Effect of species 2 on species

Fig. 9.1. The continuum of species interactions (redrawn from Bronstein, 1994a). If we use the 'cat and mouse' example, the cat (species 1) has a negative effect on the mouse (species 2), and the mouse has a positive effect on the cat.

Herbivores include mammals such as grazing deer and zebra, sap-sucking insects, seedling-eating molluscs, root-feeding larvae, leaf-eating grasshoppers, and seed-eating mice and beetles. Plant herbivores range from specialists (typically invertebrates), that eat only one or a few types of food, to generalists (typically vertebrates) that are unselective feeders (Crawley, 1989). Some herbivores can be both specialist and generalist because they change their feeding behaviour depending on the relative density of the plants.

Herbivory is usually non-lethal unless all of the plant or an essential tissue (e.g. all roots) is eaten, or if the plant is already stressed. If a plant is not able to compensate for the loss of tissue, such as when a tree is girdled by a deer, it will die. The more immediate effects of herbivory are the loss of photosynthetic tissue, stored nutrients and meristems (i.e. sites of active growth) (Noy Meir, 1993). These losses may lessen a plant's ability to photosynthesize, absorb nutrients and water, and grow. There are, however, mechanisms that allow plants to compensate for herbivory. Plants respond by mobilizing stored nutrients, increasing their rate of photosynthesis, stimulating dormant meristems, or growing more roots or shoots (depending on what was eaten) (Crawley, 1992) (Box 9.1). The net effect of long-term herbivory will depend on the age of the foliage, the distribution of damage on the plant, and the stage of development and seasonal timing (Crawley, 1992). For example, the loss of young leaves from herbivores may have more long-term repercussions than the loss of older leaves. No plant species is immune to herbivory completely, but many have evolved ways to defend or compensate for it.

Plant defences and compensation to herbivory

Plants cannot run away from potential herbivores, but they do have ways to avoid being consumed. The two types of defences

Box 9.1. Mechanisms by which plants respond to herbivory (adapted from Crawley, 1992).

• Increased light intensity for surviving leaf area

• Increase in the rate of carbon fixation at a given light intensity

• Improved water and nutrient availability to the surviving leaf tissue

• Delayed senescence (plus rejuvenation) of leaves

• Increased duration of the growing period

• Redistribution of the photosynthate to the production of new leaves and away from roots, flowers, fruits or storage

• Reduced rate of flower abortion

• Production of new shoots from dormant buds or newly produced epicormic buds

• Ungrazable reserve (e.g. storage in roots and woody stems)

• Not regrowing while the herbivore is still around

Table 9.1. Types of herbivore avoidance and tolerance strategies used by plants to defend against herbivory.

Defence

Type

Example

Explanation

Avoidance Structural Hairs, spines, trichomes

Digestibility reducers

Protective coating Chemical Chemical defences

Phenological Rare or ephemeral

Early growth or reproduction Tolerance Compensate Increase net photosynthetic rate

High relative growth rates Increase branching or tillering

High carbon storage

Carbon re-allocation

Make it harder to consume tissue Cellulose, lignin, cutins, tannins effect digestion by blocking digestive enzymes Shells of fruits make them difficult to eat

Reduce the palatability of plants or makes them poisonous Makes plants hard to find when herbivores are active Plant escapes later emerging herbivores

Plants produce more above-ground biomass after being grazed than non-grazed individuals

After apical dominance is released

Pre-existing stores of carbons in roots can be re-allocated for above-ground production Can quickly move carbon from roots to shoots are direct (i.e. avoidance and tolerance) and indirect (i.e. defend themselves by recruiting bodyguards to protect them from herbivores).

Avoidance

Avoidance defences reduce the chance that a plant will be eaten or reduce the performance of the herbivore. Plants have three strategies to avoid herbivory: structural, phe-nological and chemical (Table 9.1). Structural and phenological defences are 'constituent' traits present in the plant whether or not a herbivore is present. Constituent defences deter a herbivore from damaging the plant. Chemical defences, however, may not exist until induced by herbivory. These chemicals can inhibit digestion, deter feeding or intoxicate the herbivore, thereby reducing herbivore damage. However, some herbivores adapt and can detoxify chemical defences. For example, saliva from the corn earworm caterpillar (Helicoverpa zea) suppresses the induction of the toxin nicotine in tobacco (Nicotiana tabacum) (Musser et al., 2002). Herbivores may even use the plant chemicals to their own benefit. The classic example of this is the monarch butterfly (Danaus plexippus) and common milkweed (Asclepias syriaca) association. Milkweed produces a glycoside that is toxic to the heart and circulatory system in most herbivores. Monarch larvae, however, are able to consume milkweed leaves, and the glyco-side, in turn, makes them more unpalatable to their predators.

Tolerance

Tolerance is the ability to minimize damage from herbivory (Belsky et al., 1993; Strauss and Agrawal, 1999). While tolerance may be an alternative to avoidance under certain types of herbivory, both tolerance and avoidance may be used simultaneously. For example, if slugs start eating ginger (Asarum caudatum), its palatability decreases (avoidance) and its growth and seed production decreases (tolerance) (Cates, 1975).

The degree to which a plant tolerates herbivory is called 'compensation'. There are several mechanisms used by plants to compensate and increase their tolerance to herbivory or other types of damage (Table 9.1) (Belsky et al, 1993). Regardless of the mechanism, however, the success of any compensation is related to the cost the individual incurs because it has to allocate resources away from growth or reproduction. Ultimately, this re-allocation of resources can reduce the fitness of an individual; for example, jimsonweed (Datura stramonium) experienced 15-25% reductions in fitness after defoliation (Foroni and Nunez-Farfan, 2000). As long as the reduction in fitness does not lead to complete extinction of a genotype, tolerance is a good strategy.

Tolerance responses vary with the type of herbivory and the constraints on the plant, i.e. what is morphologically or physiologically possible? For example, cotton (Glossypium hirsutum) responds to phloem-sucking aphids by decreasing axillary branching; however, if buds are eaten, branching increases (Sandras, 1996). The weedy leafy spurge (Euphorbia esula) seems to be more constrained as it only tolerates defoliation by allocating more resources to its large root system that, after herbivores leave, will produce more shoots (Olson and Wallander, 1999). The internal mechanisms that allow a plant to respond to herbivory are moderated by the timing of herbivory, nutrient, light and water availability, and the presence of plant competitors (Strauss and Agrawal, 1999).

A special type of tolerance is 'over-compensation', as found in weeds such as purple loosestrife (Venecz and Aarssen, 1998). This occurs when herbivory actually benefits plants and increases fitness (Aarssen, 1995). The mechanism is relatively simple: if the apical (shoot) meristem is eaten, the lateral meristems (on the branch-

es) are signalled chemically to grow. As a result, the extra branches and all their leaves may allow the damaged plant to increase photosynthesis and carbohydrate production relative to undamaged plants. If this extra production allows for more sexual or asexual success, then fitness increases (Venecz and Aarssen, 1998; Agrawal, 2000). Over-compensation may only occur under certain conditions such as low competition, and optimum light and moisture (Strauss and Agrawal, 1999).

Indirect plant defences

Indirect plant defences mean that an individual uses another organism to defend itself against herbivory. For example, a plant may be protected when it grows near an unpalatable species. The unpalatable species can mask features, such as scent, that otherwise would attract herbivores (Price et al., 1980). Some plants decrease herbivore damage by recruiting 'bodyguards'. This means an individual provides pollen, nectar, habitat or other rewards that increases the foraging effectiveness of species that harm herbivores (Price et al., 1980; Sabelis et al., 1999; Elliot et al., 2000). In some cases, bodyguards are recruited only as an induced defence, e.g. predatory mites are attracted by chemicals released when herbivorous spider mites damage leaves. It appears that few weeds use bodyguards, though weeds can have the general characteristic of induced defences (e.g. Jennings et al., 2000).

Seed predation: a special case of herbivory

When herbivores eat seeds, it is called 'seed predation'. The term 'predation' is used because the whole individual (as a seed) is consumed just as with the consumption of a whole animal. While seed predation can be severe, the rates are variable because of interactions among plants, herbivores and the environment. It is also difficult to detect the effect of seed predation on population dynamics (Crawley, 1992; Cromar et al., 1999).

Table 9.2. The effect of pre-dispersal flower and seed predation, post-dispersal seed predation and seedling competition with established vegetation (switchgrass - Paricum virgatum) on the recruitment of Platte thistle seedlings at Arapaho Prairie, Nebraska (adapted from Louda et al., 1990).

(a) Pre-dispersal flower and seed predation

With insects, water-spray control

Without insects, insecticide spray

Stage

(number per plant)

(number per plant)

Number seeds initiated

577

716

Number viable seeds

41

105

Seedlings established

0.5

3.0

Adults matured

0.07

0.37

(b) Post-dispersal seed predation

With herbivores, no cage

Without herbivores, with cage

Habitat type

(number per 30x30cm plot)

(number per 30x30cm plot)

Blowout (open)

0.01

0.02

Grass

2.0

0.01

(c) Seedling survival

Time after transplant

No competition (% survival)

In competition (% survival)

9 weeks

43

5

1 year

19

5

2 years

10

0

Seed predation can occur while seeds are still on the plant ('pre-dispersal') or after they have abscised ('post-dispersal'). Pre-dispersal seed predators are usually invertebrates (mainly insects) with a narrow host range or specialized feeding habits. There is a wider variety of post-dispersal seed predators including vertebrates (birds or rodents), insects (ants and carabid beetles) and molluscs (snails and slugs) (Crawley, 1989; Blaney and Kotanen, 2001).

Louda et al. (1990) compared the effect of pre-dispersal flower and seed predation, post-dispersal seed predation, and seedling competition with established vegetation on the recruitment of Platte thistle (Cirsium canescens) seedlings (Table 9.2). Pre-dispersal predation by insects reduced seed production and seedling establishment. Post-dispersal seed predation had a more pronounced effect on seedling establishment in exposed open sites than in protected grassy sites. Competition of Platte thistle seedlings with grasses greatly reduced seedling survival, with no seedlings surviving after 2 years when planted in switchgrass (Panicum virgatum). The authors concluded that competition confined the distribution of Platte thistle to open areas, while predation limited its abundance.

Some species have defences against seed predators. For example, velvetleaf seeds that are small and have a hard seed coat can often survive intact after being ingested and defaecated. In this case, the seed predator actually serves to disperse seeds. Giant Parramatta grass (Sporobolus indicus var. major), a major weed of pastures and disturbed areas in Australia, can pass through the gut of cattle (Andrews, 1995). Therefore, to prevent invasion of the weed into uninfested fields, cattle must be isolated for 7 days after grazing in an infested field. Other seeds are unpalatable or are protected by a fruit that is difficult to consume (e.g. cocklebur).

Producing large seed crops at irregular intervals (masting) is a further method of defence against seed predators, because it reduces the chances that all seeds will be destroyed by seed predators. Usually, one to a few years of heavy seed production (mast years) are followed by a period of low seed production. During mast years, the number of seeds consumed by predators is high but the probability of any one seed escaping predation is also high; therefore new seedlings are produced through the sheer quantity of seeds available (Silvertown, 1980). This appears to be a more effective strategy against invertebrate than vertebrate predators because vertebrates are more likely to migrate towards areas of mast seeding. Vertebrates also have other food sources to support them during non-mast years (Crawley, 1989). Weeds that mast include Norway maple (Acer plantanoides) and Monterey pine (Pinus radiata).

Effect of herbivory on populations

As in the case of testing for competition (Chapter 8), it is relatively simple to determine if herbivory will affect the performance of an individual plant, but less easy to determine if it leads to population or communitylevel effects. Nevertheless, herbivory can influence the distribution and abundance of populations. The effect will generally depend on the type of herbivore involved, the intensity and frequency of herbivory, the plant species, the type and age of tissue consumed, and the abiotic environment.

We have already presented the example of herbivores controlling the abundance and distribution of a native weed species, i.e. the Platte thistle. In contrast, when weedy exotics are introduced to a habitat, there may be few herbivores that consume them and, consequently, their population distribution and abundance may increase. This is termed 'herbivore release' because the plant species is released from the pressure of herbivory, e.g. garlic mustard (Alliaria petiolata). Consequently, one approach to managing weeds is introducing specialist herbivores (often insects) as 'biological control agents'. These herbivores may be exotics themselves but are found in the same area of origin as the weed. While weed species usually are not eradicated, even if the biological control agent consumes only a small proportion of biomass, it may be enough to alter the competitive balance between it and otherwise less-competitive native species.

The biological control of prickly pear cacti (Opuntia spp.), introduced from Mexico and the southern USA into Australia, exemplifies both successful biological control and the risks involved. The cactus moth borer (Cactoblastis cactorum) was introduced from Argentina as a biological control agent to help control prickly pear cacti in 1926. As a caterpillar, the cactus moth borer consumes the tissue and this introduces bacterial soft rot and other pathogens into the cactus. In 1925, the cactus covered 24 million hectares (Mha) of Australia, but by 1930, the cactus was under control. The cactus still survives in small populations that last only until they are detected by the moths. Recently, however, the cactus moth borer was accidentally introduced to eastern North America from Argentina. Unlike in Australia, prickly pear cacti are native to eastern North America and are not considered weeds in general. Eventually, the moth may spread to Mexico and southwestern North America, where it would find many more species of native cacti and cause serious damage (Cory and Myers, 2000). The cactus moth borer is a native part of the ecosystem in Argentina, a saviour in Australia and a serious pest in North America. This is why using herbivores as biological control agents must be tested carefully - it is not always clear whether the herbivore will do more harm than good and this varies from location to location, e.g. introducing beetles to control purple loosestrife (Blossey et al., 2001a,b).

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