Chapter 15 Mutualism
A
hummingbird darts
among the red blossoms of a plant growing at the edge of a forest glade
As it inserts its bill into a flower, hovering to sip nectar,
the hummingbird head brushes up against the anthers of the flower and
picks up pollen (fig.15.1). This pollen will be deposited on the stigmas
of other flowers as the hummingbird goes about gathering its meal of
nectar. The hummingbird disperses the plant's pollen in trade for a
meal of nectar.
Belowground we encounter another partnership.
The roots of the hummingbird-pollinated plant are intimately connected
with fungi in an association called mycorrhizae.
The hyphae of the mycorrhizal fungi
extend out from the roots, increasing the capacity of the plant to harvest
nutrients from the environment. In exchange for the nutrients, the plant
delivers sugars and other products of photosynthesis to its fungal partner.
Meanwhile, back aboveground a deer enters
the forest glade and wanders over to the plant recently visited by the
hummingbird. The deer systematically grazes it to the ground, lightly
chews the plant material, and then swallows it. As the plant material
enters the deer's stomach, it is attacked by a variety of protozoans
and bacteria. These microorganisms break down and release energy from
compounds such as cellulose, which the deer's own enzymatic machinery
cannot handle. In return, the protozoans and
bacteria receive a steady food supply from the feeding activities of
the deer as well as a warm, moist place in which to live.
FIGURE
15.1 Hummingbirds feeding on nectar transfer pollen from
flower to flower.
These are examples of mutualism, that is, interactions between individuals of different
species that benefit both partners. Some species can live without their
mutualistic partners and so the relationship is called facultative mutualism. Other species are
so dependent upon the mutualistic relationship
that they cannot live in its absence. Such a relationship is an obligate mutualism. It is a curious fact
that though observers of nature as early as Aristotle recognized such
mutualisms, mutualistic interactions have
received much less attention from ecologists than have either competition
or exploitation. Does this lack of attention reflect the rarity of mutualism
in nature? As you will see in the following pages, mutualism is virtually
everywhere.
Mutualism may be common, but is it important?
Does it contribute substantially to the ecological integrity of the
biosphere? The answer to both these questions is yes. Without mutualism
the biosphere would be entirely different. Let's remove some of the
more prominent mutualisms from the biosphere and consider the consequences.
An earth without mutualism would lack reef-building corals as we know
them. So we can erase the
On
land, there would be no animal-pollinated plants: no orchids, no sunflowers,
and no apples. The pollinators themselves would also be gone: no bumblebees,
no hummingbirds, and no monarch butterflies. Gone too would be all the
herbivores that depend on animal-pollinated plants. Without plant-animal
mutualisms tropical rain forests, the most diverse terrestrial biome
on the planet, would be all but gone. Many wind-pollinated plants would
remain. However, many of these species would also be significantly affected
since approximately 90% of all plants form mycorrhizae.
Those plants capable of surviving without mycorrhizal
fungi would likely be restricted to the most fertile soils.
Even if wind-pollinated, nonmycorrhizal plants remained on our hypothetical world there
would be no vast herds of African hoofed mammals, no horses, and no
elephants, camels, or even rabbits or caterpillars. There would be few
herbivores to feed on the remaining plants since herbivores and detritivores depend upon microorganisms to gain access to
the energy and nutrients contained in plant tissues. The carnivores
would disappear along with the herbivores. And so it would go. A biosphere
without mutualism would be biologically impoverished.
The impoverishment that would follow the elimination
of mumalism, however, would go deeperthan we might expect. Lynn Margulis
and others (Margulis and Fester 1991) have
amassed convincing evidence that all eukaryotes, both heterotrophic
and autotrophic, originated as mutualistic
associa, tions between
different organisms. Eukaryotes are apparently the product of mutualistic
relationships so ancient that the mutualistic
partners have become cellular organelles (e.g., mitochondria and chloroplasts)
whose mumalistic origins long went unrecognized. Consequently, without
mutualism all the eukaryotes, from Homo sapiens to the protozoans, would be gone and the history of life on earth
and biological richness would be set back about 1.4 billion years.
But back here in the present, let's accept
that mutualism is an integral part of nature and review what is known
of the ecology of mutualism. The first part of this brief review emphasizes
experimental studies. Then, in the last part of the chapter, we examine
some theoretical approaches to the study of mutualism.
CONCEPTS
l
Plants benefit from mutualistic
partnerships with a wide variety of bacteria, fungi, and animals.
l
Beef-building corals depend
upon mutualistic relationships with algae
and animals.
l
Theory predicts that mutualism
will evolve where the benefits of mutualism exceed the costs.
CASE HISTORIES: plant mutualisms
Plants
benefit from mutualistic partnerships with
a wide variety of bacteria, fungi, and animals.
Plants are the center of mumalistic relationships that provide benefits ranging from
nitrogen fixation and nutrient absorption to pollination and seed dispersal.
It is no exaggeration to say that the integrity of the terrestrial portion
of the biosphere depends upon plant-centered mutualism. However, to
understand the extent to which ecological integrity may depend upon
these relationships we need careful observational studies and experiments.
Here are some drawn from studies of mycorrhizae.
Plant
Performance and Mycorrhizal Fungi
The fossil record shows that mycorrhizae arose early in the evolution of land plants, perhaps
as long as 400 million years ago. Over evolutionary time, a mutualistic relationship between plants and fungi evolved
in which mycorrhizal fungi provide plants
with greater access to inorganic nutrients while feeding off the root
exudates of plants. The two most common types of mycorrhizae
are (1) arbuscular mycorrhizal
fungi (AMF), in which the mycorrhizal fungus
produces arbuscules, sites of exchange between
plant and fungus, hyphae, fungal filaments,
and vesicles, fungal energy storage organs within root cortex cells,
and (2) ectomycorrhizae (ECM), in which the fungus
forms a mantle around
roots and a netlike structure around root cells (fig. 15.2). Mycorrhizae
are especially important in increasing plant access to phosphorus and
other immobile nutrients (nutrients that do not move freely through
soil) such as copper andzinc, as well as to
nitrogen and water.
FIGURE 15.2
Mutuatistic associations between fungi and plant roots: (a)
arbuscular mycorrhizal
fungus stained so that fungal structures appear blue; and (b) ectomycorrhizae, which give a white fuzzy appearance to these
roots.
Mycorrhizae and the Water Balance of Plants
Mycorrhizal fungi appear to improve the ability of many
plants to extract soil water. Edie Allen and Michael Allen (1986) studied
how mycorrhizae affect the water relations
of the grass Agropyron smithii
by comparing the leaf water potentials of plants with and without mycorrhizae. Figure 15.3 shows that
Agropyron with mycorrhizae
maintained higher leaf water potentials than those without mycorrhizae.
This means that when growing under similar conditions of soil moisture,
the presence of mycorrhizae helped the grass
maintain a higher water potential. Does this comparison show that mycorrhizae are directly responsible for the higher leaf water
potential observed in the mycorrhizal grass?
No, they do not. These higher water potentials may be an indirect effect
of greater root growth resulting from the greater access to phosphorus
provided by mycorrhizae.
FIGURE
15.3 Influence of mycorrhizae on
leaf water potential of the grass Agropyron
smithii (data from Allen and Allen 1986).
Plants with greater access to phosphorus may
develop roots that are more efficient at extracting and conducting water;
mycorrhizal fungi may not be directly involved in the extraction
of water from soils. Kay Hardie (1985) tested
this hypothesis directly with an ingenious experimental manipulation
of plant growth form and mycorrhizae. First, she grew mycorrhizal
and nonmycorrhizal red clover, Trifoliurn
pratense, in conditions in which their growth
was not limited by nutrient availability. These conditions produced
plants with similar leaf areas and root:shoot
ratios. Under these carefully controlled conditions, mycorrhizal
red clover showed higher rates of transpiration than nonmycorrhizal
plants.
Hardie took her study one step further by removing
the hyphae of mycorrhizal
fungi from half of the red clover with mycorrhizae.
She controlled for possible side effects of this manipulation by using
a tracer dye to check for root damage and by handling and transplanting
all study plants, including those in her control group. Removing hyphae
significantly reduced rates of transpiration (fig. 15.4), indicating
a direct role of mycorrhizal fungi in the
water relations of plants. Hardy suggests that mycorrhizal
fungi improve water relations of plants by giving more extensive contact
with moisture in the rooting zone and provide extra surface area for
absorption of water.
FIGURE
15.4 Effect of removing mycorrhizal
hyphae on rate of transpiration by red clover
(data from Hardie 1985).
So far, it seems that plants always benefit
from mycorrhizae. That may not always be the
case. Environmental conditions may change the flow of benefits between
plants and mycorrhizal fungi.
Nutrient
Availability and the Mutualistic Balance Sheet
Mycorrhizae supply inorganic nutrients to plants in exchange
for carbohydrates, but not all mycorrhizal
fungi deliver nutrients to their host plants at equal rates. The relationship
between fungus and plant ranges from mutualism to parasitism, depending
on the environmental circumstance and mycorrhizal
species or even strains within species.
Nancy Johnson (1993) performed experiments
designed to determine whether fertilization can select for less mutualistic mycorrhizal fungi. Before
discussing her experiments, we have to ask what would constitute a "less
mutualistic" association. In general,
a less mutualistic relationship would be one
in which there was a greater imbalance in the benefits to the mutualistic
partners. In the case of mycorrhizae, a less
mutualistic mycorrhizal fungus would
be one in which the fungal partner received an equal or greater quantity
of photosynthetic product in trade for a lower quantity of nutrients.
Johnson pointed out that there are several
reasons to predict that fertilization would favor less mutualistic
mycorrhizal fungi. The first is that plants
vary the amount of soluble carbohydrates in root exudates as a function
of nutrient availability. Plants release more soluble carbohydrates
in root exudates when they grow in nutrient-poor soils and decrease
the amount of carbohydrates in root exudates as soil fertility increases.
Consequently, fertilization of soils should favor strains, or species,
of mycorrhizal fungi capable of living in
a tow-carbohydrate environment. Johnson suggested that the mycorrhizal
fungi capable of colonizing plants releasing low quantities of carbohydrates
will probably be those that are aggressive in their acquisition of carbohydrates
from their host plants, perhaps at the expense of host plant performance.
She addressed this possibility using a mixture of field observations
and greenhouse experiments.
In the first phase of her project, Johnson
examined the influence of inorganic fertilizers on the kinds of mycorrhizal fungi found in soils. She collected soils from
12 experimental plots in a field on the Cedar Creek Natural History
Area in central
Johnson
sampled the populations of mycorrhizal fungi
from fertilized and unfertilized soils and showed that the composition
of mycorrhizal fungi differed substantially.
Of the 12 mycorrhizal species occurring in the samples, unfertilized
soil supported higher densities of three mycorrhizal
fungi, Gigaspora gigantea,
G. margarita, and Scutellispora caIospora,
while fertilized soil supported higher densities of one species, GIomus intraradix. Spores of G.
intraradix accounted for over 46% of the spores recovered
from fertilized soils but only 27% of the spores from unfertilized soils.
Johnson used greenhouse experiments to assess
how these differences in the composition of mycorrhizal
fungi might affect plant performance. She chose big bluestem grass,
Andropogon gerardii, as a study
plant for these experiments because it is native to the Cedar Creek
Natural History Area and is well adapted to the nutrient-poor soils
of the area. Seedlings of Andropogon were
planted in pots containing
To each pot Johnson added a mycorrhizal "inoculum"
of
FIGURE
15.5 Testing the effects of long-term fertilizing on interactions
between mycorrhizal fungi and plants on agricultural
lands.
Why did Johnson create her inocula by mixing sterilized and unsterilized
soils from the fertilized and unfertilized study areas? She did so to
control for the possibility that some nonbiological
factor such as trace nutrients in one of the two soil types might have
a measurable effect on plant performance. The completely sterilized
inoculum acted as a control to assess the
performance of plants in the absence of mycorrhizae. Why did Johnson's control consist of sterilized
composite soil from all the study areas? Again, she had to guard against
the possibility that the soils themselves without mycorrhizal
fungi might affect plant performance.
Pots were next assigned to one of four nutrient
treatments in which Johnson (1) added no supplemental nutrients (None),
(2) added phosphorus only (+P), (3) added nitrogen only (+N), or (4)
added both nitrogen and phosphorus (+N+P). The subsurface sand from
the Cedar Creek Natural History Area contained a fairly low concentration
of nitrogen but considerably higher concentrations of phosphorus. Nutrient
additions were adjusted so that the supplemented treatments offered
nitrogen and phosphorus concentrations comparable to those of the topsoil
in the fertilized study plots.
Johnson harvested five replicates of each
of the treatments at two points in time: at 4 weeks, when Andropogon
was actively growing, and at 12.5 weeks, when the grass was fully grown.
At each harvest she measured several aspects of plant performance: plant
height, shoot mass, and root mass; and at 12.5 weeks she also recorded
the number of inflorescences per plant.
At 12.5 weeks shoot mass was significantly
influenced by nutrient supplements and by whether or not plants were
mycorrhizal but not by the source of the mycorrhizal inoculum (fig. 15.6).
Shoot mass was greatest in the double nutrient supplement treatment
(+N+P), somewhat lower in the nitrogen supplement (+N), and very low
in the other two treatments (None and +P). Figure
Nutrient supplements and mycorrhizae also significantly influenced root:shoot ratios (fig. 15.6b). As
we saw in chapter 6, plants invest differentially in roots and shoots
depending on nutrient and light availability. It also appears that variation
in investment is aimed at increasing supplies of resources in short
supply. For instance, in nutrient-poor environments many plants invest
disproportionately in roots and consequently have high root:shoot
ratios, which decline with increasing nutrient availability. The results
of Johnson's experiments
are consistent with this generalization. Root: shoot ratios were
highest in the treatments without nitrogen supplements (None and +P)
and lowest in the treatments with nitrogen supplements (+N and +N+P).
In other words, higher plant investment in roots in the low-nitrogen
treatments suggests greater nutrient limitation than in the high-nitrogen
treatments.
FIGURE
15.6 Effect of nutrient additions and mycorrhizae
on the grass Andropogon gerardii
(data from Johnson 1993).
Now let's look a bit deeper into Johnson's
results, where we find evidence for increased nutrient availability
to mycorrhizal plants. In both the +N and "None" treatments,
root:shoot ratios
were significantly lower in plants with mycorrhizae
(fig. 15.6b). Mycorrhizal plants in these
treatments invest less in roots, suggesting that they have greater access
to nutrients. Here we also see a hint that the source of the inoculum
significantly influenced plant performance. Plants in the +N+P treatment
that were inoculated with soils from the unfertilized plots had slightly
lower root:shoot ratios than those inoculated
with soil from fertilized plots. These lower root:shoot ratios suggest that the mycorrhizal
fungi from unfertilized soils were supplying their plant partners with
more nutrients, freeing the plants to invest more of their energy budget
in aboveground photosynthetic tissue.
Inflorescence production provides the strongest
evidence for an effect of inoculum source
on plant performance (fig.
In summary, Johnson's study produced two pieces
of evidence that bear on the question posed at the outset of her study:
Can fertilization of soil select for less mutualistic
mycorrhizal fungi? First, in the early stages of her experiment,
Andropogon inoculated with fertilized soil
had lower shoot mass than those inoculated with unfertilized soil. Second,
Andropogon inoculated with unfertilized soils
produced more inflorescences than did Andropogon
inoculated with fertilized soils. In other words, Andropogon
inoculated with mycorrhizal fungi from unfertilized
soils showed faster shoot growth as young plants and reproduced at a
higher rate when mature. These results suggest that plants receive more
benefit from association with the mycorrhizal
fungi from unfertilized soils. Johnson's simultaneous studies of the
mycorrhizal fungi indicate the mechanisms
producing these patterns. It appears that altering the nutrient environment
does alter the mutualistic balance sheet,
an influence of potential importance to agricultural practice.
Plants engage in a wide variety of mutualisms
with many other organisms. One of those involves associations that provide
protection from exploiters and competitors. Writing about the natural
history of mutualism, Daniel Janzen (1985)
included "plant-ant protection mutualisms" as one of his general
categories of mutualism. Janzen (1966,
Ants
and Bullshorn Acacia
The ants mutualistic
with swollen thorn acacias are members of the genus Pseudomyrmex
in the subfamily Pseudomyrmecinae. This subfamily
of ants is dominated by genera and species that have evolved close relationships with
living plants. Pseudomyrmex spp.
are generally associated with trees and show
several characteristics that Janzen suggested
are associated with arboreal living. They are generally fast and agile
runners, have good vision, and forage independently. To this list, the
Pseudomyrmex spp.
associated with swollen thorn acacias, or "acacia-ants," add
aggressive behavior toward vegetation and animals contacting their home
tree, larger colony size, and 24-hour activity outside of the nest.
This combination of characteristics means that any herbivore attempting
to forage on an acacia occupied by acacia-ants is met by a large number
of fast, agile, and highly aggressive defenders and is given this reception
no matter what time of the day it attempts to feed. Janzen listed six species of Pseudomyrmex
with an obligate mutualistic relationship
with swollen thorn acacias and refers to three additional undescribed
species. His experimental work focused principally on one species, Pseudomyrmexferruginea.
Worldwide, the genus Acacia includes over
700 species. Distributed throughout the tropical and subtropical regions
around the world, acacias are particularly common in drier tropical
and subtropical environments. The swollen thom
acacias, which form obligate mutualisms with Pseudomyrmex
spp., are restricted to the New World, where
they are distributed from southern
Janzen's detailed natural history of the interaction
between bullshorn acacia and ants paints a
rich picture of mutual benefits to both partners (fig. 15.7). Newly
mated Pseudomyrmex queens fly and run through the vegetation searching
for unoccupied seedlings or shoots of bullshorn
acacia. When a queen finds an unoccupied acacia, she excavates an entrance
in one of the green thorns or uses one carved previously by another
ant. The queen then lays her first eggs in the thorn and begins to forage
on her newly acquired home plant. She gets nectar for herself and her
developing larvae from the foliar nectaries
and gets additional solid food from the Beltian
bodies. As time passes, the number of workers in the new colony increases,
and while they take up all the chores of the colony, the queen shifts
to a mainly reproductive function; her abdomen enlarges and she becomes
increasingly sedentary.
FIGURE
15.7 Split thorn of a bullshorn
acacia, revealing a nest of its ant mutualists.
In exchange for food and shelter, ants protect
acacias from attack by herbivores and competition from other plants.
Workers have several duties, including foraging for themselves, the
larvae, and the queen. One of their most important activities is protecting
the home plant. Workers will auack, bite,
and sting nearly all insects they encounter on their home plant or any
large herbivores such as deer and cattle that attempt to feed on the
plant. They will also attack and kill any vegetation encroaching on
the home tree. Workers sting and bite the branches of other plants that
come in contact with their home tree or that grow near its base. These
activities keep other plants from growing near the base of the home
tree and prevent other trees, shrubs, and vines from shading it. Consequently
the home plant's access to light and soil nutrients is increased.
Once a colony has at least 50 to 150 workers,
which takes about 9 months, they patrol the home plant day and night.
About one-fourth of the total colony is active at all times. Eventually
colonies grow so large that they occupy all the thorns on the home tree
and may even spread to neighboring acacias. The queen, however, generally
remains on the shoot that she colonized originally. When the colony
reaches a size of about 1,200 workers, it begins producing a more or
less steady stream of winged reproductive males and females, which fly
off to mate. The queens among them may eventually establish new colonies
on other bullshorn acacias or one of the other
Central American swollen thorn acacias. Colonies may eventually reach
a total population of 30,000 workers.
Experimental
Evidence for Mutualism
While much of the natural history of this
mutualism was known at the time Janzen conducted
his studies, no one had experimentally tested the strength of its widely
supposed benefits, Janzen took his work beyond
natural history to experimentally test for the importance of ants to
bullshorn acacias. It was clear that the ant
needs swollen thorn acacias, but do the acacias need the ants? Janzen's
experiments concentrated on the influence of ants on acacia performance.
He also tested the effectiveness of the ants at keeping acacias free
of herbivorous insects. Janzen removed ants from acacias by clipping occupied thorns
or by cutting out entire shoots with their ants. He then measured the
growth rate, leaf production, mortality, and insect population density
on acacias with and without ants.
Janzen's experiments demonstrated that ants significantly
improve plant performance. Differences in plant performance were likely
the result of increased competition with other plants and increased
attack by insects faced by acacias without their tending ants. Suckers
growing from stumps of acacias occupied by ants lengthened at seven
times the rate of suckers without ants (fig. 15,8).
Suckers with ants were also more than 13 times heavier than suckers
without ants and had more than twice the number of leaves and almost
three times the number of thorns. Suckers with ants also survived at
twice the rate of suckers without ants (fig. 15.9).
FIGURE
15.8 Growth by bullshorn acacia
with and without resident ants (data from Janzen
1966).
FIGURE
15.9 Survival of bullshorn acacia
shoots with and without resident ants (data from Janzen
1966).
What produces the improved performance of
acacias with ants? One factor appears to be reduced populations of herbivorous
insects. Janzen found that acacias without
ants had more herbivorous insects on them than did acacias with ants
(fig.15.10). Janzen's experiments provide strong evidence that bullshorn acacias need ants as much as the ants need the acacia.
It appears that this is a truly mutualistic
situation and that it is obligate for both partners.
FIGURE
15.10 Ants and the abundance of herbivorous insects on bullshorn acacia (data from Janzen
1966).
While tropical plant protection mutualisms
are most often cited, there are many examples of mutualism between plants
and ants in the temperate zone. A particularly wellstudied
interaction is that between ants and the aspen sunflower, Helianthella
quinquenervis.
A
Temperate Plant Protection Mutualism
Aspen sunflowers live in wet mountain meadows
of the Rocky Mountains from
The extrafloral
nectar produced by aspen sunflowers is rich in sucrose and contains
high concentrations of a wide variety of amino acids. So, like the swollen
thorn acacias studied by Janzen the aspen sunflower
provides food to ants. In contrast to swollen thorn acacias,
however, this sunflower does not provide living places. This contrast
is general across temperate ant-plant mutualisms, which involve food
as an attractant but no living quarters.
David Inouye and Orley
Taylor (1979) recorded five species of ants on aspen sunflowers, including
Formica
obscuripes, F.fusca, F. integroides planipilis, Tapinoma sessile, and Myrmica sp.
These ants are not obligately associated with
aspen sunflowers and can be found tending aphids on other species of
plants or even collecting flower nectar on some plants. However, Inouye
and Taylor never observed them collecting nectar from aspen sunflower
blossoms nor tending aphids on this plant. Apparently, the extrafloral
nectar produced by the aspen sunflower is a sufficient attractant. Ants
find the plant so attractive that Inouye and Taylor observed up to 40
ants on a single flower stalk.
While the ants visiting the extrafloraI nectaries of Helianthella clearly derive benefit, it is not obvious that
the plant receives any benefits from the association. What benefits
might this sunflower gain by having ants roaming around its flowers
and flower buds? Inouye and Taylor proposed that the ants may protect
the sunflower's developing seeds from seed predators. In the central
The high densities of ants that can occur
on a single
The question asked by Inouye and Taylor was
whether or not the presence of ants on aspen sunflowers reduces the
rate of attack by seed predators. They addressed this question in several
ways. First, they compared rates of attack by seed predators on flowers
tended by ants with rates of attack on flowers where ants were naturally
absent. This comparison showed that flowers without ants suffered two
to four times as much seed predation (fig.15.11). The researchers also
found that the average number of ants per flower stalk decreased with
distance from an ant nest and that the plants with fewer ants suffered
higher rates of seed damage by seed predators.
FIGURE
15.11 Predation on the seeds of aspen sunflower with and without
ants (data from Inouye and Taylor 1979).
Next, Inouye and Taylor performed an experiment
in which they prevented ants from moving onto some plants by applying
a sticky barrier to the base of flower stalks. They used adjacent plants
as controls. How did this experimental manipulation strengthen Inouye
and Taylor's study? Why wasn't the comparison of plants naturally with
and without ants sufficient to assess the influence of ants on rates
of seed predation? It might have been that the flowers frequented by
ants are visited less often by seed predators for some other reason.
If so, then demonstrating that flowers without ants experience greater
seed predation may have simply reflected a low overlap in the distributions
of ants and seed predators. The results of Inouye and Taylor's experiment
rule out this possibility (fig. 15.12). At two of their study sites,
exclusion of ants from flowers resulted in significantly higher rates
of seed predation.
FIGURE
15.12 Effect of excluding ants on rates of seed predation
on aspen sunflowers (data from lnouye and
As in the tropical swollen thorn acacia-ant
mutualism, ants associated with aspen sunflowers provide protection
while receiving substantial benefits in the form of food. Unlike the
tropical system, the association between aspen sunflowers and ants incorporates
a significant degree of flexibility. This flexibility may be a hallmark
of many temperate mutualisms.
Why does the relationship between ants and
aspen sunflowers remain facultative? In other words, why hasn't there
been strong selection for the kind of obligate relationship, such as
that between bullshorn acacia and the ant P. ferruginea?
Continuing studies by David Inouye provide clues. He estimated the abundance
of aspen sunflowers on two study plots for more than two decades. This
long-term study shows that every few years the flower heads of aspen
sunflowers are killed by late frosts. From 1974 to 1995,
FIGURE 15.13
Annual variation in numbers of flower heads produced by aspen
sunflowers on two plots at the
If we venture into tropical seas and probe
their inhabitants, we soon uncover a wide variety of mutualistic
relationships at least as rich as those we examined between terrestrial
plants and their partners. The most striking marine counter parts to
the mutualisms of terrestrial plants are those centered around
reef-building corals.
CASE HISTORIES:coral
mutualisms
Reef-building
corals depend upon mutualistic relationships
with algae and animals.
Because of the importance of mutualism in
the lives of reefbuilding corals, it appears
that the ecological integrity of coral reefs depends upon mutualism.
Coral reefs show exceptional productivity and diversity. Recent estimates
put the number of species occurring on coral reefs at approximately
0.5 million, and coral reef productivity is among the highest of any
natural ecosystem. As we saw in chapter 3, the paradox is that this
overwhelming diversity and exceptional productivity occurs in an ecosystem
surrounded by nutrient-poor tropical seas. The key to explaining this
paradox lies with mutualism; in this case, between reef-building corals
and unicellular algae called zooxanthellae,
members of the phylum Dinoflagellata. Most
of these organisms are free-living unicellular marine and freshwater
photoautotrophs.
Zooxanthellae and Corals
The association between corals and zooxanthellae is functionally similar to the relationship
between plants and mycorrhizal fungi. Zooxanthellae live within coral tissues at densities averaging
approximately 1 million cells per square centimeter of coral surface.
Like plants, zooxanthellae receive nutrients
from their animal partner. In return, like mycorrhizal
fungi, the coral receives organic compounds synthesized by zooxanthellae
during photosynthesis.
One of the most fundamental discoveries concerning
the relationship between corals and zooxanthellae
is that the release of organic compounds by zooxanthellae
is controlled by the coral partner. Corals induce zooxanthellae
to release organic compounds with "signal" compounds, which
alter the permeability of the zooxanthellae
cell membrane. Zooxanthellae grown
in isolation from corals release very little organic matehal
into their environment. However, when exposed to extracts of
coral tissue, zooxanthellae immediately increase
the rate at which they release organic compounds. This response appears
to be a specific chemically mediated communication between corals and
zooxanthellae. Zooxanthellae
do not respond to extracts of other animal tissues, and coral extracts
do not induce leaking of organic molecules by any other algae that have
been studied.
Corals not only control the secretion of organic
compounds by zooxanthellae, they also control
the rate of zooxanthellae population growth
and population density. In corals, zooxanthellae
populations grow at rates 1/10 to 1/100 the rates observed when they
are cultured separately from corals. Corals exert control over zooxanthellae
population density through their influence on organic matter secretion.
Normally, unicellular algae show balanced growth, growth in which all
cell constituents, such as nitrogen, carbon, and DNA, increase at the
same rate. However, zooxanthellae living in coral tissues show unbalanced growth,
producing fixed carbon at a much higher rate than other cell constituents.
Moreover, the coral stimulates the zooxanthellae
to secrete 90% to 99% of this carbon, which the coral uses for its own
respiration. Carbon secreted and diverted for use by the coral could
otherwise be used to produce new zooxanthellae,
which would increase population growth.
What benefits do the zooxanthellae
get out of their relationship with corals? The main benefit appears
to be access to higher levels of nutrients, especially nitrogen. Corals
feed on zooplankton, which gives them a means of capturing nutrients,
especially nitrogen and phosphorus. When corals metabolize the protein
in their zooplankton prey, they excrete ammonium as a waste product.
L. Muscatine and C. D'Elia (1978) showed that
coral species such as Tubastrea aurea that do not harbor zooxanthellae
continuously excrete ammonium into their environment, while corals such
as Pocillopora damicornis do not excrete
measurable amounts of ammonia (fig. 15.14). What happens to the ammonium
produced by Pocillopora during metabolism
of the protein in their zooplankton prey?
FIGURE
15.14 Zooxanthel lae, corals, and ammonium fiux (data
from
A
Coral Protection Mutualism
The ant-acacia mutualism that we reviewed
previously has a striking parallel on coral reefs. Corals in the genera
Pocillopora and Acropora host a
variety of crabs ill the family Xanthidae,
mainly Trapezia spp. and Tretralia spp. as well as a species
of pistol shrimp,
FIGURE
15.15 Pistol shrimp will defend their home coral from attacking
predators.
Peter Glynn (1983) surveyed the coral-crustacean
mutualism and found that the eastern, central, and western areas of
the
Glynn used field and laboratory experiments
to test whether this aggression by crustaceans is effective at repelling
attacks by predatory sea stars. He conducted a field experiment at 8
to
FIGURE
15.16 Attacks on corals with and without pistol shrimp and
crabs (data from Glynn 1983).
Observations by Glynn and also John Stimson (1990) suggest that mutualistic
crabs also protect corals from other less conspicuous attackers. Glynn
observed that the presence of crabs seems to enhance the condition of
coral tissues. Stimson found that when he removed crabs, corals showed tissue
death in the deep axils of their branches and that these areas were
soon invaded by algae, sponges, and tunicates. It appears that, in addition
to protecting corals from the attacks of large predators, the activities
of crabs promote the health and integrity of coral tissues. If this
is a mutualistic relationship, what do the crabs receive in return
for their investment?
Like swollen thorn acacias, corals provide
their crustacean mutualists with shelter and
food. The corals harboring crabs and pistol shrimp have a tightly branched
growth form that offers shelter, and the crustaceans feed on the mucus
produced by the corals.Trapezia spp.,
the most common crabs guarding pocilloporid
corals, stimulate mucus flow from corals by inserting their legs into
coral polyps, a behavior not reported for any other crabs. Corals contain
large quantifies of lipids that constitute 30% to 40% of the dry weight
of their tissues, much of which they release with mucus. This release
may constitute up to 40% of the daily photosynthetic production by zooxanthellae.
The pocilloporid
corals that host crustaceans concentrate some of this lipid into fat
bodies that are 300 to 500 μm in length. Glynn
suggested that the fat bodies produced by pocilloporid
corals hosting protective crabs may be a part of their mutualistic
relationship. Stimson tested this hypothesis
by determining whether commensal crabs influence
the production of fat bodies by coral polyps. He conducted his experiments
at the Hawaii Institute of Marine Biology on
After 24 days, Stimson
compared the number of fat bodies on corals with and without crabs.
He also compared these experimental results with the density of fat
bodies on Pocillopora in
FIGURE 15.17
Fat body production by the coral Pocillopora
damicornis in the presence and absence of
crabs (data from Stimson 1990).
The extent of benefit may be the essential
factor driving the evolution of mutualisms. In the following case histories,
we review theoretical analyses of how the relative benefits and costs
of an association influence the evolution of mutualistic
relationships.
CASE HISTORIES: evolution of mutualism
Theory
predicts that mutualism will evolve where the benefits of mutualism
exceed the costs.
We have reviewed several complex mutualisms
both on land and in marine environments. There are many others (fig.15.18),
every one a fascinating example of the intricacies of nature. Ecologists
not only study the present biology of those mutualisms but also seek
to understand the conditions leading to their evolution and persistence.
Theoretical analyses point to the relative costs and benefits of a possible
relationship as a key factor in the evolution of mutualism.
Modeling of mutualism has generally taken
one of two approaches. The earliest attempts involved modifications
of the Lotka-Volterra equations to represent the population dynamics
of mutualism. The alternative approach has been to model mutualistic
interactions using cost-benefit analysis to explore the conditions under
which mutualisms can evolve and persist. In chapters 13 and 14, where
we discussed models of competition and predation, we focused on the
population dynamic approach to modeling species interactions. Here,
we concentrate on cost-benefit analyses of mutualism.
FIGURE
Kathleen Keeler (1981) developed models to
represent the relative costs and benefits of several types of mutualistic interactions. Among them are two of the mutualistic interactions we discussed in this chapter: ant-plant
protection mutualisms and mycorrhizae. Keeler's
approach requires that we consider a population polymorphic for mutualism
containing three kinds of individuals: (1) successful mutualists, which give and receive
measurable benefits to another organism; (2) unsuccessful mutualists,
which give benefits to another organism but, for some reason, do not
receive any benefit in return; and (3) nonmutualists,
neither giving nor receiving benefit from a mutualistic
partner. The bottom line in Keeler's approach is that for a population
to be mutualistic, the fitness of successful mutualists
must be greater than the fitness of either unsuccessful mutualists
or nonmutualists. In addition, the combined
fitness of successful and unsuccessful mutualists
must exceed that of the fitness of nonmutualists.
If these conditions are not met, Keeler proposed that natural selection
will eventually eliminate the mutualistic
interaction from the population.
In general, we can expect mutualism to evolve
and persist in a population when and where mutualistic
individuals have higher fitness than nonmutualistic
individuals.
Keeler represented the fitness of nonmutualists as:
Wnm
= fitness of nonmutualists
(Fitness has been traditionally represented
by the symbol w and though it might be clearer to use another symbol,
such as f the traditional symbol is used here.) Keeler represents the
fitness of mutualists as:
Wm= pWms
+ qWmu (1)
where:
p = the proportion of the population consisting of
successful mutualists
wms = the fitness of successful
mutualists
q = the proportion of the population consisting of
unsuccessful mutualists
Wmu = the fitness of unsuccessful mutualists.
We can represent Keeler's conditions for the
evolution and persistence of mutualism as:
Wm > Wnm (2)
or
pWms
+ qWmu > Wnm (3)
Keeler predicts that mutualism will persist
when the combined fitness of successful and unsuccessful mutualists
exceeds the fitness of nonmutualists. Why
do we have to combine the fitness of successful and unsuccessful mutualists?
Remember that both confer benefit to their partner, but only the successful
mutualists receive benefit in return.
The analysis is more convenient if we think
of these relationships in terms of selection coefficients (s), the relative
selective costs associated with being either a
successful mutualist, an unsuccessful mutualist,
or a nonmutualist:
s = 1 - w and w = (1 - s).
Using selective coefficients, Keeler expressed
the selective cost of being a successful mutualist,
an unsuccessful mutualist, or a nonmutualist
as:
Sms
= (H)(1 - A)(1 - D) + IA + ID
(4)
Smu
= (H)(1 - D) + lA
+ ID (5)
Snm
= H(1 - D) + ID (6)
where:
H = the proportion of the plant
tissue damaged in the absence of any defenses
D = the amount of protection
given to the plant tissues by defenses other than ants (e.g. chemical
defenses); so, 1 - D is the amount of tissue damage that would occur
in spite of these alternative defenses
A = the amount of herbivory prevented by ants (so, again, 1 - A is the amount
of herbivory that occurs in spite of ants)
Ia = the investment by the plant in benefits
extended to the
ants
ID = investment
in defenses other than ants Using these selective coefficients we can
express Keeler's conditions for evolution and persistence of the antplant
mutualism as:
p(1 - Sms) - q(1 - Smu)
> 1 -- Snm
into which Keeler substituted the relationships
given in equations (4), (5), and (6). By simplifying the resulting equation,
she produced the following expression of benefits relative to costs:
p[H (1 - D) A] > IA
Facultative
Ant-Plant Protection Mutualisms
Keeler applied her cost-benefit model to facultative
mutualisms involving plants with extrafloral
nectaries and ants that feed at the nectaries and provide protection to the plant in return. These
are mutualisms like that between Helianthella
quinquenervis and ants, which we discussed earlier in the
chapter in the Case Histories section on plant mutualism. Her model
is not appropriate for obligate mutualisms like that between swollen
thom acacias and their mutualistic
ants. In addition, Keeler wrote her model from the perspective of the
plant side of the mutualism. Let's step through the general model and
connect each of the terms with the ecology of facultative plant-ant
protection mutualisms.
In this model, Wms
is the fitness of a plant that produces extrafloral
nectaries and that successfully attracts ants effective at
guarding it,while
Wmu is the fitness of a plant that produces extrafloral nectaries but that has
not attracted enough ants to mount a successful defense. You may remember
that Inouye and Taylor found that Helianthella
far away from ant nests attracted few ants. These plants would correspond
to Keeler's unsuccessful mutualists. In addition,
Keeler includes the fitness of nonmutualistic
plants, Wnm, which would be the fitness of individuals
of a plant such as Helianthella that does
not produce extrafloral nectaries.
Are there such individuals in the population of Helianthella
studied by Inouye and Taylor? We don't know, but that is not the point.
The reason Keeler includes nonmutualists in
her model is to provide an assessment of the potential costs and benefits
of such a strategy against which she can weigh the mutualistic
strategy.
Keeler's model represents potential benefits
to the host plant as:
p
[H (1 - D) A]
where:
p = the proportion of
the plant population attracting sufficient ants to mount a defense.
Keeler's model represents the plant's costs
of mutualism as:
IA = n[m+
d (a + c + h)]
where:
n = the number of extrafloral nectaries per plant
m = the energy content
of nectary structures
d = the period of time
during which the nectaries are active
a = costs of producing
amino acids in nectar
c = costs of producing
the carbohydrates in nectar
h = costs of providing
water for nectar
Again, Keeler's hypothesis is that for mutualism
to persist, benefits must exceed costs. In terms of her model:
p[H(1 - D)A] >
lA
This model proposes that for a facultative
ant-plant mutualism to evolve and persist, the proportion of the plant's
energy budget that ants save from destruction by herbivores must exceed
the proportion of the plant's energy budget that is invested in extrafloral
nectaries and nectar.
The details of Keeler's model offer insights
into what conditions may produce higher benefits than costs. First,
and most obviously, IA, the proportion of the plant's energy
budget that is invested in extrafloral nectaries
and nectar should be low. This means that plants living on a tight energy
budget, for example, plants living in a shady forest understory, should be less
likely to invest in attracting ants than those living in full sun. Higher
benefits result from (1) a high probability of attracting ants, that
is, high p; (2) a high potential for herbivory, H; (3) low effectiveness of alternative defenses,
low D, and (4) highly effective ant defense, high A.
The task for ecologists is to determine how
well these requirements of the model match values of these variables
in nature.
APPLICATIONS AND TOOLS: mutualism and humans
Mutualism has been important in the lives
and livelihood of humans for a long time. Historically, much of agriculture
has depended upon mutualistic associations
between species and much of agricultural management has been aimed at
enhancing mutualisms, such as nitrogen fixation, mycorrhizae,
and pollination to improve crop production. Agriculture itself has been
viewed as a mutualistic relationship between
humans and crop and livestock species. However, there may be some qualitative
differences between agriculture as it has been generally practiced and
mutualisms among other species. How much of agriculture is pure exploitation
and how much is truly mutualistic remains
an open question.
There is, however, at least one human mutualism
that fits comfortably among the case histories that we have discussed
in this chapter, a mutualism involving communication between humans
and a wild species with clear benefit to both. This mutualism joins
the traditional honey gatherers of
FIGURE
15.19 The greater honeyguide, Indicator
indicator.
There is, however, at least one human mutualism
that fits comfortably among the case histories that we have discussed
in this chapter, a mutualism involving communication between humans
and a wild species with clear benefit to both. This mutualism joins
the traditional honey gatherers of
The
Honeyguide
Honeyguides belong to the family Indicatoridae
in the order Piciformes, an order that also
includes the woodpeckers. The family Indicatoridae
includes a total of 17 species, 15 of which are native to
The greater honeyguide
is found throughout much of sub-Saharan
Greater honeyguides
are capable of completely independent life without mutualistic
interactions with humans, so we would classify their mutualism as facultative.
Living independently, honeyguides feed on
beeswax, and on the adults, larvae, pupae, and eggs of bees. They also
feed on a wide variety of other insects. Greater honeyguides
show highly opportunistic feeding behavior and sometimes join flocks
of other bird species foraging on the insects stirred up by large mammals.
The most distinguishing feature of the greater honeyguide,
however, is its habit of guiding humans and ratels,
or honey badgers, to bees' nests.
Guiding
Behavior
The first written report
of the guiding behavior of 1. indicator was authored in 1569 by Joao Dos Santos,
a missionary in the part of East Africa that is now
Friedmann's report of some of the African legends surrounding
the greater honeyguide suggests that a wide
variety of African cultures prescribed rewarding the bird for its guiding
behavior and that native Africans recognized the need for reciprocity
in their interactions with honeyguide. One
proverb reported by Friedmann was, "If you do not leave anything for the
guide [I. Indicator], it will not lead you at all in the future."
Another proverb stated more ominously, "If you do not leave anything
for the guide, it will lead you to a dangerous animal the next time."
Friedmann also observed that many African cultures forbid
killing a honeyguide and once "inflicted
severe penalties" for doing so. These observations suggest long
association between humans and honeyguides and that the association has been consciously
mutualistic on the human side of the balance sheet.
The mutualistic
association between humans and honeyguides
may have developed from an earlier association between the bird and
the ratel, or honey badger, Mellivora
capensis. The honey badger is a powerful animal,
well equipped with strong claws and powerful muscles to rip open bees'
nests, that readily follows honeyguides. The
honey badger, though secretive, has been observed often following honeyguides
while vocalizing. African honey gatherers also vocalize to attract honeyguides, and Friedmann reported
that some of their vocalizations imitate the calls of honey badgers.
The most detailed and quantitative study of
this mutualism to date is that of H. lsack
of the National Museum of Kenya and H.-U. Reyer
of the
The greater honeyguide
attracts the attention of a human by flying close and calling as it
does so. Following this initial attention-getting behavior the bird
will fly off in a particular direction and disappears for up to 1 minute.
After reappearing, the bird again perches in a conspicuous spot and
calls to the following humans. As the honey gatherers follow, they whistle,
bang on wood, and talk loudly in order to "keep the bird interested.''
When the honey gatherers approach the perch from which the honeyguide
is calling, the bird again flies off, calling and displaying its white
tail feathers as it does so, only to reappear at another conspicuous
perch a short time later. This sequence of leading, following, and leading
is repeated until the bird and the following honey gatherers arrive
at the bees' nest. Isack, who is aBoran,
interviewed Boran honey gatherers to determine
what information they obtained from honeyguides.
The main purpose of the study was to test assertions by the honey gatherers
that the bird informs them of (1) the direction to the bees' nest, (2)
the distance to the nest, and (3) when they arrive at the location of
the nest. The data gathered by Isack and Reyer
support all three assertions.
Honey gatherers reported that the bird indicated
direction to the bees' nest on the basis of the direction of its guiding
flights. One method used by Isack and Reyer to test how well flight direction indicated direction
was to induce honeyguides to guide them from
the same starting point to the same known bees' nest on five different
occasions. Figure
FIGURE
15.20 Paths taken by honeyguides
leading people to bees' nests (data from lsack
and Reyer 1989).
The Boran honey
gatherers said that three variables decrease as distance to the nest
decreases: (1) the time the bird stays out of sight during its first
disappearance following the initial encounter, (2) the distance between
stops made by the bird on the way to the bees' nest, and (3) the height
of the perch on the way to the nest. Data gathered by Isack
and Reyer support all three statements (fig. 15.21).
FIGURE
15.21 Changes in behavior of the honeyguide
as it nears a bees' nest (data from lsack
and Reyer 1989).
The honey gatherers also report that they
can determine when they arrive in the vicinity of a bees' nest by changes
in the honeyguide's behavior and vocalizations
(fig. 15.22). Isack and Reyer
observed several of these changes. While on the path to a bees' nest
a honeyguide emits a distinctive guiding call and will answer
human calls by increasing the frequency of the guiding call. On arriving
at a nest, the honeyguide perches close to
the nest and gives off a special "indication" call. After
a few indication calls, it remains silent and does not answer to human
sounds. If approached by a honey gather, a honeyguide
flies in a circle around the nest location before perching again nearby.
FIGURE
15.22 Vocal communication between
honeyguides and humans.
Isack and Reyer observe
that their data do not allow them to test other statements by the Boran honey gatherers, including that when bees' nests are
very far away (over
SUMMIARY CONCEPT
Mutualism, interactions between individuals
that benefit both partners, is a common phenomenon in nature that has
apparently made important contributions to the evolutionary history
of life and continues to make key contributions to the ecological integrity
of the biosphere. Mutualisms can be divided into those that arefacultative,
where species can live without their mutualistic
partners, and obligate, where species are so dependent on the mutualistic
relationship that they cannot live without their mutualistic
partners.
Plants benefit from mutualistie
partnerships with a wide variety of bacteria, fungi, and animals. Mutualism provides benefits to plants ranging
from nitrogen fixation and enhanced nutrient and water uptake to pollination
and seed dispersal. Ninety percent of terrestrial plants form mutualistic relationships with mycorrhizal
fungi, which make substantial contributions to plant performance. Mycorrhizae, which are mostly either vesicular-arbuscular mycorrhizae or ectomycorrhizae, are important in increasing plant access
to water, nitrogen, phosphorus, and other nutrients. In return for these
nutrients, mycorrhizae receive energy-rich
root exudates. Experiments have shown that the mutualistic
balance sheet between plants and mycorrhizal
fungi can be altered by the availability of nutrients. Plant-ant protection
mutualisms are found in both tropical and temperate environments. In
tropical environments, many plants provide ants with food and shelter
in exchange for protection from a variety of natural enemies. In temperate
environments, mutualistic plants provide ants
with food but not shelter in trade for protection.
Reef-building
corals depend upon mutualistic relationships
with algae and animals. The coral-centered mutualisms of tropical seas show striking
parallels with terrestrial plant-centered mutualisms. Mutualistic algae
called zooxanthellae provide reef-building
corals with their principal energy source; in exchange for this energy,
corals provide zooxanthellae with nutrients,
especially nitrogen, a scarce resource in tropical seas. The mutualism
between corals and zooxanthellae appears to be largely under the control of the
coral partner, which chemically solicits the release of organic compounds
from zooxanthellae and controls zooxanthellae
population growth. Crabs and shrimp protect some coral species from
coral predators in exchange for food and shelter.
Theory
predicts that mutualism will evolve where the benefits of mutualism
exceed the costs.
Keeler built a cost-benefit model for the evolution and persistence
of facultative plant-ant protection mutualisms in which the benefits
of the mutualism to the plant are represented in terms of the proportion
of the plant's energy budget that ants protect from damage by herbivores.
The model assesses the costs of the mutualism to the plant in terms
of the proportion of the plant's energy budget invested in extrafloral nectaries and the water,
carbohydrates, and amino acids contained in the nectar. The model predicts
that the mutualism will be favored where there are high densities of
ants and potential herbivores and where the effectiveness of alternative
defenses are low.
Humans have developed a variety of mutualistic relationships with other species, but one of the
most spectacular is that between the greater honeyguide
and the traditional honey gatherers of
REVIEW QUESTIONS
1. List and briefly describe mutualistic relationships that seem to contribute to the ecological
integrity of the biosphere.
2. What contributions do mycorrhizal fungi make to their plant partners? What do plants
contribute in return for the services of mycorrhizal
fungi? How did Hardie (1986) demonstrate that mycorrhizae
improve the water balance of red clover? How do mycorrhizae
improve the capacity of plants to take up water from their environment?
3. Outline the experiments of Johnson (1993),
which she designed to test the possibility that artificial fertilizers
may select for less mutualistic mycorrhizal
fungi. What evidence does Johnson present in support of her hypothesis?
4. Explain how mycorrhizal
fungi may have evolved from ancestors that were originally parasites
of plant roots. Do any of Johnson's results (1993) indicate that present-day
mycorrhizal fungi may act like parasites?
Be specific,
5. Janzen (1985)
encouraged ecologists to take a more experimental approach to the study
of mutualistic relationships. Outline the details of Janzen's own experiments on the mutualistic
relationship between swollen thom
acacias and ants.
6. Inouye and Taylor's study (1979) of the
relationship between ants and the aspen sunflower, HeliantheIla
quinquenervis, pro-Vides a reasonable representative
of temperate ant-plant protection mutualisms. Compare this mutualism
with that of the tropical mutualism between swollen thorn acacias and
ants.
7. How are the coral-centered mutualisms similar
to the plant-centered mutualisms we discussed in this chapter? How are
they different? The exchanges between mutualistic
partners in both
systems revolve around energy, nutrients, and protection. Is this an
accident of the case histories discussed or are these key factors in
the lives of organisms?
8. Outline the benefits and costs identified
by Keeler's (1981) cost-benefit model for facultative ant-plant mutualism.
From what perspective does Keeler's model view this mutualism? From the perspective of plant or ant? What would be some of
the costs and benefits to consider if the model was built from the perspective
of the other partner?
9, How could you
change the Lotka-Volterra model of competition
we discussed in chapter 13 into a model of mutualism? Would the resulting
model be a cost-benefit model or a population dynamic model?
10. Outline how the honeyguide-human
mutualism could have evolved from an earlier mutualism between honeyguides and honey badgers. In many parts of