CHAPTER 14

Species Interactions

W
hen prickly pear cactus (Opuntia) was introduced into Australia as an orna-
mental plant and to establish “living fences” for pastures, it spread rapidly
over the island continent, covering thousands of acres of valuable pasture
and rangeland. After several unsuccessful attempts to eradicate the plant, the cactus
moth (Cactoblastis cactorum) was introduced from South America in the 1920s. The
caterpillar of the cactus moth feeds on growing shoots of the prickly pear and quickly
destroys the plant—literally nipping it in the bud and inoculating it with various patho-
gens and rot-causing organisms.
Once they became established in Australia, cactus moths exerted such effective con-
trol that within a few years, prickly pear had become a pest of the past (Figure 14.1).
Cactus moths have since been introduced into South Africa and Hawaii to control intro-
duced Opuntia species. Since their introduction into the West Indies for control purposes,
however, the moths have invaded Mexico and Florida, where they are threatening native
species of Opuntia.
The cactus moth has not eradicated the prickly pear in Australia because the cactus
still manages to disperse to moth-free areas, thereby keeping one jump ahead of the
moth. Thus, the cactus population maintains a low-level equilibrium in a continually shift-
ing mosaic of isolated patches, as in a metapopulation. Indeed, a casual observer would
probably never guess that the cactus moth keeps the prickly pear at its present low popu-
lation levels because the moths are scarce in the remaining stands of cactus in Australia
today. (The same moth probably controls prickly pear populations in some areas of its
native range in South America, but its decisive role might have gone unnoticed if the
appropriate experiment had not been performed in Australia.)
The cactus–cactus moth example shows the potentially strong influence of consumers
on resource populations. Consumer–resource interactions are just one of the many types

287
288 CHAPTER 14

(a) (b)

FIGURE 14.1 The prickly pear cactus population is
controlled by its predator, the cactus moth. Photographs of
a pasture in Queensland, Australia, (a) 2 months before and
(b) 3 years after the introduction of the cactus moth to control
the prickly pear cactus. Main photos from A. P. Dodd, in A. Keast,
R. L. Crocker, and C. S. Christian (eds.), Biogeography and Ecology
in Australia, W. Junk, The Hague (1959), courtesy of W. H. Haseler,
Department of Lands, Queensland, Australia. Inset photos by (a) D.
Habeck and F. Bennet, University of Florida and (b) Peggy Greb/
Agricultural Services/U.S. Department of Agriculture.

of interactions between species that influence species’ populations and guide their evolu-
tion through natural selection. This chapter provides a brief overview of the many kinds
of species interactions in nature, including both antagonistic and mutually beneficial rela-
tionships. These interactions define the structure of biological communities and ecosys-
tems and influence the functioning of those systems. They also emphasize the overriding
influence of the biological environment on the behavior of individuals, the demography
of populations, and the evolution of species.

CHAPTER CONCEPTS

interactions
interactions

interactions

P redator–prey, herbivore–plant, and parasite–host rela-

tionships are all examples of consumer–resource
interactions, which organize biological communities
into food chains, along which food energy is passed
through the ecosystem. It is typical of consumer–resource
interactions that consumers benefit individually and their
numbers may increase, while resource populations are
decreased. Thus, while energy and nutrients move up a
food chain, populations are controlled both from below
by resources and from above by consumers.
Although consumer–resource interactions constitute
the most fundamental ecological relationship between
species, these interactions are the basis for two additional
types of interactions: competition and mutualism. When
two consumers share the same resource, each reduces the
availability of the resource to the other, and they are said
to be engaged in competition. As we shall see in Chapter
16, competition influences population processes and can
determine whether a population can persist in a particular
environment.
Mutualisms are interactions between two species
that benefit both. They take on many forms, but partners
in mutualisms generally supply complementary resources
or services. For example, many insects pollinate plants in
 Species Interactions 289

TABLE 14.1
Effect on species 1 Effect on species 2 Type of interaction
Consumer–resource interactions, including predator–prey, herbivore–
plant, and parasite–host interactions
Competition
Mutualism
0 Commensalism
0 Amensalism, perhaps mostly incidental

return for nectar or pollen rewards; bacteria in the roots
of plants provide nitrogen to their hosts in return for car-
bon sources; ruminant mammals, such as sheep and cat-
tle, maintain bacteria in specialized compartments in their
stomachs, and in return the bacteria digest compounds in
plants that the ruminant cannot.
Species interactions can be classified conveniently by
the effect of each species on the other. When we consider
that a species can benefit from an interaction ( ), suffer
( ), or be unaffected (0), the possible combinations of
effects are / , / , / , /0, or /0 (0/0 represents
the absence of any consequential interaction), as summa-
rized in Table 14.1.
The interactions /0 (commensalism) and /0
(amensalism) are common in ecology and are impor-
tant for many populations, but are not often considered
in experimental and theoretical studies because of the
absence of a mutual dynamic between the two partici-
pants. For example, when a bird places its nest in a tree, or
a hermit crab uses the shell of a long-dead snail, the bird
and the crab gain protection from predators ( ), but the
populations of trees and snails are unaffected (0). When
an elephant crushes a grasshopper underfoot, the popula-
tion of grasshoppers suffers ( ), but the elephant is unaf-
fected (0). We shall have little more to say about such
interactions in nature.
Another term commonly used to describe some
kinds of species interactions is symbiosis (literally, “liv-
ing together”), which refers to individuals of different spe-
cies that live in close association. Many cases of symbiosis
involve partners in mutualisms whose lives are intimately
intertwined, such as the algae and fungi that constitute
lichens. However, the term symbiosis also extends to para-
sites that live within their hosts; both parties to such rela-
tionships are often specifically adapted to maintain the
delicate balance between life and death. As we encoun-
ter the various relationships between species in more
detail, you should keep in mind the endless complexity of
these interactions and the indistinct boundaries between
predation, parasitism, and mutualism. To begin our dis-
cussion, we’ll turn to the elemental consumer–resource
relationship.
All organisms are involved in
consumer–resource interactions
Consumer–resource interactions are the most fundamen-
tal interactions in nature because all non-photosynthetic
organisms must eat, and all organisms are at risk of being
eaten. Consumers go by many names. The most familiar
are predator, parasite, parasitoid, herbivore, and detriti-
vore. From the standpoint of species interactions, some
of these distinctions are useful, but others can be confus-
ing. Let’s start with predator. Images of an owl eating a
mouse or of a spider eating a fly capture the essentials of
predation (Figure 14.2). Predators capture individuals and
consume them, thereby removing them from the prey
population and gaining nutrition to support their own
reproduction.
In contrast, a parasite consumes parts of a living
prey organism, or host. Parasites attach themselves to, or
invade the bodies of, their hosts and feed on their tissues,
their blood, or partially digested food in their intestines.
Parasites that cause disease symptoms are called patho-
gens. Although parasitism may increase the probability of
a host’s dying from other causes or reduce its fecundity, a
parasite generally does not, by itself, remove an individual
from the host population. Indeed, it would be contrary
to a parasite’s best interests to kill the host upon which it
feeds and depends for its survival.
Parasitoid is the term applied to species of wasps and
flies whose larvae consume the tissues of living hosts—
usually the eggs, larvae, or pupae of other insects. This
strategy inevitably leads to the host’s death, but not until
the parasitoid larvae have completed their development
and pupated (Figure 14.3). Parasitoids resemble para-
sites, because they reside within and eat the tissues of a
290 CHAPTER 14
FIGURE 14.2 African lions are
specialized for pursuing large prey.
With their powerful legs and jaws, lions
can subdue prey somewhat larger than
themselves. But because they cannot
maintain speed over long distances,
successful hunting relies on stealth and
surprise. Photo by Peter Blackwell/naturqpl.com.
living host, and predators, because they inevitably kill their
host. Not surprisingly, parasitoids have their own parasites,
which are called hyperparasitoids.
Herbivores eat whole plants or parts of plants. From
the standpoint of consumer–resource relationships, her-
bivores function as predators when they consume whole
plants, and as parasites when they consume living plant
tissues but do not kill their victims. Thus, a deer browsing
on a few leaves and stems functions as a parasite, while a
sheep that consumes an entire plant, pulling it up by the
roots and macerating it into lifeless shreds, functions as a
predator. Consumption of a portion of a plant’s tissues is
referred to as grazing (when applied to grasses and other
herbaceous vegetation, and to algae) or browsing (when
applied to woody vegetation).
Detritivores consume dead organic material—such
as leaf litter, feces, and carcasses—and therefore have
no direct effect on the populations that produce those
resources. In other words, detritivory is a commensal
( /0) interaction. Because they live off the wastes of
FIGURE 14.3 Parasitoid wasps develop inside the larvae or
pupae of other insects. Photo by Scott Bauer.
other species, detritivores do not directly affect the abun-
dance of their food supplies, and their activities do not
usually influence the evolution of the living sources of
their food. Detritivores are important in the recycling of
nutrients within ecosystems, as we will see in Chapter 22.
However, because detritivore populations generally are
not dynamically coupled to their resource populations,
detritivores will not be considered further in this chapter.
The various kinds of consumer–resource interactions
we have just described can be organized usefully accord-
ing to the duration and “intimacy” of the relationship
between the interacting species and the probability that
the interaction will lead to the death of resource individu-
als (Table 14.2).
The dynamics of consumer–resource
interactions reflect mutual
evolutionary responses
Resource organisms have as many tactics to avoid being
eaten as their consumers have to hunt them. Because the
fitness of both is at stake, evolutionary responses con-
stantly adjust relationships between consumers and their
resources, as we shall describe in more detail in Chapter
17. The commonplace images of cat and mouse or spider
and fly might lead one to think that consumers have the
upper hand. However, hiding, escape, and many other
kinds of defensive tactics can be effective, depending on
the particular circumstances of a consumer–resource rela-
tionship. For example, grasslands offer few hiding places
for deer, antelope, and other grazers, so their escape
depends on early detection of predators and swift move-
ment. Plants cannot flee like animals, but many produce
thorns and defensive chemicals that dissuade herbivores.
Where animals are able to hide or seek refuge in safer
microhabitats, they are often sensitive to the presence of
predators and adjust their behavior accordingly. Small fish
 Species Interactions 291

TABLE 14.2
Probability of death of resource organism
Duration and/or intimacy of the association Low High
Short and casual Grazers and browsers Predators; seed predators
Long and close Parasites and many arthropod herbivores Parasitoids

Source: A. J. Pollard, in R. S. Fritz and E. L. Simms (eds.), Plant Resistance to Herbivores and Pathogens: Ecology,
Evolution, and Genetics, University of Chicago Press, Chicago (1992), pp. 216–239.

living in ponds with larger predatory fish avoid the best
feeding areas in open water and spend most of their time
lurking in safer weed beds close to the water’s edge. The
following case study shows, however, that staying out of
harm’s way can have costs.
ECOLOGISTS Predator avoidance and growth
IN THE FIELD performance in frog larvae. Staying
safe from predators requires trade-offs. When prey indi-
viduals must remain in poor feeding areas to avoid preda-
tors, for example, their growth rates can be depressed.
Slowly growing prey take longer to mature, extending the
period during which an individual is most vulnerable to
predation. They are also smaller as adults and therefore
produce fewer offspring.
The effect of predation risk on the growth of frog lar-
vae was demonstrated in laboratory and field experiments
on bullfrog (Rana catesbiana) tadpoles by Rick Relyea and
Earl Werner at the University of Michigan. They conducted
laboratory experiments in which newly hatched tadpoles
were placed in aquaria with caged dragonfly larvae
or fish, which prey on small bullfrog tadpoles in natural
ponds. The tadpoles reduced their activity in the presence
of the predators, especially the dragonfly larvae, and also
avoided the side of the aquarium where the caged preda-
tor was located (Figure 14.4). Similar experiments within
enclosures set in a natural pond further demonstrated that
the presence of caged dragonfly larvae reduced growth
rates significantly in some species of frogs.
Other studies (see Figure 7.20, for example) emphasize
that the ability to perceive predation risk is widespread in
the animal world and has a strong effect on the behavior
and habitat selection, as well as on the demography, of
prey organisms. Of course, prey organisms respond to
the presence of predators because such responses have
been strongly selected over the evolutionary history of the
consumer–resource interaction.
When prey cannot hide or escape, they often adopt
protective defenses. These defenses rarely involve physi-
cal combat because few types of prey can match their

When housed with predators, …and avoided the side Presence of predators
(a) tadpoles reduced their activity (b) of the aquarium with (c) lowered growth rates
movements… the caged predator. of tadpoles.

20 60 16.0
Growth rate (mg per day)
Tadpoles on the predator

50
15 12.0
Time active (%)

cage side (%)

40

10 30 8.0

20
5 4.0
10

0 0 0.0
No With fish With No With fish With Alone With With With
predator dragonfly predator dragonfly fish dragonfly both
larvae larvae larvae

FIGURE 14.4 Avoiding predators may result in reduced
growth rates. Relyea and Werner housed bullfrog tadpoles with
and without caged predators (fish and dragonfly larvae) and
recorded (a) the activity levels of the tadpoles, (b) the number of
tadpoles found on the side of the aquarium where the predator
cage was located, and (c) the growth rates of the tadpoles. The
dragonfly larvae, in particular, led to reduced activity, avoidance
of areas near predators, and reduced growth rates on the part of
the tadpoles. After R. A. Relyea and E. E. Werner, Ecology 80:2117–
2124 (1999).
292 CHAPTER 14
FIGURE 14.5 Many organisms have evolved chemical
defenses to ward off predators. A bombardier beetle sprays
a noxious liquid at the temperature of boiling water toward a
predator. Courtesy of Thomas Eisner, Cornell University.
predators, and predators carefully avoid those that can.
Instead, many seemingly defenseless organisms produce
foul-smelling or stinging chemical secretions to dissuade
predators. For example, whip scorpions and bombardier
beetles direct sprays of noxious liquids at threatening ani-
mals (Figure 14.5). Many plants and animals contain chem-
ical substances that make them unpalatable or poisonous.
Slow-moving animals, such as porcupines and armadillos,
protect themselves with spines or armored body coverings.
These defenses, too, have costs, as they require resources
that could otherwise be allocated to growth and reproduc-
tion. At the same time, predator populations are evolving
adaptations to circumvent prey defenses, as we shall see
in more detail in Chapter 17.
Parasites maintain a delicate
consumer–resource relationship
with their hosts
Parasites are usually much smaller than their hosts and
live either on their body surfaces (for example, ticks, lice,
and mites) or inside their bodies (for example, viruses,
bacteria, protozoans, various roundworms, flukes, tape-
worms, and arthropods). Many parasites are only casu-
ally associated with their hosts, as in the case of mosqui-
toes that “graze” blood meals. Others remain within their
hosts throughout their entire life cycles, and may even be
transmitted between host mother and offspring through
the host’s eggs. One such parasite is the symbiotic bac-
terium Wolbachia, which infects the cells of many insects
and other invertebrates (Figure 14.6). Although Wolbachia
infect many types of host cells, it is their presence in cells
of the ovaries and testes that reduces host fitness most
profoundly, principally by modifying sexual function.
Infected males may be killed, develop as females, or be
rendered incapable of mating with any female not already
infected by the same strain of Wolbachia. In some host
species, Wolbachia infections cause females to reproduce
parthenogenetically, without having to mate with males.
The effects of parasites on host fitness vary dramati-
cally, ranging in humans, for example, from the passing
inconvenience of a cold virus to the deadly effects of HIV
and the avian H5N1 influenza virus. Whereas Wolbachia is
a serious threat to fitness, other symbionts that might have
been parasitic in the past may evolve to become benefi-
cial to their hosts. One example is Buchnera, a beneficial
bacterial symbiont of insects, particularly aphids. Buchnera
and its hosts are mutualists. The Buchnera symbionts are
maintained in specialized cells, called bacteriocytes, and
although they obtain carbohydrates and other nutrients
from their hosts, they provide essential amino acids in
return. Aphids feed on the phloem of plants, which con-
tain virtually no amino acids, and so without the amino
acids from the Buchnera, the aphids could not grow and
reproduce. The genome of Buchnera, like those of many
symbionts, is greatly reduced, and the symbiont relies on
its host for many of its essential functions. The contrast
between Wolbachia and Buchnera emphasizes the range of
interactions that exist between symbionts and their hosts,
from strict parasitism to mutualism. Indeed, it is thought
that many mutualistic relationships have evolved from
host–parasite interactions, and perhaps vice versa.
Parasite life cycles
Parasites that live inside, or in close association with, a
larger organism enjoy a benign physical environment reg-
ulated by their host. Tapeworms, for example, are bathed
FIGURE 14.6 Wolbachia is a common bacterial parasite of
insects. In this electron micrograph, Wolbachia are visible in an
insect cell (arrow). Courtesy of Scott O’Neill, from PLoS Biology 2(3):
e76 (2004), doi:10.1371/journal.pbio.0020076.
 Species Interactions 293

7 A feeding 8 After a mosquito 9 The resulting zygote, the only diploid

mosquito ingests ingests blood, male stage in the life cycle, enters the mosquito's
them and the cycle and female game- gut wall and forms a cyst.
begins again. tocytes develop into
gametes, which fuse. 10 The cyst divides
into sporozoites…

6 Eventually, some merozoites develop

into male and female gametocytes.

5 48-hour cycles
of invasion, lysing,
and reinvasion cause
the characteristic
fevers and chills in
11 …that invade
the host.
the salivary gland.

(Start here) 1 The mosquito

injects sporozoites into a
4 Merozoites also 2 The sporozoites penetrate liver human's blood when it feeds.
invade red blood cells and develop into merozoites.
cells, where they
grow, divide, and 3 Merozoites can reinfect the
break out of (lyse) liver, producing new generations.
the cells.

FIGURE 14.7 Many parasites have complex life cycles. dispersal between hosts. After R. Buchsbaum, Animals without
Different stages in the life cycle of the malaria parasite Backbones, 2nd ed., University of Chicago Press, Chicago (1948); M.
Plasmodium are adapted to life in two different hosts and to Sleigh, The Biology of Protozoa, American Elsevier, New York (1973).

in a predigested food supply and retain for themselves
little more than a highly developed capacity to produce
eggs. Nonetheless, the life of a parasite is not easy. Host
organisms have a variety of mechanisms to recognize
invaders and destroy them. Moreover, parasites must
disperse through a hostile environment to get from one
host to another. Many accomplish this via complicated life
cycles, often involving two or more hosts and at least one
stage that can cope with the external environment.
The life cycle of the protozoan parasite Plasmodium,
which causes malaria in humans, is a common textbook
example (Figure 14.7). This parasite has two hosts, one a
294 CHAPTER 14
mosquito and the other a human or some other mammal,
bird, or reptile. When an infected mosquito bites a human,
cells called sporozoites are injected into the bloodstream
with the mosquito’s saliva. The sporozoites at first prolif-
erate by mitosis in liver cells, then enter red blood cells
as merozoites, where they feed on hemoglobin and grow.
When a merozoite becomes large enough, it undergoes a
series of divisions (asexual reproduction), and the daugh-
ter merozoites break out of the red blood cell. Each mero-
zoite can enter a new red blood cell, grow, and repeat the
cycle, which takes about 48 hours. (When the infection
has built up to a high level, the emergence of daughter
cells corresponds to periods of high fever resulting from
the inflammation reaction of the host’s immune system.)
After several of these cycles, some of the merozoites that
enter red blood cells change into sexual forms called
gametocytes. If gametocytes are swallowed by a mosquito
along with a meal of blood, they are transformed into eggs
and sperm, and fertilization (sexual reproduction) takes
place. The resulting zygotes penetrate the mosquito’s gut
wall and then undergo a series of divisions to produce
sporozoites. These work their way into the salivary glands
of the mosquito, from which they may enter a new host.
Parasite virulence and host resistance
The complex life histories of parasites involve a variety
of interactions with hosts, and different sets of factors
affect each stage of the parasite life cycle. The balance
between parasite and host populations is influenced by
the virulence of the parasite and by the immune response
and other defenses of the host. Virulence is a measure
of the capacity of a parasite to invade host tissues and
proliferate in them. The virulence of an invading parasite
may be reduced by actions of the host’s immune system,
including inflammation responses and the production of
antibodies. Antibodies recognize and bind to foreign pro-
teins, such as those on the outer surfaces of bacteria and
protozoans, targeting them for attack by macrophage cells,
which bind to the parasites and engulf them. The disabled
parasites are then transported to the spleen and cleared
from the body.
An immune response takes time to develop, however,
and the delay gives the parasite a chance to multiply within
a host. Parasites also have ways of circumventing the host’s
immune system. Some parasites produce chemical factors
that suppress the immune system; this is the most trouble-
some feature of HIV. Others have surface proteins that
mimic the host’s own proteins and thus escape notice by
the host’s immune system. Trypanosomes, which are flagel-
late protists that cause sleeping sickness in humans, escape
the immune system by continually coating their surfaces
with novel proteins produced by gene rearrangements.
Some schistosomes (trematode worms of the genus
Schistosoma) excite an immune response when they enter
a host, but do not succumb to antibody attack because
they coat themselves with the host’s proteins before its
antibodies become numerous. As a consequence, other
schistosomes that subsequently infect that host face a bar-
rage of antibodies stimulated by the earlier entrance of the
now entrenched individuals. When this response targets
schistosome species closely related to the original para-
site, it is known as cross-resistance. For example, many
people in tropical regions are infected by schistosomes.
One extremely virulent schistosome species, found only
in humans, causes a debilitating disease called schistoso-
miasis or bilharziasis. But when a person has been infected
previously by other schistosome species from wild game
or domestic livestock, some of which have little effect on
humans, the effect of infection by the bilharziasis parasite
is moderated considerably.
Herbivory varies with the quality of
plants as resources
Plants cannot hide or flee, so they rely on other tactics to
escape their consumers. Plant defenses against herbivores
include the inherently low nutritional value of most plant
tissues as well as toxic compounds that plants produce
and sequester for their defense. Plants also employ struc-
tural defenses, such as spines, hairs, tough seed coats, and
sticky gums and resins (Figure 14.8).
The nutritional quality and digestibility of plants is
critical to herbivores. Herbivores usually select plant food
according to its nutrient content, preferring young leaves
because of their low proportion of indigestible cellulose.
Fruits and seeds are particularly nutritious compared with
leaves, stems, and buds because of their higher nitrogen,
fat, and sugar contents. Many plants use chemicals to
reduce the availability of their proteins to herbivores, and
thereby reduce their nutritional quality. Oaks and other
plants sequester compounds called tannins in vacuoles
in their leaves, which bind to plant proteins and inhibit
their digestion. As a consequence, tannins can slow the
growth of caterpillars and other herbivores that feed on
the plant. However, insects that feed on tannin-rich plants
can reduce the effects of tannins by producing detergent-
like surfactants in their gut fluids, which tend to disperse
tannin–protein complexes.
Tannins are an example of a secondary compound:
a compound used by plants not for metabolism, but for
 Species Interactions 295

(a) (b) FIGURE 14.8 Structural and

chemical defenses protect the stems
and leaves of many plants from
herbivores. (a) This cholla cactus
(Opuntia) from Arizona is protected
by sharp spines. (b) The white latex
sap oozing from the stem of this
milkweed plant (Asclepias syriaca)
is toxic to most herbivores. Photos
by (a) R. E. Ricklefs and (b) Bill Beatty/
Animals Animals, Earth Scenes.

other purposes—chiefly defense. Whereas tannins react

with proteins of all types, many secondary compounds
interfere with specific metabolic pathways or physiologi-
cal processes of herbivores. Secondary compounds fall
into three major classes based on their chemical struc-
ture: nitrogen compounds (ultimately derived from amino
acids), terpenoids, and phenolics. The nitrogen com-
pounds include indigestible structural compounds, such
as lignin; alkaloids, including morphine (derived from Induction of chemical
poppies), atropine, and nicotine (from various members defenses in cotton plants
of the tomato family); nonprotein amino acids such as following exposure to one
mite species resulted in
L-canavanine; and cyanogenic glycosides, which produce
reduced populations of
hydrogen cyanide (HCN). Terpenoids include essential
adult mites of another
oils, latex, and resins. Among the phenolics, many sim- species…
ple phenols have antimicrobial properties. 300
Some types of defensive chemicals are maintained at Control …and their eggs.
Number of T. urticae

high levels in plant tissues at all times; these are called

constitutive defenses. Others, known as induced
defenses, are activated by herbivore damage in a man-
ner analogous to the way foreign proteins induce an
immune response in vertebrate animals (Figure 14.9).
These chemicals increase dramatically in many plants fol-
lowing defoliation by herbivores (or the clipping of leaves
by investigators). Wounding may cause the production
of toxic, noxious, or nutrition-reducing compounds—
locally in the area of a wound or systemically throughout
the plant—that reduce subsequent herbivory. In some
cases, these responses take only minutes or hours; in oth-
ers, they require a new season of growth. When shoots
of aspen, poplar, birch, and alder are heavily browsed by
snowshoe hares, shoots produced during the following
200
100
Exposed
0
Adult mites Eggs
FIGURE 14.9 Plant defenses can be induced by herbivory.
Mean numbers of the mite Tetranychus urticae were lower on
cotton plants that had been previously exposed to a closely
related mite species, T. turkestani, than on control plants with no
previous mite exposure. This finding suggests that exposure to T.
turkestani induced chemical defenses in the plants. From R. Karban
and J. R. Carey, Science 225:53–54 (1984); photo by J. K. Clark.
296 CHAPTER 14
year have exceptionally high concentrations of terpenes
and phenolic resins, which are extremely unpalatable to
hares. Some defenses can be induced even in untouched
plants by volatile compounds released by neighboring
plants that have been damaged—chemical communica-
tion among plants!
Inducibility suggests that some chemical defenses are
too costly to maintain when herbivory is light or absent.
Several studies have shown trade-offs between the pro-
duction of defensive chemicals and plant growth. In addi-
tion, where soils are low in the nutrients required for the
production of defensive chemicals, the costs of defense
are relatively high. Undoubtedly, the strategies herbivores
use to counter plant defenses are also costly, emphasiz-
ing once more the close connection between consumer–
resource interactions and life history optimization.
Competition may be an indirect result
of other types of interactions
Up to this point, we have considered direct interactions
in which individuals of one species directly influence
the well-being of individuals of another species. Interac-
tions between resource and consumer individuals are the
primary case in point. However, such interactions have
indirect consequences for other species in an ecological
system.
Consider a simple food chain, in which a predator
species feeds on an herbivore species, which in turn feeds
on a plant species. The interaction between the preda-
tor and its prey is a straightforward consumer–resource
interaction; that is,
consumer ( ) l resource ( )
However, the herbivore also is a consumer, and when its
population is reduced by its predator, the plant species
enjoys the benefit of reduced herbivory. Thus, the preda-
tor and the plant are engaged in an indirect interaction:
predator ( ) l herbivore ( ) l plant ( )
Because such indirect interactions are felt across multiple
trophic levels, they are often called trophic cascades. We
shall consider interactions of this kind in more detail in
Part 5 of this book.
Another kind of indirect interaction results from the
use of a single resource by two or more consumers. This
interaction can be diagrammed simply as
consumer 1 ( ) l resource ( ) k consumer 2 ( )
However, because each of the consumers reduces the
availability of the resource to the other, the indirect inter-
action between the two consumer populations can be
seen as
consumer 1 ( ) i consumer 2 ( ).
Thus, even though individuals of consumer 1 and con-
sumer 2 may never come into contact with each other,
their populations are nonetheless affected by their use
of a common resource. This interaction is referred to as
exploitation competition, or indirect competition, and we shall
consider it in detail in Chapter 16. However, individuals of
different species that share a common resource may also
interact directly through the kinds of antagonistic behav-
iors that we have already discussed in Chapter 9 in the
context of interactions among individuals within species.
A competition–facilitation continuum
Interactions between species are not rigid; indeed, it is
common for these interactions to change over the life
cycle, and even for a direct relationship to become an
indirect one. An increasingly important theme in the ecol-
ogy of species interactions is the often-blurred distinction
between competition and various forms of facilitation,
such as commensalism and mutualism. A prominent case
in point is the phenomenon of so-called nurse plants, in
which individuals of one species facilitate the germination
and growth of a second species. In desert environments
of western North America, for example, several species
of small trees, including paloverde and ironwood, provide
protected sites for the establishment of various species of
columnar cacti (Figure 14.10). The trees and the cacti may
compete for water and soil nutrients, but small seedlings
of the cacti have little effect on the resources available to
established nurse plants, which fortuitously provide the
seedlings with shade from the sun and protection from
herbivores among their dense branches. Thus, early in
its life cycle, the cactus is a commensal of the tree. As
the cactus grows, it may have an increasingly negative
effect on the resources available to its nurse plant, but
the growth forms of the two species often differ so much
that their growth is limited by different factors, and they
can coexist.
Facilitation is a common theme in the development of
biological communities, as we shall see in Chapter 19. The
initial colonizers of newly exposed soil, for example, are
often plants that can tolerate the heat and water stress of
a completely open environment. The shade and organic
soil materials provided by these pioneers allow other

FIGURE 14.10 Nurse plants provide shade and protection
for other species. This saguaro cactus established itself under
a nurse plant, a paloverde tree. Without the nurse plant, it
might not have survived the seedling stage in its harsh desert
environment. Initially a commensal, the cactus may now be
competing with its nurse plant for water and other resources.
Photo by Bill Pogue/bpogue@billpogue.com.
species to invade the area, much as nurse plants facilitate
the establishment of some desert cacti. However, as the
new colonists grow, they capture progressively more sun-
light and soil nutrients and shift from being commensals
of the initial colonizers to being competitors.
Individuals of different species can
collaborate in mutualistic interactions
Many interactions between species benefit both partici-
pants. For example, flowers provide honeybees with nec-
tar, and the bees carry pollen between plants. These kinds
of interactions are known as mutualisms. In most cases,
Species Interactions 297
each party to a mutualism is specialized behaviorally or
physiologically to perform a function lacking in the other.
Many mutualisms are symbioses, such as the relation-
ship between the algae and fungi that make up lichens
(see Figure 1.8). In other instances, such as seed dispersal
mutualisms, the partners are only loosely associated and
may interact mutualistically with a variety of species.
Mutualisms are widespread in the living world, and
humans are no exception. Humans have beneficial gut
bacteria that aid us in digestion and assimilation of nutri-
ents. An unusual mutualism involves the honeyguides of
southern Africa, which lead various mammals, including
humans, to beehives. The birds eat the wax left behind
after the humans have extracted the honeycombs. The
honeyguides depend on a further mutualism with bacteria
in their guts that secrete enzymes needed to digest the
wax. We humans also have created our own mutualis-
tic associations through the domestication of various pet,
livestock, and crop species.
In fact, it is fair to say that all organisms are engaged in
mutualistic interactions. The cells of all eukaryotic organ-
isms are the product of ancient mutualisms between sym-
biotic bacteria. One partner in these relationships became
a cellular organelle: the mitochondrion and, in plants, the
chloroplast. These organelles even retain some of the orig-
inal genetic material of their free-living ancestors.
Mutualisms occur in every kind of environment, but
may be particularly important under stressful conditions.
For example, the giant tubeworms living close to hydro-
thermal vents thousands of meters below the ocean sur-
face depend entirely on symbiotic bacteria that can use
energy from hydrogen sulfide in the hot vent water to
synthesize organic molecules. Indeed, the worms lack
mouths and digestive tracts as adults. Instead, they form
special structures called trophosomes, which the bacteria
invade through the skin from the surrounding water. Nei-
ther the bacteria nor the worms can live and reproduce
without the other species.
In very general terms, mutualisms fall into three cat-
egories: trophic, defensive, and dispersive. The partners
in trophic mutualisms are usually specialized in com-
plementary ways to obtain energy and nutrients; hence
the term trophic, which pertains to feeding relationships.
We have just seen such a mutualisms between bacteria
and giant tubeworms. Similarly, bacteria in the rumens of
cows and other ungulates can digest the cellulose in plant
fibers, which a cow’s own digestive enzymes cannot break
down. The cows benefit because they assimilate some of
the by-products of bacterial digestion and metabolism for
their own use (they also digest some of the bacteria). The
298 CHAPTER 14
bacteria benefit by having a steady supply of food in a
warm, chemically regulated environment that is optimal
for their own growth. In these cases, each of the partners
supplies a limiting nutrient or energy source that the other
cannot obtain by itself.
Species in defensive mutualisms receive food or
shelter from their partners in return for defending those
partners against their consumers. For example, in some
marine ecosystems, specialized fishes and shrimps clean
parasites from the skin and gills of other fish species
(Figure 14.11). These cleaners benefit from the food value
of parasites they remove, and the groomed fish are unbur-
dened of some of their parasites. Cleaning mutualisms are
most highly developed in clear, warm tropical waters.
Many cleaners display their striking colors at locations,
called cleaning stations, to which other fish come to be
groomed. As might be expected, a few predatory fish spe-
cies mimic the cleaners: when other fish come to them
and expose their gills to be groomed, they get a bite taken
out of them instead.
FIGURE 14.11 Cleaning mutualisms benefit both
participants. The prawn Lysmata amboinensis is removing
parasites from a moray eel. From this interaction, the prawn gets
food, and the eel gets rid of some of its external parasites. Photo
by Doug Perrine/DRK Photo.
ECOLOGISTS Acacias house and feed the ants
IN THE FIELD that protect them from herbivores.
Each population constantly adapts to evolutionary chang-
es in other populations with which it interacts. These inter-
actions shape the adaptations of all species, occasionally
producing exceedingly intricate and complex living
arrangements. One example, a mutualistic relationship
between ants and acacias in Central America, drives
home the lesson of this complexity.
Acacias and ants engage in mutually beneficial rela-
tionships in which the plants provide food and nesting
sites for the ants, while the ants provide the plants with
protection from herbivores and competing plants. The
bull’s-horn acacia (Acacia cornigera) has large, swollen,
hornlike thorns with a tough woody covering and a soft
pithy interior. To start a colony in an acacia, a queen ant
of the species Pseudomyrmex ferruginea bores a hole in
the base of one of these thorns and clears out some of
the soft material inside to make room for her brood. In
addition to housing the ants, the acacia provides carbo-
hydrate-rich food for them in nectaries at the bases of the
leaves as well as fats and proteins in the form of nodules,
called Beltian bodies, at the tips of some leaves. The ants,
in turn, protect their host plant from other insects. As the
colony grows, ants occupy more and more of the acacia’s
thorns. A colony may increase to more than a thousand
workers within a year, and may eventually include tens of
thousands of workers. At any one time, about a quarter
of the ants are outside their nests, actively gathering food
and defending the acacia.
The relationship between Pseudomyrmex and Acacia
is so tight that neither the ant nor the acacia can survive
without the other. The ants require the nutrients provided
by the acacia’s Beltian bodies and cannot be reared on
other foods. Acacias lacking ants are quickly devoured
by insect herbivores. This last point was made dramati-
cally by ecologist Daniel Janzen in a set of experiments
conducted in Oaxaca, in southern Mexico. Janzen cut
acacias to stimulate growth of new shoots and then kept
ants from colonizing one set of plants. After 10 months of
one such experiment, the shoots lacking ants weighed less
than one-tenth as much as those with intact ant colonies,
and they produced fewer than half the leaves and one-
third the number of swollen thorns (Figure 14.12).
The mutualism between ants and acacias has been
accompanied by adaptations in both species to increase
the effectiveness of their association. For example,
Pseudomyrmex is active both night and day—an unusual
trait for ants—and thereby can provide protection for the
acacia at all times. In addition, these ants have a true
sting, like their wasp relatives, and will swarm vertebrate
herbivores that attempt to feed on their host plant. The ants
also clear away potential plant competitors by attacking

Survival
Shoots without ants
Weight
weighed less than 1/10
of shoot
as much, had fewer than
Number of 1/2 the leaves, and had 1/3
leaves the number of swollen
thorns, as shoots with ant
Number of
thorns colonies.
0 10 20 30 40 50 60 70
Value as a percentage of
shoots with ants
FIGURE 14.12 Some mutualists need their partners to
survive and grow. Removal of ant (Pseudomyrmex) colonies
from shoots of bull’s-horn acacia (Acacia cornigera) in Oaxaca,
Mexico, decreased their growth and survival rates. Data from
D. H. Janzen, Evolution 20:249–275 (1966).
seedlings near their host plant’s base as well as any vines
or overhanging branches of other plants. In a similar
adaptive gesture, the acacia retains its leaves throughout
the year, although rainfall in its environment is extremely
seasonal. By doing so, the bull’s-horn acacia provides a
year-round source of food for the ants. Most related plant
species lose their leaves during the dry season.
Relegating defense against herbivores to a mercenary
apparently makes good evolutionary sense under some
circumstances. The fidelity of the defender is guaranteed
by its absolute dependence on the host for food. One can
imagine, however, that such an intimate relationship must
be the result of a long history of increasingly close asso-
ciation. Acacia species that lack ants provide their own
defenses against herbivores by sequestering toxic chemi-
cals in their leaves. This strategy can be costly compared
with providing food and nesting places for ants, but it also
SUMMARY
1. Species interactions influence population dynamics,
define the structure of ecological systems, and provide a
rich context for evolution.
2. The primary types of species interactions are
consumer–resource interactions, competition, and mutu-
alism, although many variations on these themes blur the
boundaries between them.
3. Species can benefit from ( ) or suffer from ( ) an
interaction, or be unaffected by it (0). We can represent
Summar y 299
allows the plant to shed its leaves during the dry season
and therefore to live in more arid environments than ant-
dependent acacias can tolerate.
Animals participating in dispersive mutualisms
include those that transport pollen between flowers in
return for rewards such as nectar, or that eat nutritious
fruits and disperse the seeds they contain to suitable
habitats. Dispersive mutualisms rarely involve close living
arrangements. Seed dispersal mutualisms are not usually
highly specialized; for example, a single bird species may
eat many kinds of fruit, and each kind of fruit may be
eaten by many kinds of birds. Plant–pollinator relation-
ships tend to be more restrictive because it is in a plant’s
interest that a flower visitor carry its pollen to another
plant of the same species.
M ORE
Seed Dispersal. The seeds of many plant species
WEB are widely distributed by animals, often to habitats
favorable for germination and growth.
M ORE
Pollination. Plants have many ways of manipulat-
WEB ing their pollinators so as to increase the efficiency
of pollen transfer between individuals.
In the next chapter, we shall consider the dynamics
of interactions between consumers and their resources,
building on the development of models for individual
populations. A key insight is that a resource and its con-
sumer have a unique interaction that can result in cyclic
changes in populations of both species. Such insights rein-
force the idea that ecological systems create their own
dynamic properties that cannot be inferred from the indi-
vidual components of the system, but rather depend on
the ways in which species interact.
consumer–resource interactions as / , competition as
/ , and mutualism as / .
4. Individuals of different species that live in close asso-
ciation are said to form a symbiosis. Symbioses may be
mutualistic relationships, as in the case of the algae and
fungi that form lichens, or consumer–resource relation-
ships, as in the case of many parasites and their hosts.
5. Predators are consumers that remove individuals
from prey populations as they consume them. Parasites
300 CHAPTER 14
consume portions of living host organisms, but usually do
not kill them. Parasitoids (mostly small flies and wasps) kill
the hosts they consume, but not immediately.
6. Herbivores can function either as predators, in the
case of consumers that remove whole plants, or parasites,
in the case of grazers or browsers that remove only a por-
tion of a plant’s tissues.
7. Consumer–resource interactions can also be classified
by the duration and intimacy of the association between
individuals, as well as by the probability that resource indi-
viduals will be killed.
8. Organisms avoid being consumed through tactics such
as avoiding detection, remaining in safe refuges, or fleeing
predators, as well as by means of chemical and structural
defenses. All of these tactics impose costs on their users.
9. Many parasites are characterized by complex life cycles
that may include multiple hosts and stages specialized to
make the difficult journey from one host to another.
REVIEW QUESTIONS
1. Compare and contrast the feeding habits of predators,
parasites, and parasitoids.
2. If animal prey can reduce their risk of predation by
hiding, why not hide all the time?
3. In parasite–host relationships, what abilities might nat-
ural selection favor in the parasite and in the host?
4. Some animals defer reproduction so that they can put
more of their energy into rapid growth to become too
large for predators to eat. What trade-off are these animals
making?
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10. Parasite–host interactions often evolve a delicate bal-
ance between the immune response and other defenses
of the host and parasite virulence.
11. Plants have numerous structural and chemical
defenses to deter herbivores. These defenses include fac-
tors that influence the nutritional quality and digestibility
of plant parts as well as specialized chemicals—secondary
compounds—that have negative effects on herbivores.
12. Plant defenses may be constitutive, meaning that they
are always present, or they may be induced by herbivory.
The existence of induced defenses suggests that defenses
are costly and impose trade-offs.
13. When two or more consumers utilize the same
resource, each reduces resource availability for the other.
This type of indirect interaction is called exploitation
competition.
14. Mutualisms between species may involve trophic,
defensive, and dispersive interactions. Each partner in a
mutualism usually provides some product (such as nutri-
ents) or service (such as defense against consumers) that
the other cannot provide for itself.
5. Given the ubiquity of the defenses that have evolved
in plants, what would you predict about the evolved
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6. When a plant population possesses inducible defenses,
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7. Why is competition between two species for a shared
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