Townsend C.R., Begon M., Harper J.L. Essentials of Ecology

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Chapter 8 Evolutionary ecology

269

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Cleaner fish

No cleaner fish

(b)

(a)

(c)

Gnathiids per fishGnathiids per fishGnathiids per fish

Figure 8.9

Cleaner ﬁsh really do clean their clients. The

mean number of gnathiid parasites per client,

Hemigymnus melapterus, at ﬁve reefs, from

three of which cleaners, Labroides dimidiatus,

were experimentally removed. (a) In a long-term

experiment, clients without cleaners had more

parasites after 12 days (F = 17.6, P = 0.02).

(b) In a short-term experiment, clients without

cleaners did not have signiﬁcantly more parasites

at dawn after 12 hours (F = 1.8, P = 0.21),

presumably because cleaners do not feed at night.

further 12 hours of daylight (F = 11.6, P = 0.04).

Bars are standard errors.

AFTER GRUTTER, 1999

(a) (b)

ant–plant mutualisms...

The idea that there are mutualistic, ‘protective’ relationships between plants

and ants was put forward by Belt (1874) after observing the behavior of aggressive

ants on species of Acacia with swollen thorns in Central America. For example,

the Bull’s horn acacia (Acacia cornigera) bears hollow thorns that are used by

its associated ant, Pseudomyrmex ferruginea, as nesting sites (Figure 8.10b); its

Figure 8.10

Structures of the Bull’s horn acacia

(Acacia cornigera) that attract its ant

mutualist. (a) Protein-rich Beltian bodies at

the tips of the leaﬂets. (b) Hollow thorns

used by the ants as nesting sites.

(a) © MICHAEL FOGDEN, OXFORD SCIENTIFIC FILMS IHY360FOM00201; (b) © C. P. HICKMAN, VISUALS UNLIMITED

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leaves have protein-rich ‘Beltian bodies’ at their tips (Figure 8.10a) which the ants

collect and use for food; and it has sugar-secreting nectaries on its vegetative parts

that also attract the ants. The ants, for their part, protect these small trees from

competitors by actively snipping off shoots of other species and also protect the

plant from herbivores – even large (vertebrate) herbivores may be deterred.

In fact, ant–plant mutualisms appear to have evolved many times (even repeatedly

in the same family of plants); and nectaries are present on the vegetative parts

of plants of at least 39 families and in many communities throughout the world.

Their precise role is not easy to establish. They clearly attract ants, sometimes in

vast numbers, but carefully designed and controlled experiments are necessary to

show that the plants themselves beneﬁt, such as a study of the Amazonian canopy

tree Tachigali myrmecophila, which harbors the stinging ant Pseudomyrmex

concolor in specialized hollowed-out structures (Figure 8.11). The ants were

removed from selected plants. These then bore 4.3 times as many phytophagous

insects as control plants and suffered much greater herbivory, such that leaves

on plants that carried a population of ants lived more than twice as long as those

on unoccupied plants and nearly 1.8 times as long as those on plants from which

ants had been deliberately removed.

8.4.2 The culture of crops or livestock

At least in terms of geographic extent, some of the most dramatic mutualisms are

those of human agriculture. The numbers of individual plants of wheat, barley,

oats, corn and rice, and the areas these crops occupy, vastly exceed what would

have been present if they had not been brought into cultivation. The increase

in the human population since the time of hunter–gatherers is some measure of

the reciprocal advantage to Homo sapiens. Even without doing the experiment,

we can easily imagine the effect the extinction of humans would have on the

world population of rice plants or the effect of the extinction of rice plants on the

Part III Individuals, Populations, Communities and Ecosystems

270

Bottom leaves

Leaf longevity (months)

100

(b)

Control

(20)

Unoccupied

(17)

Experimental

(22)

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SNJMMJSNJ

1988 19901989

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SNJMMJSNJ

Treatments

Figure 8.11

(a) The intensity of leaf herbivory (based on the cumulative proportion of leaf area removed) on plants of Tachigali myrmecophila naturally occupied

by the ant Pseudomyrmex concolor (, n = 22) and on plants from which the ants had been experimentally removed ( , n = 23). Bottom leaves

were those present at the start of the experiment and top leaves were those emerging subsequently. (b) The longevity of leaves on plants of T.

myrmecophila occupied by P. concolor (control) and from which ants were experimentally removed or from which ants were naturally absent.

Error bars ± SE.

AFTER FONSECA, 1994

. . . but do the plants beneﬁt?

human agriculture

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population of humans. Similar comments apply to the domestication of cattle,

sheep and other mammals.

Similar ‘farming’ mutualisms have developed in termite and especially ant

societies, where the farmers may protect individuals they exploit from competitors

and predators and may even move or tend them. Ants, for example, farm many

species of aphids (homopterans) in return for sugar-rich secretions of honeydew.

The ‘ﬂocks’ of aphids beneﬁt through suffering lower mortality rates caused

by predators, showing increased feeding and excretion rates, and forming larger

colonies; but it would be wrong to imagine that this is a cosy relationship with

nothing but beneﬁts on both sides: the aphids are being manipulated – is there

a cost to be entered on the other side of the balance sheet? This question has

been addressed for colonies of the aphid Tuberculatus quercicola attended by the

red wood ant Formica yessensis on the island of Hokkaido, northern Japan

(Figure 8.12). As expected, in the presence of predators, aphid colonies survived

signiﬁcantly longer when attended by ants than when ants were excluded by

smearing ant repellent at the base of the oak trees on which the aphids lived

(Figure 8.12a). However, there were also costs for the aphids: in an environment

from which predators were excluded, and the effects of ant attendance on aphids

could thus be viewed in isolation, ant-attended aphids grew less well and were less

fecund than those where ants as well as predators were excluded (Figure 8.12b).

8.4.3 The dispersal of seeds and pollen

Very many plant species use animals to disperse their seeds and pollen. About

10% of all ﬂowering plants possess seeds or fruits that bear hooks, barbs or glues

that become attached to the hairs, bristles or feathers of any animal that comes

into contact with them. They are frequently an irritation to the animal, which

often cleans itself and removes them if it can, but usually after carrying them some

distance. In these cases the beneﬁt is to the plant (which has invested resources

in attachment mechanisms) and there is no reward to the animal.

Quite different are the true mutualisms between higher plants and the birds

and other animals that feed on ﬂeshy fruits and disperse the seeds. Of course,

for the relationship to be mutualistic, it is essential that the animal digests only

Chapter 8 Evolutionary ecology

271

Survival rate

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1002468

Days after the start of experiments

14 18 30 1 1 1122 2222 26

Ant attended

Ant excluded

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Average hind femur

length (mm)

Average number of embryos

AFTER YAO ET AL., 2000

Figure 8.12

(a) Ant-excluded colonies of the aphid Tuberculatus quercicola were more likely to become extinct than those attended by ants (χ

= 15.9,

P < 0.0001). (b) But in the absence of predators (experimentally removed), ant-excluded colonies performed better than those attended by ants.

Shown are averages for aphid body size (hind femur length; F = 6.75, P = 0.013) and numbers of embryos (F = 7.25, P = 0.010), ± SE, for

two seasons (1: July 23 to August 11, 1998; 2: August 12 to August 31, 1998). Maroon circles, predator-free and ant-excluded treatment;

black circles, predator-free and ant-attended treatment.

aphids farmed by ants:

do they pay a price?

seed dispersal

fruits

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the ﬂeshy fruit and not the seeds, which must remain viable when regurgitated

or defecated. Thick strong defenses that protect plant embryos are usually part

of the price paid by the plant for dispersal by fruit-eaters.

Many different kinds of animals have entered into pollination liaisons with

ﬂowering plants, including humming-birds, bats and even small rodents and

marsupials (Figure 8.13). Most animal-pollinated ﬂowers offer nectar, pollen or

Part III Individuals, Populations, Communities and Ecosystems

272

(a)

(b)

pollination

Figure 8.13

Pollinators. (a) Honeybee (Apis mellifera) on raspberry

ﬂowers. (b) Cape sugarbird (Promerops cafer) feeding

on Protea eximia.

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both as a reward to their visitors. Floral nectar seems to have no value to the

plant other than as an attractant to animals and it has a cost to the plant, because

the nectar carbohydrates might have been used in growth or some other activity.

Presumably, the evolution of specialized ﬂowers and the involvement of animal

pollinators have been favored because an animal may be able to recognize and

discriminate between different ﬂowers and so move pollen between different

ﬂowers of the same species but not to ﬂowers of other species. Passive transfer of

pollen, for example by wind or water, does not discriminate in this way and is

therefore much more wasteful. On the other hand, where the vectors and ﬂowers

are highly specialized, as is the case in many orchids, virtually no pollen is wasted

even on the ﬂowers of other species.

The pollinators par excellence are, without doubt, the insects. Pollen is a

nutritionally-rich food resource and in the simplest insect-pollinated ﬂowers,

pollen is offered in abundance and freely exposed to all and sundry. The plants

rely for pollination on the insects being less than wholly efﬁcient in their pollen

consumption, carrying their spilt food with them from plant to plant. In more

complex ﬂowers, nectar (a solution of sugars) is produced as an additional or

alternative reward. In the simplest of these, the nectaries are unprotected, but,

with increasing specialization, nectaries are enclosed in structures that restrict

access to the nectar to just a few visitor species. This range can be seen within the

family Ranunculaceae. In the simple ﬂower of Ranunculus ﬁcaria the nectaries

are exposed to all visitors, but in the more specialized ﬂower of R. bulbosus there

is a ﬂap over the nectary, and in Aquilegia the nectaries have developed into

long tubes and only visitors with long probosces (tongues) can reach the nectar.

Unprotected nectaries have the advantage of a ready supply of pollinators, but

because these pollinators are unspecialized they transfer much of the pollen to

the ﬂowers of other species. Protected nectaries have the advantage of efﬁcient

transfer of pollen by specialists to other ﬂowers of the same species, but are reliant

on there being sufﬁcient numbers of these specialists.

Charles Darwin (1859) recognized that a long nectary, as in Aquilegia, forced

a pollinating insect into close contact with the pollen at the nectary’s mouth.

Natural selection may then favor even longer nectaries, and as an evolutionary

reaction, the tongues of the pollinator would be selected for increasing length:

reciprocal coevolution. Nilsson (1988) deliberately shortened the nectary tubes

of the long-tubed orchid Platanthera and showed that the ﬂowers then produced

many fewer seeds – presumably because the pollinator was not forced into a

position that maximized the efﬁciency of pollination.

8.4.4 Mutualistic gut inhabitants

Most of the mutualisms discussed so far have depended on patterns of behavior,

where neither species lives entirely ‘within’ its partner. In many other mutualisms,

one of the partners is a unicellular eukaryote or bacterium that is integrated more

or less permanently into the body cavity or even the cells of its multicellular

partner. The microbiota occupying parts of various animals’ alimentary canals

are the best known extracellular symbionts.

The crucial role of microbes in the digestion of cellulose by vertebrate herbivores

has long been appreciated, but it now appears that the gastrointestinal tracts of

all vertebrates are populated by a mutualistic microbiota. Protozoa and fungi are

Chapter 8 Evolutionary ecology

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insect pollinators: from

generalists to ultraspecialists

the vertebrate gut

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usually present but the major contributors to these ‘fermentation’ processes are

bacteria. Their diversity is greatest in regions of the gut where the pH is relatively

neutral and food retention times relatively long. In small mammals (e.g. rodents,

rabbits, hares), the cecum is the main fermentation chamber, whereas in larger

non-ruminant mammals such as horses the colon is the main site. In ruminants,

like cattle and sheep, and in kangaroos and other marsupials, fermentation occurs

in specialized stomachs (see Figure 3.24).

The basis of the mutualism is straightforward. The microbes receive a steady

ﬂow of substrates for growth in the form of food that has been eaten, chewed

and partly homogenized. They live within a chamber in which the pH and, in

endotherms, temperature are regulated and anaerobic conditions are maintained.

The vertebrate hosts, especially the herbivores, receive nutrition from food that

they would otherwise ﬁnd, literally, indigestible. The bacteria produce short-chain

fatty acids (SCFAs) by fermentation of the host’s dietary cellulose and starches

and of the endogenous carbohydrates contained in host mucus and sloughed

epithelial cells. SCFAs are often a major source of energy for the host: for example,

they provide more than 60% of the maintenance energy requirements for cattle

and 29–79% of those for sheep (Stevens & Hume, 1998). The microbes also con-

vert nitrogenous compounds (amino acids that escape absorption in the midgut,

urea that would otherwise be excreted by the host, mucus and sloughed cells)

into ammonia and microbial protein, conserving nitrogen and water; and they

synthesize B vitamins. The microbial protein is useful to the host if it can be

digested – in the intestine by foregut fermenters and following coprophagy (eating

their own feces) in hindgut fermenters – but ammonia is usually not useful and

may even be toxic to the host.

8.4.5 Mycorrhizas

Most higher plants do not have roots, they have mycorrhizas – intimate mutualisms

between fungi and root tissue. Plants of only a few families, such as the Cruciferae,

are exceptions. Broadly, the fungal networks in mycorrhizas capture nutrients from

the soil, which they transport to the plants in exchange for carbon. Many plant

species can live without their mycorrhizal fungi in soils where neither nutrients

nor water are ever limiting, but in the harsh world of natural plant communities,

the symbioses, if not strictly obligate, are nonetheless ‘ecologically obligate’: that

is, necessary if the individuals are to survive in nature (Buscot et al., 2000).

Generally, three major types of mycorrhiza are recognized. Arbuscular

mycorrhizas are found in about two-thirds of all plant species, including most

non-woody species and tropical trees. Ectomycorrhizal fungi form symbioses with

many trees and shrubs, dominating boreal and temperate forests and also some

tropical rain forests. Finally, ericoid mycorrhizas are found in the dominant plant

species of heathland.

In ectomycorrhizas (ECMs), infected roots are usually concentrated in the

litter layer of the soil. Fungi form a sheath of varying thickness around the roots.

From there, hyphae radiate into the litter layer, extracting nutrients and water

and also producing large fruiting bodies that release enormous numbers of

wind-borne spores. The fungal mycelium also extends inward from the sheath,

penetrating between the cells of the root cortex to give intimate cell-to-cell con-

tact with the host and establishing an interface with a large surface area for the

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ectomycorrhizas

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exchange of the products of photosynthesis, soil water and nutrients between

the host plant and its fungal partner.

The ECM fungi are effective in extracting the sparse and patchy supplies

of phosphorus and especially nitrogen from the forest litter layer. Carbon ﬂows

from the plant to the fungus, very largely in the form of simple hexose sugars:

glucose and fructose. Fungal consumption of these may represent up to 30% of

the plants’ net rate of photosynthate production. The plants, though, are often

nitrogen-limited, since in forest litter there are low rates of nitrogen mineraliza-

tion (conversion from organic to inorganic forms), and inorganic nitrogen is itself

mostly available as ammonia. It is therefore crucial for forest trees that ECM

fungi can access organic nitrogen directly through enzymic degradation, and

utilize ammonium as a preferred source of inorganic nitrogen. Nonetheless, the

idea that this relationship between the fungi and their host plants is mutually

exploitative rather than ‘cosy’ is emphasized by its responsiveness to changing

circumstances. ECM growth is directly related to rate of ﬂow of hexose sugars

from the plant. But when the direct availability of nitrate to the plants is high,

either naturally or through artiﬁcial supplementation, plant metabolism is directed

away from hexose production (and export) and towards amino acid synthesis.

As a result the ECM degrades: the plants seem to support just as much ECM as

they appear to need.

Arbuscular mycorrhizas (AMs) do not form a sheath but penetrate within

the roots of the host. Roots become infected from mycelium present in the soil

or from germ tubes that develop from asexual spores, which are very large and

produced in small numbers: a striking contrast with the ECM fungi. Initially, the

fungus grows between host cells but then enters them and forms a ﬁnely branched

intracellular ‘arbuscule’.

There has been a tendency to emphasize facilitation of the uptake of phosphorus

as the main beneﬁt to plants from AM symbioses (phosphorus is a highly immobile

element in the soil, and is therefore frequently limiting to plant growth), but the

truth appears to be more complex than this, with beneﬁts demonstrated, too, in

nitrogen uptake, pathogen and herbivore protection, and resistance to toxic metals

(Newsham et al., 1995). Certainly, there are cases where the inﬂow of phosphorus

is strongly related to the degree of colonization of roots by AM fungi. This has

been shown for the bluebell, Hyacinthoides non-scripta, as colonization pro-

gresses during its phase of subterranean growth from August to February through

to its above-ground photosynthetic phase thereafter (Figure 8.14a). Indeed, blue-

bells cultured without AM fungi are unable to take up phosphorus through their

poorly branched system of roots (Merryweather & Fitter, 1995).

On the other hand, a set of experiments examined the growth of the annual

grass Vulpia ciliata ssp. ambigua (Figure 8.14b) in which seedlings of Vulpia were

grown with an AM fungus (Glomus sp.), with the pathogenic fungus Fusarium

oxysporum, with both, and with neither. Growth was not enhanced by Glomus

alone, but growth was harmed by Fusarium in the absence of Glomus. When

both were present, growth returned to normal levels. Clearly, the mycorrhiza did

not beneﬁt the phosphorus economy of the Vulpia, but it did protect it from the

harmful effects of the pathogen.

The key difference appears to be that Vulpia, unlike the bluebell, has a highly

branched system of roots (Newsham et al., 1995). Plants with ﬁnely branched roots

have little need for supplementary phosphorus capture, but development of that

Chapter 8 Evolutionary ecology

275

arbuscular mycorrhizas

a range of beneﬁts?

it depends on the species

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same root architecture provides multiple points of entry for plant pathogens. In

such cases AM symbioses are therefore likely to have evolved with an emphasis on

plant protection. By contrast, root systems with few lateral and actively growing

meristems are relatively invulnerable to pathogen attack, but these root systems

are poor foragers for phosphorus. Here, AM symbioses are likely to have evolved

with an emphasis on phosphorus capture.

8.4.6 Fixation of atmospheric nitrogen in

mutualistic plants

The inability of most plants and animals to ﬁx atmospheric nitrogen is one of

the great puzzles in the process of evolution, since nitrogen is in limiting supply

in many habitats. However, the ability to ﬁx nitrogen is widely though irregu-

larly distributed amongst both the eubacteria (‘true’ bacteria) and the archaea

(Archaebacteria), and many of these have been caught up in tight mutualisms

with distinct groups of eukaryotes. The best known, because of the huge agri-

cultural importance of legume crops, are the rhizobia, which ﬁx nitrogen in

the root nodules of most leguminous plants and just one non-legume, Parasponia

(a member of the family Ulmaceae, the elms).

The establishment of the liaison between rhizobia and legume plants proceeds

by a series of reciprocating steps. The bacteria occur in a free-living state in the

soil and are stimulated to multiply by root exudates and cells that have been

sloughed from roots as they develop. In a typical case, a bacterial colony develops

Part III Individuals, Populations, Communities and Ecosystems

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Sept 1

–1

2(a)

–2

Dec 1 Mar 1 Jun 1

(b)

–Fus

–Glm

200

300

100

–Fus +Fus

–Glm

+Fus

+GlmDate +Glm

Mean root length (cm)

P inflow (pmol m

–1

) ( )

Percentage root length colonized by AM fungi ( )

Figure 8.14

(a) Curves ﬁtted to rates of phosphorus inﬂow (dashed line, left axis) and root colonization by arbuscular mycorrhiza (AM) fungi (solid line, right

axis) in the bluebell, Hyacinthoides non-scripta, over a single growing season. Phosphorus uptake appears to be strongly linked to root colonization

by the fungi. (b) The effects of a factorial combination of Fusarium oxysporum (Fus, a pathogenic fungus) and an AM fungus, Glomus sp. (Glm) on

growth (root length) of Vulpia plants. Values are means of 16 replicates per treatment; bars are standard errors; the asterisk signiﬁes a signiﬁcant

difference at P < 0.05 in a Fisher’s pairwise comparison. In this case, the beneﬁt provided by AM fungi seems not to be an improvement in nutrient

uptake but protection against the pathogen.

(A) AFTER MERRYWEATHER & FITTER, 1995; NEWSHAM ET AL., 1995; (B) AFTER NEWSHAM ET AL., 1994, 1995

mutualisms of rhizobia and

leguminous plants:

several steps to a liaison

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on the root hair, which then begins to curl and is penetrated by the bacteria. The

host responds by laying down a wall that encloses the bacteria and forms an

‘infection thread’, which grows within the host root cortex, and within which

the rhizobia proliferate. Rhizobia in the infection thread cannot ﬁx nitrogen, but

some are released into host cells in a developing ‘nodule’, where, surrounded

by a host-derived peribacteroid membrane, they differentiate into ‘bacteroids’

that can ﬁx nitrogen. Meanwhile, a special vascular system develops in the host,

supplying the products of photosynthesis to the nodule tissue and carrying away

ﬁxed-nitrogen compounds to other parts of the plant.

The costs and beneﬁts of this mutualism need to be considered carefully.

From the plant’s point of view, we need to compare the energetic costs of

alternative processes by which supplies of ﬁxed nitrogen might be obtained.

The route for most plants is direct from the soil as nitrate or ammonium ions.

The metabolically cheapest route is the use of ammonium ions, but in most

soils ammonium ions are rapidly converted to nitrates by microbial activity

(nitriﬁcation). The energetic cost of reducing nitrate from the soil to ammonia

is about 12 mol of adenosine triphosphate (ATP, the cell’s energy currency) per

mole of ammonia formed. The mutualistic process (including the maintenance

costs of the bacteroids) is energetically slightly more expensive to the plant: about

13.5 mol of ATP. However, we must also add the costs of forming and main-

taining the nodules, which may be about 12% of the plant’s total photosynthetic

output. It is this that makes nitrogen ﬁxation energetically inefﬁcient. Energy,

though, may be much more readily available for green plants than nitrogen. A

rare and valuable commodity (ﬁxed nitrogen) bought with a cheap currency

(energy) may be no bad bargain. On the other hand, when a nodulated legume

is provided with nitrates (i.e. when nitrate is not a rare commodity) nitrogen

ﬁxation declines rapidly.

On the other hand, the mutualisms of rhizobia and legumes (and other nitrogen-

ﬁxing mutualisms) must not be seen as isolated interactions between bacteria

and their own host plants. In nature, legumes normally form mixed stands in

association with non-legumes. These are potential competitors with the legumes

for ﬁxed nitrogen (nitrates or ammonium ions in the soil). The nodulated legume

sidesteps this competition by its access to its unique source of nitrogen. It is in this

ecological context that nitrogen-ﬁxing mutualisms gain their main advantage.

Where nitrogen is plentiful, however, the energetic costs of nitrogen ﬁxation

often put the plants at a competitive disadvantage.

Figure 8.15, for example, shows the results of a classic experiment in which

soybeans (Glycine soja, a legume) were grown in mixtures with Paspalum, a

grass. The mixtures either received mineral nitrogen, or were inoculated with

Rhizobium, or received both. The experiment was designed as a ‘replacement

series’, which allows us to compare the growth of pure populations of the grass

and legume with their performances in the presence of each other. In the pure

stands of soybean, yield was increased very substantially either by inoculation

with Rhizobium, or by application of fertilizer nitrogen, or by receiving both.

The legumes can use either source of nitrogen as a substitute for the other. The

grass, however, responded only to the fertilizer. Hence, when the species com-

peted in the presence of Rhizobium alone, the legume contributed far more to the

overall yield than did the grass: over a succession of generations, the legume

would have outcompeted the grass. When they competed in soils supplemented

Chapter 8 Evolutionary ecology

277

costs and beneﬁts of rhizobial

mutualisms

interspeciﬁc competition:

a classic ‘replacement series’

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with fertilizer nitrogen, however, whether or not Rhizobium was also present, it

was the grass that made the major contribution: long term, it would have out-

competed the legume.

Quite clearly, then, it is in environments deﬁcient in nitrogen that nodulated

legumes have a great advantage over other species. But their activity raises the

level of ﬁxed nitrogen in the environment. After death, legumes augment the level

of soil nitrogen on a very local scale with a 6–12-month delay as they decompose.

Thus, their advantage is lost – they have improved the environment of their

competitors, and the growth of associated grasses will be favored in these local

patches. Hence, organisms that can ﬁx atmospheric nitrogen can be thought of as

locally suicidal. This is one reason why it is very difﬁcult to grow repeated crops

of pure legumes in agricultural practice without aggressive grass weeds invading

the nitrogen-enriched environment. It may also explain why leguminous herbs or

trees usually fail to form dominant stands in nature.

Grazing animals, on the other hand, continually remove grass foliage, and the

nitrogen status of a grass patch may again decline to a level at which the legume

is once more at a competitive advantage. In a stoloniferous legume, such as white

clover, the plant is continually ‘wandering’ through the sward, leaving behind it

local grass-dominated patches, whilst invading and enriching with nitrogen new

patches where the nitrogen status has become low. The symbiotic legume in such

a community not only drives its nitrogen economy but also some of the cycles that

occur within its patchwork (Cain et al., 1995).

We end this section, then, on a theme that has recurred repeatedly. To under-

stand the ecology of mutualistic pairs, we must look beyond those species to the

wider community of which they are part.

Part III Individuals, Populations, Communities and Ecosystems

278

–R –N +R –N –R +N

Dry weight per container (g)

+R +N

Figure 8.15

The growth of soybeans (Glycine soja, G, ) and a grass (Paspalum, P, ) grown alone and in mixtures

with and without nitrogen fertilizer (N) and with and without inoculation with nitrogen-ﬁxing Rhizobium (R).

The plants were grown in pots containing 0–4 plants of the grass together with 0–8 plants of Glycine.

Thus, moving left to right on the horizontal axis, the treatments are zero Paspalum (0P) and 8 Glycine

(8G), 1P with 6G, 2P with 4G, 3P with 2G and, ﬁnally, 4P with 0G. The vertical scale on each ﬁgure shows

the mass of plants of the two species in each container. −R −N, no Rhizobium and no fertilizer; +R −N,

inoculated with Rhizobium but no fertilizer; −R +N, no Rhizobium but nitrate fertilizer was applied; +R +N,

inoculated with Rhizobium and nitrate fertilizer was supplied. When the two species competed in the

presence of nitrogen-ﬁxing Rhizobium and without fertilizer, the soybeans (with their mutualistic

relationship to Rhizobium) performed best, but in the presence of nitrogen fertilizer (with or without the

Rhizobium) the grass outperformed the soybeans.

AFTER DE WIT ET AL., 1966

the shifting balance between

nitrogen-ﬁxers and non-ﬁxers

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