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Biologiral Journal of the Linncan Socity (1984), 23: 269-286. With 1 figure
Enemy free space and the structure of
ecological communities
M. J. JEFFRIES AND J. H. LAWTON
Department of Biology, University of York, Heslington, York YO1 5DD
Acccptcd for publication May I983
We define ‘enemy free space’ as ways of living that reduce or eliminate a species’ vulnerability to
one or more species of natural enemies. Many aspects of species’ niches, in ecological and
evolutionary time have apparently been moulded by interactions with natural enemies for enemy
free space. We review a large number of examples. Yet many ecologists continue to think and write
as though classical resource based competition for food or space is the primary determinant of
species’ niches. Often it is not. The recognition that the struggle for enemy free space is an
important component of many species’ ecologies may have important consequences for studies of
community convergence, limits to species packing, and the ratio of predator species to prey species
in natural communities.
KEY WORDS:-Natural
structure.
enemies - interspecific competition
-
niche - escape space - community
C0N TEN TS
Introduction . . . . . . . . . . . . . . .
Historical perspective . . . . . . . . . . . . .
Theoretical arguments: a brief summary . . . . . . . .
Examples . . . . . . . . . . . . . . . . .
Species exclusion by natural enemies: community composition effects
Fixed and flexible responses . . . . . . . . . .
Evolution and enemy free space . . . . . . . . .
Taxonomic range . . . . . . . . . . . . .
Consequences . . . . . . . . . . . . . . .
Caveats and conclusions . . . . . . . . . . . .
Acknowledgements
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References.
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INTRODUCTION
Ecological theory relies heavily on the notion that species’ niches are moulded
primarily by interspecific competition for limited resources, particularly food
(e.g. Hutchinson, 1957; MacArthur & Levins, 1967; MacArthur, 1970, 1972;
May & MacArthur, 1972; May, 1974). In ecology texts, niche theory and
interspecific competition for limited resources are often discussed together (e.g.
Krebs, 1978; Pianka, 1978; May, 1981). Predation, if it is discussed at all in this
context, is usually regarded as something which modifies the primary role of
interspecific competition, for example by promoting co-existence of potential
0024-4066/84/120269+ 18 $03.00/0
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01984 The Linnean Society of London
270
M. J. JEFFRIES AND J. H. LAWTON
competitors. Only in marine (e.g. Paine, 1966) and freshwater systems (Zaret,
1980) has predator-structuring of ecological communities been coherently and
extensively studied.
This paper reviews the role of natural enemies in moulding ecological niches.
Our aim is to show how many numerous aspects of the ecology of animal species
that are traditionally reviewed as components of their niche, (body size, feeding
stations, feeding methods, etc.), have been influenced, not by competitors, but
by natural enemies. Although all ecologists recognize that this must be so, many
continue to act and write as though classical resource-based competition,
especially for food, is the primary constraint operating on species’ niches, and to
interpret community structure in this light. Hence, we have assembled a wide
range of examples illustrating the extent to which natural enemies influence
species niches.
‘Niche’ can be defined in several ways (Elton, 1927; Hutchinson, 1957, 1978;
Whittaker et ul., 1973; Maguire, 1973). For present purposes, differences
between these definitions are unimportant. Ecologists use the niche concept in
its broadest sense to discuss a number of questions. Are there limits to the
number of co-existing species in communities, i.e. are there limits to niche-space
and niche-overlap? How and why do species differ in their use of resources, i.e.
what is the significance of differences between species? These are some of the
questions that we address in this paper.
Species’ niches are influenced by many variables, including the physical
environment, the nature and rate of supply of food resources, interspecific
competition for limiting resources such as food or space and natural enemies.
Because natural enemies have so often been ignored, we wish to focus on their
effects, This does not mean we believe that other forces moulding species’ niches
are unimportant. The idea of predator moulded niches is not a new one.
Connell (1975) and Zaret (1980) cover many examples; Salt (1967) suggests the
inter-relatedness of prey and predator niches, and our tables show the repeated,
independent discovery of these same ideas. This review draws the disparate
examples together.
Twenty-five years ago. Williamson (1957) argued cogently that the
consequences for two species sharing a natural enemy are, in general terms,
iden tical to more conventional forms of interspecific competition for limiting
resources. Indeed, Lotka (1925: 94) makes much the same point. These
theoretical arguments were elaborated by Holt (1977) (see below), who coined
the term “apparent competition” for cases where two or more victim species
interact via a shared enemy, or enemies. Lotka, Williamson and Holt show that
the abundance of species may be reduced, or species eliminated entirely from a
community by populations of polyphagous enemies sustained by alternative
prey species. Hence there may be competition between victim species for
“enemy free space”. By enemy free space we mean ways of living that reduce or
eliminate a species’ vulnerability to one or more species of natural enemies.
Absolute enemy free space is extremely rare in nature. Life styles that reduce or
eliminate attacks by one group of enemies will usually expose victim species to
alternative modes of attack. Species co-existing and surviving in a community
have by definition found sufficient enemy free niche space to sustain their
populations. Inter aliu, species may be eliminated from a community because
they are critically vulnerable to one or more species of resident natural enemy;
ENEMY FREE SPACE
271
and in the long run species may evolve to reduce this vulnerability (Vermeij,
1982). Hence a study of enemy free space has two components, contemporary
interactions taking place in ‘ecological time’ and much longer responses in
‘evolutionary time’.
Our aim in this review is not to show how predators control species diversity,
except in passing. Such data have already been summarized by Connell (1975)
and Zaret (1980) amongst others. Rather our objectives are:
(1) to show how species niches are influenced by the presence or absence of
natural enemies, in ecological and evolutionary time;
(2) to summarize examples of species competing via shared natural enemies,
and to clarify the nature of enemy free space;
(3) to consider the sorts of communities where competition for enemy free
space may be paramount in determining community structure;
(4) to consider the implications of enemy free space arguments for such
phenomena as community convergence, limits to species packing and the ratios
of number of predator species to number of prey species in ecological
communities.
By ‘enemy’ we mean any consumer that eats living victims; these need not be
only conventional predators, they may also be insect parasitoids hunting for
hosts (Askew, 1971; Hassell, 1978), or even internal parasites (Freeland, 1983).
Our own expertise and knowledge of the literature is unevenly distributed across
these three types of enemy, being strongest in the first two. We have, for good
measure, included some plant (victim)-herbivore (enemy) examples, although
our main emphasis is on animals and their enemies. For convenience, we have
used ‘predation’ to include attack by all these enemies. We have made no
attempt to provide an exhaustive review, but have assembled examples that are
familiar to us. We believe they are sufficient to sustain our case.
HISTORICAL PERSPECTIVE
The notion that species may compete for enemy free space has a long history.
T o our knowledge the idea has been explicitly formulated by at least 15 authors,
or implicitly developed or hinted at by several others (Table I ) , but for some
reason it has never received full attention, nor do workers in independent fields
always appreciate that much the same mechanism is a t work in many types of
ecological system. All the papers in Table 1 explicitly argue that major aspects
of species’ lifestyles (i.e. niche) are moulded by the impact of natural enemies.
Charles Darwin was the first to argue this when he wrote (quoted in
Hutchinson, 1978: 153) “one is sometimes tempted to conclude, falsely as I
believe, that nature has worked for mere variety. Thus when we h e a r . . . that
M r Bates collected within a days journey, in a quite uniform part of the valley of
the Amazons, 600 different species of butterflies one may at first doubt whether
each is adapted to its own peculiar and different line of life; but from what we
know of our own British Lepidoptera we may confidently believe that most of
the 600 caterpillars would have different habits, or be exposed to different
dangers from birds and hymenopterous insects”: In other words, many of these
species characteristics are important for avoiding natural enemies.
After this paper was accepted for publication, Dr R. D. Holt kindly drew our
attention to a further important historical example. Grinnell (1917) in his
M. J. JEFFRIES AND J. H. LAWTON
272
Table 1. Papers developing the concept of enemy free space, in date order, by
author. Numbers refer to these examples in the text.
Source
I Darwin
2 Brower (1958)
3 Askew (1961)
4 Moment (1962)
5 Huffaker (1971)
6 Root (1973)
7 Hebert cf al. (1974)
8 Gilbert (1975)
9 Ricklefs & ORourke (1975)
10 Zwoelfer (1975)
11 Charnov cf al. (1976)
12 Orians & Solbrig (1977)
13 Otte & Joern (1977)
14 Schultz cf al. (1977)
15 Lawton (1978), Lawton &
Strong (1981)
16 Price cf al. (1980)
1 7 Zaret (1980)
18 Atsatt (1981)
19 Kitchell cf al. (1981)
20 Freeland (1983)
System
Amazonian Lepidoptera
Phytophagous insects
Role of enemy free space
See text
Pressure to diversify to avoid
predation
Oak gall wasps and parasites Evolution of vaned gall shapes to
minimize attacks by others’
parasi toids
Many Phyla
Notes individual variation; suggests
this aids predator avoidance.
“Reflexive evolution”
Many systems
Suggest role of predator pressure in
diversification
Insect communities
Role of enemy free space hinted at for
system structuring
Canadian moths
Most abundant species had fewest
close relatives, suggesting shared
predation upon similar species may
reduce numbers of each
Hcliconius and PasnjYora species Plant diversity dictated by number of
leaf shape options to avoid other
species’ caterpillar attackers
Tropical and temperate moths Moth aspect diversity shows consistent
limits. Siggests limit.to enemy free
space
Insects
Explicitly discusses insect speciation
and role of enemy free space in niche
differentiation
Many systems
Complementarity of predator
avoidance and system structuring
Number and variety of ‘hiding places’
Insects on desert bushes
profoundly influences community
structure
Grasshoppers
System diversity related to “Escape
space”
Insects on Creosote bush,
Number and variety of ‘hiding places’
profoundly influences community
L.uwca sp.
structure
Phytophagous insects
Pressure to avoid other species’
predators; enemy free space may
mould community form
Role of plant/herbivore interaction in
Phytophagous insects
avoiding predation. Use term “Escape
Space”
Freshwater zooplankton
Role of enemy free space identified in
communities
detail
Lycaenid butterflies
Lycaenid radiation and patterns of
host use linked to use of ant-associated
enemy free space
Fossil gastropods
Predation produces competition
among prey species to reduce
attractiveness towards predators
Explicitly identifies parasites as being
Animal hosts
of major importance in determining
niche differences between host-species
ENEMY FREE SPACE
273
famous paper on the niche of the California thrasher concluded that cover for
escaping predation is an essential component, and that ‘it is not any peculiarity
of food-source, or way of getting at it’, that alone limits the thrasher’s niche ( p
432). As Dr Holt pointed out to us, it is ironic that one of the very first instances
of the use of the word ‘niche’ in ecology emphasized predation rather than
competition as a constraint.
THEORETICAL ARGUMENTS: A BRIEF SUMMARY
Consider the simplest possible case of whether or not a species can invade and
maintain itself in an established community. As Holt (1977) shows the
conditions for invasion are identical to those needed for the invader to have a
positive equilibrium density in the community, namely that its rate of increase
must be higher than the rate at which established polyphagous natural enemies
find and destroy it.
Formally, for invasion and establishment:
?> ujp
(1)
Where ?=instantaneous rate of increase of invading victim species j ;
uj= attack rate (or area of discovery-see Varley et uf., 1973; Hassell, 1978) of
an established natural enemy population on species j ;
p = density of established polyphagous enemies.
Characteristics of species j that reduce uj, for instance their size, colour or
feeding place, will favour the establishment o f j in the community. Clearly, the
more speciesj differs from victim populations already in the community the less
likely enemies are to recognize it as food, or the less likely they are to be able to
deal with it successfully (i.e. the lower f j ) and the more likely speciesj is to
invade. Likewise small densities of established enemies (p small) brought about
by a shortage of alternative victim populations will also favour the establishment
of j . In general terms such effects are identical to those seen in more
conventional cases of competition, promoting co-existence of species with
different ecologies, invasion in the absence of similar species and exclusion in
their presence.
Species may, of course, fortuitously possess characteristics that allow them to
invade an established community. In a n ideal world such preadaptions (or
exaptations”, Gould & Vrba, 1982) should be distinguished from character
evolution as a direct result of predation (e.g. Vermeij, 1982). Unfortunately in
the examples that follow we are often unable to do this. O u r inability to
distinguish evolved adaptations from exaptations makes little difference to
arguments about the importance of enemy free space as a force structuring
communities, but it makes a big difference to understanding the evolution of
enemy free space.
Figure 1 formulates the notion of enemy free space diagrammatically. I n this
hypothetical example three characteristics define species’ vulnerability to a set of
existing predators, body size, rate of movement and toxicity. Clearly n such axes
could exist, and the analogy with Hutchinson’s ‘hypervolume’ is very close.
(Hutchinson, 1957). In the example there are five co-existing victim species with
characteristics as indicated, subject to attack by established enemies. Invasion of
two further species is not possible, because for both equation (1) is not satisfied.
6‘
M. J. JEFFRIES AND J. H. LAWTON
274
Increasing speed
o f movement
4
Increasing
body size
Increasing
toxity
Figure 1 . Hypothetical example of species’ characteristics that determine their vulnerability to
natural enemies. Five species (solid dots) are established in the community, with characteristics of
speed of movement, size and toxicity as indicated. Two further species ( A and B) are excluded by
the established natural enemies of species 1-5 because they possess characteristics that make them
particularly vulnerable to predation. (See text for further discussion.)
In one case (B, Fig. 1) we might imagine that the potential invader is too similar
to one set of established species; the other potential invader (A, Fig. 1) is very
slow, non-toxic and hence very vulnerable.
A moment’s thought makes plain that enemy free space is unlikely to be fixed.
In any habitat, it will depend upon the nature of established victims and
enemies, as well as on the size and age of the potential invader. We return to
these problems later. They do not make the concept of enemy free space
impossible to work with. They do mean that critically testing the idea in real
communities requires care and thought.
EXAMPLES
Despite such complication, examples of enemy free space and predator
moulded niches abound in the literature. I t is to these that we now turn.
Table 2 summarizes a wide range of examples of enemy free space in
ecological communities, grouped by habitat and by taxa within habitat. Each
example has been given a number as have the examples in Table 1. The
phenomena gathered together in Tables 1 and 2 are many and varied, but each
illustrates one or more aspects of the broad problem of enemy free space as
follows.
Species exclusion by natural enemies: community comfiosition efects
Experimental manipulation of predators in communities often reveals victim
species that are unable to survive in the presence of particular enemy species.
275
ENEMY FREE SPACE
Table 2. Examples of enemy free space in a wide variety of ecological systems,
grouped by taxa and habitat and thereafter in date order. Numbers refer to
examples in the text.
Source
Freshwater systems
21 Porter (1973)
22 Briand & McCauley
(1979)
Victim
Enemy
Nature of enemy free space
Phytoplankton
Zooplankton
S, M and other (toxins)
Phytoplankton
Zooplankton
S. Sized based differential
predation
M. Spined morphs in e.f.s.
Rotifers
Invertebrate predators S, M. Size morph based
differential predation
23 Gilbert (1967)
24 Kerfoot (1977)
Rotifers
Zooplankton
25 Hebert & Loaring
( 1980)
Zooplankton
26 Hrbacek (1959)
Zooplankton
27 Brooks & Dodson
( 1965)
Zooplankton
Fish
28 Rief and Tappa (1966) Zooplankton
Fish
29 Galbraith (1967)
Zooplankton
Fish
30 Green (1967)
Zooplankton
Fish
31
Zooplankton
Fish
32 Zaret (1969)
Zooplankton
Fish
33 Zaret (1972)
Zooplankton
Fish
34 Allen (1974)
Zooplankton
Fish
35 Stich & Lampert (1981)Zooplankton
Fish
Brooks (1968)
36 Sprules (1972)
37 Giguere (1979)
Zooplankton
Zooplankton
38 Lynch (1979)
39 Stein & Magnuson
(1976)
Zooplankton
40 Johnson & Crowley
( 1980a)
41 Johnson & Crowley
(1980b)
42 James (1967)
43 Bay (1974)
44 Hulbert el al. (1972)
Invertebrate predators S, M. Size morph based
differential predation
S, M. Size morph based
Fish
differential predation
Salamander
Salamander and
Chaoborus
Salamander
S, P. Differential predation
of sizes and littoral/pelagic
morphs
S. Differential predation of
sizes
S. Differential predation of
sizes
M. Differential predation of
morphs
S. M. Differential predation
of sizes and morphs
M. Differential morph
predation
M. Differential morph
predation
S. Size based differential
predation in a model system
P. Differential predation
based on position in water
column
S. Differential size predation
S. Differential size
predation
S. Differential size predation
S, M, P. All criteria alter
e.f.s.; crayfish may change
many aspects of behaviour
in presence of a predator
P. Differential predation
Fish
Odonata larvae
based on microhabitat
available
P. Differential predation
Fish
Odonata larvae
based on microhabitat
available
Invertr 'ate pre tors P. Differential predation
Mosquito larvae
based on position in pond
Invertebrate predators P. Differential predation
Mosquito larvae
based on position in pond
Most prey not in enemy
Many invertebrate taxa Fish
free space. Differential
predation of some due to
position
Crayfish
Fish
M. J. JEFFRIES AND J. H.LAWTON
276
Table 2.
45
Source
Victim
Kerfoot (1982)
Many invertebrate taxa Various
46 McPhail (1969)
47
Moodie (1972)
Enemy
Sticklebacks
Fiah
Sticklebacks
Fish
48 Fraser & Ccm (1982) Minnows
Fish
49 Morin (1981)
Tadpoles
Salamander
50 Sih (1981, 1982)
Freshwater systems
Coastal and shallow marine systems
51 Randall (1965)
Sea grass
Fish
52 Paine (1969)
Gastropods
Starfish
53 Vermeij (1974)
Gastropods
Fish and crabs
54 Dayton (1971)
Barnacles
Limpet
55 Coen ct al. (1981)
Shrimps
Fish
56 Birkeland (1974)
Sea pen
Starfish
57 Menge (1976)
Rocky shore system as a
whole
58 Vance (1979)
Rocky shore system as a
whole
59 Campbell & Denno
(1978)
Salt marsh pool
invertebrates
60 Evans (1979)
Benthic and burrowing Shore-birds
invertebrates
Terrestrial invertebrates
61 Coeden & Louda
(1976)
Fish
Biological control agents Predators and
(phytophagous insects) parasitoids
62 Heinrich (1979)
Caterpillars
Various
63 Polis (1980)
Scorpions
Scorpions
64 Thornhill (1980)
Scorpion flies
Various
65 Opler (1981)
Mantispidi
Various
Nature of enemy free space
Other. Distaste and
a m m a t i c coloration
M. Morph bared
differential predation
M. Morph bared
differential predation
P. Change in distribution
in presence of predator
Differential predation of
species. Precise form of e.f.s.
not identified
Predator avoidance has a
major effect on species’
feeding ecology
P. Differential predation
based on distance from reef
that harbours fish. Reef in
e.Es. for the fish themselves
P. Position on shore
determines e.f.s.
S, M. Shells give e.Es.
Global and local scale
S, M. Differential resistance
to limpet grazing size and
morph based
P. e.f.s. based on
microhabitat
Other. Specific defences
against certain species of
starfish
P. Barnacle dominance on
upper shore due to absence
of predation high up shore
Most species of plant lost
due to urchins. No e.Es. A
few have morphological
e.Es.
Others. Toxic corixids in
e.ts. Other species removed
by fish
P. Position in mud changes
vulnerability
Some introduced biological
control agents arc not
successfid because they are
attacked by local predators.
Not in e.Es.
P. Foraging position gives
efs.
P. Position of feeding sites
and activity patterns affect
e.Es.
P. E.Es. gained from
position in vegetation
M. Role of e.Es. and
mimicry d i s c u d
ENEMY FREE SPACE
277
Table 2.
Source
Terrestrial vertebrates
66 Janzen (1976)
Victim
Enemy
Reptiles (African)
Various
67 Carlquist (1965)
Endemic bird species,
often flightless
68 Barnard (1979)
House sparrow
69 Howe (1979)
Frugivorous birds
70 Nilsson (1979)
Passerines
71 Grubb & Greenwald
( 1982)
72 Karr (1982)
Sparrows
73 Patterson & Pascual
( 1968)
S American fossil
74 Barbehenn (1969)
Small mammals
75 Grant (1972)
Snowshoe and Arctic
hares
76 Leuthold (1977)
African ungulates
Terrestrial vegetation
77 Janzen (1966)
Ground feeding birds
marsupials
Suggests paucity of reptile
species due to low e.f.s.largely positional
Various, e.g. cats, rats, Many examples of
extinctions on islands are
man
due to lack of e.f.s. against
new predators
P. Feeding sites selected to
Sparrowhawks
reduce predation
P. Feeding sites selected to
Various
reduce predation
P. Feeding sites selected to
Sparrowhawks
reduce predation
P. Feeding sites selected to
Various
reduce predation
Extinctions caused by lack
Snakes, coatis
of e.f.s.
N American mammal Extinction of marsupial
herbivores may be due to
predators
lack of e.f.s. from invading
predators. Prey actually
duplicate predators’
previous prey type due to
convergence, but lack coevolved defences
P. Community defined by
Parasites
resistance to parasites.
Cannot invade areas
containing parasites of
other species to which own
species is not immune
P. Arctic hare’s reduction
Lynx
due to alternative prey
increasing lynx numbers
Mammalian predators P. Differ in drinking sites
due to predation
Thorn acacia
Phytophagous insects
78 Harper (1969)
Plants
Herbivores
79 Gilbert (1971)
Passijlora spp.
Heliconiid butterflies
Microbial systems
80 Mitchell (1971)
81 Levin el a f . (1977)
Microbial communities
Escherichia coli
Nature of enemv free space
T. phage
Other. Acacias derive
protection from ant
association
Several instances of role of
e.f.s. given e.g. Hypericum
perfliatum in shade
M. Trichome defence in
some species
Immigrant species do not
flourish, have no e.f.s. to
resident pathogens
M. Differential morph
resistance to 7.
phage attack
The nature of enemy free space (e.f.s.) classifies the means of avoiding or reducing the impact of natural
enemies under three broad headings: M, morphology, e.g. possession of a shell, or defensive exoskeleton; S,
size, i.e. the species is too small or too large to be attacked by resident enemies; P, position occupied in the
habitat reduces or eliminates predation. Other mechanisms embrace a ragbag of alternatives, including
toxicity, speed of movement etc.
278
M.J. JEFFRIES AND J. H.LAWTON
For these victims of predation, enemy free space in the community in question is
absent or too scarce a resource to ensure survival. At least one species, often
more, falls into this category in many of the examples in Table 2.
There is then a continuum of examples from total vulnerability to complete
indifference to the presence or absence of particular predators. Examples of
species immune to attacks of specific predators within a system can be found in
several references (Table 2).
Hence, predators may have profound effects in determining which, and how
many species co-exist in ecological communities. This point has been made by
Connell (1975), Zaret (1980) and other workers. The control of species numbers
is, however, only one part of the problem. There are a whole set of important,
but largely ignored questions about the characteristics distinguishing vulnerable
species from non-vulnerable species, and how the non-vulnerable species escape
enemies.
Species may avoid predation in many ways (see Zaret, 1980 for detailed
comments on freshwater systems), but we can classify these into three broad
groups, listed in Table 2 as size (S), morphology (M) and position (P), together
with a ragbag of mechanisms (‘other’) that do not conveniently fall into any
category. The effects of size, position and morphology may be evaluated intraor interspecifically. No one species of predator has infinitely flexible hunting
behaviour; so what constitutes enemy free space against one species, or guild, of
predators may make a victim hopelessly vulnerable to others. T h e species that
co-exist in one habitat do so because they are not fatally vulnerable to any of the
enemies in that habitat. Usually we have no idea how this is achieved for all
the enemies that a species may be exposed to, but we do know, or can guess,
how it is achieved for particular enemies and potential victims (summarized in
Table 2).
Enemy free space may be achieved for some species by virtue of their size;
they are either too large or too small to be killed by the predator(s) (e.g. Table
1: 17; Table 2: 22, 24, 25, 26, 27, 28, 29, 31, 34, 35, 36, 37, 38, 54). Similarly
they may have morphologies that markedly reduce or eliminate predation
(Table 1: 3, 8; Table 2: 21, 23, 25, 26, 30, 31, 32, 33, 46, 47, 54, 79, 81) or they
may occupy parts or places in the habitat where they are not vulnerable (e.g.
Table 2: 40, 41,42, 43, 44, 51, 52, 55, 57, 60, 74, 78). These three characteristics
of size, morphology and position in the habitat are the very same criteria often
given as ‘separating’ species in classical competition theory. Body size and
position in the habitat, particularly feeding sites, are often cited as niche
characteristics moulded by ‘conventional’ forms of competition for limiting food
or space. Table 2 makes it obvious that the need to avoid enemies had identical
effects.
Morphological defences and many of the miscellaneous ways of avoiding or
reducing predation (e.g. Table 2: 21, 56, 59, 65), are not usually cited as being
directly influenced by interspecific competition for limiting resources. However,
if species have evolved particular ways of avoiding predation, this may
automatically impose constraints on many aspects of their ecology. Hence, many
other aspects of a species’ niche may be a secondary, but inevitable,
consequence of selection pressures imposed by predators, not competitors; or a
compromise between the need to minimize the risk of predation, and the effects
of competition.
ENEMY FREE SPACE
279
Fixed andjexible responses
Some species minimize or avoid the effects of certain predators because of
genetically fixed features of their ecology; their size, shape or feeding site (e.g.
Table 2: 27, 39, 42, 43, 46, 47, 65, 79). Some species display genetically flexible
responses over several generations in the face of selection by predators (e.g.
Table 2: 23). Still others change their short term behaviour, adopting one
feeding mode or site in the absence of a predator and another in its presence
(Table 2: 39, 48, 50, 68, 70, 71). This process has previously been called
‘depression’ by Charnov et al. (1976). Prey availability is lowered under
predation, without necessarily any harvesting. There may be a brief, local
behavioural change in prey availability or a longer term change.
Several workers on optimal foraging theory have recently discussed risk
avoidance by victims (e.g. Hassell & Southwood, 1978). This is exactly the
problem of predators inducing short-term changes in a species’ feeding niche. I n
the absence of a predator individuals may prefer to forage in one particular part
of their habitat. In the presence of a predator behaviour changes markedly,
foraging in the preferred site is abandoned or much reduced, and foraging
concentrated in safer places (Table 2: 39, 48, 50, 68, 69, 70, 71). Such ‘niche
shifts’ by the same species in different places are often attributed to changes in
competitors (e.g. Diamond, 1975). They may equally well be due to the
presence or absence of particular enemies.
Sometimes vulnerability to enemies is altered by whether or not a second
enemy involved. Parasites may modify host niches to enhance their host’s
vulnerability and so ensure their being eaten by the next host in the parasite’s
life-history (Holmes & Bethel, 1972). Alternatively insect parasitoids may alter
host behaviour to lessen predation by normal host enemies. Fritz (1982) cites
examples involving movement reduction, microhabitat shifts and morphological
changes in parasitized hosts. In all such cases the parasitelparasitoids are
manipulating host enemy free space to increase their own survival.
Enemy free space considerations may impinge widely upon other behaviours,
not strictly of ecological interest. We include two examples for completeness.
Strong (1973) demonstrates that predation is a powerful modifier of amplexus in
amphipods. Those in amplexus are more conspicuous and slower (reduced
enemy free space). The time spent in amplexus correlated negatively with
degree of predation, even in populations only a short distance apart. Similarly,
mating calls in tropical frogs may be impaired by the presence of predatory bats
(Tuttle & Ryan, 1981).
Evolution and enemy free space
The universal distribution of means of defence against enemies of one form or
another, of mimicry, camouflage, aposematic coloration, spines, toxins, armour
and so forth attests to the enormous selection pressures imposed by enemies
upon their victims (see Vermeij, 1982 for recent discussion).
What is not clear is how many of the examples of enemy free space
summarized in Tables 1 and 2 are genuine cases of evolution or even of coevolution of sets of victim species with one or more enemies, and how many are
fortuitously evolved characteristics selected for in other circumstances and/or by
280
M. J. JEFFRIES AND J. H. LAWTON
other enemies in other habitats that now permit species to co-exist with little or
no evolutionary history-exaptations in the sense of Gould & Vrba (1982).
Distinguishing exaptations from evolved adaptations from co-evolution is a
major challenge for future research. However, it would be bizarre if many
predators have not played some part in the evolution of defences of prey that
they feed upon at the present time. In other words, many of the niche
characteristics influenced by predation, summarized in Table 2. are evolved
responses to contemporary enemies. Others have undoubtedly been evolved in
response to enemies long gone. Co-evolution, the reciprocal long-term
evolutionary interaction of a n enemy and its victims is a more difficult problem.
For example, Vermeij (1982) has recently retracted his earlier views (e.g.
Vermeij & Covich, 1968) that enemy and victim are locked into an
evolutionary ‘arms race’. The conditions under which co-evolution is to be
expected are much more restricted than commonly supposed (Thompson,
1982).
Problems of co-evolution aside, it does not seem to be widely appreciated how
rather small differences between individual victims may radically alter
predation pressures and hence selection pressures. Consider the case where
predators forage optimally (see Krebs & Davies, 1978). Now, quite small
changes in prey body size or in the form and strength of protective cases may
sufficiently alter the predator’s ratio of food gain to effort as to make a
previously desirable victim species no longer profitable, and vice versa. A former
victim may simply be dropped from the optimum diet set if the predator’s ratio
of energy gain to handling time with that victim falls below a critical level.
Livdahl ( 1979) reports interesting differences in predator handling times with
the same species of mosquito larvae collected from areas with and without
predators; handling times were longer and hence prey profitability was less in
mosquitoes from areas exposed to predation.
The evolutionary implication of small changes in prey profitability are easy to
envisage. Community effects are less clear. They suggest that enemy free space
may depend critically on the relative profitabilities and abundances of other
species in the habitat, making it difficult to discover why a species is able to
invade one habitat, but not another area supporting the same, or similar,
enemies, but different victims.
Taxonomic range
The effect of enemy free space is very clear and well documented in
freshwater planktonic systems and is apparently the major factor determining
species composition, with ‘classical’ interspecific competition only secondarily
affecting the details of community structure (Zaret, 1980). Phytophagous insect
communities also appear to provide some clear examples (Lawton & Strong,
1981; Strong, Lawton & Southwood, 1984). However, all taxa and habitats are
represented to some extent in Tables 1 and 2, although major differences in the
importance and mode of action of enemy free space are to be expected. Most
important, Table 2 is not a random sample of the world’s biota and the
distribution of examples across habitats and taxa are determined to a
considerable extent by our own grasp of the literature, and a predisposition of
workers on particular taxa or habitats to ignore or be interested in enemy free
ENEMY FREE SPACE
28 1
space. The distribution of examined material certainly does not reflect the
importance of enemy free space in nature.
Bird populations, for example, have traditionally been regarded as food
limited (Lack, 1966) and sets of bird species are widely assumed to be structured
by interspecific competition for food (e.g. Cody, 1974; Diamond, 1975), but
even here the role of natural enemies in determining the presence of absence of
species, their distribution and feeding niches cannot be ignored (e.g. Table 2:
68, 69, 71, 72).
In passing it is worth noting an important difference between ‘enemy effects’
and ‘competitive effects’. Interspecific competition for food by definition implies
density dependent resource limitation. Niche differences and community
structure determined by conventional competition are extremely unlikely
without density dependent resource limitation (see Strong et al., 1984; Lawton,
1984 for further discussion). But we do not think it is necessary for species to be
controlled by predation (in a direct or delayed density dependent fashion) for
competition for enemy free space to be a significant ecological and evolutionary
force. Predation may kill species in a density independent manner or inverse
density dependent manner and selection will still favour not being killed. Hence
one cannot deduce the likely importance of enemy free space in structuring a
community or moulding niches from the nature of the density dependent
controlling mechanisms (or lack of them) operating on species in a community.
CONSEQUENCES
The examples summarized in Tables 1 and 2 point logically to two
conclusions, and lead us to speculate about two interesting theoretical
possibilities.
First, niche differences between similar species sharing a habitat, ‘co-existing
species’, might often just as easily be explained by the effects of natural enemies
as by more conventional competitive effects. Wherever populations of
polyphagous natural enemies are sustained by more than one species of prey,
selection may favour divergence in the characteristics of one or more of those
prey species to minimize the impact of the natural enemy.
Of course other scenarios are possible. Species may converge on the same
solution, enhancing species’ similarities. Other ‘differences between species’ and
the niche characteristics of particular species may be imposed by selection from
strictly monophagous enemies, and so on. Our aim is not to become embroiled
in such possibilities at this stage, but merely to remind ecologists of the profound
effect that predators have upon species’ niches, and by so doing divert attention
away from the widely held, and in our opinion, mistaken, view that niche
differences between species are usually due to the historical effects of ‘classical’
resource based competition. The effects of competition for enemy free space
deserve much more serious study.
Second, numerous examples of niche shifts now exist in the literature, when a
particular species behaves in one way in one community or place, but behaves
differently somewhere else. Such niche shifts are almost invariably attributed to,
or correlated with, the presence or absence of competition. Table 2 gives several
examples where niche shifts appear to be due to the presence or absence of
particular natural enemies. These changes in feeding behaviour, feeding site and
282
M. J. JEFFRIES AND J. H. LAWTON
so on may be facultative and flexible or apparently genetically fixed in different
populations. We do not argue that all niche shifts are enemy induced. We do
argue that ecologists rarely consider enemies, and too often consider
competitors, as the explanation for niche shifts when they find them.
From the empirical base established in Tables 1 and 2 speculation is easy. We
restrict ourselves to two possibilities, namely problems of convergence in
community structure and the ratio of predators to prey in food webs.
The theoretical arguments of Williamson (1957) and Holt (1977) (loc. cit.),
show that competition for enemy free space has many of the consequences of
more traditional forms of competition: limits to the number of co-existing species
in a community, niche differences between species and so forth. But, whereas
standard competition for limiting resources may, at least in theory, lead to
convergence in community structure under similar climatic conditions (for
discussion see Orians & Solbrig, 1977; Cody & Mooney, 1978), communities
constrained by natural enemies will not converge unless the enemies are the
same, or have similar properties, in the same environments. Zaret (1980)
discusses this problem at length for the effects of fish predation on the structure
of freshwater communities. This problem is worthy of more theoretical and
empirical attention. We see no reason why convergence in community structure
should necessarily be expected, even under similar climatic conditions, if
communities of predators and prey start off, by chance, from different initial
conditions, as often they must. Enemy free space depends on the nature of the
predators, which often depend upon the nature of the prey, and simultaneously
upon selection pressures being imposed by what everybody else is doing. We see
no reason why this lottery should have only one unique configuration of niche
space as its end point.
But, given that only a limited number of prey types are able to co-exist with a
particular type of predator, competition for enemy free space does lead to one
interesting general feature of communities: namely, a broadly constant ratio of
prey (victims) to predators (enemies) in food webs (e.g. Arnold, 1972; Cameron,
1972; Cohen, 1977, 1978; Moran & Southwood, 1982). The data on which such
a generalization is based is nothing like as reliable as we should wish and our
interpretation may simply be wrong (see for example Evans & Murdoch, 1968
versus Cole, 1980), in which case, speculation is idle. But if the data are even
crudely correct, then a constant ratio of prey to predators in food webs may find
its underlying theoretical explanation in competition for enemy free space
among victim species and limits to the number of species able to co-exist with
different species of predators (seeJeffries & Lawton, 1984 for further discussion).
CAVEATS AND CONCLUSIONS
Niche differences between species driven by competition for enemy free space,
indeed the whole notion of enemy free space, is only a hypothesis. Tables 1 and
2 do not test the hypothesis, or any of its corollaries in detail. They merely
gather evidence that is broadly in agreement with these ideas. It will require
great efforts to distinguish the relative roles of predation and competition in
moulding species’ niches and community structure in particular systems. Zaret’s
(1980) work on freshwater communities is a pioneering example.
Our main purpose in this paper has been to gather comparable examples
ENEMY FREE SPACE
283
from a large number of different systems, illustrating the independent discovery
of the same basic idea many times over. These examples are now so many that
we do not understand why so many ecologists continue to write and think about
niches and community structure as though they were almost always moulded by
classical interspecific competition for limiting resources such as food. Enemy free
space deserves more critical attention.
ACKNOWLEDGEMENTS
Professor Mark Williamson, Doctors Phillip Crowley and Malcolm
MacGarvin, Philip Heads, and Simon Fowler read and made very helpful
comments on earlier drafts of this paper. Dr R. D. Holt drew our attention to
several early examples, particularly those by Lotka and Grinnell. M. J. Jeffries
is supported by an NERC studentship.
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