Plant tolerance to herbivory

Damage can occur in almost any part of the plants, including the roots, stems, leaves, flowers and seeds (Strauss and Zergerl 2002).

Agricultural studies on tolerance, however, are mainly concerned with the compensatory effect on the plants' yield and not its fitness, since it is of economical interest to reduce crop losses due to herbivory by pests (Trumble 1993; Bardner and Fletcher 1974).

Many aspects of plant tolerance such as its geographic variation, its macroevolutionary implications and its coevolutionary effects on herbivores are still relatively unknown (Fornoni 2011).

An increase in photosynthetic rate in undamaged tissues is commonly cited as a mechanism for plants to achieve tolerance (Trumble et al. 1993; Strauss and Agrawal 1999).

Several different pathways may lead to increases in photosynthesis, including higher levels of the Rubisco enzyme and delays in leaf senescence (Stowe et al. 2000).

Studies have found branching after AMD to undercompensate, fully compensate and overcompensate for the damage received (Marquis 1996, Haukioja and Koricheva 2000, Wise and Abrahamson 2008).

The wide occurrence of overcompensation after AMD has also brought up a controversial idea that there may be a meristem relationship between plants and their herbivores (Belsky 1986; Agrawal 2000; Edwards 2009).

How plants respond to these phenological delays is likely a tolerance mechanism that will depend highly on their life history and other ecological factors such as, the abundance of pollinators at different times during the season (Tiffin 2000).

When these reproductive structures are not present, resources are allocated to other tissues, such as leaves and shoots as seen in juvenile Plantago lanceolata (Trumble et al. 1993; Barton 2008).

Although plant vasculature may play important roles in tolerance, it is not well studied due to the difficulties in identifying the flow of resources (Marquis 1996).

Tolerance is often presented as a reaction norm, where slopes larger than, equal to and less than zero reflect overcompensation, full compensation and undercompensation, respectively (Strauss and Agrawal 1999).

A majority of studies use simulated or manipulated herbivory, such as clipping leaves or herbivore exclusions, due to the difficulty in controlling damage levels under natural conditions (Tiffin and Inouye 2000).

Even if the plots are grown in natural settings, the methods of excluding or including herbivores, such as using cages or pesticides, may also affect plant tolerance (Tiffin and Inouye 2000).

Many studies have shown that using different measurements of fitness may give varying outcomes of tolerance (Strauss and Agrawal 1999; Suwa and Maherali 2008; Banta et al. 2010).

For this trade-off to exist, it requires that tolerance and resistance be redundant defense strategies with similar costs to the plant (Nunez-Farfan et al. 2007).

Models have shown that intermediate levels of resistance and tolerance are evolutionary stable as long as the benefits of having both traits are more than additive (Nunez-Farfan et al. 2007).

Although many studies find lower tolerance in seedlings, this is not always the case, as seen in juveniles of Plant ago lanceolata which can fully compensate for 50% defoliation (Barton 2008).

There is also the added complexity of shifts in herbivore communities as the plant develops and so may favor tolerance or resistance at different life stages (Barton and Koricheva 2010).

The major resources that affect plant growth and also tolerance are water, light, carbon dioxide and soil nutrients.

However, there are exceptions such as evidence of decreased tolerance in Madia sativa with increased water availability (Wise and Abrahamson 2007, Gonzales et al. 2008).

Meta-analyses by Hawkes and Sullivan (2001) and Wise and Abrahamson (2007, 2008a) found that the CCH and GRM were insufficient in predicting the diversity of plant tolerance to herbivory.

This is in contrast to traits that confer resistance, which are likely to affect herbivore fitness and lead to a co-evolutionary arms race (Stinchcombe 2002; Espinosa and Fornoni 2006).

One mechanism requires a genetic association between loci that confers resistance and tolerance either through tight linkage or pleiotropy (Stinchcombe 2002).

Assuming that investment in tolerance will reduce plant fecundity, infection by pathogens will decrease the number of uninfected hosts.

Such benefits include the release from apical dominance, inducing resistance traits to temporally separate herbivores, providing information of future attacks and pollination (Agrawal 2000).

Due to the predictability of attacks, these plants have evolved to overcompensate for the damage and produce the majority of their seeds after the initial bout of herbivory (Edwards 2009).

Another example involves endophytic fungi, such as Neophtodium, which parasitize plants and produce spores that destroy host inflorescences (Edwards 2009).

Tolerance may also be involved in the mutualism between the myremecophyte, Cordia nodosa, and its ant symbiont Allomerus octoarticulatus (Edwards and Yu, 2008).

Modern agriculture has focuses on using genetically modified crops which possess toxic compounds to reduce damage by pests (Nunez-Farfan et al. 2007).

However, the effectiveness of resistance traits may decrease as herbivores fungi counter adaptations to the toxic compound, especially since most farmers are reluctant to assign a proportion of their land to contain susceptible crops (Nunez-Farfan et al. 2007).