187:, 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 meristem 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
35:, 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).
640:(Stinchcombe 2002). photosynthetic for either trait will then also affect the other. If there is a positive correlation between the two traits, then selection for increased tolerance will also increase resistance in the plants. If there is a negative correlation between the two traits then selection for increased tolerance will decrease resistance. How common this association exists, however, is uncertain as there are many studies which find no
737:
712:(late-seral) being replaced by species that occur in the middle of ecological succession (mid-seral) after high herbivory is due to differences in tolerance between them (Anderson and Briske 1995; Off and Ritchie 1998). However, tolerance between these two groups of species do not always differ and other factors, such as selective herbivory on late-seral species, may contribute to these observations (Anderson and Briske 1995).
704:
competitive but intolerant plant species, thereby increasing diversity (Mariotte et al. 2013). Pejman et al. (2009) found support for this idea in an experimental study on grassland species. In low resource environments, highly competitive (dominant) plants species had lower tolerance than the less competitive (subordinate) species. They also found that the addition of
586:, are growing below their maximum growth rate and so may have a higher capacity for regrowth after receiving damage (Hilbert et al. 1981). In contrast, plants in relatively benign conditions are growing near their maximum growth rate. These plants are less able to recover from damage since they are already near their innate maximum growth rate (Hilbert et al. 1981).
483:
Nunez-Farfan et al. 2007; Muola et al. 2010). 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). Tolerance and resistance may not be redundant strategies since tolerance could be necessary for damage from large
479:(Nunez-Farfan et al. 2007). If this is the case, then plants that are able to tolerate damage will suffer little decrease in fitness and so resistance would not be selectively favored. For highly resistant plants, allocating resources to tolerance would not be selectively favored as the plant received minimal damage in the first place.
608:
different modes of herbivory may cause different resources to be affected by herbivory. The LRM encompasses every possible outcome of tolerance (i.e. equal tolerance in both environments, higher tolerance in low stress environments and lower tolerance in low stress environments) and allows multiple pathways to reach these outcome.
615:
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. Banta et al. (2010), however, suggested that the LRM should be represented as a set of seven models, instead of one, since each
607:
This recently proposed model takes into account the resource that is limiting plant fitness, the resource affected by herbivory and how the acquisition of resources is affected by herbivory (Wise and
Abrahamson 2005). Unlike the GRM and CCH, it is able to incorporate the type of damage received since
478:
It is classically assumed that there is a negative correlation between the levels of tolerance and resistance in plants (Stowe et al. 2000; Nunez-Farfan et al. 2007). For this trade-off to exist, it requires that tolerance and resistance be redundant defense strategies with similar costs to the plant
720:
The large number of studies indicating overcompensation in plants following herbivory, especially after apical meristem damage, has led some authors to suggest that there may be meristem relationships between plants and herbivores (Belsky 1986; Agrawal 2000; Edwards 2009). If herbivores provide some
655:
Espinosa and
Fornoni (2006) was one study which directly investigated whether tolerance may impose selection on herbivores. As suggested by Stinchcombe (2002), they used plants which had similar resistance but differed in tolerance to more easily differentiate the effects of each trait. As expected,
651:
If the traits that allow for tolerance affects the plant tissue's quality, quantity or availability, tolerance may also impose selection on herbivores. Consider a case where tolerance is achieved through activation of dormant meristems in the plants . These new plant tissues may be of lower quality
362:
will prevent collapse after sustaining damage, increasing plant tolerance (Tiffin 2000). Since plants have a meristemic construction, how resources are restricted among different regions of the plants, referred to as sectoriality, will affect the ability to transfer resources from undamaged areas to
121:
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
703:
Past studies have suggested plant resistance to play the major role in species diversity within communities, but tolerance may also be an important factor (Stowe et al. 2000; Pejman et al. 2009). Herbivory may allow less competitive, but tolerant plants to survive in communities dominated by highly
508:
and juveniles are less tolerant of herbivory since they did not develop the structures required for resource acquisition and so will rely more on traits that confer resistance (Boege et al. 2007; Barton 2008, Barton and
Koricheva 2010; Tucker and Avila-Sakar 2010). Although many studies find lower
430:
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). The advantage of using natural herbivory is that plants will experience the pattern of
166:
enzyme and delays in leaf senescence (Stowe et al. 2000). However, detecting an increase in environment 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
461:
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). Banta et al. (2010) found that their measure of tolerance will differ depending on whether fruit production or total
482:
There is now increasing evidence that many plants allocate resources to both types of defense strategies (Nunez-Farfan et al. 2007). There is also evidence that there may not be a trade-off between tolerance and resistance at all and that they may evolve independently (Leimu and
Koricheva 2006;
117:
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
421:
eaten. Wise and Carr (2008b) suggested that it is best to keep the measure of fitness and the measure of damage on the same scale when analyzing tolerance since having them on different scales may result is misleading outcomes. Even if the data were measured using different scales, data on the
491:
herbivores which have the ability to circumvent resistance traits of the plant (Nunez-Farfan et al. 2007; Muola et al. 2010). Also, as traits that confer tolerance are usually basic characteristics of plants, the result of photosynthetic on growth and not herbivory may also affect tolerance
118:
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).
829:
and increase nutrient uptake for the plant in exchange for food resources. These fungi are also able to alter the tolerance of plants to herbivory and may cause undercompesation, full compensation and overcompensation depending on the species of fungi involved (Bennett and Bever 2007).
193:, 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
869:
have undoubtedly also caused changes in various plant growth traits, such as decreased resource allocation to non-yield tissues (Welter and
Steggall 1993). Alterations in growth traits is likely to affect plant tolerance since the mechanisms overlap. That
113:, 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
599:, are better able to tolerate herbivory since they have abundant resources to replace lost tissues and recover from the damage. Plants growing in stressful environments are then predicted to have lower tolerance (Maschinski and Whitham 1989).
453:, may also affect plant tolerance (Tiffin and Inouye 2000). Lastly, models have predicted that manipulated herbivory may actually result in less precise estimates of tolerance relative to that from natural herbivory (Tiffin and Inoue 2000).
130:(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
98:(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
624:
It is classically assumed that tolerance traits do not impose selection on herbivore fitness (Strauss and
Agrawal 1999). This is in contrast to traits that confer resistance, which are likely to affect herbivore fitness and lead to a
313:
2009). However, the importance of this mechanism to tolerance is not well studied and it is unknown how much it contributes to tolerance since stored reserves mostly consist of carbon resources, whereas tissue damage causes a loss of
412:
Both fitness and herbivory can be measured or analyzed using an absolute (additive) scale or a relative (multiplicative) scale (Wise and Carr 2008b). The absolute scale may refer to number of fruits produced or total area of
1019:
Mariotte, P., Buttler, A., Kohler, F., Gilgen, A.K., Spiegelberger, T. (2013)."How do subordinate and dominant species in semi-natural grasslands relate to productivity and land-use change?" Basic and Applied Ecology, 14:
581:
The GRM proposes that the growth rate of the plant at the time of damage is important in determining its response (Hilbert et al. 1981). Plants that are growing in stressful conditions, such as low resource levels or high
391:
between fitness and level of damage (Stinchcombe 2002). Since an individual plant can only sustain one level of damage, it is necessary to measure fitness using a group of related individuals, preferably full-sibs or
1039:
Pejman, T.K., Bossuyt, B., Bonte, D., Hoffman, M. (2009). "Differential herbivory tolerance of dominant and subordinate plant species along gradients of nutrient availability and competition". Plant Ecology, 201:
652:
than what was previously eaten by herbivores. herbivores which have higher rates of consumption or can more efficiently use this new resource may be selectively favored over those that cannot (Stinchcombe 2002).
443:
variables, but replicating natural herbivory is difficult, causing plants to respond differently from imposed and natural herbivory (Tiffin and Inouye 2000). Growing plants in the control environment of the
1026:
Muola, A., Mutikainen, P., Laukkanen, L., Leim, R. (2010). "Genetic variation in herbivore resistance and tolerance: the role of plant life-history and type of damage". Journal of Evolutionary Biology, 23:
594:
The CCH suggests that there is a continuum of responses to herbivory (Maschinski and Whitham 1989). It predicts that plants growing in less stressful environment conditions, such as high resource or low
448:
may also affect their response as it is still a novel environment to the plants. Even if the plots are grown in natural settings, the methods of excluding or including herbivores, such as using cages or
798:
which protect the plant from herbivores and so the plant may have evolved tolerance to flower damage to acquire this benefit (Edwards 2009). Tolerance may also be involved in the mutualism between the
671:, so that their plant host will survive long enough to produce enough offspring for future pathogens to infect (Restif and Koelle 2003). However, this may only have limited application to herbivores.
1013:
Leimu, R., Koricheva, J. (2006). "A meta-analysis of tradeoffs between pant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies". Oikos, 112: 1-9.
1071:
Suwa, T., Maherali, H. (2008). "Influence of nutrient availability on the mechanisms of tolerance to herbivory in an annual grass, Avena barbata (Poaceae)". American Journal of Botany, 95: 434-440.
696:(Anderson and Briske 1995; Stowe et al. 2000; Pejman et al. 2009). Thus, plant defense strategies are important in determining temporal and spatial variation of plant species as it may change the
995:
Gonzales, W.L., Suarez, L.H. Molina-Montenegro, M.A., Gianoli, E. (2008). "Water availability limits tolerance of apical damage in the Chilean tarweed Madia sativa". Acta Oecologica, 34: 104-110.
158:
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
62:, 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
556:. Water and light levels are generally assumed to be positively associated with tolerance (Strauss and Agrawal 1999). However, there are exceptions such as evidence of decreased tolerance in
1016:
Machinski, J., Whitham, T.G. (1989). "The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing". American Naturalist, 134: 1-9.
810:(Edwards and Yu, 2008). The plant provides the ant with shelter and food bodies in return for protection against herbivory, but the ants also sterilize the plant by removing flower buds.
959:
Banta, J.A., Stevens, M.H.H., Pigliucci, M. (2010). "A comprehensive test of the 'limiting resource' framework applied to plant tolerance to apical meristem damage". Oikos, 119: 359-369.
1092:
Wise, M.J., Abrahamson, W.G. (2007). "Effects of resource availability on tolerance of herbivory: a review and assessment of three opposing models". American Naturalist, 169: 443-454.
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levels to decrease tolerance in plants (Lau and Tiffin 2009). Increased nutrient levels are also commonly found to be negatively associated with tolerance (Wise and Abrahamson 2007).
150:
changes, utilizing stored reserves, reallocating resources, increase in nutrients uptake, and plant architecture (Rosenthal and Kotanen 1994; Strauss and Agrawal 1999; Tiffin 2000).
953:
Anderson, V.J., Briske, D.D. (1995). "Herbivore-induced species replacement in grasslands: is it driven by herbivory tolerance or avoidance?". Ecological Applications, 5: 1014-1024.
1058:
Stowe, K.A., Marquis, R.J., Hochwender, C.G., Simms, E.L. (2000). "The evolutionary ecology of tolerance to consumer damage". Annual Review of Ecology and Systematics, 31: 565-595.
167:
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).
1030:
Nunez-Farfan, J., Fornoni, J., Valverde, P.L. (2007). "The evolution of resistance and tolerance to herbivores". Annual Review of Ecology, Evolution, and Systematics, 38: 541-566.
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siring in damaged plants compared to undamaged plants (Figure 4; Edwards 2009). The probability of attack after the first bout of herbivory is low in the environment inhabited by
1086:
Welter, S.C., Steggall, J.W. (1993). "Contrasting the tolerance of wild and domesticated tomatoes to herbivory: agroecological implications". Ecological Applications, 3: 271-278.
1052:
Stephan C.W., Steggall, J.W. (1993). "Contrasting the tolerance of wild and domesticated tomatoes to herbivory: agroecological implications". Ecological Applications, 3: 271-278.
289:(Trumble et al. 1993; Barton 2008). Utilizing stored reserves may be an important tolerance mechanism for plants which have abundant time to collect and store resources, such as
1007:
Irwin, R.E., Galen, C., Rabenold, J.J., Kaczorowski, R., McCutcheon, M.L. (2008). "Mechanisms of tolerance to floral larceny in two wildflower species". Ecology, 89: 3093-3104.
986:
Erb, M., Lenk, C., Degenhardt, J., Turlings T.C.J. (2009). "The underestimated role of roots in defense against leaf attackers". Trends in Ecology and Evolution, 14: 653-659.
965:
Barton, K.E., Koricheva, J. (2010). "The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis". The American Naturalist, 174: 481-493.
878:
suggests this as well (Welter and Steggall 1993). Most agricultural studies however, are more focused on comparing tolerance between damaged and undamaged crops, not between
962:
Bardner, R., Flectcher K.E. (1974). "Insect infestations and their effects on the growth and yield of field crops: a review". Bulletin of Entomological Research 64: 141-160.
1077:
Tiffin, P., Inouye, B.R. (2000). "Measuring tolerance to herbivory: accuracy and precision of estimates made using natural versus imposed damage". Evolution, 54: 1024-1029.
894:, can fully compensate and overcompensate for the damaged received (Trumble et al. 1993). A recent study by Poveda et al. (2010) also found evidence of overcompensation in
1046:
Restif, O., Koella, J.C. (2003). "Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions". The American Naturalist, 161: 827-836.
956:
Bagchi, S., Ritchie, M.E. (2011). "Herbivory and plant tolerance: experimental tests of alternative hypothesis involving non-substitutable resources". Oikos, 120: 119-127.
659:
A recent model by Restif and Koella (2003) found that plant tolerance can directly impose selection on pathogens. Assuming that investment in tolerance will reduce plant
1010:
Lau, J.A., Tiffin, P. (2009). "Elevated carbon dioxide concentrations indirectly affect plant fitness by altering plant tolerance to herbivory". Oecologia, 161: 401-410.
162:
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
977:
Boege, K., Dirzo, R., Siemens, D., Brown, P. (2007) "Ontogenetic switches from plant resistance to tolerance: minimizing costs with age?". Ecology Letters, 10: 177-187.
179:
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
721:
benefit for the plant despite causing damage, the plant may evolve tolerance to minimize the damage imposed by the herbivore to shift the relationship more towards
858:
is to use lines that are tolerant to herbivory and can compensate or even overcompensate for the damage inflicted (Nunez-Farfan et al. 2007; Poveda et al. 2010).
367:
may play important roles in tolerance, it is not well studied due to the difficulties in identifying the flow of resources (Marquis 1996). Increasing a plant's
1089:
Wise, M.J., Abrahamson, W.G. (2005). "Beyond the compensatory continuum: environmental resource levels and plant tolerance of herbivory". Oikos, 109: 417-428.
1095:
Wise, M.J., Carr, D.E. (2008a). "Applying the limiting resource model to plant tolerance of apical meristem damage". The American Naturalist, 172: 635-647.
371:
would seem advantageous since it increases the flow of resources to all sites of damage but it may also increase its susceptibility to herbivores, such as
950:
Agrawal, A.A. (2000). "Overcompensation of plants in response to herbivory and the by-product benefits of mutualism". Trends in Plant Science, 5: 309-313.
537:
and varies according to the conditions it is experiencing (Wise and Abrahamson 2005). The major resources that affect plant growth and also tolerance are
396:
to minimize other factors that may influence tolerance, after sustaining different levels of damage (Stinchcombe 2002). Tolerance is often presented as a
927:
1098:
Wise, M.J., Carr, D.E. (2008b). "On quantifying tolerance of herbivory for comparative analyses". The Society for the Study of Evolution, 62: 2429-2434.
281:
increased flower production after flower larceny. When these reproductive structures are not present, resources are allocated to other tissues, such as
1043:
Poveda, K., Jimenez, M.I.G., Kessler, A. (2010). "The enemy as ally: herbivore-induced increase in crop yield". Ecological Applications, 20: 1787-1793.
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they found evidence that resistance in plants affected herbivore fitness, but they were unable to find any effects of tolerance on herbivore fitness .
611:
Currently, the LRM seems to be most useful in predicting the effects that varying resources levels may have on tolerance (Wise and Abrahamson 2007).
404:
larger than, equal to and less than zero reflect overcompensation, full compensation and undercompensation, respectively (Strauss and Agrawal 1999).
1004:
Hilbert, D.W., Swift, D.M., Detling, J.K., Dyer, M.I. (1981). "Relative growth rates and the grazing optimization hypothesis". Oecologia, 51: 14-18.
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systems (Trumble et al. 1993). Resources are most often allocated to reproductive structures after damage, as shown by Irwin et al. (2008) in which
1001:
Hawkes, C.V., Sullivan, J.J. (2001). "The impact of herbivory on plants in different resource conditions: a meta-analysis". Ecology 82: 2045-2058.
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arms race (Stinchcombe 2002; Espinosa and Fornoni 2006). However, there are possible mechanisms in which tolerance may affect herbivore fitness .
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is able to compensate for this by reallocating resources to produce flowers on branches not occupied by castrating ants (Edwards and Yu, 2008).
1111:
1061:
Strauss, S.Y., Agrawal, A.A. (1999). "The ecology and evolution of plant tolerance to herbivory". Trends in Ecology and Evolution, 14: 179-185.
1080:
Trumble J.T., Kolodny-Hirsch, D.M., Ting, I.P. (1993). "Plant compensation for arthropod herbivory". Annual Review of Entomology, 38: 93-119.
968:
Barton, K.E. (2008). "Phenotypic plasticity in seedling defense strategies: compensatory growth and chemical induction". Oikos, 117: 917-925.
309:, and studies have shown evidence that these resources are allocated for regrowth following herbivory (Trumble et al. 1993; Tiffin 2000; Erb
980:
Edwards, D.P. (2009). "The roles of tolerance in the evolution, maintenance and breakdown of mutualism". Naturwissenschaften, 96: 1137-1145.
974:
Bennett, A.E., Bever, H.D. (2007). "Mycorrhizal species differentially alter plant growth and response to herbivory". Ecology, 88: 210-218.
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offset the negative effects of herbivory on dominant plants. It has also been suggested that the observation of species that occur late in
146:
Plants utilize many mechanisms to recover fitness from damage. Such traits include increased photosynthetic activity, compensatory growth,
983:
Edwards, D.P, Yu, D.W. (2008). "Tolerating castration by hiding flowers in plain site". Behavioral Ecology and Sciobiology, 63: 95-102.
488:
470:. Careful considerations must be made to choose traits that are linked to fitness as closely as possible when measuring tolerance.
1033:
Off, H., Ritchie, M.E. (1998). "Effects of herbivory on grassland plant diversity". Trends in Ecology and Evolution, 13: 261-265.
989:
Espinosa, E.G., Fornoni, J. (2006). "Host tolerance does not impose selection on natural enemies". New Phytologist, 170: 609-614.
1049:
Rosenthal, J.P., Kotanen, P.M. (1994). "Terrestrial plant tolerance to herbivory". Trends in Ecology and Evolution, 9: 145-148.
998:
Haukioja, E., Koricheva, J. (2000). "Tolerance to herbivory in woody vs. herbaceous plants". Evolutionary Ecology, 14: 551-562.
992:
Fornoni, J. (2011). "Ecological and evolutionary implications of plant tolerance to herbivory". Functional Ecology 25: 399-407.
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to the toxic compound, especially since most farmers are reluctant to assign a proportion of their land to contain susceptible
79:
32:
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and Olle Pellmyr. Plant-animal interactions an evolutionary approach. Victoria: Blackwell Publishing Company. pp. 77–106.
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and so have higher nutrition than most other tissues on the plants . Damage to apical meristems of plants may release it from
1083:
Tucker, C., Avila-Sakar, A. (2010). "Ontogenetic changes in tolerance to herbiory in Arabidopsis:. Oecologia, 164: 1005-1015.
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absolute scale can be log-transformed to be more similar to data on a relative (multiplicative) scale (Wise and Carr 2008b).
83:
1116:
937:
573:
There are currently three prominent models that predict how resource levels may alter a plants 's tolerance to herbivory.
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which can fully compensate for 50% defoliation (Barton 2008). There is also the added complexity of shifts in herbivore
1074:
Tiffin, P. (2000). "Mechanisms of tolerance to herbivore damage: what do we know?". Evolutionary Ecology, 14: 523-536.
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Alterations in resource allocation due to herbivory is studied heavily in agricultural systems (Trumble et al. 1993).
846:(Nunez-Farfan et al. 2007). However, the effectiveness of resistance traits may decrease as herbivores fungi counter
632:
One mechanism requires a genetic association between loci that confers resistance and tolerance either through tight
1055:
Stinchcombe, J.R. (2002). "Can tolerance traits impose selection on herbivores?". Evolutionary Ecology, 15: 595-602.
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Biomass regrowth following herbivory is often reported as an indicator of tolerance and plant response after apical
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645:
641:
1023:
Marquis, R.J. (1996). "Plant architecture, sectoriality and plant tolerance to herbivores". Vegetatio, 127: 85-97.
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78:
scientists (Painter 1958; Bardner and Fletcher 1974). Tolerance was actually initially classified as a form of
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Belsky, A.J. (1986). Does herbivory benefit plants? A review of the evidence. American Naturalist 127: 870-92.
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favored over those that cannot as they will pass on more of their offspring to the next generation. In longer
903:
729:, inducing resistance traits to temporally separate herbivores, providing information of future attacks and
633:
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will decrease the number of uninfected hosts. There may then be selection for decreased virulence in the
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variables that may affect both plant and herbivores. Using simulated herbivory allows for the control of
50:(Strauss and Agrawal 1999). Many factors intrinsic to the plants, such as growth rate, storage capacity,
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697:
685:
596:
583:
534:
123:
63:
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plant does not reallocate resources, but actually increases overall productivity to increase mass of
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It has been suggested that the trade-off between resistance and tolerance may change throughout the
334:, at the time of damage, unlike the induced mechanisms mentioned above. plant architecture includes
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693:
518:
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436:
388:
214:
189:
114:
99:
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778:
1036:
Painter, R.H. (1958). "Resistance of plants to insects". Annual Review of Entomology 3: 267-290.
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Strauss, S.Y., Zangerl, A.R. (2002). "Plant-insect interactions in terrestrial ecosystems". In
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and so may favor tolerance or resistance at different life stages (Barton and Koricheva 2010).
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432:
397:
242:
87:
47:
20:
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331:
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eaten, while the relative scale may refer to proportion of fruits damaged or proportion of
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to shoots ratio will allow plants to better absorb nutrients following herbivory and rigid
843:
736:
368:
364:
351:
110:
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82:(Painter 1958). Agricultural studies on tolerance, however, are mainly concerned with the
55:
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after the initial bout of herbivory (Edwards 2009). Another example involves endophytic
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abilities of plants following herbivory. (Anderson and Briske 1995; Stowe et al. 2000).
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339:
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before the season ends regardless of damage. In this case, plants that can shorten the
246:
230:
131:
106:
59:
51:
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between them (Leimu and Koricheva 2006; Nunez-Farfan et al. 2007; Muola et al. 2010).
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production caused by herbivory are more tolerant than those that cannot shorten this
180:
689:
558:
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127:
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It was soon recognized that many factors involved in plants tolerance, such as
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359:
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28:
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has favored tolerance for, but there may be biases resulting from unmeasured
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Studies have shown herbivory can cause delays in plant growth, flowering and
765:
660:
450:
254:
238:
210:
147:
24:
883:
875:
795:
668:
664:
553:
542:
522:
510:
505:
501:
319:
257:
delay are not any more tolerant than those that cannot as all plants can
176:
39:
213:
delays is likely a tolerance mechanism that will depend highly on their
887:
218:
163:
562:
with increased water availability (Wise and Abrahamson 2007, Gonzales
910:
895:
484:
372:
315:
226:
74:
Studies of tolerance to herbivory has historically been the focus of
768:
to overcompensate for the damage and produce the majority of their
644:
between tolerance and resistance and others which find significant
138:
effects on herbivores are still relatively unknown (Fornoni 2011).
914:
899:
787:
773:
735:
538:
401:
384:
330:
This form of tolerance relies on constitutive mechanisms, such as
302:
206:
879:
851:
826:
769:
757:
753:
550:
463:
418:
414:
355:
335:
306:
298:
282:
250:
234:
159:
91:
874:
tomato plants have lower tolerance to folivory than their wild
269:
Resource allocation following herbivory is commonly studied in
249:, however, there may be enough time for most plants to produce
66:
also have an effect on tolerance (Rosenthal and Kotanen 1994).
882:
and their wild counterparts. Many have found crops, such as
241:
change (Tiffin 2000). These faster recovering plant will be
27:. It is one of the general plant defense strategies against
616:
individual part of the LRM requires different assumptions.
126:
have also provided evidence that tolerance to herbivory is
764:. Due to the predictability of attacks, these plants have
854:(Nunez-Farfan et al. 2007). Another method to increase
725:(Edwards 2009). Such benefits include the release from
513:, this is not always the case, as seen in juveniles of
233:
is short, plants that are able to shorten the delay of
209:
production (Tiffin 2000). How plants respond to these
842:which possess toxic compounds to reduce damage by
19:is the ability of plants to mitigate the negative
817:A similar type of meristem involves plants and
90:, since it is of economical interest to reduce
917:and aboveground tissues (Poveda et al. 2010).
533:The response of plants to herbivory is often
363:damaged areas (Marquis 1996). Although plant
8:
38:Traits that confer tolerance are controlled
466:production was used to reflect fitness in
375:suckers (Marquis 1996, Stowe et al. 2000).
928:Inducible plant defenses against herbivory
383:Tolerance is operationally defined as the
265:Stored reserves and resource reallocation
838:Modern agriculture has focuses on using
684:Herbivory can have large effects on the
504:of the plants. It is often assumed that
794:(Edwards 2009). The fungi also produce
590:Compensatory continuum hypothesis (CCH)
529:Effects of resource levels on tolerance
301:and specialized storage organs such as
70:History of the study of plant tolerance
261:before the season ends (Tiffin 2000).
297:2009). Resources are often stored in
7:
354:(Marquis 1996, Tiffin 2000). A high
748:One of the best examples occurs in
322:and other nutrients (Tiffin 2000).
865:of plants by selecting for higher
221:factors such as, the abundance of
14:
566:2008). Many studies have found CO
86:on the plants' yield and not its
909:. Unlike previous examples, the
821:fungi (Bennett and Bever 2007).
933:Plant defense against herbivory
285:and shoots as seen in juvenile
492:(Rosenthal and Kotanen 1994).
474:Tolerance-resistance trade-off
426:Simulated vs natural herbivory
225:at different times during the
1:
1112:Biological defense mechanisms
938:Plant perception (physiology)
603:Limiting resource model (LRM)
122:studies using techniques in
102:relationship (Belsky 1986).
94:losses due to herbivory by
1143:
840:genetically modified crops
197:(Suwa and Maherali 2008).
808:Allomerus octoarticulatus
752:where there is increased
906:Phthorimaea operculella
806:, and its ant symbiont
620:Selection on herbivores
577:Growth rate model (GRM)
142:Mechanisms of tolerance
898:plants in response to
745:
229:(Tiffin 2000). If the
739:
710:ecological succession
408:Scales of measurement
134:implications and its
124:quantitative genetics
1117:Plants by adaptation
825:fungi inhabit plant
675:Species interactions
515:Plant ago lanceolata
154:Photosynthetic rates
904:potato tuber moth,
786:plants and produce
750:Ipomopsis aggregata
742:Ipomopsis aggregata
468:Arabdopsis thaliana
379:Measuring tolerance
350:rigidity and plant
287:Plantago lanceolata
279:Ipomopsis aggregata
275:Polemonium viscosum
201:Phenological change
190:Ipomopsis aggregata
171:Compensatory growth
111:nutrient allocation
84:compensatory effect
56:nutrient allocation
790:that destroy host
746:
496:Ontogenetic shifts
326:Plant architecture
293:(Tiffin 2000; Erb
42:and therefore are
31:, the other being
23:effects caused by
1066:Carlos M. Herrera
680:Plant communities
132:macroevolutionary
1134:
733:(Agrawal 2000).
727:apical dominance
291:perennial plants
185:apical dominance
1142:
1141:
1137:
1136:
1135:
1133:
1132:
1131:
1127:Plant cognition
1102:
1101:
947:
942:
923:
836:
756:production and
718:
682:
677:
663:, infection by
627:co-evolutionary
622:
605:
592:
579:
569:
531:
498:
476:
459:
428:
410:
381:
328:
267:
247:growing seasons
203:
173:
156:
144:
72:
12:
11:
5:
1140:
1138:
1130:
1129:
1124:
1119:
1114:
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1103:
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1087:
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1078:
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1062:
1059:
1056:
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1050:
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1037:
1034:
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1024:
1021:
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1005:
1002:
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993:
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987:
984:
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978:
975:
972:
969:
966:
963:
960:
957:
954:
951:
946:
943:
941:
940:
935:
930:
924:
922:
919:
902:damage by the
835:
832:
792:inflorescences
717:
714:
681:
678:
676:
673:
621:
618:
604:
601:
591:
588:
578:
575:
567:
547:carbon dioxide
530:
527:
497:
494:
487:herbivores or
475:
472:
458:
457:Fitness traits
455:
427:
424:
409:
406:
380:
377:
327:
324:
266:
263:
231:growing season
202:
199:
181:cell divisions
172:
169:
155:
152:
143:
140:
136:coevolutionary
107:photosynthetic
71:
68:
52:photosynthetic
13:
10:
9:
6:
4:
3:
2:
1139:
1128:
1125:
1123:
1120:
1118:
1115:
1113:
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1107:
1097:
1094:
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1076:
1073:
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1060:
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1054:
1051:
1048:
1045:
1042:
1038:
1035:
1032:
1029:
1025:
1022:
1018:
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1009:
1006:
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1000:
997:
994:
991:
988:
985:
982:
979:
976:
973:
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967:
964:
961:
958:
955:
952:
949:
948:
944:
939:
936:
934:
931:
929:
926:
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920:
918:
916:
912:
908:
907:
901:
897:
893:
889:
885:
881:
877:
873:
868:
864:
863:Domestication
859:
857:
853:
849:
845:
841:
833:
831:
828:
824:
820:
815:
813:
809:
805:
804:Cordia nodosa
801:
800:myremecophyte
797:
793:
789:
785:
781:
780:
775:
771:
767:
763:
759:
755:
751:
744:
743:
738:
734:
732:
728:
724:
715:
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695:
691:
687:
679:
674:
672:
670:
666:
662:
657:
653:
649:
647:
643:
639:
635:
630:
628:
619:
617:
614:
613:Meta-analyses
609:
602:
600:
598:
589:
587:
585:
576:
574:
571:
565:
561:
560:
555:
552:
548:
544:
540:
536:
528:
526:
524:
521:as the plant
520:
516:
512:
509:tolerance in
507:
503:
495:
493:
490:
486:
480:
473:
471:
469:
465:
456:
454:
452:
447:
442:
441:environmental
438:
437:environmental
434:
425:
423:
420:
416:
407:
405:
403:
399:
398:reaction norm
395:
390:
386:
378:
376:
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366:
361:
357:
353:
349:
345:
341:
337:
333:
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308:
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296:
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153:
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133:
129:
125:
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108:
103:
101:
97:
93:
89:
85:
81:
77:
69:
67:
65:
61:
57:
53:
49:
46:traits under
45:
41:
36:
34:
30:
26:
22:
18:
905:
892:cauliflowers
872:domesticated
860:
837:
816:
811:
807:
803:
777:
762:I. aggregata
761:
749:
747:
740:
719:
702:
683:
658:
654:
650:
646:correlations
631:
623:
610:
606:
593:
580:
572:
563:
559:Madia sativa
557:
532:
514:
499:
481:
477:
467:
460:
431:damage that
429:
411:
382:
329:
310:
294:
286:
278:
274:
271:agricultural
268:
255:phenological
239:phenological
215:life history
211:phenological
204:
195:reproduction
188:
174:
157:
148:phenological
145:
120:
115:environments
104:
76:agricultural
73:
37:
16:
15:
876:progenitors
848:adaptations
834:Agriculture
823:Mycorrhizal
819:mycorrhizal
779:Neophtodium
731:pollination
706:fertilizers
698:competitive
694:communities
642:correlation
597:competition
584:competition
519:communities
502:development
369:vasculature
365:vasculature
352:vasculature
243:selectively
223:pollinators
100:mutualistic
64:competition
40:genetically
1106:Categories
1027:2185-2196.
945:References
856:crop yield
784:parasitize
776:, such as
716:Mutualisms
692:of plants
686:succession
638:pleiotropy
489:specialist
451:pesticides
446:greenhouse
389:regression
332:morphology
219:ecological
217:and other
109:rates and
80:resistance
54:rates and
33:resistance
29:herbivores
1122:Herbivory
884:cucumbers
812:C. nodosa
796:alkaloids
723:mutualism
690:diversity
669:pathogens
665:pathogens
661:fecundity
554:nutrients
511:seedlings
506:seedlings
485:mammalian
433:selection
259:reproduce
128:heritable
48:selection
44:heritable
25:herbivory
17:Tolerance
1040:611-619.
1020:217-224.
921:See also
888:cabbages
782:, which
523:develops
400:, where
346:number,
342:ratios,
320:nitrogen
177:meristem
766:evolved
634:linkage
535:plastic
462:viable
387:of the
164:Rubisco
88:fitness
21:fitness
915:tubers
911:potato
896:potato
788:spores
564:et al.
419:leaves
402:slopes
394:clones
373:phloem
340:shoots
316:carbon
311:et al.
303:tubers
299:leaves
295:et al.
283:leaves
227:season
160:leaves
60:uptake
900:tuber
880:crops
867:yield
852:crops
844:pests
827:roots
774:fungi
770:seeds
543:light
539:water
385:slope
360:stems
356:roots
336:roots
307:roots
251:seeds
207:fruit
96:pests
890:and
758:seed
754:seed
688:and
551:soil
549:and
464:seed
415:leaf
348:stem
344:stem
305:and
277:and
235:seed
92:crop
58:and
636:or
338:to
1108::
886:,
802:,
545:,
541:,
318:,
568:2
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