn and senescent individuals, due to locomotor and

energetic limitations (Knight & Gutzwiller, 1995; Berger

et al., 2007; Seltmann et al., 2012). At ‘intermediate’ ages,

ﬂushing responses will show a U-shaped relationship, with

juvenile and older adults (but not senescent) age classes

tending to escape earlier than middle-aged adults (Berger

et al., 2007; Seltmann et al., 2012; Møller, 2014).

Animal responses to human activities can also vary

depending on the spatio-temporal context (Table 1, Fig. 2).

We observe that these responses often vary throughout

the day and year (Fig. 2J, K), i.e. depending on circadian

and circa-annual variations in physiology, activity and

motivation (e.g. nocturnality versus diurnality, territory

establishment versus moulting or migratory phase) (Romero &

Remage-Healey, 2000; Stankowich, 2008; Tillmann, 2009;

Llewelyn, Webb & Shine, 2010; Riou et al., 2010). In addition,

in recent years smaller-scale cycles have been described

for at least some species, in which within a given daily

cycle individuals experience ultradian HPA axis pulsatility

(Sarabdjitsingh et al., 2012). The stress response of a given

individual will, thus, be time-speciﬁc and depend on the

phase of the ultradian cycle when human disturbance

occurs. Habitat characteristics will also affect reactions

towards human presence, since apart from their effect on

food availability, and thus, body condition, they differ in

refuge availability for animals exposed to human recreation.

Wildlife having options to hide or retreat to refuges (e.g.

dense canopy, cavities or steep slopes), will ‘feel’ safer and

react differently from individuals or species found in more

open habitats and that have to traverse larger distances for

protection (Lazarus & Symonds, 1992; Fernandez-Juricic

et al., 2002; Camp et al., 2012; Tadesse & Kotler, 2012).

Weather can also directly affect animal behavioural

responses. For example, higher ambient temperatures tend to

increase an animal’s ‘tolerance’ to approaching people, due

to their faster capacity of reaction when warmer. In addition,

animals may want to limit their stress responses to, to some

extent, avoid excessive heat build-up due to stress-related

increases in metabolism and movement (Fernandez-Juricic

et al., 2002; Cooper et al., 2009). Other contextual factors that

determine the psychological and physiological excitability of

animals are the relative position of the animal to humans

(e.g. animals ‘feel’ safer when located higher or closer to

escape routes) (MacArthur, Geist & Johnston, 1982; Steidl &

Anthony, 1996; Thiel et al., 2007; Tadesse & Kotler, 2012),

predation pressure (Berger et al., 2007; St Clair et al., 2010;

Januchowski-Hartley et al., 2011), and simultaneous stressful

events, such as extreme weather or agonistic encounters with

conspeciﬁcs (Romero, Reed & Wingﬁeld, 2000; Romero,

2004). Increases in the latter two usually lead to high levels

of awareness and baseline CORT that, in turn, may lower

response thresholds to disturbance (Thaker, Lima & Hews,

2009a; Thaker et al., 2010).

IV. LEVEL 3: IMPACTS OF RECREATIONAL

ACTIVITIES ON FITNESS AND SPACE USE

(1) Mechanisms

If individuals respond behaviourally or physiologically to the

presence of recreationists, their ﬁtness (reproductive output

and survival as proxies) and habitat use may be compromised.

This can happen both through single disturbance events and

through more continuous or frequent disturbances (Bowles,

1995; Knight & Gutzwiller, 1995; Wingﬁeld et al., 1997;

Frid & Dill, 2002; Buckley, 2011). Regarding the negative

effects of single disturbances on ﬁtness, one of the most

common cases is when parents are ﬂushed, leaving eggs or

newborn offspring unattended. The temporarily abandoned

offspring or eggs may then be depredated, starve, or die from

thermal stress (Ellison & Cleary, 1978; Anderson & Keith,

1980; Major, 1990; Buckley, 2011). Some predators may

even specialize in this type of opportunistic hunting (Kury

& Gochfeld, 1975; Strang, 1980; Knight & Cole, 1995).

Disturbance-related single panic reactions may cause acci-

dental self-injury or damage to conspeciﬁcs and progeny, thus

decreasing survival and reproductive output (Bowles, 1995;

Buckley, 2011). An understudied phenomenon is that single

disturbance events during settling periods (e.g. dispersal and

territory formation) might cause signiﬁcant changes in habitat

use or even lead to abandonment (Buckley, 2004b, 2011).

If disturbances are frequent or continuous, they may

also cause negative effects through chronic stress (i.e.

continuous activation of HPA axis and disruption of negative

feedback, which impedes the return to basal CORT levels),

longer-term changes in activity budget patterns, behaviour

(e.g. movement patterns) and energy expenditure (Knight &

Gutzwiller, 1995; Wingﬁeld et al., 1997; Frid & Dill, 2002;

Romero, 2004). Note that this might not apply in cases in

which habituation occurs [see Level 2 (Section III) for further

information on the modulating effect of previous experience

on animal responses to humans]. Chronic high levels of stress

hormones can lead to infertility, an offspring sex-ratio biased

towards the less costly sex, immunosuppression, weight

and muscle loss, growth inhibition, damage to the central

nervous system with accompanying impairment of cognitive

functions, among others (Sapolsky et al., 2000; Elenkov, 2004;

Wikelski & Cooke, 2006; Breuner, 2010). Regularly disturbed

areas may also be avoided or used only when humans are

not present, altering spatial use and/or activity patterns

(Tuite, Owen & Paynter, 1983; Pﬁster, Harrington & Lavine,

1992; Bejder et al., 2006, 2009). This can lead to a shift in

home range and displace wildlife into suboptimal habitats,

either permanently or temporarily, with all the possible

consequences for animal body condition and ﬁtness (Olsson

et al., 2007; Paquet & Darimont, 2010; Kerley, Kowalczyk &

Cromsigt, 2012). Finally, waste of energy, as a consequence

of recurrent disturbance can lower body condition of

animals and, in turn, compromise survival and reproduction,

especially if it occurs during periods of high energetic needs,

such as migration, harsh winter conditions, breeding or moult

(Madsen, 1995; Buckley, 2004b;Barshepet al., 2013).

226 Zulima Tablado and Lukas Jenni

(2) Modulators

The impact of human intrusion on ﬁtness and habitat use

will not be the same for all individuals and situations, but will

be modiﬁed by the characteristics of the disturbance itself,

the properties inherent to the species or individuals, and

the circumstances around the disturbance event. Human

recreation will tend to have a higher impact on breeding

success, survival, habitat selection and/or chronic stress

when it causes more frequent or intense behavioural or

physiological responses. This is the case for animals in

areas with frequent, continuous or intense human use (i.e.

higher number of people using an area at the same time)

and that fail to habituate to the disturbance (Robert &

Ralph, 1975; Niles & Clark, 1989; Harper & Eastman, 2000;

Thiel et al., 2008; Wheeler, Villiers & Majiedt, 2009; French

et al., 2011).

The outcome of disturbance at this intermediate level will

vary among species and individuals. Social aggregation may

modulate the effects of disturbance, since gregarious species

are more likely to suffer self-injury and injure conspeciﬁcs

during panic behaviour (Robert & Ralph, 1975; Carney &

Sydeman, 1999; Buckley, 2004a). The spatial response to

human recreation will likely differ between gregarious and

solitary taxa, since habitat selection of gregarious species

will depend not only on characteristics of the habitat (and

degree of disturbance) but also on group decisions and social

attraction that might increase the reluctance to abandon

a certain area (Burger, 1988; Serrano et al., 2004). Higher

cognitive ability will most likely also play an important role

in helping animals to recognise quickly and, thus, habituate

to non-dangerous human activities and reduce the likelihood

of suffering chronic stress and decreased ﬁtness (Carrete &

Tella, 2011; Lendvai et al., 2013). In addition, individual

coping style may inﬂuence the speed of recovery after a

stressful perturbation, leading to differences in long-term

stress levels (Fowler, 1999; Romero, 2004; Bejder et al.,

2009). That is, animals with a more reactive HPA axis,

i.e. generally shyer, possess less efﬁcient negative feedback

systems to facilitate the return of CORT to baseline levels

and, as a result, will be more prone to suffer chronic stress.

As mentioned above, human disturbance causing increases

in energy expenditure or decreases in food intake may lead to

decreases in animal survival and reproduction, especially in

periods of harsh weather conditions or during periods crucial

for reserve accumulation (e.g. during premigratory staging)

(Madsen, 1995; Buckley, 2004b;Barshepet al., 2013). This

will predominantly affect individuals and species that are

energetically constrained, reducing their limited capacity to

compensate for additional expenditures. An example of this

are species which are limited by the capacity of their digestive

tract (e.g. grouse species in winter feeding on coniferous nee-

dles) or performing costly activities (e.g. moulting, breeding)

(Smith, 1976; Millar, 1978; Koteja, 1996; Sedinger, 1997).

Other cases are, for instance, animals whose survival and

reproduction depend on especially high rates of energy accu-

mulation, such as long-distance migrating birds or animals

storing energy for wintering (MacKinnon, 1972; Piersma,

1990). If their fuel deposition rate is lowered through human

activities, their time schedule may be delayed, causing

reproduction and survival to be compromised (Madsen,

1995; Buckley, 2004b; Klaassen et al., 2006). Similarly, indi-

viduals in suboptimal condition (e.g. living in a suboptimal

habitat, harsh climatic conditions, low social rank, and/or

suffering from parasites or disease) will have a lower capacity

to buffer the deleterious effects of acute or prolonged

disturbances. These animals will not be able to compensate

with additional broods after stress-induced failures or will

produce smaller, more vulnerable offspring (Weimerskirch,

1999; Weimerskirch et al., 2002). Interestingly, poor body

condition may impede the abandonment of disturbed areas

as only individuals with enough energy reserves will be able

to search for new suitable habitat (Gill et al., 2001; Bejder

et al., 2009). The degree of psychological and energetic

investment in settling in a given area may also determine

the willingness and likelihood of abandoning it after being

disturbed by recreationists. The more an individual invests

in an area, the less prone will it be to leave, even though this

attachment may lead to chronic stress, since it will continue

to be exposed to human visitation (Gill et al., 2001; Bejder

et al., 2009).

Finally, timing and environmental characteristics will

also inﬂuence the ﬁtness and spatial consequences of

human–wildlife encounters. For example, disturbance will

have a higher impact on survival, reproduction and spatial

use if it occurs during especially vulnerable moments (e.g.

during territory establishment or when nestlings are small and

more vulnerable to predation or to anxiety-induced HPA axis

alterations) (Bolduc & Guillemette, 2003; Kapoor et al., 2006;

Buckley, 2011). Additionally, apart from the effect of habitat

quality on body condition mentioned above, habitat quality

may induce spatial-use changes, namely a trade-off between

the quality of the current habitat and that of alternative

areas. If alternative habitats are poor or not available,

animals may be reluctant to abandon an area despite

human activities (Gill et al., 2001; Weidinger, 2002; Lambert

& Kleindorfer, 2006; Bejder et al., 2009). Relatively high

predation pressure can also aggravate the detrimental effects

of human activities (Gutzwiller, Riffell & Anderson, 2002;

Bolduc & Guillemette, 2003). For example, human-induced

momentary abandonment of offspring might have a higher

impact in cases in which the number of predators and

their probability of accessing the offspring are higher (e.g.

ground breeding location versus trees or cliffs). Bad weather

and harsh climate will also aggravate the impact of human

disturbance on animal ﬁtness. Difﬁcult weather conditions

will increase both the energetic expenditure associated with

escaping and the likelihood of mortality of unattended and

unprotected offspring (Cowles, 1956; Buckley, 2004b, 2011;

Carr & Lima, 2012). Similarly, harsh climatic conditions

will limit the capacity to compensate for the effects of

disturbance, given that such conditions are usually associated

with poorer body condition, lower resource availability,

and shorter breeding seasons (Wingﬁeld, 1984; Martin &

Wiebe, 2004).

Modulators of wildlife response to recreation 227

V. LEVEL 4: CONSEQUENCES OF HUMAN

DISTURBANCE FOR ANIMAL POPULATIONS

AND SPECIES

(1) Mechanisms

If human activities reduce the ﬁtness of at least some

individuals of a population and/or change their habitat use,

population demographic processes (rates of reproduction,

survival, immigration, and emigration) may be negatively

affected. Thus, population growth rate may decrease and

even reach negative values. This reduction in population

growth rates may, in turn, result in reductions in population

size, increased probability of local extirpation, and potential

changes in distribution (Tuite et al., 1983; Pﬁster et al., 1992;

Stevens & Boness, 2003; Bejder et al., 2006; Gill, 2007;

Lusseau & Bejder, 2007).

(2) Modulators

Even though the association between demographic processes

and population growth seems straightforward, the ﬁnal

impact will vary depending on characteristics of the

recreational activity, of the animals and of the context

(Table 1, Fig. 2). Regarding recreational activity, both the

spatial and temporal scale, as well as the pervasiveness of

human disturbance will affect the fate of populations. That is,

if the effect of disturbance is widespread throughout a larger

portion of a population or species range, and/or occurs

over long periods of the year, then we would expect greater

decreases in population growth rate than if disturbance only

affects a small part of the population locally or occurs only

occasionally (Lima, 1993; Riffell, Gutzwiller & Anderson,

1996; Finney, Pearce-Higgins & Yalden, 2005). If human

presence has a large ecological effect, that is, if it affects

several taxa simultaneously, disturbance-induced decreases

of competitor or predator species might indirectly favour

species expected to be negatively affected by humans.

Conversely, the direct effect of recreation on a given

species may be further aggravated if human activities

concurrently reduce other species on which they depend

(e.g. human-induced reductions of prey availability will

indirectly affect predators) (Skagen, Knight & Orians, 1991;

Hebblewhite et al., 2005; Price, 2008; Møller, 2012).

The effect of human activities at the population level

will also vary according to the properties of the populations

and species themselves. Differences in life-history traits (e.g.

survival rates, number of reproductive attempts, generation

times) will determine how quickly the population changes

in the face of reductions in reproduction or survival caused

by human recreation. For example, some species will be

more sensitive to decreases in survival, while other will

be more responsive to declines in reproduction (Heppell,

Caswell & Crowder, 2000; Saether & Bakke, 2000; Oli &

Dobson, 2003; Church et al., 2007; Lima, 2009). That is,

some species dynamics will be able to buffer or compensate

losses due to disturbance better than others. Higher degrees

of philopatry and site ﬁdelity of a species (Yohannes, Hobson

& Pearson, 2007) will further modulate the consequences of

disturbance. That is, the reluctance to abandon a disturbed

area due to site ﬁdelity in some species may produce an

evolutionary or ecological trap (Stamps & Krishnan, 1999;

Schlaepfer, Runge & Sherman, 2002; Igual et al., 2007;

Yohannes et al., 2007), leading to negative population trends.

Human recreation can also have stronger effects on social

species than on solitary ones, since disturbances in areas

where animals aggregate (e.g. bird colonies) will affect most

individuals simultaneously, which is further aggravated by

the usually higher site ﬁdelity in gregarious species (Burger,

1981; Carney & Sydeman, 1999).

Additionally, characteristics such as population density

or meta-population dynamics are expected to have an

important role in modulating the effect of disturbance

at the population and species level. For example, small

populations, which are more vulnerable to stochasticity, are

more likely to be affected by human disturbances, even by

single events, that result in reductions in reproductive output,

habitat-use changes, or increased mortality that affect only

a few individuals (Lande, 1993; Lacy, 2000; McGowan et al.,

2011). On the other hand, in populations with high densities

entailing negative density dependence, the detrimental effects

of human disturbance could go unnoticed via release of

density dependence (Sinclair & Pech, 1996; Mallord et al.,

2007). When two or more populations are connected as a

meta-population system, recreational activities affecting sink

populations are expected to have a smaller impact because

the population is maintained primarily by immigration

from other sources. Conversely, in those instances in

which disturbance affects source populations, the overall

meta-population system might suffer the consequences

(Pulliam, 1988; Brawn & Robinson, 1996; Dias, 1996).

An important modulator of the consequences of distur-

bance at this level is the capacity of a given species or

population to adapt to humans, as demonstrated by the many

species that thrive in urban environments. That is, popula-

tions and species with a greater genetic and phenotypic

variability (e.g. variability of coping styles), as well as pheno-

typic plasticity, will be able to adjust more easily to human

presence by replacement of sensitive individuals by less sen-

sitive (usually bolder and less fearful) individuals (Carvalho,

1993; Lande & Shannon, 1996; Dufty, Clobert & Moller,

2002). However, adaptation to humans may come at a cost.

For example, reduction of fear will only be positive at the

population level if it does not increase the probability of being

depredated by non-human predators or result in a reduction

in reproduction (Dahlgren, 1990; Smith & Blumstein, 2008).

Finally, regardless of the species or human activities,

there exist many other factors that may modify or obscure

the demographic consequences of human disturbance by

causing similar or opposing effects. First, we emphasize that,

in most cases, human recreation is associated with habitat

deterioration (e.g. construction of roads or ski resorts) and

it is often difﬁcult to separate the inﬂuence of direct human

presence from that of habitat degradation. Thus, habitat

modiﬁcation associated with some recreational activities

228 Zulima Tablado and Lukas Jenni

may negatively affect populations by decreases in both

habitat quality and foraging opportunities. Clearly, this

might obscure or even worsen the consequences of stress

due to direct interactions with people (Cole & Landres,

1995; Buckley, 2004b; Braunisch, Patthey & Arlettaz, 2010).

Environmental changes independent of human disturbance

may inﬂuence population-level responses to recreation.

Factors with potentially positive effects on populations, such

as, for example, increases in reproduction, carrying capacity,

or immigration rates due to climate change, might increase

population growth rate obscuring or compensating for any

negative effects of disturbance (Ozgul et al., 2010; Tablado

& Revilla, 2012). On the other hand, factors that negatively

impact populations or species, such as biological invasions,

changes in land use, or detrimental effects of climate

change on ecosystems and migration patterns, might further

exacerbate negative effects of disturbance on populations

or species (Dextrase & Mandrak, 2006; Foden et al.,

2013).

VI. CONCLUSIONS

(1) From this synthesis, we conclude that the difﬁculties

in ﬁnding general patterns in the ﬁeld of recreational

disturbance are due to three main reasons. First, for all

levels of response there are many diverse factors likely to

modulate the impact of human outdoor activities on wildlife,

and the combined inﬂuence of these factors within each

level may obscure or confound the effects of disturbance.

That is, the impact of human disturbance not only depends

on the intensity and type of the recreational activity, but

also on the characteristics of the species, and the context in

which interactions occur. For instance, whether individuals

respond behaviourally, physiologically, or not will depend

on their assessment of the risk imposed by humans, their

options to hide or escape, and the potential consequences

on their offspring’s and their own welfare. The impact of

recreational activities will also vary among populations or

species depending on a combination of factors (e.g. extent of

human activities, species ecology and context characteristics)

which may or may not allow them to compensate for or adapt

to disturbance.

(2) Second, the difﬁculty in ﬁnding general patterns

is due to the fact that some modulators might affect

wildlife responses in complex non-linear ways, such as the

bell-shaped dependence of behavioural response on ﬂushing

performance (see Fig. 2D) (Ydenberg & Dill, 1986; Losos,

1990; Iriarte-Diaz, 2002). Many such relationships may

be non-linear; however, they still need to be explored. In

other instances, factor complexity results from contrasting

effects at different levels of response. For instance, group

size and predator (human) detection are positively related

(Schaik et al., 1983; Beauchamp, 2010). However, at the

next level, this relationship may not be positive because

animals in groups may feel safer than single animals and,

therefore, exhibit a dampened behavioural or physiological

reaction to humans (Fernandez-Juricic et al., 2002; Kikusui

et al., 2006). Moreover, the same modulating factor may

have contrasting impacts even within the same level of

response, depending on the response mechanism. This

entails a lack of correlation between different measures

of stress response, such as differences in behavioural versus

physiological responses (Killen et al., 2013). This would be,

for example, the case for body condition. Better body

condition tends to increase active behavioural responses

(e.g. ﬂushing distance), however, the physiological response

tends to be dampened (i.e. HPA axis reactivity) as body

condition improves (Beale & Monaghan, 2004a;Breuner

et al., 2008).

(3) Third, another complication in ﬁnding general

patterns of the impacts of human disturbance on wildlife

exists because of the accumulation of modulating factors

across different levels of response which may confound the

patterns, especially at higher levels (such as reproductive

success, survival, or population and species trends) (Burger

et al., 1995; Gill et al., 2001; Price, 2008; Bonier et al., 2009).

The more levels of response (i.e. from Level 1 to 2 to 3,

etc.), the more factors accumulate, adding uncertainty to

the probability of ﬁnding generalizable associations (Fig. 1).

That is, even if negative reactions to human disturbance

are clearly observed at lower levels, we cannot readily infer

detrimental consequences at the demographic level since

the inﬂuence of many factors (e.g. habitat quality, previous

experience, climate, or density dependence) may confound

the expected effect at the population level.

(4) All the modulators and relationships considered here,

as well as those yet to be considered may explain why few

studies have shown general patterns for the relationships

between direct human disturbance and wildlife. However,

this should not discourage researchers in the ﬁeld of human

disturbance. We rather hope to have set, with this synthesis,

a comprehensive basis that may be used as a future approach

and reference for identifying the type of factors that may

affect animals’ responses to human disturbance and the

complexity of their effects. There is a need for more research

to validate across populations and taxa the generality of

some of the modulating effects presented herein. Inclusion,

or at least acknowledgement, of factors that may modulate

responses to disturbance in a given system, and consideration

of the complexity and likely interactions of such factors

will facilitate improved study designs and interpretation

of ﬁndings. We are conﬁdent that doing so will improve

our understanding of the complex nature by which human

recreation inﬂuences wildlife.

VII. ACKNOWLEGDEMENTS

We thank Susi Jenni-Eiermann, Bettina Almasi, Benjamin

Homberger, Yves B¨

otsch, Juanita Olano, Gilberto Pasinelli,

and Michael Schaub for their comments on previous ver-

sions of the manuscript. We also thank two reviewers for their

Modulators of wildlife response to recreation 229

input, which substantially improved the manuscript, in par-

ticular Steve Schoech for additionally improving the English.

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Human Presence as a Factor Determining the Circadian Activity of Mammal Species in the Sinite Kamani Nature Park

Article

Full-text available

Jun 2024

The circadian activity of selected mammal species and the temporal overlap with human presence or between species were analysed in 2013-2014 on the territory of the Sinite Kamani Nature Park, Eastern Stara Planina. The purpose of this study was to determine how the human presence affected the circadian activity of mammal species in this protected area. The wild boar (n = 68) showed 22% overlap with the humans (n = 54) in its circadian activity (Δ = 0.22, CI 0.02-0.21) while the roe deer (n = 144) activity overlapped in 49% with the human activity (Δ = 0.49, CI 0.29-0.51). The European brown hare (n=26) activity had a 23% overlap (Δ = 0.23, CI 0.07-0.26), the golden jackal (n = 42)-36% (Δ = 0.36, CI 0.22-0.49) and the red fox (n = 131)-24% (Δ = 0.24, CI 0.06-0.25). The overlap between the red fox and European brown hare activity was 81% (Δ = 0.81, CI 0.71-0.93), between red fox and golden jackal-71% (Δ = 0.71, CI0.49-0.77) and between red fox and Martes sp.-81% (Δ = 0.81, CI 0.72-0.93). The target species avoided the range of time when humans were active. This forced the species to use a narrower temporal niche when sharing the same space. These results provided insights for the better management of the species in the protected areas.

Do agricultural practices on meadows reduce or increase flight initiation distance in the White Stork Ciconia ciconia?

Preprint

Full-text available

Apr 2024

Human activities often negatively affect the time birds spend on activities such as parental care, foraging and resting. Forms of antipredator behaviour among birds such as vigilance can be an adaptation to human disturbances which can enhance their fitness in human‐managed habitats. We studied the flight initiation distance (FID) of White Storks Ciconia ciconia foraging on hay meadows during their breeding season. Our study showed that farm work, the type of meadows and starting distance (the distance between the bird’s position and the observer at the start of his walk) all had an influence on FID. Conversely, the numbers of storks in a particular foraging flock had no effect on an individual bird’s FID. The lower FID could have been due to the presence of machinery operating in the meadows, because storks then have opportunities to catch energy-rich prey that has been scared off by the machines. Unlike meadows cleared of hay, mown meadows with cut grass are more attractive to storks, and the FID there is shorter. The starting distance positively affected stork responses. These findings suggest that the FID of White Storks, treated as a measure of the risk of predation, depends largely on the degree of attractiveness of the feeding grounds.

A review and risk analysis on potential impacts of riverine recreational activities on Atlantic Salmon (Salmo salar) in eastern Canada

Article

May 2024

Atlantic salmon populations face a number of significant, human-driven threats such as overfishing and thermal stress from anthropogenically-accelerated climate change. A considerable body of research has been devoted to such large-scale threats as well as catch-and-release fishing, while the potential impacts of other recreational activities on Atlantic salmon while in rivers have been largely overlooked. Here, we undertook a systematic literature review of the effects that recreational activities (excluding direct impacts of catch-and-release angling) might have on the welfare and survival of Atlantic salmon in riverine systems at all relevant life history stages. Examples of relevant activities examined here include swimming, all-terrain vehicle (ATV) use, and underwater photography. We also performed a relative risk assessment of such activities based on the likelihoods of their occurrence and the severities of their potential impacts. For the most part, the impacts of non-angling recreational activities on Atlantic salmon are likely widespread but largely temporary. Redds, eggs, and juveniles were generally found to be more susceptible to most threats than smolts and adults. However, some activities have significant destructive potential such as ATV use in or around spawning habitats. Significant risks also remain concerning pathogen and invasive species transfer via angling gear, waders, canoes, and other equipment that may be moved across systems without proper cleaning. Although we focused primarily on risks to native Atlantic salmon populations in eastern Canada, the risk assessment framework developed here is broadly applicable and easily adaptable for management in other contexts and jurisdictions with populations of riverine Atlantic salmon and potentially other migratory salmonids too.

Assessment of Suitable Habitat of the Demoiselle Crane (Anthropoides virgo) in the Wake of Climate Change: A Study of Its Wintering Refugees in Pakistan

Article

Full-text available

May 2024

The inevitable impacts of climate change have reverberated across ecosystems and caused substantial global biodiversity loss. Climate-induced habitat loss has contributed to range shifts at both species and community levels. Given the importance of identifying suitable habitats for at-risk species, it is imperative to assess potential current and future distributions, and to understand influential environmental factors. Like many species, the Demoiselle crane is not immune to climatic pressures. Khyber Pakhtunkhwa and Balochistan provinces in Pakistan are known wintering grounds for this species. Given that Pakistan is among the top five countries facing devastating effects of climate change, this study sought to conduct species distribution modeling under climate change using data collected during 4 years of field surveys. We developed a Maximum Entropy distribution model to predict the current and projected future distribution of the species across the study area. Future habitat projections for 2050 and 2070 were carried out using two representative concentration pathways (RCP 4.5 and RCP 8.5) under three global circulation models, including HADGEM2-AO, BCC-CSM1-1, and CCSM4. The most influential factors shaping Demoiselle Crane habitat suitability included the temperature seasonality, annual mean temperature, terrain ruggedness index, and human population density, all of which contributed significantly to the suitability (81.3%). The model identified 35% of the study area as moderately suitable (134,068 km2) and highly suitable (27,911 km2) habitat for the species under current climatic conditions. Under changing climate scenarios, our model predicted a major loss of the species’ current suitable habitat, with shrinkage and shift towards western–central areas along the Pakistan–Afghanistan boarder. The RCP 8.5, which is the extreme climate change scenario, portrays particularly severe consequences, with habitat losses reaching 65% in 2050 and 85% in 2070. This comprehensive study provides useful insights into the Demoiselle Crane habitat’s current and future dynamics in Pakistan.

Flight initiation distance in waterbirds o two coastal wetlands wit different protection regimes

Article

Mar 2024

Human activities can impact avian populations leading to impaired fitness. It is, therefore, important to monitor their response to direct disturbance. Flight initiation distance (FID) is considered a measure of tolerance to humans and can be affected by age and gregariousness, yet few systematic data are available across species in similar environments. We measured FID in eight species of waterbirds in two coastal lagoon environments with different protection regimes, taking into account age classes and whether individuals were grouped or alone. Species markedly differed in FID: average distance ranged between 50 (little egret, Egretta garzetta, singletons) and 188m (spoonbill, Platalea leucorodia, flocks). Overall, adults were more cautious than immatures, likely due to learning and experience, while flocks flew up sooner than singletons likely due to the “many eyes” effect. In areas strictly protected, where only low and non-threatening human activities are allowed, birds flew at a shorter distance than in areas with a less strict regime of protection. Interestingly, large-sized species flew at longer distance than small-sized species. These findings have important implications for management to reduce disturbance to avian wildlife by human activities and to assess the effectiveness of protected areas.

Spatial and temporal factors influencing wildlife use of overpass crossing structures and landscape siphons along a major canal

Article

Mar 2024
BIOL CONSERV

Anthropogenic linear infrastructures can reduce landscape connectivity for wildlife, and crossing structures are a mitigation strategy to facilitate animal movement across potential barriers. However, the spatial and temporal factors promoting crossing structure use by the wildlife community across scales are not fully understood, especially for major water canals. We tested multiple hypotheses and predictions to evaluate how wildlife use of crossing structures was influenced by (1) landscape features (i.e., fine landscape-scale vegetation cover and broad landscape-scale plant productivity, topography, and human development), (2) season, and (3) time of day. We used remote cameras to monitor 43 overpasses and 13 siphons (i.e., natural crossing areas where the canal traveled underground) along the Central Arizona Project canal across three seasons (i.e., hot-dry, hot-wet, cool-wet) during one year. We detected 17 small- to large-sized herbivore and carnivore species using overpasses and siphons. When using crossing structures, each wildlife species exhibited unique habitat relationships in relation to vegetation cover, plant productivity, and topography. Several species decreased use of overpasses as the amount of human development increased. Crossing frequency increased in the hot-dry and cool-wet seasons for many species at overpasses (11 species) and siphons (9 species). Daily activity patterns of individual species were similar across seasons, and between overpasses and siphons. Ultimately, this study suggests that to promote movement across canals for the wildlife community, it is important to provide a variety of crossing types that occur away from human development and across a range of vegetation and topographic characteristics.

Fine-Tuning Coexistence: Wildlife's Short-Term Responses to Dynamic Human Disturbance Patterns

Article

Full-text available

Jun 2024

Anthropogenic disturbance elicits adaptive responses in wildlife, generally aimed at risk-avoidance, ultimately imposing constraints on their spatial and temporal niches. Previous studies have largely focused on long-term adaptive responses to stable human pressure, but rapid adjustments in wildlife’s diel and habitat use patterns in response to fine-scale variations in human presence have so far been overlooked. In this study we estimate short-term spatio-temporal deviations in local habitat use and diel activity of medium and large mammal species in response to rapid variations in human disturbance. We employed a year-long camera-trapping within a small private reserve, and recorded spatio-temporal information on all sources of anthropogenic disturbance in the area. By controlling for the average habitat use and diel activity, we explored fine-scale spatiotemporal adjustments in seven mammal species. We found evidence of spatial and/or temporal avoidance across all species, except wild boar, with variations in magnitude and direction coherent with species traits and expected levels of human-tolerance. Most species exhibited temporal avoidance of human activities, with porcupine and roe deer eliciting particularly strong responses. Notably, foxes concurrently displayed temporal avoidance and spatial attraction, likely driven by the presence of anthropogenic trophic resources. Our study underscores the role of behavioral plasticity in enabling wildlife to adjust daily habitat use and activity patterns to varying levels of human pressure across space and time. Understanding these nuanced behavioral strategies can help to promote wildlife-human coexistence and mitigating the adverse impacts of human presence on wildlife fitness.

Captures do not affect escape response to humans in Alpine marmot

Article

Full-text available

Jun 2024

Capture and manipulation are an integral part of wildlife research and management. These practices, however, can affect animals either directly or indirectly, and studies should generally evaluate the consequences of captures to ensure animal welfare and reduce sampling bias. Here, we investigated the indirect, behavioural effects of live‐capture on escape response to humans in Alpine marmot Marmota marmota within the Stelvio National Park (central Italian Alps) over three seasons (2021–2023). We used flight initiation distance (FID) as a measure of escape response and tested it in relation to capture status using linear mixed modelling. Captures did not have any detectable effect on escape response, and FID was best explained by covariates such as starting distance, distance to nearest burrow, current behaviour during the observation and year of observation. It might be that, in marmots, escape response to humans is a rather inert behaviour. As such, although we cannot rule out unmeasured effects, capture may not represent an excessively traumatic experience which could trigger immediate behavioural modification. In turn, capture is unlikely to compromise animal welfare or cause scientific bias in studies investigating escape response in this species, at least over the short term.

Captures do not affect escape response to humans in Alpine marmot

Preprint

May 2024

Capture and manipulation are an integral part of wildlife research and management. These practices, however, can affect animals either directly or indirectly, and studies should generally evaluate the consequences of captures to ensure animal welfare and reduce sampling bias. Here, we investigated the indirect, behavioural effects of live-capture on escape response to humans in Alpine marmot Marmota marmota within the Stelvio National Park (central Italian Alps) over three seasons (2021- 2023). We used flight initiation distance (FID) as a measure of escape response and tested it in relation to capture status using linear mixed modelling. Captures did not have any detectable effect on escape response, and FID was best explained by covariates such as starting distance, distance to nearest burrow, current behaviour during the observation and year of observation. It might be that, in marmots, escape response to humans is a rather inert behaviour, and as such, although we cannot rule out unmeasured effects, capture may not represent an excessively traumatic experience which could trigger immediate behavioural modification. In turn, capture is unlikely to compromise animal welfare or cause scientific bias in studies investigating escape response in this species, at least over the short term.

Behavioral response of Bornean ungulates, including bearded pigs and sambar deer, to anthropogenic disturbance in Sabah, Malaysia

Preprint

Full-text available

Apr 2024

Understanding wildlife behavioral responses is crucial for assessing the effects of anthropogenic disturbance. We used camera traps to investigate the behavioral responses of two ungulate species, bearded pigs (Sus barbatus) and sambar deer (Rusa unicolor), to anthropogenic disturbance in three protected areas in Sabah, Malaysia, that have varying levels of human activity. We found that human activities generally influence the activity patterns of both ungulates, albeit with variations among the sites. The temporal activity pattern of bearded pigs was affected by anthropogenic disturbance, especially in the area targeted by poachers. While the core activity pattern of sambar deer remained consistent across sites, poaching pressure appeared to impact their behavior within specific environments. Bearded pigs approached plantations at times of low human activity, presumably to forage, indicating that they adjust spatiotemporal activity patterns to minimize human contact. We observed a reduction in active times for both species at sites of high anthropogenic disturbance. Despite these challenges, both species demonstrated behavioral adaptability to anthropogenic disturbance by utilizing artificial environments such as roads and oil palm plantations as foraging places, thereby potentially compensating for reduced feeding times. Our study underscores the negative impact of human activities on the activity patterns of the two ungulate species. Nevertheless, it also highlights their behavioral plasticity in response to anthropogenic disturbance, suggesting their ability to efficiently utilize alternative food resources. Our methodology provides insights into wildlife management strategies. We recommend urgent long-term monitoring of wildlife population dynamics, including behavioral responses, especially in Southeast Asia.

Physiological responses of wildlife to disturbance

Article

Full-text available

Jan 1995

Antarctic Tourism: Environmental Concerns and the Importance of Antarctica’s Natural Attractions for Tourists

Chapter

Full-text available

Jun 2012

This chapter draws on the results of surveys of tourists who undertook an Antarctic journey in January 2003 aboard the Antarctic cruise ship, Akademik Ioffe. These surveys were designed to determine the socioeconomic profile of these travellers, to evaluate the importance to them of Antarctic wildlife for their travel, and to discover their attitudes to Antarctic wildlife conservation as well as to environmental issues involving Antarctica, both prior to and following their visit to Antarctica. This chapter reports on the socio-economic profile of respondents, their willingness to pay for their Antarctic trip, and their knowledge of Antarctica. The comparative importance of Antarctic wildlife as a factor motivating respondents to undertake their journey is assessed and the evaluation by travellers of the features of their journey following their visit is considered. The relative importance of different Antarctic wildlife species is taken into account as well as attractions other than wildlife. The attitudes of respondents to several environmental issues involving Antarctica (for example, the commercial use of its natural resources and global environmental change impacting on Antarctica) are canvassed and summarised. In the concluding section, the relevance of the survey results for Antarctic conservation is discussed. Particular attention is given to the question of whether Antarctic tourism favours or threatens Antarctic nature conservation.

Environmental stress, field endocrinology, and conservation biology

Article

Full-text available

Jan 1997

Heart rate and energy expenditure of incubating wandering albatrosses: basal levels, natural variation, and the effects of human disturbance

Article

Feb 2002

We studied the changes in heart rate (HR) associated with metabolic rate of incubating and resting adult wandering albatrosses (Diomedea exulans) on the Crozet Islands. Metabolic rates of resting albatrosses fitted with external HR recorders were measured in a metabolic chamber to calibrate the relationship between HR and oxygen consumption (V̇O2) (V̇O2=0.074×HR+0.019, r2=0.567, P<0.001, where V̇O2 is in ml kg–1 min–1 and HR is in beats min–1). Incubating albatrosses were then fitted with HR recorders to estimate energy expenditure of albatrosses within natural field conditions. We also examined the natural variation in HR and the effects of human disturbance on nesting birds by monitoring the changes in HR. Basal HR was positively related to the mass of the individual. The HR of incubating birds corresponded to a metabolic rate that was 1.5-fold (males) and 1.8-fold (females) lower than basal metabolic rate (BMR) measured in this and a previous study. The difference was probably attributable to birds being stressed while they were held in the metabolic chamber or wearing a mask. Thus, previous measurements of metabolic rate under basal conditions or for incubating wandering albatrosses are likely to be overestimates. Combining the relationship between HR and metabolic rate for both sexes, we estimate that wandering albatrosses expend 147 kJ kg–1 day–1 to incubate their eggs. In addition, the cost of incubation was assumed to vary because (i) HR was higher during the day than at night, and (ii) there was an effect of wind chill (<0°C) on basal HR. The presence of humans in the vicinity of the nest or after a band control was shown to increase HR for extended periods (2–3 h), suggesting that energy expenditure was increased as a result of the disturbance. Lastly, males and females reacted differently to handling in terms of HR response: males reacted more strongly than females before handling, whereas females took longer to recover after being handled.

THE ROLE OF GENETIC VARIATION IN ADAPTATION AND POPULATION PERSISTENCE IN A CHANGING ENVIRONMENT

Article

Feb 1996
EVOLUTION

THE EVOLUTION OF FORM AND FUNCTION: MORPHOLOGY AND LOCOMOTOR PERFORMANCE IN WEST INDIAN ANOLIS LIZARDS

Article

Aug 1990
EVOLUTION

Jonathan B Losos

I tested biomechanical predictions that morphological proportions (snout-vent length, forelimb length, hindlimb length, tail length, and mass) and maximal sprinting and jumping ability have evolved concordantly among 15 species of Anolis lizards from Jamaica and Puerto Rico. Based on a phylogenetic hypothesis for these species, the ancestor reconstruction and contrast approaches were used to test hypotheses that variables coevolved. Evolutionary change in all morphological and performance variables scales positively with evolution of body size (represented by snout-vent length); size evolution accounts for greater than 50% of the variance in sprinting and jumping evolution. With the effect of the evolution of body size removed, increases in hindlimb length are associated with increases in sprinting and jumping capability. When further variables are removed, evolution in forelimb and tail length exhibits a negative relationship with evolution of both performance measures. The success of the biomechanical predictions indicates that the assumption that evolution in other variables (e.g., muscle mass and composition) did not affect performance evolution is probably correct; evolution of the morphological variables accounts for approximately 80% of the evolutionary change in performance ability. In this case, however, such assumptions are clade-specific; extrapolation to taxa outside the clade is thus unwarranted. The results have implications concerning ecomorphological evolution. The observed relationship between forelimb and tail length and ecology probably is a spurious result of the correlation between these variables and hindlimb length. Further, because the evolution of jumping and sprinting ability are closely linked, the ability to adapt to certain microhabitats may be limited.

Ovis ammon

Article

Jul 2005

Interaction between wildfowl and recreation at Llangorse Lake and Talybont Reservoir, South Wales

Article

Jan 1983

The role of body condition on breeding and foraging decisions in albatrosses and petrels

Article

Jan 1999

Henri Weimerskirch

Ligand-dependent down-regulation of stably transfected human glucocorticoid receptors is associated with the loss of functional glucocorticoid responsiveness.

Article

Dec 1992

The effect of glucocorticoids on the regulation of stably transfected human glucocorticoid receptors has been examined. Exposure of a Chinese hamster ovary-derived cell line containing stably transfected human glucocorticoid receptor genes and glucocorticoid-responsive dihydrofolate reductase genes to 5 nM dexamethasone resulted in a rapid, time-dependent reduction in the level of glucocorticoid receptor protein to 50% of control levels within 5 h of steroid treatment. This decrease in receptor protein was persistent, with a maximal 70% reduction observed even after 4 weeks of dexamethasone treatment. Immunocytochemical analysis of the influence of dexamethasone on stably transfected glucocorticoid receptors revealed efficient translocation of receptors to the nucleus within 1 h of hormone treatment. However, upon longer exposure to dexamethasone (5 h), immunoreactive glucocorticoid receptors were localized primarily to the cytoplasm. By 24 h of treatment, glucocorticoid receptors were absent from the cyt...

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