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Habitat heterogeneity and mammalian


predatorprey interactions

Article in Mammal Review April 2011


DOI: 10.1111/j.1365-2907.2011.00189.x

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Mammal Rev. 2011

REVIEW
Habitat heterogeneity and mammalian
predatorprey interactions

Lucrezia GORINI* Hedmark University College, Department of Applied Ecology and


Agricultural Sciences, Evenstad, NO-2480 Koppang, Norway, and Department of
Animal and Human Biology, University of Rome La Sapienza, Viale dellUniversit
32, 00185, Rome, Italy. E-mail: lucrezia.gorini@hihm.no
John D. C. LINNELL Norwegian Institute for Nature Research, Tungasletta-2,
NO-7485 Trondheim, Norway. E-mail: john.linnell@nina.no
Roel MAY Norwegian Institute for Nature Research, Tungasletta-2, NO-7485
Trondheim, Norway. E-mail: roel.may@nina.no
Manuela PANZACCHI Norwegian Institute for Nature Research, Tungasletta-2,
NO-7485 Trondheim, Norway. E-mail: manuela.panzacchi@nina.no
Luigi BOITANI Department of Animal and Human Biology, University of Rome
La Sapienza, Viale dellUniversit 32, 00185, Rome, Italy.
E-mail: luigi.boitani@uniroma1.it
Morten ODDEN Hedmark University College, Department of Forestry and Wildlife
Research, Evenstad, NO-2480 Koppang, Norway. E-mail: morten.odden@hihm.no
Erlend. B. NILSEN Norwegian Institute for Nature Research, Tungasletta 2,
NO-7485 Trondheim Norway. E-mail: erlend.nilsen@nina.no

ABSTRACT
1. In predatorprey theory, habitat heterogeneity can affect the relationship
between kill rates and prey or predator density through its effect on the predators
ability to search for, encounter, kill and consume its prey. Many studies of predator
prey interactions include the effect of spatial heterogeneity, but these are mostly
based on species with restricted mobility or conducted in experimental settings.
2. Here, we aim to identify the patterns through which spatial heterogeneity affects
predatorprey dynamics and to review the literature on the effect of spatial hetero-
geneity on predatorprey interactions in terrestrial mammalian systems, i.e. in freely
moving species with high mobility, in non-experimental settings. We also review
current methodologies that allow the study of the predation process within a spatial
context.
3. When the functional response includes the effect of spatial heterogeneity, it
usually takes the form of predator-dependent or ratio-dependent models and has
wide applicability.
4. The analysis of the predation process through its different stages may further
contribute towards identifying the spatial scale of interest and the specific spatial
mechanism affecting predatorprey interactions.
5. Analyzing the predation process based on the functional response theory, but
separating the stages of predation and applying a multiscale approach, is likely to

*Correspondence author.

2011 The Authors. Mammal Review 2011 Mammal Society


2 L. Gorini et al.

increase our insight into how spatial heterogeneity affects predatorprey dynamics.
This may increase our ability to forecast the consequences of landscape transforma-
tions on predatorprey dynamics.

Keywords: anti-predator behaviour, functional response, hunting behaviour,


predation stage, spatial features
Mammal Review (2011)
doi: 10.1111/j.1365-2907.2011.00189.x

INTRODUCTION
The past 70 years have seen the development of a large body of theory in predation
ecology that has centred on the concept of functional response (Solomon 1949,
Holling 1959). In its simplest form, the functional response relates predator kill rate,
i.e. the number of prey items killed by a predator in a given time interval, to prey
and/or predator density. Most of the predictions derived from this theoretical back-
ground find support in model systems and experiments, but they rest on a number of
assumptions that are usually violated in heterogeneous biological systems (see
Jeschke et al. 2002 for a review of the functional response). Spatial heterogeneity is
one of the factors affecting the rate at which a predator can kill and consume its prey.
The form of predatorprey interactions in heterogeneous and dynamic landscapes
may deviate significantly from that of interactions in homogeneous and static systems
such as the environments used in controlled experiments and model simulations. The
spatially mediated mechanisms that affect kill rates can ultimately be related to the
fact that spatial heterogeneity introduces a difference between the total prey popu-
lation density and the proportion which the predator has the potential to kill and
consume. If this difference is not taken into account when estimating the form of a
functional response, the outcome may be biased, or the type of functional response
may be mistaken (e.g. Nachman 2006). A large body of empirical and theoretical
evidence, including that based on invertebrate systems (Gause 1934, Huffaker et al.
1963, Luckinbill 1974, Pacala et al. 1990, Denno et al. 2005, Bergstrm et al. 2006),
suggests that spatial heterogeneity may affect predatorprey dynamics through a
number of mechanisms (e.g. altered prey vulnerability or predator hunting success).
Most studies of predatorprey interactions including the effect of spatial heteroge-
neity have so far been based on highly simplified experimental conditions (Sih 2005):
either the predator or the prey species has reduced mobility (or is caged) or the
predators presence is simulated (but see also Lima 2002). Studies of the spatial
distribution and habitat selection of highly mobile terrestrial mammals as a response
to predation risk and prey availability confirm, however, the importance of spatial
heterogeneity in understanding observed kill rates (e.g. Hebblewhite et al. 2005,
Hopcraft et al. 2005, Kauffman et al. 2007, Zub et al. 2008). For instance, trait-
mediated mechanisms (sensu Preisser et al. 2005) induced by perceived predation risk
have the potential to affect prey population dynamics more strongly than kill rates, as
these also involve the individuals that are not consumed (Preisser et al. 2005). Spatial
heterogeneity may affect prey vulnerability, and therefore determine the relative
importance of these induced behavioural responses on predatorprey interactions
(Luttbeg et al. 2003). Alteration of kill rates associated with habitat-dependent prey
vulnerability and predator hunting success in simple one prey/one predator systems

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Predatorprey interactions in a spatial world 3

may have consequences on other trophic levels and the overall food web (Denno et al.
2005 and references therein). Changes in the landscape caused by human activity are
among the most important drivers affecting species and ecosystems worldwide
(Houghton 1994, Noss et al. 1997) and urge the understanding of the impact of spatial
heterogeneity on predatorprey and community dynamics.
In this review, we aim to explore how habitat spatial heterogeneity may affect
predatorprey dynamics in terrestrial mammalian systems, i.e. in systems character-
ized by highly mobile species, and focus on predation by mammals on mammals with
a few exceptions of avian predation on mammals. We provide evidence from the
literature that the consequences of spatial heterogeneity on anti-predator behav-
iour, hunting strategy or risk perception in natural conditions are essential for
improving our understanding of predatorprey dynamics. We emphasize the impor-
tance of separately investigating the effect of spatial heterogeneity on each of the
four stages of predation described by Endler (1986), i.e. searching, encountering,
killing and consuming prey. We will also touch on wider consequences: how changes
in predatorprey interactions may influence the overall community. Lastly, we will
review models and field methods that have the potential to take spatial heteroge-
neity into account and suggest directions for further research.

EFFECTS OF SPATIAL HETEROGENEITY ON PREDATORPREY INTERACTIONS


Spatial heterogeneity can modify the form of the functional response by introducing
a difference between the total prey population density and the proportion that is
actually available to the predators. Predator habitat selection can often best be
explained by the hunting success associated with certain habitat types (e.g. Hopcraft
et al. 2005), or by constraints such as territoriality and competition that violate the
assumptions of the ideal-free distribution (e.g. Kauffman et al. 2007). Spatial het-
erogeneity can thus modify prey availability through several mechanisms that can be
grouped based on the stage of the predation process, i.e. searching, encountering,
killing and consuming prey (Endler 1986), which they affect (Tables 1 and 2).

First and second stages: searching and encountering


The distribution and detection probability of prey can influence the search efficiency
of predators. The spatial distribution of predators and prey is largely the result of
trade-off decisions between energy intake, risk of predation and intra-guild compe-
tition (Palomares & Caro 1999, Linnell & Strand 2000, Lima 2002) causing spatial
variation in reproduction and mortality rates. Prey can respond to predator presence
by avoiding areas or patches with high predator density or perceived risk (Lima & Dill
1990). This type of behavioural response may be particularly strong during certain
phases of the individuals life when its own survival or that of its offspring is critically
dependent on access to safe structures such as nests and den sites (Olsson et al. 2008),
and behavioural flexibility is necessary to maintain high fitness (Charnov 1976). Shifts
in space use may also be responses to temporal variation in predation risk (Lima & Dill
1990), i.e. prey may use a given high-quality habitat, or may venture farther from a
safe but poor habitat, depending on the presence or absence of predators at the fine
temporal scale (e.g. Creel & Winnie 2005, van Dijk et al. 2008). Behavioural responses
including alteration of fine-scale habitat use induced by risk perception alone may
affect a larger number of prey individuals than is actually killed and consumed by a
predator, and may therefore strongly affect predatorprey dynamics (Luttbeg &

2011 The Authors. Mammal Review 2011 Mammal Society


Table 1. Evidence, from the literature, of the effect of habitat spatial heterogeneity on the predation process in terrestrial mammalian systems

Stage of predation Mechanism Predator Prey Reference

Search efficiency and Space use Canis lupus Cervus elaphus Creel and Winnie (2005)
encounter probability alteration C. lupus C. elaphus Fortin et al. (2005b)
4 L. Gorini et al.

Human caused mortality Lynx lynx Bunnefeld et al. (2006)


C. lupus C. elaphus Christianson and Creel (2008)
Puma concolor Ovis canadensis Wehausen (1996)
Canis latrans Odocoileus virginianus, Odocoileus Lingle (2002)
hemionus
P. concolor, C. lupus C. elaphus, O. hemionus Atwood et al. (2009)
C. lupus C. elaphus Mao et al. (2005)
C. lupus C. elaphus Creel et al. (2006)
C. lupus C. elaphus Creel et al. (2008)
C. lupus Rangifer tarandus caribou Wittmer et al. (2007)
Migratory ungulates Fryxell et al. (1988)
C. lupus O. virginianus, C. elaphus, Alces alces Kunkel et al. (2004)
Detection Panthera pardus 6 ungulate species Balme et al. (2007)
probability Martes americana Myodes gapperi (former Clethrionomys Andruskiw et al. (2008)
gapperi)
Vulpes vulpes Capreolus capreolus Panzacchi et al. (2009, 2010)
Mortality mainly due to Panthera leo Acynonix jubatus Laurenson (1993)
C. lupus C. elaphus Hebblewhite et al. (2005)
C. lupus, L. lynx, Gulo gulo, Ursus Several prey species May et al. (2008)
arctos
Kill Refuges Mustela nivalis nivalis Rodentia Oksanen et al. (2001)
M. nivalis nivalis Rodentia Ylnen et al. (2003)
Small Mustelida Myodes glareolus Sundell and Norrdahl (2002)
M. nivalis nivalis, Mustela erminea Microtus agrestis, sibling vole Microtus Norrdahl and Korpimki (2005)
rossiaemeridionalis
M. nivalis nivalis Rodentia Zub et al. (2008)
C. lupus A. alces Kunkel and Pletscher (2000)
V. vulpes C. capreolus Panzacchi et al. (2010)
P. pardus, P. leo Papyo cynocephalus ursinus Cowlishaw (1997)
C. lupus, P. concolor C. elaphus, O. hemionus Atwood et al. (2007)

2011 The Authors. Mammal Review 2011 Mammal Society


Hunting A. jubatus Different medium-sized herbivores Mills et al. (2004)
strategy P. concolor O. hemionus Pierce et al. (2004)
P. concolor Antilocapra americana Ockenfels (1994)
C. lupus C. elaphus Hopcraft et al. (2005)
C. lupus C. elaphus Kauffman et al. (2007)
M. americana M. gapperi Andruskiw et al. (2008)
C. latrans Lepus americanus Thibault and Ouellet (2005)
Accipiter nisus Several avian species Cresswell et al. (2003)
Anti-predator A. jubatus Gazella thomsoni Fitzgibbon (1994)
tactic C. lupus, P. concolor C. elaphus, O. hemionus Husseman et al. (2003)
P. concolor O. hemionus Pierce et al. (2004)
P. concolor, C. lupus C. elaphus, O. hemionus Atwood et al. (2009)
P. leo Connochaetes taurinus Fryxell et al. (2007)
V. vulpes C. capreolus Panzacchi et al. (2009)
Kill Physical Two potential predators: C. lupus, A. alces Dussault et al. (2005)
features Ursus americanus
(snow C. lupus O. virginianus, C. elaphus, A. alces Kittle et al. (2008)
depth, C. lupus, C. latrans, G. gulo Large ungulates Telfer and Kelsall (1984)
rainfall) G. gulo Rangifer tarandus Landa et al. (1999)
C. lupus, P. concolor C. elaphus, O. hemionus Husseman et al. (2003)
C. lupus A. alces Post et al. (1999)

2011 The Authors. Mammal Review 2011 Mammal Society


Martes martes Rodentia Helldin (2000)
C. lupus C. elaphus Huggard (1993)
P. leo 12 prey species Owen-Smith and Mills (2008)
C. lupus O. virginianus, C. elaphus Kunkel et al. (2004)
Consumption Kleptoparasitism A. jubatus Mills et al. (2004)
C. lupus C. elaphus Huggard (1993)
Scavenging C. lupus C. elaphus Hopcraft et al. (2005)
C. lupus C. elaphus Wilmers et al. (2003)

The evidence is grouped according to the stage of the predation process (see text and Endler 1986) and according to the spatial mechanisms that each
study is focused on. A few studies are included in more than one group, as the authors analyzed more than one stage of predation. Species are given by
their scientific names to avoid confusion.
Predatorprey interactions in a spatial world 5
6 L. Gorini et al.

Table 2. Summary of the effect that each spatially mediated mechanism can have on the
encounter, kill and consumption rate

Mechanism Effect

Encounter rate
Shift in space-use of the prey In most cases it decreases the encounter rate
Use of risky habitat types due to: low In most cases it increases the encounter rate
availability of safe habitat types, inter- and
intra-specific competition
Use of cover (sensu Mysterud & stbye 1999) It can increase or decrease the encounter rate
depending on the species community
composition
Occurrence of snow It can increase or decrease the encounter rate
depending on the specific hunting behaviour
Kill rate
Cover (sensu Mysterud & stbye 1999) It decreases the kill rate
Snow It increases the kill rate
Poor physiological condition of the prey It increases the kill rate
associated with space use
Consumption rate
Caching in open areas It decreases the consumption rate due to
kleptoparasitism

The dominant effect (i.e. the most common one) based on the literature is shown. See the text
for further discussion on each of the mechanisms.

Kerby 2005). At a larger spatial scale, migratory movements may primarily represent
an optimization of the use of food resources but may also render the individuals less
vulnerable to predation if the predator is not capable of following its prey (Fryxell
et al. 1988, Skogland 1991, but see Hofer & East 1993, Forbes & Theberge 1995,
Walton et al. 2001). All these shifts in space use can strongly decrease prey availabil-
ity and encounter rates, both temporally and spatially. Therefore, failure to consider
space shifts in research may lead to an overestimation of prey availability, unless
shifting habitat use increases vulnerability to another co-occurring predator (see
below). However, when either the availability of high-quality habitats is low or when
individuals are energetically stressed, prey may be forced to use patches in which
predation risk is high (Lima & Dill 1990, Hugie & Dill 1994, Sinclair & Arcese 1995,
Battin 2004) or may be forced to increase their inter-patch movements (Johannesen
et al. 2003). Although other anti-predator responses may occur in these cases, such as
increased vigilance, decreased foraging time or changes in group size (e.g. Laundr
et al. 2001), the search efficiency of the predator probably also increases (e.g. Storaas
et al. 1999). Hence, by increased chances of encountering prey due to increased
inter-patch movements or use of risky habitats, the proportion of prey available to a
given predator may increase. It would be valuable to investigate if and under which
conditions the increase in inter-patch movements or use of risky habitats may lead to
a shift from food-limited (i.e. bottom-up) to predator-driven (i.e. top-down) popu-
lation dynamics.
Variation in cover availability in different habitat types can greatly affect the
predators search efficiency (Caro 2005). The term cover includes any structural
or non-structural feature of the landscape which protects, hides or conceals
(sensu Mysterud & stbye 1999). Structural features are those provided by vegeta-
tion and topography, including canopy and ground cover, shelters and bed-sites.

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Predatorprey interactions in a spatial world 7

Well-hidden dens, nests and dense vegetation associated with certain habitat types
may decrease prey detection probability, particularly for specific age-classes (Fortin
et al. 2005a, Hebblewhite et al. 2005, Panzacchi et al. 2009), thus decreasing the
amount of available prey. Habitat types with dense vegetation cover may also be
risky for the prey due to their reduced chances of detecting an approaching preda-
tor. Besides vegetation cover, snow can provide shelter for burrowing species but
can also hinder movements, and hence result in increased use of corridors where
the probability of encountering a predator is high (e.g. Post et al. 1999). Specialist
predators such as small mustelids may benefit from a well-developed layer of snow,
as they rely on the subnivean space when hunting microtines (Hansson & Henttonen
1988, Oksanen et al. 2001 and below). It has been suggested that a decreased
amount of snow-cover in winter may on the other hand improve the hunting
efficiency of generalist predators such as the red fox Vulpes vulpes at the expense of
the specialist weasel Mustela nivalis nivalis, and thus alter the population dynamics
of their microtine prey (Oksanen et al. 2001). In summary, the spatially mediated
mechanisms discussed here can lead to either overestimation or underestimation of
prey availability, depending on whether their effect on the encounter rate is positive
or negative.

Third and fourth stages: killing and consuming


Provided that prey is encountered, a predator may still not be capable of capturing
and killing it. There might be a danger associated with the prey (e.g. due to
competing predator individuals or prey defence responses); the predator might be
prevented from capturing or killing the prey by spatially mediated mechanisms such
as habitat differences in availability of escape structures or presence of physical
obstacles (a river, a fence), or the likelihood of capture and killing might be
affected by habitat-dependent prey vulnerability and hunting success, conditions of
the terrain (e.g. snow depth) or physiological condition of the prey (see Table 1 for
references on each of these). Escape structures such as holes, burrows, cliffs or
dense vegetation inaccessible to predators are regarded as refuges (Caro 2005) but
are sometimes included in a more general definition of cover (see above, Mysterud
& stbye 1999). If the number of individuals that can use refuges is constant, and
the availability of refuges is a limiting factor, there is a density dependent feedback
on predation rates (Berryman & Hawkins 2006), and competition mechanisms arise
for the limiting resource (see also the concept of a doomed surplus; Errington
1963).
Both prey and predators are capable of adjusting their respective anti-predator or
hunting strategy based on the habitat type they are using (e.g. Fitzgibbon 1994,
Kunkel et al. 1999). For instance, prey can adjust group size, vigilance or activity
patterns depending on the degree of visibility (Fitzgibbon 1994, Panzacchi et al.
2010). Similarly, a given predator can behave as an ambush stalker in wooded
habitats and as a cursorial hunter in open habitats (e.g. Cresswell 1996). If these
spatially mediated factors are not taken into account, prey availability may be
overestimated in the first example or underestimated in the second one. Open
habitats usually imply high visibility and high encounter rates but also cause prey to
be more easily alerted, and thus affect the distance at which a hunter may start the
chase attempt (Mills et al. 2004). The chance of a successful hunt for a cursorial
predator depends more on the type of terrain through which the pursuit takes place

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8 L. Gorini et al.

than on the habitat features where it detects its prey. On the contrary, an ambush
predators success depends more on the cover present where prey is detected, as this
affects the distance at which the chase can start (Husseman et al. 2003, see below).
The amount of cover can also affect the preys capacity to exploit refuges, and
hence its chances of escaping an attack (Sundell et al. 2008). Variation in snow depth
and consistency associated with different habitat types can affect the pursuit success
of a cursorial predator. Certain prey species may become accessible to a predator
(e.g. Landa et al. 1999), or a specialist predator may be capable of exploiting its
limited niche (e.g. Oksanen et al. 2001), only when specific snow conditions are
present. Within a prey community, however, the effect of snow depth may be
stronger on some prey species than on others, and may thus affect prey mortality
patterns for different species differentially (Kittle et al. 2008). The capacity of a prey
to escape an attack may also depend on its physiological conditions which, in turn,
can be a consequence of space use. For instance, avoidance of high-quality habitats
as an anti-predator response or because of temporal variation in the physical con-
ditions of the habitat (e.g. yearly variation in amount of snow) may have costs for the
physiological state of individuals and, in turn, alter their vulnerability to predation
(Post et al. 1999, Abramski et al. 2002, Creel et al. 2006, Christianson & Creel 2008) or
their reproductive output (Hik 1995). All these mechanisms can affect the chances of
a predator successfully killing its prey, and may therefore lead to either an overes-
timation or an underestimation of prey availability.
Once a kill is made, further spatially mediated mechanisms can affect the con-
sumption rate. During the period of time in which a carcass is consumed, it might be
scavenged or kleptoparasitized by other predatory or scavenger species (e.g. Kac-
zensky et al. 2005). If a kill is made in an open habitat, it might be exploited by
scavengers or kleptoparasitized by dominant predators more rapidly because of the
higher visibility (Mills et al. 2004). Caching behaviour may decrease the accessibility
of carcasses to scavengers, and thereby affect the consumption rates of both scav-
enger and killer. Even when a carcass is cached, however, the chances of other species
scavenging on the carcass are affected by its location. Snow depth or dense under-
growth, for instance, may reduce the chances of finding a carcass by affecting
the movement rates and distances travelled (Huggard 1993, Wilmers et al. 2003).
However, when carcasses of individuals dying due to starvation or diseases are
scavenged, their location is often associated with high prey density areas (Hopcraft
et al. 2005).
Thus, spatial heterogeneity can lead to an increase or a decrease in kill rates
depending on the specific behavioural characteristics of the species considered (e.g.
cursorial and ambush stalker, see below) and the community composition. Differ-
ences in hunting behaviour or alternative prey availability may explain the switch
from a type 2 to a type 3 functional response for the same predator in two differ-
ent areas (Keith et al. 1977, ODonoghue et al. 1998). Particularly in the case of
habitat fragmentation and loss, the effect of spatial heterogeneity on generalist
and specialist species may lead to very different consequences both for predators
and for prey populations (Ryall & Fahrig 2006). Generally, mechanisms of interfer-
ence between species in a community that are mediated by spatial heterogeneity,
such as predator interference (Preisser et al. 2005, Berec 2010), are very common,
and the potential for consequences on community dynamics deserves careful
investigation.

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Predatorprey interactions in a spatial world 9

SPATIAL HETEROGENEITY AND THE IMPACTS OF COMMUNITY STRUCTURE ON


PREDATORPREY INTERACTIONS
Predators can affect the population dynamics of their prey directly through the
number of prey individuals killed, and indirectly through trait-mediated or indirect
density-mediated mechanisms, such as behavioural responses to predation risk (Pre-
isser et al. 2005) or apparent competition (Holt & Lawton 1994). For instance, when
prey face predation from multiple predator species, their behavioural responses may
be complex: shifting habitat use to reduce the probability of being detected by one
predator species may simultaneously increase the chances of encountering another
one. Hence, by shifting to a densely forested area, prey may decrease their vulner-
ability to a cursorial predator while simultaneously increasing it to a stalker (e.g.
Atwood et al. 2009). Similarly, use of a certain habitat by a given prey species may
decrease its exposure to an avian predator and increase its exposure to a terrestrial
predator (e.g. Korpimki et al. 1995). According to Preisser et al. (2005), predator-
predator facilitation accounts for ca. 50% of the total trait-mediated effects of
predation on prey survival, which suggests that it may be a relatively common
mechanism. On the other hand, intra-guild competition is widespread among
mammals (Palomares & Caro 1999) and may result in spatial avoidance (e.g. Helldin
et al. 2006) or reduced scavenging opportunities. Carcasses can be a valuable
resource for predators within the same guild but can also be very risky places (e.g.
Linnell & Strand 2002, van Dijk et al. 2008). Intra-specific competition among preda-
tors may also limit the use of habitats that provide good hunting grounds (Kauff-
man et al. 2007), and hence affect hunting success. Similarly, sympatric prey species
may compete for access to refuges and safe dens (Koivunen et al. 1998), thus affect-
ing their relative vulnerability to predation. The use of different hunting strategies
in different habitats may reduce potential conflicts within a community, at least
when the densities of the competing species are not very high and habitat availabil-
ity allows it (May et al. 2008). Similarly, the hunting strategy of a predator may be
more successful on one of two sympatric prey species, if the different vulnerability of
the prey species is associated with different habitat features (Lingle 2002, Sundell
et al. 2008). Cursorial predators tend to select weak individuals and have a relatively
low hunting success (Kunkel et al. 1999) compared with stalking predators. Differ-
ence in prey selection affects the demography, and thus population dynamics of the
prey population. It has been suggested that differences in environmental sensitivity
among functionally similar species (e.g. coyote Canis latrans and wolf Canis lupus)
favour community stability, whereas differences in sensitivity among functionally
different species (e.g. ungulate prey vs. large carnivores) make communities more
vulnerable to change (Chapin et al. 1997, Muradian 2001, Hooper et al. 2005).
More complex interactions can further affect predator and prey population
dynamics among trophic levels. If one prey species is relatively abundant, it may
support a large predator population which in turn can exert high predation pressure
on a rarer sympatric prey species (e.g. Storaas et al. 1999, Wittmer et al. 2007, Kojola
et al. 2009, Wegge et al. 2009). In community dynamics, this type of mechanism has
received increasing attention, as it has been suggested to be in some cases enhanced
by habitat fragmentation and loss, thus relating kill rates to spatial heterogeneity
(e.g. Storch et al. 2005, Wittmer et al. 2007). Certain predator species may in fact be
capable of affecting populations of different prey species not only in their usual
habitat but also in neighbouring areas through spill-over predation (Schneider 2001).

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10 L. Gorini et al.

In fragmented landscapes, the presence of predators in adjacent areas may nega-


tively affect prey species population dynamics, even if 70% of the prey species
habitat is still intact (Schneider 2001). Generalist consumers, in particular, appear to
benefit more than specialists from heterogeneous landscapes with high edge to area
ratios (Tattersall et al. 2002). This is supported both by theoretical predictions
(Melian & Bascompte 2002) and by strong empirical evidence showing an increase in
prey vulnerability parallel to the abundance and diversity of generalist predators
associated with ecotones (Angelstam 1986, Andrn & Angelstam 1988, Andrn 1994).
Hence, increased landscape heterogeneity and mechanisms of apparent competition
(sensu Holt 1977) may have combined effects on the kill rates within a community
(e.g. Oliver et al. 2009). Apparent competition has been used to explain the dramatic
decline in woodland caribou Rangifer tarandus caribou in North America and
Europe. Initially, increased timber harvesting negatively affected the demography of
the population, as woodland caribou are tightly connected to old serial forest stages
for foraging (Terry et al. 2000). However, the increase in timber harvest also ben-
efited the moose Alces alces population, which has increased in abundance. This
increase in the prey base has in turn subsidized a denser wolf population, which has
in turn further contributed to the woodland caribou decline (Seip 1992, Wittmer
et al. 2007, Kojola et al. 2009).
Much emphasis has been placed on predicting species-specific responses to habitat
fragmentation and loss in the past years, as these are considered to be among the
greatest threats to ecosystems worldwide (Soul 1991). However, most of the studies
so far have been based on short-term and small-scale field investigations, or are
flawed in other ways (see Mortelliti et al. 2010 for a review on the consequences of
habitat loss and fragmentation). In addition, few researchers have investigated in
detail the relationship between habitat loss and the structure of the community or
food web (Melian & Bascompte 2002). Including the effects of spatial heterogeneity
in community studies is challenging because of the increasing number of indirect
effects linking trophic levels; these include mechanisms of predator interference,
saturation and apparent competition, the effect of the scale of observation, and
species variation in hunting and anti-predator behaviour.
MODELLING PREDATORPREY INTERACTIONS IN SPATIALLY
HETEROGENEOUS LANDSCAPES
At the core of predatorprey theory is the concept of functional and numerical
responses (Solomon 1949). To include the effect of spatial heterogeneity on kill rates,
the classic prey-dependent functional response may be made more complex by
accounting for predator interference (Beddington 1975, Arditi & Akakaya 1990) or
aggregated spatial distributions (Cosner et al. 1999). The challenges that still remain
derive from the fact that measures of kill rates and habitat features vary with the
scale of observation (Jost et al. 2005, Bergstrm et al. 2006) and that the effect of
habitat structure on individual species may depend on their life-history traits (e.g.
Fahrig 2003). Alternative approaches such as individual-based models (e.g. Nabe-
Nielsen et al. 2010) based on simulations are beyond the scope of this review and are
not discussed here.
Functional response
Despite variation in spatially mediated mechanisms, which may affect kill rates,
simple prey-dependent functional responses are used in a remarkably large number

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Predatorprey interactions in a spatial world 11

of studies (ODonoghue et al. 1998, Jeschke et al. 2002 and references. therein). This
is because the main predictions of the functional response, i.e. kill rates reach an
asymptote at increasing prey density, and predators may switch to an alternative
prey if the density of the main prey species is below a certain threshold, can be
caused by several mechanisms. According to theory, for instance, saturation at high
prey density explains the asymptote effect and may be associated with constraints in
predators handling (and digesting) time or with local prey clumping. Among the
spatially mediated mechanisms that can cause prey switching are changes in vulner-
ability of the prey due to changes in physical condition or habitat use (e.g. Wolff
1980, McNamara & Houston 1987, Hik 1995). In general, in the forms of functional
response, which include spatial heterogeneity (e.g. non-random encounters between
predator and prey, heterogeneous distribution of the prey and/or the predator), the
effect of predator density on kill rates is explicitly added, and takes the form of
either predator dependency (Hassell & Varley 1969, Beddington 1975, Cosner et al.
1999, Jost et al. 2005) or ratio dependency (e.g. Arditi & Ginzburg 1989, Arditi &
Akakaya 1990, Jost et al. 2005). The main prediction of these types of functional
responses is that per capita kill rates decrease at increasing predator density because
of direct aggressive interactions among searching predators (McCarthy et al. 1995,
van Gils & Piersma 2004, Kratina et al. 2009); they may describe well predator
dependence at low predator densities as well (Kratina et al. 2009). Group hunting
predators may increase (e.g. by positive interference, Abrams & Ginzburg 2000) or
decrease (e.g. Fryxell et al. 2007) their per capita kill rate with increasing group size.
This provides an example of how predator interference may have both negative and
positive effects on kill rates. Furthermore, Fryxell et al. (2007) demonstrated how
prey grouping had as large an effect on per capita kill rate as predator grouping.
Thus, the functional response has the great merit of describing patterns of preda-
tion that can derive from a large number of mechanisms. However, to be useful in
practical management, the focus should be on both the form that the functional
response takes and the values of the parameters that make up the model structure.
While saturation affects the consumption rate, the effect of interference is on the
encounter rate and their impacts may counteract each other (Bergstrm et al. 2006).
A classic prey-dependent computation of the functional response may therefore fail
to detect these factors if they have opposite effects, e.g. predator interference
may decrease kill rates thus preventing the functional response from reaching the
saturation threshold. A modification of the functional response based on moment
approximation may, on the other hand, allow such distinction by using statistical
moments (e.g. variance, covariance) to estimate the effect of prey and predatorprey
density on the functional response as proposed by Bergstrm et al. (2006). These
authors applied this statistical method to a predatorprey system with invertebrate
species and obtained explicit estimates of variance and covariance effects. Because
the estimated covariance is related to predator and prey density, its effect may be
explained by an alteration of the encounter rate. On the other hand, the estimated
effect of spatial variance in prey density may be explained by local predator satura-
tion (Bergstrm et al. 2006). This difference might be important in changing land-
scapes where alterations in predatorprey systems induced by habitat fragmentation
could remain undetected at first, when the focus is on overall kill rates. Hence, spatial
heterogeneity may affect the predation process even if the form of the functional
response does not change. According to theoretical models, the effect of predator

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12 L. Gorini et al.

facilitation may also vary depending on the stage of the predation process which is
altered. It may destabilize predatorprey dynamics if it affects the encounter rate,
while it may have a stabilizing effect if it affects the consumption rate (Berec 2010).
Empirical tests of such effects would be extremely valuable as they may improve the
predictive power of the functional response associated with changes in spatial
heterogeneity.
The impact of spatially mediated effects on kill rates also depends on the spatial
scale of observation (Jost et al. 2005). Jost et al. (2005) found that predator depen-
dency and saturation were included in the best performing functional response
models at all spatial scales and suggested that kill rates in the moosewolf system on
Isle Royale, Michigan, USA should be measured per single pack as a function of
population densities over the whole island (i.e. at a mixed scale). At this spatial scale,
Jost et al. (2005) found strong evidence for a ratio-dependent functional response and
suggested that this was due to increased complexity in interference mechanisms.
However, such long-term field data are seldom available from mammalian systems
(Jost et al. 2005). In addition, and perhaps most importantly, the identification of the
precise mechanisms of predator dependency (e.g. interference or saturation) taking
place may not be possible. Models based on moment approximation have the
potential to solve this latter problem by estimating separately variance and covariance
effect but are also sensitive to the scale of observation (Bergstrm et al. 2006).
Another study from the Isle Royale system shows that variation in the availability of
vulnerable prey (i.e. moose over 9 years old) accounts for a larger portion of variation
in wolf population growth rate than other abiotic factors (i.e. stochasticity) or total
prey density (Vucetich & Peterson 2004). Determining the availability of vulnerable
prey as a function of spatial features might be a promising extension of this approach.

Spatial scale and predation stage


The effect of spatial heterogeneity on predation, as predicted by the functional
response, is also dependent on the specific predation stage. Such an effect can be
either positive or negative: high levels of habitat fragmentation may increase the
searching efficiency of a generalist predator (Storaas et al. 1999), while lack of snow
cover may hinder the killing efficiency of a specialist (Oksanen et al. 2001). This might
explain the pattern that shows a correlation between kill rates and prey density at
the landscape scale (Hopcraft et al. 2005, Zub et al. 2008) and supports the theory of
prey density-dependent kill rates (Palomares et al. 2001, Spong 2002). However,
spatially mediated mechanisms are necessary to explain the observed predation
patterns, and the functional response may change form not only at the local scale
(Hopcraft et al. 2005, Jost et al. 2005, Zub et al. 2008) but also at the landscape scale
when predator density dependency is taken into account (e.g. Abrams & Ginzburg
2000, Jost et al. 2005). Ryall and Fahrig (2006) observed in their review that while the
majority of theoretical models fit the landscape scale, most empirical studies are
conducted at the patch scale. It is therefore important that theoretical predictions of
the effects of spatial heterogeneity on the predation process are tested empirically
at the appropriate spatial scale (Bergstrm et al. 2006, Ryall & Fahrig 2006).
The effect of spatial heterogeneity on kill rates is therefore sensitive to the scale
of observation, and the specific predation stage on which habitat structure has its
strongest impact depends, among other factors, on behavioural differences
between species. For instance, in cursorial predators, such as many canids, the most

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Predatorprey interactions in a spatial world 13

Table 3. Summary of the advantages and disadvantages or potential biases of the functional
response in describing predatorprey interactions

Advantages Disadvantages/potential biases

Predictions have wide applicability Sensitive to the spatial scale of observation


Can easily be modified to take more parameters Does not distinguish explicitly between the
into account spatially mediated mechanisms which affect
Tested on a large number of studies and with final consumption rates (but see moment
different species approximation, in Bergstrm et al. 2006)

critical stage of the predation process which ultimately determines the success or
the failure of the hunt is the pursuit (Kunkel et al. 1999). The habitat type in which
the prey is encountered is therefore less important than the terrain over which the
chase takes place. On the other hand, solitary stalkambush predators, such as
many felids, rely more heavily on good cover to approach their prey (Schaller 1972,
Beier et al. 1995, Balme et al. 2007). Even for very fast predators like cheetahs
Acynonix jubatu, the distance from the prey at which the chase starts can be crucial
(Purchase & du Toit 2000, Mills et al. 2004). Hunting success for ambush predators
is therefore associated with a high degree of structural complexity, and the habitat
features of the encounter location can have a strong impact on the outcome of the
hunt (Mills et al. 2004). Hence, differences between areas selected for hunting by
different predator species can be explained by their different hunting strategies
(Balme et al. 2007). Similarly, differences in habitat use by prey species facing the
same predator may be due to differences in their anti-predator behaviour (e.g.
Lingle 2002). For instance, white-tailed deer Odocoileus virginianus are fast and
adopt a fleeing tactic against coyotes. Mule-deer Odocoileus hemionus, on the
other hand, are slower and retreat towards higher altitudes and rugged terrain to
avoid predation (Lingle 2002). The anti-predator behaviour of white-tailed deer
reduces their chances of being killed once detected, while mule deer reduce their
risk of encountering a predator.
The functional response has great potential to describe predatorprey dynamics,
taking into account spatial heterogeneity, and can take advantage of a large body of
theory. The analysis of each stage of the predation process separately may, in
addition, contribute to the identification of the spatial scale of relevance and the
specific spatial mechanism affecting predatorprey interactions. Predator- or ratio-
dependent computations of the functional response may successfully take into
account the effect of spatial heterogeneity based on final consumption rates directly
(e.g. Jost et al. 2005) but are sensitive to the scale of analyses and in most cases do
not explicitly distinguish between the specific spatially mediated mechanisms affect-
ing the interaction (Table 3). Hence, the separation between each predation stage
may contribute to our understanding of the predation process and potentially
increase our ability to forecast the consequences of landscape transformation on
long-term population dynamics.

Spatially explicit kill rates


Most empirical tests of predatorprey models including spatial heterogeneity were
conducted in experimental settings (e.g. Arditi & Ginzburg 1989, Blaine & DeAngelis

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14 L. Gorini et al.

1997, Cosner et al. 1999, Arditi et al. 2001, Bergstrm et al. 2006, Hammond et al.
2007). Furthermore, simulation models often rest on a number of assumptions that are
not realistic in biological systems under natural conditions: e.g. identical patches
(Nachman 2006), equal deterministic dynamics for all the patches after a consumer
visit (Nisbet et al. 1998) and equal predation pressure in all patches (deRoos et al.
1998). A considerable effort in field data collection is necessary in order to analyze
each predation stage separately in free-ranging highly mobile species in heteroge-
neous landscapes. The most common methods linking predation and spatial hetero-
geneity to habitat-related measures affecting prey vulnerability are summarized in
Table 4. Most of these methods allow the distinction between at least some of the
different stages of predation.
The so-called giving-up density, the density of resources within a patch at which
an individual ceases foraging (Brown 1988) separates the effects of resource
availability and perceived predation risk on prey space use (Andruskiw et al. 2008,
Searle et al. 2008) and can be combined with information on predator movements
and hunting behaviour to relate habitat heterogeneity to kill rates. Although the
method is semi-experimental and applies more easily to herbivores than to other
mammals, it has potential for wider application (see Andruskiw et al. 2008). Unless
predator presence or absence is known at any given time, however, this method fails
to take into account the effect of short-term variation in predation risk (i.e. direct
predator encounters) as opposed to long-term effects (perceived predation risk in
specific habitats). Kittle et al. (2008) showed the importance of this distinction in a
wolfungulate system.

Table 4. Field data used to


Data type Stages of predation relate kill rates to spatial
Hunting and anti-predator behaviour heterogeneity
Giving up density Kill
Consumption
Kill locations Kill
Consumption
Snow tracking Search
Kill
Consumption
Radio tracking Search
Kill
Consumption
Field observations Search
Kill
Consumption
Capturemarkrecapture Kill

Habitat features
Cover measures Search
Kill
Visibility measures Search
Kill
Distances to refuges Search
Kill

The table shows which stages of predation can be analyzed


separately through the use of certain data types.

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Predatorprey interactions in a spatial world 15

Studying kill and carcass locations (e.g. Hopcraft et al. 2005, Balme et al. 2007,
Kauffman et al. 2007) represents the final part of the predation process but, if done
in isolation, does not allow distinction between the different predation stages, nor
does the method explicitly take into account failed hunting attempts. Hence, the
locations can be used only to derive a relative measure of hunting success in relation
to spatial heterogeneity. However, in systems where kleptoparasitism and scaveng-
ing are important, analysis of kill locations is the most useful tool for investigating
the effect of habitat on the last stage of predation (e.g. Mills et al. 2004).
Data based on snow tracking have great potential, as they can provide information
on searching, failed hunting attempts and consumption rates. The major sources of
bias are in the sampling regime (e.g. the process leading to the start of the track) and
in the high variability of snow conditions, which may not permit enough of the track
to be followed. These data should therefore be combined with data from radio-
telemetry (Hebblewhite & Pletscher 2002, Andruskiw et al. 2008), which allows
the track to be calibrated against time. Also, this method is obviously temporally
and spatially constrained as appropriate snow cover is available only in certain
regions and only for a certain amount of time during the year. Direct observation of
encounters and field observations of hunting behaviour (Fanshaw & Fitzgibbon
1993, Cresswell & Quinn 2004) can also provide information on all stages of preda-
tion. However, complete observations are seldom available and may be biased by the
differential visibility afforded by different habitats.
Data on movements and behaviour of the predator obtained through Global
Positioning System-telemetry can in some cases be used to interpret hunting behav-
iour: clusters of positions observed in wolf or lynx Lynx lynx, for instance, preying on
large ungulates such as moose or roe deer Capreolus capreolus, may be interpreted
as kill sites (Sand et al. 2005, Zimmermann et al. 2007, Nilsen et al. 2009b). Caution is
needed as this method is sensitive to the radius chosen to define a cluster (Sand et al.
2005) and cannot be used for smaller prey that are consumed faster and in their
entirety. Also, it does not provide information on the encounter rates or on failed
hunts. However, it provides a large amount of data in a relatively short time, thanks
to technological improvements in radio-collar equipment (but see Hebblewhite et al.
2007) and may reduce the effort required in fieldwork (Zimmermann et al. 2007). A
combination of GPS-telemetry and observations of kill sites, together with observa-
tions of hunting behaviour from snow tracking or direct observations for validation
purposes, may, however, provide the insight into the predation process. Measures of
cover, visibility and distance to refuges can then be related to each stage of preda-
tion and can therefore provide good insight into how habitat features can affect kill
rates (Fortin et al. 2005b, Hebblewhite et al. 2005, May et al. 2008).
Use of capturemarkrecapture data (CMR, Lebreton et al. 1992) allows the estima-
tion of prey survival as a function of predator abundance and/or alternative prey
presence or absence, which can then be used to derive the functional response (Miller
et al. 2006). CMR methods have greatly advanced in recent times, making possible the
estimation of crucial demographic parameters (e.g. survival, recruitment and repro-
duction probability) as a function of environmental variation and predation (e.g.
White & Burnham 1999, MacKenzie et al. 2006, Miller et al. 2006). Similar information
on prey mortality rates can be obtained through telemetry studies (Boutin 1992),
although Marshall and Boutin (1999) have also shown that to be able to distinguish
correctly between different types of functional responses, a large data set is necessary,

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16 L. Gorini et al.

especially when a high number of parameters are estimated. As observing the


predation process throughout all the different stages poses practical challenges in
highly mobile species, CMR or telemetry data providing information on prey mortality
rates may represent a good option (Marshall & Boutin 1999, Miller et al. 2006, Nilsen
et al. 2009a). Information on changes in demographic parameters of the prey popu-
lation so obtained could also help us understand the relative roles played by the
trait-mediated mechanisms of predation (e.g. Luttbeg & Kerby 2005, Kittle et al.
2008).

DISCUSSION AND SYNTHESIS


Habitat heterogeneity introduces a difference between the total prey population
density and the proportion available to the predator. The density of vulnerable prey
may account for a larger variation in predators growth rates (i.e. numerical
response) than total prey density or stochasticity (e.g. Vucetich & Peterson 2004),
suggesting that the difference between total and available prey could have impor-
tant consequences for the population dynamics of both prey and predators. When
the functional response is calculated including the effect of spatial heterogeneity, it
generally takes the form of predator- or ratio-dependency in kill rates (e.g. Abrams
& Ginzburg 2000). As spatially mediated factors have the potential to counteract
each other under certain conditions and affect individual predation stages (e.g. prey
aggregation and predator interference), studying kill rates only might not always
reveal the underlying mechanisms. Theoretical advances in predatorprey dynamics
should be complemented by empirical analysis of (i) kill rates at different spatial
scales; (ii) the proportion of vulnerable prey within the population; and (iii) separa-
tion between each stage of predation.
The first point, analysis of kill rates at different spatial scales, allows the identifi-
cation of the scale of observation at which habitat structure becomes relevant, which
is well defined by Englund & Cooper (2003) as the smallest scale of spatial variation
in a driving variable which affects the outcome of the process. An evaluation of the
relevant spatial scale of observation could be attempted either by computing the
functional response at different spatial scales, as done by Jost et al. (2005), or by
using statistical approaches as indicated by Bergstrm et al. (2006) and references
therein. The second point, quantifying the proportion of the prey population which
is vulnerable, should be attempted following the example of Vucetich and Peterson
(2004) but also by assessing availability of vulnerable prey as a function of features
of the habitat. For instance, CMR or telemetry data can be used to model survival
rates in the prey population as functions of direct and indirect predation, alternative
prey and spatial distribution. Spatial analyses of foraging behaviour based on telem-
etry data and investigated with resource selection-based models may also help us to
understand the relationship between individuals trade-off decisions and habitat
structure (May et al. 2010). The third point, making a distinction in habitat depen-
dency between predation stages, requires, where available, knowledge of the
behavioural characteristics of both the predator and the prey species examined (e.g.
cursorial pursuit; ambushstalker encounter rate; generalist specialist). This
knowledge will not only help us to identify the most relevant landscape properties
but may also shed light on which spatially mediated mechanisms affect the predation
rate, i.e. on the distinction between saturation and interference for instance. The
dominating effect of spatial heterogeneity appears to be the dampening of oscilla-

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Predatorprey interactions in a spatial world 17

tion dynamics (Huffaker et al. 1963, Arditi & Ginzburg 1989, Oksanen et al. 1999,
Pascual et al. 2001, Melian & Bascompte 2002, but see Bergstrm et al. 2006 for an
example of the opposite effect), and a similar dampening effect is predicted for
generalist predators (Hanski et al. 1991), as they can switch to an alternative prey if
their preferred prey density falls below a certain threshold (Kjellander & Nordstrm
2003) or according to variation in prey vulnerability (Owen-Smith & Mills 2008).
However, it has also been shown that in highly fragmented landscapes, generalists
are capable of exerting high kill rates on different prey species through spill-over
predation. This trophic generalization (Melian & Bascompte 2002) is mediated by
transformations of the landscape, which lead to altered kill rates, and the conse-
quences on population dynamics differ greatly depending on the species considered
(Ryall & Fahrig 2006). As more interactions are taken into account (i.e. in community
analyses), a larger number of indirect effects appear and affect these interactions.
However, as space-use itself is the result of multiple mechanisms (e.g. predation risk,
resource availability, intra-guild interactions), insight into predation ecology through
a spatial approach may strongly increase our understanding of predatorprey
interactions in heterogeneous landscapes.

ACKNOWLEDGEMENTS
The first author was supported by an individual cultural exchange scholarship from
the Research Council of Norways international scholarship programme. The other
authors were mainly funded by the Research Council of Norways Environment 2015
programme and by the Norwegian Directorate for Nature Management.

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Submitted 5 March 2010; returned for revision 20 May 2010; revision accepted 13 December 2010
Editor: KH

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