Svata M. Louda

Effect of Inflorescence‐Feeding Insects on the Demography and Lifetime of a Native Plant

The importance of herbivorous insects for plant demography and fitness is still controversial. The fact that their effect has not been fully evaluated within the context of the complete plant life cycle contributes to this controversy. This study is the first to test directly the influence of flower and seed consumption by a guild of inflorescence- feeding insects on the demography and fitness of a native plant over its whole life cycle within its natural environment. First, we discuss the evidence required to assess the effect of inflorescence-feeding insects on sequential stages in the plant life cycle. Then, we present the detailed results of two experiments that quantify the effect of inflorescence-feeding insects on seeds, seedlings, juveniles, and subsequent flowering progeny of Cirsium ca- nescens (Platte thistle), a native, monocarpic perennial species of Sandhills prairie, Ne- braska. Exclusion of inflorescence-feeding insects by insecticide had four main effects. Total seed output increased (P < 0.0005 in both experiments), indicating that resources were not limiting seed production. Flower heads produced later in the season contributed to the seed pool when insects were reduced (P < 0.01), suggesting that insect feeding restricted the phenology of flowering and pollination. The density of seedlings increased around plants protected from inflorescence-feeding insects (P < 0.0005), showing that safe sites were not limiting. Finally, the increase in seedlings led to higher numbers of flowering adults (P < 0.009), demonstrating that inflorescence-feeding insects significantly reduced lifetime fitness. Neither individual compensation for seed loss, nor density-dependent com- pensation for increased plant population densities, was observed when insects were ex- cluded. Thus, we conclude that the inflorescence-feeding insect herbivores limited seed production, seedling recruitment, plant density, and maternal fitness of this plant under natural conditions. This outcome challenges current theoretical models of the effect of insects on plant population dynamics. We predict that our result will be general for short- lived perennial plants with life histories in which persistence is tightly linked to regeneration from current seed, such as for fugitive perennials with transient seed banks.

Distribution Ecology: Variation in Plant Recruitment over a Gradient in Relation to Insect Seed Predation

Although predispersal seed predation by insects is common, no test exists of its effect on plant recruitment. This study examines seed predation in the population dynamics of a native, temperate shrub, Haplopappus squarrosus H. and A. (Asteraceae), over an elevational gradient in the coastal sage scrub vegetation of San Diego County, California USA. Frequency and abundance of H. squarrosus increase from coast to mountains. Expected abundance, based on flowers initiated, was highest at the coast and lowest in the interior, the opposite of the observed adult plant distribution. Overall flower and seed predation by insects was high (44-73%) and was greatest at the coast. Insect exclusion experiments at sites along the gradient had three main results. (1) Seedling recruitment was proportional to the number of viable seeds after seed predation. The exclusion plots had significantly higher numbers of seedlings established at all sites than did control plots; the greatest increase was at the coast. (2) Seedling survivorship was independent of both seedling and adult densities. (3) Juvenile recruitment was proportional to seedling establishment. Predation by insects prior to release of seeds played a critical role in the population recruitment of H. squarrosus within and among sites along the gradient. Survivorship of established plants, in addition, was as high at the coast as it was in the interior. These results suggest that indigenous insect seed predators can be a major force controlling the dynamics of a native plant species over its natural distributional range.

Seed Predation and Seedling Mortality in the Recruitment of a Shrub, Haplopappus venetus (Asteraceae), along a Climatic Gradient

Haplopappus venetus is a characteristic shrub of the coastal sage scrub of southern California. Its relative frequency decreases rapidly and significantly from the coast to the central valleys of southern California. Insect damage to developing flowers and seeds is high (35-61%). Experimental exclusion of predispersal flower and seed predators caused a significant increase in the number of viable seeds released because of: (I) a decrease in insect-caused abortion of flower heads (1 1%), (2) an increase in pollination success (19%), and (3) a decrease in damage to developing seeds (104%). A significant and proportionate increase in the number of seedlings established at sites over the climatic gradient from coast to inland valleys followed the exclusion of seed predators. In the inland area, however. extremely high mortality among established seedlings prevented recruitment of juveniles. Mortality of established adult plants, in contrast, was higher at the coast than inland (41 vs. 31%, respectively), suggesting that the geographic difference in the abundance of juveniles would persist. These results differ from those for a parallel experiment on H. squarrosus in which juvenile recruitment was determined by differential predispersal seed predation along the gradient and was not altered by differential mortality among seedlings. Consequently, I conclude that insect seed predation can be the critical factor limiting population recruitment, as in the case of H. squarrosus, but it need not be, as in the case of H. venetus. In the latter case, seedling mortality patterns, superimposed on seed predation, were critical to an explanation of plant recruitment and occurrence over the climatic gradient.

PLANT RESISTANCE TO INSECT HERBIVORES: A FIELD TEST OF THE ENVIRONMENTAL STRESS HYPOTHESIS'

We tested the hypothesis that environmental stresses decrease overall plant resistance to insect herbivory in the field and evaluated biochemical mechanisms proposed to explain insect response to stressed plants. To impose a stress treatment, we severed lateral roots and rhizomes of a native crucifer (bittercress, Cardamine cordifolia) and quantified plant and herbivore responses for treatment and control clones. Severing roots and rhizomes once, early in the growing season: (1) produced moderate, but detectable, changes in plant physiological traits, specifically greater transient leaf water deficits at midday (P < .05) and elevated nitrate-nitrogen concentrations (P < .05); (2) altered plant quality, by causing an increase in soluble carbohydrates (P < .003), isoleucine concentra- tions in leaves (P < .01), and possibly glucosinolate concentration (P < .10), but made no differences in most primary nutrient concentrations, including total nitrogen, total free amino nitrogen, total amino acids, proline, and leaf water content; and (3) led to increased herbivore by chewing and leaf-mining (P < .001), but not by sap-feeding, insect herbivores. Trends toward decreased plant stature and fruit reproduction were not significant after 1 mo. In addition to the significant effect of our treatment, we found extensive variation in the magnitude of response to stress and herbivory among replicates. We hypothesize that environmentally induced physiological variation among plants within a plant population commonly distributes insect herbivore disproportionately onto a subset of the individuals, and in so doing influences the demography, distribution, and evolution of that plant pop- ulation.

DEMOGRAPHIC AND EVOLUTIONARY IMPACTS OF NATIVE AND INVASIVE INSECT HERBIVORES ON CIRSIUM CANESCENS

Invasive species have the potential to alter trade-offs leading to selection in the populations they invade. Here we quantify the demographic and selective effects of herbivory by native insects and the introduced floral feeder Rhinocyllus conicus on Platte thistle (Cirsium canescens), a sparse monocarpic thistle endemic to North America. Rhin- ocyllus first invaded the Platte thistle population in 1993. Since then, its numbers have increased exponentially, while the Platte thistle population size has decreased. Data from 11 years were analyzed to determine how demographic rates varied with plant size and damage by native insects and Rhinocyllus. Individual growth, survival, flowering proba- bility, and seed set were all size dependent. Damage to vegetative structures did not influence demographic rates; damage to flower heads did because Platte thistle is seed limited. These analyses were used to parameterize a series of integral projection models (IPMs) that investigated the effects of floral herbivory on the population growth rate l, equilibrium population size, and the evolutionary stable (ES) flowering strategy. The IPMs showed that native insects have significant impact on the equilibrium population size and l, but not the ES flowering strategy, because they use the flowers of different-sized plants indiscrimi- nately. In contrast, Rhinocyllus has the potential to drive Platte thistle extinct. Rhinocyllus preferentially fed and oviposited on the flowers of larger plants and therefore selected for a reduction in flowering size. However, as the thistle population went into decline, this pattern reversed. Thus, selection imposed by an invader may be complex and will reflect behavioral interactions between herbivore and host, as well as demographic changes in the host population.

Herbivore Effect on Stature, Fruiting, and Leaf Dynamics of a Native Crucifer

The impact of a native, leaf-feeding chrysomelid beetle (Phaedon sp. nr. oviformis) on bittercress (Cardamine cordifolia: Cruciferae), was evaluated in an exclusion experiment. Multivariate statistical analysis showed a significant increase in plant performance in the rotenone exclusion com- pared to performance in the paired control treatment. Plant response to the reduction of herbivory was a complicated, interrelated syndrome of changes. When insects were excluded, the amount of missing leaf area decreased significantly (3.6-fold; 3.2-0.9 cm2 per plant), and the total leaf area increased 5.7-fold (12.9-73.4 cm2 per plant). Plant height (5.7-20.3 cm) and fruit production (0.1- 3.9 siliques per plant) also increased significantly when the number of insects was reduced. Furthermore, the 570% expansion in leaf area due to the exclusion of insects involved significant increases both in the initiation of new leaves and in the survival of mature leaves. Nevertheless, insect herbivory at a level well below complete defoliation (25% of the leaf area) changed leaf demography (both phenology and dynamics) and reduced plant performance by decreasing the plant stature, leaf area, and fruit production of this native forb. Thus, further experimental assessment is necessary before general- izations can be made regarding the effects of herbivory on plant dynamics.

Predispersal seed predation, postdispersal seed predation and competition in the recruitment of seedlings of a native thistle in Sandhills prairie.

-Platte thistle (Cirsium canescens Nutt.) is a native monocarpic plant species of Sandhills prairie. We concurrently tested three biological interactions that could influence its recruitment and population density: (1) predispersal flower and seed consumption by insects; (2) postdispersal loss of seeds to vertebrates, and (3) seedling competition with established plants. Few previous experimental studies have analyzed more than one of these processes at a time. Each interaction had a significant negative impact on seedling establishment. Insect seed predation caused major losses that were magnified in each succeeding life history stage. A 3-fold reduction in viable seeds by insects led to a 6-fold decrease in seedling establishment and a 6to 37-fold reduction in the eventual number of new adults. Germination was low (1.7%) and 80% of the seedlings were in exclosure cages, particularly in those cages placed in an open disturbed area instead of in the grassland. Competition between seedlings and established grasses led to a 9.5-fold decrease in seedling survival. Platte thistle populations were thus limited successively, first by seed predation and then by competition with established grasses. Both processes therefore reinforce selection for the fugitive life history observed in this species.

Chemistry of Cirsium and Carduus: A role in ecological risk assessment for biological control of weeds?

Prediction of host plant range and ecological impact of exotic phytophagous insects, such as insects for classical biological control of weeds, represents a major challenge. Recently, the flowerhead weevil ( Rhinocyllus conicus Frol.), introduced from Europe into North America to control exotic thistles (Carduus spp.), has become invasive. It feeds heavily on some, but not all species of native North American thistles (Cirsium spp.). We hypothesized that such non-target use among native plants could be better predicted by knowledge of characteristic chemical profiles of secondary compounds to supplement the results of host specificity testing. To evaluate this hypothesis, we reviewed the literature on the chemistry of Cirsium and Carduus thistles. We asked what compounds are known to be present, what is known about their biological activity, and whether such information on chemical profiles would have better predicted realized host range and ecological effects of R. conicus in North America. We found an extensive, but incomplete literature on the chemistry of true thistles. Two main patterns emerged. First, consistent chemical similarities and interesting differences occur among species of thistles. Second, variation occurs in biologically active groups of characteristic compounds, specifically flavonoids, sterols, alkaloids and pheno lic acids, that are known to influence host plant acceptance, selection, and feeding by phy tophagous insects. Surprisingly, sesquiterpene lactones, which are characteristic in closely related Asteraceae, have not been extensively reported for Cirsium or Carduus. The minimal evidence on sesquiterpene lactones may reflect extraction methods vs. true absence. In summary, our review suggests further research on thistle chemistry in insect feeding is warranted. Also, since the exotic Canada thistle (Cirsium arvense) is an invasive thistle of current concern in North America, such research on mechanisms underlying host range expansion by exotic insects would be useful.

EXOTIC WEED INVASION INCREASES THE SUSCEPTIBILITY OF NATIVE PLANTS TO ATTACK BY A BIOCONTROL HERBIVORE

Landscape change has great, yet infrequently measured, potential to influence the susceptibility of natural systems to invasive species impacts. We quantified attack by an invasive biological control weevil (Rhinocyllus conicus) on native thistles in relation to two types of landscape change: agricultural intensification and invasion by an exotic thistle, Carduus nutans, the original target of biological control. Weevil egg load was measured on native thistles in three landscape types: (1) agriculture dominated, (2) grassland dominated with exotic thistles, and, (3) grassland dominated without exotic thistles. We found no difference in egg load on native thistles within grassland landscapes without exotic thistles vs. within agricultural landscapes, suggesting that agricultural intensification per se does not influence levels of weevil attack. However, attack on the native Cirsium undulatum increased significantly (three- to fivefold) with increasing exotic thistle density. Within-patch exotic thistle density explained >50% of the variation in both the intensity and frequency of weevil attack. Since R. conicus feeding dramatically reduces seed production, exotic thistles likely exert a negative indirect effect on native thistles. This study provides some of the first empirical evidence that invasion by an exotic plant can increase attack of native plants by shared insect herbivores.

Herbivory by leaf miners in response to experimental shading of a native crucifer

SummaryWe tested the hypothesis that light intensity was the direct, proximal mechanism causing significantly higher vulnerability of Bittercress (Cardamine cordifolia A. Gray) clones in the sun to herbivory by a leaf-mining fly (Scaptomyza nigrita Wheeler). Clones in the sun were experimentally shaded. Plant performance and losses to leaf miners were compared to controls in the sun and natural willow shade. Leaf-mining damage was significantly higher on artificially-shaded plants (P<0.01), opposite of our expectation. Shading sun plants shifted their growth pattern toward that of naturally-shaded plants. No significant differences were detected in leaf water status or glucosinolate concentrations, eliminating water stress and variation in defensive posture for mediating the between habitat differences in levels of herbivory. Although soluble sugars varied significantly, they were higher in sun than either shade treatment. Total and free amino nitrogen concentrations were highest in the artificially-shaded plants and lowest in naturally-occurring sun plants. Adult flies were more abundant on sun and on artificially-shaded plants than on naturally-shaded plants. Thus, relative abundance of ovipositing flies in the sun-exposed area, combined with the higher nitrogen availability in artificially-shaded plants, form the most plausible hypothesis for factors mediating the experimentally documented pattern of herbivory.