Juha Tuomi

Nutrient stress: an explanation for plant anti-herbivore responses to defoliation

SummaryA hypothesis is put forward that the long-lasting inducible responses of trees to herbivores, particularly lepidopteran defoliators, may not be active defensive responses, but a by-product of mechanisms which rearrange the plant carbon/nutrient balance in response to nutrient stress caused by defoliation. When defoliation removes the foliage nutrients of trees growing in nutrient-poor soils, it increases nutrient stress wich in turn results in a high production of carbon-based allelochemicals. The excess of carbon that cannot be diverted to growth due to nutrient stress is diverted to the production of plant secondary metabolites. The level of carbon-based secondary substances decays gradually depending on the rate at which nutrient stress is relaxed after defoliation. In nutrient-poor soils and in plant species with slow compensatory nutrient uptake rates the responses induced by defoliation can have relaxation times of several years. The changes in leaf nitrogen and phenolic content of mountain birch support this nutrient stress hypothesis. Defoliation reduces leaf nitrogen content while phenolic content increases. These responses of mountain birch to defoliation are relaxed within 3–4 years.

Genetic structure and gene flow in a metapopulation of an endangered plant species, Silene tatarica

We investigated the distribution of genetic variation within and between seven subpopulations in a riparian population of Silene tatarica in northern Finland by using amplified fragment length polymorphism (AFLP) markers. A Bayesian approach‐based clustering program indicated that the marker data contained not only one panmictic population, but consisted of seven clusters, and that each original sample site seems to consist of a distinct subpopulation. A coalescent‐based simulation approach shows recurrent gene flow between subpopulations. Relative high FST values indicated a clear subpopulation differentiation. However, amova analysis and UPGMA‐dendrogram did not suggest any hierarchical regional structuring among the subpopulations. There was no correlation between geographical and genetic distances among the subpopulations, nor any correlation between the subpopulation census size and amount of genetic variation. Estimates of gene flow suggested a low level of gene flow between the subpopulations, and the assignment tests proposed a few long‐distance bidirectional dispersal events between the subpopulations. No apparent difference was found in within‐subpopulation genetic diversity among upper, middle and lower regions along the river. Relative high amounts of linkage disequilibrium at subpopulation level indicated recent population bottlenecks or admixture, and at metapopulation levels a high subpopulation turnover rate. The overall pattern of genetic variation within and between subpopulations also suggested a ‘classical’ metapopulation structure of the species suggested by the ecological surveys.

INDUCTION OF OVERCOMPENSATION IN THE FIELD GENTIAN, GENTIANELLA CAMPESTRIS

We present field evidence for the induction of overcompensation, or increased fruit and seed yield as a consequence of damage, in the grassland biennial field gentian, Gentianella campestris (Gentianaceae). We compared equally sized clipped and unclipped plants in two populations in central Sweden during three years, 1992-1994, and plants clipped at different occasions, from 20 June to 2 August. Clipping once, by removing half of the biomass, significantly increased fruit production without affecting the number of seeds per fruit or seed mass. The degree of compensation was sensitive to the timing of clipping. Damage induced overcompensation only during a restricted inductive time period (ITP) in July. Plants clipped before about 1 July or after about 22 July achieved no overcompensation. The early limit of ITP was presumably determined by the availability of resources that could be mobilized for regrowth after damage. The late limit, on the other hand, depended primarily on the differentiation of meristems close to flowering in early August. The effects of clipping varied between years, presumably due to drought in 1994. During 1992-1993, plants consistently overcompensated for clipping on 1-20 July, whereas in 1994 only early clipping from 1 to 12 July induced overcompensation. In 1994, plants clipped in late July compensated less well, due to delayed fruit maturation leading to a high proportion of immature fruits at the end of the season. Because of this between-year variation, we used geometric mean fitness to calculate the expected long-term effects of damage over generations. The analysis suggests that the long-term effects can vary from positive to negative, depending on the frequency of bad fruiting years. The time limits of ITP fit well the hypothesis that predictable damage in July may have selected for a capacity of overcompensation in the field gentian. Because the ultimate limits of ITP are set by the length of the vegetation period, we expect overcompensation in this species to be more common in regions with a longer growing season.

EVIDENCE FOR AN EVOLUTIONARY HISTORY OF OVERCOMPENSATION IN THE GRASSLAND BIENNIAL GENTIANELLA CAMPESTRIS (GENTIANACEAE)

Swedish University of Agricultural Sciences, Department of Conservation Biology, Section of Conservation Botany, Box 7072, 750 07 Uppsala, Sweden; University of Oulu, Department of Biology, Linnanmaa, 90 570 Oulu, Finland, and University of Lund, Department for Theoretical Ecology, Ecology Building, 223 62 Lund, Sweden; University of Lund, Department for Theoretical Ecology, Ecology Building, 223 62 Lund, Sweden

Defensive Responses of Trees in Relation to Their Carbon/Nutrient Balance

Haukioja and Hakala (1975), Rhoades (1979), and Haukioja (1980) outlined the hypothesis that herbivore cycles are associated with changes in the inducible defense level of individual plants. For example, the herbivore population’s increase begins when host-plant resistance decreases to a low level. On the other hand, the herbivore population’s decrease is precipitated by an increasing plant resistance. The minimum length of the latent phase depends on the rate of relaxation of resistance as the plant recovers from defoliation (May 1975, Haukioja 1980). Although the detailed mechanisms of these changes in plant resistance are still unclear, defoliation has been shown to induce changes in trees that have adverse effects on the growth, reproduction, and survival of lepidopteran defoliators (Haukioja and Niemela 1977, Wallner and Walton 1979, Werner 1979, Haukioja 1980) and which can have relaxation times of several years (Benz 1974, Haukioja 1982). However, in other cases, defoliation caused no observable increase in plant resistance (Myers 1981), and defoliation may even reduce resistance of the host plant (Niemela et al. 1984). Furthermore, no evidence for defensive responses to clipping was found in dormant twigs of juvenile woody plants when twig age and diameter were controlled (Chapin et al. 1985).

Plant Compensatory Responses: Bud Dormancy as an Adaptation to Herbivory

Some plants can compensate, and even overcompensate, for the loss of productivity caused by herbivory. The presence of latent meristems, or dormant buds, is one of the basic prerequisites of such compensation mechanisms. We present a mathematical model in order to analyze compensation responses in relation to the intensity of herbivory. The model generates a number of qualitatively different kinds of compensation curves when seed production is plotted against the proportion of active meristems lost per grazed plant. The shape of the curves depends on the proportion of dormant buds and their activation sensitivity in relation to meristem loss. Overcompensation is most probable when dormant buds are easily activated. When plants are grazed only once, as assumed in our model, selection favors high bud sensitivity. However, we expect that repeated damage may select for a more restrained pattern of bud activation. When relatively few buds remain dormant, plants can overcompensate for low levels of damage only. On the other hand, when most buds remain dormant, they can overcompensate even for high levels of damage. We consider compensation capacity a potential benefit of bud dormancy when plants are subject to damage. However, bud dormancy may also imply costs on plant productivity and fecundity in the absence of herbivory. Still, intense herbivory may favor bud dormancy in spite of the potential costs. Selection for bud dormancy requires both that the risk of herbivory is high and that herbivores remove a large fraction of active meristems per plant. Consequently, overcompensation is a theoretically plausible possibility, and intense herbivory is a potential selective force that favors bud dormancy. None of these results, however, imply that herbivory is beneficial to plants. In our case, plants with bud dormancy never have higher seed production than plants that have no dormant buds and that are not grazed.

Evolution of heterospecific attraction: using other species as cues in habitat selection

We analyzed the ecological conditions that may favor a habitat selection process in which later arriving individuals (colonists) use the presence of earlier established species (residents) as a cue to profitable breeding sites (heterospecific attraction). In our model, colonists assessing potential breeding patches could select between high-quality source and low-quality sink patches. A proportion of the source patches were occupied by residents. Colonists could either directly sample the relative quality of the patches (termed samplers) or, alternatively, they could also use residents as a cue of patch quality (cue-users). Cue-users gained benefit from lowered costs when assessing occupied source patches. The cue-using strategy is an efficient way to choose the best possible patch not only when interspecific competition is intense, but also when benefits from social aggregation exceed the effects of competition. High relative cost of sampling empty patches increases the fitness of the cue-using strategy relative to samplers. The strongest attraction to heterospecifics was predicted when the benefit from aggregating with residents exceeded the effects of competition, and approximately half of the landscape consisted of occupied, high-quality source patches.

Associational effects of plant defences in relation to within- and between-patch food choice by a mammalian herbivore: neighbour contrast susceptibility and defence.

A basic idea of plant defences is that a plant should gain protection from its own defence. In addition, there is evidence that defence traits of the neighbouring plants can influence the degree of protection of an individual plant. These associational effects depend in part on the spatial scale of herbivore selectivity. A strong between-patch selectivity together with a weak within-patch selectivity leads to a situation where a palatable plant could avoid being grazed by growing in a patch with unpalatable plants, which is referred to as associational defence. Quite different associational effects will come about if the herbivore instead is unselective between patches and selective within a patch. We studied these effects in a manipulative experiment where we followed the food choice of fallow deer when they encountered two patches of overall different quality. One of the two patches consisted of pellets with low-tannin concentration in seven out of eight buckets and with high concentration in the remaining bucket. The other patch instead had seven high- and one low-tannin bucket. We performed the experiment both with individuals one at a time and with a group of 16–17 deer. We found that the deer were unselective between patches, but selective within a patch, and that the single low-tannin bucket among seven high-tannin buckets was used more than a low-tannin bucket among other low-tannin buckets. This corresponds to a situation where a palatable plant that grows among unpalatable plants is attacked more than if it was growing among its own kind, and for this effect we suggest the term neighbour contrast susceptibility, which is the opposite of associational defence. We also found that the high-tannin bucket in the less defended patch was less used than the high-tannin buckets in the other patch, which corresponds to neighbour contrast defence. The neighbour contrast susceptibility was present both for individual and group foraging, but the strength of the effect was somewhat weaker for groups due to weaker within-patch selectivity.

Tolerance of Gentianella campestris in relation to damage intensity: an interplay between apical dominance and herbivory

Meristem allocation models suggest that the patterns of compensatory regrowth responses following grazing vary, depending on (i) the number of latent meristems that escape from being damaged, and (ii) the activation sensitivity of the meristems in relation to the degree of damage. We examined the shape of compensatory responses in two late-flowering populations (59°20′N and 65°45′N) of the field gentian. Plants of equal initial sizes were randomly assigned to four treatment groups with 0, 10, 50 and 75% removal of the main stalk. The plants were clipped before flowering, and their performance was studied at the end of the growing season. The northern population showed a linear decrease in shoot biomass and fecundity with increasing biomass removal, while the response in the southern population was quadratic with maximum performance at the damage level of 50% clipping. This nonlinear shape depended upon the activation sensitivity of dormant meristems in relation to their position along the main stem. The highest plant performance was achieved by inflicting intermediate damage which induced regrowth from basally located meristems. In contrast, the topmost branches took over the dominance role of the main stem after minor apical damage (10% clipping). Consequently, the breakage of apical dominance is a necessary precondition of vigorous regrowth in this species. However, compensation in the field gentian is unlikely to be a mere incidental by-product of apical dominance. The ability to regrow from basally located meristems that escape from being damaged by grazing may well be a sign of adaptation to moderate levels of shoot damage.

Induced Accumulation of Foliage Phenols in Mountain Birch: Branch Response to Defoliation?

Plant phenols are frequently considered unspecific defensive substances that protect plants against herbivores (Feeny 1970, 1976). Although the lack of specificity of phenolic compounds (Zucker 1983) and their protein-precipitation efficiency in vivo (Bernays 1981) have been questioned, ecological evidence suggests that phenolic compounds can function as a potential chemical defense against some folivorous insects. These compounds have adverse effects on lepidopteran larvae (Feeny 1968; Lincoln et al. 1982), and they are abundant in tissues most susceptible to attacks by herbivores (McKey 1979). Phenolic compounds can also be induced to accumulate in foliage in response to leaf damage and defoliation (Levin 1971; Schultz and Baldwin 1982; Wagner and Evans 1985; Bergelson et al. 1986; Faeth 1986). In mouintain birch, Betula pubescens ssp. tortuosa (Ledeb.) Nyman, phenols have been observed to accumulate in current foliage shortly after adjacent leaves have sustained damage (Niemela et al. 1979) and as long as 3-4 yr after the entire tree had been defoliated (Tuomi et al. 1984). Both kinds of inducible responses in mountain birch foliage are also associated with retarded larval growth of the natural defoliator Epirrita autumnata (Haukioja and Niemela 1977, 1979; Haukioja 1980, 1982); foliage phenols are therefore at least potentially defensive characteristics of birch trees (Haukioja et al. 1985a). A tacit assumption in plant-herbivore studies seems to be that the presence of phenols and other potentially defensive secondary compounds in plant tissues is an adaptation for maximizing the fitness of whole individual plants (Janzen 1974; Rhoades and Cates 1976; Haukioja and Niemela 1976; Rhoades 1979). Since individual plants should therefore be the actively responding units, the cues indicating an increased risk of herbivory should trigger an induced production of secondary substances in the entire plant (Rhoades 1979; Haukioja and Neuvonen 1985). In this study, we tested whether phenolic accumulation can be induced separately in individual branches of mountain birch. The study was carried out at the Kevo Subarctic Research Institute of the University of Turku in northern Lapland. We examined separate branches on 10 birch trees (2.5-3.5 m in height) growing on the same hill, Puksalskaidi. Five branches per tree were manually defoliated after leaf flush (June 20, 1985) and the other five branches later toward the end of the growing season (August 17, 1985). Foliage phenols (Folin-Denis method) and total nitrogen (H-N-C analyzer) were determined for samples of mature leaves collected (July 26, 1986) from the recovered, previously defoliated branches and untreated control branches. We made a pairwise comparison of branches of the same trees, and the mean con-