Plant Adaptations to Herbivory: Mutualistic versus Antagonistic Coevolution Johannes Järemo; Juha Tuomi; Patric Nilsson; Tommy Lennartsson Oikos, Vol. 84, No. 2. (Feb., 1999), pp. 313-320. Stable URL: http://links.jstor.org/sici?sici=0030-1299%28199902%2984%3A2%3C313%3APATHMV%3E2.0.CO%3B2-X Oikos is currently published by Nordic Society Oikos.
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FORUM is intended for new ideas or new ways of interpreting existing information. It provides a chance for suggesting hypotheses and for challenging current thinking on ecological issues. A lighter prose, designed to attract readers, will be permitted. Formal research reports, albeit short, will not be accepted, and all contributions should be concise with a relatively short list of references. A summary is not required.
Plant adaptations to herbivory: mutualistic versus antagonistic coevolution Johannes Jaremo', Juha Tuomi2, Patric Nilsson' and Tommy Lennavtsson3. 'Dept of Theoretical Ecology, Lund Univ., Ecology Building. SE-223 62 Lund, Sweden (iohannes.
[email protected].). 'Dept of Biology, Unitj. of Oulu, Linnanmaa, FIN-90570 Oulu, Finland. "ept of Conseraation Biology, Swedish Univ. of Agricultural Sciences, Box 7072, SE-750 07 Uppsala, Sweden. The discovery of overcompensatory responses to damage in some plant species has inspired attempts to classify some plant-herbivore interactions as mutualism. Since the debates over plant-herbivore mutualism and overcompensation have been intense, we attempt to outline three conceptual models of plant-animal interactions and evaluate the status of interactions with help of three different fitness criteria: relative fitness, absolute fitness, and mean absolute fitness. Our three plant-animal interactions are assumed to represent "plant-pollinator mutualism", "plantherbivore antagonism" and "the evolution of overcompensation", respectively. Each case describes how absolute fitness, and consequently also the other two fitness criteria, is assumed to change with animal encounters for plants with special adaptations to cope with those encounters and for plants with no such adaptations. As a result, all these types of interactions may be considered as mutualism when taken relative fitness only into account. Obviously, this criterion is too weak because any trait, evolving under natural selection, should improve fitness relative to other, alternative traits. Absolute fitness increases with animal encounters for the adapted phenotype in the f h t and in the last case and thus, in the context of absolute fitness, overcompensation in plants would indicate plant-herbivore mutualism. However, absolute fitness as such may not be sufficient when discussing the evolutionary history of plant-animal mutualism. In the light of mean fitness, overcompensation as presented in earlier studies does not represent mutualism between plants and herbivores. Mean absolute fitness in plant populations decrease with the risk of herbivore attack in our model of overcompensation, while the reverse trend characterises our plant-pollinator model. We, therefore, suggest that mean absolute fitness may well provide an appropriate criterion for distinguishing mutualistic and antagonistic plant-animal interactions in coevolutionary contexts. In order to evaluate our model-system, we compare the predicted patterns with empirical data on the grassland biennial Gentianella campestris.
"It is time to look beyond biases and preconceived notions that herbivory is always, unquestionably, detrimental to the plant" (Paige 1994). This claim was provoked by observations that some plants increase vegetative productivity or improve seed yield when being naturally or artificially damaged as compared to undamaged plants. i.e. overcompensation (McOIKOS 84 2 ( 1999)
Naughton 1979, Paige and Whitham 1987. Maschinski and Whitham 1989, Lennartsson et al. 1997, 1998). The vivid debate following the observations of overcompensation involves two major questions: on the one hand? the generality of overcompensatory responses among plants, and on the other, whether herbivory may be beneficial to plants or not. The benefits are in turn assumed to imply a mutualistic relationship between plants and herbivores (Paige 1992, 1994, Vail 1992: 1994). This view seems first to have appeared in Owen's (1980) discussion on "How plants may benefit from animals that eat them". The plant-herbivore mutualism was critically evaluated and discussed by Belsky (1986) who both reviewed empirical data on plant compensatory growth (e.g. McNaughton 1979: 1983) and questioned the notion that plants might benefit from being eaten. Belsky et al. (1993) restated the critique and incorporated compensatory responses into the same category of anti-herbivory adaptations as plant defences or. more generally, as an adaptation to all kinds of damage that a plant may experience. including drought and frost. This objection together with the fact that "rapid plant regrowth is more likely to have evolved as a strategy to reduce the negative impacts of all types of damage than as a strategy to increase fitness following herbivory above ungrazed levels", makes the mutualism hypothesis less attractive according to Beisky et al. (1993). We believe that much of the controversy surrounding the possibility of plant-herbivore mutualism can be resolved by carefully distinguishing among fitness measures when considering the consequences for plants. In this paper. we will review the history of ideas about plant-herbivore mutualism, show how conflicting points of view can be attributed to differing implicit meanings of "fitness". and present three plant-animal interactions 313
based on consequences for absolute fitness, relative fitness and mean fitness in plant populations. These ideas will be applied to the interpretation of the result from a previous study of overcompensation in plants, from which it is possible to derive estimates of all three fitness measures. Since our main interest concerns the conceptual interpretation of data and models, we shall not take any stand of whether experiments showing overcompensation have been correctly performed or not (for critlcal discussion, see Belsky 1986, Bergelson and Crawley 1992, Belsky et al. 1993, Bergelson et al. 1996). Note also that we are treating compensatory responses as adaptation to herbivory or shoot damage in general, but this need not always be true (e.g. Aarssen and Irwin 1991, Aarssen 1995, Jaremo et al. 1996).
Mutualism or antagonism: a brief retrospect Owen and Wiegert (1976) developed the hypothesis that "consumers like pollinators, have a mutualistic relationship with plants" and they proceeded by examining interactions between grasses and grazers in the context of their mutualism hypothesis. They suggested that grasses and grazers "have evolved mutualism to an extent that one group would not have been possible without the other" (Owen and Wiegert 1981). Owen and Wiegert (1981) further argued that grasses have a number of adaptations that have evolved as "responses to selection by grazers and which increase the fitness of individual grass plants". These adaptations include the position of basal meristems being out of reach to most grazers. the longevity of grasses, and their high palatability. However, the mutualism hypothesis was not originally formulated for explaining the evolution of plant compensatory regrowth following grazing, which was merely a possible instance of a general view of plant-herbivore interactions advocated by Owen and Wiegert (1981). The discovery of potential overcompensation in Ipomopsis aggregata (Paige and Whitham 1987) further fuelled the debate of plant-herbivore mutualism (e.g. Paige 1992, Vail 1992). Vail (1992) presented a mathematical model suggesting that "when herbivory is sufficiently strong and size selective, the optimal plant strategy is to withhold a large proportion of its reproductive resources against the possibility that an initial investment will be consumed. Under these conditions, plant fitness is enhanced by herbivory, and selection should favor plant traits that increase the probability of being eaten". However, the main question remains; if true, does this really imply a mutualism between grazed and grazers or not? McNaughton (1979, 1983) discussed more specifically plant-tolerance to ungulate grazing. His view of 314
grasses and grazers originates from observations of Serengeti grasslands and contrasts that of Owen and Wiegert (1981). According to McNaughton (1979), the net above-ground primary production of Serengeti grasslands is strongly regulated by grazing intensity. Moderate grazing by ungulate herbivores was found to stimulate the productivity of grassland plots up to twice the level of ungrazed control plots. From these findings he suggested that "the high grazing load of the Serengeti ecosystem has constituted strong selection on the plants for compensatory growth upon defoliation". However, as he later pointed out in his reply to Belsky (1986), his coevolutionary hypothesis neither implied that that "the mere act of herbivory is beneficial to any affected plant" (McNaughton 1986) nor that "the relationship between plants and herbivores is symbiotic by any conventional definition of that term" (McNaughton 1979, 1986). Although McNaughton's (1979, 1983, 1986) view of compensatory growth as a tolerance strategy against herbivores is not, in this respect, much different from that of Vail's (1992), he did not consider that the plant benejits from herbivory or that overcompensation is a mutualistic adaptation. Still, how can we otherwise interpret that fact that some plants actually increase vegetative productivity as well as seed production after herbivore encounters? We have presented these contrasting views following closely the original works because it is not at all obvious why McNaughton (1979, 1985, 1986) and Owen and Wiegert (1981) as well as Vail (1992) arrived at different interpretations of the same phenomena, and what is the crucial difference between their antagonistic coevolutionary and mutualism hypotheses, respectively. A reason for the discrepancy may be that they used plant fitness in different meanings. Owen and Wiegert (1981) explicitly stated that they use fitness in the relative meaning as "the contribution to the next generation of one genotype in a population relative to the contribution of others". Furthermore, they state that "by mutualism we mean the association of two, often unrelated organisms such that the relative fitness of both is higher than it would be if each existed by itself' (Owen and Wiegert 1987). McNaughton (1979: 698), on the other hand, applied both relative and absolute fitness when discussing the responses of grazingadapted plants to intensive herbivory: "the disappearance of A. greenwayi and of the other most dominant grasses from plots protected from grazing for several years indicates that they have comparatively higher fitness under intense grazing than other species, which become dominant when grazing was curtailed. This does not imply that the absolute fitnesses of the present dominants is enhanced by grazing". McNaughton (1979) thus seems to accept the antagonistic coevolutionary and not the mutualistic view because he asOIKOS 84 2 (1999)
selection. Our third fitness criterion is mean absolute fitness in the population, or w = p, W, p, W,. where p, is the frequency of phenotype i, W, is the absolute fitness of phenotype i, and i = A , N (cf. mean fitness, Maynard Smith 1989). We will simplify our analysis by assuming that if absolute fitness for an adapted phenotype exceeds that of a non-adapted ( W, > W,) then the frequency of adapted phenotypes increases until it dominates completely (p, = 1) The reversed situation (p, = 0) occurs when absolute fitness of non-adapted phenotypes IS larger than for adapted (W, > W,). Consequently, W = W, for p , = 1 and W = IV, for p , = O since p, + p , = 1. In the recent debate on overcompensation, the absolute fitness criterion seems to have had the most prominent role when discussing potential benefits of herbivory and plant-herbivore mutualism. The observation that grazed plants produce more seeds than ungrazed plants is thus considered as sufficient evidence for potential mutualistic interactions between plants and herbivores (Vail 1992). In his reply to a critique by Mathews (1994). Vail (1994) explained that in most studies of plant compensatory growth, mutualism refers to the usual ecological meaning of mutual positive interactions between organisms or populations. However, we may relate this ecological usage of the term to coevolutionary processes between plants and herbivores. It is in this context. where the proposed mutualistic adaptations are supposed to have evolved, that both Mathews (1994) and Tuomi et al. (1994) indicated that the absolute fitness criterion presented above is not sufficient for identifying the benefits of herbivory or mutualistic adaptations. They independently proposed that we have to distinguish ( I ) how well a given plant phenotype (or genotype) succeeds in grazed versus ungrazed conditions, and (2) how well a given grazingThree plant-animal relations adapted plant type manages in grazed conditions as We present three examples which all may, or may not, compared to non-adapted types in ungrazed conditions. be considered to represent a mutualistic relation be- i.e. examining mean absolute fitness. The first comparitween plants and animals. depending on what fitness son quantifies the compensatory capacity of the tested criterion we use. We will consider "relative fitness", plant type. while the second could be used to test "absolute fitness", and "mean absolute fitness" in each whether grazing is beneficial or detrimental for plants. We are interested in changes in the three plant fitness specific case. Absolute fitness ( W , ) quantifies the expected life-time reproductive success of plants that are measures above. in response to animal encounters. Un( i = A ) or are not (i = iV) adapted to encounter with der condition that relative fitness increases with probaanimals. In contrast, relative fitness is the absolute bility of animal encounters, there are three plausible fitness of a genotype scaled to the fitness of one geno- model situat~ons. referred to as cases A-C (Fig. 1). type which is reduced to unity (e.g. Roughgarden 1983. These cases differ qualitatively. They are naturally ideMaynard Smith 1989). In our case, the relative fitness alised and extreme situations. and in nature we may criterion comprises a comparison of the absolute fitness find a continuum of all possible intermediates. The first of a plant with our target trait (W,) under given case may suit plant-pollinator interactions, and the conditions relative to the absolute fitness of plants with second one corresponds to the general view of plant alternative traits (W,+,)u nder the same conditions. Se- defences in relation to herbivores. Case C represents a lection will favour the adapted plant type only if WWY; model of o\~ercompensationin relation to the risk of W, < 1, or W, > W,. If the absolute fitness is fiot damage. As we shall show below, the three cases differ higher for adapted type than for alternative pheno- from each other when taking all fitness criteria into types, the trait in question cannot evolve by natural consideration (Table 1). Note that in all cases we sumes that "while competitive fitness is enhanced by grazing, absolute fitness may be impaired in comparison to the ungrazed condition". According to him. selective advantage in terms of relative fitness does not suffice as a criterion for mutualistic coevolutionary adaptations. Consequently, there exist two contrasting views of the evolution of overcompensation in plants in relation to herbivory. On the one hand, overcompensation following grazing has been considered as an indication of mutualism between grazed plants and grazers. On the other hand, the mere fact that herbivores actually damage and remove tissue from plants makes it tempting for others to consider compensatory growth as a strategy to minimise the negative effects of damage. This strategy has evolved by an antagonistic coevolution, a game of hide and seek between grazers and grasses. comparable to the evolution of various plant defences. We take Mch'aughton's position in the sense that relative fitness is related to the evolution of plant traits by natural selection, but it does not provide any demarcation between mutualistic and antagonistic coevolution. In addition. one should make a clear distinction between absolute fitness of grazed plants and mean absolute fitness in the plant population. Grazing can improve absolute fitness of overcompensating plants, but mean absolute fitness may still decrease. We propose that mutualistic coevolution is associated with an increase in mean absolute fitness of plants, whereas antagonistic coevolution is characterised by a decrease in mean absolute fitness of plants as a function of probability of animal encounters.
+
specifically assume that the plant traits maintaining adaptations to pollinators or herbivores are costly for the plants, and hence such traits are selected against in the absence of animal encounters.
Case A: Mutualism In Fig. 1A we have illustrated the absolute fitness of plants in the presence as well as absence of animals. Hence. the fitnesses of adapted plants (solid line. Fig. IA) and non-adapted plants (broken line, Fig. 1A) are
Table 1. The change in various fitness measures in relation to increased risk of animal encouter in the three cases A-C (Fig. I ) discussed. Case
A. Plant-pollinator model
B. Plant defence model
C. Overcompensation model
Fitness criteria Relative
Absolute
Mean absolute
+ + +
+
+
-
-
+
-
drawn as functions of risk of animal encounter ( m ) . In the absence of animals (m = 0), adaptive structures are costly ( W,,, < W.,,, Fig. IA). However, as the probability of encountering animals increases, the benefits in absolute fitness increase (W,, > W,,, Fig. 1A). Moreover, the fitness of adapted plants relative the fitness of other plants which d o not carry the costly traits increases with m (W,, > W,,, Fig. 1A) which is a prerequisite for the evolution of such adaptations. Since a high risk of animal encounter implies a higher absolute fitness for an animal-adapted plant than an unadapted plant can achieve even under conditions of total animal absence (W,, > W,,), mean absolute fitness increases with m. If n7 is to the left of the intersection between the two lines in Fig. IA, the population will eventually consist of only non-adapted plants (p, = 0) and @= W,,. If m is to the right of the critical point, the population will be dominated by animal-adapted phenotypes (p, = 1) and w= w,,. This is a consequence of our assumption of no polymorphisn~sin this idealised system. Hence, irrespective of fitness criterion, animal encounters have a positive effect on plant fitness (Table 1). The result may be a mutualistic relation where the plants are better off as the animal population increases whilst the animals are better off as the plant population increases. A plant-animal interrelationship as the one described in case A may be found among flowering plants and their pollinators. Generally, the relationship between flowering plants and pollinators is considered advantageous to both, and selection is expected to favour, on the one hand, plants with special adaptations to encourage pollinators and, on the other hand, pollinators with adaptations to find plants with pollinator-specific traits. Those special adaptations are flowers with signals and the production of nectar which limits pollen predation and attracts insects. ~ h e s ereciprocal adaptations suggest mutualistic coevolution. but it may well have started as an antagonistic relation
Fig. 1. The absolute fitness (U.3 of adapted (solid line) and non-adapted (dotted line) plants as function of risk of animal encounter ( m ) . Three hypothetical cases are shown (A) plantpollinator system where pollinators benefit the adapted plants attracting pollinators, (B) plant-herbivore system where herbivores consume less the adapted plants which have evolved effective mechanical or chemical defences, and (C) plant-herbivore system where the adapted plants overcompensate for (pollen predation) that gradually changed to the benefit grazing damage. of plants
Case B: Antagonism In case B, the absolute fitness of a non-adapted plant decreases as the risk of animal encounter increases (W,, < W,,, solid line; Fig. IB), and so does that of animal-adapted plant (W,,, < W.,. broken line; Fig. 1B). However, the absolute fitness of an adapted plant does not decrease with probability of animal encounter as much as that of the non-adapted one, implying that relative fitness increases (W,, > W,,: Fig. 1B). The absolute fitnesses are negatively influenced by interactions with animals, and so is the case when considering mean absolute fitness (W,,, < W,,,: Fig. 1B). It is obvious that we are in this case dealing with some kind of plant defence strategy against herbivores. Both the absolute and mean absolute fitness decreases, indicating that animal encounters are detrimental for plants. This is the general view of the ecological context where plant defence strategies should evolve in order to repel herbivores and to reduce the damage made by herbivores. Since phenotypes without any anti-herbivore adaptations are more vulnerable to herbivores, the relative fitness of adapted plants increases with risk of herbivore interaction which thus promotes the evolution of anti-herbivore adaptations (e.g. Tuomi and Augner 1993). This example is important because it clearly demonstrates that relative fitness does not provide a sufficient basis for a demarcation between antagonistic and mutualistic coevolution. If we only consider this fitness criterion, following Owen and Wiegert (1981). then almost all herbivore-adapted plant types would live in an obligate mutualism with herbivores. Instead, antagonistic interactions are here suggested by the fact that the absolute fitnesses of the different plant types and the mean fitness in the popula. tion decrease with risk of animal encounters. his makes a clear distinction between this example of plant defences and our earlier model of plant-pollinator interactions (cases A and B. Table 1).
C. First, the increase of absolute fitness of the adapted plant type indicates overcompensation capacity (Fig. 1C). This is consistent with the design of empirical studies (e.g. Paige and Whitham 1987, Paige 1992. 1994) where the productivity of damaged plants that are adapted to herbivory is compared to undamaged ones of the same phenotype. That is the same as comparing the two end points of the solid line in Fig. 1C and, hence, only the absolute fitness criterion is taken into consideration. Second, the increase of relative fitness as a consequence of the encounter with herbivores is necessary for the evolution of overcompensation if it implies costs for the plants in the absence of herbivores. In the case C , the adapted plant type achieves a selective advantage over the non-adapted ones because it tolerates better damage caused by herbivores. This is consistent with Belsky et al. (1993), but we do not consider relative fitness as a proper way to quantify plant compensatory responses which should be done on the basis of absolute fitness as suggested above. Third, there is a question of benefits of her~nteractions.Vail (1992) equated bivory or mutual~st~c overcompensation and the benefits of herbivory. In Fig. 1C. the absolute fitness of the adapted phenotype increases with herbivore encounter and one should, following Vail (1992). then identify the relationship as mutualistic. However. considering the mean absolute fitness criterion (Mathews 1994, Tuomi et al. 1994), fitness decreases with herbivore encounter (Fig. 1C). That is, ungrazed plants without any special adaptations to herbivory have higher fitness than grazed overcompensating plants. Thus. using the mean absolute fitness criterion. this s~tuationis. in this respect. comparable to the antagonism of the case B (Table 1).
-
Case C: Plant life between mutualism and antagonism The case C presents a combination of the two earlier models. As in the case of mutualism, the absolute fitness of adapted phenotypes increases with animal interactions (W,, > W,,; Fig. 1C). The difference to the case A is the decrease of mean absolute fitness with risk of animal encounter (W,, > W,,; Fig. 1C). Hence, animal interactions have a positive impact on absolute fitness of adapted plants whilst it has negative implications on mean absolute fitness (Table 1). The latter trend is similar to the case B which we characterised as antagonism. Tuomi et al. (1994) suggested that overcompensation might well have evolved in a context similar to our case
Discussion Above we have described three plant-animal relations whose differences and similarities are surnmarised and presented in Table 1. When using the relative fitness criterion on plants that interact with animals, then obviously the plants that have ways of dealing with animals are better off. The increase in relative fitness when encountering herbivores is seen as W,, > WdV,in all three cases. This is however a trivial result as none of the special adaptations considered in this paper would exist otherwise. When using the "absolute fitness" criterion; we come closer to what is studied in most empirical tests on overcompensation (e.g. Paige and Whitham 1987, Paige 1992. 1994, Lennartsson et al. 1997). Also here, in an ecological sense, plants benefit from animal encounters in the case A and also in the case C which would thus indicate plant-herbivore mutualism in the case of overcompensation. How-
ever, we have taken also a third criterion into consideration, that of mean absolute fitness. When doing so, only in case A plants have a positive interaction with animals (Table I). Mutualism is characterised by two species or two individuals that interact in a way that is beneficial to both, i.e. there is a ( + , + ) relation between them. It seems as the definitions of mutualism on species level and on individual level coexist (Boucher et al. 1982). However, the definition of the term itself does not account for a coevolutionary history between the two participants in the interaction. It only describes the present effects of one interactor on the other and vice versa. The past and the future of the interrelation are unknown, uninteresting, and, above all, the nature of it is probably changing over a n evolutionary time-scale. Consequently, the ecological usage of the term mutualism may well justify the conclusions of Paige (1992, 1994) and Vail (1992, 1994). The situation changes when we discuss the terms "mutualistic coevolution" or "mutualistic adaptations". Following the above line of reasoning, a necessary, but as such probably not sufficient, requirement for mutualistic coevolutionary adaptations might be that (1) the given trait improves relative fitness as compared to other alternative plant traits in grazed conditions (relative fitness criterion), (2) the trait increases absolute fitness of grazed plants as compared to ungrazed plants (absolute fitness criterion), and that (3) mean absolute fitness increases with increased intensity of interactions. The first requirement is needed in order to allow the trait to evolve by natural selection, and the second one is necessary for the trait to be beneficial to the animaladapted plant in the presence of animals. The third requirement comprises the two others in an evolutionary perspective in that it considers phenotypes in conformity with their environment and compare their fitnesses in this context. It would be extremely interesting to compare empirical data on overcompensation to our three models in the context of various fitness criteria as outlined above. As far as we know, only one study supplies the data required for such a presentation. Lennartsson et al. (1997) monitored compensatory responses of the field gentian, Gentianella campestris (L.) Borner (Gentianaceae), by comparing fruit and seed production of clipped and unclipped plants in common garden experiments. They found five overcompensating populations that were late-flowering and originated from grazed or mown semi-natural grasslands. Three late-flowering populations from outside grazed or mown habitats did not overcompensate. In Fig. 2, we have compared the fruit production of overcompensating ("grazingadapted plants") and non-overcompensating ("nonadapted plants") populations when the plants are
clipped (m = 1) or not ( m = 0). The response patterns of the two plant types are similar to our postulated case C (Fig. 1C). First, fruit production of plants from nonovercompensating populations tends to decrease with clipping. Second, fruit production of plants from overcompensating populations increases following clipping (Lennartsson et al. 1997; cf. W,, > W,, in Fig. 1C). However, the question over antagonism versus mutualism is less clear cut. We have assumed, following Tuomi et al. (1994), that the non-adapted type still has a higher absolute fitness in the absence of herbivores than the adapted type in the presence of herbivores, i.e. W,,,> WA, in Fig. IC. That is, the situation would be similar to the case B of antagonistic coevolution, while mutualism would assume the reverse pattern, i.e. W,, < WAl (Fig. 1A). These possibilities require that the statistical null hypothesis W,,, = W,, can be rejected. We tested this by comparing unclipped plants from non-overcompensating populations (n = 3) and clipped plants from overcompensating populations (n = 5), but could not reject the null hypothesis of equal fruit production (Mann-Whitney Us = 13; p = 0.1). That is, the data indicate neither strong antagonism nor any substantial benefits of being grazed. Because our sample size is small (8 populations), and one could argue that, if there is any pattern in Fig. 2, it is closer to the mutualism than the antagonism hypothesis. A counterargument in favour of the antagonism hypothesis is that the present estimate of W,,,, may not present an appropriate phylogenetic control or an ancestral phenotype which has not been adapted to grazing andior mowing. Note further that the compensation responses of G. campestris vary depending on timing of damage (Lennartsson et al. 1998). degree of damage
Fig. 2. The mean fruit production ( W) of the field gentian, G. campestris, in overcompensating (solid line, n = 5) and nonovercompensating (dotted line, n = 3) populations as function of risk of artificial damage ( m ) . Unclipped plants: m = 0; clipped plants: HZ = 1. The vertical bars Indicate standard errors. As a comparison, see Fig. 1C and also Fig. IA.
(Huhta et al. unpubl.), and plant size (Lennartsson unpubl.). In Fig. 2, sufficiently large, late-flowering plants were moderately damaged (50% of aboveground biomass being removed) in mid-July, i.e. in conditions which appear to be most favourable for regrowth in this species. However, for the present purposes our empirical example suffices because it demonstrates that the cases A-C (Fig. 1 ) are, at least in principle, empirically testable hypotheses and that such tests would require appropriate phylogenetic controls. In conclusion, the use of fitness criteria is crucial when identifying ecological interactions. For instance, the relative fitness concept implies a mutualism between species or taxa whenever phenotypes with a specific trait that is related to interactions have evolved. Obviously, this criterion is too weak. Absolute fitness is a handy and measurable criterion that is of use when outlining the interactions between species on an ecological time-scale. Differences in absolute fitness provide the driving force of evolution by natural selection, but may not help in attempts to classify various kinds of plant-animal interactions in coevolutionary contexts. We have tried to highlight this problem with the three examples in this essay. In contrast to the concepts of relative and absolute fitness, mean absolute fitness may provide a possibility to outline the history behind what we today see as mutualism or antagonism. In other words, when it comes to plant-animal interactions, mean absolute fitness makes a clear separation of adaptations that originate from "mutualistic plant-animal interactions" and adaptations that are consequences of "antagonistic plant-animal interactions". We cannot. however, ignore the possibility that this criterion may be more valuable for theoretical studies than for empirical purposes. It should also be noticed that we have discussed only the potential effects of herbivores on plant fitness and not the effect of plant adaptations on herbivores. For instance. we d o not know any study where overcompensation is shown to benefit herbivores or that, for instance, overcompensating plants were more palatable to herbivores than non-overcompensating plants. This was a major expectation of Vail's (1992) mutualism argument as cited above: "Under these conditions, plant fitness is enhanced by herbivory. and selection should favor plant traits that increase the probability of being eaten". Therefore, the criteria we have presented here provide at best necessary conditions for mutualism and antagonism in evolutionary contexts. This also casts doubts that strong generalisations should be avoided on the basis of the general classification of ecological interactions from mutualism to parasitism. The effects of one species on another can vary both quantitatively and qualitatively in time and space (e.g. Johnson et al. 1997), and that. hence, the generalisations may be especially misleading when applied to entire organism groups. such as plants and herbivores. OIKOS 84 2 (1999)
Ackno~rledgenzents - We would like to thank S. Vail for valuable comments. The study was financially supported by grants from the Swedish Natural Science Research Council and the Academy of Finland.
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