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Benevolent herbivores?
TREE vol. 2, no. 6, June 1987
Nielsen and others favouring other hypotheses should realize that any credible theory of small mammal cycles must be able to explain the observed facts. As I understand the present evidence, the various versions of the plant-microtine hypothesis are not supported by recent observationaP.5 and experimentaP7 studies from Fennoscandia. It is not obvious to me how these theories will explain the geographical and
interspecific patterns which were the impetus for my news article. I. Hanski Departmentof Zoology,Universityof Helsinki, P.Rautatiekatu13,SF-00100Helsinki,Finland.
References 1 Hansson, L. and Henttonen,
H. (1985)
Oecologia 67,394402 2 Henttonen, Ii. and Hansson,
L. HoIarct.
Ecol. (in press) 3 Henttonen, H., McGuire, A.D. and Hansson, L. (1985) Ann. Zoo/. Fem. 22, 221-227 4 Anderson, M. and Jonasson, S. (1986) Oikos46,93-106 5 Jonasson, S., Bryant, J.P., Chapin, F.S., 111 and Anderson, M. (1986) Am. Nat. 128, 394-409 6 Henttonen, t-l., Oksanen, T., Jortikka, A. and Haukisalmi, V. Oikos (in press) 7 Laine, K.M. and Henttonen, H. Oikos (in press)
Benevolent Herbivores? Two questions dominate current thinking on plant-herbivore interactions: what is the impact of feeding by herbivores on the distribution and abundance of plants; and what is the role of herbivory as an agency of natural selection, leading to differential performance of host plant genotypes? These two questions come together in discussions of how the evolutionary consequences of herbivory are manifest at the population and ecosystem levels.
within a plant population? The alternative view is championed by the ecosystem ecologists. They can’t understand how anyone could seriously doubt the answer. Of course herbivory is good for plants. Where would plants like grasses be without the large mammalian herbivores that stop the grasslands from becoming woodlands? They claim that there are lots of different ways Some controversies seem desin which multispecies interactions tined to run forever. No sooner does could resolve themselves as positive a sensible compromise seem to have correlations between herbivore feedemerged, than a new generation, ing and plant performance (as when having escaped exposure to the depolyphagous herbivores feed on a bate last time around, rediscovers range of plant species, but prefer the the polarized positions that have just species that would otherwise be the been abandoned. In recent months, competitive dominant). for example, these pages have witRecent publications in the Amernessed the resurgence of the density ican Naturalist suggest that adherdependence debate (TREE Letters, ents of both doctrines are in combaMarch 1987), and the argument ab- tive mood, and that, if anything, the out whether or not competition is temperature of the debate is rising. important in structuring communiBelskyl presents the case for the 1986). ties (TREE Letters, November evolutionary ecologists. She sugOne of the more peculiar of the long gests that all the evidence allegedly running disputes has also recently showing increased fitness under herreturned to the limelight. This conbivory is flawed in one way or cerns the question of whether or not another (and see Verkaa?), and conherbivory is good for plants. cludes that ‘Although herbivores As with so many heated conmay benefit certain plants by reductroversies, the proponents of the exing competition or removing senestreme viewpoints are divided by a cent tissue, no convincing evidence common language. \n this case, the supports the theory that herbivory semantic problems hinge on what, benefits grazed plants’. is meant by ‘good for exactly, In reply, McNaughton3 condemns To darwinian population plants’. Belsky for invoking the aristotlean the whole question ecologists, ‘fallacy of many questions’, by posseems to be complete nonsense. ing the problem in a manner that When, they ask, has defoliation of an demands a single answer, when only individual plant ever been shown to a complex answer will do. He acincrease its genetic fitness? Under cuses her of ‘logical errors, papers what circumstances would an invitauncited . , . that refute her principal tion to be defoliated ever constitute points, a misrepresentation of the an evolutionarily stable strategy methods . . used in field studies, and errors of fact and interpretation’. M.J. Crawley is at the Department of Pure and He concludes ‘Many effects of herbivores upon their food plants that are Applied Biology, Imperial College at Silwood presently perceived to be deleterious Park, Ascot, Berks SL5 7PY, UK.
M, J, Crawley may be less deleterious than expected due to compensatory growth of the plant’. He goes on ‘I do not contend that herbivory maximises plant fitness, but that plants have the capacity to compensate for herbivory and may, at low levels of herbivory, overcompensate for damage so that fitness may be increased’. Despite protestations of individual selectionism“ a good many of the alleged benefits of herbivory are blatantly group selectionist (e.g. improved rates of nutrient cycling or enhanced rates of nitrogen fixation by soil organisms fed by a rain of honeydew). Nevertheless, there are a number of clearly defined ways in which a single, negative process could have a positive net effect when it acts in concert with an additional, stronger negative process. Hay5 provides an example from interspecific competition between marine algae. In this case, the superior competitor increases the fitness of the inferior plant in the presence of herbivory by providing it with a physical refuge from attack. Similarly, one mortality factor may be highly damaging on its own, but beneficial when acting in concert with another, more severe mortality factor. Forrester (pers. commun.) is studying the combined effects of curculionid weevils, cynipid gall wasps and small mammals on the survivorship of acorns of English oak. Small mammals inflict exceptionally high rates of mortality on sound acorns, but ignore galled or weevily acorns. While almost all the acorns attacked by insects are killed, some do survive, and these are ignored by small mammals. This may be the first example of herbivore feeding increasing the survivorship (and, presumably, the fitness) of a plant. Up to now, the problem of resolving the question as to whether herbivory 167
TREE vol. 2, no. 6, June 1987
Fig. 1. Browsed (left) and uneaten (right1 scarlet gilia plants, about 12 cm tall. The original inflorescence of the left hand plant was browsed by herbivores at the position from Ref. 6. indicated. Reproduced, with permission,
could ever be good for plants has been that convincing data have not been published. A recent experiment, however, carried out in Arizona by Paige and Whitham on scarlet gilia, lpomopsis aggregata, really puts the cat amongst the pigeons. These authors show that individuals browsed by deer or elk have nearly 2.5 times the relative fitness of intact, ungrazed plants. This comes about because instead of producing a single flowering shoot, the browsed plants produce four regrowth shoots, each of which bears flowers (Fig. 1). The paper caused a considerable stir when it was read at the Ecological Society of America in Syracuse, last August. A great many of the audience were simply unwilling to believe the results. Surely there was some mistake? The experiment could not have been randomized properly. There must have been confounding effects. Subtle costs of herbivory must have been overlooked. And so on. In fact, it is extremely difficult to fault either the quality of the data or the nature of the experimental de-
sign. It is true that only 40 plants were used in the manipulative experiment, but careful measurements of seed numbers per fruit, individual seed weights, the timing of seed production, germination rate and seedling survival consistently point to the fact that removal of the primary shoot leads to the production of substantially more seeds on regrowth shoots, and that these seeds are not disadvantaged compared with seeds from primary shoots. This is in marked contrast to some other studies of fruiting on regrowth shoots, in which the seeds were smaller, ripened later, and produced less competitive seedlings7. These results immediately raise two questions that are not addressed by Paige and Whitham. Why do we not witness the prospering of plants that branch from the base when they are not grazed? And why do the regrowth shoots not suffer defoliation by the same deer and elk that eat the primary shoots? On the first point, the only really plausible suggestion is that the probability of herbivore attack on the primary shoots is so high that a mutant plant which produced multiple shoots from the outset would lose them all to herbivores, thereby depleting its presumably limited resources. In years or in places where herbivory was low, of course, this relative advantage would be lost, and the proliferation of fecund, multistemmed individuals might be expected. The second question is linked to the fitness implications of the first. In other systems where regrowth has been studied in detail (e.g. ragwort attacked by cinnabar moth*) the plant can compensate partially for the removal of its entire crop of flowers, because it is able to produce regrowth shoots after its insect herbivores have pupated. These secondary shoots can then produce regrowth seeds under conditions of greatly reduced herbivory7. In the case of gilia grazed by ungulates, it is not clear why the multistemmed, regrowth plants escape being eaten. It is possible that the regrowth shoots are better defended9 or, simply, that the herbivores have moved on in the meantime, either to other places, or to other food plants. Although Paige and Whitham present no data bearing directly on this question, it is likely that repeated defoliation of plants would eventually deplete their carbohydrate and protein reserves. Thus, the benefit gained by browsed plants depends absolutely on differential herbivore attack rates between primary and
regrowth shoots. If the attack rates per plant were as high for the regrowth shoots as for the primaries, it is hard to see how fitness could be increased. If the predictability of herbivore attack on the primary shoots is sufficiently high, it is not difficult to imagine that an evolutionary advantage might accrue to a strategy of restrained early reproduction, leading to the production of single, primary shoots, followed by vigorous, multistemmed regrowth following herbivore attack. However, this argument requires that attack on the regrowth shoots is predictably low. Even with this plethora of ‘ifs’ the story fails to explain why ungrazed plants do not put on a second burst of shooting once the risk of herbivory has passed, for, if it is advantageous to produce new flowering shoots following defloration of the primary shoot, then surely it is just as advantageous to produce them when ungrazed? The essential point is that we really don’t know exactly what herbivores do to plants in the majority of cases. We simply haven’t got enough long term, manipulative field experiments to draw upon . We know what herbivores could do to plants, and there is an abundance of models of plantherbivore dynamics. From the intriguing variety of dynamic behaviour exhibited by existing experimental data, it is quite clear that all herbivores don’t do the same things to plants. But before we can say how often, and under what herbivores might circumstances, benefit plants, we shall need dozens more field experiments. Paige and Whitham’s results are fascinating, but they raise more questions than they answer. McNaughton is right to point out that herbivores could increase plant fitness. Belsky is right to stress that the weight of evidence suggests that they almost never do.
References 1 Belsky, A.J. (1986) Am. Nat. 127, 870-892 2 Verkaar, H.J. (1986) Trends&o/.
ho/.
168 3 McNaughton,
S.J. (1986) Am. Nat. 128, 766-770 4 Owen, D.F. and Wiegert, R.G. (1984) Oikos 43,403 5 Hay, M. (1986) Am. Nat. 128,617-641 6 Paige, K.N. and Whitham, T.G. (1987) Am. Nat. 129,407-416 7 Crawley, M.J. and Nachapong, M. (1985) J. Ecol. 73,255-261 8 Cameron, E. (1935) J. Ecol. 23,265322 9 Crawley, M.J. and Nachapong, M.
(1984) Ecol. Entomol. 9,389-393
1,
Nielsen and others favouring other hypotheses should realize that any credible theory of small mammal cycles must be able to explain the observed facts. As I understand the present evidence, the various versions of the plant-microtine hypothesis are not supported by recent observationaP.5 and experimentaP7 studies from Fennoscandia. It is not obvious to me how these theories will explain the geographical and
interspecific patterns which were the impetus for my news article. I. Hanski Departmentof Zoology,Universityof Helsinki, P.Rautatiekatu13,SF-00100Helsinki,Finland.
References 1 Hansson, L. and Henttonen,
H. (1985)
Oecologia 67,394402 2 Henttonen, Ii. and Hansson,
L. HoIarct.
Ecol. (in press) 3 Henttonen, H., McGuire, A.D. and Hansson, L. (1985) Ann. Zoo/. Fem. 22, 221-227 4 Anderson, M. and Jonasson, S. (1986) Oikos46,93-106 5 Jonasson, S., Bryant, J.P., Chapin, F.S., 111 and Anderson, M. (1986) Am. Nat. 128, 394-409 6 Henttonen, t-l., Oksanen, T., Jortikka, A. and Haukisalmi, V. Oikos (in press) 7 Laine, K.M. and Henttonen, H. Oikos (in press)
Benevolent Herbivores? Two questions dominate current thinking on plant-herbivore interactions: what is the impact of feeding by herbivores on the distribution and abundance of plants; and what is the role of herbivory as an agency of natural selection, leading to differential performance of host plant genotypes? These two questions come together in discussions of how the evolutionary consequences of herbivory are manifest at the population and ecosystem levels.
within a plant population? The alternative view is championed by the ecosystem ecologists. They can’t understand how anyone could seriously doubt the answer. Of course herbivory is good for plants. Where would plants like grasses be without the large mammalian herbivores that stop the grasslands from becoming woodlands? They claim that there are lots of different ways Some controversies seem desin which multispecies interactions tined to run forever. No sooner does could resolve themselves as positive a sensible compromise seem to have correlations between herbivore feedemerged, than a new generation, ing and plant performance (as when having escaped exposure to the depolyphagous herbivores feed on a bate last time around, rediscovers range of plant species, but prefer the the polarized positions that have just species that would otherwise be the been abandoned. In recent months, competitive dominant). for example, these pages have witRecent publications in the Amernessed the resurgence of the density ican Naturalist suggest that adherdependence debate (TREE Letters, ents of both doctrines are in combaMarch 1987), and the argument ab- tive mood, and that, if anything, the out whether or not competition is temperature of the debate is rising. important in structuring communiBelskyl presents the case for the 1986). ties (TREE Letters, November evolutionary ecologists. She sugOne of the more peculiar of the long gests that all the evidence allegedly running disputes has also recently showing increased fitness under herreturned to the limelight. This conbivory is flawed in one way or cerns the question of whether or not another (and see Verkaa?), and conherbivory is good for plants. cludes that ‘Although herbivores As with so many heated conmay benefit certain plants by reductroversies, the proponents of the exing competition or removing senestreme viewpoints are divided by a cent tissue, no convincing evidence common language. \n this case, the supports the theory that herbivory semantic problems hinge on what, benefits grazed plants’. is meant by ‘good for exactly, In reply, McNaughton3 condemns To darwinian population plants’. Belsky for invoking the aristotlean the whole question ecologists, ‘fallacy of many questions’, by posseems to be complete nonsense. ing the problem in a manner that When, they ask, has defoliation of an demands a single answer, when only individual plant ever been shown to a complex answer will do. He acincrease its genetic fitness? Under cuses her of ‘logical errors, papers what circumstances would an invitauncited . , . that refute her principal tion to be defoliated ever constitute points, a misrepresentation of the an evolutionarily stable strategy methods . . used in field studies, and errors of fact and interpretation’. M.J. Crawley is at the Department of Pure and He concludes ‘Many effects of herbivores upon their food plants that are Applied Biology, Imperial College at Silwood presently perceived to be deleterious Park, Ascot, Berks SL5 7PY, UK.
M, J, Crawley may be less deleterious than expected due to compensatory growth of the plant’. He goes on ‘I do not contend that herbivory maximises plant fitness, but that plants have the capacity to compensate for herbivory and may, at low levels of herbivory, overcompensate for damage so that fitness may be increased’. Despite protestations of individual selectionism“ a good many of the alleged benefits of herbivory are blatantly group selectionist (e.g. improved rates of nutrient cycling or enhanced rates of nitrogen fixation by soil organisms fed by a rain of honeydew). Nevertheless, there are a number of clearly defined ways in which a single, negative process could have a positive net effect when it acts in concert with an additional, stronger negative process. Hay5 provides an example from interspecific competition between marine algae. In this case, the superior competitor increases the fitness of the inferior plant in the presence of herbivory by providing it with a physical refuge from attack. Similarly, one mortality factor may be highly damaging on its own, but beneficial when acting in concert with another, more severe mortality factor. Forrester (pers. commun.) is studying the combined effects of curculionid weevils, cynipid gall wasps and small mammals on the survivorship of acorns of English oak. Small mammals inflict exceptionally high rates of mortality on sound acorns, but ignore galled or weevily acorns. While almost all the acorns attacked by insects are killed, some do survive, and these are ignored by small mammals. This may be the first example of herbivore feeding increasing the survivorship (and, presumably, the fitness) of a plant. Up to now, the problem of resolving the question as to whether herbivory 167
TREE vol. 2, no. 6, June 1987
Fig. 1. Browsed (left) and uneaten (right1 scarlet gilia plants, about 12 cm tall. The original inflorescence of the left hand plant was browsed by herbivores at the position from Ref. 6. indicated. Reproduced, with permission,
could ever be good for plants has been that convincing data have not been published. A recent experiment, however, carried out in Arizona by Paige and Whitham on scarlet gilia, lpomopsis aggregata, really puts the cat amongst the pigeons. These authors show that individuals browsed by deer or elk have nearly 2.5 times the relative fitness of intact, ungrazed plants. This comes about because instead of producing a single flowering shoot, the browsed plants produce four regrowth shoots, each of which bears flowers (Fig. 1). The paper caused a considerable stir when it was read at the Ecological Society of America in Syracuse, last August. A great many of the audience were simply unwilling to believe the results. Surely there was some mistake? The experiment could not have been randomized properly. There must have been confounding effects. Subtle costs of herbivory must have been overlooked. And so on. In fact, it is extremely difficult to fault either the quality of the data or the nature of the experimental de-
sign. It is true that only 40 plants were used in the manipulative experiment, but careful measurements of seed numbers per fruit, individual seed weights, the timing of seed production, germination rate and seedling survival consistently point to the fact that removal of the primary shoot leads to the production of substantially more seeds on regrowth shoots, and that these seeds are not disadvantaged compared with seeds from primary shoots. This is in marked contrast to some other studies of fruiting on regrowth shoots, in which the seeds were smaller, ripened later, and produced less competitive seedlings7. These results immediately raise two questions that are not addressed by Paige and Whitham. Why do we not witness the prospering of plants that branch from the base when they are not grazed? And why do the regrowth shoots not suffer defoliation by the same deer and elk that eat the primary shoots? On the first point, the only really plausible suggestion is that the probability of herbivore attack on the primary shoots is so high that a mutant plant which produced multiple shoots from the outset would lose them all to herbivores, thereby depleting its presumably limited resources. In years or in places where herbivory was low, of course, this relative advantage would be lost, and the proliferation of fecund, multistemmed individuals might be expected. The second question is linked to the fitness implications of the first. In other systems where regrowth has been studied in detail (e.g. ragwort attacked by cinnabar moth*) the plant can compensate partially for the removal of its entire crop of flowers, because it is able to produce regrowth shoots after its insect herbivores have pupated. These secondary shoots can then produce regrowth seeds under conditions of greatly reduced herbivory7. In the case of gilia grazed by ungulates, it is not clear why the multistemmed, regrowth plants escape being eaten. It is possible that the regrowth shoots are better defended9 or, simply, that the herbivores have moved on in the meantime, either to other places, or to other food plants. Although Paige and Whitham present no data bearing directly on this question, it is likely that repeated defoliation of plants would eventually deplete their carbohydrate and protein reserves. Thus, the benefit gained by browsed plants depends absolutely on differential herbivore attack rates between primary and
regrowth shoots. If the attack rates per plant were as high for the regrowth shoots as for the primaries, it is hard to see how fitness could be increased. If the predictability of herbivore attack on the primary shoots is sufficiently high, it is not difficult to imagine that an evolutionary advantage might accrue to a strategy of restrained early reproduction, leading to the production of single, primary shoots, followed by vigorous, multistemmed regrowth following herbivore attack. However, this argument requires that attack on the regrowth shoots is predictably low. Even with this plethora of ‘ifs’ the story fails to explain why ungrazed plants do not put on a second burst of shooting once the risk of herbivory has passed, for, if it is advantageous to produce new flowering shoots following defloration of the primary shoot, then surely it is just as advantageous to produce them when ungrazed? The essential point is that we really don’t know exactly what herbivores do to plants in the majority of cases. We simply haven’t got enough long term, manipulative field experiments to draw upon . We know what herbivores could do to plants, and there is an abundance of models of plantherbivore dynamics. From the intriguing variety of dynamic behaviour exhibited by existing experimental data, it is quite clear that all herbivores don’t do the same things to plants. But before we can say how often, and under what herbivores might circumstances, benefit plants, we shall need dozens more field experiments. Paige and Whitham’s results are fascinating, but they raise more questions than they answer. McNaughton is right to point out that herbivores could increase plant fitness. Belsky is right to stress that the weight of evidence suggests that they almost never do.
References 1 Belsky, A.J. (1986) Am. Nat. 127, 870-892 2 Verkaar, H.J. (1986) Trends&o/.
ho/.
168 3 McNaughton,
S.J. (1986) Am. Nat. 128, 766-770 4 Owen, D.F. and Wiegert, R.G. (1984) Oikos 43,403 5 Hay, M. (1986) Am. Nat. 128,617-641 6 Paige, K.N. and Whitham, T.G. (1987) Am. Nat. 129,407-416 7 Crawley, M.J. and Nachapong, M. (1985) J. Ecol. 73,255-261 8 Cameron, E. (1935) J. Ecol. 23,265322 9 Crawley, M.J. and Nachapong, M.
(1984) Ecol. Entomol. 9,389-393
1,