Townsend C.R., Begon M., Harper J.L. Essentials of Ecology
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Parasites therefore include some obvious examples: animal parasites
and pathogens such as tapeworms and the tuberculosis bacterium, plant
pathogens like tobacco mosaic virus, parasitic plants like mistletoes, and
the tiny wasps that form ‘galls’ on oak leaves. But aphids that extract sap
from one or a very few plants with which they enter into an intimate
association, and even caterpillars that spend their whole life on one
host plant, are also, in effect, parasites.
On the other hand, these distinctions between ‘true’ predators, grazers and
parasites, as with most categorizations of the living world, have been drawn
in large part for convenience – certainly not because every organism fits neatly
into one and only one category. We could, for example, have included a fourth
class, the parasitoids, which are little known to non-biologists but are extensively
studied by ecologists (and immensely important in the biological control of insect
pests; see Chapter 12). Parasitoids are flies and wasps whose larvae consume their
insect larva host from within, having been laid there as an egg by their mother.
Parasitoids therefore straddle the ‘parasite’ and ‘true predator’ categories (only
one host individual, which it always kills), fitting neatly into neither and con-
firming the impossibility of constructing clear boundaries.
There is, moreover, no satisfactory term to describe all the ‘animal consumers
of living organisms’ to be discussed in this chapter. Detritivores and plants are also
‘consumers’ (of dead organisms, or of water, radiation, and so on); whilst the term
‘predator’ inevitably tends to suggest a ‘true’ predator even after we have defined
it to encompass grazers and parasites too. But neither is it very satisfactory to be
continually using the qualifier ‘true’ when discussing conventional predators.
Thus, throughout this chapter, ‘predator’ will often be used as a shorthand term
to encompass true predators, grazers and parasites, when general points are being
made; but it will also be used to refer to predators in the more conventional sense,
when it is obvious that this is what is being done.
Chapter 7 Predation, grazing and disease
219
parasitoids – and the artificiality
of boundaries
A parasitoid wasp, which uses its long ovipositor
to insert its eggs into the larvae of other insects,
where they develop by consuming their host.
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7.2 Prey fitness and abundance
The fundamental similarity between predators, grazers and parasites is that each,
in obtaining the resources it needs, reduces either the fecundity or the chances of
survival of individual prey and may therefore reduce prey abundance. The effects
of true predators on the survival of individual prey hardly need illustrating – the
prey die. But the effects of grazers and parasites can be equally profound, if more
subtle, as illustrated by the following two examples.
When the sand-dune willow, Salix cordata, was grazed by a flea beetle in
two separate years – 1990 and 1991 – the reduction in the growth rate of the
willow was marked in both years (Figure 7.1), but the consequences were rather
different. Only in 1991 were the plants also subject to a severe shortage of water.
Thus it was only in 1991 that the reduced growth rate was translated into plant
mortality: 80% of the plants died in the high grazing treatment, 40% died in the
low grazing treatment, but none of the ungrazed control plants died.
The pied flycatcher is a bird that migrates early each summer from tropical
West Africa to Finland (and elsewhere in northern Europe) to breed. Males that
arrive relatively early are particularly successful at finding mates. Late arrival
therefore has a serious detrimental effect on the expected ‘fecundity’ of a male:
the number of offspring that it can expect to father. Significantly, the later arrivals
are disproportionately infected with the blood parasite Trypanosoma (Figure 7.2).
Part III Individuals, Populations, Communities and Ecosystems
220
(a) Jul 19 – Aug 17, 1990 (b) Aug 10 – Aug 21, 1991
12345
Clone number
6789
Clone number
0.8
0.6
0.4
0.2
0.0
0.6
0.4
0.2
0.0
Relative change in height
No herbivory
Low herbivory
High herbivory
Figure 7.1
Relative growth rates (changes in
height, with standard errors) of a
number of different clones of the
sand-dune willow, Salix cordata, in
1990 (a) and in 1991 (b), subjected
either to no herbivory, low herbivory
(four flea beetles per plant) or high
herbivory (eight beetles per plant).
AFTER BACH, 1994AFTER RÄTTI ET AL., 1993
predators reduce the fecundity
and/or survival of individual prey
Early Late
Proportion of males infected
with Trypanosoma
0.5
0.4
0.3
0.2
0.1
0.0
Standardized arrival time
Figure 7.2
The proportion of males of male pied
flycatchers (Ficedula hypoleuca) infected with
Trypanosoma amongst groups of migrants
arriving in Finland at different times.
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Infection with the parasite therefore has a profound effect on the reproductive
output of individual birds.
It is not so straightforward, though, to demonstrate that reductions in the sur-
vival or fecundity of individual prey translate into reductions in prey abundance
– we need to be able to compare prey populations in the presence and the absence
of predators. As so often in ecology, we cannot rely simply on observation: we
need experiments – either ones we set up ourselves, or natural experiments set up
for us by nature.
For example, Figure 7.3 contrasts the dynamics of laboratory populations
of an important pest, the Indian meal moth, with and without a parasitoid wasp,
Venturia canescens. Ignoring the rather obvious regular fluctuations (cycles) in
both moth and wasp, it is apparent that the wasp reduced moth abundance to
less than one-tenth of what it would otherwise be (notice the logarithmic scale
in the figure).
A particularly graphic example of the impact grazers can have is provided by
the story of the invasion of Lake Moon Darra in North Queensland (Australia)
by Salvinia molesta, a water fern that originated in Brazil. In 1978, the lake carried
an infestation of 50,000 metric tons of the fern. In Salvinia’s native habitat in
Brazil, the black long-snouted weevil (Cyrtobagous spp.) was known to graze
only on Salvinia. Hence in June 1980, 1500 adults were released at an inlet to the
lake and a further release was made in January 1981. By April 1981, Salvinia was
dying throughout the lake, supporting an estimated population of one billion
beetles. By August 1981, less than 1 metric ton of Salvinia remained. This was a
‘controlled’ experiment in that other lakes in the region continued to bear large
populations of Salvinia.
All sorts of predators can cause reductions in the abundance of their prey. We
shall see as this chapter develops, however, that they do not necessarily do so.
Chapter 7 Predation, grazing and disease
221
AFTER BEGON ET AL., 1995
Time (days)
0 50 100 150 200 250 300 350 400 500
0 50 100 150 200 250 300 350 400
3.0
2.5
2.0
1.5
1.0
0.5
0.0
Log number of adults
3.0
2.5
2.0
1.5
1.0
0.5
0.0
Log number of adults
Host
Parasitoid
Figure 7.3
Long-term population dynamics in laboratory population cages of a
host (Plodia interpunctella), with and without its parasitoid (Venturia
canescens). (a) Host and parasitoid, and (b) the host alone.
predators can reduce prey
abundance – but do not
necessarily do so
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7.3 The subtleties of predation
There is much to be gained by stressing the similarities between different types of
predators. On the other hand, it would be wrong to make this an excuse for over-
simplification (there are important differences between true predators, grazers and
parasites), or to give the impression that all acts of predation are simply a question
of ‘prey dies, predator takes one step closer to the production of its next offspring’.
7.3.1 Interactions with other factors
Grazers and parasites, in particular, often exert their harm not by killing their
prey immediately like true predators, but by making the prey more vulnerable
to some other form of mortality. For example, grazers and parasites may have a
more drastic effect than is initially apparent because of an interaction with com-
petition between the prey. This can be seen in a southern Californian salt marsh,
where the parasitic plant, dodder (Cuscuta salina) attacks a number of plants
including Salicornia (Figure 7.4). Salicornia tends to be the strongest competitor
in the marsh, but it is also the preferred host of dodder. The distribution of plants
in the marsh can therefore only be understood as a result of the interaction
between competition and parasitism (Figure 7.4).
Infection or grazing may also make hosts or prey more susceptible to predation.
For example, postmortem examination of red grouse (Lagopus lagopus scoticus)
showed that birds killed by predators in the spring and summer carried significantly
Part III Individuals, Populations, Communities and Ecosystems
222
Salicornia
Cuscuta
Salicornia
Cuscuta
Salicornia Arthrocnemum
0
100
1994
60
80
(b)
20
0
25
(c)
5
10
15
20
(a)
40
Plant mass (g)
1995 1994 1995
ArthrocnemumSalicornia
Uninfected Infected
Uninfected Infected FrankeniaLimonium
Cover (%)
Arthrocnemum–Salicornia border
• Strong parasite impact
• Strong parasite preference
• Strong symmetric competition
• Strong indirect positive effect
High Salicornia zone
• Strong parasite impact
• Strong parasite preference
• Strong asymmetric competition
• Strong indirect positive effect
Limonium
Frankenia
–
–
–
+
–
–
+
Figure 7.4
The effect of dodder, Cuscuta salina,
on competition between Salicornia
and other species in a southern
Californian salt marsh. (a) A schematic
representation of the main plants in
the community in the upper and
middle zones of the marsh and the
interactions between them (solid
arrows: direct effects; dashed
arrows: indirect effects). Salicornia
(the relatively low growing plant in the
figure) is most attacked by, and most
affected by, dodder (which is not
itself shown in the figure); but when
uninfected, Salicornia competes
strongly and symmetrically with
Arthrocnemum at the Arthrocnemum–
Salicornia border, and is a dominant
competitor over Limonium and
Frankenia in the middle (high
Salicornia) zone. However, dodder
significantly shifts the competitive
balances. (b) Over time, Salicornia
decreased and Arthrocnemum
increased in plots infected with
dodder. (b) Large patches of dodder
suppress Salicornia and favor
Limonium and Frankenia.
AFTER PENNINGS & CALLAWAY, 2002
grazers and parasites may make
prey more vulnerable to other
forms of mortality
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greater burdens of the gut nematode parasite Trichostrongylus tenuis than the
birds that remained in the fall (Figure 7.5).
7.3.2 Compensation and defense by individual prey
The effects of parasites and grazers, however, are not always more profound than
they first seem. They are often less profound because, for example, individual
plants can compensate in a variety of ways for the effects of herbivory (Strauss
& Agrawal, 1999). The removal of leaves from a plant may decrease the shading
of other leaves and thereby increase their rate of photosynthesis. Or, following
herbivore attack, many plants compensate by utilizing stored reserves. Herbivory
frequently alters the distribution of newly synthesized material within the plant,
usually maintaining a balanced root : shoot ratio. When shoots are defoliated, an
increased fraction of net production is channeled to the shoots themselves; when
roots are destroyed, the switch is towards the roots. Often, there is compensatory
regrowth of defoliated plants when buds that would otherwise remain dormant
are stimulated to develop. There is also commonly a reduced subsequent death
rate of surviving plant parts.
For example, when herbivory on the biennial plant field gentian (Gentianella
campestris) was simulated by clipping to remove half its biomass (Figure 7.6a),
subsequent production of fruits was increased (Figure 7.6b), but the outcome
depended on the timing of clipping. Fruit production was much increased over
controls if clipping occurred between July 12 and 20, but if clipping occurred later
than this, fruit production was less in clipped plants than in unclipped controls.
The period when the plants show compensation coincides with the time when
damage by herbivores normally occurs.
Plants may also respond by initiating or increasing their production of defensive
structures or chemicals. For example, a few weeks of grazing on the brown seaweed
Ascophyllum nodosum by snails (Littorina obtusata) induced substantially increased
Chapter 7 Predation, grazing and disease
223
AFTER HUDSON ET AL., 1992
(a) n = 1736
(b) n = 41
0 5000 10,000 15,000 20,000 25,000 30,000
Worms per bird
0
5
10
15
20
0
5
10
15
20
25
30
Frequency (% total number of grouse)
Figure 7.5
Infection with a nematode worm parasite makes red grouse more
susceptible to predation. (a) Worm burdens of birds that are shot
for ‘sport’, which may be taken as a representative sample of the
whole population. (b) Worm burdens of those found killed by
predators. The vertical line is the mean in each case, and the worm
burdens of those caught by predators are clearly higher, typically,
than those in the population as a whole.
compensatory plant responses
defensive plant responses
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Part III Individuals, Populations, Communities and Ecosystems
224
(a)
(b)
July 12Control July 20 July 28
Date of clipping
Number of fruits
30
25
20
15
10
5
0
Unclipped Clipped
Before clipping
Figure 7.6
(a) Clipping of field gentians to
simulate herbivory causes changes
in the architecture and numbers of
flowers produced. (b) Production
of mature (maroon histograms) and
immature fruits (blue histograms) of
unclipped control plants and plants
clipped on different occasions from
July 12 to 28, 1992. Means and
standard errors are shown and all
means are significantly different
from each other (P < 0.05). Plants
clipped on July 12 and 20 developed
significantly more fruits than
unclipped controls. Plants clipped
on July 28 developed significantly
fewer fruits than controls.
AFTER LENNARTSSON ET AL., 1998
Control
Phlorotannin content
(% of dry mass)
8
6
4
2
0
Consumption (g wet mass)
0.2
0.1
0
(a) (b)
a
a
a
b
Littorina
obtusata
Momentary
clipping
Continuous
clipping
Ungrazed
control plants
Previously
grazed plants
P = 0.02
Figure 7.7
(a) Phlorotannin content of Ascophyllum nodosum plants after
exposure to simulated herbivory (removing tissue with a hole
punch) or grazing by the snail Littorina obtusata. Only the snail had
the effect of inducing increased concentrations of the defensive
chemical in the seaweed. Means and standard errors are shown.
Different letters indicate that means are significantly different
(P < 0.05). (b) In a subsequent experiment, the snails were
presented with algal shoots from the control and the snail-grazed
treatments in (a) – the snails ate significantly less of plants with
high phlorotannin content.
AFTER PAVIA & TOTH 2000
concentrations of phlorotannins (Figure 7.7a), which reduce further snail grazing
(Figure 7.7b). Interestingly, simple clipping of the plants did not have the same
effect. The snails can stay and feed on the same plant for long time periods. Induced
responses that take time to develop can still be effective in reducing damage.
The snails in Figure 7.7 suffer as a consequence of the seaweed’s response
(they eat less), and the plants benefit in that less of them is eaten. But that benefit
comes to the plants at a cost (that of producing the chemicals), and it is therefore
never straightforward to establish whether plants experience a net benefit in
the longer term. One attempt to address this question looked at lifetime fitness
of wild radish plants (Raphanus sativus) assigned to one of three treatments:
(i) grazed by caterpillars, Pieris rapae; (ii) leaf-damage controls (an equivalent
amount of biomass removed using scissors); and (iii) overall controls (undamaged).
Earwigs (Forficula spp.) and other chewing herbivores caused 100% more leaf
damage on control and damage control plants than on grazed plants, and there were
30% more phloem-sucking aphids on them (Figure 7.8a, b): the response induced
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by the caterpillars protected the plants from additional herbivory. Moreover,
despite any costs, this increased significantly (by more than 60%) the lifetime fitness
of induced plants compared to the control plants. Plants cut with scissors, on the
other hand, had 38% lower fitness than the overall controls, emphasizing the
negative effect of tissue loss without the benefits of induction (Figure 7.8c). This
fitness benefit occurred, however, only in environments containing herbivores. In
their absence, the costs of producing the chemicals outweighed the benefits and
plants suffered a reduction in fitness (Karban et al., 1999). Thus the benefits in
the presence of herbivores were net benefits: benefits outweighed costs.
7.3.3 From individual prey to prey populations
In spite of these various qualifications, the general rule is that predators are harm-
ful to individual prey. But the effects of predation on a population of prey are not
always so predictable. The impact of predation is most commonly limited by com-
pensatory reactions amongst the survivors as a result of reduced intraspecific
competition. Outcomes of predation may, therefore, vary with food availability.
When there is plenty of good food, and no competition, the effects of predation
should be detectable. But when food is short and competition intense, predation
Chapter 7 Predation, grazing and disease
225
AFTER AGRAWAL, 1998
Apr 6
0
5
10
15
Apr 20
Apr 6 Apr 20
(a)
Number of aphids per plant
0
10
30
(b)
0
1
2
3(c)
20
40
Sampling date
Leaf area damaged (%)
Plant fitness
(seeds × seed mass)
Treatment
Control
Induced
Damage
control
Figure 7.8
(a) Percentage leaf area consumed by
chewing herbivores and (b) number of aphids
per plant, measured on two dates (April 6 and
20) in three field treatments: overall control,
damage control (tissue removed by scissors)
and induced (caused by grazing of caterpillars
of Pieris rapae). (c) Fitness of plants in the
three treatments calculated by multiplying
the number of seeds produced by the mean
seed mass (in milligrams).
compensatory reactions amongst
surviving prey...
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may relieve competitive pressures and allow individuals to survive who would
not otherwise do so. The results of an experiment that tested this are shown in
Figure 7.9. The survival of grasshoppers (Ageneotettix deorum) was monitored
in caged prairie plots with food (grass) that was either plentiful (fertilized) or
limited (not fertilized), and in the presence or absence of predatory spiders. As
predicted, with plentiful food, spider predation reduced the numbers surviving:
a non-compensatory response. But with limited food, spider predation and food
limitation were compensatory: the same numbers of grasshoppers were recovered
at the end of the 31-day experiment.
Predation may also have a negligible impact on prey abundance if an increased
loss of prey to predators at one stage of the prey’s life simply leads to a decreased
loss to predators at some other stage. If, for example, recruitment to a population
of adult plants is not limited by the number of seeds produced, then insects that
reduce seed production are unlikely to have an important effect on plant popula-
tion dynamics. The point is illustrated by a study of the shrub, Haplopappus venetus,
in California (Louda, 1982, 1983). The level of insect damage to the developing
flowers and seeds was high. Experimental exclusion of flower and seed predators,
therefore, caused a 104% increase in the number of developing seeds escaping
damage. This led to an increase in the number of seedlings established. But sub-
sequently this was followed by a much greater loss of seedlings, probably to
vertebrate herbivores. As a consequence, original abundances were re-established
in spite of the short-term importance of the seed predators.
Compensation, however, is by no means always perfect. Figure 7.10, for
example, shows the results of an experiment in which Douglas fir seeds were
sown both in open plots and in plots screened from rodents and birds. The
immediate effect of this was an enormous reduction in the loss of seeds (though
the screens were not totally effective). There were, however, compensatory
increases in mortality from other causes. Nonetheless, in spite of this, the over-
all effect of screening was to more than double the number of seedlings still
surviving 1 year after germination.
Part III Individuals, Populations, Communities and Ecosystems
226
No spiders, no fertilizer
No spiders, fertilizer
Spiders, no fertilizer
Spiders, fertilizer
20155
0
0
1
2
3
10 25 30 35
Log
e
(number of grasshoppers)
Time (days)
Figure 7.9
Trajectories of numbers of grasshoppers surviving
(mean ± SE) for fertilizer and predation treatment
combinations in a field experiment involving caged
plots in the Arapaho Prairie, Nebraska, USA.
AFTER OEDEKOVEN & JOERN, 2000
. . . but compensation is often
imperfect
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Chapter 7 Predation, grazing and disease
227
AFTER LAWRENCE & REDISKE, 1962
Rodent
and bird
pre-germination
18%
Other
pre-germination
35%
Post-
germination
13%
Surviving
8%
Germination
period
26%
Rodent and bird
pre-germination
3%
Other
pre-germination
35%
Post-
germination
17%
Surviving
17%
Germination
period
28%
Open Screened
Figure 7.10
When Douglas fir seeds are protected
from vertebrate predation by screens, the
lowered mortality is compensated for
(but not fully compensated for) by
increased mortality from other sources.
AFTER FITZGIBBON & FANSHAWE, 1989; FITZGIBBON, 1990
Percentage
80
60
40
20
0
80
60
40
20
0
Fawns
Half-growns
Adolescents
Fawns
Half-growns
Adolescents
Fawns
Half-growns
and adolescents
Adults
Subadults
Adults
Percentage of chased
gazelles escaping
Distance lost (m)
2.0
(a) (b) (c)
1.5
1.0
0.5
0.0
–0.5
–1.0
–1.5
Killed by cheetahs
Killed by wild dogs
Percentage in population
Figure 7.11
(a) The proportions of different age classes (determined by tooth wear) of Thomson’s gazelles in cheetah and wild dog kills is quite different from
their proportions in the population as a whole. (b) Age influences the probability for Thomson’s gazelles of escaping when chased by cheetahs.
(c) When prey (Thomson’s gazelles) zigzag to escape chasing cheetahs, prey age influences the mean distance lost by the cheetahs.
predators often attack the
weakest and most vulnerable
Predators may also have little impact on prey populations as a whole because
of the particular individuals they attack. Many large carnivores, for example,
concentrate their attacks on the old (and infirm), on the young (and naive) or on
the sick. Thus, a study in the Serengeti found that cheetahs and wild dogs killed
a disproportionate number from the younger age classes of Thomson’s gazelles
(Figure 7.11a) because: (i) these young animals were easier to catch (Figure 7.11b);
(ii) they had lower stamina and running speeds; (iii) they were less good at out-
maneuvering the predators (Figure 7.11c); and (iv) they may even have failed
to recognize the predators. The effects of predation on the prey population will
therefore have been less than would otherwise have been the case, because these
young gazelles will have been making no present reproductive contribution to
the population, and many would have died anyway, from other causes, before
they were able to do so.
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It is apparent, then, that the effects of a predator on an individual prey are
crucially dependent on the response of the prey; and the effects on prey populations
are equally dependent on which prey are attacked and on the responses of other
prey individuals and other natural enemies of the prey. The effect of a predator
may be more drastic than it appears, or less drastic. It is only rarely what it seems.
7.4 Predator behavior: foraging and
transmission
So far, we have been looking, in effect, at what happens after a predator finds its
prey. Now, we take a step back and examine how contact is established in the first
place. This is crucially important, because this pattern of contact is critical in deter-
mining the predator’s consumption rate, which goes a long way to determining its
own level of benefit and the harm it does to the prey, which determines, in turn,
the impact on the dynamics of predator and prey populations, and so on.
True predators and grazers typically ‘forage’. Many move around within
their habitat in search of their prey, and their pattern of contact is therefore itself
determined by the predators’ behavior – and sometimes by the evasive behavior
of the prey (Figure 7.12a). This foraging behavior is discussed below. Other
predators, web-spinning spiders for instance, ‘sit and wait’ for their prey, though
almost always in a location they have selected (Figure 7.12b).
With parasites and pathogens, on the other hand, we usually talk about trans-
mission rather than foraging. This may be direct transmission between infectious
and uninfected hosts when they come into contact with one another (Figure 7.12c),
or free-living stages of the parasite may be released from infected hosts, so that
it is the pattern of contact between these and uninfected hosts that is important
(Figure 7.12d). The simplest assumption we can make for directly transmitted
parasites – and one that often is made when attempting to understand their
dynamics (discussed in Section 7.5) – is that transmission depends on infectious
and uninfected hosts ‘bumping into one another’. In other words, the overall rate
of parasite transmission depends both on the density of uninfected, susceptible hosts
(since these represent the size of the ‘target’) and on the density of infectious
hosts (since this represents the risk of the target being ‘hit’) (Figure 7.12c).
Part III Individuals, Populations, Communities and Ecosystems
228
Thomson’s gazelle.
sit-and-wait predators
parasite transmission
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