Plant tolerance to herbivory

Tolerance is the ability of plants to mitigate the negative fitness effects caused by herbivory. It is one of the general plant defense strategies against herbivores, the other being resistance, which is the ability of plants to prevent damage (Strauss and Agrawal 1999). Plant defense strategies play important roles in the survival of plants as they are fed upon by many different types of herbivores, especially insects, which may impose negative fitness effects (Strauss and Zangerl 2002). Damage can occur in almost any part of the plants, including the roots, stems, leaves, flowers and seeds (Strauss and Zergerl 2002). In response to herbivory, plants have evolved a wide variety of defense mechanisms and although relatively less studied than resistance strategies, tolerance traits play a major role in plant defense (Strauss and Zergerl 2002, Rosenthal and Kotanen 1995). Tolerance is the ability of plants to mitigate the negative fitness effects caused by herbivory. It is one of the general plant defense strategies against herbivores, the other being resistance, which is the ability of plants to prevent damage (Strauss and Agrawal 1999). Plant defense strategies play important roles in the survival of plants as they are fed upon by many different types of herbivores, especially insects, which may impose negative fitness effects (Strauss and Zangerl 2002). Damage can occur in almost any part of the plants, including the roots, stems, leaves, flowers and seeds (Strauss and Zergerl 2002). In response to herbivory, plants have evolved a wide variety of defense mechanisms and although relatively less studied than resistance strategies, tolerance traits play a major role in plant defense (Strauss and Zergerl 2002, Rosenthal and Kotanen 1995). Traits that confer tolerance are controlled genetically and therefore are heritable traits under selection (Strauss and Agrawal 1999). Many factors intrinsic to the plants, such as growth rate, storage capacity, photosynthetic rates and nutrient allocation and uptake, can affect the extent to which plants can tolerate damage (Rosenthal and Kotanen 1994). Extrinsic factors such as soil nutrition, carbon dioxide levels, light levels, water availability and competition also have an effect on tolerance (Rosenthal and Kotanen 1994). Studies of tolerance to herbivory has historically been the focus of agricultural scientists (Painter 1958; Bardner and Fletcher 1974). Tolerance was actually initially classified as a form of resistance (Painter 1958). 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). One surprising discovery made about plant tolerance was that plants can overcompensate for the damaged caused by herbivory, causing controversy whether herbivores and plants can actually form a mutualistic relationship (Belsky 1986). It was soon recognized that many factors involved in plants tolerance, such as photosynthetic rates and nutrient allocation, were also traits intrinsic to plant growth and so resource availability may play an important role (Hilbert et al. 1981; Maschinski and Whitham 1989). The growth rate model proposed by Hilbert et al. (1981) predicts plants have higher tolerance in environments that does not allow them to grow at maximum capacity, while the compensatory continuum hypothesis by Maschinski and Whitham (1989) predicts higher tolerance in resource rich environments. Although it was the latter that received higher acceptance, 20 years later, the limiting resource model was proposed to explain the lack of agreement between empirical data and existing models (Wise and Abrahamson 2007). Currently, the limiting resource model is able to explain much more of the empirical data on plant tolerance relative to either of the previous models (Wise and Abrahamson 2008a). It was only recently that the assumption that tolerance and resistance must be negatively associated has been rejected (Nunez-Farfan et al. 2007). The classical assumption that tolerance traits confer no negative fitness consequences on herbivores has also been questioned (Stinchcombe 2002). Further studies using techniques in quantitative genetics have also provided evidence that tolerance to herbivory is heritable (Fornoni 2011). Studies of plant tolerance have only received increased attention recently, unlike resistance traits which were much more heavily studied (Fornoni 2011). 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). Plants utilize many mechanisms to recover fitness from damage. Such traits include increased photosynthetic activity, compensatory growth, phenological changes, utilizing stored reserves, reallocating resources, increase in nutrients uptake, and plant architecture (Rosenthal and Kotanen 1994; Strauss and Agrawal 1999; Tiffin 2000). 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). This is possible since leaves often function at below their maximum capacity (Trumble et al. 1993). 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). However, detecting an increase in photosynthesis does not mean plants are tolerant to damage. The resources gained from these mechanisms can be used to increase resistance instead of tolerance, such as for the production secondary compounds in the plant (Tiffin 2000). Also, whether the increase in photosynthetic rate is able to compensate for the damage is still not well studied (Trumble et al. 1993; Stowe et al. 2000). Biomass regrowth following herbivory is often reported as an indicator of tolerance and plant response after apical meristem damage (AMD) is one of the most heavily studied mechanisms of tolerance (Tiffin 2000; Suwa and Maherali 2008; Wise and Abrahamson 2008). Meristems are sites of rapid cell divisions and so have higher nutrition than most other tissues on the plants . Damage to apical meristems of plants may release it from apical dominance, activating the growth of axillary meristems which increases branching (Trumble et al. 1993; Wise and Abrahamson 2008). 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 variation in the extent of growth following herbivory may depend on the number and distribution of meristems, the pattern in which they are activated and the number of new meristems (Stowe et al. 2000). The wide occurrence of overcompensation after AMD has also brought up a controversial idea that there may be a mutualistic relationship between plants and their herbivores (Belsky 1986; Agrawal 2000; Edwards 2009). As will be further discussed below, herbivores may actually be mutualists of plants, such as Ipomopsis aggregata, which overcompensate for herbivory (Edwards 2009). Although there are many examples showing biomass regrowth following herbivory, it has been criticized as a useful predictor of fitness since the resources used for regrowth may translate to fewer resources allocated to reproduction (Suwa and Maherali 2008). Studies have shown herbivory can cause delays in plant growth, flowering and fruit production (Tiffin 2000). 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). If the growing season is short, plants that are able to shorten the delay of seed production caused by herbivory are more tolerant than those that cannot shorten this phenological change (Tiffin 2000). These faster recovering plant will be selectively favored over those that cannot as they will pass on more of their offspring to the next generation. In longer growing seasons, however, there may be enough time for most plants to produce seeds before the season ends regardless of damage. In this case, plants that can shorten the phenological delay are not any more tolerant than those that cannot as all plants can reproduce before the season ends (Tiffin 2000).