Simultaneous evolution of competitiveness and defense: induced switching in Arabis drummondii

Optimality theory for plant defense against herbivores predicts an evolutionary tradeoff between the abilities to compete and defend. We tested this hypothesis by studying the effects of genetic variation in competitiveness on defense expression. Two closely related and differentially competitive congeners were compared for levels of resistance, tolerance, and secondary metabolite production. In a growth room experiment, plants of Arabis drummondii and A. holboellii were grown in the presence and absence of the common bunch grass Boutelloua gracilis, the specialist herbivore Plutella xylostella, and generalist herbivore Trichoplusia ni. Tolerance to competition, measured as growth next to the grass relative to controls in the absence of grass, was greatest for A. drummondii, the species that occurred in communities with higher densities of inter-specific neighbors. Measures of defense (resistance to herbivores, tolerance to damage, and concentrations of glucosinolates) varied inconsistently between the Arabis, species, depending on type of herbivore, competition level, and type of defense. The better competitor A. drummondii was more resistant to specialist herbivores, as in the field, and exhibited greater herbivore- and competition-induced changes in glucosinolate profiles. Further, when plants of A. drummondii were fed upon in competitive environments, the induced glucosinolate response was reduced while tolerance levels increased in an apparent switching of induced strategies. We suggest that competitiveness and defense responses are sometimes positively correlated because some defensive traits also function as competitive traits. A competitive function for defenses may also explain why defenses were affected by competition. Alternatively, since the induced response did not increase estimates of total glucosinolate content significantly, minimal defense costs might also allow the simultaneous evolution of competitiveness and defense. Finally, when faced with both herbivory and competition, some competitive species, such as A. drummondii, may switch to growth-based rather than toxin-based strategies as recent theoretical models predict.     

Costs and benefits of induced resistance in a clonal plant network

Plant defense theory suggests that inducible resistance has evolved to reduce the costs of constitutive defense expression. To assess the functional and potentially adaptive value of induced resistance it is necessary to quantify the costs and benefits associated with this plastic response. The ecological and evolutionary viability of induced defenses ultimately depends on the long-term balance between advantageous and disadvantageous consequences of defense induction. Stoloniferous plants can use their inter-ramet connections to share resources and signals and to systemically activate defense expression after local herbivory. This network-specific early-warning system may confer clonal plants with potentially high benefits. However, systemic defense induction can also be costly if local herbivory is not followed by a subsequent attack on connected ramets. We found significant costs and benefits of systemic induced resistance by comparing growth and performance of induced and control plants of the stoloniferous herb Trifolium repens in the presence and absence of herbivores.     

Competitive impacts and responses of an invasive weed: dependencies on nitrogen and phosphorus availability

Changes in competitive interactions under conditions of enhanced resource availability could explain the invasion success of some problematic plant species. For one invader of North American grasslands, Centaurea diffusa (diffuse knapweed), we test three hypotheses: (1) under ambient (high resource) conditions, C. diffusa is better able to tolerate competition from the resident community (competitive response), (2) under ambient conditions, C. diffusa strong impacts the competitive environment (competitive effect), and (3) reductions in nitrogen and/or phosphorus availability diminish these advantages. In support of our first hypothesis, C. diffusa was the most tolerant to neighbor competition of the four focal species under current resource conditions. In opposition to our second hypothesis, however, neighborhoods that contained C. diffusa and those where C. diffusa had been selectively removed did not differ in their impact on the performance of target transplant individuals or on resource conditions. Reduction in resource availability influenced competitive tolerance but not competitive impact, in partial support of our last hypothesis. Reduction in soil nitrogen (via sucrose carbon addition) enhanced the degree of neighbor competition experienced by all species but did not change their relative rankings; C. diffusa remained the best competitor under low nitrogen conditions. Reduction of soil phosphorus (via gypsum addition) weakened the ability of C. diffusa to tolerate neighbor competition proportionately more than the other focal species. Consequently, under low phosphorus conditions, C. diffusa lost its competitive advantage and tolerated neighbor competition similarly to the other focal species. We conclude that C. diffusa invasion may be double-edged: C. diffusa is less limited by nitrogen than the other focal species and is better able to utilize phosphorus to its competitive advantage.     

Competitive dominance among Cladocera: Are single-factor explanations enough?

I examine several hypotheses for competitive dominance among zooplankton using data from 20 studies containing field and laboratory experiments on competition between cladoceran species. In threeDaphnia species from rockpools studied in the laboratory, the largeD. magna was the superior competitor at higher food levels and at 15°, while the smallerD. pulex andD. longispina were dominants at low food levels at 20°.D. pulex usually excludedD. longispina. No single-factor hypothesis gives a satisfying explanation for these results. A review of the literature data suggests that none of the following hypotheses for competitive dominance have sufficient support to be considered general: The size-efficiency hypothesis (supported in 60% of the tests), ther-max hypothesis (68% support), efficiency at low food levels (36% support), and that small species are superior competitors (only 17% support). Competitive ability and susceptibility to predation appear to be positively related (9 out of 10 cases). 76% of the experiments carried out under different environmental conditions showed varying outcomes. Competition between cladocerans should evidently be studied within a multi-factor framework. Since shifts in competitive advantage with environmental changes were common, the competitive exclusion principle may often not apply in zooplankton assemblages. Non-equilibrium coexistence of competitors in a variable environment, i.e. the paradox of the plankton, is a framework worthy of consideration in zooplankton, and possibly also in many other natural communities.     

Resistance and tolerance in <Emphasis Type="Italic">Populus tremuloides</Emphasis>: genetic variation,costs, and environmental dependency

Plants defend themselves against herbivores via resistance, which reduces damage, and tolerance, which minimizes the negative effects of damage. Theory predicts the existence of tradeoffs between defense and growth, as well as between resistance and tolerance, that could maintain the genetic variation for resistance and tolerance often observed in plant populations. We examined resistance and tolerance among aspen (Populus tremuloides) trees grown under divergent soil nutrient regimes. This common garden experiment revealed substantial genetic variation for resistance and tolerance under both low- and high-nutrient conditions. Costs of resistance exist, particularly under high-nutrient conditions where allocation to resistance chemicals competes directly with growth for limited carbon resources. We found no significant costs of tolerance, however, under either nutrient condition. Despite genetic variation for both resistance and tolerance, we found no evidence for a tradeoff between these two defense traits suggesting that resistance and tolerance are complementary, rather than mutually exclusive, defenses in aspen.     

Myrmecophytic Cecropia: antiherbivore defenses under different nutrient treatments

In greenhouse experiments, we compared putative biotic, chemical, physical and phenological defenses of six myrmecophytic Cecropia species cultivated under high and low nutrient regimes. We tested the intraspecific predictions of the C:N balance hypothesis for a broader range of defenses than included in other studies to date. Treatment effects on defenses appear to depend on the nutrient constituents of those defenses. Only strictly carbon-based defenses such as tannins and phenolics reached higher concentrations at the lower nutrient level. The production of glycogen-rich and membrane-bound Müllerian body ant rewards (MBs) increased with greater levels of both nutrients (this study) and light (Folgarait and Davidson 1994). In contrast, lipid- and amino acid-rich pearl body food rewards (PBs) were produced in greater numbers under conditions of high nutrient levels (this study) and low light (Folgarait and Davidson 1994), both of which should have contributed to a relative excess of nitrogen. Nutrient effects on toughness and leaf expansion rates (perhaps serving as phenological defenses) were inconsistent with the predictions of the C:N balance hypothesis. Mature leaves are protected principally by chemical and physical defenses, and new leaves, by biotic defenses. As in a previous study, interspecific comparisons agreed with the resource availability theory of plant defense. Plant investment in immobile defenses (tannins and phenolics, and leaf toughness), and in a defense with high initial construction costs (trichilia differentiated to produce MBs) were greater in each of three comparatively slow-growing gap Cecropia typical of small openings in primary forest, than in closely related and fast-growing pioneer species of large-scale disturbances (riparian edge and land slips). In contrast, both production of PBs (with negligible initial construction costs) and leaf expansion rates were greater in pioneers than in gap species. Rapid onset of biotic defenses during new leaf development (earlier in pioneers) may reduce new leaf herbivory in all species.     

Nitrogen and water affect direct and indirect plant systemic induced defense in cotton

Plants have direct and indirect constitutively produced and inducible defenses against herbivores and pathogens, which can substantially aid in their ability to defend themselves. However, very little is known about the influence of agronomic factors on such defenses. Here, we tested the effects of nitrogen levels and water availability on the ability of cotton plants to deter feeding by Spodoptera exigua through induction of anti-feedants, and to attract Microplitis croceipes through systemic induction of volatile emission. Cotton plants were grown with various nitrogen levels and were either exposed to water stress or normal water before being exposed to S. exigua for 48 h for induction of defenses. Dual choices of various nitrogen and water treatments were provided to M. croceipes in flight tunnel bioassays. Dual choices of leaf tissue from the various nitrogen and water treatments were provided to S. exigua larvae. Both water stress and nitrogen levels under and over the recommended levels increased leaf tissue consumption and decreased attraction of M. croceipes to the plants. Analyses of induced volatiles released from herbivore damaged plants indicate that their concentrations differ among the nitrogen levels tested with plants receiving no nitrogen or twice the recommended dose having amounts much lower than plants receiving the recommended dose. Because both direct and indirect plant defense mechanisms are negatively affected by improper nitrogen and insufficient water, we argue that these factors should be considered for a better natural control of pests in cotton and most probably in other crops.     

Nitrogen addition does not reduce belowground competition in a salt marsh clonal plant community in Mississippi (USA)

Previous studies have suggested that belowground competition for nutrients influences plant zonation in salt marshes. In this study, I tested the hypothesis that competition for nitrogen structured a clonal plant community in a nitrogen-limited salt marsh in coastal Mississippi, USA. In contrast to most previous field studies that have investigated mechanisms of competition, I examined clonal growth responses of established genets of a nitrogen-demanding low-intertidal species (Spartina alterniflora) to nitrogen addition and the removal of a nitrogen-conserving high-intertidal species (Juncus roemerianus). Nitrogen addition stimulated clonal invasion of the Juncus zone by Spartina but did not reduce the significant competitive effects of Juncus on Spartina. Simulated Juncus shade did not reduce invasion of the Juncus zone by Spartina, indicating that belowground competition reduced clonal invasion. In the last year of the study, the border shifted unexpectedly towards the Spartina zone, resulting in competitive displacement of Spartina by Juncus. Nitrogen addition did not prevent or slow this displacement, further contradicting the nitrogen competition hypothesis. Although growth rates were much more strongly limited by nitrogen in Spartina than in Juncus, nitrogen addition did not cause the displacement of Juncus by Spartina after three growing seasons. I conclude that zonation of Spartina and Juncus is maintained by preemption of space and greater tolerance of low nitrogen supplies by Juncus in the high marsh. These results contrast sharply with findings of reduced belowground competition with nutrient addition in previous studies and highlight the important role of nutrient-mediated competition for space between clonal plants.     

Direct and ecological costs of resistance and tolerance in the stinging nettle

Plant resistance and tolerance to herbivores, parasites, pathogens, and abiotic factors may involve two types of costs. First, resistance and tolerance may be costly in terms of plant fitness. Second, resistance and tolerance to multiple enemies may involve ecological trade-offs. Our study species, the stinging nettle ( Urtica dioica L.) has significant variation among seed families in resistance and tolerance as well as costs of resistance and tolerance to the holoparasitic plant Cuscuta europaea L. Here we report on variation among seed families (i.e. genetic) in tolerance to nutrient limitation and in resistance to both mammalian herbivores (i.e. number of stinging trichomes) and an invertebrate herbivore (i.e. inverse of the performance of a generalist snail, Arianta arbustorum). Our results indicate direct fitness costs of snail resistance in terms of host reproduction whereas we did not detect fitness costs of mammalian resistance or tolerance to nutrient limitation. We further tested for ecological trade-offs among tolerance or resistance to the parasitic plant, herbivore resistance, and tolerance to nutrient limitation in the stinging nettle. Tolerance of nettles to nutrient limitation and resistance to mammalian herbivores tended to correlate negatively. However, there were no significant correlations among resistance and tolerance to the different natural enemies (i.e. parasitic plants, snails, and mammals). The results of this greenhouse study thus suggest that resistance and tolerance of nettles to diverse enemies are free to evolve independently of each other but not completely without direct costs in terms of plant fitness.     

Increased chemical resistance explains low herbivore colonization of introduced seaweed

The success of introduced species is often attributed to release from co-evolved enemies in the new range and a subsequent decreased allocation to defense (EICA), but these hypotheses have rarely been evaluated for systems with low host-specificity of enemies. Here, we compare herbivore utilization of the brown seaweed, Fucus evanescens, and its coexisting competitors both in its native and new ranges, to test certain predictions derived from these hypotheses in a system dominated by generalist herbivores. While F. evanescens was shown to be a preferred host in its native range, invading populations supported a less diverse herbivore fauna and it was less preferred in laboratory choice experiments with important herbivores, when compared to co-occurring seaweeds. These results are consistent with the enemy release hypothesis, despite the fact that the herbivore communities in both regions were mainly composed of generalist species. However, in contrast to the prediction of EICA, analysis of anti-grazing compounds indicated a higher allocation to defense in introduced compared to native F. evanescens. The results suggest that the invader is subjected to less intense enemy control in the new range, but that this is due to an increased allocation to defense rather than release from specialized herbivores. This indicates that increased resistance to herbivory might be an important strategy for invasion success in systems dominated by generalist herbivores.     

Heritable variation in the foliar secondary metabolite sideroxylonal in <Emphasis Type="Italic">Eucalyptus</Emphasis> confers cross-resistance to herbivores

Plants encounter a broad range of natural enemies and defend themselves in diverse ways. The cost of defense can be reduced if a plant secondary metabolite confers resistance to multiple herbivores. However, there are few examples of positively correlated defenses in plants against herbivores of different types. We present evidence that a genetically variable chemical trait that acts as a strong antifeedant to mammalian herbivores of Eucalyptus also deters insect herbivores, suggesting a possible mechanism for cross-resistance. We provide field confirmation that sideroxylonal, an important antifeedant for mammalian herbivores, also determines patterns of damage by Christmas beetles, a specialist insect herbivore of Eucalyptus. In a genetic progeny trial of Eucalyptus tricarpa, we found significant heritabilities of sideroxylonal concentration (0.60), overall insect damage (0.34), and growth traits (0.30–0.53). Population of origin also had a strong effect on each trait. Negative phenotypic correlations were observed between sideroxylonal and damage, and between damage and growth. No relationship was observed between sideroxylonal concentration and any growth trait. Our results suggest that potential for evolution by natural selection of sideroxylonal concentrations is not strongly constrained by growth costs and that both growth and defense traits can be successfully incorporated into breeding programs for plantation trees.     

Competition at the population level along a standing crop gradient: a field experiment in successional grassland

I measured competitive responses of experimentally-established populations of the perennial grass, Andropogon gerardi, across a complex gradient of standing crop and species composition in the successional grasslands of southwest Michigan. The goal was to assess whether long-term (three year) population-level responses of Andropogon to competition matched the inferences made from a previous phytometer study that examined transplant responses to competition across this same gradient over a single growing season.Replicate experimental populations of Andropogon were established at seven grassland sites by sowing seed into 0.5×0.5 m plots that had been denuded of all vegetation. During the first year of the study, all Andropogon populations were maintained as monocultures by hand weeding. At the end of the first growing season, half of the monocultures were selected for continued weeding and half were left open to invasion by competitors for three years. Invasion of the unweeded populations by neighboring plants varied strongly among sites and was positively correlated with standing crop. Increased susceptibility to invasion and competition resulted in the extinction of the unweeded Andropogon populations at the two most productive sites, supporting the hypothesis that Andropogon is restricted by competition to low productivity sites in these grasslands. The finding that the intensity of competition was positively correlated with standing crop is consistent with the previous transplant study, suggesting that short-term experimental assays of competition on the growth of individual transplants may have predictive value for longer-term outcomes of competition at the population level.     

Competition in natural populations of Daphnia

I investigated the competitive relationships between two species of Daphnia, D. galeata and D. cucullata, and their interspecific hybrid. The term hemispecific competition was introduced to describe competition between parental species and hybrids. In eutrophic Tjeukemeer both parental species were found to compete with the hybrid, whereas competition between D. galeata and D. cucullata seemed limited. Although the effect of competition on life history traits of daphnids may be profound, the influence of the competitors on the seasonal dynamics of the Daphnia species seems limited.     

Evolution of Pair-Living in <Emphasis Type="Italic">Phaner furcifer</Emphasis>

Pair-living evolved several times independently in the primate lineage and most likely for more than one reason. Currently, there are 7 hypotheses regarding the evolution of pair-living in primates. They may explain several but not all cases. I investigated the applicability of the explanations to fork-marked lemurs Phaner furcifer. I used information from a long-term study on 8 fork-marked lemur families in Kirindy Forest to evaluate the hypotheses. Fork-marked lemurs live in uniform dispersed pairs, which share and defend a territory but spend three-quarters of their activity time apart from each other. Unconditional female dominance and lack of permanent close association between pair-partners disqualify most hypotheses. Lack of male parental care and long travel distances in small home ranges disqualify other explanations. I conclude that there is no support a priori for any current pair-living hypothesis and that the newly formulated intersexual-feeding-competition hypothesis best explains the evolution of pair-living in fork-marked lemurs. Accordingly, female range exclusivity evolved first as a consequence of intense feeding competition. Subsequently, indirect feeding competition drove females to accept a single male to share their territory as a defense against feeding competition from males whose ranges unsystematically overlap those of several females. This situation led to pair-living because formation of dispersed one-male-multifemale-units was too costly for males in terms of reduced foraging efficiency.     

The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa

Although the evolution of plant response to herbivory can involve either resistance (a decrease in susceptibility to herbivore damage) or tolerance (a decrease in the per unit effect of herbivory on plant fitness), until recently few studies have explicitly incorporated both of these characters. Moreover, theory suggests these characters do not evolve independently, and also that the pattern of natural selection acting on resistance and tolerance depends on their costs and benefits. In a genotypic selection analysis on an experimental population of Brassica rapa (Brassicaceae) I found a complex set of correlational selection gradients acting on resistance and tolerance of damage by flea beetles (Phyllotreta cruciferae: Chrysomelidae) and weevils (Ceutorhynchus assimilis: Curculionidae), as well as directional and stabilizing selection on resistance to attack by weevils. Evolution of response to flea beetle attack is constrained by a strong allocation cost of tolerance, and this allocation cost may be caused by a complex correlation among weevil resistance, weevil tolerance, flea beetle resistance, and flea beetle tolerance. Thus, one important conclusion of this study is that ecological costs may involve complex correlations among multiple characters, and for this reason these costs may not be detectable by simple pairwise correlations between characters. The evolution of response to weevil attack is probably constrained by a series of correlations between weevil resistance, weevil tolerance, and fitness in the absence of weevil damage, and possibly by a cost of tolerance of weevil damage. However, the nature of these constraints is complicated by apparent overcompensation for weevil damage. Because damage by both flea beetles and weevils had non-linear effects on plant fitness, standard measures of tolerance were not appropriate. Thus, a second important contribution of this study is the use of the area under the curve defined by the regression of fitness on damage and damage-squared as a measure of tolerance. This revised version was published online in July 2006 with corrections to the Cover Date.     

Competitive equivalence maintains persistent inter-clonal boundaries

Clear boundaries often separate adjacent conspecific competitors. These boundaries may reflect bordering animal territories or regions of inter-organism contact in mobile and non-mobile organisms, respectively. Sessile, clonal organisms often form persistent inter-clonal boundaries despite great variation in competitive ability among genotypes within a population. I show that neighboring clones in the sea anemone Anthopleura elegantissima and three species of the marine hydroid genus Hydractinia are more evenly matched in terms of competitive ability than expected by chance. Hypotheses of genetic relatedness or similar environmental regime shared by neighboring clones are inconsistent with the observed similarities between adjacent competitors in one or both taxa. Instead, inter-clonal borders evidently persist as standoffs between evenly matched competitors. Large differences in competitive ability between bordering clones were rarely observed, suggesting that dominant clones quickly displace or eliminate others in competitive mismatches. This ecological parallel between taxa (i.e., competitive equivalence) exists despite several fundamental differences (e.g., geographical distribution, habitat, body size, longevity), suggesting that competitive equivalence may be a widespread determinant of boundary persistence between adjacent competitors.     

Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on <Emphasis Type="Italic">Datura wrightii</Emphasis>

The costs and benefits of defensive traits in plants can have an ecological component that arises from the effect of defenses on the natural enemies of herbivores. We tested if glandular trichomes in Datura wrightii, a trait that confers resistance to several species of herbivorous insects, impose an ecological cost by decreasing rates of predation by the natural enemies of herbivores. For two common herbivores of D. wrightii, Lema daturaphila and Tupiocoris notatus, several generalized species of natural enemies exhibited lower rates of predation on glandular compared to non-glandular plants. Lower rates of predation were associated with reductions in the residence time and foraging efficiency of natural enemies on plants with glandular trichomes, but not with direct toxic effects of glandular exudate. Our results suggest that the benefit of resistance to herbivores conferred by glandular trichomes might be offset by the detrimental effect of this trait on the natural enemies of herbivores, and that the fitness consequences of this trichome defense might depend on the composition and abundance of the natural-enemy community.     

Primary function for a chemical defense? Nicotine does not protect Datura stramonium L from UV damage

The chemical defenses of plants are thought to play many different functional roles, all of which in some way decrease the costs of deploying the defense. However, few of these other functions have been tested with metabolites that are clearly defensive. Nicotine is a potent chemical defense with a high molar extinction coefficient in the UV, is a potent quencher of free radical pecies produced by UV absorption in vitro, and is known to increase in concentration after exposure to UV radiation. Hence this chemical defense may also function to protect against UV-induced damage. We examined nicotine's potential photoprotective role in two experiments by culturing Datura stramonium L plants in hydroponic solutions containing nicotine at two concentrations, and by exposing nicotine-containing and nicotine-free plants to UV radiation, which allowed us to manipulate nicotine contents independently of UV exposure. Plants with high levels of nicotine were not more resistant to UV-induced damage but, instead, exhibited greater decreases in photosynthetic capacity than did nicotine-free controls. Proposed multifunctional roles for chemical defenses deserve closer scrutiny.     

Contingency rules for pathogen competition and antagonism in a genetically based,plant defense hierarchy

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Unadapted behaviour of native,dominant ant species during the colonization of an aggressive,invasive ant

Among the factors driving the invasive success of non-indigenous species, the “escape opportunity” or “enemy release” hypothesis argues that an invader’s success may result partly from less resistance from the new competitors found in its introduced range. In this study, we examined competitive interactions between the little fire ant Wasmannia auropunctata (Roger) and ant species of the genus Pheidole in places where both are native (French Guiana) and in places where only species of Pheidole are native (New Caledonia). The experimental introduction of W. auropunctata at food resources monopolized by the Pheidole species induced the recruitment of major workers only for the Guianian Pheidole species, which were very effective at killing Wasmannia competitors. In contrast, an overall decrease in the number of Pheidole workers and no recruitment of major workers were observed for the New Caledonian species, although the latter were the only ones able to kill the Wasmannia workers. These results emphasize the inappropriate response of native dominant New Caledonian species to W. auropunctata and, thus, the importance of enemy recognition and specification in the organization of ant communities. This factor could explain how invasive animal species, particularly ants, may be able to successfully invade species-rich communities.